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Increasing picocyanobacteria success in shelf waters contributes to long‐term food web degradation

Increasing picocyanobacteria success in shelf waters contributes to long‐term food web degradation
Increasing picocyanobacteria success in shelf waters contributes to long‐term food web degradation
Continental margins are disproportionally important for global primary production, fisheries and CO2 uptake. However, across the Northeast Atlantic shelves, there has been an ongoing summertime decline of key biota—large diatoms, dinoflagellates and copepods—that traditionally fuel higher tropic levels such as fish, sea birds and marine mammals. Here, we combine multiple time series with in situ process studies to link these declines to summer nutrient stress and increasing proportions of picophytoplankton that can comprise up to 90% of the combined pico‐ and nanophytoplankton biomass in coastal areas. Among the pico‐fraction, it is the cyanobacterium Synechococcus that flourishes when iron and nitrogen resupply to surface waters are diminished. Our field data show how traits beyond small size give Synechococcus a competitive edge over pico‐ and nanoeukaryotes. Key is their ability to grow at low irradiances near the nutricline, which is aided by their superior light‐harvesting system and high affinity to iron. However, minute size and lack of essential biomolecules (e.g. omega‐3 polyunsaturated fatty acids and sterols) render Synechococcus poor primary producers to sustain shelf sea food webs efficiently. The combination of earlier spring blooms and lower summer food quantity and quality creates an increasing period of suboptimal feeding conditions for zooplankton at a time of year when their metabolic demand is highest. We suggest that this nutrition‐related mismatch has contributed to the widespread, ~50% decline in summer copepod abundance we observe over the last 60 years. With Synechococcus clades being prominent from the tropics to the Arctic and their abundances increasing worldwide, our study informs projections of future food web dynamics in coastal and shelf areas where droughts and stratification lead to increasing nutrient starvation of surface waters.
Synechococcus, Western Channel Observatory, climate change, copepods, food quality, iron, nitrate, picoeukaryotes, stratification, time series
1354-1013
5574-5587
Schmidt, Katrin
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Birchill, Antony
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Atkinson,
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Brewin,
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Clark,
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Hickman, Anna
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Johns,
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Lohan, Maeve
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Milne, Angela
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Pardo, Silvia
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Polimene,
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Smyth, Timothy
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Tarran, Glen
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Widdicombe, Claire E.
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Woodward, E. Malcolm S.
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Ussher, S.
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Schmidt, Katrin
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Birchill, Antony
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Atkinson,
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Brewin,
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Clark,
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Hickman, Anna
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Johns,
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Lohan, Maeve
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Milne, Angela
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Pardo, Silvia
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Polimene,
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Smyth, Timothy
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Tarran, Glen
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Widdicombe, Claire E.
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Woodward, E. Malcolm S.
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Ussher, S.
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Schmidt, Katrin, Birchill, Antony, Atkinson, , Brewin, , Clark, , Hickman, Anna, Johns, , Lohan, Maeve, Milne, Angela, Pardo, Silvia, Polimene, , Smyth, Timothy, Tarran, Glen, Widdicombe, Claire E., Woodward, E. Malcolm S. and Ussher, S. (2020) Increasing picocyanobacteria success in shelf waters contributes to long‐term food web degradation. Global Change Biology, 26 (10), 5574-5587. (doi:10.1111/gcb.15161).

