Assessing eutrophication in the Portuguese continental Exclusive Economic Zone within the European Marine Strategy Framework Directive

Ecological Indicators 58 (2015) 286–299

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Assessing eutrophication in the Portuguese continental Exclusive Economic Zone within the European Marine Strategy Framework Directive Maria Teresa Cabrita ∗ , Alexandra Silva, Paulo B. Oliveira, Maria Manuel Angélico, Marta Nogueira Portuguese Institute of Sea and Atmosphere (IPMA), Av. Brasília, 1449-006 Lisboa, Portugal

a r t i c l e

i n f o

Article history: Received 14 August 2014 Received in revised form 20 May 2015 Accepted 22 May 2015 Keywords: Eutrophication assessment Portuguese continental EEZ Marine Strategy Framework Directive

a b s t r a c t This study reports the state and causes of eutrophication in the Portuguese continental Exclusive Economic Zone (EEZ), during a 14-year period (1995–2008), following the European Marine Strategy Framework Directive (MSFD) and using the trophic index TRIX for an integrated evaluation of indicators of eutrophication, and identifies areas where monitoring is needed to improve the eutrophication assessment. A non-continuous dataset for the 8 indicators specified by the MSFD for eutrophication assessment was used, including published and grey data. Eutrophication indicators were validated and thresholds reviewed, considering regional differences. The diatom:flagellate ratio was found a poor indicator of eutrophication as shifts in the diatom:flagellate ratio naturally occur associated with alternating water column turbulence and upwelling, and stratification, and therefore, could not be associated with anthropogenic nutrient enrichment effects. Assessment areas were, as a whole, classified as non-problem areas concerning eutrophication. Although nutrient enrichment was observed in coastal waters, related to river plume influence, nutrient enrichment direct and indirect effects were generally not detectable, possibly due to water column dispersion and mixing processes. Only occasionally, mild eutrophication was found in specific areas under the influence of major river (Douro, Vouga and Guadiana) plumes, associated with high nutrient and phytoplankton biomass levels and seagrass decline, which indicates the need for directed monitoring on eutrophication in those areas. © 2015 Elsevier Ltd. All rights reserved.

1. Introduction Eutrophication, defined as “the enrichment of water by nutrients, especially compounds of nitrogen (N) and/or phosphorus (P) causing an accelerated growth of algae and higher forms of plant life to produce an undesirable disturbance to the balance of organisms present in the water and to the quality of the water concerned” (Ferreira et al., 2010), has been one of the most important causes of water quality impairment and a major threat to the health of estuarine, coastal and marine ecosystems, for more than four decades (Ryther and Dunstan, 1971; Nixon, 1995; Bachmann et al., 2006; Howarth et al., 2011). The increasing number of areas worldwide experiencing symptoms of eutrophication stresses the global scale of the problem (OSPAR, 2003; Bricker et al., 2007;

∗ Corresponding author at: IPMA, Av. de Brasília, 1449-006 Lisboa, Portugal. Tel.: +351 213 027 000; fax: +351 213 015 948. E-mail address: [email protected] (M.T. Cabrita). http://dx.doi.org/10.1016/j.ecolind.2015.05.044 1470-160X/© 2015 Elsevier Ltd. All rights reserved.

Selman et al., 2008). Approximately 65% of Europe’s Atlantic coast displays signs of eutrophication. Human activity in coastal areas has greatly accelerated the rate and the extent of eutrophication through N and P overloading (Nixon, 1995; Rabalais, 2002), triggered by point discharges (e.g. municipal and industrial effluents) and diffuse input (e.g. agricultural leaching and run-off, and atmospheric deposition) into the coastal and marine environment (Carpenter et al., 1998). Consequences of eutrophication are oxygen deficiency in bottom waters, occurrence of harmful algal blooms, benthic organism death, declines in seagrasses, and changes of biodiversity (Riegman, 1995; Smith et al., 1999; Cloern, 2001; Glibert et al., 2005). These environmental damaging events compromise the sustainable provision of services and goods by coastal and marine ecosystems (Liquete et al., 2013). According to Costanza et al. (1997) and Martinez et al. (2007), the oceans and mainly the coastal zone contribute to around 60% of the total economic value of the biosphere. Landscape, recreation activities, fish and shellfish are only a few of the services and goods threatened by eutrophication in coastal and marine areas, with dramatic impact

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on the coastal communities’ subsistence and on the economy of the countries. Human-induced eutrophication can be minimized through management measures that include the reduction in nitrogen (N) and phosphate (P) loadings to coastal waters (Kemp and Goldman, 2008). However, these actions might not result into immediate recovery towards a more pristine state because eutrophication in coastal ecosystems shows various patterns of spatial inshore-offshore and along shore gradients, have intrinsic large interannual variability in both intensity and extension, particularly in areas under direct influence of major rivers (Rinaldi and Montanari, 1988; Riisgard et al., 1996). Moreover, released nutrients in these coastal marine areas may be diluted and dissipated through tidal action, currents, weather and wind conditions, and also rapid uptake by marine plants (Glibert and Goldman, 1981; Wheeler et al., 1982; Vollenweider et al., 1998), and therefore, direct measurement of water column N and P concentrations alone to estimate over-enrichment has been found useless (Lee et al., 2004). An integrated evaluation of indicators of eutrophication, particularly in the over-enrichment early stages, also including oxygen saturation and plant biomass, is thus critical for effective eutrophication assessment and management. In fact, the multidimensional nature of eutrophication means that no single variable is representative of the eutrophication status. More robust trophic state criteria or indices using multivariate approaches have been proposed, mostly for lakes (Carlson, 1977; Walker, 1979; Aizaki et al., 1981; Xu et al., 2001). The trophic state index (TSI) based on several physical, chemical and biological indicators, particularly the Carlson-type TSI, offers a suitable and acceptable method which has been widely used to evaluate lake eutrophication (Carlson, 1977). Direct transfer of limnological models unmodified to marine conditions, however, is largely inappropriate because gradients in lakes are usually modest, and limnological trophic criteria intend to characterize lakes in their entirety. The development of a trophic index (TRIX), suitably adapted to marine water features, based on Carlson’s TSI, was created by Vollenweider et al. (1998), allowing to synthesize key data into a simple numeric expression to make information comparable over a wide range of spatial and temporal trophic situations. The use of this marine water adapted trophic index will greatly improve eutrophication assessments and increase the feasibility of marine ecosystem management planning. In Europe, conventions and legislation, and more recently the Marine Strategy Framework Directive (MSFW, European Commission, 2008) have been developed to improve water quality. The MSFD establishes a framework to support marine strategies aiming to prevent deterioration or restore adversely affected marine areas, and to prevent and reduce inputs in the marine environment, to achieve or maintain Good Environmental Status (GES) by 2020, within the European Union (EU) Exclusive Economic Zone (EEZ). The directive explicitly considers eutrophication among the water quality descriptors, providing practical guidelines and methodologies (European Commission, 2008; Ferreira et al., 2011) that may be used for coastal and marine eutrophication assessment, to ensure that the specificity of each EU marine region or subregion is taken into consideration. As an EU member state, Portugal is committed to apply the integrated ecosystem-based approach provided by the MSFD, giving priority to the attainment of “good environmental status” through the assessment of the environmental descriptors, including eutrophication (Descriptor 5). The Portuguese EEZ comprises three large areas associated with the Azores and Madeira archipelagos and the Portuguese continental EEZ which is the focus of the present work. This area in particular is part of the North-east Atlantic Ocean marine region included in the target areas defined by the MSFD, and was classified as NonProblem Area, according to the national initial assessment report (MAMAOT, 2012) for the application of the Directive in Portugal.

