Articles | Volume 18, issue 1
https://doi.org/10.5194/bg-18-327-2021
© Author(s) 2021. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
https://doi.org/10.5194/bg-18-327-2021
© Author(s) 2021. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Research article
| 
15 Jan 2021
Research article |
| 15 Jan 2021
| 15 Jan 2021
Denitrification by benthic foraminifera and their contribution to N-loss from a fjord environment
Constance Choquel
CORRESPONDING AUTHOR
UMR 6112 LPG BIAF, Univ. Angers, Univ. Nantes, CNRS, Angers, France
Emmanuelle Geslin
CORRESPONDING AUTHOR
UMR 6112 LPG BIAF, Univ. Angers, Univ. Nantes, CNRS, Angers, France
Edouard Metzger
UMR 6112 LPG BIAF, Univ. Angers, Univ. Nantes, CNRS, Angers, France
Helena L. Filipsson
Department of Geology, Lund University, Lund, Sweden
Nils Risgaard-Petersen
Department of Biology, Aquatic Biology, Aarhus University, Aarhus, Denmark
Patrick Launeau
UMR 6112 LPG BIAF, Univ. Angers, Univ. Nantes, CNRS, Angers, France
Manuel Giraud
UMR 6112 LPG BIAF, Univ. Angers, Univ. Nantes, CNRS, Angers, France
Thierry Jauffrais
Ifremer, IRD, Univ. Nouvelle-Calédonie, Univ. La Réunion, CNRS, UMR 9220 ENTROPIE, Noumea, New Caledonia
UMR 6112 LPG BIAF, Univ. Angers, Univ. Nantes, CNRS, Angers, France
Bruno Jesus
Université de Nantes, Mer Molécules Santé, EA 2160, Nantes, France
BioISI – Biosystems & Integrative Sciences Institute, Campo Grande, Faculty of Sciences, University of Lisbon, Lisbon, Portugal
Aurélia Mouret
UMR 6112 LPG BIAF, Univ. Angers, Univ. Nantes, CNRS, Angers, France
Related authors
Babette A.A. Hoogakker, Catherine Davis, Yi Wang, Stephanie Kusch, Katrina Nilsson-Kerr, Dalton S. Hardisty, Allison Jacobel, Dharma Reyes Macaya, Nicolaas Glock, Sha Ni, Julio Sepúlveda, Abby Ren, Alexandra Auderset, Anya V. Hess, Katrin J. Meissner, Jorge Cardich, Robert Anderson, Christine Barras, Chandranath Basak, Harold J. Bradbury, Inda Brinkmann, Alexis Castillo, Madelyn Cook, Kassandra Costa, Constance Choquel, Paula Diz, Jonas Donnenfield, Felix J. Elling, Zeynep Erdem, Helena L. Filipsson, Sebastián Garrido, Julia Gottschalk, Anjaly Govindankutty Menon, Jeroen Groeneveld, Christian Hallmann, Ingrid Hendy, Rick Hennekam, Wanyi Lu, Jean Lynch-Stieglitz, Lélia Matos, Alfredo Martínez-García, Giulia Molina, Práxedes Muñoz, Simone Moretti, Jennifer Morford, Sophie Nuber, Svetlana Radionovskaya, Morgan Reed Raven, Christopher J. Somes, Anja S. Studer, Kazuyo Tachikawa, Raúl Tapia, Martin Tetard, Tyler Vollmer, Xingchen Wang, Shuzhuang Wu, Yan Zhang, Xin-Yuan Zheng, and Yuxin Zhou
Biogeosciences, 22, 863–957, https://doi.org/10.5194/bg-22-863-2025, https://doi.org/10.5194/bg-22-863-2025, 2025
Short summary
Short summary
Paleo-oxygen proxies can extend current records, constrain pre-anthropogenic baselines, provide datasets necessary to test climate models under different boundary conditions, and ultimately understand how ocean oxygenation responds on longer timescales. Here we summarize current proxies used for the reconstruction of Cenozoic seawater oxygen levels. This includes an overview of the proxy's history, how it works, resources required, limitations, and future recommendations.
