Articles | Volume 20, issue 16
https://doi.org/10.5194/bg-20-3423-2023
© Author(s) 2023. 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-20-3423-2023
© Author(s) 2023. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Reviews and syntheses
| 
17 Aug 2023
Reviews and syntheses |
| 17 Aug 2023
| 17 Aug 2023
Benthic foraminifera and gromiids from oxygen-depleted environments – survival strategies, biogeochemistry and trophic interactions
Nicolaas Glock
CORRESPONDING AUTHOR
Institute for Geology, University of Hamburg, Bundesstraße 55,
20146 Hamburg, Germany
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This article is included in the Encyclopedia of Geosciences
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Benthic organisms show aggregated distributions due to the spatial heterogeneity of niches or food. We analysed the distribution of Globobulimina turgida in the Gullmar Fjord, Sweden, with a data–model approach. The population densities did not show any underlying spatial structure but a random log-normal distribution. A temporal data series from the same site depicted two cohorts of samples with high or low densities, which represent hypoxic or well-ventilated conditions in the fjord.
This article is included in the Encyclopedia of Geosciences
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The project "Climate-Biogeochemistry Interactions in the Tropical Ocean" (SFB 754) was a multidisciplinary research project active from 2008 to 2019 aimed at a better understanding of the coupling between the tropical climate and ocean circulation and the ocean's oxygen and nutrient balance. On 34 research cruises, mainly in the Southeast Tropical Pacific and the Northeast Tropical Atlantic, 1071 physical, chemical and biological data sets were collected.
This article is included in the Encyclopedia of Geosciences
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Recent observations from today’s oceans revealed that oxygen concentrations are decreasing, and oxygen minimum zones are expanding together with current climate change. With the aim of understanding past climatic events and their relationship with oxygen content, we looked at the fossils, called benthic foraminifera, preserved in the sediment archives from the Peruvian margin and quantified the bottom-water oxygen content for the last 22 000 years.
This article is included in the Encyclopedia of Geosciences
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Today’s oceans show distinct mid-depth oxygen minima while whole oceanic basins became transiently anoxic in the Mesozoic. To constrain past bottom-water oxygenation, we compared sediments from the Peruvian OMZ with the Cenomanian OAE 2 from Morocco. Corg accumulation rates in laminated OAE 2 sections match Holocene rates off Peru. Laminated deposits are found at oxygen levels of < 7µmol kg-1; crab burrows appear at 10µmol kg-1 today, both defining threshold values for palaeoreconstructions.
This article is included in the Encyclopedia of Geosciences
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Our study explores the correlation of I/Ca ratios in four benthic foraminiferal species (three calcitic, one aragonitic) from the Peruvian OMZ with bottom water oxygenation ([O2]BW), and evaluates foraminiferal I/Ca ratios as a possible redox proxy. All species have a positive trend in the I/Ca ratios as a function of [O2]BW. Only for the aragonitic species Hoeglundina elegans is this trend not significant. The highest significance has been found for Uvigerina striata.
This article is included in the Encyclopedia of Geosciences
N. Glock, J. Schönfeld, A. Eisenhauer, C. Hensen, J. Mallon, and S. Sommer
Biogeosciences, 10, 4767–4783, https://doi.org/10.5194/bg-10-4767-2013, https://doi.org/10.5194/bg-10-4767-2013, 2013
Babette Hoogakker, Catherine Davis, Yi Wang, Stepanie Kusch, Katrina Nilsson-Kerr, Dalton Hardisty, Allison Jacobel, Dharma Reyes Macaya, Nicolaas Glock, Sha Ni, Julio Sepúlveda, Abby Ren, Alexandra Auderset, Anya Hess, Katrina Meissner, Jorge Cardich, Robert Anderson, Christine Barras, Chandranath Basak, Harold Bradbury, Inda Brinkmann, Alexis Castillo, Madelyn Cook, Kassandra Costa, Constance Choquel, Paula Diz, Jonas Donnenfield, Felix Elling, Zeynep Erdem, Helena Filipsson, Sebastian Garrido, Julia Gottschalk, Anjaly Govindankutty Menon, Jeroen Groeneveld, Christian Hallman, Ingrid Hendy, Rick Hennekam, Wanyi Lu, Jean Lynch-Stieglitz, Lelia Matos, Alfredo Martínez-García, Giulia Molina, Práxedes Muñoz, Simone Moretti, Jennifer Morford, Sophie Nuber, Svetlana Radionovskaya, Morgan Raven, Christopher Somes, Anja Studer, Kazuyo Tachikawa, Raúl Tapia, Martin Tetard, Tyler Vollmer, Shuzhuang Wu, Yan Zhang, Xin-Yuan Zheng, and Yuxin Zhou
EGUsphere, https://doi.org/10.5194/egusphere-2023-2981, https://doi.org/10.5194/egusphere-2023-2981, 2024
Short summary
Short summary
Paleo-oxygen proxies can extend current records, bound 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.
This article is included in the Encyclopedia of Geosciences
Joachim Schönfeld, Nicolaas Glock, Irina Polovodova Asteman, Alexandra-Sophie Roy, Marié Warren, Julia Weissenbach, and Julia Wukovits
J. Micropalaeontol., 42, 171–192, https://doi.org/10.5194/jm-42-171-2023, https://doi.org/10.5194/jm-42-171-2023, 2023
Short summary
Short summary
Benthic organisms show aggregated distributions due to the spatial heterogeneity of niches or food. We analysed the distribution of Globobulimina turgida in the Gullmar Fjord, Sweden, with a data–model approach. The population densities did not show any underlying spatial structure but a random log-normal distribution. A temporal data series from the same site depicted two cohorts of samples with high or low densities, which represent hypoxic or well-ventilated conditions in the fjord.
This article is included in the Encyclopedia of Geosciences
Gerd Krahmann, Damian L. Arévalo-Martínez, Andrew W. Dale, Marcus Dengler, Anja Engel, Nicolaas Glock, Patricia Grasse, Johannes Hahn, Helena Hauss, Mark Hopwood, Rainer Kiko, Alexandra Loginova, Carolin R. Löscher, Marie Maßmig, Alexandra-Sophie Roy, Renato Salvatteci, Stefan Sommer, Toste Tanhua, and Hela Mehrtens
Earth Syst. Sci. Data Discuss., https://doi.org/10.5194/essd-2020-308, https://doi.org/10.5194/essd-2020-308, 2021
Preprint withdrawn
Short summary
Short summary
The project "Climate-Biogeochemistry Interactions in the Tropical Ocean" (SFB 754) was a multidisciplinary research project active from 2008 to 2019 aimed at a better understanding of the coupling between the tropical climate and ocean circulation and the ocean's oxygen and nutrient balance. On 34 research cruises, mainly in the Southeast Tropical Pacific and the Northeast Tropical Atlantic, 1071 physical, chemical and biological data sets were collected.