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This study presents the outcome of a second application of the MSFD to the Portuguese continental EEZ, using an extended dataset to support a more complete coverage of coastal areas affected by river plumes of major rivers and submarine outfalls. A thorough review was undertaken of the thresholds applied for each of the Assessment Criteria, considering regional differences. The present assessment follows the MSFD recommendations as closely as possible in the light of the characteristics of Portuguese waters, but taking account of lessons learned from the first application and our developing understanding of overall ecological status. Here we hypothesize that fluctuations in eutrophication in the Portuguese continental EZZ are triggered by the seasonality of the hydrodynamic regime (e.g. river runoff) and by geographic specificities. We have employed methods that were considered to be more accurate and improve the quality of the assessment and evaluated the trophic status and water quality, following MSFD indications and also by using the trophic index TRIX. This study investigates effective and reliable eutrophication indicators for open coastal areas, reports the trophic status and causes of eutrophication in the Portuguese continental EEZ, and identifies areas where an increased monitoring effort is needed to improve the assessment, within the scope of the MSFD. A noncontinuous dataset over a 14-year period (1995–2008) for the 8 indicators specified by the MSFD for the assessment of eutrophication is presented, by gathering both published and grey data. A comprehensive assessment of eutrophication for the Portuguese continental ZEE has never been published, and therefore the results herein presented should be significantly important, at international, national and regional levels, and definitely to an integrated overview of eutrophication worldwide.

2. Materials and methods 2.1. Assessment areas The Portuguese continental EEZ comprises 327 667 km2 (Fig. 1) corresponding to 19% of the total Portuguese EEZ area, one of the largest in Europe. Its geography can be briefly summarized as a continental margin divided into subregions by the occurrence of seamounts, submarine canyons and abyssal plains. The shelf break occurs at depths of around 150 m throughout the region, with steep slopes in the northwest and south coasts and gentle slopes down to 1000 m off the southwest coast. From the oceanographic point of view, the main distinctive characteristics are a strong seasonal and interannual variability on the hydrology and circulation of the upper layers (0–200 m), and the influence of the Mediterranean outflow on the water mass characteristics at depths around 1000 m, also impacting the upper-layer dynamics through its interaction with the Azores Current (Peliz et al., 2007; Kida et al., 2008). A large fraction of this variability is forced by the winds and fresh water input from river runoff that change at seasonal and interannual time-scales. At the seasonal timescale, the fluctuations are driven by the alternation between the summer northerly winds (responsible for a coastal upwelling current system along the west coast) and low precipitation regime, and the more variable winter winds with events of strong southerly winds and high precipitation (Wooster et al., 1976; Fiúza et al., 1982). In summer, coastal upwelling jets bring cold and nutrient rich subsurface waters to the surface and promote the export of shelf waters rich in organic matter into offshore oligotrophic waters (Fiuza, 1983; Haynes et al., 1993; Álvarez-Salgado et al., 2007). During winter, the river runoff is responsible for the formation of low salinity plumes, still traceable in summer, especially in the northern coast, where a higher number of coastal water bodies can be found in comparison with the remaining coastal areas

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2.2. Dataset and confidence in the assessment

Fig. 1. Map of the Portuguese continental EEZ showing bathymetry, the 100 m isobath, assessment areas (A1, A2, B1, B2, C1, C2), sampling and reference (RA1, RA2, RB1, RB2, RC1, RC2) stations. Location of major river mouths (Douro, Vouga, Tagus, Guadiana) and other less important rivers is also indicated.

(Fig. 1). These buoyant plumes respond rapidly to wind changes and have a strong impact both on the inner-shelf dynamics, due to the increased density gradients, and on the biological fields due to their efficiency in providing a mean for organic matter retention (Santos et al., 2004; Ribeiro et al., 2005; Otero et al., 2008). The Portuguese continental EEZ was divided into smaller sub-areas due to the geographic and oceanographic spatial heterogeneity of this wide region (Fig. 1). The limits of the assessment areas were adopted from the Water Framework Directive (WFD) for coastal waters (Bettencourt et al., 2004) and were lengthen up to the EEZ boundaries, resulting in three major areas, herein designated as A, B and C, from north to south (Fig. 1). These areas included zones of coastal water under the influence of both river (Oliveira, 1994) and upwelling plumes (Fiúza et al., 1982; Silva, 1987, 1992), and offshore areas, either well mixed or seasonally stratified. Assuming that eutrophication is mostly associated with nutrient enriched freshwater inputs and to ensure that any eutrophication problems were not overlooked, the assessment areas A, B and C were further divided longitudinally on the basis of salinity gradients that resulted from the mixing of freshwater and seawater, in order to separate the coastal plume influenced strip (A1, B1 and C1, Fig. 1) from the offshore area (A2, B2 and C2, Fig. 1). The salinity regimes adopted were 30.0–34.5 for coastal waters and >34.5 for offshore waters, as recommended by the OSPAR North-East Atlantic Strategy guidelines (OSPAR, 2002). Assessment sampling stations were located over 7 cross-shelf transects, each composed of 10 stations on average), and 4 high spatial resolution areas (covering Tagus, Sado, Ria Formosa and Guadiana adjacent waters), over the Portuguese continental shelf up to the 3000 m isobath (Fig. 1). The sampling stations located in offshore areas were few but considered representative, as the influence of terrestrial anthropogenic input is almost absent in offshore areas.

Table 1 presents information on the dataset analyzed in this paper, regarding data sources and bibliography, sampling period, spatial and temporal data coverage, and sampling methods for each eutrophication parameter. A non-continuous 14-year period (1995–2008) was covered, including (i) unpublished data from Instituto Português do Mar e da Atmosfera (IPMA), and data from SNIRH (Sistema Nacional de Informac¸ão de Recursos Hídricos), and Programa Nacional de Amostragem Biológica/Data Collection Framework (PNAB/DCF) Portuguese monitoring programs, regarding salinity (S), dissolved inorganic nitrogen (DIN: NH4 + + NO3 − + NO2 − ), dissolved inorganic phosphate (PO4 3− ), dissolved inorganic silicate (Si(OH)4 ), chlorophyll a concentration (Chl a), water transparency, and dissolved oxygen (DO), and (ii) published data on phytoplankton composition, opportunistic macroalgae, and perennial seaweeds and seagrasses, and (iii) satellite remote sensing data on Chl a, obtained on a weekly basis, from ESA’s GlobColour Project (Lavender et al., 2008). Sampling methods varied from in situ sampling to satellite remote sensing which was essentially used to obtain Chl a data. The sampling period varied for each assessment indicator, covering all or most of this study time frame, with the exception of water transparency and DO, with short sampling periods. Data referred largely to coastal areas, which were intensively surveyed, over the Portuguese continental shelf up to the 3000 m isobath; most of the offshore areas beyond the 3000 m bathymetric line were rarely or never sampled (see also Fig. 1). There were also variations in data coverage between areas and different parameters, reflecting the level of sampling effort and monitoring practicalities. Although in situ records were scattered for all the assessment parameters, temporal data coverage was moderate in western coastal areas due to the availability of relatively extensive datasets, but low in the south coast. In spite of the additional data covering river plumes of major rivers and submarine outfalls zones used in the present study in relation to the first MSFD report dataset (MAMAOT, 2012), in this area temporal coverage was still poor and variable, ranging from monthly observations to occasional samples in limited periods of the year, in particular for water transparency, HABs, macroalgae and DO. Therefore, confidence in the assessment of eutrophication within coastal areas and for coastal and offshore waters was not carried out on a comparable basis. Confidence rating of individual indicators was based on the number of years with complete data coverage, considering high (≥5 years), moderate (3–4 years) or low (1–2 years) scores, following HELCOM (2013). Chlorophyll a scored high for the entire EEZ area, nutrients scored moderate for the areas A1, A2, B1, and B2, and low for areas C1 and C2, the remaining indicators scored low for the entire EEZ. Overall, confidence was considered moderate for the western coastal areas, but low in the south coast. 2.3. Indicators for eutrophication assessment Eight indicators grouped within 3 criteria categories were used for the assessment of eutrophication, following the MSFD (Table 2). Statistical measures employed for each indicator followed recommendations by MSFD (OSPAR, 2012), and are also presented in Table 2. Mean values were used for nutrients, N:P ratio, water transparency, diatom:flagellate ratio, 90th percentile (P90) for Chl a, and 10th percentile (P10) for DO. 2.4. Methodologies, reference conditions, thresholds and scoring system In order to find the temporally appropriate datasets to be used for the assessment of each eutrophication indicator: (i) seasonal datasets (e.g. the productive period and/or winter nutrients), or

