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Growth and Mortality of Coccolithophores During Spring in a Temperate Shelf T Sea (Celtic Sea, April 2015) ⁎ K.M.J

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Growth and Mortality of Coccolithophores During Spring in a Temperate Shelf T Sea (Celtic Sea, April 2015) ⁎ K.M.J Progress in Oceanography 177 (2019) 101928 Contents lists available at ScienceDirect Progress in Oceanography journal homepage: www.elsevier.com/locate/pocean Growth and mortality of coccolithophores during spring in a temperate Shelf T Sea (Celtic Sea, April 2015) ⁎ K.M.J. Mayersa, , A.J. Poultonb,1, C.J. Danielsb, S.R. Wellsc, E.M.S. Woodwardd, G.A. Tarrand, C.E. Widdicombed, D.J. Mayorb, A. Atkinsond, S.L.C. Gieringb a Ocean and Earth Science, National Oceanography Centre Southampton, University of Southampton, Southampton, UK b National Oceanography Centre, Waterfront Campus, European Way, Southampton, UK c Institute of Biological and Environmental Sciences, University of Aberdeen, Oceanlab, Newburgh, Aberdeenshire, UK d Plymouth Marine Laboratory, Prospect Place, The Hoe, Plymouth, UK ARTICLE INFO ABSTRACT Keywords: Coccolithophores are key components of phytoplankton communities, exerting a critical impact on the global Coccolithophores carbon cycle and the Earth’s climate through the production of coccoliths made of calcium carbonate (calcite) Growth rates and bioactive gases. Microzooplankton grazing is an important mortality factor in coccolithophore blooms, Microzooplankton grazing however little is currently known regarding the mortality (or growth) rates within non-bloom populations. Calcite production Measurements of coccolithophore calcite production (CP) and dilution experiments to determine micro- Dissolution zooplankton (≤63 µm) grazing rates were made during a spring cruise (April 2015) at the Central Celtic Sea Spring bloom (CCS), shelf edge (CS2), and within an adjacent April bloom of the coccolithophore Emiliania huxleyi at station J2. CP at CCS ranged from 10.4 to 40.4 µmol C m−3 d−1 and peaked at the height of the spring phytoplankton bloom (peak chlorophyll-a concentrations ∼6 mg m−3). Cell normalised calcification rates declined from ∼1.7 to ∼0.2 pmol C cell−1 d−1, accompanied by a shift from a mixed coccolithophore species community to one dominated by the more lightly calcified species E. huxleyi and Calciopappus caudatus. At the CCS, coccolithophore abundance increased from 6 to 94 cells mL−1, with net growth rates ranging from 0.06 to 0.21 d−1 from the 4th to the 28th April. Estimates of intrinsic growth and grazing rates from dilution experiments, at the CCS ranged from 0.01 to 0.86 d−1 and from 0.01 to 1.32 d−1, respectively, which resulted in variable net growth rates during April. Microzooplankton grazers consumed 59 to >100% of daily calcite production at the CCS. Within the E. huxleyi bloom a maximum density of 1986 cells mL−1 was recorded, along with CP rates of 6000 µmol C m−3 d−1 and an intrinsic growth rate of 0.29 d−1, with ∼80% of daily calcite production being consumed. Our results show that microzooplankton can exert strong top-down control on both bloom and non-bloom coccolithophore populations, grazing over 60% of daily growth (and calcite production). The fate of consumed calcite is unclear, but may be lost either through dissolution in acidic food vacuoles, and subsequent release as CO2, or export to the seabed after incorporation into small faecal pellets. With such high microzooplankton- mediated mortality losses, the fate of grazed calcite is clearly a high priority research direction. 1. Introduction (e.g. Holligan et al., 1993; Buitenhuis et al., 1996). Calcite can also act as a ballast for sinking material, enhancing the deep-sea flux of organic Coccolithophores are a diverse and biogeochemically important matter (Bach et al., 2016; Klaas and Archer, 2002; Ziveri et al., 2007). group of marine phytoplankton which contribute towards the marine Coccolithophores are globally distributed, from polar to tropical low- carbon cycle through the production and subsequent export of cellular latitude waters, with the most cosmopolitan and abundant species scales (coccoliths) formed of calcium carbonate (calcite). The cellular being Emiliania huxleyi (e.g. Winter and Siesser, 1994). E. huxleyi often 2 process of calcite production (calcification) fixes and releases CO2 and forms extensive, large-scale (>100,000 km ) blooms in the open ocean hence coccolithophores have an important role in air-sea CO2 fluxes (e.g. Holligan et al., 1993), along continental shelves (e.g. Holligan ⁎ Corresponding author. E-mail address: [email protected] (K.M.J. Mayers). 