Dependency of Antarctic zooplankton species on ice algae-produced carbon suggests a sea ice-driven pelagic ecosystem during winter

Doreen Kohlbach; Martin Graeve; Benjamin A. Lange; Carmen David; Fokje L. Schaafsma; Jan Andries van Franeker; Martina Vortkamp; Angelika Brandt; Hauke Flores

doi:10.1111/gcb.14392

Dependency of Antarctic zooplankton species on ice algae-produced carbon suggests a sea ice-driven pelagic ecosystem during winter

Doreen Kohlbach, Martin Graeve, Benjamin A. Lange, Carmen David, Fokje L. Schaafsma, Jan Andries van Franeker, Martina Vortkamp, Angelika Brandt, Hauke Flores

Research output: Contribution to journal › Article › peer-review

38 Citations (Scopus)

Abstract

How the abundant pelagic life of the Southern Ocean survives winter darkness, when the sea is covered by pack ice and phytoplankton production is nearly zero, is poorly understood. Ice-associated (“sympagic”) microalgae could serve as a high-quality carbon source during winter, but their significance in the food web is so far unquantified. To better understand the importance of ice algae-produced carbon for the overwintering of Antarctic organisms, we investigated fatty acid (FA) and stable isotope compositions of 10 zooplankton species, and their potential sympagic and pelagic carbon sources. FA-specific carbon stable isotope compositions were used in stable isotope mixing models to quantify the contribution of ice algae-produced carbon (α_Ice) to the body carbon of each species. Mean α_Ice estimates ranged from 4% to 67%, with large variations between species and depending on the FA used for the modelling. Integrating the α_Ice estimates from all models, the sympagic amphipod Eusirus laticarpus was the most dependent on ice algal carbon (α_Ice: 54%–67%), and the salp Salpa thompsoni showed the least dependency on ice algal carbon (α_Ice: 8%–40%). Differences in α_Iceestimates between FAs associated with short-term vs. long-term lipid pools suggested an increasing importance of ice algal carbon for many species as the winter season progressed. In the abundant winter-active copepod Calanus propinquus, mean α_Ice reached more than 50% in late winter. The trophic carbon flux from ice algae into this copepod was between 3 and 5 mg C m⁻² day⁻¹. This indicates that copepods and other ice-dependent zooplankton species transfer significant amounts of carbon from ice algae into the pelagic system, where it fuels the food web, the biological carbon pump and elemental cycling. Understanding the role of ice algae-produced carbon in these processes will be the key to predictions of the impact of future sea ice decline on Antarctic ecosystem functioning.

Original language	English
Pages (from-to)	4667-4681
Number of pages	15
Journal	Global Change Biology
Volume	24
Issue number	10
DOIs	https://doi.org/10.1111/gcb.14392
Publication status	Published - Oct 2018
Externally published	Yes

Bibliographical note

Funding Information:
Funding information This study was conducted under the Helmholtz Association Research Programme Polar regions and coasts in the changing earth system II (PACES II), Topic 1, WP 5 as part of the Helmholtz Association Young Investigators Group Iceflux: Ice ecosystem carbon flux in polar oceans (VH-NG-800). SUIT was developed by Wageningen Marine Research with support from the Netherlands Ministry of EZ (project WOT-04-009-036) and the Netherlands Polar Program (project ALW 866.13.009). We would like to thank Captain Stefan Schwarze and the crew of the RV “Polarstern” expedition PS81 for their excellent support with work at sea. We thank Michiel van Dorssen, André Meijboom, Evgeny Pakhomov and Brian Hunt for technical support with work at sea. We are grateful for the support with the laboratory analyses of Theresa Geißler and Dieter Janssen. We thank Bettina Meyer for kindly providing ice algae samples, and Anya Waite for supporting the development of the manuscript. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Funding Information:
This study was conducted under the Helmholtz Association Research Programme Polar regions and coasts in the changing earth system II (PACES II), Topic 1, WP 5 as part of the Helmholtz Association Young Investigators Group Iceflux: Ice ecosystem carbon flux in polar oceans (VH‐NG‐800). SUIT was developed by Wageningen Marine Research with support from the Netherlands Ministry of EZ (project WOT‐04‐009‐036) and the Netherlands Polar Program (project ALW 866.13.009).

