Effects of organic pollution and physical stress on benthic macroinvertebrate communities from two intermittently closed and open coastal lagoons (ICOLLs)

Accepted Manuscript Effects of organic pollution and physical stress on benthic macroinvertebrate communities from two intermittently closed and open coastal lagoons (ICOLLs) Susana Coelho, Angel Pérez-Ruzafa, Sofia Gamito PII:

S0272-7714(15)30070-6

DOI:

10.1016/j.ecss.2015.08.013

Reference:

YECSS 4880

To appear in:

Estuarine, Coastal and Shelf Science

Received Date: 6 October 2014 Revised Date:

8 August 2015

Accepted Date: 16 August 2015

Please cite this article as: Coelho, S., Pérez-Ruzafa, A., Gamito, S., Effects of organic pollution and physical stress on benthic macroinvertebrate communities from two intermittently closed and open coastal lagoons (ICOLLs), Estuarine, Coastal and Shelf Science (2015), doi: 10.1016/ j.ecss.2015.08.013. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Effects of organic pollution and physical stress on benthic macroinvertebrate communities from two intermittently closed and open coastal lagoons (ICOLLs) Susana Coelho¹, Angel Pérez-Ruzafa2 and Sofia Gamito¹* 1

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MARE – Marine and Environmental Sciences Center, Faculdade de Ciências e Tecnologia, Universidade do Algarve, Campus de Gambelas, 8005-139 Faro, Portugal Departamento de Ecologia e Hidrologia, Facultad de Biología. Regional Campus of International Excellence Mare Nostrum, University of Murcia, 30100 Murcia, Spain

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* Corresponding author. E-mail address: [email protected]

ABSTRACT

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Benthic macroinvertebrate communities and environmental conditions were studied in two intermittently closed and open coastal lakes and lagoons (ICOLLs), located in southern Algarve (Foz do Almargem e Salgados), with the purpose of evaluating the effects of organic pollution, originated mainly from waste water discharges, and the physical stress caused by the irregular opening of the lagoons. Most of the year, lagoons were isolated from the sea, receiving the freshwater inputs from small rivers and in Salgados, also from the effluents of a wastewater plant.

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According to environmental and biotic conditions, Foz do Almargem presented a greater marine influence and a lower trophic state (mesotrophic) than Salgados (hypereutrophic). Benthic macroinvertebrate communities in the lagoons were distinct, just as their relations with environmental parameters. Mollusca were the most abundant macroinvertebrates in Foz do

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Almargem, while Insecta, Oligochaeta and Crustacea were more relevant in Salgados. Corophium multisetosum occurred exclusively in Salgados stations and, just as Chironomus sp., other Insecta and Oligochaeta, densities were positively related to total phosphorus, clay content and chlorophyll

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a concentration in the sediment, chlorophyll a concentration in water and with total dissolved inorganic nitrogen. Abra segmentum, Cerastoderma glaucum, Peringia ulvae and Ecrobia ventrosa occurred only in Foz do Almargem, with lower values of the above mentioned parameters. Both lagoons were dominateFoz dod by deposit feeders and taxa tolerant to environmental stress, although in Salgados there was a greater occurrence of opportunistic taxa associated to pronounced unbalanced situations, due to excess organic matter enrichment.

Keywords: Physical stress; organic pollution; macrobenthic communities, coastal lagoons, Lagoa dos Salgados, Lagoa Foz do Almargem

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ACCEPTED MANUSCRIPT 1. Introduction Benthic macroinvertebrates represent a relevant component of coastal ecosystems, playing a vital role in nutrient cycling, detrital decomposition and as a food source for higher trophic levels (Pearson and Rosenberg, 1978). Due to the relatively sedentary habits and, thus, the incapability to avoid unfavorable conditions, macrobenthic species are sensitive indicators of changes in the environment caused by natural or anthropogenic disturbances (Salas et al., 2006). Since benthic

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species are relatively long-lived they integrate water and sediment quality conditions with time and thereby, indicate temporary and chronic disturbances (Warwick et al., 1990). Effects of these disturbances include changes in diversity, biomass, abundance of stress tolerant or sensitive benthic species, and changes in the trophic or functional structure of the benthic community

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(Pearson and Rosenberg, 1978; Reiss and Kröncke, 2005; Gamito, 2006, 2008).

Coastal lagoons are shallow aquatic ecosystems that evolve at the transition between terrestrial

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and marine ecosystems, being classified either as coastal water bodies or as transitional systems under the Water Framework terminology (McLusky and Elliott, 2007). Their location subjects them to strong anthropogenic pressures due to tourism and shellfish or fish farming, and also to diffuse pollution through agricultural and industrial effluents and domestic sewage drainage from their catchment areas (Alliaume et al., 2007). Coastal lagoons exhibit a wide range of salinity values, depending on the hydrological balance and on local climatic conditions (Kjerfve, 1994), and may vary from nearly freshwater to hyperhaline systems. Apart from climate, the hydrological

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features are shaped to a certain extent by the morphology of the lagoon and by the dimension of the inlets or canals through which exchange of water with the sea occurs (Kjerfve, 1994). The hydrological characteristics are also influenced by the balance of precipitation, freshwater input,

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evaporation, tidal range and tidal flushing of the lagoon (Bird, 1994). Kjerfve (1986; 1994) divided coastal lagoons into three types: choked, restricted and leaky. Those lagoon types show an increasing degree of water exchange with the ocean, together with an

