First steps of ecological restoration in Mediterranean lagoons: Shifts in phytoplankton communities
Introduction
Eutrophication has been defined as a suite of adverse symptoms resulting from the nutrient and organic inputs (De Jonge and Elliott, 2001). High biomass decreases light availability, favoring among the primary producers the community that is most competitive for light, i.e., phytoplankton at the expense of macrophytes (Cebrian et al., 2014). This over-production causes a loss of diversity (Schramm, 1999, De Jonge and de Jong, 2002), habitat destruction and mortalities due to anoxia (Smith, 2006, Carlier et al., 2008). These phenomena negatively impact ecosystem health, result in increased vulnerability to disturbances (Heemsbergen et al., 2004, Worm and Lotze, 2006) and loss of ecosystem services (Bullock et al., 2011). In coastal areas, which are characterized by strong demographic growth, eutrophication has become a serious threat since the 1950s (Nixon, 1995). Coastal lagoons are particularly sensitive to eutrophication, since these systems tend to concentrate anthropogenic nutrient inputs (Knopper, 1994, Cloern, 2001, Kennish and Paerl, 2010) due to restricted exchanges with the sea and long water residence time (Boesch, 2002, Kennish and Paerl, 2010, Glibert et al., 2011).
In 2000, The Water Framework Directive (WFD) was established in Europe requiring member states to monitor the ecological and chemical quality state of water bodies and implement ways to achieve good status by 2021 (Sherrard et al., 2006, Cartaxana et al., 2009). Efforts have been made in many parts of the world to combat eutrophication by reducing nutrient inputs from watersheds and initiate ecological restoration. Ecological restoration is well documented in lakes which have been subjected to water quality improvement programs since the 70s (Jeppesen et al., 2005, Jeppesen et al., 2007). Studies on lake restoration have shown that the response trajectories during re-oligotrophication are not simply the inverse of the previous eutrophication processes and are characterized by hysteresis. Accordingly, the recovery of ecosystem functions often lagged behind the reduction of external nutrient loadings, due to nutrient regeneration from sediments or the persistence of turbid alternative states because of dense blooms of phytoplankton or the presence of a pool of easily resuspendable organic matter (Scheffer et al., 1993, Scheffer and Carpenter, 2003, Sondergaard et al., 2003, Ibelings et al., 2007). Because of these phenomena, re-oligotrophication processes are difficult to understand and predict for degraded systems (Van Donk et al., 2008). Hence, ecological restoration generally takes much longer than water degradation due to eutrophication. At first, it results in modifications of the composition and structure of primary producers communities. Phytoplankton is generally the first autotrophic compartment responding to the change of nutrient availability and other anthropogenic pressures (Livingston, 2000, Paerl et al., 2003). In restored lakes, this response has resulted in considerable changes of phytoplankton biomass, community structure and functional diversity (Ruggiu et al., 1998, Anneville and Pelletier, 2000, Katsiapi et al., 2013).
A functional approach to phytoplankton ecology appears particularly useful to study the adaptive responses of phytoplankton communities to re-oligotrophication. This approach is based on defining the functional traits of species that impact on their performance and survival (Violle et al., 2007) and, thus provides a better understanding of how phytoplankton communities respond to environmental changes. The functional approach has been used to understand how environmental changes or gradients drive phytoplankton community structure (Litchman et al., 2010). Some morphological and physiological traits particularly reflect the phytoplankton adaptations to nutrient availability, such as cell size, maximum growth rate and trophic regime (Litchman and Klausmeier, 2008, Litchman et al., 2010). During re-oligotrophication, the reduction of nutrient inputs could thus favor small cells, which compete more effectively for nutrient uptake and show high growth rates (Chisholm, 1992, Kamenir and Morabito, 2009, Litchman et al., 2010), and mixotrophic species that present some advantages over strictly autotrophic cells (Anneville and Pelletier, 2000). These functional traits highlight phytoplankton adaptations to the reduction of nutrient availability and represent an interesting tool to evaluate the impact of changing eutrophication status.
Since the implementation of the WFD, coastal waters represent a major issue for management and ecological restoration which has been used to reestablish ecosystems services. So far, little is known about the responses of coastal ecosystems to ecological restoration (Vidal et al., 1999, Duarte et al., 2009, Nixon, 2009). The recent literature describes a diversity of responses to restoration (Boesch, 2002, Elliott et al., 2007, Ho et al., 2008, Duarte et al., 2009), including a decrease of primary production while phytoplankton biomass remained stable (Philippart et al., 2007), reappearance of macrophyte communities (De Jonge and de Jong, 2002), and decrease of biomass and frequency of bloom occurrence (Lie et al., 2011). As shallow lakes, coastal lagoons have been particularly subjected to cultural eutrophication process due to nutrient over-enrichment from watersheds and long residence time (Kennish and Paerl, 2010, Glibert et al., 2011). Ecological restoration of coastal lagoons has started recently and studies of this process are still scarce. Given the high variability and dynamics of these systems, we can expect variable and complex restoration trajectories. During the re-oligotrophication process in a Mediterranean coastal lagoon (Collos et al., 2009), phytoplankton community changes were similar to those observed in some freshwater lakes, i.e. characterized by the appearance of dinophytes species and small-sized cyanobacteria (Ruggiu et al., 1998, Kamenir and Morabito, 2009). The results suggest some similar responses of lakes and coastal lagoons to re-oligotrophication process.