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Table 1 Data sources and bibliography, sampling methods, sampling period, and spatial and temporal data coverage, for each eutrophication parameter used for the assessment of eutrophication in the Continental Portugal ZEE. Assessment parameter

Data sources and bibliography

Sampling methods

Sampling period

Spatial data coverage

Temporal data coverage

S

IPMA’s unpublished data SNIRH Amostragem Biológica/Data Collection Framework (PNAB/DCF) Portuguese monitoring programs IPMA’s unpublished data SNIRH

In situ multiple digital sensor measuring

2000–2008

Coastal waters and up to the 3000 m isobath

Numerous, scattered records

In situ water sampling

1995–2000, 2002–2005 (A1) 1995–2000, 2004–2005 (A2) 1995–2007 (B1, B2) 1995–96, 1998–2004 (C1) 1995–96, 1998–2001 (C2)

Coastal waters and up to the 3000 m isobath

Numerous, scattered records (A1, A2, B1, B2) Few, scattered records (C1, C2)

IPMA’s unpublished data SNIRH d’Andon null 2008

In situ water sampling

1995–2008 1998–2008

Coastal waters and up to the 3000 m isobath Entire EEZ

In situ determination

1995–1998

Coastal waters

Numerous, scattered records (A1, A2, B1, B2) Few, scattered records (C1, C2) Numerous records evenly distributed Few, scattered records

In situ water sampling

1995–2008

Coastal waters and up to the 3000 m isobath

Few, scattered records

In situ sampling

1995–2008

Coastal waters

Few, scattered records

In situ sampling

1995–2008

Coastal waters

Numerous, scattered records

In situ sampling

1995–2008

Coastal waters

Numerous, scattered records

In situ water sampling

1998–2000

Coastal waters

Few, scattered records

DIN

PO4 3− Si(OH)4 Chl a

Water transparency

Phytoplankton composition

Opportunistic macroalgae abundance Perennial seaweed abundance

Seagrass abundance

DO

IPMA’s unpublished data SNIRH IPMA’s unpublished data Sordo et al. (2000) Moita (2001) Moita and da Silva (2002) Pitcher et al. (2010) Mateus et al. (2013) Pardo et al. (2011)

Palminha (1951) Mesquita Rodrigues (1963) Ardré (1970, 1971) Melo and Santos (1982) Sousa-Pinto and Araújo (1998, 2006) Cardoso et al. (2004) Marques (2012) Cunha et al. (2013) Green and Short (2003) Krause-Jensen et al. (2004) Cunha et al. (2013) IPMA’s unpublished data SNIRH

Satellite remote sensing

(ii) annual cycle, more adequate for marine areas with less well defined seasonality, as recommended by Ferreira et al. (2010), deviations of monthly medians to the grand median for nutrient and Chl a concentrations were used to highlight seasonal patterns, as suggested by Cloern et al. (2007). Because data concerning these parameters did not follow normal distribution, with occasional unusual values, median was used as more representative measure of central tendency to evaluate seasonal patterns. Firstly, monthly medians were calculated by gathering data (mean values for nutrients and 90th percentile for Chl a) from all stations in an assessment area, for the same month of all the different years (i.e. median of all January months), and designated hereafter as the monthly median. Secondly, data from all stations and

dates from an assessment area were used to compute the grand median. Seasonal patterns were then highlighted by the deviation of the monthly medians from the grand median. Average values relative to the temporally appropriate period found, winter nutrients/productive period or annual cycle, were then calculated for each indicator, and used to assess deviations from threshold values. This method greatly improved the accuracy in the definition of the above-mentioned assessment periods, in comparison with the methodology applied in the first MSFD assessment for Portuguese continental EEZ (MAMAOT, 2012). In the case of the N:P ratio, monthly median deviation from the Redfield N:P ratio, used as reference (C:N:P, 106:16:1), was determined to measure variability within the month and assess imbalance in dissolved inorganic N

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Table 2 Criteria (I: Nutrient enrichment, II: Direct effects of nutrient enrichment, III: Indirect effects of nutrient enrichment), indicators, statistical measures and determination of assessment values (thresholds) for the assessment of eutrophication for the Continental Portugal ZEE. Criteria

Indicator

Statistical measures

Determination of assessment level (threshold)

Category I: Nutrient enrichment

DIN PO4 3− Si(OH)4 N:P ratio

Monthly mean and median concentration

Increased level of winter or annual DIN, PO4 3− and Si(OH)4 not exceeding 50% from background

Monthly mean and median 90th percentile concentration Monthly mean

Elevated winter or annual N:P ratio, using as reference the Redfield N:P ratio (16) and threshold (24) Elevated level of productive period or annual Chl a concentration not exceeding 50% from background Reduced water transparency related to increase in suspended algae, in relation to background Shifts in diatom:flagellate ratio Elevated levels of nuisance/toxic phytoplankton species

Chl a Category II: Direct effects of nutrient enrichment

Water transparency Diatom:flagellate ratio Nuisance/toxic algal bloom events

Opportunistic macroalgae abundance Perennial seaweed and seagrass abundance Category III: Indirect effects of nutrient enrichment