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increasing tidal influence. Recently, another lagoon type has been defined, the intermittently closed and open coastal lakes and lagoons (ICOLLs) (see Tagliapietra et al., 2009 and references therein). The ICOLLs refers to small coastal lagoons with entrances that are closed must of the time, as well as occasionally closed barrier estuaries with untrained entrances (Roy et al., 2001, Tagliapietra et al., 2009). ICOLLs are periodically closed by longshore drift along the coast and by wave driven sediment accumulation, and then reopened by high river discharges (McSweeney et al., 2014). The two lagoons studied, Foz do Almargem and Salgados, fall into these category type. Coastal lagoons need to be investigated by a multifactorial approach, considering different ecological aspects like water renewal rates, trophic status and also the main environmental

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ACCEPTED MANUSCRIPT conditions that affect and determine the fixation and development of the lagoonal organisms, such as salinity and dissolved oxygen variation and sediment type (Gamito et al., 2005 and references therein). For ICOLLs, the numbers of days with sea-connection, together with the period of the year the connections occur, allowing for the migration of marine species, are also important factors for species colonization (Pérez-Ruzafa and Marcos, 1992; Gamito et al., 2005). In a recent revision of benthic conceptual models, a unifying conceptual benthic succession

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lagoonal model has been proposed – the saprobity system, that is, a gradient of organic matter enrichment shaping the benthic communities (Tagliapietra et al., 2012).

Foz do Almargem and Salgados are located in southern Portugal. Most of the year, the lagoons were isolated from the sea, receiving the freshwater inputs from small rivers and, in Salgados,

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also from the effluents of a wastewater plant. Occasionally, the sand barriers were artificially or naturally opened and these lagoons were in connection with the sea either for short or long periods, the duration of these openings depending on various factors, namely weather conditions

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and the water level in the lagoons. Foz do Almargem presented a greater marine influence and a lower trophic state (mesotrophic) than Salgados (hypereutrophic) (Coelho, 2013; Coelho et al., 2007). These trophic classifications were based on several indices and indicators applied to chlorophyll a and nutrient concentration data, collected in the same lagoons and sampling occasions. Some few studies have already been done in Salgados lagoon, mainly focused on the landscape, fauna and flora characterization and management (e.g. Fernandes, 2001; Ministro,

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2002) and water quality (e.g. Neves, 1999). Regarding Foz do Almargem, to the best of our knowledge, no previous studies were available.

The present study intends to compare environmental conditions and benthic macroinvertebrate communities of two ICCOL type coastal lagoons, with the purpose of evaluating the effects of

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organic pollution from wastewater discharges and the physical stress caused by the irregular

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opening of the lagoons.

2. Material and methods

2.1. Description of study sites The two lagoons are located in the southern coast of Portugal, in Algarve (Fig. 1). Foz do Almargem drainage basin comprises two small rivers, Almargem and Fonte Santa, with a seasonal dynamics strongly influenced by meteorological conditions. The lagoon is a small brackish wetland, which occupies around 20 ha, most of it shallow and only with a deeper main channel. When all the lagoon area is flooded, the mean depth is approximately 1m and the maximum depth is about 2.5 m. During most of the year, the lagoon is isolated from the sea by a thin sand barrier, but from autumn until spring this barrier is sometimes destroyed, either naturally

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ACCEPTED MANUSCRIPT by waves, or artificially by fishermen, forming then a channel between the lagoon and the sea. The frequency and duration of natural channel opening depends mainly on the wave height and tide amplitude. When the lagoon is opened, there is some tidal influence but only in the main channel, as the remaining area is not flooded and the sediment becomes exposed. The tidal amplitude, in the sea side, is about 3 to 3.5 m during spring tides. However, since most of the bottom of the lagoon is above the mean sea level, only the main channel remains with water and

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under tidal influence when the lagoon is opened. No sources of organic pollution were known, besides the runoff from agriculture lands.

Salgados coastal lagoon occupies a total surface of about 40 ha, most of it shallow and only with a deeper area downstream. The mean depth is approximately 1 m and the maximum depth is

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about 5 m. The drainage basin comprises Espiche and Vale Rabelo rivers. A thin sand barrier separates the lagoon from the sea and in natural conditions, when the water level in the lagoon reaches 5.7 m above the hydrographic zero (which in Portugal corresponds to 2m below the

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mean sea level), a channel is formed connecting the lagoon to the sea. Nowadays, a channel is artificially opened every time the water level in the lagoon rises from 4.5 to 5.0 m above the hydrographic zero, with the purpose of renewing the lagoon water and preventing the flooding of a golf course located nearby. Usually, the period of connection between the lagoon and the sea does not exceed a week, depending on the freshwater inputs, the wave height and tide amplitude.

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Besides the freshwater inputs from the small rivers, Salgados lagoon also used to receive the discharges of two wastewater treatment plants, which accounted approximately for 27% of the total freshwater input in summer (Neves, 1999) and maintained the water level high in this season. These wastewater treatment plants worked inefficiently most of the time, and effluents

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were discharged with high concentrations of organic matter, phosphorous and nitrogen, presenting values higher than those allowed by national legislation. Wastewater was therefore the

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main direct source of organic pollution in the lagoon (Neves, 1999). Nevertheless, in the drainage basin there were also some sources of diffuse organic pollution namely, the runoff from agriculture lands and from a golf course implanted in one of the lagoon margins.

