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

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Highlights

  • Freshwater inputs from the watershed strongly influenced the phytoplankton of Biguglia lagoon.

  • Nanoflagellates dominated phytoplankton communities in autumn and spring with high N:P ratios.

  • Phycocyanin-rich picocyanobacteria bloomed in the sampling in September with low N:P ratios.

  • Phytoplankton showed differential responses to nutrient enrichments and induced limitations.

  • Phytoplankton was generally co-limited by N and P, with exceptions depending on seasons.

Abstract

Short-term bioassays were conducted in Biguglia lagoon (Corsica) to study the physiological and behavioral responses of phytoplankton to N- and P-availability. Natural communities were collected in two stations representative of the two sub-basins, at three periods with contrasting environmental characteristics to address the impact of seasonal variability. These samples were separately enriched with a full N and P enrichment, and with enrichments minus N or minus P. Phytoplankton size structuration, diversity, and growth of the total phytoplankton, the micro-, nano- and ultraphytoplankton were evaluated using spectrofluorimetry, and optical microscopy. Results showed that the communities were fueled by NO3 in the wet periods (autumn and spring) and NH4+ in summer. The phytoplankton communities displayed highest cell size in autumn, with high abundances of nanoflagellates, and smallest cell size in summer with a large dominance of phycocyanin-rich picocyanobacteria. Blooms of dinoflagellates also occurred during the wet periods, coinciding with high N:P ratios. The full enrichment has not stimulated phytoplankton growth in autumn, suggesting the importance of other controlling factors such as light, a possible NH4+ inhibition or the use of mixotrophic abilities. In spring, communities have displayed single P-limitation in the northern basin and different N and P co-limitations in the southern basin. In summer, the full enrichment consistently stimulated the growth of all cell sizes. The communities showed high N and P co-limitations, which is consistent with growing observations in aquatic ecosystems, and reflects the different functional responses of phytoplankton communities to the nutrient availability.

Graphical abstract

Chlosrophyll a (Chl a) concentration, DIN:DIP ratio, main taxa/morphotypes, response to the full nutrient enrichment, and N- and/or P-limitation during the three bioassay periods in the two stations representatives of the Northern and the Southern basins of Biguglia lagoon.

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Introduction

Coastal lagoons are very productive ecosystems at the sea-land interface hosting a high degree of biodiversity and providing numerous ecosystem services for human wellbeing (Barbier et al., 2011). These services confer a high economical value for the coastal lagoons, e.g. as water and food supply (fishing, shellfish farming), tourism and recreation (Franco et al., 2010; Rochette et al., 2010). However, because of their location in densely populated littoral areas and the services they provide, coastal lagoons and their surroundings have been increasingly exploited for human uses. Overexploitation combined with the hydromorphology of these semi-enclosed systems and climate change have increased their vulnerability to anthropogenic impacts. Hence, coastal lagoons are among the most threatened ecosystems (Nixon, 2009). This threat is mainly associated with changes in their hydrology and with an increase of nutrients and pollutants inputs from sewage effluents and watershed run-off (Mouillot et al., 2000; Cloern, 2001). Due to shallowness and confinement, these inputs result in high concentration of nutrients and pollutants in coastal lagoons, thereby exacerbating their degradation (Donald et al., 2013).

An excessive or unbalanced input of nutrients disturbs the community of primary producers, leading to an increase of the eutrophication processes and to drastic changes in the biodiversity of the autotrophic compartment. Thus, it may promote fast-growing opportunistic algae in the first place and finally phytoplankton at the expense of benthic organisms such as macrophytes, and may result in an increase of the frequency of harmful algal blooms (Schramm, 1999; Livingston, 2000; Le Fur et al., 2018). These changes in the composition of the autotrophic communities impact all the trophic levels, altering the ecosystem functioning (Cloern, 2001). High nutrient inputs can also, through an accumulation of macroalgal or phytoplankton biomass, lead to the development of dystrophic crisis and hypoxia and anoxia events, having dramatic impacts on all the living organisms (Cloern, 2001). Therefore, the management of a eutrophicated coastal lagoon needs to target the reduction of nutrient loadings. In addition, knowledge is required about the availability of nutrients within lagoons and the autotrophic communities responses (Duarte et al., 2000; Glibert et al., 2015). This allows to assess the resilience of the aquatic communities, and to estimate the critical nutrient loading for the ecosystem (Pasqualini et al., 2017; Le Fur et al., 2018).

Phytoplankton represents the basis of food webs and biochemical cycles, and is generally the first autotrophic compartment responding to a change of nutrient availability (Leruste et al., 2016). Understanding how the ecosystem functioning influences the composition of phytoplankton communities and their growth mechanisms is indispensable (Livingston, 2000; Paerl et al., 2003). Hence, it is particularly important to understand and predict how N and P inputs affect the growth and community assembly of phytoplankton. These responses are indicators of water quality, and are consequently informative for water management (Duarte et al., 2000; Reed et al., 2016). Morphological and physiological traits such as cell size and maximal growth rates shape the phytoplankton functional responses to nutrient availability. Small-size fast-growing algae are competitive at low nutrient concentrations and low light, while larger cells can generally thrive under a pulsed nutrient supply and higher light intensities (Litchman et al., 2007; Bec et al., 2011; Andersen et al., 2015). The community composition also reflects which nutrients are available. Diatoms are particularly competitive for nitrate, while green algae and picocyanobacteria are more competitive for ammonium. The latter often originates from regenerated internal sources. Dinoflagellates can develop even under dissolved inorganic nutrient limitation, because of their relatively low growth rates and potential mixotrophic abilities (Litchman et al., 2007; Glibert et al., 2015).