Publisher Copyright:
© 2018 The Authors. Global Change Biology Published by John Wiley & Sons Ltd

ASJC Scopus Subject Areas

Global and Planetary Change
Environmental Chemistry
Ecology
General Environmental Science

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10.1111/gcb.14392

Cite this

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title = "Dependency of Antarctic zooplankton species on ice algae-produced carbon suggests a sea ice-driven pelagic ecosystem during winter",

abstract = "How the abundant pelagic life of the Southern Ocean survives winter darkness, when the sea is covered by pack ice and phytoplankton production is nearly zero, is poorly understood. Ice-associated (“sympagic”) microalgae could serve as a high-quality carbon source during winter, but their significance in the food web is so far unquantified. To better understand the importance of ice algae-produced carbon for the overwintering of Antarctic organisms, we investigated fatty acid (FA) and stable isotope compositions of 10 zooplankton species, and their potential sympagic and pelagic carbon sources. FA-specific carbon stable isotope compositions were used in stable isotope mixing models to quantify the contribution of ice algae-produced carbon (αIce) to the body carbon of each species. Mean αIce estimates ranged from 4% to 67%, with large variations between species and depending on the FA used for the modelling. Integrating the αIce estimates from all models, the sympagic amphipod Eusirus laticarpus was the most dependent on ice algal carbon (αIce: 54%–67%), and the salp Salpa thompsoni showed the least dependency on ice algal carbon (αIce: 8%–40%). Differences in αIceestimates between FAs associated with short-term vs. long-term lipid pools suggested an increasing importance of ice algal carbon for many species as the winter season progressed. In the abundant winter-active copepod Calanus propinquus, mean αIce reached more than 50% in late winter. The trophic carbon flux from ice algae into this copepod was between 3 and 5 mg C m−2 day−1. This indicates that copepods and other ice-dependent zooplankton species transfer significant amounts of carbon from ice algae into the pelagic system, where it fuels the food web, the biological carbon pump and elemental cycling. Understanding the role of ice algae-produced carbon in these processes will be the key to predictions of the impact of future sea ice decline on Antarctic ecosystem functioning.",

author = "Doreen Kohlbach and Martin Graeve and Lange, {Benjamin A.} and Carmen David and Schaafsma, {Fokje L.} and {van Franeker}, {Jan Andries} and Martina Vortkamp and Angelika Brandt and Hauke Flores",

note = "Funding Information: Funding information This study was conducted under the Helmholtz Association Research Programme Polar regions and coasts in the changing earth system II (PACES II), Topic 1, WP 5 as part of the Helmholtz Association Young Investigators Group Iceflux: Ice ecosystem carbon flux in polar oceans (VH-NG-800). SUIT was developed by Wageningen Marine Research with support from the Netherlands Ministry of EZ (project WOT-04-009-036) and the Netherlands Polar Program (project ALW 866.13.009). We would like to thank Captain Stefan Schwarze and the crew of the RV “Polarstern” expedition PS81 for their excellent support with work at sea. We thank Michiel van Dorssen, Andr{\'e} Meijboom, Evgeny Pakhomov and Brian Hunt for technical support with work at sea. We are grateful for the support with the laboratory analyses of Theresa Gei{\ss}ler and Dieter Janssen. We thank Bettina Meyer for kindly providing ice algae samples, and Anya Waite for supporting the development of the manuscript. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Funding Information: This study was conducted under the Helmholtz Association Research Programme Polar regions and coasts in the changing earth system II (PACES II), Topic 1, WP 5 as part of the Helmholtz Association Young Investigators Group Iceflux: Ice ecosystem carbon flux in polar oceans (VH‐NG‐800). SUIT was developed by Wageningen Marine Research with support from the Netherlands Ministry of EZ (project WOT‐04‐009‐036) and the Netherlands Polar Program (project ALW 866.13.009). Publisher Copyright: {\textcopyright} 2018 The Authors. Global Change Biology Published by John Wiley & Sons Ltd",

year = "2018",

month = oct,

doi = "10.1111/gcb.14392",

language = "English",

volume = "24",

pages = "4667--4681",

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T1 - Dependency of Antarctic zooplankton species on ice algae-produced carbon suggests a sea ice-driven pelagic ecosystem during winter

AU - Kohlbach, Doreen

AU - Graeve, Martin

AU - Lange, Benjamin A.

AU - David, Carmen

AU - Schaafsma, Fokje L.