2.2. Sampling and laboratory procedures Field work was done from June 2001 to July 2002, with an interval of approximately 45 days. In this way, 8 field campaigns were carried out, corresponding to two campaigns in each season or 4 campaigns during the dry period and another 4 during the wet period. In Foz do Almargem and Salgados lagoons, sampling took place in three stations along a gradient of distance from the sea inlet (1- upstream; 2 – intermediate and 3 – downstream), although in Salgados lagoon there

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ACCEPTED MANUSCRIPT were just two sampling stations for sediment analysis (1- upstream and 3 – downstream). The intermediate station was difficult to access due to the channel depth and the existing high density of emergent vegetation, which prevented an efficient sediment sampling. Sampling always took place during the morning, between 9 and 12 am. In total, 24 water and sediment samples were taken in Almargem (3 stations x 8 sampling occasions). However, in Salgados, though 24 water samples were also taken, only 16 sediment samples for macroinvertebrate and sediment

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characteristics analysis were taken.

Water parameters, such as salinity, temperature, dissolved oxygen and pH, were measured in locu with a multi-parameter probe, at a mean depth of 0.5 m. At the same depth, water samples were collected for the determination in laboratory of suspended matter, chlorophyll a and

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nutrients, following Greenberg et al., 1992. Pigment concentration was measured by spectrophotometry (Parsons et al., 1984; Greenberg et al., 1992) and calculations were done

and 665 nm (Margalef, 1960).

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according to Lorenzen (1967). Pigment diversity was determined based in the absorbance at 430

Sediment samples were taken for analysis of grain-size distribution, water and organic matter content, and phytopigments concentration. Grain-size distribution was determined following Holme and McIntyre (1984) and samples classified based on clay, silt and sand ratios, according to Flemming (2000). For the determination of water and organic matter, and phytopigments concentration, three replicates were collected from the superficial sediment layer (1.5 cm depth),

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using a core with 2 cm internal diameter. Phytopigments (chlorophyll a and phaeo-pigments) were extracted from the sediment with acetone 90% for 24 hours. Concentrations were determined by spectrophotometry according to the equations of Lorenzen (1967) modified by Plante-Cuny (1974). Pigments diversity (Margalef, 1960) and the percentage of chlorophyll a

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degradation Plante-Cuny (1974). were calculated. Three core replicates of sediments (with an internal area of 0.01 m-2 and to a depth of approximately 20 cm) were collected, in each station

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and sampling occasion, to determine benthic macroinvertebrates composition. Each replicate sample was washed through a 1 mm mesh sieving bag and the remains preserved in a solution of 70 % ethanol colored with Rose Bengal.

2.3. Data analysis

No detailed spatial analysis was done since no significant differences were found in previous statistical tests carried out, for most environmental parameters and for benthic invertebrate densities, considering the three or two sediment samples in each lagoon. For each benthic sample, taxa density and richness, diversity using Shannon-Wiener diversity index (Shannon and Weaver, 1963), and evenness (Pielou, 1966), were determined. Taxa were

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ACCEPTED MANUSCRIPT classified in terms of: 1) taxonomic groups; 2) trophic groups, following the same criteria as Gamito (2008) and references therein; 3) ecological groups, according to their sensitivity to an increasing stress gradient (i.e. increasing organic matter enrichment), as defined in Grall and Glémarec (1997) and Borja et al. (2000), and obtained from http://ambi.azti.es/ (accessed in January 2014). In order to see how the benthic macroinvertebrates were associated with the environmental

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variables studied, Canonical Correspondence Analysis (CCA) was applied to the data (mean densities of the most abundant taxa, in each station). Previously, Principal Component Analysis (PCA) was performed on the mean values of water and sediment parameters, to determine which variables were correlated and to summarize lagoons characteristics in an ordination diagram.

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CCA included just the environmental variables that were not highly correlated in PCA. Environmental data were first centred and standardized, once variables had different units (Pielou, 1984). T-Student and Mann-Whitney U tests were used to compare the annual mean

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values of benthic macroinvertebrate parameters from the two lagoons. The significance level used was 95% (p ≤ 0.05). The software used for statistical analysis was CANOCO (version 4.54) and SPSS (IBM, version 19).

3. Results

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3.1. Hydrological parameters

The climate in southern Portugal, where both lagoons are located, can be characterized by warm temperatures, dry and hot summers (Table 1). In both lagoons, the raining season started in

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September 2001, and December 2001 was the month with maximum rainfall (Fig. 2). The water level in the lagoons increased during the raining season, till the sand barrier was artificially or naturally destroyed. In Foz do Almargem there were four openings of the lagoon, three of which

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were induced by local fishermen. During December 2001, a natural opening occurred and the lagoon stayed in connection with the sea until mid-January. Salgados lagoon was artificially opened three times. Also in December, after the artificial opening, the lagoon became naturally connected to the sea for nine days and in January 2002, the lagoon reopened naturally for more nine days, after a period of strong rainfall and sea storms. Although Salgados lagoon was opened five times and in Foz do Almargem there were only four openings, the total number of days Foz do Almargem lagoon was in connection with the sea (63 days) almost doubled the period of connection in Salgados (32 days). Both lagoons maintained the connection with the sea for a longer time after natural openings, than after artificial interventions.

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ACCEPTED MANUSCRIPT 3.2. Water and sediment parameters Foz do Almargem presented higher annual means of salinity, N:P ratio and pigment diversity, while in Salgados lagoon greater values were found for pH, total solids in suspension, dissolved oxygen, nitrites, ammonia, total dissolved inorganic nitrogen, orthophosphates, total phosphorus, chlorophyll a and phaeo-pigments concentrations (Table 2). The nutrients concentration in Salgados was more than 50 to 60 times greater for phosphates and total phosphorus, and 8 or 17

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times greater for nitrites and ammonia. Also chlorophyll a in Salgados lagoon was much higher than in Almargem, more than 50 times.

