Articles | Volume 22, issue 14
https://doi.org/10.5194/bg-22-3463-2025
© Author(s) 2025. 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-22-3463-2025
© Author(s) 2025. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Reviews and syntheses: A trait-based approach to constrain controls on planktic foraminiferal ecology – key trade-offs and current knowledge gaps
School of Geography, Earth and Environmental Sciences, University of Birmingham, Birmingham, B15 2TT, UK
School of Earth Sciences, University of Bristol, Wills Memorial Building, Queen's Road, Bristol, BS8 1RJ, UK
Maria Grigoratou
School of Earth Sciences, University of Bristol, Wills Memorial Building, Queen's Road, Bristol, BS8 1RJ, UK
now at: European Polar Board, A Working Lab Universum, Universums gränd 8, 907 36 Umeå, Sweden
Fanny M. Monteiro
BRIDGE, School of Geographical Sciences, University of Bristol, Bristol, BS8 1SS, UK
iC3, Department for Geosciences, The Arctic University of Norway, 9010 Tromsø, Norway
Ruby Barrett
School of Earth Sciences, University of Bristol, Wills Memorial Building, Queen's Road, Bristol, BS8 1RJ, UK
School of Earth Sciences, University of Bristol, Wills Memorial Building, Queen's Road, Bristol, BS8 1RJ, UK
now at: School of Environmental Sciences, University of East Anglia, Norwich, NR4 7TJ, UK
Daniela N. Schmidt
School of Earth Sciences, University of Bristol, Wills Memorial Building, Queen's Road, Bristol, BS8 1RJ, UK
Related authors
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.
This article is included in the Encyclopedia of Geosciences
Tom Dunkley Jones, Yvette L. Eley, William Thomson, Sarah E. Greene, Ilya Mandel, Kirsty Edgar, and James A. Bendle
Clim. Past, 16, 2599–2617, https://doi.org/10.5194/cp-16-2599-2020, https://doi.org/10.5194/cp-16-2599-2020, 2020
Short summary
Short summary
We explore the utiliity of the composition of fossil lipid biomarkers, which are commonly preserved in ancient marine sediments, in providing estimates of past ocean temperatures. The group of lipids concerned show compositional changes across the modern oceans that are correlated, to some extent, with local surface ocean temperatures. Here we present new machine learning approaches to improve our understanding of this temperature sensitivity and its application to reconstructing past climates.
This article is included in the Encyclopedia of Geosciences
Gordon N. Inglis, Fran Bragg, Natalie J. Burls, Marlow Julius Cramwinckel, David Evans, Gavin L. Foster, Matthew Huber, Daniel J. Lunt, Nicholas Siler, Sebastian Steinig, Jessica E. Tierney, Richard Wilkinson, Eleni Anagnostou, Agatha M. de Boer, Tom Dunkley Jones, Kirsty M. Edgar, Christopher J. Hollis, David K. Hutchinson, and Richard D. Pancost
Clim. Past, 16, 1953–1968, https://doi.org/10.5194/cp-16-1953-2020, https://doi.org/10.5194/cp-16-1953-2020, 2020
Short summary
Short summary
This paper presents estimates of global mean surface temperatures and climate sensitivity during the early Paleogene (∼57–48 Ma). We employ a multi-method experimental approach and show that i) global mean surface temperatures range between 27 and 32°C and that ii) estimates of
This article is included in the Encyclopedia of Geosciences
bulkequilibrium climate sensitivity (∼3 to 4.5°C) fall within the range predicted by the IPCC AR5 Report. This work improves our understanding of two key climate metrics during the early Paleogene.
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.
This article is included in the Encyclopedia of Geosciences
Ruby Barrett, Joost de Vries, and Daniela N. Schmidt
Biogeosciences, 22, 791–807, https://doi.org/10.5194/bg-22-791-2025, https://doi.org/10.5194/bg-22-791-2025, 2025
Short summary
Short summary
Planktic foraminifers are a plankton whose fossilised shell weight is used to reconstruct past environmental conditions such as seawater CO2. However, there is debate about whether other environmental drivers impact shell weight. Here we use a global data compilation and statistics to analyse what controls their weight. We find that the response varies between species and ocean basin, making it important to use regional calibrations and consider which species should be used to reconstruct CO2.
This article is included in the Encyclopedia of Geosciences
Joost de Vries, Fanny Monteiro, Gerald Langer, Colin Brownlee, and Glen Wheeler
Biogeosciences, 21, 1707–1727, https://doi.org/10.5194/bg-21-1707-2024, https://doi.org/10.5194/bg-21-1707-2024, 2024
Short summary
Short summary
Calcifying phytoplankton (coccolithophores) utilize a life cycle in which they can grow and divide into two different phases. These two phases (HET and HOL) vary in terms of their physiology and distributions, with many unknowns about what the key differences are. Using a combination of lab experiments and model simulations, we find that nutrient storage is a critical difference between the two phases and that this difference allows them to inhabit different nitrogen input regimes.
