Articles | Volume 18, issue 3
https://doi.org/10.5194/bg-18-977-2021
© 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-18-977-2021
© Author(s) 2021. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Vertical distribution of planktic foraminifera through an oxygen minimum zone: how assemblages and test morphology reflect oxygen concentrations
Catherine V. Davis
CORRESPONDING AUTHOR
Department of Earth and Planetary Sciences, Yale University, New Haven,
CT 06511, USA
Karen Wishner
Graduate School of Oceanography, University of Rhode Island,
Narragansett, RI 02882, USA
Willem Renema
Department of Ecosystem & Landscape Dynamics, Institute for
Biodiversity & Ecosystem Dynamics (IBED), University of Amsterdam,
Amsterdam, the Netherlands
Naturalis Biodiversity Center, Leiden, the Netherlands
Pincelli M. Hull
Department of Earth and Planetary Sciences, Yale University, New Haven,
CT 06511, USA
Peabody Museum of Natural History, Yale University, New Haven, 06511,
USA
Related authors
Emily Havard, Katherine Cherry, Claudia Benitez-Nelson, Eric Tappa, and Catherine V. Davis
Biogeosciences, 22, 4035–4060, https://doi.org/10.5194/bg-22-4035-2025, https://doi.org/10.5194/bg-22-4035-2025, 2025
Short summary
Short summary
This study explores the impact of modern climate change on single-celled, marine organisms in the Santa Barbara Basin called foraminifera. We collect their shells as they sink to the seafloor and compare our record (2014–2021) to previous studies (1993–1998). We find substantial decreases in total foraminifera and warm-water species. Likely influenced by ocean acidification and regional water circulation, these changes have implications for the marine carbon cycle, ecosystem, and fossil record.
Anjaly Govindankutty Menon, Aaron L. Bieler, Hanna Firrincieli, Rachel Alcorn, Niko Lahajnar, Catherine V. Davis, Ralf Schiebel, Dirk Nürnberg, Gerhard Schmiedl, and Nicolaas Glock
EGUsphere, https://doi.org/10.5194/egusphere-2025-1182, https://doi.org/10.5194/egusphere-2025-1182, 2025
Short summary
Short summary
The pore density (number of pores per unit area) of unicellular eukaryotes is used to reconstruct past bottom-water nitrate at the Sea of Okhotsk, the Gulf of California, the Mexican Margin and the Gulf of Guayaquil. The reconstructed bottom-water nitrate at the Sea of Okhotsk, the Gulf of California and the Gulf of Guayaquil are influenced by the intermediate water masses, while the nitrate at the Mexican Margin is related to the deglacial NO3− variability in the Pacific Deep Water.
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.
Emily Havard, Katherine Cherry, Claudia Benitez-Nelson, Eric Tappa, and Catherine V. Davis
Biogeosciences, 22, 4035–4060, https://doi.org/10.5194/bg-22-4035-2025, https://doi.org/10.5194/bg-22-4035-2025, 2025
Short summary
Short summary
This study explores the impact of modern climate change on single-celled, marine organisms in the Santa Barbara Basin called foraminifera. We collect their shells as they sink to the seafloor and compare our record (2014–2021) to previous studies (1993–1998). We find substantial decreases in total foraminifera and warm-water species. Likely influenced by ocean acidification and regional water circulation, these changes have implications for the marine carbon cycle, ecosystem, and fossil record.
Anjaly Govindankutty Menon, Aaron L. Bieler, Hanna Firrincieli, Rachel Alcorn, Niko Lahajnar, Catherine V. Davis, Ralf Schiebel, Dirk Nürnberg, Gerhard Schmiedl, and Nicolaas Glock
EGUsphere, https://doi.org/10.5194/egusphere-2025-1182, https://doi.org/10.5194/egusphere-2025-1182, 2025
Short summary
Short summary
The pore density (number of pores per unit area) of unicellular eukaryotes is used to reconstruct past bottom-water nitrate at the Sea of Okhotsk, the Gulf of California, the Mexican Margin and the Gulf of Guayaquil. The reconstructed bottom-water nitrate at the Sea of Okhotsk, the Gulf of California and the Gulf of Guayaquil are influenced by the intermediate water masses, while the nitrate at the Mexican Margin is related to the deglacial NO3− variability in the Pacific Deep Water.
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.