Statistical analyses found significant (0.01 < p ≤ 0.05) and highly significant (p ≤ 0.01) differences between the annual mean values of most water parameters in the two lagoons. Only for

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temperature, nitrates and dissolved oxygen concentrations, did the results indicated that differences between the two lagoons were not significant (p > 0.05).

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Foz do Almargem presented annual mean values of clay content, silt content, chlorophyll a and phaeo-pigments concentrations lower than Salgados and higher means of sand content, water content, chlorophyll a degradation index and pigments diversity (Table 2). Statistical analyses performed with the mean annual values revealed that, for most sediment parameters, differences between lagoons were not significant. Only chlorophyll a and pigments diversity showed evidences of significant differences in the two lagoons (0.01 < p ≤ 0.05).

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Several PCA ordinations were performed, the first one considering only the water parameters and the second the sediment parameters. From these analyses, the parameters with longer arrows, which means that they have greater influence and importance on stations characterisation were selected and used in a third PCA (Fig. 3). This analysis has the main objective of understanding

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the relations between environmental parameters and their relevance in the characterization of Foz do Almargem and Salgados lagoons. The ordination biplot disposed all samples from Foz do Almargem in the left side of axis I and most samples of Salgados lagoon in the right side of this

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axis. Thereby, the majority of Salgados samples were characterized by higher mean values of clay content, chlorophyll a in the sediment, orthophosphates concentration, organic matter content, phaeo-pigments concentration in the sediment, chlorophyll a in the water, dissolved oxygen concentration; and lower mean values of pigments diversity in water and N:P ratio. Foz do Almargem had the opposite characteristics, with lower values of most parameters except pigment diversity and N:P ratios. The assessment of chlorophyll a in the water (mg m-2) and chlorophyll a in the sediment (mg m-2) in the two lagoons revealed that in Foz do Almargem the amount of benthic chlorophyll was greater than pelagic chlorophyll, while in Salgados lagoon the inverse situation was observed.

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ACCEPTED MANUSCRIPT Only in June and in October 2001, did chlorophyll a in Salgados sediment present higher values than chlorophyll a in the water (Fig. 4).

3.3. Benthic macroinvertebrate communities The number of taxa identified in both lagoons was very low (table 3). The T-Student test and

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Mann-Whitney U test, used to compare the annual mean values of benthic macroinvertebrate parameters from Foz do Almargem and Salgados lagoons, showed that total macroinvertebrate densities presented significant differences (0.05 ≥ p > 0.01) and that Chironomus sp. densities and Lekanesphaera hookeri densities had highly significant differences (p ≤ 0.01) in the two

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lagoons.

The two lagoons were dominated by different groups of benthic macroinvertebrates, with Mollusca being the most abundant group in Foz do Almargem, while Insecta, Oligochaeta and

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Crustacea were the more relevant groups in Salgados lagoon (Table 3 and Fig. 5). Regarding trophic groups, both lagoons were dominated by deposit feeders and although the other trophic groups were present they were so only in low quantities. The AMBI Ecological Group III dominated the macrobenthic community in both lagoons.

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3.4. Environmental parameters and benthic macroinvertebrate communities The CCA showed that the macroinvertebrate communities in the two lagoons were distinct and that densities of the main taxonomic groups were associated with different environmental variables (Fig. 6).

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The bivalves Abra segmentum and Cerastoderma glaucum and the gastropods Peringia ulvae and Ecrobia ventrosa occurred only in Foz do Almargem and their densities were negatively related to total phosphorus and chlorophyll a concentration in water, clay content and chlorophyll

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a concentration in the sediment. Higher densities of the polychaetes Capitella capitata and Hediste diversicolor were also associated with lower concentrations of chlorophyll a in water and total dissolved inorganic nitrogen, clay content and chlorophyll a concentration in the sediment. The Amphipoda Corophium multisetosum occurred exclusively in Salgados stations and, just as Chironomus sp., other Insecta and Oligochaeta, densities were positively related to total phosphorus concentration, clay content and chlorophyll a concentration in the sediment, chlorophyll a concentration in water and with total dissolved inorganic nitrogen. The Isopoda Lekanesphaera hookeri was placed closer to the centre of the diagram, and as it was present in most samples from the two lagoons, it was not strongly influenced by any of these environmental variables. The Monte Carlo permutations test determined significant relations (p=0,002) between

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ACCEPTED MANUSCRIPT the benthic macroinvertebrate groups from the two lagoons and the selected environmental variables.

4. Discussion Hydrological conditions:

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Foz do Almargem and Salgados lagoons showed some differences in their hydrological regimens, which were mainly related to the sources of freshwater, the date and process of lagoon opening, the morphology and the geographic location of the lagoons.

Freshwater inputs in Foz do Almargem were determined by rainfall and river runoff. When the

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lagoon was isolated from the sea, water level resulted from the balance between freshwater inputs and water evaporation. In Salgados lagoon, besides the natural freshwater inputs, water

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level was also influenced by the volume of wastewater discharged, which is usually particularly relevant during the dry season, keeping water in the lagoon at a medium level (Coelho, 2013). The different water sources result in different nutrient loads. In Foz do Almargem. nitrates from agricultural activities dominate, which implies a higher N:P ratio. On the contrary, in Salgados, phosphates and ammonium from waste water dominate, thus showing a lower N:P ratio. With the start of the raining season, water level increased and several openings occurred in the

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lagoons. Salgados lagoon was opened five times and in Foz do Almargem there were four openings, but the total number of days Foz do Almargem lagoon was in connection with the sea almost doubled the period of connection in Salgados. The shorter or longer time lagoons maintained the connection with the sea depended on different factors. Longer periods of