Lukas Jonkers, Tonke Strack, Montserrat Alonso-Garcia, Simon D'haenens, Robert Huber, Michal Kucera, Iván Hernández-Almeida, Chloe L. C. Jones, Brett Metcalfe, Rajeev Saraswat, Lóránd Silye, Sanjay K. Verma, Muhamad Naim Abd Malek, Gerald Auer, Cátia F. Barbosa, Maria A. Barcena, Karl-Heinz Baumann, Flavia Boscolo-Galazzo, Joeven Austine S. Calvelo, Lucilla Capotondi, Martina Caratelli, Jorge Cardich, Humberto Carvajal-Chitty, Markéta Chroustová, Helen K. Coxall, Renata M. de Mello, Anne de Vernal, Paula Diz, Kirsty M. Edgar, Helena L. Filipsson, Ángela Fraguas, Heather L. Furlong, Giacomo Galli, Natalia L. García Chapori, Robyn Granger, Jeroen Groeneveld, Adil Imam, Rebecca Jackson, David Lazarus, Julie Meilland, Marína Molčan Matejová, Raphael Morard, Caterina Morigi, Sven N. Nielsen, Diana Ochoa, Maria Rose Petrizzo, Andrés S. Rigual-Hernández, Marina C. Rillo, Matthew L. Staitis, Gamze Tanık, Raúl Tapia, Nishant Vats, Bridget S. Wade, and Anna E. Weinmann
J. Micropalaeontol., 44, 145–168, https://doi.org/10.5194/jm-44-145-2025, https://doi.org/10.5194/jm-44-145-2025, 2025
Short summary
Short summary
Our study provides guidelines improving the reuse of marine microfossil assemblage data, which are valuable for understanding past ecosystems and environmental change. Based on a survey of 113 researchers, we identified key data attributes required for effective reuse. Analysis of a selection of datasets available online reveals a gap between the attributes scientists consider essential and the data currently available, highlighting the need for clearer data documentation and sharing practices.
Babette A.A. Hoogakker, Catherine Davis, Yi Wang, Stephanie Kusch, Katrina Nilsson-Kerr, Dalton S. Hardisty, Allison Jacobel, Dharma Reyes Macaya, Nicolaas Glock, Sha Ni, Julio Sepúlveda, Abby Ren, Alexandra Auderset, Anya V. Hess, Katrin J. Meissner, Jorge Cardich, Robert Anderson, Christine Barras, Chandranath Basak, Harold J. Bradbury, Inda Brinkmann, Alexis Castillo, Madelyn Cook, Kassandra Costa, Constance Choquel, Paula Diz, Jonas Donnenfield, Felix J. Elling, Zeynep Erdem, Helena L. Filipsson, Sebastián Garrido, Julia Gottschalk, Anjaly Govindankutty Menon, Jeroen Groeneveld, Christian Hallmann, Ingrid Hendy, Rick Hennekam, Wanyi Lu, Jean Lynch-Stieglitz, Lélia Matos, Alfredo Martínez-García, Giulia Molina, Práxedes Muñoz, Simone Moretti, Jennifer Morford, Sophie Nuber, Svetlana Radionovskaya, Morgan Reed Raven, Christopher J. Somes, Anja S. Studer, Kazuyo Tachikawa, Raúl Tapia, Martin Tetard, Tyler Vollmer, Xingchen Wang, Shuzhuang Wu, Yan Zhang, Xin-Yuan Zheng, and Yuxin Zhou
Biogeosciences, 22, 863–957, https://doi.org/10.5194/bg-22-863-2025, https://doi.org/10.5194/bg-22-863-2025, 2025
Short summary
Short summary
Paleo-oxygen proxies can extend current records, constrain pre-anthropogenic baselines, provide datasets necessary to test climate models under different boundary conditions, and ultimately understand how ocean oxygenation responds on longer timescales. Here we summarize current proxies used for the reconstruction of Cenozoic seawater oxygen levels. This includes an overview of the proxy's history, how it works, resources required, limitations, and future recommendations.
Maxime Daviray, Emmanuelle Geslin, Nils Risgaard-Petersen, Vincent V. Scholz, Marie Fouet, and Edouard Metzger
Biogeosciences, 21, 911–928, https://doi.org/10.5194/bg-21-911-2024, https://doi.org/10.5194/bg-21-911-2024, 2024
Short summary
Short summary
Coastal marine sediments are subject to major acidification processes because of climate change and human activities, but these processes can also result from biotic activity. We studied the sediment acidifcation effect on benthic calcareous foraminifera in intertidal mudflats. The strong pH decrease in sediments probably caused by cable bacteria led to calcareous test dissolution of living and dead foraminifera, threatening the test preservation and their robustness as environmental proxies.
K. Mareike Paul, Martijn Hermans, Sami A. Jokinen, Inda Brinkmann, Helena L. Filipsson, and Tom Jilbert
Biogeosciences, 20, 5003–5028, https://doi.org/10.5194/bg-20-5003-2023, https://doi.org/10.5194/bg-20-5003-2023, 2023
Short summary
Short summary
Seawater naturally contains trace metals such as Mo and U, which accumulate under low oxygen conditions on the seafloor. Previous studies have used sediment Mo and U contents as an archive of changing oxygen concentrations in coastal waters. Here we show that in fjords the use of Mo and U for this purpose may be impaired by additional processes. Our findings have implications for the reliable use of Mo and U to reconstruct oxygen changes in fjords.