In the South of France, to improve the ecological quality of eight eutrophied coastal lagoons close to Montpellier, a drastic and persistent reduction of anthropogenic nutrient inputs has been achieved since December 2005, leading to a dynamic of ecological restoration. In the framework of a monitoring network, these lagoons and sixteen other lagoons have been monitored from 2000 to 2013 to assess their eutrophication status. These 24 lagoons presented a large eutrophication gradient ranging from oligotrophy to hypertrophy (Souchu et al., 2010), the most eutrophied lagoons showed phytoplankton dominance with high biomasses (>100 μgChla L−1). The phytoplankton size structure was dominated by small eukaryotic algae (3–6 μm) with relatively high growth rates (Bec et al., 2008, Bec et al., 2011).
Prior to the reduction in nutrient loadings, the complex of eight lagoons represented a eutrophication gradient ranging from mesotrophic to hypertrophic, including the most hypertrophic lagoons of the region. This context offered us a unique opportunity to study how the initial eutrophication status of lagoons influences the re-oligotrophication trajectories and to assess the success of ecological restoration in these highly degraded systems. We focused on phytoplankton community shifts to investigate the impact of ecological restoration in coastal lagoons for this range of eutrophication levels. Using data from a 13-year monitoring program, we describe changes of phytoplankton biomass and structure (i.e., size class structure and community composition), by comparing two periods: before and after the nutrient reduction. In addition, after implementation of the nutrient reduction, HPLC pigment analyses were added to the monitoring program. This allowed us to study the dynamics of functional and taxonomic groups as well as phytoplankton diversity, based on pigment biomarkers, during re-oligotrophication trajectories.
Section snippets
Studied sites
The Palavasian lagoon complex is located on the French Mediterranean coast, near Montpellier city (urban population 250,000 inhabitants). Since the 17th century, infilling and human constructions have compartmentalized a large natural lagoon to give rise to the current complex of eight interlinked shallow lagoons covering 38.8 km2 (Fig. 1). A major human intervention was the building of a navigation canal through the natural lagoon oriented NE-SW, named the Rhône-to-Sète canal which divided the
Characterization of the lagoons for the entire monitoring period (2000–2013)
During summer, both the average temperature and their variations in the lagoons were very similar, i.e. around 25 °C with a range between 20 and 31 °C, respectively. A salinity gradient was observed from MW, the less saline lagoon station subject to recurrent freshwater inputs from the Lez River, to IS without freshwater tributaries and connected with the sea by an inlet (Table 2). The lagoons also presented a trophic gradient, from mesotrophy (IN, IS) to hypertrophy (MW) based on the Chl a and
Discussion
This study represented a unique opportunity to assess the impact of re-oligotrophication processes in shallow Mediterranean coastal lagoons in conjunction with their contrasting trophic states. The results show that phytoplankton responded quickly, and that the amplitude and qualitative changes depend on the prior eutrophication status of the lagoon.
Acknowledgements
Amandine Leruste was supported by a PhD fellowship from the French Ministry of Education, Higher Education and Scientific Research attributed by the Doctoral School SIBAGHE in Montpellier. This paper uses data from the Lagoon Monitoring Network (Réseau de Suivi Lagunaire) funded by Agence de l’Eau, Région Languedoc-Roussillon and Ifremer. We thank the staff of the Ifremer laboratories in Languedoc-Roussillon for data collection. We thank Annie Pastoureaud and André Vaquer for having initiated
References (98)
- et al.
Effects of nutrient enrichment in the nation's estuaries: a decade of change
Harmful Algae
(2008) - et al.
Restoration of ecosystem services and biodiversity: conflicts and opportunities
Trends Ecol. Evol.
(2011) - et al.
Effect of sewage nutrients on algal production, biomass and pigments in tropical tidal creeks
Mar. Pollut. Bull.
(2012) - et al.
Trophic state of Foz de Almargem coastal lagoon (Algarve, South Portugal) based on the water quality and the phytoplankton community
Estuar. Coast. Shelf Sci.
(2007) - et al.
Oligotrophication and emergence of picocyanobacteria and a toxic dinoflagellate in Thau lagoon, southern France
J. Sea Res.
(2009) - et al.
Eutrophication
- et al.
Phytoplankton taxonomy based on CHEMTAX and microscopy in the northwestern Black Sea
J. Mar. Syst.
(2012) - et al.
Estuarine, coastal and marine ecosystem restoration: confusing management and science – a revision of concepts
Estuar. Coast. Shelf Sci.
(2007) - et al.
Characterizing estuarine plume discharge into the coastal ocean using fatty acid biomarkers and pigment analysis
Mar. Environ. Res.
(2014) - et al.