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connection are favored by waves with low energy, which accumulate less sand in the channel; greater rainfall and river runoff, which keep a permanent flow into the sea; high water level in the lagoon when the barrier is opened, which allows for the formation of a larger and deeper channel;

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and tides with low range (neap tides), which have a smaller effect on sediment deposition in the channel (Pinto et al., 2001)

Besides the greater rainfall in Foz do Almargem, two other factors might have contributed to its longer period of connection with the sea. Those were the smaller dimension of the lagoon and its location in a coastal area with greater erosion. The lower capacity of water retention by the lagoon, associated with greater rainfall and river runoff, facilitated the connection with the sea. There is also the fact that Foz do Almargem is located in one of the areas of Algarve with highest rate of coastal erosion (Teixeira, 2009) and, during winter, storms removed great part of the sand from the beach and easily destroyed the sand barrier.

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ACCEPTED MANUSCRIPT Salgados lagoon has a greater capacity of water retention due to its larger surface and is located in a coastal area (Armação de Pêra bay) that tends to accumulate sediments from the sea and that does not suffer from significant coastal erosion (Teixeira, 2009). Thereby, the formation of the sand barrier and the closing of the lagoon would take less time than in Foz do Almargem. The artificial openings in Foz do Almargem were illegally done by local fishermen with the purpose of catching fish in the channel and in the mouth of the lagoon, while in Salgados, artificial

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openings were performed by the regional environmental services to promote water renewal and prevent flooding in the golf course nearby. The natural openings in both lagoons happened after artificial interventions, when the sand barriers were thinner and more exposed to the sea.

When the lagoons were in connection with the sea, water renewal was dependent not only on

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freshwater inputs but also on the strength and height of tides. In many occasions, the sea water influence was noticed only in the downstream and intermediate stations, and water was flowing

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just in the deepest channels of the lagoons, leaving a great extension of emerged sediment. Sea water inflow was greater in Foz do Almargem. Nevertheless, the shallowest areas of the lagoon were not submerged most of the times, since most of the lagoon bottom is above the mean sea water level, that is, more than 2m above the hydrographic zero. Consequently, there is a sudden changed on the main characteristics of the habitat of the lagoons. Large extensions of their bottom remained exposed to the air, when the inlet is open, being only temporally covered by water with the high tides. In the opposite situation, when the inlet is closed, the lagoon’s bottom is

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permanently covered by water.

Benthic macrofauna structure:

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Both lagoons presented lower richness compared to other Portuguese ICOLLs such as Santo André lagoon (Correia et al., 2012). The benthic macrofauna density in both lagoons was higher

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than in Albufeira coastal lagoon (Quintino and Gentil, 1988) and approximately 50% higher than the ones observed in Santo André, where mean annual densities were always lower than 10x103 ind.m-2 (Correia et al., 2012).

Taxa richness in both lagoons was very low, with only 9 taxa in Foz do Almargem, and 15 in Salgados. The range of diversity values found in Foz do Almargem (0.59 - 1.52 bits ind-1) and Salgados (0.51 - 2.03 bits ind-1) were similar to those determined by Cancela da Fonseca (1989) in Santo André coastal lagoon (0.5-1.5 bits ind-1) and lower than the values described for Albufeira coastal lagoon (2-3.5 bits ind-1) (Quintino and Gentil, 1988). This low diversity is probably due to the extreme isolation of both coastal lagoons from the open sea. In addition, periods of channel opening, whether natural or artificial, occur in autumn and winter, outside the

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ACCEPTED MANUSCRIPT breeding and larval dispersal season of most benthic species. Thus, only the migratory species or adults with high mobility can colonize the lagoons and eventually settle down. Benthic macroinvertebrate communities in the two lagoons were distinct, as well as their relations with environmental parameters. Foz do Almargem, a lagoon with a higher marine influence and with an important benthic primary production, is dominated by small deposit-feeder gastropods of the Hydrobiidae family. The inlet of this lagoon opened several times during the wet season.

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When that happened, a sudden increase of salinity occurs, and most of its bottom remained uncovered by water for several days, preventing the establishment of a stable community. Most of the benthic fauna died when the bottoms turned tidal. The harsh physical environment is clearly controlling the community.

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Salgados lagoon is a hypereutrophic lagoon, characterised by high nutrients concentrations, which results in an almost permanent bloom of phytoplankton (Coelho 2013). Few benthic

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organisms resist to these extreme conditions except deposit-feeder insect larvae of the Chironomidae family.

In choked lagoons and in ICOLLs (such as Foz do Almargem, Salgados, Santo André and Albufeira lagoons), the diversity is low and communities are usually dominated by a few, but very abundant, small sized opportunistic species (r - selected species, characterized by a short generation time, a high reproductive effort and many small offspring) (Gamito et al., 2005).

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Most taxa that occurred in Foz do Almargem were also identified in other Portuguese lagoons (e.g. Abra segmentum, Cerastoderma glaucum, Chironomus sp., Hediste diversicolor, Peringia ulvae, Lekanesphaera hookeri,) (Correia et al., 2012 and references therein) and in Mediterranean lagoons (see, for example Amanieu et al., 1978-1979, Tagliapietra et al., 2000;

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Basset et al., 2006). In Ria Formosa coastal lagoon, one of the sites studied by Gamito (2006, 2008) presented a benthic macroinvertebrate community similar to that found in Foz do Almargem, which was dominated by P. ulvae, E. ventrosa, C. glaucum, A. segmentum, C.