DO

Monthly mean and median Concentration Bloom occurrence Community structure changes Bloom occurrence Biomass and community structure changes 10th percentile concentration

and P concentrations (N:P, 16:1). The Dortch and Whitledge (1992) criteria was also used to evaluate nutrient limitation. Reference conditions (background values) for each coastal area (A1, B1 and C1) were established using existing data from areas located as far away as possible from areas adjacent to river plumes of major rivers and submarine outfalls (Fig. 1). Therefore, three reference coastal sites with available data were selected on the basis of an apparent lowest physical degree of cultural impact (Fig. 1, Sites RA1, RB1 and RC1), to set the background and assessment (threshold) values, and used in this study to represent the least disturbed conditions possible. This was better achieved in the south coastal area (Fig. 1). Offshore reference sites (Fig. 1, Sites RA2, RB2 and RC2) were located on the same latitude as coastal reference sites. Comparison of the obtained nutrient reference values with those referred for the Eastern Mediterranean Sea, indicated as oligotrophic by many authors (see Karydis, 2009 and references therein), and for other open coastal areas (OSPAR, 2008), was performed for validation. Threshold values were calculated as deviation from areaspecific reference conditions for each indicator (Table 2). According to the MSFD, all measured indicators were compared against thresholds for each criterion to produce a (+) or (−) score, with (+) scores indicating values exceeding thresholds. For each area, an overall score was assigned for each category (I: Nutrient enrichment; II: Direct Effects; III: Indirect Effects); scores for all categories were combined to produce the final classification of the status of the area. The assessment areas were classified, according to the OSPAR (2005) common procedure, as suggested by the MSFD, as: (i) problem area (PA) where increased degree of nutrient enrichment occurs concomitantly with direct and/or indirect effects, or where direct and/or indirect effects are shown but there is no evident increased nutrient enrichment; (ii) potential problem area (PPA) where there is not enough data to perform an assessment; (iii) non-problem area (NPA) with no nutrient enrichment and related direct/indirect effects, or either there is evidence of the absence of direct/indirect eutrophication effects, although the increased degree of nutrient enrichment in these areas may contribute to eutrophication problems elsewhere. Problem areas are defined by two or more (+) scores, in any of the three categories, or one (+) score in categories II or III. Non-problem areas are characterized

Shift from long-lived to short-lived nuisance species (e.g. Ulva) Elevated opportunistic macroalgae levels Shift from long-lived to short-lived nuisance species (e.g. Ulva)

Decreased levels (<4 mg L−1 : acute toxicity; 4–6 mg/l: deficiency)

by (−) score for all categories, or a (+) score for category I and (−) scores for categories II and III (OSPAR, 2005). In order to provide a more integrated evaluation of eutrophication, the trophic index TRIX was calculated for each month in all stations in an assessment area, according to Vollenweider et al. (1998), and then averaged by season for each assessment area, and also by assessment area as a whole. TRIX was scaled from 0 to 10, covering a range of four trophic states (0–4 high quality and low trophic level, 4–5 good quality and moderate trophic level, 5–6 moderate quality and high trophic level, and 6–10 degraded quality and very high trophic level), according to Giovanardi and Vollenweider (2004) and Penna et al. (2004). The TRIX results were then compared with the OSPAR (2005) common procedure classification results for each assessment area. Mean values of TRIX, nutrient and Chl a concentrations were tested for normality and not found to be normally distributed. Therefore, differences in the parameters and trophic index between temporally appropriate periods (winter nutrients/productive period) and the remaining part of the year, as well as between assessment areas were compared through Kruskal Wallis non-parametric test. Results yielding p < 0.05 were considered statistically significant. To understand what could be driving the TRIX values, the relationship between index and parameters in each assessment area was tested using the Pearson correlation coefficients. All statistical analyses were performed with Statistica 6.1 Software (StatSoft, Inc.).

3. Results 3.1. Delimitation of the assessment areas The salinity regime criteria adopted (30.0–34.5: coastal waters, >34.5: offshore waters), separates the coastal plume influenced strip (A1, B1 and C1, Fig. 1) from the offshore area (A2, B2 and C2, Fig. 1) at an average depth of 81 m (Fig. 2). However, given the observed large intra- and inter-annual variability, denoted by the high standard deviation, the 100 m isobath was cautiously selected and used hereafter to separate coastal from offshore waters so that any eutrophication problems were not overlooked.

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0

Depth (m)

-50

-100

-150

Mean

Median 25%-75% Non-Outlier Range Outliers

-200 Salinity (< 34.5)

Fig. 2. Mean, median, percentile 25% and 75%, maximum and minimum of salinity (S) values (<34.5) in the water column up to the 200 m, for the Portuguese continental EEZ. Outliers are identified.

3.2. Assessing nutrient enrichment 3.2.1. Nutrient concentration in the water column Nutrient levels were significantly (p < 0.05) higher in coastal (A1, B1 and C1) than in offshore (A2, B2 and C3) areas (Fig. 3). The mean concentrations for coastal waters were 4.6, 0.32 and 2.9 ␮M for DIN, PO4 3− and Si(OH)4 + , respectively, twice the values determined in offshore waters (DIN: 2.4 ␮M, PO4 3− : 0.18 ␮M and Si(OH)4 + : 1.8 ␮M). In coastal waters, mean nutrient levels were not significantly (p > 0.05) different between areas A1 (DIN: 4.5 ␮M, PO4 3− : 0.37 ␮M and Si(OH)4 + : 3.2 ␮M), B1 (DIN: 4.8 ␮M, PO4 3− : 0.30 ␮M and Si(OH)4 + : 2.9 ␮M) and C1 (DIN: 4.2 ␮M, PO4 3− : 0.29 ␮M and Si(OH)4 + : 2.5 ␮M). Likewise, differences in nutrient levels between the areas located in offshore waters were non-significant (p > 0.05), A2 (DIN: 2.6 ␮M, PO4 3− : 0.16 ␮M and Si(OH)4 + : 1.9 ␮M), B2 (DIN: 2.3 ␮M, PO4 3− : 0.18 ␮M and Si(OH)4 + : 1.5 ␮M) and C2 (DIN: 2.0 ␮M, PO4 3− : 0.20 ␮M and Si(OH)4 + : 2.3 ␮M). Concentrations of PO4 3− were low in all areas, frequently reaching values below the detection limit. Significantly (p < 0.05) higher values were observed in the areas adjacent to river plumes (Minho to Douro, Tagus, Sado and Guadiana rivers) and to submarine outfalls than those found in the rest of the coastal waters, where DIN, PO4 3− and Si(OH)4 + averaged 8.3, 0.49 and 4.5 ␮M, respectively. Dissolved inorganic nitrogen (Fig. 4) displayed a seasonal pattern with positive deviation values highlighting the winter period, in coastal areas and offshore areas. Winter period values were significantly (p < 0.05) higher than those found during the rest of the year. The concentration values obtained from the winter period were 6.5, 6.1, 5.6, 4.5, 2.6 and 2.2 ␮M for A1, B1, C1, A2, B2 and C2, respectively. Regarding PO4 3− (Fig. 5), seasonal patterns, less visible than those found for DIN, were only found in areas A1, B2 and C1, with levels significantly (p < 0.05) higher during the winter period than throughout the rest of the year. The concentration values were obtained from the winter period mean for areas A1 (0.52 ␮M), B2 (0.21 ␮M) and C1 (0.41 ␮M), and from the annual mean for areas A2 (0.18 ␮M), B1 (0.32 ␮M) and C2 (0.22 ␮M). Concentration of Si(OH)4 + (Fig. 6) presented a seasonal pattern in all assessment areas, with positive deviation values generally occurring from December to April (winter period), and corresponding concentration values of 5.2, 2.7, 4.7, 2.2, 4.2 and 3.1 ␮M for A1, A2, B1, B2, C1, C2, respectively. Winter period levels were significantly (p < 0.05) higher than those found during the rest of the year.

