Factors structuring temporal and spatial dynamics of macrobenthic communities in a eutrophic coastal lagoon (Óbidos lagoon, Portugal)

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Abstract

The present work aimed to identify the main environmental drivers shaping temporal and spatial dynamics of macrobenthic communities within a eutrophic coastal lagoon. Sediments in the Óbidos lagoon showed a gradient of increasing metal contamination from the inlet area to inner branches. The mid-lower lagoon area exhibited an intermediate contaminated condition between the inlet and upstream areas, suggesting that the effects of the organic loadings into the lagoon may be reflected until this area. This transitional feature was corroborated by biological data, with macrobenthic assemblages displaying characteristics of down- and upstream areas. Macrobenthic abundance peaked in winter, which was associated with a higher nutrient availability (mainly ammonium) and the proliferation of green macroalgae in mid-lower and inner lagoon areas. However, massive macroalgae growth resulted in a sharp decrease of macrobenthic diversity and abundance in spring, particularly where the higher amounts of decaying algae were detected. Higher dissimilarities between assemblages were detected during winter (and spring, for trophic composition), while in summer, differences were highly attenuated. The least contaminated area (close to the sea inlet) experienced smaller temporal variations for environmental variables, as well as the lowest temporal biological variability. This area was dominated by carnivores, which were related with increased salinity. Deposit-feeders were numerically dominant in the lagoon, being generally spread within organically enriched sandy and muddy areas. The high concentration of chlorophyll a and suspended particulate matter in water was reflected in the abundance of deposit-feeders/suspension-feeders, taking benefit of the high primary productivity. On the other hand, deposit-feeders/herbivores responded to the decay of macroalgae mats in the sediment. Biological associations varied with the biological data used (taxonomic versus trophic group composition; abundance versus biomass), highlighting the relevance of the combination of different data analysis’ approaches. In general, BIOENV analysis indicated total phosphorus, biomass of Ulva, metals and organic carbon and nitrogen as being significantly influencing benthic patterns. On the other hand, discrepancies in ecological behaviours of some taxa were also detected in the present study stressing the need for additional studies on the relationships between macrobenthic communities and environmental variables. Implications of the present results for monitoring studies are discussed.

Research highlights

► Total phosphorus, biomass of Ulva, metals, organic carbon and nitrogen were significantly related with macrobenthic patterns. ► Massive macroalgae growth resulted in a sharp decrease of macrobenthic diversity and abundance. ► The nature of biological data used was reflected in the biological patters. ► Relationship between biological and environmental data highlighted some discrepancies in ecological behaviours of dominant taxa.

Introduction

Coastal lagoons are often characterized by generally restricted water exchange with the open sea and shallow depths (UNESCO, 1981), reducing dilution processes and enhancing sediment retention of contaminants (Pérez-Ruzafa et al., 2005). Their association with the adjacent draining basin makes such systems vulnerable to eutrophication, leading to low water oxygenation and the production of toxic hydrogen sulphide (UNESCO, 1981). In some cases, anoxic conditions can even occur in the sediment during the night favouring the release of metals and nutrients from the sediment to the overlying water (Point et al., 2007, Pereira et al., 2009a). Thus, coastal lagoons may experience an additional problem of metal contamination, with potential repercussions in the biota.

Macrobenthos is a key component of coastal ecosystems (including lagoons), playing a vital role in detritus decomposition, nutrient cycling and energy flow to higher trophic levels (Masero et al., 1999, Heilskov and Holmer, 2001, Mermillod-Blondin et al., 2005, Carvalho et al., 2007). This faunal component has been frequently used in environmental quality assessment of coastal systems (e.g. Ponti and Abbiati, 2004, Carvalho et al., 2006b, Carvalho et al., 2010, Munari and Mistri, 2008). Nevertheless, it is often difficult to discriminate between natural and human-induced changes based on macrobenthic communities (Elliott and Quintino, 2007). The heterogeneous distribution of benthic organisms in marine soft sediments and sediment-related variables (e.g. contaminants, sediment particle-size, organic matter content) has been frequently reported (Luoma and Phillips, 1988, Koutsoubas et al., 2000, Ysebaert and Herman, 2002, Blanchet et al., 2005). The spatial and temporal distributions have been related either to physical (e.g. water depth, water temperature, hydrodynamics, sediment grain size) or biological factors (life cycle, larval settlement dynamics, microbial activity, bioturbation, competition, predation) or interactions between them (Snelgrove and Butman, 1994, Mancinelli et al., 1998, Ysebaert and Herman, 2002, Blanchet et al., 2005, Como and Magni, 2009).