Corentin Guilhermic, Maria Pia Nardelli, Aurélia Mouret, Damien Le Moigne, and Hélène Howa
Biogeosciences, 20, 3329–3351, https://doi.org/10.5194/bg-20-3329-2023, https://doi.org/10.5194/bg-20-3329-2023, 2023
Short summary
Short summary
Coastal seas experience sediment discharges whose intensity and frequency can strongly be affected by human activities and climate change. We analysed the response of benthic species in an experimental set-up. After the burial under a single thick layer of sediment or multiple thin layers at different times, the analysed species migrate rapidly towards the surface. A stronger effect of a single thick deposit on standing stocks and biodiversity is visible compared to frequent low-sediment inputs.
Christiane Schmidt, Emmanuelle Geslin, Joan M. Bernhard, Charlotte LeKieffre, Mette Marianne Svenning, Helene Roberge, Magali Schweizer, and Giuliana Panieri
Biogeosciences, 19, 3897–3909, https://doi.org/10.5194/bg-19-3897-2022, https://doi.org/10.5194/bg-19-3897-2022, 2022
Short summary
Short summary
This study is the first to show non-selective deposit feeding in the foraminifera Nonionella labradorica and the possible uptake of methanotrophic bacteria. We carried out a feeding experiment with a marine methanotroph to examine the ultrastructure of the cell and degradation vacuoles using transmission electron microscopy (TEM). The results revealed three putative methanotrophs at the outside of the cell/test, which could be taken up via non-targeted grazing in seeps or our experiment.
Inda Brinkmann, Christine Barras, Tom Jilbert, Tomas Næraa, K. Mareike Paul, Magali Schweizer, and Helena L. Filipsson
Biogeosciences, 19, 2523–2535, https://doi.org/10.5194/bg-19-2523-2022, https://doi.org/10.5194/bg-19-2523-2022, 2022
Short summary
Short summary
The concentration of the trace metal barium (Ba) in coastal seawater is a function of continental input, such as riverine discharge. Our geochemical records of the severely hot and dry year 2018, and following wet year 2019, reveal that prolonged drought imprints with exceptionally low Ba concentrations in benthic foraminiferal calcium carbonates of coastal sediments. This highlights the potential of benthic Ba / Ca to trace past climate extremes and variability in coastal marine records.
Julien Richirt, Magali Schweizer, Aurélia Mouret, Sophie Quinchard, Salha A. Saad, Vincent M. P. Bouchet, Christopher M. Wade, and Frans J. Jorissen
J. Micropalaeontol., 40, 61–74, https://doi.org/10.5194/jm-40-61-2021, https://doi.org/10.5194/jm-40-61-2021, 2021
Short summary
Short summary
The study presents (1) a validation of a method which was previously published allowing us to recognize different Ammonia phylotypes (T1, T2 and T6) based only on their morphology and (2) a refined biogeographical distribution presented here supporting the putatively invasive character of phylotype T6. Results suggest that phylotype T6 is currently spreading out and supplanting autochthonous phylotypes T1 and T2 along the coastlines of the British Isles and northern France.
Martijn Hermans, Nils Risgaard-Petersen, Filip J. R. Meysman, and Caroline P. Slomp
Biogeosciences, 17, 5919–5938, https://doi.org/10.5194/bg-17-5919-2020, https://doi.org/10.5194/bg-17-5919-2020, 2020
Short summary
Short summary
This paper demonstrates that the recently discovered cable bacteria are capable of using a mineral, known as siderite, as a source for the formation of iron oxides. This work also demonstrates that the activity of cable bacteria can lead to a distinct subsurface layer in the sediment that can be used as a marker for their activity.
Cited articles
Aller, R. C.:
The Effects of Macrobenthos on Chemical Properties
of Marine Sediment and Overlying Water, in: Animal-Sediment
Relations, edited by: McCall, P. L. and Tevesz, M. J. S., Springer
US, 53–102, 1982.
Aller, R. C.:
The sedimentary Mn cycle in Long Island Sound: Its role as intermediate oxidant and the influence of bioturbation, O2, and Corg flux on diagenetic reaction balances,
J. Mar. Res.,
52, 259–29, 1994.