Eutrophication and harmful algal blooms: a scientific consensus
Harmful Algae
(2008)
Seasonal and spatial dynamics of nutrients and phytoplankton biomass in Victoria harbour and its vicinity before and after sewage abatement
Mar. Pollut. Bull.
Changes in the nutrient ratios and phytoplankton community after declines in nutrient concentrations in a semi-enclosed bay in Hong Kong
Mar. Environ. Res.
Population growth and plastid type of Myrionecta rubra depend on the kinds of available cryptomonad prey
Harmful Algae
Spectrofluorometric assay of chlorophylls and phaeopigments using the least squares approximation technique
Deep Sea Res. Part Oceanogr. Res. Pap.
Changes to chronic nitrogen loading from sewage discharges modify standing stocks of coastal phytoplankton
Mar. Pollut. Bull.
Alternative equilibria in shallow lakes
Trends Ecol. Evol.
Catastrophic regime shifts in ecosystems: linking theory to observation
Trends Ecol. Evol.
Combining HPLC pigment markers and ecological similarity indices to assess phytoplankton community structure: an environmental tool for eutrophication?
Sci. Total Environ.
Strategies of marine dinoflagellate survival and some rules of assembly
J. Sea Res.
The significance of autotrophic and heterotrophic picoplankton in hypertrophic ecosystems
FEMS Microbiol. Ecol.
The impact of mixotrophy on planktonic marine ecosystems
Ecol. Model.
Temporal stability of otolith elemental fingerprints discriminates among lagoon nursery habitats
Estuar. Coast. Shelf Sci.
Re-oligotrophication by phosphorus reduction and effects on seston quality in lakes
Limnologica
Coastal eutrophication research in Europe: progress and imbalances
Mar. Pollut. Bull.
A comparison of eutrophication impacts in two harbours in Hong Kong with different hydrodynamics
J. Mar. Syst. GEOHAB Model.
The Seto inland sea––eutrophic or oligotrophic?
Mar. Pollut. Bull.
Nutrient and temperature control of the contribution of picoplankton to phytoplankton biomass and production
Limnol. Oceanogr.
Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences
Estuaries
A new method for non-parametric multivariate analysis of variance
Austral Ecol.
Recovery of lake Geneva from eutrophication: quantitative response of phytoplankton
Arch. Hydrobiol.
Growth rate peaks at intermediate cell size in marine photosynthetic picoeukaryotes
Limnol. Oceanogr.
Distribution of picophytoplankton and nanophytoplankton along an anthropogenic eutrophication gradient in French Mediterranean coastal lagoons
Aquat. Microb. Ecol.
The contribution of picophytoplankton in marine and freshwater systems of different trophic status and depth
Limnol. Oceanogr.
The Physiological Ecology and Natural Distribution Patterns of Cryptomonas Algae in Coastal Aquatic Ecosystems
Challenges and opportunities for science in reducing nutrient over-enrichment of coastal ecosystems
Estuaries
Influence of hydrology on phytoplankton species composition and life strategies in a subtropical coastal lagoon periodically connected with the Atlantic Ocean
Estuaries
The use of pigment “fingerprints” in the study of harmful algal blooms
Rev. Biol. Trop
Food web structure of two Mediterranean lagoons under varying degree of eutrophication
J. Sea Res.
Phytoplankton and ecological assessment of brackish and freshwater coastal lagoons in the Algarve, Portugal
Lakes Reserv. Res. Manag.
Eutrophication-driven shifts in primary producers in shallow coastal systems: implications for system functional change
Estuaries Coasts
Seasonal and spatial variation of phytoplankton assemblages, biomass and cell size from spring to summer across the north-eastern New Zealand continental shelf
J. Plankton Res.
Phytoplankton size
Our evolving conceptual model of the coastal eutrophication problem
Mar. Ecol. Prog. Ser.
Comparaison Climatologique Annuelle – Infoclimat
Ecological restoration in coastal areas in the Netherlands: concepts, dilemmas and some examples
Hydrobiologia
Ammonium, nitrate and phytoplankton interactions in a freshwater tidal estuarine zone: potential effects of cultural eutrophication
Aquat. Sci.
Comparative effects of urea, ammonium, and nitrate on phytoplankton abundance, community composition, and toxicity in hypereutrophic freshwaters
Limnol. Oceanogr.
Return to Neverland: shifting baselines affect eutrophication restoration targets
Estuaries Coasts
The relationship between phytoplankton diversity and community function in a coastal lagoon
Hydrobiologia
Cited by (48)
Hydrodynamic influences on water exchange capacity of a coastal lagoon after phasic restoration projects
2024, Estuarine, Coastal and Shelf ScienceEnvironmental effects on zooplankton dynamics of a shallow Mediterranean coastal lagoon (October 2020–March 2021)
2021, Regional Studies in Marine ScienceThe impact of academic information supply and familiarity on preferences for ecosystem services
2021, Ecological EconomicsStorage capacity for phosphorus during growth and maturation in a brown alga Sargassum macrocarpum
2021, Science of the Total Environment