Two decades of oligotrophication: Evidence for a phytoplankton community shift in the coastal lagoon of Thau (Mediterranean Sea, France)

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Highlights

  • The decrease in water nutrients confirms oligotrophication in the period 1998–2016.

  • The decrease in phytoplankton biomass (−60%) was associated with a decrease in diatom abundance (−66%).

  • A change in phytoplankton community structure was observed with a shift from Skeletonema-Chaetoceros to Chaetoceros-Pseudo-nitzschia dominance.

  • The median proportion of dinoflagellates relative to diatoms increased significantly, although the total dinoflagellate abundance did not change significantly.

Abstract

Mediterranean costal lagoons have been exposed to anthropic eutrophication for decades. Thau lagoon is one of the largest among them and provides many ecosystem services including shellfish farming. Considerable efforts were made between the 1970s and the late 2000s to improve the wastewater treatment systems in the lagoon watershed. A decrease in nutrient inputs to Thau lagoon was subsequently observed, evidence for the start of a recovery process in Thau lagoon, following oligotrophication. This decrease has significant consequences for ecosystem communities, above all primary producers. In our study, we characterised and quantified long-term changes by analysing long monitoring time-series (1998–2016) of phytoplankton biomass, abundance and composition of the taxa, nutrients and climate conditions, using univariate and multivariate statistics. Our results revealed that two decades of mitigation actions in the Thau lagoon watershed have led to a significant progressive reduction in nutrient concentrations and in phytoplankton biomass (−60%), associated with a decrease in diatom abundance (−66%), particularly affecting Skeletonema spp. The changes were associated with a community shift characterised by a shift in phytoplankton taxonomic dominance from Skeletonema-Chaetoceros to Chaetoceros-Pseudo-nitzschia. The median proportion of dinoflagellates relative to diatoms increased, although the total dinoflagellate abundance did not change significantly.

We hypothesise that the shift in phytoplankton communities is the result of the mixed effects of the reduction in nutrient inputs and of climatic-related variables. Finally, we present a conceptual scheme of the main drivers of phytoplankton community structure to clarify the ecosystem functioning of a Mediterranean lagoon used for shellfish farming, under oligotrophication and climate change.

Introduction

Anthropic eutrophication and its effects on coastal ecosystems and primary producers are well described in the literature (de Jonge and Elliott, 2001; Cloern et al., 2014). The geomorphology and functioning of transitional ecosystems, including coastal lagoons, make them inherently extremely vulnerable to eutrophication (Newton et al., 2014). Eutrophication effects can jeopardise the natural goods and services provided by these ecosystems, whose value is among the highest among natural ecosystems (Basset et al., 2013). As Mediterranean coastal lagoon ecosystems are very densely inhabited, in recent decades, they have been particularly exposed to anthropic eutrophication, mainly due to urbanisation (Zaldívar et al., 2008; Souchu et al., 2010).

Thau lagoon is one of the largest Mediterranean coastal lagoons and provides many ecosystem services including shellfish farming (C. gigas oysters and M. galloprovincialis mussels). Oyster production dominates and represents roughly 10% of French national oyster production, with 12 000 t produced in the 2000s (Gangnery et al., 2001) and 7 300 t in 2016 (DDTM, 2017). Since the 1960s, the increase in anthropogenic inputs, linked to the exponential growth of the human population in the lagoon watershed, has contaminated shellfish farms and caused the eutrophication of Thau lagoon, with significant socio-economic and ecological impacts, such as frequent bans on shellfish sales and major anoxic events (Souchu et al., 1998; Loubersac et al., 2007). In the eutrophic conditions which prevailed in the 1970s and 1980s, large quantities of dissolved inorganic nitrogen (DIN) and phosphorus (DIP) inputs from the watershed resulted in high levels of dissolved nutrients in the lagoon (up to 70 μM for NO3 and 10 μM for DIP, Casellas et al., 1990; Souchu et al., 1998), leading to phytoplankton blooms associated with fast growing diatoms (up to 30 μg Chl a L−1, Tournier and Pichot, 1987; Collos et al., 2003). Thus, diatoms were long identified as the dominant phytoplankton group in Thau lagoon (Pavillard, 1905; Hénard, 1978; Jarry et al., 1990). Skeletonema costatum and Chaetoceros spp. were the most frequent diatom genera in the lagoon, Skeletonema costatum were observed during winter blooms, and Chaetoceros spp. in spring and summer blooms (Collos et al. 1997, 2003; Bec et al., 2005). Dinoflagellates were also present but their contribution to total abundances of phytoplankton communities remained low, except during autumn-winter blooms (Collos et al. 2009, 2014). In the 1970s, improvements were made to waste-water treatment systems in the watershed. A decrease in nutrient inputs to Thau lagoon has been observed ever since, reinforced in the late 2000s, thanks to the EU Nitrates Directive and the Water Framework Directive (WFD) (EC, 1991a; 1991b and 2000), which gradually led to the oligotrophication of the ecosystem (Deslous-Paoli et al., 1998; La Jeunesse et al., 2002; Collos et al., 2003).