Arne M. E. Winguth, Mikaela Brown, Pincelli Hull, Elizabeth Griffith, Christine Shields, Ellen Thomas, and Cornelia Winguth
EGUsphere, https://doi.org/10.5194/egusphere-2024-4209, https://doi.org/10.5194/egusphere-2024-4209, 2025
Short summary
Short summary
The Paleocene-Eocene Thermal Maximum (PETM) about 56 million years ago is characterized by a rapid perturbation of the global carbon cycle. Comparison of sedimentary records with results from a comprehensive Earth system model suggest that environmental changes including benthic foraminifera extinction may have caused by a massive carbon input at the PETM and associate collapse of the ocean circulation due to the greenhouse-gas induced warming.
Daniel E. Gaskell and Pincelli M. Hull
Clim. Past, 19, 1265–1274, https://doi.org/10.5194/cp-19-1265-2023, https://doi.org/10.5194/cp-19-1265-2023, 2023
Short summary
Short summary
One of the most common ways of reconstructing temperatures in the geologic past is by analyzing oxygen isotope ratios in fossil shells. However, converting these data to temperatures can be a technically complicated task. Here, we present a new online tool that automates this task.
Cited articles
Bates, N. R.: Seawater carbonate chemistry distributions across the Eastern
South Pacific Ocean sampled as part of the GEOTRACES project and changes in marine
carbonate chemistry over the past 20 years, Front. Mar. Sci., 5, 398, https://doi.org/10.3389/fmars.2018.00398, 2018.
Bernhard, J. M.: Characteristic assemblages and Morphologies of benthic
foraminifera from anoxic, organic-rich deposits: Jurassic through Holocene,
J. Foramin. Res., 16, 207–215, 1986.
Bernhard, J. M. and Alve, E.: Survival, ATP pool, and ultrastructural
characterization of benthic foraminifera from Drammensfjord (Norwar): response to anoxia, Mar.
Micropaleontol., 28, 5–17, 1996.
Bernhard, J. M. and Bowser, S. S.: Peroxisome proliferation in Foraminifera
inhabiting the chemocline: an adaptation to reactive oxygen species
exposure?, J. Eukaryot. Microbiol., 55, 135–144, 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, US
Pacific continental margin, J. Foramin. Res., 27, 301–310, 1997.
Bernhard, J. M., Edgcomb, V. P., Casciotti, K. L., McIlvin, M. R., and
Beaudoin, D. J.: Dentrification likely catalyzed by endobionts in an allogromiid foraminifer,
ISME J., 6, 951–960, 2011.
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, 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, J. Geophys.
Res.-Biogeo., 117, G03002, https://doi.org/10.1029/2012JG001949, 2012b.
Bijma, J., Faber, W. W., and Hemleben, C.: Lunar and semi-lunar reproductive
cycles in some spinose planktonic foraminifers, J. Foramin. Res., 20,
117–127, 1990.
Bijma, J., Faber, W. W., and Hemleben, C: Temperature and salinity limits
for
growth and survival of some planktonic foraminfiers in laboratory cultures,
J. Foramin. Res., 20, 95–116, 1990.
Bijma, J., Honisch, B., and Zeebe, R. E.: Impact of the ocean carbonate
chemistry on
living foraminiferal shell weght: Comment on “Carbonate ion concentration
in glacia-age deep waters of the Caribbean Sea” by W. S. Broecker and E.
Clark, Geochem. Geophy. Geosy., 3, 1–7, 2002.
Birch, H., Coxall, H. K., Pearson, P. N., Kroon, D., and O'Regan, M.: Planktonic
foraminifera stable isotopes and water column structure: Disentangling
ecological signals, Mar. Micropaleontol., 101, 127–145, 2013.
Bird, C., Darling, K. F., Russell, A. D., Fehrenbacher, J. S., Davis, C. V.,
Free, A., and Ngwenya, B. T.: 16S rRNA gene metabarcoding and TEM reveals different
ecological strategies within the genus Neogloboquadrina (planktonic
foraminifer), PloS one, 13, e0191653, https://doi.org/10.1371/journal.pone.0191653, 2018.
Breitburg, D., Levin, L. A., Oschlies, A., Gregoire, M., Chavez, F. P.,
Conley, D. J.,
Garcon, V., Gilbert, D., Gutierrez, 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.
Buchwald, C., Santoro, A. E., Stanley, R. H. R., and Casciotti, K. L.:
Nitrogen
cycling in the secondary nitrite maximum of the eastern tropical North
Pacific off
Coasta Rica, Global Biogeochem. Cy., 29, 1656–1673, https://doi.org/10.1002/2015GB005198, 2015.