This article is included in the Encyclopedia of Geosciences
Zeynep Erdem, Joachim Schönfeld, Anthony E. Rathburn, Maria-Elena Pérez, Jorge Cardich, and Nicolaas Glock
Biogeosciences, 17, 3165–3182, https://doi.org/10.5194/bg-17-3165-2020, https://doi.org/10.5194/bg-17-3165-2020, 2020
Short summary
Short summary
Recent observations from today’s oceans revealed that oxygen concentrations are decreasing, and oxygen minimum zones are expanding together with current climate change. With the aim of understanding past climatic events and their relationship with oxygen content, we looked at the fossils, called benthic foraminifera, preserved in the sediment archives from the Peruvian margin and quantified the bottom-water oxygen content for the last 22 000 years.
This article is included in the Encyclopedia of Geosciences
J. Schönfeld, W. Kuhnt, Z. Erdem, S. Flögel, N. Glock, M. Aquit, M. Frank, and A. Holbourn
Biogeosciences, 12, 1169–1189, https://doi.org/10.5194/bg-12-1169-2015, https://doi.org/10.5194/bg-12-1169-2015, 2015
Short summary
Short summary
Today’s oceans show distinct mid-depth oxygen minima while whole oceanic basins became transiently anoxic in the Mesozoic. To constrain past bottom-water oxygenation, we compared sediments from the Peruvian OMZ with the Cenomanian OAE 2 from Morocco. Corg accumulation rates in laminated OAE 2 sections match Holocene rates off Peru. Laminated deposits are found at oxygen levels of < 7µmol kg-1; crab burrows appear at 10µmol kg-1 today, both defining threshold values for palaeoreconstructions.
This article is included in the Encyclopedia of Geosciences
N. Glock, V. Liebetrau, and A. Eisenhauer
Biogeosciences, 11, 7077–7095, https://doi.org/10.5194/bg-11-7077-2014, https://doi.org/10.5194/bg-11-7077-2014, 2014
Short summary
Short summary
Our study explores the correlation of I/Ca ratios in four benthic foraminiferal species (three calcitic, one aragonitic) from the Peruvian OMZ with bottom water oxygenation ([O2]BW), and evaluates foraminiferal I/Ca ratios as a possible redox proxy. All species have a positive trend in the I/Ca ratios as a function of [O2]BW. Only for the aragonitic species Hoeglundina elegans is this trend not significant. The highest significance has been found for Uvigerina striata.
This article is included in the Encyclopedia of Geosciences
N. Glock, J. Schönfeld, A. Eisenhauer, C. Hensen, J. Mallon, and S. Sommer
Biogeosciences, 10, 4767–4783, https://doi.org/10.5194/bg-10-4767-2013, https://doi.org/10.5194/bg-10-4767-2013, 2013
Cited articles
Alve, E. and Murray, J.: Temporal variability in vertical distributions of
live (stained) intertidal foraminifera, Southern England, J. Foramin. Res., 31, 12–24, https://doi.org/10.2113/0310012, 2001.
Austin, H. A., Austin, W. E. N., and Paterson, D. M.: Extracellular cracking
and content removal of the benthic diatom Pleurosigma angulatum (Quekett) by the benthic
foraminifera Haynesina germanica (Ehrenberg), Mar. Micropaleontol., 57, 68–73,
https://doi.org/10.1016/J.MARMICRO.2005.07.002, 2005.
Auten, R. L. and Davis, J. M.: Oxygen toxicity and reactive oxygen species:
The devil is in the details, Pediatr. Res., 66, 121–127,
https://doi.org/10.1203/PDR.0b013e3181a9eafb, 2009.
Barras, C., Mouret, A., Nardelli, M. P., Metzger, E., Petersen, J., La, C.,
Filipsson, H. L., and Jorissen, F.: Experimental calibration of manganese
incorporation in foraminiferal calcite, Geochim. Cosmochim. Ac., 237,
49–64, https://doi.org/10.1016/j.gca.2018.06.009, 2018.
Bernhard, J. M.: Characteristic assemblages and morphologies of benthic
foraminifera from anoxic, organic-rich deposits; Jurassic through Holocene,
J. Foraminifer. Res., 16, 207–215, https://doi.org/10.2113/GSJFR.16.3.207,
1986.
Bernhard, J. M.: Potential Symbionts in Bathyal Foraminifera, Science, 299, p. 861, https://doi.org/10.1126/science.1077314, 2003.
Bernhard, J. M. and Alve, E.: Survival, ATP pool, and ultrastructural
characterization of benthic foraminifera from Drammensfjord (Norway):
response to anoxia, Mar. Micropaleontol., 28, 5–17,
https://doi.org/10.1016/0377-8398(95)00036-4, 1996.
Bernhard, J. M. and Bowser, S. S.: Benthic foraminifera of dysoxic
sediments: chloroplast sequestration and functional morphology,
Earth-Sci. Rev., 46, 149–165,
https://doi.org/10.1016/S0012-8252(99)00017-3, 1999.
Bernhard, J. M. and Sen Gupta, B. K.: Foraminifera of oxygen-depleted
environments, Mod. Foraminifera, 201–216,
https://doi.org/10.1007/0-306-48104-9_ 12, 1999.
Bernhard, J. M. and Bowser, S. S.: Peroxisome proliferation in foraminifera
inhabiting the chemocline: An adaptation to reactive oxygen species
https://doi.org/10.1111/j.1550-7408.2008.00318.x, 2008.
Bernhard, J. M., Sen Gupta, B. K., and Borne, P. F.: Benthic foraminiferal
proxy to estimate dysoxic bottom-water oxygen concentrations; Santa Barbara
Basin, U.S. Pacific continental margin, J. Foraminifer. Res., 27, 301–310,
https://doi.org/10.2113/GSJFR.27.4.301, 1997.
Bernhard, J. M., Buck, K. R., Farmer, M. A., and Bowser, S. S.: The Santa
Barbara Basin is a symbiosis oasis, Nature, 403, 77–80, https://doi.org/10.1038/47476, 2000.
Bernhard, J. M., Buck, K. R., and Barry, J. P.: Monterey Bay cold-seep
biota: Assemblages, abundance, and ultrastructure of living foraminifera,
Deep. Res. Pt. I, 48, 2233–2249, 2001.
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, Paleoceanography, 21,
https://doi.org/10.1029/2006PA001290, 2006.
Bernhard, J. M., Goldstein, S. T., and Bowser, S. S.: An ectobiont-bearing
foraminiferan, Bolivina pacifica, that inhabits microxic pore waters: cell-biological and
paleoceanographic insights, Environ. Microbiol., 12, 2107–2119,
https://doi.org/10.1111/j.1462-2920.2009.02073.x, 2010a.
Bernhard, J. M., Martin, J. B., and Rathburn, A. E.: Combined carbonate
carbon isotopic and cellular ultrastructural studies of individual benthic
foraminifera: 2. Toward an understanding of apparent disequilibrium in
hydrocarbon seeps, Paleoceanography, 25,
https://doi.org/10.1029/2010PA001930, 2010b.
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, 951–60,
https://doi.org/10.1038/ismej.2011.171, 2012a.
Bernhard, J. M., Casciotti, K. L., Mcilvin, M. R., Beaudoin, D. J.,
Visscher, P. T., and Edgcomb, V. P.: Potential importance of physiologically
diverse benthic foraminifera in sedimentary nitrate storage and respiration,
117, 1–14, https://doi.org/10.1029/2012JG001949, 2012b.
