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Estuarine, Coastal and Shelf Science 114 (2012) 59e69

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Estuarine, Coastal and Shelf Science

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Annual characterisation of four Mediterranean coastal lagoons subjectedto intense human activity

Miguel Cañedo-Argüelles a,*, Maria Rieradevall a, Roser Farrés-Corell b, Alice Newton c,d

a F.E.M (Freshwater Ecology & Management) Research Group, Department d’Ecologia, Universitat de Barcelona, Diagonal 645, 08028 Barcelona, SpainbCSIC (Centro Superior de Investigaciones Científicas), 17300-Blanes, Girona, Spainc IMAR, FCT-Gambelas, Universidade do Algarve, 8000-117 Faro, PortugaldNILU, Center of Ecology and Economics, PO Box 100, 2027 Kjeller, Norway

a r t i c l e i n f o

Article history:Received 22 July 2011Accepted 22 July 2011Available online 25 August 2011

Keywords:coastal lagoonstransitional waterseutrophicationTRIXTSIEEA categorieshuman pressures

* Corresponding author.E-mail address: mcanedo-arguelles@ub.edu (M. Ca

0272-7714/$ e see front matter � 2011 Elsevier Ltd.doi:10.1016/j.ecss.2011.07.017

a b s t r a c t

In the present study the annual variability of the physico-chemical parameters of four coastal lagoonssubjected to intense human activity was characterised. The trophic state indices (TSI) of Carlson (1977)and the water quality index TRIX of Vollenweider et al. (1998) were tested and compared with the waterquality categories proposed by the European Environmental Agency (2009). All the parameters weresampled monthly fromMay 2004 to July 2005. There were important differences in the annual variabilityof the physico-chemical parameters between the lagoons, reflecting the importance of human-inducedpressures and the heterogeneity of these environments. The lagoons were in a eutrophic/hypereutrophicstate most of the year. Trophic state indices classified the lagoons in a bad or poor trophic state most ofthe year, and they were not able to discriminate the effect of secondary variables such as freshwaterreleases, ground waters fluxes or water renewal. Nitrogen was the limiting factor in the lagoon witha higher exchange rate with the sea, while phosphorous was the limiting factor in the other lagoons, dueto the high nitrogen external loads and the poor water renewal. The need for developing indicesspecifically designed for coastal lagoons in order to asses their trophic state is discussed.

� 2011 Elsevier Ltd. All rights reserved.

1. Introduction

Coastal lagoons are critical transition zones between fresh-watersand the sea, and, in consequence, they are highly heterogeneous anddynamic systems (Levin et al., 2001;Pérez-Ruzafaet al., 2007).Ononeside theyareusually subjected to intermittentorpermanent seawaterinfluxes during high tides and storms, and seawater also percolatesthrough sand barriers in their mouths; on the other side, freshwaterenters as runoff and stream discharges. Moreover, the ionic compo-sition of the underground waters also exerts an influence over theionic composition of the lagoons. The mix of salt and fresh watersdetermines the physico-chemical characteristics of these transitionalzones, which vary greatly within and between annual cycles becauseof theunpredictabilityof the incomingfluxes. In the last centuries, theestablishment of large human populations in the coastal areas havealtered the amount and nature of these fluxes (Smith, 2003; Elliottand Quintino, 2007; Viaroli et al., 2007) incrementing their unpre-dictability and their trophic charge. The human pressure over these

ñedo-Argüelles).

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ecosystems has considerably increased the amount of incomingnutrients, especially since the 1970’s, when the rate of creation ofreactive nitrogen from human activity was accelerated (Nixon,1995;Howarth andMarino, 2006). The continuous and increasing nutrientdischarges led to the eutrophication of many coastal areas in theworld.

In spite of the importance of the phenomenon, causingdisruptions in the coastal ecosystems’ functioning (Viaroli andChristian, 2003) and leading to detrimental effects over the goodsand services that they provide and over their associated flora andfauna (Pearson and Rosenberg, 1978; Breitburg, 2002; Zaldívaret al., 2008), its scientific understanding is still in progress(Newton et al., 2003; Maier et al., 2009).

Nonetheless, in the last years the concern of managers andscientists has grown and different categorizations of the trophicstate of coastal waters based on nutrients and oxygen thresholdshave been settled (Best et al., 2007; Devlin et al., 2007; EuropeanEnvironmental Agency, 2009). In the European Union, the goal isfor all the water masses to arrive to good ecological status by 2015(EU Water Framework Directive, 2000); but in the case of transi-tional waters there is a considerable delay due to the arisendifficulties in the Directive’s implementation (Zaldívar et al.,

M. Cañedo-Argüelles et al. / Estuarine, Coastal and Shelf Science 114 (2012) 59e6960

2008). As mentioned before, these ecosystems are naturallyenriched and highly dynamic, making it difficult to separatehuman-induced from natural-induced changes (Elliott andQuintino, 2007). Moreover, there is still a lack of knowledgeregarding the biogeochemical dynamics of these systems and howdo they respond to human-induced disturbances. Althougheutrophication is the main problem, because of affecting most ofthe world’s coastal areas and because of its severe and long-lastingeffects, there are many other problems concerning coastal lagoons,as i.e.: alteration of incoming fluxes, landscape fragmentation andgeomorphological modification (Stora and Arnoux, 1983; de Jonge& de Jong, 2002). These problems should be taken into accountwhen assessing the lagoons’ ecological state, and there is anurgent need for them to be solved and integrated withinmanagement policies and strategies (Zaldívar et al., 2008). For thatpurpose, a deep knowledge of the natural dynamics of the systemand the effect of the different kinds of stressors, which can interactaffecting restoration targets (Duarte et al., 2009), will beundoubtedly required.