Burke, J. E., Renema, W., Henehan, M. J., Elder, L. E., Davis, C. V., Maas, A. E., Foster, G. L., Schiebel, R., and Hull, P. M.: Factors influencing test porosity in planktonic foraminifera, Biogeosciences, 15, 6607–6619, https://doi.org/10.5194/bg-15-6607-2018, 2018.
Burke, J. E., Renema, W., Schiebel, R., and Hull, P. M.: Three-dimensional
analysis of
inter-and intraspecific variation in ontogenetic growth trajectories of
planktonic foraminifera, Mar. Micropaleontol., 155, 101794, https://doi.org/10.1016/j.marmicro.2019.101794, 2020.
Cannariato, K. G., Kennett, J. P., and Behl, R. J.: Biotic response to late
Quaternary rapid climate switches in Santa Barbara Basin: Ecological and
evolutionary implications, Geology, 27, 63–66, 1999.
Cassman, N., Prieto-Davo, A., Walsh, K., Silva, G. G. Z., Angly, F., Akhter,
S., Barott, K., Busch, J., McDole, T., Haggerty, J. M., Willner, D., Alarcon,
G., Ulloa, O., DeLong, E. F., Dutilh, B. E., Rohwer, F., and Dinsdale, E.
A.: Oxygen minimum zones harbor novel viral communities with low diversity,
Environ. Microbiol., 14, 3043–3065, 2012.
Cignoni, P., Callieri, M., Corsini, M., Dellepiane, M., Ganovelli, F., and
Ranzuglia, G.: MeshLab: an open-source mesh processing tool, in: Proceedings of the Sixth
Eurographics Italian Chapter Conference, 2–4 July 2008, Salerno, Italy, 129–136, 2008.
Corliss, B. H.: Microhabitats of benthic foraminifera within deep-sea
sediments, Nature, 314, 435–439, 1985.
Coxall, H. K., Pearson, P. N., Wilson, P. A., and Sexton, P. F.: Iterative
evolution of digitate planktonic foraminifera, Paleobiology, 33, 495–516,
2007.
Davis, C. V., Hill, T. M., Russell, A. D., Gaylord, B., and Jahncke, J.: Seasonality in planktic foraminifera of the central California coastal upwelling region, Biogeosciences, 13, 5139–5150, https://doi.org/10.5194/bg-13-5139-2016, 2016.
DeVries, T., Deutsch, C., Primeau, F., Chang, B., and Devol, A.: Global rates of
water-column denitrification derived from nitrogen gas measurements, Nature Geosci.,
5, 547, https://doi.org/10.1038/ngeo1515, 2012.
Duret, M. T., Pachiadaki, M. G., Stewart, F. J., Sarode, N., Christaki, U.,
Mochy, S., Srivastava, A., and Edgcomb, V. P.: Size-fractionated diversity
of eukaryotic microbial communities in the Eastern Tropical North Pacific
oxygen minimum zone, FEMS Microbiol. Ecol., 91, fiv037, https://doi.org/10.1093/femsec/fiv037,
2017.
Eguchi, N. O., Kawahata, H., and Asahiko, T.: Seasonal Response of
Planktonic Foraminifera to surface ocean conditions: Sediment trap results
from the Central North Pacific Ocean, J. Oceanogr., 55, 681–691, 1999.
Emiliani, C.: Depth habitats of some species of pelagic foraminifera as
indicated by oxygen isotopic ratios, Am. J. Sci., 252, 149–158, 1954.
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.
Erez, J., Almogi-Labin, A., and Avraham, S.: On the life history of
planktonic
foraminifera: Lunar reproduction cycle in Globigerinoides sacculifer (Brady), Paleoceanography, 6, 295–306, 1991.
Escribano, R., Hidalgo, P., and Krautz, C.: Zooplankton associated with the
oxygen minimum zone system in the northern upwelling region of Chile during
March 2000, Deep-Sea Res., 56, 1083–1094, 2009.
Fairbanks, R. G., Sverdlove, M., Free, R., Wiebe, P. H., and Be, A. W. H.:
Vertical distribution and isotopic fractionation of living planktonic
foraminifera from the Panama Basin, Nature, 298, 841–844, 1982.
Fiedler, P. C. and Talley, L. D.: Hydrography of the eastern tropical Pacific:
A
Review, Prog. Oceanogr. 69, 143–180, 2006.
Field, D. B.: Variability in vertical distributions of planktonic
foraminifera in the California Current: Relationships to vertical ocean
structure, Paleoceanography, 19, PA2014, https://doi.org/10.1029/2003PA000970, 2004.