The general aim of this study was to explore the responses of the phytoplankton communities of a disturbed Mediterranean coastal lagoon to the nutrient availability. Therefore, we choose Biguglia lagoon, which is the largest lagoon on the island of Corsica, as the study site. This Mediterranean lagoon has been increasingly impacted since 1980 by a strong increase of the human population density, industrial and agricultural uses in its catchment and its surrounding areas. This lagoon receives particularly high amounts of nitrate from runoffs, tributaries, and from groundwater flows from a coastal aquifer connected with the lagoon (Erostate et al., 2018). Biguglia lagoon also displays a high confinement and restricted exchanges with the Tyrrhenian Sea that have induced higher levels of nutrient concentration than in most other French Mediterranean lagoons these last decades (Souchu et al., 2010; Pasqualini et al., 2017). Hence, the lagoon has experienced strong changes in its ecological state, i.e. increasing eutrophication and pollutant levels linked with changes in the composition of its autotrophic community (Mouillot et al., 2000; Pasqualini et al., 2017). Moreover, a dystrophic crisis associated with a bloom of toxic cyanobacteria in 2007 has raised the awareness of the water quality in the lagoon among the responsible management authorities. Therefore, they have taken remediation measures to reduce the confinement in order to decrease the concentration of nutrients. This included the modification of the lagoon hydrology since 2009 to increase dilution processes (Cecchi et al., 2016; Garrido et al., 2016). However, so far, no efficient direct management measures have been implemented to reduce the external nutrient loadings that remain important and uncontrolled. Moreover, although the measures taken in 2009 may have helped the development of aquatic angiosperms (Pasqualini et al., 2017), these may have also promoted the occurrence of blooms of potentially toxic and or harmfull dinoflagellate species (Cecchi et al., 2016).

The specific objectives of this study were to describe in different seasons with contrasting environmental conditions including nutrient form and origin, (1) the structure of phytoplankton communities in Biguglia lagoon submitted to a strong anthropogenic impact in term of size classes and species diversity, and (2) their growth rate in response to various forms of nutrients inputs. These two observations illustrate phytoplankton functional responses to contrasting nutrient availability, and the latter specially reflects the vulnerability of the whole ecosystem to a short-term nutrient pulse. We experimentally incubated phytoplankton communities under in situ light and temperature conditions with enrichments containing N (NO3, NH4+) and P (PO43−), either in combination or separately to selectively induce either N- or P-limitation. Exploring the responses of phytoplankton communities to a change in nutrient availability helped understanding the impact of these changes on the ecosystem functioning.

Section snippets

Characterization of the study site

Biguglia lagoon (42°36′N; 9°28′E) is a shallow brackish coastal lagoon (average depth 1.2 m), located on the East coast of Corsica, and separated from the Tyrrhenian Sea by a sandy beach barrier (Fig. 1). This choked lagoon sensu Kjerfve (1994) covers 14.5 km2 with a single inlet in the north to the sea that consists of a 1.5 km long, narrow and shallow natural channel. Biguglia lagoon is divided into two sub-basins by a peninsula in its middle. Each of these sub-basins displays a specific

Environmental variables and phytoplankton biomass

Salinities were low during the three dilution experiments, ranging from 2.0 in NB in April, to 10.9 in September 2014 (Table 1). The percentage of DO was the lowest in September 2014 for both stations, and was negatively correlated with the temperature for the three sampling periods (Table 2, Spearman's rank correlations, p-value <0.05). Turbidity was highest in the autumn sampling (Table 1).

Concentrations of dissolved inorganic nutrients (NH4+, NO3, NO2, DIN, PO43−) and of TN and TP were

Discussion

In this study, we aimed to describe functional traits of phytoplankton communities in Biguglia lagoon submitted to a strong anthropogenic impact in different seasons with contrasting environmental conditions, and the response of these communities to various forms of nutrients inputs simulating nutrient pulses to predict their impact on ecosystem functioning.

Conclusion

Experimental enrichments bioassays are particularly appropriate to explore cause-effect relationships between nutrient availability and phytoplankton dynamics, which can reflect the vulnerability of the whole ecosystem. This is an important issue for managers to draw up appropriate nutrient loading budgets, and to help evaluating the efficiency of subsequent nutrient reduction strategies. In our study, N inputs, particularly NO3 during the wet periods and NH4+ in summer, stimulated

Acknowledgements

Amandine Leruste was supported in 2018 by a Postdoctoral fellowship of the University of Corsica Pasquale Paoli (SPE CNRS 6134 Laboratory and UMS Stella Mare) and the Collectivity of Corsica, and from 2013 to 2016 by a PhD fellowship of the Doctoral School at the University of Montpellier. This work has been financed by Biguglia lagoon nature reserve, the Collectivity of Corsica and the University of Corsica Pasquale Paoli, that authors are grateful for their cooperation. We thank the Ifremer

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