Carbon 13 labelling studies and biomarkers analysis on Mediterranean plankton communities

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Oligotrophic areas under anthropogenic perturbation

Most of the experiments discussed in the previous section were performed in relatively eutrophic conditions or with nutrient addition during the experiment and were mainly carried out in relatively cold waters (Figure I-5). However, there is an important diversity of oceanic provinces (Longhurst et al., 1995), from the less productive areas (ultra-oligotrophic) to very productive areas (eutrophic). About 50 % of primary production on Earth takes place in the ocean although more than 60 % of its surface being associated with low productivity, termed oligotrophic areas. A decreased nutrient availability and expansion of low productive regions are projected in a high CO2 world, as enhanced thermal stratification is expected to lead to surface layer nutrient depletion (Polovina et al., 2008; Irwin and Oliver, 2009).
Although it is important to assess the capacity of oligotrophic provinces for carbon uptake, and further storage, and its evolution under climate change, their trophic state (i.e. auto- VS heterotrophy) is still under debate (Ducklow and Doney, 2013), as to whether these areas are autotrophic (Williams et al., 2013) or heterotrophic (Duarte et al., 2013). As reviewed in the previous section, the effects of OA and/or OW on metabolic processes are still poorly understood and the biological response to climate change seems to be conditioned by the ecosystem conditions, e.g. nutrient availability, community composition. Therefore, the different biological responses in different oceanic regions must be investigated in order to gain a better understanding on the response of the global ocean to future environmental conditions. However, oligotrophic areas have been chronically under sampled with respect to the effect of climate change.

Case study: The Mediterranean Sea

The Mediterranean Sea (MS) is considered as an oligotrophic area exhibiting a gradient from mesotrophic (western basin) to ultra-oligotrophic (eastern basin). It is semi-enclosed, warm, deep and presents higher salinity and total alkalinity levels than in the open ocean. Mediterranean waters can, therefore, absorb more CO2 than the open ocean waters. The western and eastern basins differ in their carbonate chemistry; the western basin exhibits a lower total alkalinity than the eastern basin and the opposite pattern is seen for CT (higher CT in the western than in the eastern basin). Based on satellite observations, it is estimated that the MS, as a whole, acts as a small sink of CO2 (0.24 Gt C yr-1), with the western basin acting as a sink (8.94 Gt C yr-1) and the eastern basin as a source (8.4 Gt C yr-1; D’Ortenzio et al., 2008).
It has been suggested that the MS shifted from a source of CO2 (0.62 Gt C yr-1) in 1960 to a sink (-1.98 Gt C yr-1) in 1990, but this was not accompanied by a significant decrease in pH using a surface layer box model couple with datasets available (Louanchi et al., 2009). However using data collected at the DYFAMED site, changes in surface water carbonate chemistry in the western basin were estimated and these suggest that pH has decreased by 0.15 pH units since the industrial revolution (Touratier and Goyet, 2011). It has been predicted that a decrease by another 0.3 to 0.4 pH units will occur for the end of the century in the Northwestern MS (Geri et al., 2014). From time series (1975-2004) located in the NW Mediterranean sea it has been estimated that temperature increased during this period with a rate of 0.026 to 0.033 °C yr-1 (Bensoussan et al. 2009). Using satellite observations it has been estimated that surface temperature in the MS has increased by 0.03 to 0.05 °C yr-1 in the western and eastern basins respectively corresponding to an increase of 0.66 and 1.1 °C over the time considered (1985-2006) and with noticeable seasonal variability (Nykjaer, 2009). This sea surface temperature increase rate was also found for the period 1982-2012 and CMIP5 projections predicted a further increase of 2.6 °C for 2100 for the worst case scenario (RCP 8.5; Shaltout and Omstedt, 2014), with significant seasonal and spatial variability.
Experiments on the effects of climate change on the Mediterranean plankton community are very scarce. On the western French coast, the mesocosm facilities of the Mediterranean platform for Marine Ecosystems Experimental Research (MEDIMEER) have set up a mesocosm facility in the Thau lagoon, that was used to carry out the first studies on the effect of environmental perturbation on plankton community. So far, the experiments mainly focused on the effects of increased nutrients, irradiance and temperature rather than ocean acidification effect. Vidussi et al. (2011) and Fouilland et al. (2013) showed that temperature had a greater effect than irradiance, increasing the abundance of ciliates and flagellates and decreasing the abundance of bacteria and copepods. The effects of the temperature increase on the community structure was accompanied by enhanced autotrophic processes that suggest a strengthening of the carbon pump under warmer conditions. These results cannot be extrapolated to the rest of the Mediterranean Sea because coastal lagoons have distinct environmental characteristics as well as different community compositions than open sea oligotrophic areas.
Currently, the best approximations on the effects of climate change on plankton community arise from time series of IN SITU and satellite observations, causing difficulty in identifying which environmental parameter causes the biological modification. In the Bay of Calvi (Corsica, France), a decrease in biomass from 1979 to 1998 was detected (Goffart et al., 2002) and was associated to changes in nutrient concentrations resulting from reduced winter mixing. A shift toward smaller species (picoplankton and nanoflagellates) and a decline of diatoms, associated with more regenerated production and increased primary production per unit of chlorophyll, have been suggested and linked to increased cyanobacteria abundance at DYFAMED site in the Ligurian Sea (Marty and Chiavérini, 2002). Shifts in species assemblages and phenology, and decreased richness of the dinoflagellate CERATIUM, have been linked to ocean warming based on time series and historical data (Tunin-Ley et al., 2009).
To date, and to the best of our knowledge, there has not been any reported experiments on the combined effects of ocean acidification and/or warming on the Mediterranean plankton community, despite the fact that the MS reacts rapidly to external perturbations.