The assessment of coastal areas has been mainly based ontrophic state indices developed for freshwater ecosystems, as inexample Carlson’s Trophic State Index (1977); based on themeasurement of variables such as nutrients and chlorophyll-a andthe establishment of nutrient-based classification systems. None-theless, in the last decades the applicability of these indices fortransitional waters has been questioned, and the eutrophicationconcept has evolved (Cloern, 2001). It has been recognized that,although the eutrophic symptoms (i.e.: algal blooms, anoxia, highchlorophyll-a concentrations, etc.) are mainly a consequence ofnutrients addition, nutrients addition is not necessarily a cause foreutrophication (Boyes and Elliott, 2006), and there are many otherfactors, such as tidal exchange or freshwater inflow, which can beresponsible for the apparition of these symptoms (Bricker et al.,2003). Therefore, there is a need for trophic state indices to betested, especially in coastal lagoons (Coelho et al., 2007; Salas et al.,2008), which are very vulnerable to eutrophication due to theirrestricted exchange with the adjacent ocean (Newton et al., 2003;Tett et al., 2003). The design of future tools for the assessmentand management of transitional waters will require the consider-ation of the inherent sensitivity of the ecosystems’ to nutrientenrichment and how does nutrient enrichment interact with otherstressors (Cloern, 2001).

Fig. 1. Study area and localization of the studied lagoons. The airport is delimited

The present study was conducted in four coastal lagoons locatedin the coastal area of the second largest city of Spain, Barcelona. Thelagoons were heavily influenced by the human action and sub-jected to different types of pressures. The aim of the study was tocharacterise the annual variability in the lagoon’s physico-chemicalattributes and trophic status. The lagoons were classified accordingto the European Environmental Agency standards for Mediterra-nean transitional, coastal and marine waters (EuropeanEnvironmental Agency, 2009). The Carlson (1977) Trophic StateIndex (TSI) and Vollenweider et al. (1998) water quality index(TRIX) were applied in order to asses the lagoon’s trophic state, andthe results from both indices were compared and discussed.

2. Materials and methods

2.1. Description of study site

The Llobregat’s river deltaic plain was in its origins a vastwetland formed by the deposition of alluvial material swept alongby the Llobregat’s river (Cabello and Ramos, 2007). Most of thenatural-formed lagoons were born under the influence of the river,and had no direct connection with the sea (Planas, 1984). Nowa-days, the area is profoundly transformed by human action: thewater has been dried-out for construction purposes, the aquifer hasbeen over-exploited, the river has been canalised, and some ofthese lagoons have disappeared, while some new ones have beencreated.

We focused the study in four coastal lagoons: Remolar, Ricarda,Cal’Arana and Cal Tet (Fig. 1); which are representative of the threemain human pressures that threat the delta’s lagoons: i) eutro-phication; ii) water fluxes’ alteration; and iii) morphologicalmodification:

(1) One of the most representative examples of eutrophication inthe delta is Remolar’s lagoon. It is a natural-formed lagooncovering an area of 5.75 ha and with a maximum depth of 5 m.It is connected to the sea by a narrow channel in its mouth,which is coming progressively obstructed by the accumulationof material, hindering water renewal. In spite of being insidea natural reserve, where many migratory birds coming fromNorthern Europe rest before reaching Africa, it is heavilypolluted, receiving a net annual loading of 373 gr. of N and 43

with a black line. CA ¼ Ca l’Arana; CT ¼ Cal Tet; RE ¼ Remolar; RI ¼ Ricarda.

M. Cañedo-Argüelles et al. / Estuarine, Coastal and Shelf Science 114 (2012) 59e69 61

gr. of P per m2 year�1 (Lucena et al., 2002). Sewage dischargesarrive from industrial and urban sources, and agriculturalwaters also reach the lagoon via its main channel and runoffs;

(2) Mostof the lagoons’ incomingwaterfluxes are human-regulatednowadays, since its connection with the river has been lost andsea-lagoon exchange is restricted, being often reduced togroundwater percolation. The human regulation of these waterfluxesderived insporadic large freshwater releases in theRicardaand Ca l’Arana lagoon, causing a significant salinity decrease andhaving significanteffectsover the aquatic communities (Cañedo-Argüelles and Rieradevall, 2010). The lagoons of Ricarda and Cal’Arana are good examples of this problem;

Ricarda is a naturally-formed lagoon, which has been wellpreserved from human action. It is shallow (max. depth ¼ 2 m),covering an area of 8.42 Ha and it is intermittently connected to thesea through its mouth. After the works related to the expansion ofBarcelona’s airport (which is very close to the lagoon, as can beappreciated in Fig. 1) began, all the incoming freshwater fluxeswere centralized into one single channel managed by the airport. InJanuary of 2005 the water level of the lagoon was very low due tothe prolonged drought of 2004, and this moved the owner to askthe airport manager’s for water, resulting in an important fresh-water release into the lagoon.