Aller, R. C., Hall, P. O. J., Rude, P. D., and Aller, J. Y.:
Biogeochemical heterogeneity and suboxic diagenesis in hemipelagic sediments of the Panama Basin,
Deep-Sea Res. Pt. I,
45, 133–165, 1998.
Alve, E. and Goldstein, S. T.:
Propagule transport as a key method of dispersal in benthic foraminifera (Protista),
Limnol. Oceanogr.,
48, 2163–2170, 2003.
Andersen, K., Kjær, T., and Revsbech, N. P.:
An oxygen insensitive microsensor for nitrous oxide,
Sensor. Actuat. B-Chem.,
42–48, 2001.
Arneborg, L.:
Turnover times for the water above sill level in Gullmar Fjord,
Continent. Shelf Res.,
24, 443–460, 2004.
Brandes, J. A., Devol, A. H., and Deutsch, C.:
New Developments in the Marine Nitrogen Cycle,
Chem. Rev.,
107, 577–89, 2007.
Berg, P., Risgaard-Petersen, N., and Rysgaard, S.:
Interpretation of Measured Concentration Profiles in Sediment Pore Water,
Limnol. Oceanogr.,
43, 1500–1510, 1998.
Bernhard, J. M., Ostermann, D. R., Williams, D. S., and Blanks, J. K.:
Comparison of two methods to identify live benthic foraminifera: A test between Rose Bengal and CellTracker Green with implications for stable isotope paleoreconstructions: FORAMINIFERA VIABILITY METHOD COMPARISON,
Paleoceanography,
21, PA4210,
https://doi.org/10.1029/2006PA001290, 2006.
Bernhard, J. M., Edgcomb, V. P., Casciotti, K. L., McIlvin, M. R., and Beaudoin, D. J.:
Denitrification likely catalyzed by endobionts in an allogromiid foraminifer,
ISME J.,
6, 951–960, 2012.
Björk, G. and Nordberg, K.:
Upwelling along the Swedish west coast during the 20th century,
Continent. Shelf Res.,
23, 1143–1159, 2003.
Breitburg, D., Levin, L. A., Oschlies, A., Grégoire, M., Chavez, F. P., Conley, D. J., Garçon, V., Gilbert, D., Gutiérrez, D., Isensee, K., Jacinto, G. S., Limburg, K. E., Montes, I., Naqvi, S. W. A., Pitcher, G. C., Rabalais, N. N., Roman, M. R., Rose, K. A., Seibel, B. A., Telszewski, M., Yasuhara, M., and Zhang, J.:
Declining oxygen in the global ocean and coastal waters,
Science,
359, eaam7240, https://doi.org/10.1126/science.aam7240, 2018.
Carstensen, J., Conley, D., and Müller-Karulis, B.:
Spatial and temporal resolution of carbon fluxes in a shallow coastal ecosystem, the Kattegat,
Mar. Ecol. Prog. Ser.,
252, 35–50, 2003.
Cesbron, F., Metzger, E., Launeau, P., Deflandre, B., Delgard, M.-L., Thibault de Chanvalon, A., Geslin, E., Anschutz, P., and Jézéquel, D.:
Simultaneous 2D Imaging of Dissolved Iron and Reactive Phosphorus in Sediment Porewaters by Thin-Film and Hyperspectral Methods,
Environ. Sci. Technol.,
48, 2816–2826, 2014.
Charrieau, L., Filipsson, H. L., Ljung, K., Chierici, M., Knudsen, K. L., and Kritzberg, E.:
The effects of multiple stressors on the distribution of coastal benthic foraminifera: A case study from the Skagerrak-Baltic Sea region,
Mar. Micropaleontol.,
139 (Supplement C), 42–56, 2018.
Charrieau, L. M., Ljung, K., Schenk, F., Daewel, U., Kritzberg, E., and Filipsson, H. L.: Rapid environmental responses to climate-induced hydrographic changes in the Baltic Sea entrance, Biogeosciences, 16, 3835–3852, https://doi.org/10.5194/bg-16-3835-2019, 2019.
Childs, C. R., Rabalais, N. N., Turner, R. E., and Proctor, L. M.:
Sediment denitrification in the Gulf of Mexico zone of hypoxia,
Mar. Ecol. Prog. Ser., 240, 285–290,
https://doi.org/10.3354/meps240285, 2002.
Christensen, P. B., Rysgaard, S., Sloth, N. P., Dalsgaard, T., and Schwærter, S.:
Sediment mineralization, nutrient fluxes, denitrification and dissimilatory nitrate reduction to ammonium in an estuarine fjord with sea cage trout farms,
Aquat. Microb. Ecol.,
21, 73–84, 2000.