Bernhard, J. M., Tsuchiya, M., and Nomaki, H.: Ultrastructural observations
on prokaryotic associates of benthic foraminifera: Food, mutualistic
symbionts, or parasites?, Mar. Micropaleontol., 138, 33–45,
https://doi.org/10.1016/j.marmicro.2017.09.001, 2018.
Bowser, S. S., Delaca, T. E., and Rieder, C. L.: Novel extracellular matrix
and microtubule cables associated with pseudopodia of Astrammina rara, a carnivorous
antarctic foraminifer, J. Ultrastruct. Mol. Struct. Res., 94, 149–160,
https://doi.org/10.1016/0889-1605(86)90061-3, 1986.
Bowser, S. S., Alexander, S. P., Stockton, W. L., and Delaca, T. E.:
Extracellular matrix augments mechanical properties of pseudopodia in the
carnivorous foraminiferan Astrammina rara: Role in prey capture, J. Protozool., 39,
724–732,
https://doi.org/10.1111/j.1550-7408.1992.tb04455.x, 1992.
Brinkmann, I., Ni, S., Schweizer, M., Oldham, V. E., Quintana Krupinski, N.
B., Medjoubi, K., Somogyi, A., Whitehouse, M. J., Hansel, C. M., Barras, C.,
Bernhard, J. M., and Filipsson, H. L.: Foraminiferal
Cato, I., Olsson, I., and Rosenberg, R.: Recovery and decontamination of
estuaries, in: Chemistry and Biogeochemistry of Estuaries, edited by:
Olausson, E. and Cato, I., Wiley, London, 403–440, 1980.
Cedhagen, T.: Retention of chloroplasts and bathymetric distribution in the
sublittoral foraminiferan Nonionellina labradorica, Ophelia, 33, 17–30,
https://doi.org/10.1080/00785326.1991.10429739, 1991.
Cesbron, F., Geslin, E., Le Kieffre, C., Jauffrais, T., Nardelli, M. P.,
Langlet, D., Mabilleau, G., Jorissen, F. J., Jézéquel, D., and
Metzger, E.: Sequestered chloroplasts in the benthic foraminifer Haynesina germanica: Cellular
organization, oxygen fluxes and potential ecological implications, J.
Foraminifer. Res., 47, 268–278, 2017.
Cevasco, M. E., Lechliter, S. M., Mosier, A. E., and Perez, J.: Initial
observations of kleptoplasty in the foraminifera of Coastal South Carolina,
Naturalist, 14, 361–372, https://doi.org/10.2307/26454495, 2015.
Choquel, C., Geslin, E., Metzger, E., Filipsson, H. L., Risgaard-Petersen, N., Launeau, P., Giraud, M., Jauffrais, T., Jesus, B., and Mouret, A.: Denitrification by benthic foraminifera and their contribution to N-loss from a fjord environment, Biogeosciences, 18, 327–341, https://doi.org/10.5194/bg-18-327-2021, 2021.
Clark, K., Jensen, K., and Stirts, H.: Survey for functional kleptoplasty
among West Atlantic Ascoglossa (= Sacoglossa) (Mollusca: Opisthobranchia),
Veliger, 334, 339–345, 1990.
Cook, M. K., Dial, A. R., and Hendy, I. L.: Iodine stability as a function
of pH and its implications for simultaneous multi-element ICP-MS analysis of
marine carbonates for paleoenvironmental reconstructions, Mar. Chem., 245,
104148, https://doi.org/10.1016/J.MARCHEM.2022.104148, 2022.
Corliss, B. H.: Microhabitats of benthic foraminifera within deep-sea
sediments, Nature, 314, 435–438,
https://doi.org/10.1038/314435a0, 1985.
Corliss, B. H.: Morphology and microhabitat preferences of benthic
foraminifera from the northwest Atlantic Ocean, Mar. Micropaleontol., 17,
195–236, https://doi.org/10.1016/0377-8398(91)90014-W, 1991.
Corliss, B. H. and Chen, C.: Morphotype patterns of Norwegian Sea deep-sea
benthic foraminifera and ecological implications, Geology, 16, 716–719,
https://doi.org/10.1130/0091-7613(1988)016< 0716:MPONSD>2.3.CO;2, 1988.
Correia, M. J. and Lee, J. J.: Chloroplast retention by Elphidium excavatum (Terquem). Is it a
selective process?, Symbiosis, 29, 343–355, 2000.
Correia, M. J. and Lee, J. J.: Fine structure of the plastids retained by
the foraminifer Elphidium excavatum (Terquem), Symbiosis, 32, 15–26, 2002a.
Correia, M. J. and Lee, J. J.: How long do the plastids retained by
Elphidium excavatum (Terquem) last in their host?, Symbiosis, 32, 27–38, 2002b.
Costa, K. M., Nielsen, S. G., Wang, Y., Lu, W., Hines, S. K. V, Jacobel, A.
W., and Oppo, D. W.: Marine sedimentary uranium to barium ratios as a
potential quantitative proxy for Pleistocene bottom water oxygen
concentrations, Geochim. Cosmochim. Ac., 343, 1–16,
https://doi.org/10.1016/j.gca.2022.12.022, 2023.
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,
https://doi.org/10.1016/j.dsr.2016.02.013, 2016.
Dalsgaard, T., Frank, S. J., Thamdrup, B., De Brabandere, L., Revsbech, N.
P., Ulloa, O., Canfield, D. E., and DeLong, E. F.: Oxygen at nanomolar
levels reversibly suppresses process rates and gene expression in anammox
and denitrification in the oxygen minimum Zone off Northern Chile, MBio, 5,
e01966-14, https://doi.org/10.1128/mBio.01966-14, 2014.
Davis, C. V., Wishner, K., Renema, W., and Hull, P. M.: Vertical distribution of planktic foraminifera through an oxygen minimum zone: how assemblages and test morphology reflect oxygen concentrations, Biogeosciences, 18, 977–992, https://doi.org/10.5194/bg-18-977-2021, 2021.
Davis, C. V., Sibert, E. C., Jacobs, P. H., Burls, N., and Hull, P. M.:
Intermediate water circulation drives distribution of Pliocene Oxygen
Minimum Zones, Nat. Commun., 14, 1–11,
https://doi.org/10.1038/s41467-022-35083-x, 2023.
de Freitas, T. R., Bacalhau, E. T., and Disaró, S. T.: Biovolume method
for foraminiferal biomass assessment: Evaluation of geometric models and
incorporation of species mean cell occupancy, J. Foraminifer. Res., 51,
249–266, https://doi.org/10.2113/GSJFR.51.4.249, 2021.
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.
Diaz, R. J.: Anoxia, hypoxia, and dead zones BT – Encyclopedia of Estuaries,
edited by: Kennish, M. J., Springer Netherlands, Dordrecht, 19–29,
https://doi.org/10.1007/978-94-017-8801-4_ 82, 2016.
Duijnstee, I. A. P., Ernst, S. R., and Van Der Zwaan, G. J.: Effect of
anoxia on the vertical migration of benthic foraminifera, Mar. Ecol. Prog.
Ser., 246, 85–94, https://doi.org/10.3354/MEPS246085, 2003.
