Phytoplankton community dynamics during late spring coccolithophore blooms at the continental margin of the Celtic Sea (North East Atlantic, 2006–2008)
Highlights
► Coccolithophores and diatoms were dominant phytoplankton groups during late spring. ► Nutrient stoichiometry changes drove alternation between diatoms and coccolithophores. ► High concentrations of TEP associated with stratified, coccolithophore-rich water masses.
Introduction
Continental shelves and margins are areas of high primary productivity and carbon export and, as such, play a key role in global biogeochemical cycles and ecosystems (Joint et al., 2001, Sharples et al., 2009). Spring phytoplankton blooms are a prominent seasonal feature of the North East Atlantic Ocean (NE Atlantic) (Henson et al., 2006) and are characterised by an intense diatom bloom followed by nanoplankton (among others: prymnesiophytes, prasinophytes and cyanobacteria) when first dissolved silicate and then other nutrients become depleted, and increasing water column stratification hinders nutrient replenishment to the euphotic zone (Joint et al., 1986, Lochte et al., 1993, Rees et al., 1999, Raitsos et al., 2006, Leblanc et al., 2009). Especially, coccolithophores are a prominent feature of the late spring bloom, and this has been attributed to their tolerance for high irradiances, lower nutrient requirements and/or ability to utilise organic nitrogen or phosphorus sources (Palenik and Henson, 1997, Leblanc et al., 2009 and references therein). Bloom termination follows when nutrient depletion depresses primary productivity and grazing and viral control catch up with algal growth (Brussaard, 2004, Calbet and Landry, 2004, Behrenfeld, 2010). In reality, this general NE Atlantic spring bloom scenario can be more or less scrambled due to local weather conditions and physical phenomena (Ji et al., 2010), both in the open ocean, where movements of eddies and other water masses can reset succession events (Smythe-Wright et al., 2010), and along continental margins, where vertical mixing resulting from internal tides can bring nutrient-rich deeper water into the euphotic zone (Sharples et al., 2007). Along the continental margin of the Bay of Biscay and the Celtic Sea, phytoplankton growth, and coccolithophorid blooms in particular, have been shown to be triggered and/or sustained by internal tidal wave formation at the shelf break leading to enhanced vertical mixing and the injection of inorganic nutrients to the surface waters (Holligan and Groom, 1986, Lampert et al., 2002, Sharples et al., 2009, Harlay et al., 2010).
A general scenario of late spring bloom evolution at the continental margin of the northern Bay of Biscay is proposed by Harlay et al. (2010): when the main diatom spring bloom (mid April) has depleted dissolved silicate (dSi) to levels below 2 μmol l−1, vertical inputs of nutrients along the shelf break trigger mixed blooms mainly dominated by coccolithophores. We consider blooms of coccolithophores to be a sequence of events when their biomass constitutes a significant portion of the total phytoplankton community, enabling them to influence local biogeochemistry and trophodynamics (Smayda, 1997). These blooms further exhaust nutrients as the water column stratifies and the water mass is advected over the continental shelf, following the general residual circulation in the area (Pingree and Lecann, 1989, Huthnance et al., 2001, Suykens et al., 2010), while dinoflagellates, chrysophytes, prasinophytes and cryptophytes can become increasingly more important. This succession leads to the appearance of high reflectance (HR) patches which are associated with the dissipative stage of coccolithophorid blooms (of Emiliania huxleyi in particular), when coccoliths are shed into the water column, affecting the albedo of the surface water (Westbroek et al., 1993, Harlay et al., 2010). This bloom succession considerably alters the biogeochemical characteristics of their environment through biogenic calcification and the release of transparent exopolymer particles (TEP), which affect carbon export through mineral ballasting and aggregation (Armstrong et al., 2002, Engel et al., 2004, De La Rocha and Passow, 2007), and dimethyl sulphide production, which introduces sulphur into the atmosphere (Burkill et al., 2002, Stefels et al., 2007, Seymour et al., 2010).
While the annual occurrence of extensive coccolithophore blooms in late spring in the NE Atlantic is well-documented (Leblanc et al., 2009 and references therein), there is no consensus on the factors triggering coccolithophorid blooms and modulating the turnover time of the calcite they produce (Lessard et al., 2005, Poulton et al., 2007, Poulton et al., 2010, Boyd et al., 2010). Changes in environmental control factors such as light intensity, water column stability, temperature, CO2 concentration, nitrate and phosphate levels and their ratio, and the concentration trace metals (e.g. Fe, Zn, and Mn) have been shown to influence coccolithophore physiology and control phytoplankton community assemblage to various extents (Nanninga and Tyrrell, 1996, Zondervan, 2007, Boyd et al., 2010, and references therein). However, only few studies have described the structure and the spatial and temporal dynamics of phytoplankton communities during these blooms along the western European continental margin (Head et al., 1998, Joint et al., 2001, Fileman et al., 2002, Lampert et al., 2002). This information is needed, as the importance of the phytoplankton community structure to the biological pump is still poorly understood (Smythe-Wright et al., 2010, and references therein). Changes in the community composition are expected to impact primary and export production, and as such food web structure and dynamics, as well the biogeochemical cycling of carbon and other bio-limiting elements in the sea (Guidi et al., 2009, Finkel et al., 2010).