The actual lagoon of Ca l’Arana is placed where once there wasa natural lagoon. This old lagoon disappeared and was replaced bya quarry basin of 7 m of maximum depth and an area of 1 Ha, whichis now completely filled with water coming from the superficialaquifer. This lagoon is an example of morphological modification(iii), and also of the regulation of incoming water fluxes (ii). Thisregulation was especially important during the study period, sincein November of 2004 a large amount of freshwater was releasedinto the lagoon as a consequence of a massive irrigation of thesurrounding land for trees’ maintenance purposes.

(3) As it was mentioned before, most of the natural lagoons havedisappeared or have been modified under the human influ-ence, and new lagoons have been created. The most recentexample is the lagoon of Cal Tet, which was created in 2003 asa compensation measure for the loss of natural habitats in thedelta as a consequence of the airport’s and port’s expansion.The lagoon is shallow (maximum depth 1.5 m), comprising anarea of 16 Ha and is exclusively fed by ground waters comingfrom the superficial aquifer. The water renewal is thereforevery poor, and the evaporation is progressively drying thelagoon. Along the study period the lagoon registered a shift ofstate, with vegetation changing from Chara-dominated in 2004to almost exclusive Potamogeton pectinatus dominance in 2005(Seguí and Pérez, 2006), which had effects on the macro-invertebrate community (Cañedo-Argüelles and Rieradevall, inpress).

2.2. Physico-chemical characterization

The lagoons were sampled once a month from June 2004 (May2004 in the case of Ca l’Arana and Cal Tet) to July 2005. Verticalprofiles of conductivity, pH, water temperature, and dissolvedoxygen were measured each half meter (except for Ca l’Aranalagoon, where profiles were recorded each meter) in the deepestpoint of each lagoon using a multiparametric sensor (WTW,multiparameter model 197i); and water transparency wasmeasured through Secchi disk depth. A surface water sample (1.5 L)was collected in each lagoon and preserved at 4 �C for laboratoryanalysis of nutrients (NHþ

4 , NO�3 , NO�

2 , PO3�4 ; TP, Silica), total

organic carbon (TOC), suspended solids (SSP), major ions (SO2�4 ,

Cl�, Ca2þ, Mg2þ, Naþ, Kþ) and phytoplanktonic chlorophyll-a (chl-a)following standard methods (Greenberg et al., 1999). Dissolvedinorganic nitrogen (DIN) was obtained as the sum of NeNHþ

4 ,NeNO2 and NeNO�

3 . The lagoons were classified into oligohaline(salinity < 5&) or mesohaline (5& � salinity < 18&) according tothe Venice system (1959). The conversion from conductivity tosalinity was performed taking into account the water temperatureand following standard methods (Greenberg et al., 1999).

2.3. Data analysis

In order to characterise the annual variability of the lagoons andthe relation between the variables, and to analyse which of themwere explaining a higher percentage of total variance, a principalcomponents analysis (PCA) was performed, using CANOCO 4.5software (ter Braak and Smilauer, 2002). Previously, all the variables(including bottomvalues in the case of conductivity, oxygen, pH andtemperature) were standardised and redundant information wasfiltered thorough the elimination of linearly correlated variables (aPearson’s correlation test was performed, and when two variableshad a correlation coefficient � 0.95, one of them was not includedinto principal components analysis). The correlation of eachnutrient (NHþ

4 , NO�3 , NO

�2 , PO

3�4 ; TP, Silica) and TOC (as an indicator

of organic matter load in the system) with secondary (conductivity,ions, temperature and suspended solids) and response (chlorophyll-a and dissolved oxygen) variables was evaluated using Spearmancorrelation test, and considering results with 0.01<r < 0.05 assignificative (*) and with r < 0.01 as highly significative (**).

Carlson’s (1977) classical trophic state indices (TSI) designed forthe assessment of freshwater lake’s trophic state and the indexTRIX proposed by Vollenweider et al. (1998), which can beconsidered as an adaptation of Carlson’s TSI to transitional waters,were used in order to asses the trophic state of the lagoons. Thechlorophyll-a (1) and phosphorous (2) TSI were calculated usingthe following equations (Carlson, 1977):

TSI ðchl aÞ ¼ ð9:81� ln ½chl a�Þþ30:6 ð½$� ¼ concentration inmg=lÞ(1)

TSIðTPÞ ¼ ð14:42� ln½TP�Þ þ 4:15 ð½$� ¼ concentration in mg=lÞ(2)

where chl-a refers to surface phytoplanktonic chlorophyll-a and TPrefers to surface total phosphorous. After its application, thelagoons were assigned a trophic state according to Carlson’s clas-sification: oligotrophic (TSI < 30), oligomesotrophic(30 � TSI < 40), mesotrophic (40 � TSI < 50), eutrophic(50 � TSI < 60), eutrophic to hypereutrophic (60 � TSI < 70) andhypereutrophic (70 � TSI). The TRIX (Vollenweider et al., 1998)follows the same structure, with the difference that several vari-ables related to the trophic state are included in the equation:

TRIX ¼ ðLog10ðchl a� IDOdevI� DIN� TPÞ þ 1:5Þ=1:2where chl-a, DIN and TP refer to the surface chlorophyll-a, dis-solved inorganic nitrogen and total phosphorous concentrations(mg l�1) respectively, and IDOdevI is the oxygen absolute deviationfrom saturation (%) at the surface. While the TSI has no lower andupper limits, the TRIX gives values between 0 and 10, which aredivided into four trophic state categories: high (TRIX < 4), good(4 � TRIX < 5), moderate (5 � TRIX < 6) and poor (6 � TRIX). Thetrends of the indices values were compared through a Spearmancorrelation test using PAST software (Hammer et al., 2001). Thelagoons were categorized according to their oxidized nitrogenðNO�

2 þ NO�3 Þ and orthophosphate concentrations following the

European Environmental Agency (EEA) assessment on nutrients in

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Mediterranean transitional, coastal and marine waters of January2009 (European Environmental Agency, 2009), and according totheir surface dissolved oxygen concentrations following theproposal of Best et al. (2007).