Dupuy, C., Rossignol, L., Geslin, E., and Pascal, P. Y.: Predation of
mudflat meio-macrofaunal metazoans by a calcareous foraminifer, Ammonia tepida (Cushman,
1926), J. Foraminifer. Res., 40, 305–312,
https://doi.org/10.2113/GSJFR.40.4.305, 2010.
Enge, A. J., Witte, U., Kucera, M., and Heinz, P.: Uptake of phytodetritus by benthic foraminifera under oxygen depletion at the Indian margin (Arabian Sea), Biogeosciences, 11, 2017–2026, https://doi.org/10.5194/bg-11-2017-2014, 2014.
Enge, A. J., Wukovits, J., Wanek, W., Watzka, M., Witte, U. F. M., Hunter, W. R., and Heinz, P.: Carbon and Nitrogen Uptake of Calcareous Benthic Foraminifera along a Depth-Related Oxygen Gradient in the OMZ of the Arabian Sea, Sec. Aquatic Microbiology, 7, https://doi.org/10.3389/fmicb.2016.00071, 2016.
Erdem, Z. and Schönfeld, J.: Pleistocene to Holocene benthic
foraminiferal assemblages from the Peruvian continental margin, Palaeontol.
Electron., 1–32, https://doi.org/10.26879/764, 2017.
Erez, J.: The source of ions for biomineralization in foraminifera and their
implications for paleoceanographic proxies, Rev. Mineral. Geochem., 54,
115–149, https://doi.org/10.2113/0540115, 2003.
Ettwig, K. F., Speth, D. R., Reimann, J., Wu, M. L., Jetten, M. S. M., and
Keltjens, J. T.: Bacterial oxygen production in the dark, Front. Microbiol.,
3, 273, https://doi.org/10.3389/FMICB.2012.00273/BIBTEX, 2012.
Fenchel, T. M. and Finlay, B. J.: Ecology and evolution in anoxic worlds,
edited by: Fenchel, T. M. and Finlay, B. J., Oxford University Press Inc.,
Oxford, ISBN 0198548389, 1995.
Finlay, B. J., Span, A. S. W., and Harman, J. M. P.: Nitrate respiration in
primitive eukaryotes, Nature, 303, 333–336,
https://doi.org/10.1038/303333a0, 1983.
Frank, L. and Massaro, D.: Oxygen toxicity, Am. J. Med., 69, 117–126,
https://doi.org/10.1016/0002-9343(80)90509-4, 1980.
Glock, N., Eisenhauer, A., Milker, Y., Liebetrau, V., Schonfeld, J., Mallon,
J., Sommer, S., and Hensen, C.: Evironmental influences on the pore density
of Bolivina spissa (Cushman), J. Foraminifer. Res., 41, 22–32,
https://doi.org/10.2113/gsjfr.41.1.22, 2011.
Glock, N., Erdem, Z., Wallmann, K., Somes, C. J., Liebetrau, V.,
Schönfeld, J., Gorb, S., and Eisenhauer, A.: Coupling of oceanic carbon
and nitrogen facilitates spatially resolved quantitative reconstruction of
nitrate inventories, Nat. Commun., 9, 1217,
https://doi.org/10.1038/s41467-018-03647-5, 2018.
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., Wukovits, J., and Roy, A.-S.: Interactions of Globobulimina auriculata with nematodes:
predator or prey?, J. Foraminifer. Res., 49, 66–75,
https://doi.org/10.2113/gsjfr.49.1.66, 2019a.
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, https://doi.org/10.1073/pnas.1813887116, 2019b.
Glock, N., Liebetrau, V., Vogts, A., and Eisenhauer, A.: Organic
heterogeneities in foraminiferal calcite traced through the distribution of
N, S, and I measured with NanoSIMS: A new challenge for element-ratio-based
paleoproxies?, Front. Earth Sci., 7, 175,
https://doi.org/10.3389/feart.2019.00175, 2019c.
Glock, N., Romero, D., Roy, A. S., Woehle, C., Dale, A. W., Schönfeld,
J., Wein, T., Weissenbach, J., and Dagan, T.: A hidden sedimentary phosphate
pool inside benthic foraminifera from the Peruvian upwelling region might
nucleate phosphogenesis, Geochim. Cosmochim. Ac., 289, 14–32,
https://doi.org/10.1016/j.gca.2020.08.002, 2020.
Glock, N., Erdem, Z., and Schönfeld, J.: The Peruvian oxygen minimum
zone was similar in extent but weaker during the Last Glacial Maximum than
Late Holocene, Commun. Earth Environ., 3, 1–14,
https://doi.org/10.1038/s43247-022-00635-y, 2022.
Glud, R. N., Wenzhöfer, F., Tengberg, A., Middelboe, M., Oguri, K., and
Kitazato, H.: Distribution of oxygen in surface sediments from central
Sagami Bay, Japan: In situ measurements by microelectrodes and planar
optodes, Deep. Sea Res. Pt. I, 52, 1974–1987,
https://doi.org/10.1016/J.DSR.2005.05.004, 2005.
Glud, R. N., Thamdrup, B., Stahl, H., Wenzhoefer, F., Glud, A., Nomaki, H.,
Oguri, K., Revsbech, N. P., and Kitazato, H.: Nitrogen cycling in a deep
ocean margin sediment (Sagami Bay, Japan), Limnol. Oceanogr., 54, 723–734,
https://doi.org/10.4319/lo.2009.54.3.0723, 2009.
Goldstein, S. T. and Richardson, E. A.: Fine structure of the foraminifer
Haynesina germanica (Ehrenberg) and its sequestered chloroplasts, Mar.
Micropaleontol., 138, 63–71,
https://doi.org/10.1016/J.MARMICRO.2017.10.010, 2018.
Goldstein, S. T., Bernhard, J. M., and Richardson, E. A.: Chloroplast
sequestration in the foraminifer Haynesina germanica: Application of high pressure freezing and
freeze substitution, Microsc. Microanal., 10, 1458–1459,
https://doi.org/10.1017/S1431927604885891, 2004.
Gomaa, F., Utter, D. R., Powers, C., Beaudoin, D. J., Edgcomb, V. P.,
Filipsson, H. L., Hansel, C. M., Wankel, S. D., Zhang, Y., and Bernhard, J.
M.: Multiple integrated metabolic strategies allow foraminiferan protists to
thrive in anoxic marine sediments, Sci. Adv., 7, eabf1586,
https://doi.org/10.1126/sciadv.abf1586, 2021.
Gooday, A. J., Levin, L. A., Linke, P., and Heeger, T.: The Role of Benthic
Foraminifera in Deep-Sea Food Webs and Carbon Cycling BT – Deep-sea food
chains and the global carbon cycle, edited by: Rowe, G. T. and Pariente, V.,
Springer Netherlands, Dordrecht, 63–91,
https://doi.org/10.1007/978-94-011-2452-2_ 5, 1992.
Gooday, A. J., Nomaki, H., and Kitazato, H.: Modern deep-sea benthic
foraminifera: a brief review of their morphology-based biodiversity and
trophic diversity, Geol. Soc. Spec. Publ., 303, 97–119,
https://doi.org/10.1144/SP303.8, 2008.