Garcia, H. E., Weathers, K., Paver, C. R., Smolyar, I., Boyer, T. P., Locarnini, R. A., Zweng, M. M., Mishonov, A. V., Baranova, O K., Seidov, D., and Reagan, J. R.:
World
Ocean Atlas 2018, Dissolved Oxygen, Apparent Oxygen Utilization,
and Oxygen Saturation, NOAA, Silver Spring, USA, 2018.
Garfield, P. C., Packard, T. T., Friederich, G. E., and Codispoti, L. A.: A
subsurface
particle maximum layer and enhanced microbial activity in the secondary
nitrate maximum of the northeastern tropical Pacific Ocean, J. Mar. Res.,
41, 747–768, 1983.
Gaskell, D. E., Ohman, M. D., and Hull, P. M.: Zooglider-based measurements
of
planktonic foraminifera in the California Current system, J. Foramin. Res.,
49, 390–404, 2019
Glock, N., Eisenhauer, A., Milker, Y., Liebetrau, V., Schonfeld, J., Mallon,
J., Sommer, S., and Hensen, C.: Environmental influences on the pore density
of Bolivina spissa (Cushman), J. Foramin. Res., 41, 22–32, 2011.
Glock, N., Schönfeld, J., and Mallon, J.: The Functionality of Pores in
Benthic Foraminifera in View of Bottom Water Oxygenation: A Review, in:
Anoxia, Cellular Origin, Life in Extreme Habitats and Astrobiology, edited by: Altenbach,
A. V., Bernhard, J. M., and Seckbach, J., Springer, the Netherlands,
537–552, 2012.
Glock, N., Erdem, Z., Wallmann, K., Somes, C. J., Liebetrau, V., Schonfeld,
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., Roy, A. S., Romero, D., Wein, T., Weissenbach, J., Revsbech, N.
P.,
Hogslund, 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.
Gooday, A. J., Bernhard, J. M., Levin, L. A., and Suhr, S. B.: Foraminifera
in the Arabian Sea oxygen minimum zone and other oxygen-deficient settings:
taxonomic composition, diversity, and relation to metazoan faunas, Deep-Sea
Res., 47, 25–54, 2000.
Gooday, A. J., Schoenle, A., Dolan, J. R., and Arndt, H.: Protist diversity
and function in the dark ocean – Challenging the paradigms of deep-sea
ecology with special emphasis on foraminiferans and naked protists, Eur. J.
Protistol., 75, 125721, https://doi.org/10.1016/j.ejop.2020.125721, 2020.
Gruber, N.: The marine nitrogen cycle: overview and challenges, Nitrogen in the marine
environment, 2, 1–50, Academic Press
Cambridge, MA, USA, 2008.
Henehan, M. J., Evans, D., Shankle, M., Burke, J. E., Foster, G. L., Anagnostou, E., Chalk, T. B., Stewart, J. A., Alt, C. H. S., Durrant, J., and Hull, P. M.: Size-dependent response of foraminiferal calcification to seawater carbonate chemistry, Biogeosciences, 14, 3287–3308, https://doi.org/10.5194/bg-14-3287-2017, 2017.
Hofmann, A. F., Peltzer, E. T., Walz, P. M., and Brewer, P. G.: Hypoxia by
degrees: Establishing definitions for a changing ocean, Deep-Sea Res.,
58, 1212–1226, 2011.
Hogslund, 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., 39, 85–91, 2008.
Hsiang, A. Y., Nelson, K., Elder, L. E., Sibert, E. C., Kahanamoku, S. S.,
Burke, J. E., Kelly, A., Liu, Y., and Hull, P. M.: Automorph: Accelerating
morphometrics with automated 2D and 3D image processing and shape
extraction, Methods Ecol. Evol., 9, 605–612, 2018.
Hull, P. M., Osborn, K. J., Norris, R. D., and Robison, B. H.: Seasonality and
depth distribution of a mesopelagic foraminifer, Hastigerinella digitata, in Monterey Bay,
California, Limnol. Oceanogr. 56, 562–576, 2011.
Jonkers, L., Reynolds, C. E., Richey, J., and Hall, I. R.: Lunar periodicity in the shell flux of planktonic foraminifera in the Gulf of Mexico, Biogeosciences, 12, 3061–3070, https://doi.org/10.5194/bg-12-3061-2015, 2015.