Some of the characteristics of coastal lagoons (e.g. shallow depth and limited water exchange) result in considerable daily and seasonal changes in environmental variables (e.g. temperature) with consequences for the benthic assemblages (Como and Magni, 2009). These fluctuations can have repercussions on physico-chemical processes in sediments (e.g. Lillebø et al., 2004, Mucha et al., 2004, Point et al., 2007) and act as a driving force in the dynamics of the marine benthic environment, affecting species’ life cycles (Marques et al., 1994). Therefore, besides spatial variability, knowledge on the temporal changes in macrobenthic communities from coastal lagoons can be highly relevant namely for the establishment of monitoring programmes.

The Óbidos lagoon (western Portugal) is moderately contaminated by metals and has experienced high nutrient loads of anthropogenic origin (particularly nitrogen and phosphorus) leading to signs of eutrophication (Pereira et al., 2009a, Pereira et al., 2009b). In coastal lagoons, this is a common environmental problem that can result in community dominance changes, as well as alterations in species composition (Dolbeth et al., 2003, Pranovi et al., 2008). This system has been studied in terms of the relationship between macrobenthic communities and several sediment parameters during the winter season (Carvalho et al., 2005, Carvalho et al., 2006b), and more recently regarding water quality (Pereira et al., 2009a, Pereira et al., 2009b). Concerning macrobenthic communities it was observed that some taxa such as Capitella spp., usually associated with organic enrichment (Pearson and Rosenberg, 1978), increased their abundance seawards, where no major allochtonous sources of organic enrichment are present (unpublished data). This change appeared to occur simultaneously with a generalised increase of Ulva spp., particularly within the middle area.

The present study tests whether benthic communities, sediment properties, water quality, and their relationships change along one year, in five sites located at upper (2 sites), middle (2 sites) and lower (1 site) parts of the Óbidos coastal lagoon, an ecosystem with pronounced spatial variation of macrobenthic communities, water quality and sediment properties. In order to better clarify the complex link between abiotic and biotic interactions, multivariate analysis approaches were used both for taxon and for the trophic groups’ composition, using abundance and biomass data.

Section snippets

Study area

The Óbidos lagoon is a shallow coastal ecosystem, located on the west coast of Portugal with a wet area of 7 km2, permanently connected to the sea through a narrow inlet (Fig. 1). The lagoon is characterized by semi-diurnal tides (tidal range 0.5–4.0 m depending upon location and tidal phase) (Malhadas et al., 2009). It comprises areas of different morphological and sedimentary characteristics: sand banks and narrow channels in the lower/middle lagoon; muddy sediments in the two inner branches

Water and sediment characteristics

In spring and summer, water temperature reached high values at the branches (sites 4 and 5) (Table 1). Salinity was generally lower at site 4 than in the other sites due to freshwater inputs. Dissolved oxygen at sites 1, 2 and 3 was around 100%, while it ranged within broader intervals at sites 4 and 5. In summer and fall, undersaturated levels were registered at site 4. The suspended particulate matter, phosphate, chlorophyll a, concentrations of ammonium and nitrate + nitrite were in general

Spatial and temporal dynamics

In the Óbidos lagoon, the main temporal pattern was a peak of macrofauna abundance during winter, and a general reduction in abundance and number of species during summer/fall, which is in accordance with the reported for other European lagoons (e.g. Arias and Drake, 1994, Tagliapietra et al., 1998, Magni et al., 2006, Como and Magni, 2009). This macrotidal Atlantic coastal lagoon was found to be more similar to the mesotidal Atlantic lagoon located in Arcachon Bay (Bachelet et al., 2000,

Acknowledgments

Susana Carvalho (SFRH/BPD/26986/2006) and Patrícia Pereira (SFRH/BD/17616/2004) benefit from post-doctoral and PhD grants, respectively, from the “Fundação para a Ciência e a Tecnologia” (FCT). Authors would like to thank to Leandro Sampaio and Dulce Subida for help with PERMANOVA analysis. The manuscript was greatly improved by the comments of two anonymous reviewers. This work was financially supported by the company “Águas do Oeste” within the project “Monitoring and modelling the Óbidos

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