Coupling high frequency monitoring and bioassay experiments to investigate a harmful algal bloom in the Bay of Seine (French-English Channel)

https://doi.org/10.1016/j.marpolbul.2021.112387Get rights and content

Highlights

  • Lepidodinium chlorophorum harmfull algal bloom fully monitored at high frequency

  • Triggering and fate of the bloom explore with nutrients and photosynthetic HF data

  • P limitation cause the bloom decline as flagged by the Fv/Fm and N/P ratio.

  • Enrichment experiment reveal potential N and P co limitation.

  • High TEP production under N or P limitation in enrichment experiment

Abstract

Coastal ecosystems are increasingly threatened by eutrophication and dystrophy. In this context, the full pattern of a bloom dominated by the dinoflagellate, Lepidodinium chlorophorum, was investigated by a high frequency monitoring buoy equipped with sensors allowing nutrients and photosynthesis measurements. An increase of the N/P ratio affected phytoplankton physiology leading to bloom collapse with a slight oxygen depletion. In parallel, enrichment experiments were performed on the natural bloom population. After 5 days of incubation the community structure, using flow cytometry and several physiological parameters were analysed. The data reveal a potential N and P co-limitation and a decoupling between primary production and productivity in fully enriched conditions. Under unbalanced N/P inputs, high level of alkaline phosphatase activity and transparent exopolymeric particle production, which favour phytoplankton sedimentation, were observed. Nutrient inputs and their stoichiometry control phytoplankton growth, the community structure, physiological regulations, the fate of the bloom and consequences.

Introduction

As the ocean's first frontier, coastal ecosystems are increasingly under threats that affect many essential benthic and pelagic habitats of marine species (Barbier et al., 2011). Eutrophication, which is due to excess nutrient inputs in coastal systems caused by human activities is one of the major environmental problems affecting coastal ecosystem in the world (Rabalais et al., 2009). These inputs affect both the concentration of nutrients and their stoichiometry (Martin et al., 2008; Watanabe et al., 2017). The growth and diversity of primary producers, like phytoplankton, which are at the base of the marine food web, are largely controlled by these inputs (Smith, 2006). Unbalanced nutrient inputs and dystrophy, both frequently linked with eutrophication, have several effects on phytoplankton: modification of communities (Leruste et al., 2019; Shen, 2001), alter the growth rate (Nwankwegu et al., 2020), produce allochemical-like toxins which, in turn, favour monospecific blooms (Granéli et al., 2008). Associated with other environmental parameters including light, temperature, water mass resistance time, or river discharges, nutrient inputs can lead to phytoplankton blooms (Heisler et al., 2008) that may be classified as harmful algal blooms (HAB) (Anderson, 2009). HAB species are usually split into two groups, one of which is able to produce toxins or harmful metabolites that damage wildlife, or result in poisoning of human seafood, and the second in which high densities of non-toxic cells can harm the environment by producing scums or foams which lead to oxygen depletion (Anderson et al., 2002).

Nutrient inputs into the Bay of Seine (France) are mainly controlled by inputs from the Seine River (Aminot et al., 1998) although smaller rivers inputs also have local impacts (Lemesle et al., 2015). Over the last decades, many programmes for the management of nutrient inputs have reduced nutrient discharges but have mainly had an impact on phosphorus inputs, whereas N inputs remain high (Garnier et al., 2019). The stoichiometry of nutrient inputs have been broadly modified over the last decade and very high N/P ratio inputs are regularly measured in the Seine River and Seine estuary (Meybeck et al., 2018).

Although chlorophyll biomass has decreased in recent years in the English Channel (Gohin et al., 2019), the relative proportion of the dinoflagellate group has increased (Hernández-Fariñas et al., 2014; Widdicombe et al., 2010). In the Bay of Seine, several species of dinoflagellate like Karenia mikimotoi and Lepidodinium chlorophorum are able to form large harmful algal bloom (HAB) (Napoléon et al., 2014). Lepidodinium chlorophorum is known to produce large quantities of transparent exopolymeric particles (TEP) (Claquin et al., 2008) and to be responsible for the mortality of marine organisms due to oxygen depletion induced by decomposition of the population (Sournia et al., 1992).

Many studies have shown that phytoplankton communities can respond within a few hours after an environmental change (Lefort and Gasol, 2014; Thyssen et al., 2008) which stresses out the necessity of implementing a high frequency sampling (Bouman et al., 2005). In the present work, a late summer L. chlorophorum bloom event was studied in detail using high frequency measurements made by an instrumented buoy called SMILE (0° 19.68′, 49° 21.23′). In addition to standard sensors (temperature, salinity, turbidity, oxygen, light and fluorescence), the SMILE buoy is equipped with a fast repetition rate fluorimeter (FRRf), which enables photobiological and physiological measurements of the phytoplankton communities, and two types of nutrient sensors, which together provide new and more realistic pictures of bloom dynamics.