Grzymski, J., Schofield, O. M., Falkowski, P. G., and Bernhard, J. M.: The
function of plastids in the deep-sea benthic foraminifer, Nonionella stella, Limnol.
Oceanogr., 47, 1569–1580, https://doi.org/10.4319/LO.2002.47.6.1569, 2002.
Hallock, P. and Talge, H. K.: A predatory foraminifer, Floresina amphiphaga, n. sp., from the
Florida Keys, J. Foraminifer. Res., 24, 210–213,
https://doi.org/10.2113/GSJFR.24.4.210, 1994.
Hannah, F. and Rogerson, A.: The temporal and spatial distribution of
foraminiferans in marine benthic sediments of the Clyde Sea Area, Scotland,
Estuar. Coast. Shelf Sci., 44, 377–383,
https://doi.org/10.1006/ECSS.1996.0136, 1997.
Harman, R. A.: Distribution of foraminifera in the Santa Barbara Basin,
California, Micropaleontology, 10, 81–96, https://doi.org/10.2307/1484628,
1964.
Hayward, B., Holzmann, M., Pawlowski, J., Parker, J., Kaushik, T., Toyofuku,
M., and Tsuchiya, M.: Molecular and morphological taxonomy of living
Ammonia and related taxa (Foraminifera) and their biogeography, Micropaleontology,
67, 109–313, https://doi.org/10.47894/mpal.67.2-3.01, 2021.
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.
Bio. Ecol., 359, 85–91, https://doi.org/10.1016/j.jembe.2008.02.015, 2008.
Høgslund, S., Cedhagen, T., Bowser, S. 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.
Hoogakker, B. and the PLO2P-Team: Review of proxies for low-oxygen paleo reconstructions, ID# 1273324, presented at AGU23, San Francisco CA, 11–15 Deember 2023.
Hoogakker, B. A. A., Elderfield, H., Schmiedl, G., McCave, I. N., and
Rickaby, R. E. M.: Glacial–interglacial changes in bottom-water oxygen
content on the Portuguese margin, Nat. Geosci., 8, 40–43,
https://doi.org/10.1038/ngeo2317, 2014.
Hoogakker, B. A. A., Lu, Z., Umling, N., Jones, L., Zhou, X., Rickaby, R. E.
M., Thunell, R., Cartapanis, O., and Galbraith, E.: Glacial expansion of
oxygen-depleted seawater in the eastern tropical Pacific, Nature, 562,
410–413, https://doi.org/10.1038/s41586-018-0589-x, 2018a.
Hoogakker, B. A. A., Lu, Z., Umling, N., Jones, L., and Zhou, X.: Glacial
expansion of oxygen-depleted seawater in the eastern tropical Pacific, Nature, 562, 410–413,
https://doi.org/10.1038/s41586-018-0589-x, 2018b.
Jansen, S., Walpersdorf, E., Werner, U., Billerbeck, M., Böttcher, M.
E., De Beer, D., Jansen, S., Walpersdorf, E., Werner, : U, Billerbeck, : M,
Böttcher, M. E., De Beer, D., Werner, U., and Billerbeck, M.:
Functioning of intertidal flats inferred from temporal and spatial dynamics
of O2, H2S and pH in their surface sediment, Ocean Dynam.,
59, 317–332, https://doi.org/10.1007/S10236-009-0179-4, 2009.
Jauffrais, T., Jesus, B., Metzger, E., Mouget, J.-L., Jorissen, F., and Geslin, E.: Effect of light on photosynthetic efficiency of sequestered chloroplasts in intertidal benthic foraminifera (Haynesina germanica and Ammonia tepida), Biogeosciences, 13, 2715–2726, https://doi.org/10.5194/bg-13-2715-2016, 2016.
Jauffrais, T., Jesus, B., Méléder, V., and Geslin, E.: Functional
xanthophyll cycle and pigment content of a kleptoplastic benthic
foraminifer: Haynesina germanica, PLoS One, 12, e0172678,
https://doi.org/10.1371/JOURNAL.PONE.0172678, 2017.
Jauffrais, T., LeKieffre, C., Koho, K. A., Tsuchiya, M., Schweizer, M.,
Bernhard, J. M., Meibom, A., and Geslin, E.: Ultrastructure and distribution
of kleptoplasts in benthic foraminifera from shallow-water (photic)
habitats, Mar. Micropaleontol., 138, 46–62,
https://doi.org/10.1016/J.MARMICRO.2017.10.003, 2018.
Jauffrais, T., LeKieffre, C., Schweizer, M., Geslin, E., Metzger, E.,
Bernhard, J. M., Jesus, B., Filipsson, H. L., Maire, O., and Meibom, A.:
Kleptoplastidic benthic foraminifera from aphotic habitats: insights into
assimilation of inorganic C, N and S studied with sub-cellular resolution,
Environ. Microbiol., 21, 125–141, https://doi.org/10.1111/1462-2920.14433,
2019.
Jesus, B., Jauffrais, T., Trampe, E. C. L., Goessling, J. W., Lekieffre, C.,
Meibom, A., Kühl, M., and Geslin, E.: Kleptoplast distribution,
photosynthetic efficiency and sequestration mechanisms in intertidal benthic
foraminifera, ISME J., 16, 822–832,
https://doi.org/10.1038/s41396-021-01128-0, 2021.
Jørgensen, B. B.: Bacteria and marine biogeochemistry, Mar. Geochem.,
169–206, https://doi.org/10.1007/3-540-32144-6_ 5/COVER,
2006.
Jorissen, F. J., de Stigter, H. C., and Widmark, J. G. V: A conceptual model
explaining benthic foraminiferal microhabitats, Mar. Micropaleontol., 26,
3–15, https://doi.org/10.1016/0377-8398(95)00047-X, 1995.
Jorissen, F. J., Meyers, S. R., Kelly-Gerreyn, B. A., Huchet, L., Mouret,
A., and Anschutz, P.: The 4GFOR model – Coupling 4G early diagenesis and
benthic foraminiferal ecology, Mar. Micropaleontol., 170, 102078,
https://doi.org/10.1016/j.marmicro.2021.102078, 2022.
Kaiho, K.: Benthic foraminiferal dissolved-oxygen index and dissolved-oxygen
levels in the modern ocean, Geology, 22, 719–722,
https://doi.org/10.1130/0091-7613(1994)022< 0719:BFDOIA>2.3.CO;2, 1994.
Keating-Bitonti, C. R. and Payne, J. L.: Ecophenotypic responses of benthic
foraminifera to oxygen availability along an oxygen gradient in the
California Borderland, Mar. Ecol., 38, 1–16,
https://doi.org/10.1111/maec.12430, 2017.
Knowles, R.: Denitrification, in: Terrestrial nitrogen cycles, Ecological
Bulletin, Stockholm, 315–329, 1981.
Koho, K. A. and Piña-Ochoa, E.: Benthic foraminifera: Inhabitants of
low-oxygen environments, in: Anoxia: Evidence for Eukaryote Survival and
Paleontological Strategies, edited by: Altenbach, A. V, Bernhard, J. M., and
Seckbach, J., Springer Netherlands, Dordrecht, 249–285,
https://doi.org/10.1007/978-94-007-1896-8_ 14, 2012.