Record type: Article

Abstract

Continental margins are disproportionally important for global primary production, fisheries and CO2 uptake. However, across the Northeast Atlantic shelves, there has been an ongoing summertime decline of key biota—large diatoms, dinoflagellates and copepods—that traditionally fuel higher tropic levels such as fish, sea birds and marine mammals. Here, we combine multiple time series with in situ process studies to link these declines to summer nutrient stress and increasing proportions of picophytoplankton that can comprise up to 90% of the combined pico‐ and nanophytoplankton biomass in coastal areas. Among the pico‐fraction, it is the cyanobacterium Synechococcus that flourishes when iron and nitrogen resupply to surface waters are diminished. Our field data show how traits beyond small size give Synechococcus a competitive edge over pico‐ and nanoeukaryotes. Key is their ability to grow at low irradiances near the nutricline, which is aided by their superior light‐harvesting system and high affinity to iron. However, minute size and lack of essential biomolecules (e.g. omega‐3 polyunsaturated fatty acids and sterols) render Synechococcus poor primary producers to sustain shelf sea food webs efficiently. The combination of earlier spring blooms and lower summer food quantity and quality creates an increasing period of suboptimal feeding conditions for zooplankton at a time of year when their metabolic demand is highest. We suggest that this nutrition‐related mismatch has contributed to the widespread, ~50% decline in summer copepod abundance we observe over the last 60 years. With Synechococcus clades being prominent from the tropics to the Arctic and their abundances increasing worldwide, our study informs projections of future food web dynamics in coastal and shelf areas where droughts and stratification lead to increasing nutrient starvation of surface waters.

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Accepted/In Press date: 24 April 2020
e-pub ahead of print date: 7 June 2020
Published date: 1 October 2020
Additional Information: Funding Information: This study has been conducted using E.U. Copernicus Marine Service Information and is a contribution to the Ocean Colour Component of the Climate Change Initiative of the European Space Agency (ESA). We thank the teams of plankton analysts who have contributed to the CPR survey database since 1958. We acknowledge the crews of the RV Plymouth Quest, RV MBA Sepia and scientists at Plymouth Marine Laboratory who conducted the weekly sample collection and provision of core measurements for the Western Channel Observatory (L4 monitoring site). River flow data were kindly provided by the National River Flow Archive (2007?2017) and the UK Environment Agency (2018). We thank the captains and crews of the RRS Discovery and the principal scientists A. Poulton and M. Moore for their professional support during the Shelf Sea Biogeochemistry cruises in April 2015 (DY029) and July 2015 (DY033). K. Flynn provided valuable insights on mixotrophy and iron cycling. N. Hartner and C. Harris helped with the trace metal and macronutrient analysis. The work was funded by UK Natural Environment Research Council (NERC) via the Shelf Sea Biogeochemistry programme, grants NE/L501840/1 (A.J.B.), NE/K001779/1 (A.M., S.J.U.,M.C.L.,K.S.) and NE/K001876/1 (J.R.C, L.P.), with further support from its Long-term Single Centre Science Programme, ?Climate Linked Atlantic Sector Science' grant NE/R015953/1 (A.A, T.J.S., G.A.T., C.E.W., E.M.S.W.). The authors have no conflicts of interest to declare. Publisher Copyright: © 2020 The Authors. Global Change Biology published by John Wiley & Sons Ltd
Keywords: Synechococcus, Western Channel Observatory, climate change, copepods, food quality, iron, nitrate, picoeukaryotes, stratification, time series

Identifiers

Local EPrints ID: 442303
URI: http://eprints.soton.ac.uk/id/eprint/442303
ISSN: 1354-1013
PURE UUID: 404465dc-962d-40e9-9c17-5e5357638509
ORCID for Anna Hickman: ORCID iD orcid.org/0000-0002-2774-3934
ORCID for Maeve Lohan: ORCID iD orcid.org/0000-0002-5340-3108

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Date deposited: 13 Jul 2020 16:30
Last modified: 17 Mar 2024 03:31

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Contributors

Author: Katrin Schmidt
Author: Antony Birchill
Author: Atkinson
Author: Brewin
Author: Clark
Author: Anna Hickman ORCID iD
Author: Johns
Author: Maeve Lohan ORCID iD
Author: Angela Milne
Author: Silvia Pardo
Author: Polimene
Author: Timothy Smyth
Author: Glen Tarran
Author: Claire E. Widdicombe
Author: E. Malcolm S. Woodward
Author: S. Ussher

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