Conley, D. J., Carstensen, J., Ærtebjerg, G., Christensen, P. B., Dalsgaard, T., Hansen, J. L. S., and Josefson, A. B.:
Long-Term Changes and Impacts of Hypoxia in Danish Coastal Waters,
Ecol. Appl.,
17, 165–184, 2007.
Cornwell, J. C., Kemp, W. M., and Kana, T. M.:
Denitrification in coastal ecosystems: methods, environmental controls, and ecosystem level controls, a review,
Aquat. Ecol.,
33, 41–54, 1999.
Dale, A. W., Sommer, S., Lomnitz, U., Bourbonnais, A., and Wallmann, K.:
Biological nitrate transport in sediments on the Peruvian margin mitigates benthic sulfide emissions and drives pelagic N loss during stagnation events,
Deep-Sea Res. Pt. I,
112, 123–136, 2016.
Deldicq, N., Alve, E., Schweizer, M., Asteman, I. P., Hess, S., Darling, K., and Bouchet, V. M. P.:
History of the introduction of a species resembling the benthic foraminifera Nonionella stella in the Oslofjord (Norway): Morphological, molecular and paleo-ecological evidences,
Aquat. Invasions,
14, 182–205, https://doi.org/10.3391/ai.2019.14.2.03, 2019.
Devol, A. H.:
Denitrification including Anammox, Chapter 6,
in: Nitrogen in the Marine Environment,
edited by: Elsevier Inc, 2nd Edn., Oxford, 263–292,
https://doi.org/10.1016/B978-0-12-372522-6.00006-2, 2008.
Diaz, R. J.:
Overview of Hypoxia around the World,
J. Environ. Qual.,
30, 275–281, 2001.
Diaz, R. J. and Rosenberg, R.:
Spreading Dead Zones and Consequences for Marine Ecosystems,
Science,
321, 926–929, 2008.
Engström, P., Dalsgaard, T., Hulth, S., and Aller, R. C.:
Anaerobic ammonium oxidation by nitrite (anammox): Implications for N2 production in coastal marine sediments,
Geochim. Cosmochim. Ac.,
69, 2057–65, 2005.
Filipsson, H. L., and Nordberg, K.:
Climate variations, an overlooked factor influencing the recent marine environment. An example from Gullmar Fjord, Sweden, illustrated by benthic foraminifera and hydrographic data,
Estuaries,
27, 867–881, 2004.
Galloway, J. N., Dentener, F. J., Capone, D. G., Boyer, E. W., Howarth, R. W., Seitzinger, S. P., Asner, G. P., Cleveland, C. C., Green, P. A., Holland, E. A., Karl, D. M., Michaels, A. F., Porter, J. H., Townsend, A. R., and Vöosmarty, C. J.:
Nitrogen Cycles: Past, Present, and Future,
Biogeochemistry,
70, 153–226, 2004.
Geslin, E., Risgaard-Petersen, N., Lombard, F., Metzger, E., Langlet, D., and Jorissen, F.:
Oxygen respiration rates of benthic foraminifera as measured with oxygen microsensors,
J. Exp. Mar. Biol. Ecol.,
396, 108–114, 2011.
Glock, N., Schönfeld, J., Eisenhauer, A., Hensen, C., Mallon, J., and Sommer, S.: The role of benthic foraminifera in the benthic nitrogen cycle of the Peruvian oxygen minimum zone, Biogeosciences, 10, 4767–4783, https://doi.org/10.5194/bg-10-4767-2013, 2013.
Glock, N., Roy, A-S., Romero, D., Wein, T., Weissenbach, J., Revsbech, N. P., Høgslund, S., Clemens, D., Sommer, S., and Dagan, T.:
Metabolic preference of nitrate over oxygen as an electron acceptor in foraminifera from the Peruvian oxygen minimum zone,
P. Natl. Acad. Sci. USA,
116, 2860–2865, 2019.
Goldberg, T., Archer, C., Vance, D., Thamdrup, B., McAnena, A., and Poulton, S. W.:
Controls on Mo isotope fractionations in a Mn-rich anoxic marine sediment, Gullmar Fjord, Sweden,
Chem. Geol.,
296–297, 73–82, 2012.
Gruber, N. and Sarmiento, J. L.:
Global patterns of marine nitrogen fixation and denitrification,
Global Biogeochem. Cy.,
11, 235–266, 1997.
Gustafsson, M. and Nordberg, K.:
Living (stained) benthic foraminiferal response to primary production and hydrography in the deepest part of the Gullmar Fjord, Swedish West Coast, with comparisons to Höglund's 1927 material,
J. Foramin. Res.,
31, 2–11, 2001.