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, https://doi.org/10.1111/j.1574-6941.2010.01010.x,
2011.
Koho, K. A., LeKieffre, C., Nomaki, H., Salonen, I., Geslin, E., Mabilleau,
G., Søgaard Jensen, L. H., and Reichart, G. J.: Changes in
ultrastructural features of the foraminifera Ammonia spp. in response to anoxic
conditions: Field and laboratory observations, Mar. Micropaleontol., 138,
72–82, https://doi.org/10.1016/j.marmicro.2017.10.011, 2018.
Kranner, M., Harzhauser, M., Beer, C., Auer, G., and Piller, W. E.:
Calculating dissolved marine oxygen values based on an enhanced Benthic
Foraminifera Oxygen Index, Sci. Rep., 12, 1376,
https://doi.org/10.1038/s41598-022-05295-8, 2022.
Kulakovskaya, T.: Phosphorus storage in microorganisms: Diversity and
evolutionary insight, Biochem. Physiol. Open Access, 4, 1–4,
https://doi.org/10.4172/2168-9652.1000e130, 2014.
Langlet, D., Bouchet, V. M. P., Riso, R., Matsui, Y., Suga, H., Fujiwara,
Y., and Nomaki, H.: Foraminiferal ecology and role in nitrogen benthic cycle
in the hypoxic Southeastern Bering Sea, Front. Mar. Sci., 7, 843,
https://doi.org/10.3389/FMARS.2020.582818/BIBTEX, 2020.
Lee, J. J.: Nutrition and physiology of the foraminifera, in: Biochemistry
and Physiology of Protozoa, edited by: Levandowsky, M. and Hutner, S.,
Academic Press, Inc., New York, ISBN-13 978-0124446014, 1980.
Lee, J. J. and Anderson, O. R.: Symbiosis in foraminfera, in: Biology of
Foraminifera, edited by: Lee, J. J. and Anderson, O. R., Academic Press,
London, 157–220, 1991.
Lee, J. J., Lanners, E., and Kuile, B. Ter: The retention of chloroplasts by
the foraminifer Elphidium crispum, Symbiosis, 5, 45–59, 1988.
Lekieffre, C., Jauffrais, T., Geslin, E., Jesus, B., Bernhard, J. M.,
Giovani, M. E., and Meibom, A.: Inorganic carbon and nitrogen assimilation
in cellular compartments of a benthic kleptoplastic foraminifer, Sci.
Rep., 8, 1–12, https://doi.org/10.1038/s41598-018-28455-1, 2018.
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.
LeKieffre, C., Bernhard, J. M., Mabilleau, G., Filipsson, H. L., Meibom, A.,
and Geslin, E.: An overview of cellular ultrastructure in benthic
foraminifera: New observations of rotalid species in the context of existing
literature, Mar. Micropaleontol., 138, 12–32,
https://doi.org/10.1016/j.marmicro.2017.10.005, 2018.
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.
Linke, P. and Lutze, G. F.: Microhabitat preferences of benthic
foraminifera – a static concept or a dynamic adaptation to optimize food
acquisition?, Mar. Micropaleontol., 20, 215–234,
https://doi.org/10.1016/0377-8398(93)90034-U, 1993.
Lipps, J. H. and Valentine, J. W.: The role of foraminifera in the trophic
structure of marine communities, Lethaia, 3, 279–286,
https://doi.org/10.1111/j.1502-3931.1970.tb01271.x, 1970.
Lopez, E.: Algal chloroplasts in the protoplasm of three species of benthic
foraminifera: taxonomic affinity, viability and persistence, Mar. Biol., 53,
201–211, https://doi.org/10.1007/BF00952427/METRICS, 1979.
Lu, Z. and Imlay, J. A.: When anaerobes encounter oxygen: mechanisms of
oxygen toxicity, tolerance and defence, Nat. Rev. Microbiol., 19, 774,
https://doi.org/10.1038/S41579-021-00583-Y, 2021.
Lu, Z., Hoogakker, B. A. A., Hillenbrand, C.-D., Zhou, X., Thomas, E.,
Gutchess, K. M., Lu, W., Jones, L., and Rickaby, R. E. M.: Oxygen depletion
recorded in upper waters of the glacial Southern Ocean, Nat. Commun., 7,
11146, https://doi.org/10.1038/ncomms11146, 2016.
Lutze, G. F. and Thiel, H.: Epibenthic foraminifera from elevated
microhabitats; Cibicidoides wuellerstorfi and Planulina ariminensis, J. Foraminifer. Res., 19, 153–158,
https://doi.org/10.2113/gsjfr.19.2.153, 1989.
Mackensen, A., Schmiedl, G., Harloff, J., and Giese, M.: Deep-sea
foraminifera in the South Atlantic Ocean; ecology and assemblage generation,
Micropaleontology, 41, 342–358, 1995.
Manheim, F., Rowe, G. T., and Jipa, D.: Marine phosphorite formation off
Peru, J. Sediment. Res., 45, 243–251,
https://doi.org/10.1306/212F6D20-2B24-11D7-8648000102C1865D, 1975.
McCorkle, D. C. and Emerson, S. R.: The relationship between pore water
carbon isotopic composition and bottom water oxygen concentration, Geochim. Cosmochim. Ac., 52, 1169–1178,
https://doi.org/10.1016/0016-7037(88)90270-0, 1988.
Mckenney, D. J., Drury, C. F., Findlay, W. I., Mutus, B., McDonnell, T., and
Gajda, C.: Kinetics of denitrification by Pseudomonas fluorescens: Oxygen effects, Soil Biol.
Biochem., 26, 901–908, https://doi.org/10.1016/0038-0717(94)90306-9, 1994.
Mojtahid, M., Jorissen, F., Lansard, B., and Fontanier, C.: Microhabitat
selection of benthic foraminifera in sediments off the Rhône river mouth
(NW Mediterranean), J. Foraminifer. Res., 40, 231–246,
https://doi.org/10.2113/GSJFR.40.3.231, 2010.
Nardelli, M. P., Barras, C., Metzger, E., Mouret, A., Filipsson, H. L., Jorissen, F., and Geslin, E.: Experimental evidence for foraminiferal calcification under anoxia, Biogeosciences, 11, 4029–4038, https://doi.org/10.5194/bg-11-4029-2014, 2014.
Natland, M. L.: New species of Foraminifera from off the west coast of North
America and from the later Tertiary of the Los Angeles basin, Bull. Scripps
Inst. Oceanogr. Univ. California, Tech. Ser., 1938.
Ní Fhlaithearta, S., Fontanier, C., Jorissen, F., Mouret, A., Dueñas-Bohórquez, A., Anschutz, P., Fricker, M. B., Günther, D., de Lange, G. J., and Reichart, G.-J.: Manganese incorporation in living (stained) benthic foraminiferal shells: a bathymetric and in-sediment study in the Gulf of Lions (NW Mediterranean), Biogeosciences, 15, 6315–6328, https://doi.org/10.5194/bg-15-6315-2018, 2018.