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capitata and C. salinarius. According to the author, this group of species can tolerate high salinity as well as large variations in salinity, suspended matter and pH. The site was considered to have characteristics of a stressful environment, caused by very restricted water renewal. In Salgados lagoon, Insecta was the only taxonomic group observed during the whole studied period and most of the time it showed monthly mean densities greater than the other groups. Chironomus sp., oligochaets, Lekanesphaera hookeri and Corophium multisetosum were the dominant taxa in Salgados lagoon. The benthic fauna is comparable to the one found in the Santo André coastal lagoon, during the decade of 1980, where the benthic community was dominated by lagoonal and continental taxa, presenting a great number and diversity of insect species. This period of time was characterized by eutrophic conditions (e.g. low dissolved oxygen

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ACCEPTED MANUSCRIPT concentrations) and low salinity values, associated to insufficient water renewal and interchanges with the sea (Cancela da Fonseca, 1989; Bernardo, 1990; Correia et al., 2012). Most of the insects in Salgados have brackish water affinities (Wolf et al., 2009), as well as the amphipods Corophium multisetosum (Queiroga, 1990), while the fauna of Foz do Almargem has euryhaline affinities, being common in euryhaline lagoonal systems of Southern Portugal, such as

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the Ria Formosa (Gamito, 2008). No confinement or saprobity gradient could be clearly detected in the lagoons. The large environmental variability, the short time and the season in which both coastal lagoons were connected to the sea, as well as the small size of the lagoons may have prevented strong

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gradients from the inlet upstream.

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Benthic ecological characterization:

Regarding trophic groups, Foz do Almargem presented a greater diversity of groups (suspension feeders, deposit feeders, suspension / deposit feeders, herbivorous and carnivorous / scavengers / omnivorous) than Salgados lagoon (deposit feeders, herbivorous and carnivorous / scavengers / omnivorous). Both lagoons were dominated by deposit feeders.

Benthic macroinvertebrate assemblages in lagoons with very restricted water renewal such as

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choked lagoons and ICOLLs, are mainly composed by deposit-feeders and some herbivorous crustaceans (e.g. Sphaeroma, Corophium), grazer gastropods (e.g. Hydrobia), carnivorous polychaetes (e.g. Hediste) and deposit-feeders insect larvae (e.g. Chironomids) (Gamito et al., 2005). Boaventura et al. (1999) refer to deposit feeders as the most abundant group in Santo

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André coastal lagoon. Other studies point out that this trophic group dominates benthic communities in coastal ecosystems, mentioning the relation between deposit feeders abundance

2004).

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and fine sediments, rich in organic matter (Barnes and Villiers, 2000; Levinton and Kelaher,

The effects of anoxia, due to the increase of organic matter load, cause strong changes on the benthic community by limiting the growth of benthic filter feeders and, thus, providing a shift in species composition from bivalves to polychaetes and oligochaetes (e.g. Pearson and Rosenberg, 1978; Weston, 1990; Warwick and Clarke, 1990). In Salgados lagoon, the absence of filter feeders can be related to hypoxia and anoxia events, associated to eutrophication. In terms of ecological groups, the composition of benthic macroinvertebrate communities in Foz do Almargem and Salgados was distinct, although both lagoons were dominated by taxa tolerant to excess organic matter enrichment (AMBI Ecological Group III).

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ACCEPTED MANUSCRIPT In Foz do Almargem, the densities of group III taxa accounted for 96% to 100% of the monthly mean densities, whereas in Salgados lagoon these taxa represented 49% to 94%. The remaining taxa belong to group V, which include first-order opportunistic taxa associated with pronounced unbalanced situations. Second-order opportunistic taxa, indicators of slight to pronounced unbalanced situations (Group IV - AMBI), were observed in Salgados lagoon during the entire studied period, except in July 2002. Nevertheless, some of the taxa found in Salgados are not

actualizations in AMBI software database).

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assigned to any of the AMBI groups defined by Borja et al. (2000, including the successive

In ICOLLs, which are open to the sea just in a few occasions and during short periods of time, as it happens in Foz do Almargem and Salgados lagoons, the migration of marine organisms is

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intermittent and dependent on the openings of the lagoons to the sea. The presence of marine organisms inside the lagoons can be temporary, depending on the lagoon conditions, and may lead to a situation where only few species survive throughout the year (Pérez-Ruzafa and

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Marcos, 1992; Pérez-Ruzafa et al., 1987, 1991; Gamito et al., 2005).

Lagoons hydrodynamics and management

The structure and the dynamics of benthic communities in coastal lagoons are mainly influenced by the communication with the sea and by the hydrological and meteorological conditions; this

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makes the marine renewal and the maintenance of brackish characteristics essential to the prevention of eutrophication and of the decrease in water quality (Cancela da Fonseca, 1989). The various episodes of sea-connection / isolation that occurred in the lagoons may have prevented a stable environment, adequate for the establishment of steady communities. In

community.

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Salgados lagoon, the hypereutrophic condition has also negatively influenced the benthic

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Although no strong statistical tests could have been applied to the data to show the effects of physical stress, since the lagoons were sampled only once with the inlets open, the benthic organisms have the advantage of integrating the environmental conditions they live in. Consequently, the structure of the benthic community and the relative abundance of the different functional groups gave strong indications about the surrounding environment. These functional groups may be based, for example, either on their different sensitivity to organic pollution or on the trophic relations between them. Unfortunately, no clear indicators or metrics were yet developed to allow a clear separation on the effects of organic pollution from the effects of physical stress (Elliott and Quintino, 2007), although some separation based on community species composition could be tempted (e.g. Gamito, 2008).