In addition to monitoring the bloom event, enrichment bioassay experiments were performed on samples collected during the bloom in order to understand how nutrient inputs influence the structure and physiological parameters of the communities. The specific objectives of our studies were to:

  • 1)

    Characterise bloom dynamics from an original point of view by including physiological, productivity, and nutrients measurements at a high frequency.

  • 2)

    investigate phytoplankton dynamics and the ecophysiology of a community dominated by L. chlorophorum as a function of nutrient inputs.

Section snippets

High frequency measurements using an instrumented buoy

The bloom event was monitored in situ using the SMILE buoy in the Bay of Seine (Fig. 1) measuring since 2016 which belong the COAST-HF network (French Coastal ocean observing system - High frequency). Different types of measurements were performed at different frequencies by the buoy.

Bloom time series

High frequency measurements provided by the SMILE buoy are presented in Fig. 3. An increase in FFU and oxygen saturation on the 24th of August indicated the beginning of the bloom and remained high until the end of the bloom event on the 30th of August 2019 (Fig. 3 A, B). The highest dissolved O2 concentration and FFU were measured on the 27th of August with respectively 16.5 mg O2 .l−1 and 165 FFU. This highest value of FFU was also reached the 28th, 29th and 30th August because of a

Discussion

The high frequency data provided by the instrumented buoy SMILE alerted us to the occurrence of a HAB bloom dominated by the Dinophyceae Lepidodinium chlorophorum in late August 2019, in the Bay of Seine. L. chlorophorum contained green chloroplasts probably derived from a prasinophyte endosymbiont (Hansen et al., 2007). Dinophyceae species with green chloroplasts are rare (Hansen et al., 2007) and to our knowledge L. chlorophorum is the only “green Dinophyceae” that has been identified in the

Conclusions

In this study, the entire temporal pattern of a HAB species, L. chlorophorum, identified by microscopy and flow cytometry, was monitored. We showed that the high-frequency measurements of physical-chemical and biological parameters provided by the SMILE buoy allowed to detect the triggers of the bloom and its fate. There were not flow cytometer on the buoy, but our study pointed out that such a measurement associated with the others parameter available at high frequency would represent a great

CRediT authorship contribution statement

Léon Serre-Fredj: Methodology, Resources, Formal analysis, Writing – original draft, Visualization. Franck Jacqueline: Methodology. Maxime Navon: Methodology, Investigation, Resources. Guillaume Izabel: Data curation. Léo Chasselin: Resources, Investigation. Orianne Jolly: Resources, Investigation. Michel Repecaud: Methodology. Pascal Claquin: Conceptualization, Project administration, Funding acquisition, Writing – original draft, Resources, Investigation.

Declaration of competing interest

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

We thank Bertrand Le Roy from BOREA for L. chlorophorum isolation, Tania Hernández-Fariñas from Ifremer for her comments and advices and the COAST-HF network for technical support. This work was funded by the SMILE2 and RIN ECUME projects respectively supported by l'Agence de l'Eau Seine Normandie France, the European Regional Development Fund of Normandie, France, and La Région Normandie, France and by the PLEASE PhD project supported by l'Agence de l'Eau Seine Normandie, France and La Région

References (101)

  • S. Karasiewicz et al.

    Harmful algae niche responses to environmental and community variation along the French coast

    Harmful Algae

    (2020)
  • S.-Y. Kim et al.

    Decadal-scale variations of sedimentary dinoflagellate cyst records from the Yellow Sea over the last 400 years

    Estuar. Coast. Shelf Sci.

    (2018)
  • Z.S. Kolber et al.

    Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols

    Biochim. Biophys. Acta BBA - Bioenerg.

    (1998)
  • S. Lefebvre et al.

    Spatial and temporal dynamics of size-structured photosynthetic parameters (PAM) and primary production (13C) of pico- and nano-phytoplankton in an atoll lagoon

    Mar. Pollut. Bull.

    (2012)
  • S. Lemesle et al.

    Impact of seaweed beachings on dynamics of δ15N isotopic signatures in marine macroalgae

    Mar. Pollut. Bull.

    (2015)
  • A. Leruste et al.

    Physiological and behavioral responses of phytoplankton communities to nutrient availability in a disturbed Mediterranean coastal lagoon

    Estuar. Coast. Shelf Sci.

    (2019)
  • S. Li et al.

    Compositional similarities and differences between transparent exopolymer particles (TEPs) from two marine bacteria and two marine algae: significance to surface biofouling

    Mar. Chem.

    (2015)
  • S. Li et al.

    Marine bacterial transparent exopolymer particles (TEP) and TEP precursors: characterization and RO fouling potential

    Desalination

    (2016)
  • Y. Liang et al.

    Nutrient-limitation induced diatom-dinoflagellate shift of spring phytoplankton community in an offshore shellfish farming area

    Mar. Pollut. Bull.

    (2019)
  • A.A.Y. Lie et al.

    Changes in the nutrient ratios and phytoplankton community after declines in nutrient concentrations in a semi-enclosed bay in Hong Kong

    Mar. Environ. Res.

    (2011)
  • J. Ly et al.