Jorissen, F. J., Fontanier, C., and Thomas, E.: Chapter seven
paleoceanographical proxies based on deep-sea benthic foraminiferal
assemblage characteristics, Developments in Marine Geology, 1, 263–325,
2007.
Kaiho, K.: Benthic foraminiferal dissolved-oxygen index and dissolved-oxygen
levels in the modern ocean, Geology, 22, 719–722, 1994.
Katz, M. E., Cramer, B. S., Franzese, A., Hönisch, B., Miller, K. G.,
Rosenthal, Y., and Wright, J. D.: Traditional and emerging geochemical
proxies in foraminifera, J. Foramin. Res., 40, 165–192, 2010.
Kawahata, H., Nichimura, A., and Gagan, M. K.: Seasonal change in
foraminiferal production in the western equatorial Pacific warm pool:
evidence from sediment trap experiments, Deep-Sea Res., 49, 2783–2800,
2002.
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, e12430, https://doi.org/10.1111/maec.12430, 2017.
Keeling, R. F., Körtzinger, A., and Gruber, N.: Ocean Deoxygenation in a
Warming World, Annu. Rev. Mar. Sci., 2, 199–229, 2009.
Kucera, M.: Chapter six planktonic foraminifera as tracers of past oceanic
environments, Developments in Marine Geology, 1, 213–262, 2007.
Kucera, M., Weinelt, M., Kiefer, T., Pflaumann, U., Hayes, A., Weinelt, M.,
Chen, M.-T., Mix, A. C., Barrows, T. T., Cortijo, E., Duprat, J., Juggins, S., and
Waelbroech, C.: Reconstruction of sea-surface temperatures from assemblages
of planktonic foraminifera: multi-technique approach based on geographically
constrained calibration data sets and its application to glacial Atlantic
and Pacific Oceans, Quaternary Sci. Rev., 24, 951–998, 2005.
Kuhnt, T., Friedrich, O., Schmiedl, G., Milker, Y., Machensen, A., and
Luckge, A.: Relationship between pore density in benthic foraminifera and
bottom-water oxygen content, Deep-Sea Res., 76, 85–96, 2013.
Kuhnt, T., Schiebel, R., Schmiedl, G., Milker, Y., Mackensen, A., and
Friedrich, O.: Automated and manual analyses of the pore density-to-oxygen
relationship in Globobulimina turgida (Baily), J. Foramin. Res., 44, 1–5, 2014.
Kuroyanagi, A., Kawahata, H., Nishi, H., and Hondo, M. C.: Seasonal changes
in planktonic foraminifera in the northwestern North Pacific Ocean: sediment
trap experiments from subarctis and subtropical gyres, Deep-Sea Res.,
49, 5627–5645, 2002.
Kuroyanagi, A., da Rocha, R. E., Bijma, J., Spero, H. J., Russell, A. D.,
Eggins, S. M., and Kawahata, H.: Effect of dissolved oxygen concentration on
planktonic foraminifera through laboratory culture experiments and
implications for oceanic anoxic events, Mar. Micropaleontol., 101, 28–32,
2013.
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.
Leutenegger, S. and Hansen, H. J.: Ultrastructural and radiotracer studies
of pore function in Foraminifera, Mar. Biol., 54, 11–16, 1979.
Levin, L. A.: Oxygen minimum zone benthos: Adaptation and community response
to hypoxia, Oceanogr. Mar. Biol., 41, 1–45, 2003.
Levin, L. A.: Manifestation, Drivers, and Emergence of Open Ocean
Deoxygenation, Annu. Rev. Mar. Sci., 10, 229–260, 2017.
Lin, H.: The seasonal succession of modern planktonic foraminfiera: Sediment
traps observations from southwest Taiwan waters, Cont. Shelf Res., 84,
13–22, 2010.
Maas, A. E., Frazar, S. L., Outram, D. M., Seibel, B. A., and Wishner, K.
F.: Fine-scale vertical distribution of macroplankton and micronekton in the Eastern
Tropical North Pacific in association with an oxygen minimum zone, J.
Plankton Res., 36, 1557–1575, 2014.
Marchant, M., Hebbeln, D., and Wefer, G.: Seasonal flux patterns of planktic
foraminifera in the Peru–Chile Current, Deep-Sea Res., 45, 1161–1185,
1998.
Marshall, B. J., Thunell, R. C., Henehan, M. J., Astor, Y., and Wejnert, K. E.:
Planktonic foraminiferal area density as a proxy for carbonate ion concentration: A
calibration study using the Cariaco Basin ocean time series,
Paleoceanography, 28, 363–376, 2013.
