Response of a natural Antarctic phytoplankton assemblage to changes in temperature and salinity

https://doi.org/10.1016/j.jembe.2020.151444Get rights and content

Highlights

  • Experimental response of phytoplankton to increased temperature and reduced salinity

  • Phytoplankton assemblage characterization by HPLC, light and electron microscopy

  • Dominance of nano-diatoms and phytoflagellates on high temperature and low salinity

  • Sub-polar species previously undetected in Antarctica favoured by climate change

  • The first report of Shionodiscus gaarderae (sub-Antarctic species) in Antarctica

Abstract

The climate around the Western Antarctic Peninsula (WAP) is rapidly changing and dramatically affecting marine coastal waters. Increases in air and seawater temperatures, not matter how small, can alter coastal biological communities due to both temperature increases as well as salinity reduction from glacier melting. The aim of this study was to evaluate the individual and combined effects of elevated sea surface temperature (+4 °C) and decreased salinity (−4) on growth and assemblage composition of natural summer phytoplankton from Potter Cove (King George Island, South Shetlands, northern WAP), using an outdoor microcosm experiment. Pigment composition was analyzed by high performance liquid chromatography (HPLC/Chemtax) and species composition by light and electron microscopy. Increases in phytoplankton biomass during the first 3 days at elevated-temperatures coincided with an increase in the abundance and the specific growth rate of small centric diatoms (Chaetoceros socialis and Shionodiscus gaarderae, mostly observed in temperate waters) and unidentified small phytoflagellates <5 μm. In contrast, pennate diatoms significantly decreased. At the end of the experiment on day 7, under nitrate and phosphate limitation, chlorophytes abundances increased under low salinity whereas prasinophytes decreased in all treatments. This study suggests that climate change could notably affect Antarctic phytoplankton composition by favouring temperate-water species previously undetected in Antarctic waters, such us S. gaarderae. Moreover, the observed changes in phytoplankton structure, associated with an increase of nano- over micro-size taxa, could have important implications for future Antarctic food webs.

Introduction

Over the last five decades, the West Antarctic Peninsula (WAP) has experienced strong atmospheric warming, with the highest heating rates recorded worldwide (Vaughan et al., 2003; Turner et al., 2005, Turner et al., 2014; Gutt et al., 2015). The consequent increases in air and surface seawater temperatures are responsible for the melting of glaciers that drain large amounts of freshwater and terrestrial particulate materials to coastal waters. The resulting lowering of surface seawater salinity strengthens the stratification of the water column while increased turbidity decreases light availability in surface waters (Schloss et al., 2012; Meredith et al., 2018). Since the mid-1950's, the glacial area of King George Island (KGI) in the South Shetland Archipelago (WAP) has lost 89 km2, a 7% reduction of the total area (Simões et al., 1999). This makes KGI an ideal region for the study of climate change and its impact on marine ecosystem (Meredith et al., 2017). Planktonic organisms living in extreme environments, such as Antarctica, tend to be more sensitive to changes in environmental stressors than their temperate counterparts (Clarke et al., 2007). Because marine phytoplankton contribute ~50% to total global primary production and CO2 fixation (Falkowski et al., 1998), they provide critical energy to the different components of the marine food web and ultimately to the top consumers (Waite et al., 1997). Therefore, it is critical to understand the responses of phytoplankton to temperature and salinity stress since variations in these abiotic factors can have profound consequences for marine food webs (Gleitz et al., 1995; Trathan et al., 2007; Lewandowska et al., 2014a) and biogeochemical cycles in the Southern Ocean (Nelson et al., 1991; Smetacek et al., 2004; Tagliabue et al., 2009).

Variations in seawater salinity and temperature have been shown to cause changes in Antarctic phytoplankton physiology under experimental conditions (Ralph et al., 2005; Hernando et al., 2015, Hernando et al., 2018) as well as in the taxonomic structure of natural phytoplankton assemblages (Moline et al., 2001; Montes Hugo et al., 2009; Schofield et al., 2017). Previous studies demonstrated that reduced salinity, associated with meltwater input, was responsible for the increase in the relative abundance of cryptophytes (Moline et al., 2001; Garibotti et al., 2003; Mendes et al., 2013). However, little is known about the expected changes on Antarctic phytoplankton biomass and composition to the combined effect of these two stressors.

Located in KGI, Potter Cove (PC) (Fig. 1) was historically considered a low chlorophyll-a (Chl-a) area compared to other regions of the WAP, with a mean value below 1 mg Chl-a m−3 during 25-years (Kim et al., 2018). Previous to this study, Chemtax analyses of PC plankton samples showed a dominance of diatoms during the growing season, with a relatively low contributions of other taxonomic groups such as haptophytes and chlorophytes (van de Poll et al., 2011). More recently, anomalously large phytoplankton blooms were observed in the summer of 2010 (up to 20 mg Chl-a m−3) and it was associated with the common large diatom species from PC, such as Porosira glacialis and Thalassiosira antarctica (Schloss et al., 2014).