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ACCEPTED MANUSCRIPT The comparison of data taken when the lagoons were closed (December 2001) and connected to the sea (January 2002) showed that, regarding benthic macroinvertebrate communities, total densities presented different tendencies in the two lagoons, increasing in Foz do Almargem and decreasing in Salgados. The higher density found in Foz do Almargem was due to an augment in the Gastropoda Peringia ulvae and the Isopoda Lekanesphaera hookeri, while in Salgados lagoon, the major cause for the reduction of total benthos density was the diminution of the

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Insecta Chironomus sp.

When the lagoons were in connection with the sea, some of the major effects described by other authors (Barnes, 1980; Cancela da Fonseca, 1989; Bernardo, 1990; Pereira Coutinho et al., 2012) were also observed in Foz do Almargem and Salgados lagoon, such as the increase in

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salinity and the discharge of biological, organic and inorganic material accumulated in the lagoons (e.g. total solids in suspension and chlorophyll a in the water, clay and silt from the sediment). Still, the lagoons had an increase in some nutrients concentrations, namely dissolved

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inorganic nitrogen compounds. These compounds were mainly nitrates and nitrites, which could be associated to the river runoff due to the high rainfall registered in January 2002. In Salgados lagoon, the increase and high value of ammonia concentration could have resulted from the wastewaters discards and from the release of this compound from the sediment in a situation of oxygen depletion near the bottom, as it was registered by Bernardo (1990) in Santo André lagoon.

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As already pointed out by other authors, for example McSweeney et al. (2014), prolonged closure has important management implications, such as flooding of the surrounding fields and a decrease in water quality. Nevertheless, the opening of the lagoon may also bring negative consequences for the lagoons, mainly in the lagoons with a bottom above mean water sea level,

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since they change from a permanently submerged environment to a tidal bottom, causing the

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death of most benthic organisms.

Ecological quality responses Cloern (2001) found fundamental differences in the system-level responses to nutrient enrichment in lakes when compared to estuarine-coastal ecosystems, suggesting that the old models and assumptions on the response of the system to nutrient inputs should be reviewed. The assessment of eutrophication and water quality classification in coastal lagoons is not an easy task due to the great variability of spatial and temporal conditions. Although most of the year the Foz do Almargem and Salgados lagoons were isolated from the sea and presented some characteristics similar to still waters, lakes and reservoirs, during the short periods of connection with the sea they functioned just like small estuaries. However, the tidal range was smaller than in

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ACCEPTED MANUSCRIPT real estuaries, reducing considerably the flooded area of the lagoons and increasing the area of the sediment exposed to air. The excess nutrient load and the high physical stress caused by the inlet openings pointed out to similar responses of the benthic organisms, with a dominance of few r-selected deposit-feeder species. Taxa composition is, however, different, which might be due not only to different organic matter loads but also to differences in salinity. Brackish water Insects dominated the

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hypereutrophic brackish lagoon while euryhaline gastropods dominated the lagoon subjected to long periods of physical stress.

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Acknowledgements

This study was funded by Fundação para a Ciência e Tecnologia (FCT - Portuguese National Board of Scientific Research) through the PRAXIS XXI scholarships’ program (ref. PRAXIS

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XXI/BD/21521/99), and through the MARE (Marine and Environmental Sciences Centre) Strategic Programme (ref. UID/MAR/04292/2013), and it had also the logistic support of the former Direcção Regional do Ambiente e Ordenamento do Território do Algarve. We would like to thank Ana Paula Gaspar for her collaboration; Dinamene Sousa for helping in the field trips and Carlos Afonso for taxonomic identification support. We also thank the three anonymous reviewers

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ACCEPTED MANUSCRIPT Table 1 – Main characteristics of the two lagoons:

Foz do Almargem

Csa – Warm temperate; summer dry; hot summer

Total days in connection with the sea:

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Salinity type (Venice System, 1959):

Meso-Polyhaline

Trophic type (based on nutrients and chlorophyll concentrations, in Coelho 2013; Coelho et al 2007):

Mesotrophic

Hypereutrophic

Sand (downstream station)/ Silty sandy mud (upstream station)

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Sand (downstream and upstream stations)/ extremely silty sandy mud (intermediate station)

Mesohaline

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Sediment textural classification (adapted from Flemming, 2000)

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Type of climate (Köppen-Geiger climate classification, in Kottek et al. 2006):

Salgados

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NO3 NO2 NH4 DIN

Nitrates (µM N) Nitrites (µM N) Ammonia (µM N)

Ptes TP NP Chla

Orthophosphates (µM P) Total Phosphorus (µM P) N:P ratio

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Dissolved oxygen (mg l )

Salgados 20.9 ± 3.49 8.2 ± 5.25 8.6 ± 0.61 81.1 ± 68.20

8.9 ± 1.61 26.8 ± 42.41

10.2 ± 5.07

0.7 ± 0.61 3.2 ± 3.00

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Phae-

Phaeo-pigments (µg l )

PigD

Margalef’s pigment diversity index (bits)

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Sediment parameters Clay content (%) Silt content (%) Sand content (%) Water content (%) Organic matter content (%) -1

Chlorophyll a (µg g )

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Phaeo-pigments concentration (µg g )

%PhaeS PigDS

Chlorophyll a degradation index (%) Pigment diversity index (bits)