1 Current address: The Lyell Centre, Heriot-Watt University, Edinburgh, UK. https://doi.org/10.1016/j.pocean.2018.02.024 Available online 10 March 2018 0079-6611/ Crown Copyright © 2018 Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/BY/4.0/). K.M.J. Mayers, et al. Progress in Oceanography 177 (2019) 101928 et al., 1983; Poulton et al., 2013) and in coastal shelf seas (e.g. during an E. huxleyi bloom in the Bering Sea found lower grazing rates Buitenhuis et al., 1996; Krueger-Hadfield et al., 2014; Rees et al., 2002). within bloom waters than outside bloom waters, which led to higher Phytoplankton blooms are common in shelf sea environments net growth rates compared with outside of the bloom (Olson and Strom, during late spring, when environmental conditions allow growth to 2002). A similar result was observed in the English Channel (Fileman exceed mortality and biomass to accumulate. The community structure et al., 2002), suggesting depressed grazing rates on coccolithophores within these blooms may change with time as environmental conditions could be a trigger for bloom formation and persistence. such as nutrient and light availability favour one phytoplankton group At the cellular scale, calcification accounts for ∼30% of photo- over another. Coccolithophore blooms are considered to be favoured synthetically fixed energy and hence represents a important fraction of under conditions between high-turbulence high-nutrient and low-tur- the total cellular metabolism available for key cellular processes such as bulence low-nutrient environments (Balch, 2004). However, satellite- nutrient uptake and cell division (Monteiro et al., 2016). The ecological derived particulate inorganic calcite and chlorophyll-a data from open or physiological role of calcification is not fully known, though several ocean regions suggest that blooms of coccolithophores can also co- hypotheses exist, such as protection from light stress, enhancement of occur with blooms of other phytoplankton (e.g. diatoms), and sequen- photosynthesis, buoyancy regulation and as a protection from grazing tial succession between groups may not always occur (Hopkins et al., (Young, 1994; Monteiro et al., 2016). A recent modelling study pro- 2015). In situ observations made during several phytoplankton blooms posed that calcification has different ecological roles across different support the co-occurrence of coccolithophores with other groups, in- oceanic provinces (Monteiro et al., 2016). However, experimental re- cluding diatoms and dinoflagellates in both open ocean and coastal sults have so far demonstrated less clarity on the role of calcification. environments (see Daniels et al., 2015; Poulton et al., 2013, 2014; For example, culture experiments with the heterotrophic dinoflagellate Schiebel et al., 2011), however we currently lack in situ data from shelf Oxyrrhis marina showed grazing to be higher on calcified E. huxleyi cells sea environments during spring. than naked ones (Hansen et al., 1996). More recently, another culture Blooms of E. huxleyi have been shown to be important sources of experiment has shown that grazing rates on E. huxleyi appeared to be calcite production (CP) (e.g. Balch et al., 2005; Poulton et al., 2007, dependent on the strain studied rather than cell calcite content, al- 2013), primary production (PP) (up to 30–40% (Poulton et al., 2013)), though the growth rates of the heterotrophic dinoflagellates and their CO2 fluxes (e.g. Buitenhuis et al., 1996), and the production of the overall grazing impact were depressed due to the cellular degree of bioactive gas dimethyl sulphide (e.g. Malin et al., 1993). Within some calcification (Harvey et al., 2015). shelf sea regions, E. huxleyi blooms are an annual feature (e.g. English The aim of our study was to examine the variability in the rates at Channel, Patagonian Shelf) whereas in others they appear sporadically which coccolithophore communities grow and are being grazed on by though, recently at an increased frequency (e.g. Barent’s Sea, Black Sea) microzooplankton, and how these relate to environmental conditions (Iglesias-Rodriguez et al., 2002; Smyth et al., 2004). How these blooms and the microzooplankton community. We carried out our study during fit into global budgets of CP is currently unclear, though they arelo- April, as this is the key period in temperate shelf seas for the spring calised sites of high CP and export (Holligan et al., 1993; Poulton et al., phytoplankton bloom and not generally associated with coccolitho- 2013). phore blooms which typically occur in late summer. We measured The formation of E. huxleyi blooms, which often occur in late coccolithophore growth and mortality rates, alongside observations of summer, is thought to be linked to several environmental factors in- coccolithophore species composition and CP, during April at three sites cluding; warm, stratified waters, with low silicic acid concentrations in the Celtic Sea in order to examine: (1) the role of coccolithophores in (limiting diatoms), high irradiance, low nitrate to phosphate ratios, and carbon cycling during spring, (2) coccolithophore
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