After this unusual bloom, two microcosm experiments were carried out at PC in order to study the effect of decreased salinity (Hernando et al., 2015) and the combined effects of decreased salinity and increased temperature (Hernando et al., 2018) on phytoplankton stress responses, changes in assemblage composition and fatty acid profiles. These studies conducted in the summers of 2011 and 2014, respectively, exposed assemblages dominated by large diatoms (Hernando et al., 2015, Hernando et al., 2018) to changes in these stressors. In contrast, the PC phytoplankton assemblage from the summer of 2016 used in this study was characterized by the dominance of nano-size diatoms. This is the first report of the responses of a coastal Antarctic phytoplankton assemblage dominated by small diatoms to increased temperature and decreased salinity in PC using microcosm experiments. Moreover, dominant species found at the beginning of the present experiment are mostly known to occur in subpolar waters and therefore it is relevant to analyse their potential response to increased temperature and reduced salinity conditions induced by climate change in coastal waters of the WAP. We expect their response to forecast their ability to colonize other Antarctic environments.

Section snippets

Sampling site and experimental design

Microcosm experiments were conducted at the Carlini Research Station, located on the shores of PC at KGI, South Shetland Archipelago, Antarctica (62° 14′S, 58° 38′W), from January 23 to 31, 2016. The initial phytoplankton community was collected from the entrance of the cove (“outer Potter Cove” in Fig. 1) at 5 m depth with Niskin bottles. Seawater was prefiltered with a 300 μm Nitex mesh, to eliminate mesozooplankton, and used to fill 12,100-l plastic tanks, which were previously washed with

Phytoplankton biomass, cell abundance and dissolved nutrients

At the beginning of the experiment (Day 0), Chl-a values averaged 7.8 ± 0.8 μg l−1 and showed no significant differences between treatments (p = 0.16) (Fig. 2A). In the control (S0T0) and low salinity (S-T0) treatments, Chl-a increased significantly until day 5 reaching a maximum value of 16.9 ± 0.8 μg l−1 and 17.4 ± 1.7 μg l−1, respectively (p < 0.05) (Fig. 2A). In the S0T+ treatment, Chl-a increased significantly until day 3, when it reached a maximum of 28.2 ± 4.5 μg l−1, doubling the values

Discussion

Abrupt temperature changes such as heatwaves and such as those simulated in the present study have doubled in frequency and have become longer-lasting, more intense and more extensive (IPCC, 2019). Moreover, there are very likely (i.e., there is very high confidence) for these events to further happen in the future (IPCC, 2019). Natural communities in these short-term warming scenarios will probably not have the time to acclimate to higher temperatures, a process that needs over 6–7 days (Gao

Conclusion

In this study we found that the abundance of nano-sized diatoms of the genera Chaetoceros and Shionodiscus and small unidentified phytoflagellates increased in high temperature treatments, compensating the potential damaging effects of salinity, whereas micro-size pennate diatoms decreased. Moreover, an increase in the relative abundance of chlorophytes was observed only in the low salinity treatments, under nitrate depletion. Based on our results, climate change can result in a shift towards

Funding sources

This work was supported by grants PICT 2011-130 Raíces from Agencia Nacional de Promociones Científicas (ANPCyT, Argentina) to I.R.S., and PIP-0122 from Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, Argentina) to G.O.A. and a CONICET doctoral fellowship to J.S.A. Funding from a Canadian NSERC Discovery Grant awarded to D.E.V. was used to support partial travel costs for D.E.V.

Author contribution

Julieta S. Antoni: Conceptualization, Formal analysis, Visualization, Writing - Original Draft, Writing - Review & Editing. Gastón O. Almandoz: Conceptualization, Formal analysis, Writing - Original Draft, Writing - Review & Editing, Supervision. Martha E. Ferrario: Data curation, Formal analysis, Writing - Review & Editing. Marcelo P. Hernando: Conceptualization, Methodology, Writing - Original Draft, Writing - Review & Editing. Diana E. Varela: Conceptualization, Methodology, Writing - Review

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

This research was also supported by EU FP7-People-2012-IRSES programme (IMCONet, agreement no. 318718) and is a contribution to CoastCarb (Funding ID 872609, H2020, MSCA-RISE-2019, Research and Innovation Staff Exchange). We thank Diego Giménez (IDEA-CONICET) and Gwenaëlle Gremion (ISMER-UQAR, Rimouski, Canada) for their assistance during the experiments, as well as the personnel of the Carlini Station and the divers of the Prefectura Naval Argentina for their help during field work.

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