AU - van Franeker, Jan Andries

AU - Vortkamp, Martina

AU - Brandt, Angelika

AU - Flores, Hauke

N1 - Funding Information: Funding information This study was conducted under the Helmholtz Association Research Programme Polar regions and coasts in the changing earth system II (PACES II), Topic 1, WP 5 as part of the Helmholtz Association Young Investigators Group Iceflux: Ice ecosystem carbon flux in polar oceans (VH-NG-800). SUIT was developed by Wageningen Marine Research with support from the Netherlands Ministry of EZ (project WOT-04-009-036) and the Netherlands Polar Program (project ALW 866.13.009). We would like to thank Captain Stefan Schwarze and the crew of the RV “Polarstern” expedition PS81 for their excellent support with work at sea. We thank Michiel van Dorssen, André Meijboom, Evgeny Pakhomov and Brian Hunt for technical support with work at sea. We are grateful for the support with the laboratory analyses of Theresa Geißler and Dieter Janssen. We thank Bettina Meyer for kindly providing ice algae samples, and Anya Waite for supporting the development of the manuscript. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Funding Information: This study was conducted under the Helmholtz Association Research Programme Polar regions and coasts in the changing earth system II (PACES II), Topic 1, WP 5 as part of the Helmholtz Association Young Investigators Group Iceflux: Ice ecosystem carbon flux in polar oceans (VH‐NG‐800). SUIT was developed by Wageningen Marine Research with support from the Netherlands Ministry of EZ (project WOT‐04‐009‐036) and the Netherlands Polar Program (project ALW 866.13.009). Publisher Copyright: © 2018 The Authors. Global Change Biology Published by John Wiley & Sons Ltd

PY - 2018/10

Y1 - 2018/10

N2 - How the abundant pelagic life of the Southern Ocean survives winter darkness, when the sea is covered by pack ice and phytoplankton production is nearly zero, is poorly understood. Ice-associated (“sympagic”) microalgae could serve as a high-quality carbon source during winter, but their significance in the food web is so far unquantified. To better understand the importance of ice algae-produced carbon for the overwintering of Antarctic organisms, we investigated fatty acid (FA) and stable isotope compositions of 10 zooplankton species, and their potential sympagic and pelagic carbon sources. FA-specific carbon stable isotope compositions were used in stable isotope mixing models to quantify the contribution of ice algae-produced carbon (αIce) to the body carbon of each species. Mean αIce estimates ranged from 4% to 67%, with large variations between species and depending on the FA used for the modelling. Integrating the αIce estimates from all models, the sympagic amphipod Eusirus laticarpus was the most dependent on ice algal carbon (αIce: 54%–67%), and the salp Salpa thompsoni showed the least dependency on ice algal carbon (αIce: 8%–40%). Differences in αIceestimates between FAs associated with short-term vs. long-term lipid pools suggested an increasing importance of ice algal carbon for many species as the winter season progressed. In the abundant winter-active copepod Calanus propinquus, mean αIce reached more than 50% in late winter. The trophic carbon flux from ice algae into this copepod was between 3 and 5 mg C m−2 day−1. This indicates that copepods and other ice-dependent zooplankton species transfer significant amounts of carbon from ice algae into the pelagic system, where it fuels the food web, the biological carbon pump and elemental cycling. Understanding the role of ice algae-produced carbon in these processes will be the key to predictions of the impact of future sea ice decline on Antarctic ecosystem functioning.

AB - How the abundant pelagic life of the Southern Ocean survives winter darkness, when the sea is covered by pack ice and phytoplankton production is nearly zero, is poorly understood. Ice-associated (“sympagic”) microalgae could serve as a high-quality carbon source during winter, but their significance in the food web is so far unquantified. To better understand the importance of ice algae-produced carbon for the overwintering of Antarctic organisms, we investigated fatty acid (FA) and stable isotope compositions of 10 zooplankton species, and their potential sympagic and pelagic carbon sources. FA-specific carbon stable isotope compositions were used in stable isotope mixing models to quantify the contribution of ice algae-produced carbon (αIce) to the body carbon of each species. Mean αIce estimates ranged from 4% to 67%, with large variations between species and depending on the FA used for the modelling. Integrating the αIce estimates from all models, the sympagic amphipod Eusirus laticarpus was the most dependent on ice algal carbon (αIce: 54%–67%), and the salp Salpa thompsoni showed the least dependency on ice algal carbon (αIce: 8%–40%). Differences in αIceestimates between FAs associated with short-term vs. long-term lipid pools suggested an increasing importance of ice algal carbon for many species as the winter season progressed. In the abundant winter-active copepod Calanus propinquus, mean αIce reached more than 50% in late winter. The trophic carbon flux from ice algae into this copepod was between 3 and 5 mg C m−2 day−1. This indicates that copepods and other ice-dependent zooplankton species transfer significant amounts of carbon from ice algae into the pelagic system, where it fuels the food web, the biological carbon pump and elemental cycling. Understanding the role of ice algae-produced carbon in these processes will be the key to predictions of the impact of future sea ice decline on Antarctic ecosystem functioning.

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Dependency of Antarctic zooplankton species on ice algae-produced carbon suggests a sea ice-driven pelagic ecosystem during winter

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