Max, L., Rippert, N., Lembke-Jene, L., Mackensen, A., Nurnberg, D., and
Tiedemann, R.: Evidence for enhanced convection of North Pacific
Intermediate Water to the low? latitude Pacific under glacial conditions,
Paleoceanogr. Paleocl. 32, 41–55, 2017.
Medina Faull, L., Mara, P., Taylor, G. T., and Edgcomb, V. P.: Imprint of
trace dissolved oxygen on prokaryoplankton community structure in an Oxygen
Minimumz Zone, Front. Mar. Sci., 7, 360, https://doi.org/10.3389/fmars.2020.00360, 2020.
Meiland, J., Siccha, M., Weinkauf, M. F. G., Jonkers, L., Morard, R.,
Baranowski, U., Baumeister, A., Bertlich, J., Brummer, G.-J., Debray, P.,
Fritz-Endres, T., Groeneveld, J., Magerl, L., Munz, P., Rillo, M. C.,
Schmidt, C., Takagi, H., Theara, G., and Kucera, M.: Highly replicated
sampling reveals no diurnal vertical migration but stable species-specific
vertical habitats in planktonic foraminifera, J. Plankton Res., 41, 127–141,
2019.
Moffitt, S. E., Moffitt, R. A., Sauthoff, W., Davis, C. V., Hewett, K., and
Hill, T. M.: Paleoceanographic insights on recent oxygen minimum zone
expansion: Lessons for modern oceanography, PloS One, 10, e0115246, https://doi.org/10.1371/journal.pone.0115246, 2015.
Nomaki, H., Ogawa, N. O, 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, 2008.
Ohkushi, K., Kennett, J. P., Zeleski, C. M., Moffitt, S. E., Hill, T. M.,
Robert, C., Beaufort, L., and Behl, R. J.: Quantified intermediate water
oxygenation history of the NE Pacific: A new benthic foraminiferal record
from Santa Barbara basin, Paleoceanography, 28, 453–467, 2013.
Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R.,
O'hara, R. B.,
Simpson, G. L., Solymos, P., Stevens, M. H. H., and Wagner, H.: Package “vegan”, Community ecology package, version, 2, 1–295, 2013.
Orsi, W. D., Morard, R., Vuillemin, A., Eitel, M., Worheide, G., Milucka, J.,
and Kucera, M.: Anaerobic metabolism of Foraminifera thriving below the
seafloor, ISME J., 14, 2580–2594, 2020.
Ortiz, J. D., Mix, A. C., and Collier, R. W.: Environmental control of
living symbiotic and asymbiotic foraminifera of the California Current,
Paleoceanography, 10, 987–1009, 1995.
Ortiz, J. D., Mix, A., Rugh, W., Watkins, J., and Collier, R.: Deep-dwelling
planktonic foraminifera of the northeastern Pacific Ocean reveal
environmental control of oxygen and carbon isotopic disequilibria, Geochim.
Cosmochim. Ac., 60, 4509–4523, 1996.
Paulmier, A. and Ruiz-Pino, D.: Oxygen minimum zones (OMZs) in the modern
ocean, Prog. Oceanogr., 80, 113–128, 2009.
Paulmier, A., Ruiz-Pino, D., and Garçon, V.: The Oxygen Minimum Zone
(OMZ) off Chile as intense source of CO2 and N2O, Cont. Shelf Res.,
28, 2746–2756, 2008.
Paulmier, A., Ruiz-Pino, D., and Garçon, V.: CO2 maximum in the oxygen minimum zone (OMZ), Biogeosciences, 8, 239–252, https://doi.org/10.5194/bg-8-239-2011, 2011.
Perez-Cruz, L. L. and Machain-Castillo, M. L.: Benthic foraminifera of the
oxygen minimum zone, continental shelf of the Gulf of Tehuantepec, Mexico,
J. Foramin. Res., 20, 312–325, 1990.
Pina-Ocoa, E., Hogslund, S., Geslin, E., Cedhagen, T., Revsbech, N. P.,
Nielse, L. P., Schweizer, M., Jorissen, F., Rysgaard, S., Risgaard-Petersen,
N., and Canfield, D. E.: Widespread occurrence of nitrate storage and
denitrification among Foraminifera and Gromiida, P. Natl. Acad. Sci. USA, 107, 1148–1153, 2010.