In contrast to eutrophication, oligotrophication has rarely been described in coastal ecosystems (Yamamoto, 2003; Borkman and Smayda, 2015; Riemann et al., 2016), particularly in coastal lagoons (Collos et al., 2009; Leruste et al., 2016; Derolez et al., 2019; Le Fur et al., 2019). The literature contains more case studies on freshwater ecosystems, especially lakes (Ruggiu et al., 1998; Ibelings et al., 2007; Jeppesen et al., 2007). The few examples available on oligotrophication in Mediterranean coastal lagoons report modifications in the composition and structure of phytoplankton communities (Collos et al., 2009; Leruste et al., 2016) and macrophyte communities (Pasqualini et al., 2017; Le Fur et al., 2019). Phytoplankton are generally the first autotrophic compartment to respond to a reduction in the concentrations of nutrients following remediation (Leruste et al., 2016; Derolez et al., 2019). In studies of the oligotrophication of lakes, phytoplankton responses to the reduction in nutrients are reported to have resulted in considerable changes in phytoplankton biomass, as well as in the size, structure and diversity and development of mixotrophic organisms (Gaedke, 1998; Ruggiu et al., 1998; Anneville et al., 2005). During the first stages of oligotrophication in Thau lagoon (1998–2005), some changes in phytoplankton communities were observed with the simultaneous appearance of a dinoflagellate species (Alexandrium catenella) and a picocyanobacteria species (Synechococccus) (Collos et al., 2009). However, the long-term trends of phytoplankton communities of coastal lagoons under oligotrophication have been only partially studied, as most authors focused on the main algal groups (diatoms, dinoflagellates) (Gowen et al., 2015; Leruste et al., 2016) and did not consider the whole phytoplankton community at species level.

The aim of this paper is to describe long-term changes in phytoplankton abundance and community composition in Thau lagoon in a context of oligotrophication and climate change since the late 20th century. The specific objective of our study was to check if the expected decreases in phytoplankton biomass and abundance were associated and concomitant with changes in community composition and structure. To this end, we analysed long monitoring time-series (1998–2016) of phytoplankton biomass, abundance and species composition, using univariate and multivariate statistics. The trends were analysed in parallel with changes in nutrient levels and in climate conditions (temperature and rainfall). Finally, based on our results, on the mandala of Glibert et al. (2016), and on the literature, we present a conceptual scheme representing the main drivers of phytoplankton community structure to clarify the ecosystem functioning of a Mediterranean lagoon used for shellfish farming, under oligotrophication and climate change.

Section snippets

Study site and changes in nutrient inputs

Thau is a microtidal and restricted coastal lagoon, connected to the Mediterranean Sea through two permanent inlets (Fig. 1), the Sète channel in the north, which is responsible for 90% of sea water exchanges, and the Pisses-Saumes channel in the south (Fiandrino et al., 2017). The lagoon covers 68 km2, 19.5 km long and 4.5 km wide, with a mean depth of 4 m (Fiandrino et al., 2017). A depth gradient is observed from the south-west to the north-east of the lagoon (mean depth: 3.3 m and 5.2 m,

Meteorological conditions

Air temperature and rainfall monitored by the Sète weather station from 1998 to 2016 revealed changes in the meteorological conditions in the Thau lagoon watershed. Compared with the average temperature for the period 1970–2016 (15.3 °C), annual means showed an increase in temperature from 1998 to 2016 (Fig. 2a). During this period, below average temperatures were only recorded in two years (2005 and 2010). The deviation from the average temperature increased over time, from +0.2 °C in 1998 to

Decrease in chlorophyll a biomass and diatom abundance

Remediation actions in the watershed of an originally eutrophic lagoon over a period of more than 40 years led to a significant reduction in nutrient inputs (La Jeunesse et al., 2002). Previous studies showed that the effect of these actions was a decrease in nutrient concentrations in the water column of Thau lagoon from the 1970s to the early 2000s (Fig. S2, Collos et al., 2009; Gowen et al., 2015). Our study, based on the analysis of 19-year monitoring time-series revealed that the long-term

CRediT authorship contribution statement

Valérie Derolez: Supervision, Conceptualization, Formal analysis, Methodology, Writing - original draft, Writing - review & editing. Dominique Soudant: Conceptualization, Formal analysis, Validation, Methodology, Writing - review & editing. Nathalie Malet: Conceptualization, Formal analysis, Writing - review & editing. Claude Chiantella: Validation. Marion Richard: Writing - review & editing. Eric Abadie: Project administration, Validation, Writing - review & editing. Catherine Aliaume:

Declaration of competing interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This study was based on data collected during the project REPHY (REPHY, 2017) and on the projects “Réseau de Suivi Lagunaire” and Water Framework Directive, which received financial support from Ifremer, Agence de l'Eau Rhône Méditerranée Corse, Région Languedoc-Roussillon/Occitanie and Cépralmar. The authors are extremely grateful to Grégory Messiaen, Martine Fortuné, Elodie Foucault and Dominique Munaron for nutrient analyses, to Tony Carreras, Clarisse Hubert-Renard and the national

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