Nomaki, H., Heinz, P., Nakatsuka, T., Shimanaga, M., and Kitazato, H.:
Species-specific ingestion of organic carbon by deep-sea benthic
foraminifera and meiobenthos: In situ tracer experiments, Limnol. Oceanogr.,
50, 134–146, https://doi.org/10.4319/lo.2005.50.1.0134, 2005.
Nomaki, H., Heinz, P., Nakatsuka, T., Shimanaga, M., Ohkouchi, N., Ogawa, N.
O., Kogure, K., Ikemoto, E., and Kitazato, H.: Different ingestion patterns
of 13C-labeled bacteria and algae by deep-sea benthic foraminifera,
Mar. Ecol. Prog. Ser., 310, 95–108, https://doi.org/10.3354/MEPS310095,
2006.
Nomaki, H., Ogawa, N., Ohkouchi, N., Suga, H., Toyofuku, T., Shimanaga, M.,
Nakatsuka, T., and Kitazato, H.: Benthic foraminifera as trophic links
between phytodetritus and benthic metazoans: carbon and nitrogen isotopic
evidence, Mar. Ecol. Prog. Ser., 357, 153–164,
https://doi.org/10.3354/meps07309, 2008.
Nomaki, H., Ogawa, N. O., Takano, Y., Suga, H., Ohkouchi, N., and Kitazato,
H.: Differing utilization of glucose and algal particulate organic matter by
deep-sea benthic organisms of Sagami Bay, Japan, Mar. Ecol. Prog. Ser., 431,
11–24, 2011.
Nomaki, H., Chikaraishi, Y., Tsuchiya, M., Toyofuku, T., Ohkouchi, N.,
Uematsu, K., Tame, A., and Kitazato, H.: Nitrate uptake by foraminifera and
use in conjunction with endobionts under anoxic conditions, Limnol.
Oceanogr., 59, 1879–1888, https://doi.org/10.4319/lo.2014.59.6.1879, 2014.
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, https://doi.org/10.1002/lno.10140, 2015.
Nomaki, H., Bernhard, J.M., Ishida, A., Tsuchiya, M., Uematsu, K., Tame, A.,
Kitahashi, T., Takahata, N., Sano, Y. and Toyofuku, T.: Intracellular
isotope localization in Ammonia sp. (Foraminifera) of oxygen-depleted environments:
Results of nitrate and sulfate labeling experiments, Front. Microbiol.,
7, 163, https://doi.org/10.3389/fmicb.2016.00163, 2016.
de Nooijer, L. J., Spero, H. J., Erez, J., Bijma, J., and Reichart, G. J.:
Biomineralization in perforate foraminifera, Earth-Sci. Rev., 135,
48–58, https://doi.org/10.1016/j.earscirev.2014.03.013,
2014.
Oakley, B. B., Francis, C. A., Roberts, K. J., Fuchsman, C. A., Srinivasan,
S., and Staley, J. T.: Analysis of nitrite reductase (nirK and nirS) genes
and cultivation reveal depauperate community of denitrifying bacteria in the
Black Sea suboxic zone, Environ. Microbiol., 9, 118–130,
https://doi.org/10.1111/j.1462-2920.2006.01121.x, 2007.
Orsi, W. D., Morard, R., Vuillemin, A., Eitel, M., Wörheide, G.,
Milucka, J., and Kucera, M.: Anaerobic metabolism of Foraminifera thriving
below the seafloor, ISME J., 14, 2580–2594,
https://doi.org/10.1038/s41396-020-0708-1, 2020.
Panagiota-Chronopoulou, M., Salonen, I., Bird, C., Reichart, G. J., and
Koho, K. A.: Metabarcoding insights into the trophic behavior and identity
of intertidal benthic foraminifera, Front. Microbiol., 10,
https://doi.org/10.3389/FMICB.2019.01169/FULL, 2019.
Papagiannakis, E., Van Stokkum, I. H. M., Fey, H., Büchel, C., and Van
Grondelle, R.: Spectroscopic characterization of the excitation energy
transfer in the fucoxanthin-chlorophyll protein of diatoms, Photosynth.
Res., 86, 241–250, https://doi.org/10.1007/S11120-005-1003-8/METRICS, 2005.
Pillet, L., de Vargas, C., and Pawlowski, J.: Molecular identification of
sequestered diatom chloroplasts and kleptoplastidy in foraminifera, Protist,
162, 394–404, https://doi.org/10.1016/j.protis.2010.10.001, 2011.
Pillet, L., Voltski, I., Korsun, S., and Pawlowski, J.: Molecular phylogeny
of Elphidiidae (foraminifera), Mar. Micropaleontol., 103, 1–14,
https://doi.org/10.1016/J.MARMICRO.2013.07.001, 2013.
Piña-Ochoa, E., Koho, K. A., Geslin, E., and Risgaard-Petersen, N.:
Survival and life strategy of the foraminiferan Globobulimina turgida through nitrate storage and
denitrification, Mar. Ecol. Prog. Ser., 417, 39–49,
https://doi.org/10.3354/meps08805, 2010a.
Piña-Ochoa, E., Høgslund, 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, https://doi.org/10.1073/pnas.0908440107, 2010b.
Powers, C., Gomaa, F., Billings, E. B., Utter, D. R., Beaudoin, D. J.,
Edgcomb, V. P., Hansel, C. M., Wankel, S. D., Filipsson, H. L., Zhang, Y.,
and Bernhard, J. M.: Two canonically aerobic foraminifera express distinct
peroxisomal and mitochondrial metabolisms, Front. Mar. Sci., 9, 2423,
https://doi.org/10.3389/FMARS.2022.1010319/BIBTEX, 2022.
Premvardhan, L., Sandberg, D. J., Fey, H., Birge, R. R., Büchel, C., and
Van Grondelle, R.: The charge-transfer properties of the S2 state of
fucoxanthin in solution and in fucoxanthin chlorophyll-a/c2 protein (FCP)
based on stark spectroscopy and molecular-orbital theory, J. Phys. Chem. B,
112, 11838–11853, https://doi.org/10.1021/JP802689P/SUPPL_
FILE/JP802689P-FILE003.PDF, 2008.
Rathburn, A. E., Willingham, J., Ziebis, W., Burkett, A. M., and Corliss, B.
H.: A New biological proxy for deep-sea paleo-oxygen: Pores of epifaunal
benthic foraminifera, Sci. Rep., 8, 9456,
https://doi.org/10.1038/s41598-018-27793-4, 2018.
Reichart, G.-J., Jorissen, F., Anschutz, P., and Mason, P. R. D.: Single
foraminiferal test chemistry records the marine environment, Geology, 3, 355–358,
2003.
Richirt, J., Schweizer, M., Bouchet, V. M. P., Mouret, A., Quinchard, S.,
and Jorissen, F. J.: Morphological distinction of three Ammonia phylotypes occurring
along European Coasts, J. Foraminifer. Res., 49, 76–93,
https://doi.org/10.2113/GSJFR.49.1.76, 2019.
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., Nielsen, L. P., Revsbech, N. P., Cedhagen, T., and Van
Der Zwaan, G. J.: Evidence for complete denitrification in a benthic
foraminifer, Nature, 443, 93–96, https://doi.org/10.1038/nature05070, 2006.