Podlaska, A., Wakeham, S. G., Fanning, K. A., and Taylor, G. T.: Microbial
community structure and productivity in the oxygen minimum zone of the
eastern tropical North Pacific, Deep-Sea Res., 66, 77–89, 2012.
Rao, K. K., Jayalakshmy, K. V., Kumaran, S., Balasubramanian, T., and Kutty,
M. K.:
Planktonic foraminifera in waters off the Coromandel coast, Bay of Bengal,
Indian J. Mar. Sci., 18, 1–7, 1989.
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.
Ravelo, A. C. and Fairbanks, R. G.: Oxygen isotopic composition of multiple
species of planktonic foraminfera: Recorders of the modern photic zone
temperature, Paleoceanography, 7, 815–831, 1992.
R Core Team: A language and environment for statistical computing, R
Foundation for Statistical Computing, Vienna, Austria, 2017.
Rebotim, A., Voelker, A. H. L., Jonkers, L., Waniek, J. J., Meggers, H., Schiebel, R., Fraile, I., Schulz, M., and Kucera, M.: Factors controlling the depth habitat of planktonic foraminifera in the subtropical eastern North Atlantic, Biogeosciences, 14, 827–859, https://doi.org/10.5194/bg-14-827-2017, 2017.
Regenberg, M., Steph, S., Nurnberg, D., Tiedemann, R., and Garbe-Schonberg,
D.: Calibrating Mg Ca ratios of multiple planktonic foraminiferal species
with δ18O-calcification temperatures: Paleothermometry for the upper water
column, Earth Planet. Sc. Lett., 278, 324–336, 2009.
Richirt, J., Champmartin, S., Schweizer, M., Mouret, A., Petersen, J.,
Ambari, A., and Jorissen, F. J.: Scaling laws explain foraminiferal pore
patterns, Sci. Rep., 9, 9149, https://doi.org/10.1038/s41598-019-45617-x, 2019.
Rippert, N., Nurnberg, D., Raddatz, J., Maier, E., Hathorne, E. C., Bijma,
J., and Tiedemann, R.: Constraining foraminiferal calcification depths in
the western Pacific warm pool, Mar. Micropaleontol., 128, 14–27, 2016.
Rippert, N., Max, L., Mackensen, A., Cacho, I., Povea, P., and Tiedemann,
R.: Alternating influence of northern versus southern-sourced water masses
on the equatorial Pacific subthermocline during the past 240 ka,
Paleoceanogr. Paleocl., 32, 1256–1274, 2017.
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., Pina-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, 93–97, 2006.
Ross, B. J. and Hallock, P.: Dormancy in the Foraminfiera: A review, J.
Foramin. Res., 46, 358–368, 2016.
Russell, A. D., Honisch, B., Spero, H. J., and Lea, D. W.: Effects of
seawater carbonate ion concentration and temperature on shell U, Mg, and Sr
in cultured planktonic foraminifera, Geochim. Cosmochim. Ac., 68, 4347–4361,
2004.
Saito, T., Thompson, P. R., and Breger, D.: Skeletal ultramicrostructure
of some
elongate chambered planktonic foraminifera and related species, in:
Progress in Micropaleontology, edited by: Takayanagi, Y. and Saito, T.,
American Museum of Natural History, New York, NY, USA,
278–304, 1976.
Sautter, L. R. and Thunell, R. C.: Seasonal variability in the δ18O and δ13C
of planktic foraminifera from an upwelling environments: sediment trap
results from the San Pedro Basin, Southern California Bight,
Paleoceanography, 6, 307–334, 1991.
Schiebel, R. and Hemleben, C.: Planktic foraminifers in the modern ocean,
Springer, Berlin, Germany, 2017.
Schiebel, R., Zeltner, A., Treppke, U. F., Waniek, J. J., Bollmann, J., Rixen,
T., and Hemleben, C.: Distribution of diatoms, coccolithophores and
planktic foraminifers along a trophic gradient during SW monsoon in the
Arabian Sea, Mar. Micropaleontol., 3/4, 345–371, 2004.
Schmidtko, S., Stramma, L., and Visbeck, M.: Decline in global oceanic
oxygen content
during the past five decades, Nature, 542, 335–339, 2017.
Siccha, M. and Kucera, M.: ForCenS, a curated database of planktonic
foraminifera census counts in marine surface sediment samples, Sci. Data, 4,
170109, https://doi.org/10.1594/PANGAEA.873570, 2017.
Smart, S. M., Ren, H., Fawcett, S. E., Schiebel, R., Conte, M., Rafter, P.