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3.2.2. Nutrient ratios (N:P) Deviations of the monthly average values of the N:P ratio in the water column, from the Redfield ratio (16:1), annual N:P values, and the occurrence of PO4 3− limitation according to the Dortch and Whitledge (1992) criteria, for each of the assessment areas are shown in Fig. 7. During most of the year, small positive and negative deviations from the Redfield ratio were observed in all assessment areas. Large deviations were always positive (>20) and associated with the occurrence of PO4 3− limitation. In coastal waters, these large deviations were consistently observed in spring (March–May) and in summer (August). In offshore waters, large deviations were observed in spring (A2, B2, C2), in December (A2), and in October (C2). According to the Dortch and Whitledge (1992) criteria, DIN and Si(OH)4 + never attained limiting values. 3.3. Assessing direct effects of nutrient enrichment 3.3.1. Chlorophyll a concentration in the water column A correlation between in situ and satellite Chl a data was found significant (r = 0.58, p < 0.05) for the entire Portuguese continental EEZ, validating the employment of satellite data. Because in situ Chl a spatial and temporal coverage was poor in all assessment areas, and particularly, in offshore waters, only satellite data was used to evaluate Chl a concentration in the water column. Values of P90 for Chl a for coastal waters averaged 1.8 ␮g L−1 , significantly (p < 0.05) higher than the values found in offshore waters (0.36 ␮g L−1 ). The P90 values were comparable between coastal areas (A1: 1.9, B1: 1.8, C1: 1.6 ␮g L−1 ), as well as between offshore waters (A2: 0.47, B2: 0.33, C2: 0.30 ␮g L−1 ) (Fig. 8). Significantly (p < 0.05) higher values were observed in the areas adjacent to river plumes of major rivers (Minho to Douro, Tagus, Sado and Guadiana), where P90 for Chl a averaged 2.9 (A1), 2.5 (B1) and 2.7 (C1) ␮g L−1 , than in other coastal areas. Coastal and offshore areas displayed two different consistent seasonal patterns with the positive deviations to the grand median indicating the productive period (Fig. 9), that were confirmed by the significantly (p < 0.05) higher values obtained during the productive period in comparison with the rest of the year levels. In coastal waters, the productive period was observed from April to September. In offshore waters, the productive period seemed to start earlier in the year, from January till May. The average concentration values determined were 2.1, 0.82, 2.1, 0.52, 2.0 and 0.47 ␮g L−1 for A1, A2, B1, B2, C1, C2, respectively. 3.3.2. Water transparency related to the increase in suspended algae The mean values of Secchi disc depth (m), as a measure of transparency in the water column, in the Portuguese continental EEZ, were significantly (p < 0.05) lower in coastal (8.2 ± 3.6 m) than in offshore (14 ± 5.1 m) waters. A longitudinal water transparency gradient, from north to south, was detected in both coastal (A1: 7.7 ± 3.7; B1: 7.9 ± 2.5; C1: 10 ± 4.3 m) and offshore (A2: 12 ± 4.4, B2: 14 ± 5.3, C2: 16 ± 5.2 m) areas, with the northern areas (A1, B1, A2, B2) presenting significantly (p < 0.05) lower transparency than the southern ones (C1, C2). 3.3.3. Diatom:flagellate ratio and bloom events of nuisance and toxic algal blooms Changes in the diatom:flagellate ratio alternated between diatom dominance (ratio > 0.7) associated with water column turbulence and upwelling nutrient enrichment, specially on coastal areas, during the spring-summer period (A1: 0.67, B1: 0.69, C1: 0.75), and flagellate’s abundance (ratio < 0.5) when stratification occurs in the water column (Moita, 2001; Silva et al., 2009) and in offshore areas (A2: 0.41, B1: 0.43, C1: 0.49). A ratio around 0.5 points out a balance between the two phytoplankton communities.

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Fig. 3. Spatial variation of mean values of DIN (a), PO4 3− (b) and Si(OH)4 + (c) concentrations (␮M) in the water column, in the assessment areas (A1, A2, B1, B2, C1, C2) within the Portuguese continental EEZ. The 100 m isobath line is also indicated.

Monthly median deviation from grand median for DIN (µM)

Coastal waters

Offshore waters

6.0

6.0

3.0

3.0

0.0

0.0

-3.0

Grand median = 3.2 Winter period average = 6.5

A1

-3.0

6.0

6.0

3.0

3.0

0.0

0.0

-3.0

Grand median = 3.2 Winter period average = 6.1

B1

-3.0

6.0

6.0

3.0

3.0

0.0

0.0

-3.0

Grand median = 2.7 Winter period average = 5.6

C1

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

-3.0

Grand median = 1.7 Winter period average = 4.5

A2

Grand median = 1.7 Winter period average = 2.6

B2

Grand median = 1.6 Winter period average = 2.2

C2

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Fig. 4. Temporal pattern shown by the monthly median deviations from the grand median, assessment periods, and values of DIN winter period concentration (␮M) in the water column, for each assessment area (A1, A2, B1, B2, C1, C2). Standard error bars are presented.

M.T. Cabrita et al. / Ecological Indicators 58 (2015) 286–299

Coastal waters

293

Offshore waters

0.6 0.3 0.2

0.3

Monthly median deviation from grand median for PO43- (µM)

0.1 0.0

0.0

-0.1 -0.3

Grand median = 0.24 Winter period average = 0.52

A1

0.6

-0.2

Grand median = 0.13 Annual average = 0.18

A2

0.3 0.2

0.3 0.1 0.0

0.0

-0.1 -0.3

Grand median = 0.24 Annual average = 0.32

B1

0.6

-0.2

Grand median = 0.10 Winter period average = 0.21

B2

0.3 0.2

0.3 0.1 0.0

0.0

-0.1 -0.3

Grand median = 0.20 Winter period average = 0.41

C1

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

-0.2

Grand median = 0.16 Annual average = 0.22

C2

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Fig. 5. Temporal pattern shown by the monthly median deviations from the grand median, assessment periods and values of PO4 3− winter or annual average concentration (␮M) in the water column, for each assessment area (A1, A2, B1, B2, C1, C2). Standard error bars are presented.

Events of nuisance/toxic algal blooms have been recurrently occurring along the Portuguese coastal area (Pitcher et al., 2010; Mateus et al., 2013), generally associated with the upwelling-downwelling cycle, promoting bloom transport and cell concentration (Sordo et al., 2000; Moita, 2001; Moita and da Silva, 2002; Moita et al., 2006). No relation to anthropogenic nutrient inputs could be found. No reports of HAB occurrence were found for offshore waters associated with eutrophication.

3.3.4. Abundance of opportunistic macroalgae Most of the information on opportunistic macroalgae refers to transitional waters, which was necessary to the implementation of the WFD in Portugal. Available data for subtidal macroalgae is scarce for the Portuguese coast probably due to the difficulties associated with working in such environments. In coastal waters, filamentous greens, Ulvales, filamentous browns, Ectocarpales, Anhfeltiopsis devoniensis, Asparagopsis armata, Falkenbergia rufolanosa are the opportunistic macroalgae species, accounting for less than 10% of proportion of opportunists, and of opportunist coverage (Pardo et al., 2011). Subtidal opportunistic species have been considered less representative of the open coastal waters, and therefore less likely to occur in deeper waters due to low light availability.

