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 lev...

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Veröffentlicht in:Global change biology 2020-10, Vol.26 (10), p.5574-5587
Hauptverfasser: Schmidt, Katrin, Birchill, Antony J., Atkinson, Angus, Brewin, Robert J. W., Clark, James R., Hickman, Anna E., Johns, David G., Lohan, Maeve C., Milne, Angela, Pardo, Silvia, Polimene, Luca, Smyth, Tim J., Tarran, Glen A., Widdicombe, Claire E., Woodward, E. Malcolm S., Ussher, Simon J.
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container_end_page 5587
container_issue 10
container_start_page 5574
container_title Global change biology
container_volume 26
creator Schmidt, Katrin
Birchill, Antony J.
Atkinson, Angus
Brewin, Robert J. W.
Clark, James R.
Hickman, Anna E.
Johns, David G.
Lohan, Maeve C.
Milne, Angela
Pardo, Silvia
Polimene, Luca
Smyth, Tim J.
Tarran, Glen A.
Widdicombe, Claire E.
Woodward, E. Malcolm S.
Ussher, Simon J.
description 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. See also the Commentary on this article by Brander and Kiørboe, 26, 5356-5357. Over the last ~60 years, key marine biota (large diatoms, dinoflagellates, copepods) have been declining across Northeast Atlantic shelves. We combine multiple time‐series with in situ process studies to link these declines to summer water column stratification, nutrient stress and increasing dominance of picophytoplankton. High structural investments for resource acquisition (light, iron) enable consistent, but relatively slow growth rates in the picocyanobacterium Synechococcus. This strategy proves disadvantageous
doi_str_mv 10.1111/gcb.15161
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W. ; Clark, James R. ; Hickman, Anna E. ; Johns, David G. ; Lohan, Maeve C. ; Milne, Angela ; Pardo, Silvia ; Polimene, Luca ; Smyth, Tim J. ; Tarran, Glen A. ; Widdicombe, Claire E. ; Woodward, E. Malcolm S. ; Ussher, Simon J.</creator><creatorcontrib>Schmidt, Katrin ; Birchill, Antony J. ; Atkinson, Angus ; Brewin, Robert J. W. ; Clark, James R. ; Hickman, Anna E. ; Johns, David G. ; Lohan, Maeve C. ; Milne, Angela ; Pardo, Silvia ; Polimene, Luca ; Smyth, Tim J. ; Tarran, Glen A. ; Widdicombe, Claire E. ; Woodward, E. Malcolm S. ; Ussher, Simon J.</creatorcontrib><description>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. See also the Commentary on this article by Brander and Kiørboe, 26, 5356-5357. Over the last ~60 years, key marine biota (large diatoms, dinoflagellates, copepods) have been declining across Northeast Atlantic shelves. 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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. 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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. See also the Commentary on this article by Brander and Kiørboe, 26, 5356-5357. Over the last ~60 years, key marine biota (large diatoms, dinoflagellates, copepods) have been declining across Northeast Atlantic shelves. We combine multiple time‐series with in situ process studies to link these declines to summer water column stratification, nutrient stress and increasing dominance of picophytoplankton. High structural investments for resource acquisition (light, iron) enable consistent, but relatively slow growth rates in the picocyanobacterium Synechococcus. This strategy proves disadvantageous under nutrient replete conditions, but becomes increasingly beneficial when nutrients diminish. The resulting Synechococcus ‘blooms’ are of low value for higher trophic levels that rely on larger, omega‐3 enriched primary producers for efficient carbon transfer.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>32506810</pmid><doi>10.1111/gcb.15161</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0003-3270-6764</orcidid><orcidid>https://orcid.org/0000-0002-3304-8962</orcidid><orcidid>https://orcid.org/0000-0002-3549-6937</orcidid><orcidid>https://orcid.org/0000-0002-5931-4325</orcidid><orcidid>https://orcid.org/0000-0002-1688-0212</orcidid><orcidid>https://orcid.org/0000-0001-5134-8291</orcidid><orcidid>https://orcid.org/0000-0002-7187-6689</orcidid><orcidid>https://orcid.org/0000-0002-6488-623X</orcidid><orcidid>https://orcid.org/0000-0001-6724-9212</orcidid><orcidid>https://orcid.org/0000-0002-1453-5781</orcidid><orcidid>https://orcid.org/0000-0002-1924-5871</orcidid><orcidid>https://orcid.org/0000-0001-9773-0058</orcidid><orcidid>https://orcid.org/0000-0002-5340-3108</orcidid><orcidid>https://orcid.org/0000-0003-0659-1422</orcidid><orcidid>https://orcid.org/0000-0003-3695-5151</orcidid><oa>free_for_read</oa></addata></record>
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identifier ISSN: 1354-1013
ispartof Global change biology, 2020-10, Vol.26 (10), p.5574-5587
issn 1354-1013
1365-2486
language eng
recordid cdi_proquest_journals_2444793943
source MEDLINE; Wiley Online Library Journals Frontfile Complete
subjects Animals
Aquatic birds
Aquatic crustaceans
Arctic Regions
Biodegradation
Biomass
Biomolecules
Biota
Blooms
Carbon dioxide
climate change
Coastal zone
Continental margins
copepods
Diatoms
Dinoflagellates
Drought
Fatty acids
Fish
Fisheries
Food Chain
Food chains
Food quality
Food webs
Iron
Marine fishes
Marine mammals
Marine microorganisms
Mineral nutrients
nitrate
Nutrients
Nutrition
Phytoplankton
picoeukaryotes
Plankton
Polar environments
Polyunsaturated fatty acids
Primary production
Seabirds
Seafood
Seafoods
Shelving
Starvation
Sterols
Stratification
Summer
Surface water
Synechococcus
time series
Tropical environments
Western Channel Observatory
Zooplankton
title Increasing picocyanobacteria success in shelf waters contributes to long‐term food web degradation
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