3.0 ± 3.43 0.8 ± 0.88

14.0 ± 15.21

2.4 ± 0.27

2.1 ± 0.31

3.0 ± 3.38 15.6 ± 21.51 81.4 ± 24.06 30.3 ± 8.22 3.0 ± 2.87 7.1 ± 6.66

9.5 ± 11.29 19.6 ± 20.70 71.0 ± 30.98 28.5 ± 8.21 3.8 ± 4.18 15.6 ± 13.79

6.9 ± 7.84

10.7 ± 13.83

44,44 ± 15,31 2,96±0,54

37,45±13,47 2,62±0,36

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PhaeS

17.9 ± 29.82 5.7 ± 7.79 56.0 ± 123.00 79.7 ± 128.30

55.7 ± 34.68 65.2 ± 42.04 1.5 ± 1.84 158.5 ± 177.95

0.9 ± 0.69 1.3 ± 0.76 39.1 ± 41.18

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Chlorophyll a (µg l )

30.6 ± 42.41

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Total dissolved inorganic nitrogen (µM N)

%Clay %Silt %Sand %WSed %OM ChlaS

Almargem 21.8 ± 4.59 13.1 ± 7.96 8.3 ± 0.39 38.2 ± 33.60

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Code: Temp Sali pH TSS DO

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521 ± 524

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Chironomus sp. Ephydridae Tabanidae Ceratopogonidae Empididae Rhagionidae Brachyceres Berosus spinosus Hesperocorixa sahlbergi Corixa affinis Parasigara infuscate Notonecta sp. Capitella capitata Hediste diversicolor n.ident. Lekanesphaera hookeri Corophium multisetosum Ecrobia ventrosa Peringia ulvae Abra segmentum Cerastoderma glaucum

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Diptera Diptera Diptera Diptera Diptera Diptera Diptera Coleoptera Hemiptera Hemiptera Hemiptera Hemiptera Polychaeta Polychaeta Oligochaeta Isopoda Amphipoda Gastropoda Gastropoda Bivalvia Bivalvia

Salgados 15518 ± 25154 4.38 ± 1.75 15 Trophic AMBI 1.09 ± 0.54 groups groups 0.49 ± 0.22

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Total benthos density (ind m ) Taxa richness (S / 0.03 m2) Total richness Shannon-Wiener (H’bits / 0.03 m2) Evenness (j / 0.03 m2)

Almargem 17001 ± 8987 5.48 ± 1.86 9 0.99 ± 0.39 0.43 ± 0.16

8980 ± 13732 96 ± 135 51 ± 96 29 ± 41 9 ± 26 2±5 13 ± 27 56 ± 60 5±9 10 ± 23 65 ± 141 2±5

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Table 3 – Annual mean (number of individuals m-2) and standard deviation values of benthic macroinvertebrates in Salgados and Foz do Almargem coastal lagoons. Diversity parameters – average values per sample. Each sample consisted of three corers of 0.01 m-2 internal area). Trophic Groups: CVO – Carnivorous, scavenger and omnivore; DF – deposit feeder; H – Herbivorous; S – Suspension feeder; S-DF, Suspension and deposit feeder. Based on Gamito 2008 (and references therein) and in Oscoz et al. 2011. AMBI groups: n.a.- not assigned.

206 ± 368 118 ± 67 10 ± 26 1503 ± 1508

236 ± 300 13665 ± 9715 225 ± 382 507 ± 853

2165 ± 3699 2716 ± 7174 1099 ± 2943

DF DF CVO CVO CVO CVO CVO CVO CVO CVO CVO CVO DF CVO DF H DF DF DF S-DF S

III IV IV IV IV IV IV n.a. n.a. n.a. n.a. n.a. V III V III III III III III III

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Fig. 3 - Principal Component Analysis performed on selected water and sediment parameters mean values from Foz do Almargem and Salgados coastal lagoons. Cumulative percentage variance explained by axes: I – 37.6 %; I + II – 61.9 %. Station codes: First character corresponds to the coastal lagoon (A – Foz do Almargem; S – Salgados) and subsequent ones to

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month (JN- June; A- August; O- October; D- December; J- January; MR- March; M- May; JLJuly) and year of survey (1- 2001, 2-2002). Environmental variables: see Table 2.

do Almargem and Salgados lagoons.

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Fig. 4 - Seasonal variation of chlorophyll a in the sediment and chlorophyll a in the water in Foz

Fig. 5 - Seasonal variation of benthic macroinvertebrate communities in Foz do Almargem and Salgados lagoons, according to the main taxonomic groups, trophic groups and AMBI ecological groups.

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Fig. 6 - Canonical correspondence analysis performed with the benthic macroinvertebrate groups (mean density) from Foz do Almargem and Salgados lagoon. Cumulative percentage variance explained by axes: Species - I = 51,6 % and I + II = 62,8 %; and Species-environment relation – I = 71,3 % and I + II = 87,0 %. Monte Carlo test of all canonical axes p = 0,002. Station codes and

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Environmental variables: the same as in Fig. 3. Benthic macroinvertebrates: Hedi – Hediste diversicolor; Capi – Capitella capitata; Leka – Lekanesphaera hookeri; Coro – Corophium multisetosum; Vent – Ecrobia ventrosa; Hydr – Peringia ulvae; Abr – Abra segmentum; Cera –

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Cerastoderma glaucum; Chiro –Chironomus sp.; INSE – Other Insecta; OLIG – Oligochaeta.

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ACCEPTED MANUSCRIPT Foz do Almargem and Salgados are two ICOLLs in Southern Portugal studied for 1 year. They are small sized lagoons intermittently opened for 63 and 32 days respectively. Foz do Almargem has very reduced diversity, dominated by euryhaline mollusks. Hypereutrophic Salgados is dominated by few insects and by oligochaetes. Physical disturbance and excessive nutrients’ load are the main disturbing factors.

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