3. Results

All the lagoons were mesohaline, except for Cal Tet in Februaryof 2005, when it registered oligohaline waters (Fig. 2). Surfacewaters were oxygen-saturated (dissolved oxygen z 100%), beingover-saturated in summer and spring in the lagoon of Remolar, inSummer 2004 in the lagoon of Ricarda and in summer 2005 in thelagoon of Ca l’Arana (Fig. 3). Surface waters were alkaline in all thelagoons (Fig. 4), and water temperature suddenly dropped inNovember (mean surface water temperature drop of 9.7 �C, from23.6 �C to 13.9 �C), rising again in April (mean surface watertemperature ascent of 9.1 �C, from 8.9 �C to 18.0 �C). Depth profilesshowed a major difference between the shallow lagoons of Cal Tet(max. depth 1.5 m) and Ricarda (max. depth 2 m) and the deeperlagoons of Ca l’Arana (max. depth 7 m) and Remolar (max. depth5 m). While the first ones showed no vertical stratification, the lastones did. In the deeper stratified lagoons of Ca l’Arana and Remolarthere was a superficial layer of fresher (Fig. 2), oxygenated (Fig. 3),alkaline (Fig. 4) and warmer waters, lying over a deep layer of salineanoxic cold waters with low pH (Figs. 2e5). The was around 5 mdepth in Ca l’Arana and around 1.5 m depth, shifting from 1 to 2 mdepth in June to 0.2e1.5 m depth in August, in Remolar (Figs. 2e4).In the case of Ca l’Arana the halocline was broken in November of2004 (Fig. 2), when freshwater was released into the lagoon;nonetheless, the bottom waters remained anoxic (Fig. 3) and acid(Fig. 4). In Ricarda the freshwater release of January 2005 alsoimpacted on the conductivity of its waters (Fig. 2), which droppedfrom 14.1 mS cm�1 to 9.8 mS cm�1.

Principal components analysis (PCA) showed different trendsfor each lagoon (Fig. 5). The first axis explained a 17.1% and opposedmainly Secchi depth to conductivity and temperature. The secondaxis explained a 16.3% of total variance and opposed mainly total

Fig. 2. Depth profiles of conductivity (mS cm�1) along time for each st

phosphorous to major ions and Secchi depth. The lagoons regis-tered a wide range of variation along both axes. Ca l’Arana rangedmainly along axis 1, Ricarda ranged mainly along axis 2, Cal Tetlagoon ranged mainly along the Secchi depth gradient and Remolarregistered the widest range of variation (Fig. 5).

Nutrients and total organic carbon (TOC) concentrations weresignificantly correlated to different secondary and response vari-ables depending on the lagoon (Table 1). Nitrate was positivelycorrelated with temperature in Cal’Arana and negatively in Remo-lar. It was also positively correlated to pH in Ricarda and negativelyin Remolar. Ammonium was positively correlated to bottom dis-solved oxygen concentrations in Cal Tet and negatively in Ca l’Ar-ana. Total organic carbon was the variable more significantlycorrelated to secondary and response variables, being positivelycorrelated to SSP in the lagoons of Ca l’Arana and Ricarda. It has tobe noticed that chlorophyll-a concentration, which is the responsevariable commonly used to asses the trophic state of aquaticsystems, was not significantly correlated to any nutrient concen-tration (except for its correlation with TOC in the lagoon ofRemolar).

Concerning the different forms of dissolved inorganic nitrogen(DIN), NO�

2 was almost negligible, accounting less than the 5% ofmean annual DIN in all the lagoons. On the contrary, NO�

3 was thedominant form (Fig. 6), accounting for more than the 70% of DIN inall the lagoons, except in Remolar, where peaks of NO�

3 were fol-lowed by peaks of NHþ

4 (Fig. 6). The molar N:P ratios were muchhigher than the Redfield ratio (16:1), except in the lagoon of Ricardafrom September 2004, and in Ca l’Arana in May 2005 and inRemolar in January 2005 (Fig. 6).

The application of Carlson’s (1977) trophic state indices (TSI)resulted in more eutrophic waters when applying the total phos-phorus index than the chlorophyll-a index (Fig. 7). The lagoon ofRemolar registered the most eutrophic waters, while Cal Tetregistered less eutrophic waters. According to the TRIX index(Vollenweider et al., 1998) all the lagoons were in a poor state mostof the time, except Ca l’Arana in summer of 2004 and 2005, and CalTet in winter (Fig. 8). The Spearman correlation test resulted in

udied lagoon. Y axis ¼ depth in meters; X axis ¼ studied months.

Fig. 3. Depth profiles of dissolved oxygen (%) along time for each studied lagoon. Y axis ¼ depth in meters; X axis ¼ studied months.