Hannah, F., Rogerson, R., and Laybourn-Parry, J.:
Respiration rates and biovolumes of common benthic Foraminifera (Protozoa),
J. Mar. Biol. Assoc. UK,
74, 301–312, 1994.
Herbert, R. A.:
Nitrogen cycling in coastal marine ecosystems,
FEMS Microbiol. Rev.,
23, 563–590, 1999.
Høgslund, S., Revsbech, N. P., Cedhagen, T., Nielsen, L. P., and Gallardo, V. A.:
Denitrification, nitrate turnover, and aerobic respiration by benthic foraminiferans in the oxygen minimum zone off Chile,
J. Exp. Mar. Biol. Ecol.,
359, 85–91, 2008.
Høgslund, S., Cedhagen, T., Bowser, S., and Risgaard-Petersen, N.:
Sinks and sources of intracellular nitrate in gromiids,
Front. Microbiol.,
8, 617,
https://doi.org/10.3389/fmicb.2017.00617, 2017.
Hulth, S., Aller, R. C., and Gilbert. F.:
Coupled anoxic nitrification/manganese reduction in marine sediments,
Geochim. Cosmochim. Ac.,
63, 49–66, 1999.
Jäntti, H. and Hietanen, S.:
The Effects of Hypoxia on Sediment Nitrogen Cycling in the Baltic Sea,
AMBIO,
41, 161–169, 2012.
Karlson, K., Bonsdorff, E., and Rosenberg, R.:
The Impact of Benthic Macrofauna for Nutrient Fluxes from Baltic Sea Sediments,
AMBIO,
36, 161–167, 2007.
Kamp, A., Høgslund, S., Risgaard-Petersen, N., and Stief, P.:
Nitrate Storage and Dissimilatory Nitrate Reduction by Eukaryotic Microbes,
Front. Microbiol.,
6, 2015.
Kemp, W. M., Sampou, P., Caffrey, J., Mayer, M., Henriksen, K., and Boynton, W. R.:
Ammonium recycling versus denitrification in Chesapeake Bay sediments,
Limnol. Oceanogr.,
35, 1545–1563, 1990.
Kemp, W. M., Boynton, W. R., Adolf, J. E., Boesch, D. F., Boicourt, W. C., Brush, G., Cornwell, J. C., Fisher, T. R., Glibert, P. M., Hagy, J. D., Harding, L. W., Houde, E. D., Kimmel, D. G., Miller, W. D., Newell, R. I. E., Roman, M. R., Smith, E. M., and Stevenson, J. C.:
Eutrophication of Chesapeake Bay: Historical trends and ecological interactions,
Mar. Ecol. Prog. Ser., 303, 1–29, 2005.
Koho, K. A., Piña-Ochoa, E., Geslin, E., and Risgaard-Petersen, N.:
Vertical migration, nitrate uptake and denitrification: survival mechanisms of foraminifers (Globobulimina turgida) under low oxygen conditions,
FEMS Microbiol. Ecol.,
75, 273–283, 2011.
LeKieffre, C., Spangenberg, J. E., Mabilleau, G., Escrig, S., Meibom, A., and Geslin, E.:
Surviving anoxia in marine sediments: The metabolic response of ubiquitous benthic foraminifera (Ammonia tepida),
Plos ONE,
12, e0177604,
https://doi.org/10.1371/journal.pone.0177604, 2017.
Levin, L. A., Ekau, W., Gooday, A. J., Jorissen, F., Middelburg, J. J., Naqvi, S. W. A., Neira, C., Rabalais, N. N., and Zhang, J.: Effects of natural and human-induced hypoxia on coastal benthos, Biogeosciences, 6, 2063–2098, https://doi.org/10.5194/bg-6-2063-2009, 2009.
Lindahl, O. and Hernroth, L.:
Phyto-Zooplankton Community in Coastal Waters of Western Sweden – An Ecosystem Off Balance?,
Mar. Ecol. Prog. Ser.,
10, 119–126, 1983.
Lindahl, O., Belgrano, A., Davidsson, L., and Hernroth, B.:
Primary production, climatic oscillations, and physico-chemical processes: The Gullmar Fjord time-series data set (1985–1996),
ICES J. Mar. Sci.,
55, 723–72, 2003.
Luther, G. W., Sundby, B., Lewis, B. L., Brendel, P. J., and Silverberg, N.:
Interactions of manganese with the nitrogen cycle: Alternative pathways to dinitrogen,
Geochim. Cosmochim. Ac.,
61, 4043–4052, 1997.