3.3.5. Abundance of perennial seaweeds and seagrasses Regarding the perennial seaweeds, 246 species of rhodophytes, 98 phaeophytes and 60 chlorophytes have been reported for the Portuguese coastal area, with no considerable changes over time (Ardré, 1970; Sousa-Pinto and Araújo, 1998, 2006). A sharp distribution gradient along the Portuguese coast was observed (Sousa-Pinto and Araújo, 1998, 2006) with diversity of cold temperate species (e.g. Laminaria hyperborea and L. saccharina) reducing towards the south (Ardré, 1971; Melo and Santos, 1982) where other warm temperate species become more abundant (e.g. Saccorhiza polyschides, L. ochroleuca, Polysiphonia caespitosa, Streblocladia collabens, Leptosiphonia schousboei and Herposiphonia secunda) (Sousa-Pinto and Araújo, 1998, 2006). From the north to the south of the Portuguese coast, an increase in the number of red algal species and a decrease of brown algal has been consistently observed (Palminha, 1951; Mesquita Rodrigues, 1963; Ardré, 1970, 1971). Other subtidal species, such as Gelidium sesquipedale and Gracillaria spp., could be found throughout the Portuguese continental subtidal waters (Marques, 2012; Pereira, 2008) but no reports of abundance decline associated with eutrophication were found. Bloom events of green macroalgae have been mainly observed in nutrient-rich estuarine areas (Cardoso et al., 2004), but, to our best knowledge, not for subtidal waters. Contrastingly, seagrass populations of the Portuguese coast are facing an

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Monthly median deviation from grand median for Si(OH)4+ (µM)

Coastal waters

Offshore waters

4.0

4.0

2.0

2.0

0.0

0.0

-2.0

Grand median = 2.5 Winter period average = 5.2

A1

-2.0

4.0

4.0

2.0

2.0

0.0

0.0

-2.0

Grand median = 1.9 Winter period average = 4.7

B1

-2.0

4.0

4.0

2.0

2.0

0.0

0.0

-2.0

Grand median = 1.9 Winter period average = 4.2

C1

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

-2.0

Grand median = 1.5 Winter period average = 2.7

A2

Grand median = 1.2 Winter period average = 2.2

B2

Grand median = 1.8 Winter period average = 3.1

C2

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Fig. 6. Temporal pattern shown by the monthly median deviations from the grand median, assessment periods and values of Si(OH)4 + winter period concentration (␮M) in the water column, for each assessment area (A1, A2, B1, B2, C1, C2). Standard error bars are presented.

unprecedented decline in distribution, from 1995 till 2008 (Cunha et al., 2013). This decrease followed different trends for the three species present on this coast. Zostera noltii, the mostly intertidal species, disappeared from some systems by almost 75%, is still the most abundant species. For instance, in the Mondego estuary, the drastic decline in this species was found a symptom of eutrophication (Krause-Jensen et al., 2004). Similarly, in the south coast, some areas located in the vicinity of estuarine systems have shown a reduction of Z. noltii cover associated with eutrophication (nutrients washed off from agriculture fields and golf courses) (Cunha et al., 2013). Zostera marina is presently the most endangered seagrass species, facing extinction. Cymodocea nodosa has a geographic distribution range limited to the S/SW coasts (Green and Short, 2003), and its current conservation status is uncertain, although there is evidence for the recent occurrence of several population bottlenecks. For the EEZ coastal waters, no events of concomitant water transparency decline and decrease in perennial seaweeds and seagrasses were found. According to Cunha et al. (2013), no records were reported for offshore areas. 3.4. Evaluating indirect effects of nutrient enrichment 3.4.1. Dissolved oxygen The 10th percentile values of DO (mg L−1 ) available for the coastal areas A1, B1 and C1 were 6.2, 7.4 and 7.2 mg L−1 respectively, indicating that coastal waters were well oxygenated. Even in

the areas adjacent to river plumes of major rivers (Douro, Mondego, Tejo and Guadiana) and to submarine outfalls, waters remained oxygenated, with 10th percentile values averaging 6.9 mg L−1 . No data on DO was available for offshore waters.

3.5. Trophic index TRIX The TRIX values were significantly (p < 0.05) higher at A1, B1 and C1 (5.9 ± 0.65, 5.8 ± 0.37, 5.5 ± 0.44, respectively) than in A2, B2 and C2 (4.4 ± 0.63, 4.4 ± 0.32, 4.2 ± 0.43, respectively), indicating moderate quality and high trophic level in coastal waters, and good quality and moderate trophic level in offshore waters. In specific areas under the influence of the most important river plumes, TRIX averaged 6.3 ± 0.33, pointing to a degraded and very high trophic level state. Winter period TRIX values were significantly (p < 0.05) higher than those found during the rest of the year. Values of TRIX showed significant (p < 0.05) positive relationships with DIN concentrations for all areas, except C2; the Pearson correlation coefficients (r) obtained were generally higher for coastal (A1: 0.81, B1: 0.85, C1: 0.73) than for offshore (A2: 0.91, B2: 0.80, C2: 0.51) areas. Similarly, significant (p < 0.05) relationships were obtained between TRIX values and PO4 3− (A1: 0.78, A2: 0.87, B1: 0.82, B2: 0.62, C1: 0.84, C2: 0.73). Nonsignificant relationship was found between the TRIX index and Chl a concentration.

M.T. Cabrita et al. / Ecological Indicators 58 (2015) 286–299

Monthly median deviation from Redfield ratio (16:1) for N:P

Coastal waters

Offshore waters

100

100

60

60

20

20

-20

Annual average = 35

A1

-20

100

100

60

60

20

20

-20

Annual average = 26

B1

-20

100

100

60

60

20

20

-20

Annual average = 32

295

C1

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

-20

Annual average = 41

A2

Annual average = 50

B2

Annual average = 45

C2

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Fig. 7. Temporal pattern shown by the monthly median deviations from the Redfield ratio (16:1), annual average values of N:P, and occurrence of PO4 3− limitation according to the Dortch and Whitledge (1992) criteria (white bars), for each assessment area (A1, A2, B1, B2, C1, C2).

4. Discussion 4.1. Validating eutrophication indicators

Fig. 8. Spatial variation of 90th percentile values (P90) of Chl a concentration (␮M) in the water column, in the assessment areas (A1, A2, B1, B2, C1, C2) within the Portuguese continental EEZ. The 100 m isobath line is also indicated.

The indicators considered in the scope of the Marine Strategy Framework Directive were found appropriate to assess eutrophication in the continental Portuguese waters, with the exception of the diatom:flagellate ratio. In the Portuguese coastal areas, changes in this indicator showed the natural shift between diatoms and flagellates that has been found related to alternating water column turbulence and upwelling nutrient enrichment conditions, and water column stratification, respectively (Moita, 2001). Shifts in the diatom:flagellate ratio could not be directly associated with effects of nutrient enrichment triggered by anthropogenic sources and therefore this ratio is a poor indicator of eutrophication for Portuguese coastal areas. In the case of the N:P ratios, particular caution was undertaken with the interpretation of the values obtained, as the Portuguese waters presented naturally low PO4 3− levels, and consequently the N:P ratios were frequently higher than the Redfield ratio, used as a reference (C:N:P, 106:16:1) to estimate imbalance in dissolved inorganic N and P concentrations (N:P, 16:1). The N:P ratios suggested that PO4 3− was more likely to be a limiting nutrient which was further confirmed by the application of the Dortch and Whitledge criteria (1992) that showed PO4 3− limitation in several occasions. These results imply that P, other than N, is driving the N:P interaction and, consequently, the high N:P ratios obtained could not be associated with eutrophication. Naturally increased N:P ratios resulting from PO4 3− limitation have also been observed