Ross, B. J. and Hallock, P.: Dormancy in the foraminifera: A review, J.
Foraminifer. Res., 46, 358–368, https://doi.org/10.2113/GSJFR.46.4.358,
2016.
Rybarczyk, H., Elkaim, B., Wilson, J., and Loquet, N.: L'eutrophisation en
Baie de Somme: mortalités des peuplements benthiques par anoxie,
Oceanol. Ac., 19, 131–140, 1996.
Sandberg, E.: Does short-term oxygen depletion affect predator-prey
relationships in zoobenthos?, Experiments with the isopod Saduria entomon, Mar. Ecol. Prog.
Ser., 103, 73–80, 1994.
Schmiedl, G. and Mackensen, A.: Multispecies stable isotopes of benthic
foraminifers reveal past changes of organic matter decomposition and
deepwater oxygenation in the Arabian Sea, Paleoceanography, 21, 1–14,
https://doi.org/10.1029/2006PA001284, 2006.
Schulz, H. N. and Schulz, H. D.: Large sulfur bacteria and the formation of
phosphorite, Science, 307, 416–418, https://doi.org/10.1126/science.1103096,
2005.
Schweizer, M., Jauffrais, T., Choquel, C., Méléder, V., Quinchard,
S., and Geslin, E.: Trophic strategies of intertidal foraminifera explored
with single-cell microbiome metabarcoding and morphological methods: What is
on the menu?, Ecol. Evol., 12, e9437,
https://doi.org/10.1002/ece3.9437, 2022.
Smith, M. S. and Tiedje, J. M.: Phases of denitrification following oxygen
depletion in soil, Soil Biol. Biochem., 11, 261–267,
https://doi.org/10.1016/0038-0717(79)90071-3, 1979.
Tetard, M., Licari, L., Ovsepyan, E., Tachikawa, K., and Beaufort, L.: Toward a global calibration for quantifying past oxygenation in oxygen minimum zones using benthic Foraminifera, Biogeosciences, 18, 2827–2841, https://doi.org/10.5194/bg-18-2827-2021, 2021.
Thibault de Chanvalon, A., Metzger, E., Mouret, A., Cesbron, F., Knoery, J., Rozuel, E., Launeau, P., Nardelli, M. P., Jorissen, F. J., and Geslin, E.: Two-dimensional distribution of living benthic foraminifera in anoxic sediment layers of an estuarine mudflat (Loire estuary, France), Biogeosciences, 12, 6219–6234, https://doi.org/10.5194/bg-12-6219-2015, 2015.
Tiedje, J.: Ecology of denitrification and dissimilatory nitrate reduction
to ammonium, in: Methods of Soil Analysis, Part 2. Chemical and
Microbiological Properties, 717, 179–244, 1988.
Toyofuku, T., Matsuo, M. Y., de Nooijer, L. J., Nagai, Y., Kawada, S.,
Fujita, K., Reichart, G.-J., Nomaki, H., Tsuchiya, M., Sakaguchi, H., and
Kitazato, H.: Proton pumping accompanies calcification in foraminifera, Nat.
Commun., 8, 14145, https://doi.org/10.1038/ncomms14145, 2017.
Tsaousis, A. D., Nývltová, E., Šuták, R., Hrdý, I., and
Tachezy, J.: A nonmitochondrial hydrogen production in Naegleria gruberi, Genome Biol. Evol.,
6, 792–799, https://doi.org/10.1093/GBE/EVU065, 2014.
Tsuchiya, M., Toyofuku, T., Uematsu, K., Brüchert, V., Collen, J.,
Yamamoto, H., and Kitazato, H.: Cytologic and genetic characteristics of
endobiotic bacteria and kleptoplasts of Virgulinella fragilis (Foraminifera), J. Eukaryot.
Microbiol., 62, 454–469, https://doi.org/10.1111/jeu.12200,
2015.
Usuda, K., Toritsuka, N., Matsuo, Y., Kim, D. H., and Shoun, H.:
Denitrification by the fungus Cylindrocarpon tonkinense: anaerobic cell growth and two isozyme forms
of cytochrome P-450nor., Appl. Environ. Microbiol., 61, 883–889, 1995.
Winkelbauer, H., Cordova-Rodriguez, K., Reyes-Macaya, D., Scott, J., Glock,
N., Lu, Z., Hamilton, E., Chenery, S., Holdship, P., Dormon, C., and
Hoogakker, B.: Foraminifera iodine to calcium ratios: Approach and cleaning,
Geochem. Geophys. Geosys., 22, e2021GC009811,
https://doi.org/10.1029/2021GC009811, 2021.
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,
2536–2543, https://doi.org/10.1016/j.cub.2018.06.027, 2018.
Woehle, C., Roy, A.-S., Glock, N., Michels, J., Wein, T., Weissenbach, J.,
Romero, D., Hiebenthal, C., Gorb, S., Schönfeld, J., and Dagan, T.:
Denitrification in foraminifera has an ancient origin and is complemented by
associated bacteria, P. Natl. Acad. Sci. USA, 119, e2200198119,
https://doi.org/10.1073/pnas.2200198119, 2022.
Wollenburg, J. E., Zittier, Z. M. C., and Bijma, J.: Insight into deep-sea
life – Cibicidoides pachyderma substrate and pH-dependent behaviour following disturbance, Deep.
Res. Pt. I, 138, 34–45, https://doi.org/10.1016/j.dsr.2018.07.006,
2018.
Wollenburg, J. E., Bijma, J., Cremer, C., Bickmeyer, U., and Zittier, Z. M. C.: Permanent ectoplasmic structures in deep-sea Cibicides and Cibicidoides taxa – long-term observations at in situ pressure, Biogeosciences, 18, 3903–3915, https://doi.org/10.5194/bg-18-3903-2021, 2021.
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,
https://doi.org/10.3354/meps12135, 2017.
Xu, Z., Liu, S., and Ning, X.: Potential foraminiferal nitrate transport in
sediments in contact with oxic overlying water, Limnol. Oceanogr., 66,
1510–1530, https://doi.org/10.1002/lno.11701, 2021.
Zhou, X., Thomas, E., Rickaby, R. E. M., Winguth, A. M. E., and Lu, Z.:
Zhou, X., Hess, A. V., Bu, K., Sagawa, T., and Rosenthal, Y.: Simultaneous
determination of
Zimorski, V., Mentel, M., Tielens, A. G. M., and Martin, W. F.: Energy
metabolism in anaerobic eukaryotes and Earth's late oxygenation, Free Radic.
Biol. Med., 140, 279–294,
https://doi.org/10.1016/j.freeradbiomed.2019.03.030, 2019.
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Short summary
Ocean deoxygenation due to climate warming is an evolving threat for organisms that are not well adapted to O2 depletion, such as many pelagic fish species. Other better-adapted organisms, such as some benthic foraminifera species, might benefit from ocean deoxygenation. Benthic foraminifera are a group of marine protists and can have specific adaptations to O2 depletion such as the ability to respire nitrate instead of O2. This paper reviews the current state of knowledge about these organisms.
Ocean deoxygenation due to climate warming is an evolving threat for organisms that are not well...
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