We investigated the dynamics of the main phytoplankton groups during three campaigns (2006–2008) in late spring (May–June, i.e. after the main diatom bloom in April), along and across the continental margin of the Celtic Sea. More specifically, we investigated if (1) water column properties such as stratification, nutrient levels and the ratios differed between the shelf and the slope side of the continental margin, (2) how changes in such physical and biogeochemical variables influence the phytoplankton community structure and biomass, and (3) how phytoplankton biomass and community structure are related to the standing stocks of particulate organic carbon (POC), TEP, and particulate inorganic carbon (PIC; calcite). We assessed the phytoplankton community structure using a chemotaxonomic (pigment-based) approach and its dynamics and relation to biogeochemical variables analysed using multivariate non-parametric analyses.
Section snippets
Study area and general set-up of the campaigns
The study area along the continental margin of the northern Bay of Biscay, on the shelf of the Celtic Sea included the La Chapelle Bank (LC), the Meriadzek Terrace (M), the Goban Spur (GS) area, and one station on the Armorican shelf (Fig. 1 and Table 1). Three campaigns were carried out from the 31st of May to the 9th of June 2006, from the 10th to the 24th of May 2007, and from the 7th to the 23rd of May 2008, onboard RV Belgica. Eighteen stations were located in the vicinity of the La
General setting, thermal stratification and nutrient levels
The stations were located along the shelf break and on the shelf of the Celtic Sea in the La Chapelle Bank (LC), the Meriadzek Terrace (M) and the Goban Spur (GS) areas (Fig. 1, Fig. 2, Table 1). Each campaign (2006, 2007, and 2008) took place after the main diatom spring bloom which took place in April (Fig. 3).
Sea surface temperature (SST) was on average higher in June 2006 (13.84 ± 0.76 °C) than in May 2007 (13.25 ± 0.16 °C) and May 2008 (13.04 ± 0.66 °C) (Table SP4 and pairwise tests: p2007 = 0.042
Discussion
We studied the dynamics of phytoplankton standing stocks and community structure during late spring coccolithophore blooms along the continental margin of the Celtic Sea over a period of 3 years (2006–2008). We related the spatial and temporal development of these blooms to a suite of physical, geochemical, and biological variables in order to identify the main environmental conditions driving the wax and wane of these blooms, and to discuss the potential importance of phytoplankton community
Conclusions
The recurrent scenario emerging from previous studies is that diatoms dominate the main spring bloom event, sometimes co-occurring with prymnesiophytes or dinoflagellates, and tend to be outcompeted by prymnesiophytes during later stages of the spring bloom in the North East Atlantic (Leblanc et al., 2009). Yet we showed that, during later blooms, diatom and coccolithophore can co-occur and their growth can alternate in the same area and during the same period. Alternation between diatom and
Acknowledgments
The authors sincerely thank the officers and crew members of the R.V. Belgica for their logistic support during the campaigns. J. Backers, J.-P. De Blauw, and G. Deschepper of the Unit of the North Sea Mathematical Models (Brussels/Ostend, Belgium) are acknowledged for their support in data acquisition during the field campaigns. We are grateful to C. Souffreau, A. De Wever, and D. De Bock for their assistance during sample collection and to F. Steen and N. Breine for performing the optical
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2019, Progress in OceanographyCitation Excerpt :The occurrence or lack of a time lag between PP and CRO2 may be related to the plankton community structure and the capacity of the plankton to react rapidly to an increase in resources. In our study, nanophytoplankton (2–20 µm) dominated the bloom, both in terms of cell abundance (Tarran et al., this issue), Chl-a and primary production (Hickman et al., this issue), rather than the larger diatom and dinoflagellate taxa often considered to be typical of spring blooms in this area (Rees et al., 1999; Widdicombe et al., 2010; Van Oostende et al., 2012). Plankton communities dominated by small and fast growing cells are characterised by greater interactions between species and faster organic matter and energy cycling (Legendre and Le Fèvre, 1995; D’alelio et al., 2016) which could also contribute to the lack of a time lag between the increase in production and respiration.
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Present address: Chemical Oceanography Unit, Department of Astrophysics Geophysics and Oceanography AGO, University of Liège, Institut de Physique (B5), B-4000 Sart Tilman, Belgium.