Maire, O., Barras, C., Gestin, T., Nardelli, M., Romero-Ramirez, A., Duchêne, J., and Geslin, E.:
How does macrofaunal bioturbation influence the vertical distribution of living benthic foraminifera?,
Mar. Ecol. Prog. Ser.,
561, 83–97, 2016.
Metzger, E., Thibault de Chanvalon, A., Cesbron, F., Barbe, A., Launeau, P., Jézéquel, D., and Mouret, A.:
Simultaneous Nitrite/Nitrate Imagery at Millimeter Scale through the Water–Sediment Interface,
Environ. Sci. Technol.,
50, 8188–8195, https://doi.org/10.1021/acs.est.6b00187, 2016.
Mortimer, R. J. G., Harris, S. J., Krom, M. D., Freitag, T. E., Prosser, J. I., Barnes, J., Anschutz, P., Hayes, P. J., and Davies, I. M.:
Anoxic nitrification in marine sediments,
Mar. Ecol. Prog. Ser.,
276, 37–51, 2004.
Neubacher, E. C., Parker, R. E., and Trimmer, M.:
The potential effect of sustained hypoxia on nitrogen cycling in sediment from the southern North Sea: a mesocosm experiment,
Biogeochemistry,
113, 69–84,
https://doi.org/10.1007/s10533-012-9749-5, 2013.
Nizzoli, D., Bartoli, M., Cooper, M., Welsh, D. T., Underwood, G. J. C., and Viaroli, P.:
Implications for oxygen, nutrient fluxes and denitrification rates during the early stage of sediment colonisation by the polychaete Nereis spp. in four estuaries,
Estuar. Coast. Shelf S.,
75, 125–134, 2007.
Nomaki, H., Chikaraishi, Y., Tsuchiya, M., Toyofuku, T., Suga, H., Sasaki, Y., Uematsu, K., Tame, A., and Ohkouchi, N.:
Variation in the nitrogen isotopic composition of amino acids in benthic foraminifera: Implications for their adaptation to oxygen-depleted environments,
Limnol. Oceanogr.,
60, 1906–1916, 2015.
Nordberg, K.:
Oceanography in the Kattegat and Skagerrak Over the Past 8000 Years,
Paleoceanography,
6, 461–484, 1991.
Nordberg, K., Gustafsson, M., and Krantz, A.-L.:
Decreasing oxygen concentrations in the Gullmar Fjord, Sweden, as confirmed by benthic foraminifera, and the possible association with NAO,
J. Marine Syst.,
23, 303–316, 2000.
Piña-Ochoa, E., Hogslund, S., Geslin, E., Cedhagen, T., Revsbech, N. P., Nielsen, L. P., Schweizer, M., Jorissen, F., Rysgaard, S., and Risgaard-Petersen, N.:
Widespread occurrence of nitrate storage and denitrification among Foraminifera and Gromiida,
P. Natl. Acad. Sci. USA,
107, 1148–1153, 2010.
Polovodova Asteman, I. and Nordberg, K.:
Foraminiferal fauna from a deep basin in Gullmar Fjord: The influence of seasonal hypoxia and North Atlantic Oscillation,
J. Sea Res.,
79, 40–49, 2013.
Polovodova Asteman, I. and Schönfeld, J.:
Recent invasion of the foraminifer Nonionella stella Cushman and Moyer, 1930 in northern European waters: evidence from the Skagerrak and its fjords,
J. Micropalaeontol.,
35, 20–25, 2015.
Polovodova Asteman, I., Filipsson, H. L., and Nordberg, K.: Tracing winter temperatures over the last two millennia using a north-east Atlantic coastal record, Clim. Past, 14, 1097–1118, https://doi.org/10.5194/cp-14-1097-2018, 2018.
Prokopenko, M. G., Sigman, D. M., Berelson, W. M., Hammond, D. E., Barnett, B., Chong, L., and Townsend-Small, A.:
Denitrification in anoxic sediments supported by biological nitrate transport,
Geochim. Cosmochim. Ac.,
75, 7180–7199, 2011.
Rabalais, N. N., Díaz, R. J., Levin, L. A., Turner, R. E., Gilbert, D., and Zhang, J.: Dynamics and distribution of natural and human-caused hypoxia, Biogeosciences, 7, 585–619, https://doi.org/10.5194/bg-7-585-2010, 2010.
Ramsing, N. and Gundersen J.:
Seawater and Gases-Tabulated Physical Parameters
of Interest to People Working with Microsensors in Marine Systems, Version
2.0, Unisense Internal Report, 1994.
Revsbech, N. P.:
An oxygen microsensor with a guard cathode,
Limnol. Oceanogr.,
34, 474–478, 1989.