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Monthly median deviation from grand median for Chl a (µg L-1)

Coastal waters

Offshore waters

0.8

0.8

0.4

0.4

0.0

0.0

-0.4

-0.4

-0.8

Grand median = 1.9 Productive period average = 2.1

A1

-0.8

0.8

0.8

0.4

0.4

0.0

0.0

-0.4

-0.4

-0.8

Grand median = 1.8 Productive period average = 2.1

B1

-0.8

0.8

0.8

0.4

0.4

0.0

0.0

-0.4

-0.4

-0.8

Grand median = 1.5 Productive period average = 2.0

C1

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

-0.8

Grand median = 0.33 Productive period average = 0.82

A2

Grand median = 0.28 Productive period average = 0.52

B2

Grand median = 0.23 Productive period average = 0.47

C2

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Fig. 9. Temporal pattern shown by the monthly median deviations from the grand median, assessment periods and values of Chl a productive period concentration (␮M) in the water column, for each assessment area (A1, A2, B1, B2, C1, C2). Standard error bars are presented.

in many coastal areas (e.g. Harrison et al., 1990; Diaz et al., 2001), with no relation to eutrophication. 4.2. Setting reference and assessment values The eutrophication assessment in the scope of the MSFD deeply relies on quality rating based on reference conditions. Natural background concentrations that serve as reference levels are supposed to be obtained from undisturbed, pristine areas with no or very minor human interference (Karydis, 2009). This was a challenging task because undisturbed coastal areas are increasingly less worldwide (Hinrichsen, 1998) and the Portuguese continental coast is no exception. Furthermore, the inexistence of available historical reference data from periods prior to intense human activity for the Portuguese coastal waters created an undesirable setback. The option of using areas located as far away as possible from areas adjacent to river plumes of major rivers and submarine outfalls helped to optimize finding the most possibly consistent reference levels assigned to each eutrophication related indicator. The obtained reference values (Table 3) were different from those indicated in the first MSFD report (MAMAOT, 2012), due to the extended dataset and methodologies applied. Regarding the nutrients, it was encouraging to find that the coastal reference values were generally comparable to the offshore values, particularly for the south-west and south coasts. The reference values herein obtained for these two areas were comparable to values indicated for oligotrophic waters (Karydis, 2009), and thus could be used as background levels, which supported the reference site choice. For the northwest area, reference values for nutrients were higher in coastal than in

Table 3 Reference (background) and assessment (threshold) values used for the assessment of eutrophication in the assessment areas (A1, A2, B1, B2, C1, C2), located within the Portuguese continental EEZ. Reference values

Assessment areas

Indicator

A1

A2

B1

B2

C1

C2

DIN (␮M) DIP (␮M) Si(OH)4 + (␮M) Chl a (␮g L−1 )

4.3 0.31 3.7 1.6

1.9 0.19 2.6 0.61

2.5 0.18 2.2 1.8

2.3 0.22 2.2 0.50

2.3 0.23 2.0 1.7

1.8 0.21 3.2 0.33

Assessment values

Assessment areas

Indicator

A1

A2

B1

B2

C1

C2

DIN (␮M) DIP (␮M) Si(OH)4 + (␮M) Chl a (␮g L−1 )

6.4 0.46 5.6 2.4

2.9 0.28 3.8 0.92

3.7 0.27 3.3 2.7

3.5 0.33 3.2 0.75

3.5 0.35 3.0 2.5

2.8 0.32 4.7 0.50

offshore waters, probably reflecting the higher number of transitional systems in the area in comparison with the other coastal reference stations. Nevertheless, values were generally lower than nutrient reference values indicated for other open coastal areas (OSPAR, 2008). Differences in reference values between assessment areas highlighted the importance of establishing relatively close spaced reference sites when preparing coastal marine criteria. The wide range of reference values obtained for coastal waters throughout Europe (HELCOM, 2006; Anon, 2008; OSPAR, 2008) further supports the requirement of high spatial resolution for the establishment of reference guidance for a particular area.

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297

Table 4 Eutrophication assessment showing the obtained individual scores for each parameter, overall scores for each criteria category, and final classification for the areas (A1, A2, B1, B2, C1, C2), located within the Portuguese continental EEZ. Areas were classified as problem area (PA), potential problem area (PPA) or non-problem area (NPA). Criteria

Category I: Nutrient enrichment

Category II: Direct effects of nutrient enrichment Category III: Indirect effects of nutrient enrichment

Indicator

DIN PO4 3Si(OH)4 N:P ratio Overall score Chl a Water transparency Nuisance/toxic algal bloom events Opportunistic macroalgae abundance Perennial seaweed and seagrass abundance Overall score DO Overall score Final classification

Assessment area A1

A2

B1

+ + − + + − − − − + − − −

+ − − + + − − − − − − − −

+ + + + + − − − − − − − −

4.3. Assessing eutrophication The eutrophication assessment for each of the assessment areas of the Portuguese continental EEZ was undertaken based on the reference and assessment values previously calculated, and is presented in Table 4. Assessment areas were, as a whole, classified as non-problem areas with respect to eutrophication, confirming results of the first MSFD report (MAMAOT, 2012). Nutrient enrichment was observed in all coastal waters (Table 4), possibly related to the influence of the most important river plumes, which was highlighted by the TRIX values indicating moderate quality and high trophic level for coastal waters, and good quality and moderate trophic level for offshore waters. In these specific zones located within each coastal assessment area, highest DIN (8.3 ␮M) and PO4 3− (0.49 ␮M) average levels were observed, particularly within the southern coastal waters (DIN: 13 ␮M, PO4 3− : 0.55 ␮M), with the TRIX index indicating degraded quality and very high trophic level. However, these nutrient values were among the lowest in coastal Europe areas and below those reported for most marine waters in Europe experiencing increased nutrient levels and related problems (Ærtebjerg et al., 2001). Overall, direct and indirect effects of nutrient enrichment were not detectable throughout the Portuguese coast which indicated that the hydrodynamic regime promoted dilution triggered by dispersion and mixing processes in those areas, without exhibiting eutrophication. These results are in line with previous observations in the coastal waters off southern California, showing that inputs associated with several eutrophic estuaries in the area (McLaughlin et al., 2014) had no repercussions on the water quality of the off coastal waters due to similar coastal hydrodynamic features (Boesch, 2002). Only occasionally, elevated phytoplankton biomass was found in specific areas under the influence of the Douro and Vouga (two of the major rivers in the northwest coast, 2.9 ␮g L−1 ) and Guadiana (the major river in the south coast, 2.7 ␮g L−1 ) river plumes, which appeared to be a direct effect of anthropogenic nutrient enrichment found in these areas. Although these Chl a values were indicative of bad ecological quality status, according to the eutrophication scale based on Chl a concentration, proposed by Simboura et al. (2005) and used here to express an attribute to the Chl a indicator, levels were below those observed in other highly eutrophicated coastal areas of the world (>6.0 ␮g L−1 ), as, for example, the Wadden sea (Ærtebjerg et al., 2001), or the Gulf of Mexico (Boesch, 2002). Seagrass decline associated with eutrophication, found in areas located in the vicinity of estuarine systems, was also indicative of deteriorated ecological quality status in the northwest and south coastal waters. No evidence for other undesirable disturbances, such as oxygen depletion, was found or pointed out in