    Phosphorus limitation during a phytoplankton spring bloom in the western Dutch Wadden Sea

    J. Sea Res.

    (2014)
  • X. Mari et al.

    Dynamics of transparent exopolymeric particles (TEP) production by Phaeocystis globosa under N- or P-limitation: a controlling factor of the retention/export balance

  • C. Napoléon et al.

    Spatiotemporal dynamics of physicochemical and photosynthetic parameters in the central English Channel

    J. Sea Res.

    (2012)
  • A.S. Nwankwegu et al.

    Nutrient addition bioassay and phytoplankton community structure monitored during autumn in Xiangxi Bay of Three Gorges Reservoir, China

    Chemosphere

    (2020)
  • U. Passow

    Transparent exopolymer particles (TEP) in aquatic environments

    Prog. Oceanogr.

    (2002)
  • Z.-L. Shen

    Historical changes in nutrient structure and its influences on phytoplantkon composition in Jiaozhou Bay

    Estuar. Coast. Shelf Sci.

    (2001)
  • L. Tan et al.

    The feasibility of Fv/Fm on judging nutrient limitation of marine algae through indoor simulation and in situ experiment

    Estuar. Coast. Shelf Sci.

    (2019)
  • P. Tett et al.

    N:Si ratios and the ‘balance of organisms’: PROWQM simulations of the northern North Sea

    J. Sea Res.

    (2005)
  • M. Thorel et al.

    Nutrient ratios influence variability in Pseudo-nitzschia species diversity and particulate domoic acid production in the bay of seine (France)

    Harmful Algae

    (2017)
  • Z. Wang et al.

    Utilization of dissolved organic phosphorus by different groups of phytoplankton taxa

    Harmful Algae

    (2011)
  • K. Watanabe et al.

    Estuarine circulation-driven entrainment of oceanic nutrients fuels coastal phytoplankton in an open coastal system in Japan

    Estuar. Coast. Shelf Sci.

    (2017)
  • Z. Wu et al.

    Physiological regulation of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) in response to inorganic phosphorus limitation

    Harmful Algae

    (2012)
  • Y. Zhou et al.

    Nutrients structure changes impact the competition and succession between diatom and dinoflagellate in the East China Sea

    Sci. Total Environ.

    (2017)
  • N.S.R. Agawin et al.

    Nutrient and temperature control of the contribution of picoplankton to phytoplankton biomass and production

    Limnol. Oceanogr.

    (2000)
  • A. Aminot et al.

    Dosage automatique des nutriments dans les eaux marines: méthodes en flux continu

    (2007)
  • D.M. Anderson et al.

    Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences

    Estuaries

    (2002)
  • F. Azzaro

    Automated nutrients analysis for buoys in sea-water and intercalibration

    Int. J. Environ. Monit. Anal.

    (2014)
  • E.B. Barbier et al.

    The value of estuarine and coastal ecosystem services

    Ecol. Monogr.

    (2011)
  • S. Beauvais et al.

    Transparent exopolymer particle (TEP) dynamics in relation to trophic and hydrological conditions in the NW Mediterranean Sea

    Mar. Ecol. Prog. Ser.

    (2003)
  • M.J. Behrenfeld et al.

    In search of a physiological basis for covariations in light-limited and light-saturated Photosynthesis1

    J. Phycol.

    (2004)
  • T.G. Boatman et al.

    Improving the accuracy of single turnover active Fluorometry (STAF) for the estimation of phytoplankton primary productivity (PhytoPP)

    Front. Mar. Sci.

    (2019)
  • P. Claquin et al.

    Effects of temperature on photosynthetic parameters and TEP production in eight species of marine microalgae

    Aquat. Microb. Ecol.

    (2008)
  • A. Corzo et al.

    Production of transparent exopolymer particles (TEP) in cultures of Chaetoceros calcitrans under nitrogen limitation

    Aquat. Microb. Ecol.

    (2000)
  • E.A. Davidson et al.

    Nutrients in synergy

    Nature

    (2007)
  • W. Deng et al.

    Effects of nutrient limitation on cell growth, TEP production and aggregate formation of marine Synechococcus

    Aquat. Microb. Ecol.

    (2016)
  • M. Elbrächter et al.

    Gymnodinium chlorophorum, a new, green, bloom-forming dinoflagellate (Gymnodiniales, Dinophyceae) with a vestigial prasinophyte endosymbiont

    Phycologia

    (1996)
  • P.G. Falkowski et al.

    Acclimation to spectral irradiance in algae

    J. Phycol.

    (1991)
  • P.G. Falkowski et al.

    Review of Aquatic Photosynthesis

    New Phytol.

    (1998)
  • Z.V. Finkel et al.

    Resource limitation alters the 3/4 size scaling of metabolic rates in phytoplankton

    Mar. Ecol. Prog. Ser.

    (2004)
  • A.D. Fischer et al.

    Return of the “age of dinoflagellates” in Monterey Bay: drivers of dinoflagellate dominance examined using automated imaging flow cytometry and long-term time series analysis

    Limnol. Oceanogr.

    (2020)
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