Risgaard-Petersen, N., Langezaal, A. M., Ingvardsen, S., Schmid, M. C., Jetten, M. S. M., Op den Camp, H. J. M., Derksen, J. W. M., Piña-Ochoa, E., Eriksson, S. P., Peter Nielsen, L., Peter Revsbech, N., Cedhagen, T., and van der Zwaan, G. J.:
Evidence for complete denitrification in a benthic foraminifer,
Nature,
443, 7107, 93–96, 2006.
Ross, B. J. and Hallock, P.:
Dormancy in the Foraminifera: a review,
J. Foramin. Res.,
46, 358–368, 2016.
Rysgaard, S., Risgaard-Petersen N., Sloth N. P., Jensen K., and L. P., Nielsen L. P.:
Oxygen Regulation of Nitrification and Denitrification in Sediments,
Limnol. Oceanogr.,
39, 1643–1652, 1994.
Seitzinger, S. P.:
Denitrification in freshwater and coastal marine ecosystems: Ecological and geochemical significance,
Limnol. Oceanogr.,
33, 702–724, 1988.
Sigman, D. M., Karsh, K. L., and Casciotti, K. L.:
Nitrogen Isotopes in the Ocean,
in: Encyclopedia of Ocean Sciences, Elsevier Ltd., 40–54, https://doi.org/10.1016/B978-012374473-9.00632-9, 2009.
Stachowitsch, M.:
Mass Mortality in the Gulf of Trieste: The Course of Community Destruction,
Mar. Ecol.,
5, 243–264, 1984.
Stief, P.: Stimulation of microbial nitrogen cycling in aquatic ecosystems by benthic macrofauna: mechanisms and environmental implications, Biogeosciences, 10, 7829–7846, https://doi.org/10.5194/bg-10-7829-2013, 2013.
Stockdale, A., Davison, W., and Zhang, H.:
Micro-scale biogeochemical heterogeneity in sediments: A review of available technology and observed evidence,
Earth-Sci. Rev.,
92, 81–97, 2009.
Svansson, A.:
Physical and chemical oceanography of the Skagerrak and the Kattegat, Report No. 1,
Institute of Marine Research, Göteborgs universitet, 1975.
Svansson, A.:
Hydrography of the Gullmar fjord, Meddelande fran Havsfiskelaboratoriet, Lysekil, 23, 22 pp., 1984.
Swedish Meteorological and Hydrological Institute's (SMHI):
Svenskt HavsARKivs webbplats (SHARKweb),
https://sharkweb.smhi.se/ (last access: 13 July 2020), 2020.
Thamdrup, B. and Dalsgaard, T.:
Microbial Ecology of the Oceans,
John Wiley and Sons, Ltd, Hoboken, NJ 07030, USA, 2008.
Woehle, C., Roy, A-S., Glock, N., Wein, T., Weissenbach, J., Rosenstiel, P., Hiebenthal, C., Michels, J., Schönfeld, J., and Dagan, T.:
A Novel Eukaryotic Denitrification Pathway in Foraminifera,
Curr. Biol., 28, 1–8,
https://doi.org/10.1016/j.cub.2018.06.027, 2018.
Xu, Z., Liu, S., Xiang, R., and Song, G.:
Live benthic foraminifera in the Yellow Sea and the East China Sea: vertical distribution, nitrate storage, and potential denitrification,
Mar. Ecol. Prog. Ser.,
571, 65–81, 2017.
Zhang, J., Gilbert, D., Gooday, A. J., Levin, L., Naqvi, S. W. A., Middelburg, J. J., Scranton, M., Ekau, W., Peña, A., Dewitte, B., Oguz, T., Monteiro, P. M. S., Urban, E., Rabalais, N. N., Ittekkot, V., Kemp, W. M., Ulloa, O., Elmgren, R., Escobar-Briones, E., and Van der Plas, A. K.: Natural and human-induced hypoxia and consequences for coastal areas: synthesis and future development, Biogeosciences, 7, 1443–1467, https://doi.org/10.5194/bg-7-1443-2010, 2010.
Short summary
Marine microorganisms such as foraminifera are able to live temporarily without oxygen in sediments. In a Swedish fjord subjected to seasonal oxygen scarcity, a change in fauna linked to the decrease in oxygen and the increase in an invasive species was shown. The invasive species respire nitrate until 100 % of the nitrate porewater in the sediment and could be a major contributor to nitrogen balance in oxic coastal ecosystems. But prolonged hypoxia creates unfavorable conditions to survive.
Marine microorganisms such as foraminifera are able to live temporarily without oxygen in...
Altmetrics
Final-revised paper
Preprint