M. Cañedo-Argüelles et al. / Estuarine, Coastal and Shelf Science 114 (2012) 59e69 63

a significant correlation between the indices (TSI e TP vs TSI e chl-a: rs¼ 0.64, p¼ 6.77 10�4; TSIe TP vs TRIX: rs¼ 0.70, p¼ 1.72 10�5;TRIX vs TSI e chl-a: rs ¼ 0.78, p ¼ 7.25 10�9). The lagoons’ trophicstate was categorized as “bad” in all cases and along the wholestudy period according to the EEA (EEA 2009) oxidized nitrogenand orthophosphate thresholds (Table 2). In the case of theproposed Water Framework Directive thresholds for minimumoxygen concentrations (Best et al., 2007), the stratified lagoonswith anoxic bottomwaters (Ca l’Arana and Remolar) were in “bad”state most of the year, while Cal Tet and Ricardawere in “good” and“high” state (Table 2).

Fig. 4. Depth profiles of pH along time for each studied lago

4. Discussion

The differences in the annual variability of the physico-chemicalprocesses in each lagoon, evidenced by the different ranges ofvariation in the principal components analysis (PCA) and thedifferences in the correlations of nutrients with secondary andresponse variables, reflected the unpredictability of the humanpressures that the lagoons were subjected to. In Ca l’Arana andRicarda the freshwater releases disrupted the seasonal trend ofhigh temperatures linked to high conductivity values of the warmperiod (MayeNovember). In Cal Tet this seasonal trend was very

on. Y axis ¼ depth in meters; X axis ¼ studied months.

Fig. 5. Distribution of samples and environmental variables in the bi-dimensional space of the two main components resulting from principal component analyses. Each lagoon’ssamples (black triangles) are plotted separately and the space occupied by them is delimited with a black line. CA ¼ Ca l’Arana; CT ¼ Cal Tet; RE ¼ Remolar; RI ¼ Ricarda.Surf ¼ surface value; Depth ¼ bottom value; Cond ¼ conductivity; Ox ¼ dissolved oxygen; TOC ¼ total organic carbon; SSP ¼ solid suspended particles; Ta ¼ temperature; TP ¼ totalphosphorous.

M. Cañedo-Argüelles et al. / Estuarine, Coastal and Shelf Science 114 (2012) 59e6964

pronounced due to its confinement, which probably led to anincrease in the effect of evaporation. The shift of Cal Tet lagoon froma clear to a turbid state was probably the cause for the trend ofvariation along the Secchi depth gradient of the Cal Tet samples inthe PCA analysis. In Remolar, although seasonal trends weremaintained, the influence of the incoming nutrient-enriched fluxeswas very important. These fluxes might have been responsible forthe alternative NO�

3 and NHþ4 dominance over total DIN in this

lagoon, being probably linked to reduction/oxidation processes of Nruled by organic matter mineralization under anaerobic conditions(Lucena et al., 2002). It has been proved that when no oxygen isavailable, NO�

3 acts as a source of oxygen for benthic microorgan-isms (Rheinheimer, 1992; Herbert, 1999), while NHþ

4 is releasedinto the lagoon (Pretus, 1989; Chapelle et al., 2000; Nizzoli et al.,2007). Another consequence of these sewage fluxes was thepermanent stratification of the lagoon. Surface waters were freshand oxygen-over-saturated, while bottom waters were saline(zseawater), anoxic and registered low pH values. This situationhad been previously reported by Lucena et al. (2002) for this

lagoon, and has been also reported for other enriched transitionalwaters like Vistonis lagoon in Northern Greece (Markou et al.,2007). The oxygen oversaturation of surface waters might havebeen linked to high chlorophyll-a concentrations supported bynutrients availability, while bottom anoxia and low pH might havebeen a consequence of intense mineralization of organic matter(Lucena et al., 2002; D’Autilla et al., 2004; Markou et al., 2007;Mudge et al., 2007). A similar vertical profile was registered in Cal’Arana, although in this case the halocline was deeper and wasprobably formed because of the depth of the lagoon and the poorwater renewal, which have been reported to be possible causes forstratification (López et al., 1984; da Fonseca et al., 2001). Thefreshwater release led to a better mix of waters and a homogeni-zation of the conductivity profile, but it had no influence overbottom pH and oxygen conditions. Transparency of the waterincreased (from 1.1 � 0.1 m of Secchi disk before the freshwaterrelease to 1.6 � 0.5 after it), but still light penetration was poor,inhibiting primary production at the bottom. Moreover, since thelagoon was completely confined, the freshwater release probably

Table 1Spearman correlations of nutrients with secondary (conductivity, major ions, Secchi depth, solid suspended solids and temperature) and response (chlorophyll-a and dissolvedoxygen) variables. Only significant correlations are shown. *¼ 0.01< r� 0.05; *¼ r< 0.01. DIN¼Dissolved Inorganic Nitrogen; SRP¼ Soluble Reactive Phosphorus; SI¼ Silica;TOC ¼ Total organic Carbon; TP ¼ Total Phosphorous.