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Objectives and experimental approaches followed in this thesis

This work investigates the effects of ocean acidification and warming on the plankton community of the Northwestern Mediterranean Sea focusing on several major questions:
 What is the effect of ocean acidification on the metabolic rates of a plankton community maintained in close-to-natural conditions?
 Which groups benefit or are negatively affected by ocean acidification?
 What is the effect of ocean acidification and warming on plankton community structure and functioning?
To assess these questions, different approaches have been used in terms of experimental set-up (bottle incubations vs. mesocosms) and metabolic rate measurement methods (O2 light-dark, 14C and 18O labelling). Moreover, a relatively novel approach based of 13C labelling coupled with biomarker analyses has been used in order to trace carbon flow between the different compartments of the community and to estimate specific-carbon fixation rates.
The chapters correspond to the different questions and approaches used (Figure I-6). Chapter II discusses the effects of ocean acidification on metabolic rates measured using different methods during two mesocosm experiments performed in the NW Mediterranean Sea. During the same experiments, a 13C labelling study was undertaken to investigate group-specific responses to ocean acidification, the results of which are reported in chapter III. In chapter IV, the effects of ocean acidification and warming on a post-bloom community were studied in smaller volumes. Chapter V synthesizes the results of all three studies and discusses them in a more general context.

Ocean acidification and plankton metabolism in LNLC areas

In the frame of the MedSeA project (7th framework European project;, two mesocosm experiments were performed in the Northwestern Mediterranean Sea. These experiments were coordinated by the “Laboratoire d’Océanographie de Villefranche” (LOV-UMR 7093) in June-July 2012 in the Bay of Calvi (STARESO station, Corsica, France) and in February-March 2013 in the Bay of Villefranche (LOV, France). The mesocosm facilities were developed at LOV in the frame of the DUNE project ( and were designed to avoid any contamination (e.g. metals) from the structures (Guieu et al., 2010).
The mesocosm set-up and general conditions will be fully described in Gazeau et al. (in prep, a). However, for clarity, we will briefly provide here some informations on the experimental set-up, study sites, as well as main results concerning hydrological conditions (temperature and salinity), carbonate chemistry and pigments. These data will introduce the results on plankton metabolism (Chapter II.2) and stable isotope analysis coupled with biomarkers (Chapter III.2).

Table of contents :

Chapter I-Introduction to the plankton community in the Anthropocene
1. The Anthropocene
2. Carbon pump
3. The evolution of plankton community in the Anthropocene
3.1 Effect of ocean warming
3.2 Effect of ocean acidification
3.2.1 Single cells cultures
3.2.2 Community studies
3.3 Combined effect of warming and acidification
4. Oligotrophic areas under anthropogenic perturbation
5. Objectives and experimental approaches followed in this thesis
Chapter II-Ocean acidification and plankton metabolism in LNLC
1. Context of mesocosm experiments
1.1 Mesocosms acidification and sampling
1.2 Main results of Corsica mesocosm experiment
1.3 Main results of Villefranche mesocosm experiment
2. No effect of ocean acidification on planktonic metabolism in the NW oligotrophic Mediterranean Sea: results from two mesocosm studies
2.1 Introduction
2.2 Material and Method
2.2.1 Study sites and experimental set-up
2.2.2 Irradiance
2.2.3 Oxygen light-dark method
2.2.4 GPP-18O method
2.2.5 14C primary production
2.2.6 Data analysis, statistics and data availability
2.3 Results
2.3.1 Summer conditions (Bay of Calvi)
2.3.2 Winter-spring conditions (Bay of Villefranche)
2.4 Discussion
Chapter III-Carbon 13 labelling studies and biomarkers analysis on Mediterranean plankton communities
1. Preambule
2. Carbon-13 labelling studies show no effect of ocean acidification on Mediterranean plankton communities
2.1 Introduction
2.2 Material and Method
2.2.1 Study sites, experimental set-up and sampling
2.2.2 Laboratory analysis
2.2.3 Data analysis
2.2.4 Model
2.2.5 Statistics
2.3 Results
2.3.1 Bay of Calvi
2.3.2 Bay of Villefranche
2.4 Discussion
Chapter IV-Combined effects of temperature and pCO2 increase on a plankton community
Effect of ocean warming and acidification on a plankton community in the NW
Mediterranean Sea
Supplement Material
Chapter V-Synthesis and general discussion


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