A., Ellis, K. K.,
Weigand, M. A., Oleynik, S., Haug, G. H., and Sigman, D. M.: Ground-truthing
the planktic foraminifer-bound nitrogen isotope paleo-proxy in the Sargasso
Sea, Geochim. Cosmochim. Ac., 235, 463–482 2018.
Stramma, L., Johnson, G. C., Sprintall, J., and Mohrholz, V.: Expanding
Oxygen-Minimum Zones in the Tropical Oceans, Science, 320, 655–658, 2008.
Stramma, L., Johnson, G. C., Firing, E., and Schmidtko, S.: Eastern Pacific
oxygen minimum zones: Supply paths and multidecadal changes, J. Geophys.
Res.-Oceans, 115, C09011, https://doi.org/10.1029/2009JC005976, 2010.
Stramma, L., Prince, E. D., Schmidtko, S., Luo, J., Hoolihan, J. P.,
Visbeck, M., Wallace, D. W. R., Brandt, R., and Kortzinger, A.: Expansion of
oxygen minimum zones may reduce available habitat for tropical pelagic
fishes, Nat. Clim. Change, 2, 33–37, 2012.
USNO: USNO Astronomical Applications Department, available at: http://aa.usno.navy.mil/data/docs/MoonPhase.php, last access: 10 October 2019.
Venancio, I. M., Franco, D., Belem, A. L., Mulitza, S., Siccha, M.,
Albuquerue, A. L. S.,
Schulz, M., and Kucera, M.: Planktonic foraminifera shell fluxes from a
weekly resolved sediment trap record in the southwestern Atlantic: Evidence
for synchronized reproduction, Mar. Micropaleontol., 125, 25–35, 2016.
Weiner, A., Aurahs, R., Kurasawa, A., Kitazato, H., and Kucera, M.: Vertical
niche partitioning between cryptic sibling species of a cosmopolitan marine
planktonic protist, Mol. Ecol., 21, 4063–4073, 2012.
Wejnert, K. E., Thunell, R. C., and Astor, Y.: Comparison of
species-specific oxygen isotope paleotemperature equations: Sensitivity
analysis using planktonic foraminifera from the Cariaco Basin, Venezuela,
Mar. Micropaleontol., 101, 76–88, 2013.
Wishner, K. F., Ashjian, C. J., Gelfmann, C., Gowing, M. M., Kann, L.,
Levin, L. A., Mullineaux, L. S., and Saltzman, J.: Pelagic and benthic
ecology of the lower interface of the Eastern Tropical Pacific oxygen
minimum zone, Deep-Sea Res., 42, 93–115, 1995.
Wishner, K. F., Gowing, M. M., and Gelfman, C.: Mesozooplankton biomass in
the upper 1000 m in the Arabian Sea: overall seasonal and geographic
patterns, and relationship to oxygen gradients, Deep-Sea Res., 45,
2405–2432, 1998.
Wishner, K. F., Outram, D. M., Seibel, B. A., Daly, K. L., and Williams, R.
L.: Zooplankton in the eastern tropical north Pacific: Boundary effects of
oxygen minimum zone expansion, Deep-Sea Res., 79, 122–140, 2013.
Wishner, K. F., Seibel, B. A., Roman, C., Deutsch, C., Outram, D., Shaw, C.
T., Birk, M.
A., Mislan, K. A. S., Adams, T. J., Moore, D., and Riley, S.: Ocean
deoxygenation and zooplankton: Very small oxygen differences matter, Sci.
Adv., 4, eaau5180, https://doi.org/10.1126/sciadv.aau5180, 2018.
Wishner, K. F., Seibel, B., and Roman, C.: Event log from R/V Sikuliaq
SKQ201701S from January to February 2017, Biological and Chemical Oceanography Data
Management Office (BCO-DMO), available at: http://lod.bco-dmo.org/id/dataset/755088, last access: 27 May 2020a.
Wishner, K. F., Seibel, B., and Outram, D.: Ocean deoxygenation and copepods: coping with oxygen minimum zone variability, Biogeosciences, 17, 2315–2339, https://doi.org/10.5194/bg-17-2315-2020, 2020b.
Woehle, C., Roy, A.-S., Glock, N., Wein, T., Weissenbach, J., Rosenstiel,
P., Hiebenthal, C., Michels, J., Schonfeld, J., and Dagan, T.: A novel
eukaryotic denitrification pathway in foraminifera, Curr. Biol., 28,
2536–2543, 2018.
Altmetrics
Final-revised paper
Preprint