NO�3 NOþ

4 SRP TP-SRP DIN/SRP TOC SI

rs p rs p rs p rs p rs p rs p rs p

RemolarChlorophyll-a 0.60 *

DO (Surface) 0.66 ** �0.72 **

Ta (Surface) �0.86 **

Ta (Deep) �0.68 **

Secchi (Deep) 0.64 **

SSP 0.62 *

Conductivity (Deep) �0.68 **

Cl- 0.67 **

SO2�4 0.59 *

Ca l'AranaDO (Deep) �0.58 * 0.71 **

Ta (Deep) 0.74 ** �0.59 *

SSP 0.68 **

pH (Surface) �0.68 *

Conductivity (Surface) 0.55 *

Ca2+ 0.54 *

Cl� 0.57 *

Mg+ 0.54 *

Mn2+ �0.69 **

Na+ �0.61 * 0.56 *

RicardaDO (Surface) �0.72 ** 0.90 **

DO (Deep) �0.57 *

Ta (Surface) 0.74 ** 0.54 *

Ta (Deep) 0.82 **

Secchi depth �0.57 * �0.68 ** �0.64 *

SSP 0.69 ** 0.80 **

pH (Surface) 0.65 *

Conductivity (Surface) 0.73 **

Conductivity (Deep) 0.55 * 0.65 *

SO2�4 0.58 *

Cal TetDO (Deep) 0.76 **

pH (Surface) �0.65 *

Ca2+ 0.77 **

Mg+ 0.66 **

Mn2+ 0.57 *

M. Cañedo-Argüelles et al. / Estuarine, Coastal and Shelf Science 114 (2012) 59e69 65

washed-out some suspended particles from the lagoon’s surfacewaters (as reflected in the decrease of TOC and SSP concentrations)but organic material might have remained in its bottom, main-taining a high oxygen demand due to mineralization, which isa typical situation of lagoons with poor flushing rates (Mudge andDuce, 2005; Mudge et al., 2007).

The main dissolved nitrogen formwas NO�3 . This form is a major

component of plant fertilizers, and its concentrations in transitionalwaters are usually linked to runoff discharges which lixiviate theexcess from plant uptake (Kormas et al., 2001; Newton and Mudge,2005; Coelho et al., 2007; Zaldívar et al., 2008). This might be truein Ca l’Arana, where NO�

3 concentrations were higher in the rainymonths and were negatively correlated to surface pH, but theinfluence of runoff was not evident for Remolar and Ricarda, wherepoint-source NO�

3 discharges via wastewater channels were prob-ably a more important source. Nonetheless, the high NO�

3concentrations of Cal Tet (annual mean of 95 � 91 mmol l�1), whichis a young lagoon (created in 2003) relatively isolated from humanaction and which does not receives any artificial water discharge,suggested the existence of an additional NO�

3 source. According tothe Catalonian Water Agency (Agencia Catalana de l’Aigüa), themean concentrations of dissolved nitrogen forms in 2003 in thesuperficial aquifer of the Llobregat’s delta in the area where thepresent study was performed were: NO�

2 ¼ 1.4 mmol l�1;NO�

3 ¼ 864.1 mmol l�1; NHþ4 ¼ 20.7 mmol l�1 (information available

inwww.gencat.cat/aca). This would explainwhy Cal Tet, which wasexclusively fed with ground waters, registered high NO�

3 concen-trations, and would probably have been in part responsible for thehigh NO�

3 concentrations of the rest of the lagoons.Concerning the DIN:SRP molar ratios, they were much higher

than the Redfield ratio (Redfield, 1958) in three of the four lagoons,suggesting phosphorous limitation. Accumulating evidencessuggest that P might be limiting ocean production as a wholebecause of the importance of N fixation as a source of N comparedto the limited P sources (Smith, 1984), while coastal waters mightbe N limited (Hecky and Kilham, 1988; Taylor et al., 1995; Howarthand Marino, 2006) because of the low N:P ratio in domestic sewageand the more rapid regeneration of P from dying plankton (Rytherand Dunstan, 1971). In spite of the advances, nutrients limitation incoastal waters is still an open question. In the case of the Medi-terranean coast, Kormas et al. (2001) suggested that is P-limited,while Souchu et al. (2010) suggested that the identity of theprimary growth-limiting nutrient in Mediterranean coastal lagoonsmay shift from P alone in oligotrophic lagoons to N alone aseutrophication proceeds. The low N:P ratios of Ricarda (less than16:1) suggest N-limitation in the coastal waters of the Delta, since itmaintained a good water renewal and a continuous mix withseawater. Nonetheless the N-limitation of coastal waters might notnecessarily be translated into an N-limitation of the coastal lagoons,especially when they are under high anthropic pressure. In the

Fig. 6. Nitrate/dissolved inorganic nitrogen (NO�3 /DIN) expressed as percentage (lower

graph) and phosphate/dissolved inorganic nitrogen (SRP/DIN) molar ratios (uppergraph) for each of the studied lagoons along the study period. Redfield N:P ratio (1:16)is marked with a dashed line. CA ¼ Ca l’Arana; CT ¼ Cal Tet; RE ¼ Remolar;RI ¼ Ricarda.

Fig. 7. Application of Carlson’s (1977) phosphorous (TP) and chlorophyll-a (Chl-a)trophic state indices (TSI). Class limits are separated by dashed lines. O ¼ oligotrophic;OM ¼ oligomesotrophic; M ¼ mesotrophic; E ¼ eutrophic; EH ¼ eutrophic to hyper-eutrophic; H ¼ hypereutrophic. CA ¼ Ca l’Arana; CT ¼ Cal Tet; RE ¼ Remolar;RI ¼ Ricarda.