B2 − − − + − − − − − − − − − NPA

C1

C2

+ + + + + − − − − + − − −

− − − + − − − − − − − − −

the literature for the assessment areas. The scenario of elevated nutrient levels and algae biomass, and reduction of seagrass cover, but no undesirable perturbations can be considered as mild eutrophication, which was supported by the TRIX results, and therefore the Portuguese coastal waters under the influence of major river plumes (northwest and south coastal waters) should be assessed as problem areas according to the OSPAR classification. Similarly, some British coastal areas (e.g. East England) with the same symptoms were considered as areas of ongoing concern, subject to monitoring (Anon, 2012). The multimetric trophic index TRIX provided an integrated evaluation of indicators of eutrophication (Giovanardi and Vollenweider, 2004), and simultaneously offered information that is readily understandable and meaningful to diverse stakeholders which is particularly relevant for the eutrophication assessment within the scope of the MSFD. Values of TRIX clearly highlighted eutrophication spatial and temporal patterns, and confirmed that Chl a was not a key factor, as TRIX index in all assessment areas was driven by DIN and PO4 3− . These results were generally in agreement with the MSFD overall evaluation performed, and further provided a more accurate differentiation between coastal and offshore areas, stressing the influence of the most important river plumes. This suggests that this index has potential as a suitable communicative and easy-to-use tool for the assessment of eutrophication in the Portuguese continental EEZ marine waters. A specific disadvantage may be that TRIX is derived from the combination of four parameters that are not entirely independent and, consequently, might be overemphasizing particular features (Salas et al., 2008). This implies that TRIX useful information for decision-making should to be linked with other water quality related indicators to allow for an efficient management of marine waters, as found by other authors (Giovanardi and Vollenweider, 2004; Vascetta et al., 2008). While appropriate management have not yet been implemented in all areas of the Portuguese coast (Ferreira et al., 2003), directed monitoring on eutrophication is advised for the areas under the influence of major river plumes. Monitoring planning should consider an in situ network with high temporal resolution, focused on river plume areas where anthropogenic pressure was found the highest, in order to timely and accurately detect acute effects from rapidly developing events, such as sudden and sharp peaks of oxygen depletion in bottom waters or nuisance harmful algal blooms. Simultaneous measurements of all the indicators involved should be carried out to provide more complete datasets in need, particularly for the south area, to effectively assess and fully understand eutrophication in Portuguese coastal waters. Satellite remote sensing and numerical and hydrodynamic modelling should be used to help estimate the extent of river plume influence. With our

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current understanding of eutrophication, it is difficult to forecast the direct and indirect responses of ecosystems to multiple stressors or pressures with confidence. Furthermore, effects of human inputs and those that may be triggered by climate change will become increasingly difficult to distinguish. Accurate monitoring and assessment work are therefore still needed for the appropriate management and protection of the Portuguese coastal waters in the future. 5. Conclusions Assessment areas of the Portuguese continental EEZ were, as a whole, classified as non-problem areas with respect to eutrophication, although nutrient enrichment was observed in all coastal waters, related to the influence of the major river plumes. In particular, these specific riverine influenced zones, showing high nutrient levels, elevated phytoplankton biomass, seagrass decline, although no other undesirable alterations, were associated with degraded quality and very high trophic level, and considered mildly eutrophicated. Directed monitoring on eutrophication is advised for these zones that should be considered as areas of ongoing concern. The trophic index TRIX, linked with other water quality related indicators, provided an accurate integrated evaluation of indicators of eutrophication, and was shown as suitable tool for the assessment of eutrophication in the Portuguese continental EEZ. Acknowledgements Maria Teresa Cabrita and Alexandra Silva acknowledge the grants by “Fundac¸ão para a Ciência e a Tecnologia” (FCT, Grant No. SFRH/BPD/50348/2009 and Grant No. SFRH/BPD/63106/2009, respectively). The authors would like to thank the anonymous reviewers for their valuable suggestions. References Ærtebjerg, G., Carstensen, J., Dahl, K., Hansen, J., Nygaard, K., Rygg, B., Sørensen, K., Severinsen, G., Casartelli, S., Schrimpf, W., Schiller, C., Druon, J.N., 2001. Eutrophication in Europe’s coastal waters. Topic report 7. European Environment Agency, Copenhagen, 115 pp. Aizaki, M., Iwakuma, T., Takamura, N., 1981. Application of modified Carlson’s trophic state index to Japanese lakes and its relationship to other parameters related to trophic state. Res. Rep. Natl. Inst. Environ. Stud. 23, 13–31. Álvarez-Salgado, X., Arstegui, J., Barton, E., Hansell, D., 2007. Contribution of upwelling filaments to offshore carbon export in the subtropical Northeast Atlantic Ocean. Limnol. Oceanogr. 52, 1287–1292. Anon, 2008. Common Procedure for the Identification of the Eutrophication Status of the OSPAR Maritime Area – UK National Report, 67 pp. Anon, 2012. Marine Strategy Framework Directive Consultation. UK Initial Assessment and Proposals for Good Environmental Status. HMGovernment document. Crown Publishers, UK, 148 pp. Ardré, F., 1970. Contribuition à l’étude des algues marines du Portugal I. La Flore. Port. Acta Biol. 10 (1–4), 1–423. Ardré, F., 1971. Contribuition à l’étude des algues marines du Portugal II. Ecologie et Chorologie. Bull. Cent. Etud. Rech. Sci., Biarritz 8 (3), 359–574. Bachmann, R.W., Cloern, J.E., Hecky, R.E., David, W., Schindler, D.W., 2006. Eutrophication of freshwater and marine ecosystems. Limnol. Oceanogr. 51 (1 (Part 2)), 351–800. Bettencourt, A., Bricker, S.B., Ferreira, J.G., Franco, A., marques, J.C., Melo, J.J., Nobre, A., Ramos, L., Reis, C.S., Salas, F., Silva, M.C., Simas, T., Wolff, W., 2004. Typology and Reference Conditions for Portuguese Transitional and Coastal Waters. INAG, IMAR, 99 pp. Boesch, D.F., 2002. Causes and consequences of nutrient enrichment of coastal waters. In: Ragaini, R. (Ed.), International Seminar on Nuclear war and Planetary Emergencies, 26th Session. World Scientific Publishing, Singapore, pp. 165–180. Bricker, S., Longstaff, B., Dennison, W., Jones, A., Boicourt, K., Wicks, C., Woerner, J., 2007. Effects of Nutrient Enrichment in the Nation’s Estuaries: A Decade of Change. NOAA Coastal Ocean Program Decision Analysis Series No. 26. National Centers for Coastal Ocean Science, Silver Spring, MD, 328 pp. Cardoso, P.G., Pardal, M.A., Lillebo, A.I., Ferreira, S.M., Raffaelli, D., Marques, J.C., 2004. Dynamic changes in seagrass assemblages under eutrophication and implications for recovery. J. Exp. Mar. Biol. Ecol. 302, 233–248. Carlson, R.E., 1977. A trophic state index for lakes. Limnol. Oceanogr. 22 (2), 361–369. Carpenter, et al., 1998. Non-point pollution of surface waters with phosphorus and nitrogen. Ecol. Appl. 8, 559–568.

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