M. Cañedo-Argüelles et al. / Estuarine, Coastal and Shelf Science 114 (2012) 59e6966

present study, P was the limiting factor in the more confinedlagoons of Cal Tet and Ca l’Arana, where ground waters rich in NO�

3were the main water source, and the hypereutrophic lagoon ofRemolar, which receives large amounts of nutrient-rich waters(Lucena et al., 2002). This P limitation in transitional waters due tothe high release of N from agricultural land (runoff) and streams(point-sources) might be amore common situation than it has beentraditionally assumed, since it has been recently reported for othercoastal lagoons like Ria Formosa (Newton et al., 2003; Newton andMudge, 2005) and Foz de Almargem (Coelho et al., 2007). In spite ofthe P limitation, it has to be noticed that this only means that P is inan amountmost closely approaching the critical minimum requiredto sustain algal activity (Odum, 1971), but ambient phytoplanktongrowth rates might not be affected by this limitation, especially ineutrophic waters, where the absolute concentration of N and Pmight be enough to sustain optimal growth (Maier et al., 2009). Insystems exposed to excessive nutrient overenrichment like theLlobregat’s delta, light availability is more likely to limit phyto-plankton growth than N or P (Kocum et al., 2002a, 2002b). Thiscould explain why chlorophyll-a concentrations had a low weightin the principal component analyses and were not significantly

related to any nutrient concentration in the present study. Incoastal lagoons, benthic vegetation and algal productivity wouldprobably be more coupled to nutrient enrichment and constitutea better approximation to systems’ productivity than phyto-plankton (Giordani et al., 2009).

Trophic state indices constituted a good approach to the trophicstate of the hypereutrophic lagoon of Remolar, which was placed inthe worst category according to TSI (Carlson, 1977) and TRIX(Vollenweider et al., 1998), and in agreement with the EuropeanEnvironmental Agency (2009) and the Water Framework Direc-tive (Best et al., 2007) class limits. In the case of the other threelagoons, there were important differences in their classificationregarding which index was used, and the indices did not reflect theinfluence of the main human pressures on the lagoons. In spite ofthis, the indices’ values followed similar trends. Therefore, thedifferences in the classification of the lagoons were more related todifferences in the indices’ quality class boundaries than to differ-ences in the indices’ values. Ca l’Arana and Ricarda lagoons ob-tained very similar values for the TSI and TRIX indices; nonetheless,

Fig. 8. Application of Vollenweider’s et al. (1998) TRIX index. Class limits are separatedby dashed lines. CA ¼ Ca l’Arana; CT ¼ Cal Tet; RE ¼ Remolar; RI ¼ Ricarda.

M. Cañedo-Argüelles et al. / Estuarine, Coastal and Shelf Science 114 (2012) 59e69 67

according to the WFD proposal based in minimum DO concentra-tions (Best et al., 2007) Ricardawas categorized as “good” and “fair”,while Ca l’Arana was categorized as “bad”. In this case trophic stateindices did not reflect the real trophic state of the lagoons, since thetrophic state of Ca l’Arana should be worst according to the mani-festation of eutrophic symptoms (anoxia and low pH in thebottom); and the proposal of Best et al. (2007) constituted a betterapproximation. Moreover the freshwater releases to these lagoons,in spite of having a high weight in the principal component

Table 2Categorization of the lagoon’s trophic state according to oxidized nitrogen and orthophospMinimum Dissolved Oxygen concentrations proposed for the WFD by Best et al. (2007)mmol l�1): **** ¼ 0. e0.5; *** ¼ 0.5e0.7; ** ¼ 0.7e1.1; * ¼ >1.5. WFD (DO, mg l�1): * ¼

2004

Jn Jl Ag Sp Ot Nv Dc

RemolarDIN [mmol l�1] 2391 1173 294 379 1082 545 17EEA * * * * * * *

SRP [mmol l�1] 79.68 19.03 8.39 21.29 10.00 4.19 20EEA * * * * * * *

DO [mg l�1] 0.17 0.00 0.04 0.04 0.10 0.00 0.WFD * * * * * * *

Ca l’AranaDIN [mmol l�1] 33 95 102 177 468 220 32EEA * * * * * * *

SRP [mmol l�1] 1.62 1.61 0.66 2.90 1.61 1.94 1.EEA * * *** * * * *

DO [mg l�1] 3.20 0.00 0.00 0.00 0.00 0.10 0.WFD *** * * * * * *

RicardaDIN [mmol l�1] 32 107 292 156 454 418 33EEA * * * * * * *

SRP [mmol l�1] 0.98 6.65 7.80 32.97 54.53 74.77 28EEA ** * * * * * *

DO [mg l�1] 5.10 18.80 4.20 3.50 5.72 10.56 13WFD **** ***** **** *** ***** ***** **

Cal TetDIN [mmol l�1] 34 32 127 61 725 46 33EEA * * * * * * *

SRP [mmol l�1] 0.32 0.55 1.07 0.36 3.68 1.93 0.EEA **** *** ** **** * * **

DO [mg l�1] 10.33 9.22 9.52 9.50 9.38 5.79 7.WFD ***** ***** ***** ***** ***** ***** **

analyses and important consequences for the aquatic macro-invertebrate fauna (Cañedo-Argüelles and Rieradevall, 2010), werenot detected by changes in the values of the trophic state indices orin the categorization of the lagoons according to the EEA (2009) andtheWFD proposal of Best et al. (2007). Concerning the lagoon of CalTet, trophic state indices registered important seasonal changes,probably related to the high influence of evaporation due to theconfinement of the lagoon. The best trophic state was registered inwinter, when evaporation is lower and nutrients are more diluted.The lagoon was categorized as “good” and “fair” according to DO(Best et al., 2007) class limits, while it was categorised as “bad”according to oxidized nitrogen and orthophosphate thresholds(European Environmental Agency, 2009). It has to be noticed thatthe categorization of the EEA is based on the analyses of theMediterranean coastal waters, which are oligotrophic, and it wasprecisely in the areas close to rivers’ mouths (as in example the PoRiver’s mouth in Italy) were higher oxidized nitrogen and ortho-phospate concentrations were recorded. The oxidized nitrogen andorthophosphate values recorded in the present study are far awayfrom the worst values reported for the Mediterranean coastalwaters (European Environmental Agency, 2009), suggesting thatthe proposed categorization might not be valid for Mediterraneancoastal lagoons, for which new specific approaches are required.

The results of the present investigation suggest that phase Imodels, based on nutrient loading and oxygen and chlorophyll-a response (Cloern, 2001), might have limited use when assessingthe trophic state of coastal lagoons, especially when they areheavily impacted by human action. Indices should be improved orcomplemented in order to integrate secondary variables, seasonalvariations and anthropogenic pressure (Cartensen, 2007). Thesusceptibility of the lagoons to eutrophication should also be takeninto consideration through the identification of areas of restrictedexchange with the sea (Mudge et al., 2008), which are moresensible to eutrophication (Tett et al., 2003; Zaldívar et al., 2008).

hate class limits defined by the European Environmental Agency (EEA, 2009) and the. EEA (DIN, mmol l�1): **** ¼ 0e6.5; *** ¼ 6.5e9; ** ¼ 9e16; * ¼ > 55. EEA (SRP,<1.6; ** ¼ 1.6e2.4; *** ¼ 2.4e4.0; **** ¼ 4.0e5.7; ***** ¼ >5.7.

2005

Ja Fb Mr Ap My Jn Jl

10 681 2861 1319 1637 1954 879 799* * * * * * *

.32 240.67 59.03 9.35 73.77 61.29 16.13 28.39* * * * * * *

00 0.00 0.00 0.05 2.50 0.01 0.00 0.00* * * ** * * *

6 276 40 35 33 33 75 36* * * * * * *

77 2.90 1.69 3.05 1.61 7.74 1.69 1.94* * * * * * *

60 0.00 0.00 0.00 3.00 0.08 0.07 0.00* * * *** * * *

36 32 71 52 33 85 33* * * * * * *

0.32 0.87 7.88 4.37 98.62 3.50 27.81 4.07** * * * * * *

.41 13.28 10.53 13.61 8.90 7.04 6.95 4.79*** ***** ***** ***** ***** ***** ***** ****

112 40 35 36 33 75 32* * * * * * *

57 0.24 0.26 2.28 0.16 0.16 0.36 2.26* **** **** * **** **** **** *

35 10.00 12.97 13.41 13.10 9.15 9.33 6.53*** ***** ***** ***** ***** ***** ***** *****

M. Cañedo-Argüelles et al. / Estuarine, Coastal and Shelf Science 114 (2012) 59e6968

For this purpose new tools like i.e. the physically sensitive areas(PSA) index (Druon et al., 2002), based on the physical resistance ofthe lagoons to eutrophication, can be very helpful. At the sametime, the identification of all the potential nutrients sources,including groundwaters, whichmay represent 50% of water budgetin wetlands and their associated water bodies (Howard-Williams,1985), seems indispensable to an appropriated management ofthe system (Bricker et al., 2003). According to Cloern (2001), theactual view of coastal eutrophication is still limited, since it comesfrom site-specific assessments (with limited experimentation andsimulation modelling) and from a few highly impacted regions ofthe developed world, mostly at temperate latitudes; but it seemseven more limited in the case of coastal lagoons. In these ecosys-tems there is still much work to do concerning the validation oftrophic state indices (Basset and Abbiati, 2004; Coelho et al., 2007;Salas et al., 2008) and the development and application of newtools, integrating the vulnerability of the system to the humanimpact. The correct evaluation of such pressures can have majorconsequences for restoration processes since their interactions canlead to hysterical responses of the ecosystem, meaning thatrestoring previous conditionsmight not be enough to go back to thereference state once certain thresholds have been exceeded (Duarteet al., 2009). In this sense, a helpful tool can be found in thePressure-State-Response models (Bricker et al., 2003; Boyes andElliott, 2006; Zaldívar et al., 2008), which promote an integrationof human influence (Pressure), primary and secondary eutrophi-cation symptoms (State) and the definition of future actions tosolve the problem (Response). Therefore, we suggest that theassessment of the quality of transitional waters would benefit fromthe combination of phase-I derived indices like TRIX with othertools coming from a DPSIR approach that could incorporate thesusceptibility of the system to eutrophication.

Acknowledgments

This project was financed by the Generalitat de Catalunya. Wewould like to thank the ERASMUS initiative of the European Unionfor making possible the collaboration between the University ofBarcelona and the University of Algarve. Wewould like to thank theConsorci del Delta del Llobregat and Taller d’Enginyeria Ambientalfor providing us with logistical support.

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