This article is included in the Encyclopedia of Geosciences
Aaron A. Naidoo-Bagwell, Fanny M. Monteiro, Katharine R. Hendry, Scott Burgan, Jamie D. Wilson, Ben A. Ward, Andy Ridgwell, and Daniel J. Conley
Geosci. Model Dev., 17, 1729–1748, https://doi.org/10.5194/gmd-17-1729-2024, https://doi.org/10.5194/gmd-17-1729-2024, 2024
Short summary
Short summary
As an extension to the EcoGEnIE 1.0 Earth system model that features a diverse plankton community, EcoGEnIE 1.1 includes siliceous plankton diatoms and also considers their impact on biogeochemical cycles. With updates to existing nutrient cycles and the introduction of the silicon cycle, we see improved model performance relative to observational data. Through a more functionally diverse plankton community, the new model enables more comprehensive future study of ocean ecology.
This article is included in the Encyclopedia of Geosciences
Rachel A. Kruft Welton, George Hoppit, Daniela N. Schmidt, James D. Witts, and Benjamin C. Moon
Biogeosciences, 21, 223–239, https://doi.org/10.5194/bg-21-223-2024, https://doi.org/10.5194/bg-21-223-2024, 2024
Short summary
Short summary
We conducted a meta-analysis of known experimental literature examining how marine bivalve growth rates respond to climate change. Growth is usually negatively impacted by climate change. Bivalve eggs/larva are generally more vulnerable than either juveniles or adults. Available data on the bivalve response to climate stressors are biased towards early growth stages (commercially important in the Global North), and many families have only single experiments examining climate change impacts.
This article is included in the Encyclopedia of Geosciences
Rui Ying, Fanny M. Monteiro, Jamie D. Wilson, and Daniela N. Schmidt
Geosci. Model Dev., 16, 813–832, https://doi.org/10.5194/gmd-16-813-2023, https://doi.org/10.5194/gmd-16-813-2023, 2023
Short summary
Short summary
Planktic foraminifera are marine-calcifying zooplankton; their shells are widely used to measure past temperature and productivity. We developed ForamEcoGEnIE 2.0 to simulate the four subgroups of this organism. We found that the relative abundance distribution agrees with marine sediment core-top data and that carbon export and biomass are close to sediment trap and plankton net observations respectively. This model provides the opportunity to study foraminiferal ecology in any geological era.
This article is included in the Encyclopedia of Geosciences
Markus Adloff, Andy Ridgwell, Fanny M. Monteiro, Ian J. Parkinson, Alexander J. Dickson, Philip A. E. Pogge von Strandmann, Matthew S. Fantle, and Sarah E. Greene
Geosci. Model Dev., 14, 4187–4223, https://doi.org/10.5194/gmd-14-4187-2021, https://doi.org/10.5194/gmd-14-4187-2021, 2021
Short summary
Short summary
We present the first representation of the trace metals Sr, Os, Li and Ca in a 3D Earth system model (cGENIE). The simulation of marine metal sources (weathering, hydrothermal input) and sinks (deposition) reproduces the observed concentrations and isotopic homogeneity of these metals in the modern ocean. With these new tracers, cGENIE can be used to test hypotheses linking these metal cycles and the cycling of other elements like O and C and simulate their dynamic response to external forcing.
This article is included in the Encyclopedia of Geosciences
Joost de Vries, Fanny Monteiro, Glen Wheeler, Alex Poulton, Jelena Godrijan, Federica Cerino, Elisa Malinverno, Gerald Langer, and Colin Brownlee
Biogeosciences, 18, 1161–1184, https://doi.org/10.5194/bg-18-1161-2021, https://doi.org/10.5194/bg-18-1161-2021, 2021
Short summary
Short summary
Coccolithophores are important calcifying phytoplankton with an overlooked life cycle. We compile a global dataset of marine coccolithophore abundance to investigate the environmental characteristics of each life cycle phase. We find that both phases contribute to coccolithophore abundance and that their different environmental preference increases coccolithophore habitat. Accounting for the life cycle of coccolithophores is thus crucial for understanding their ecology and biogeochemical impact.
This article is included in the Encyclopedia of Geosciences
Tom Dunkley Jones, Yvette L. Eley, William Thomson, Sarah E. Greene, Ilya Mandel, Kirsty Edgar, and James A. Bendle
Clim. Past, 16, 2599–2617, https://doi.org/10.5194/cp-16-2599-2020, https://doi.org/10.5194/cp-16-2599-2020, 2020
Short summary
Short summary
We explore the utiliity of the composition of fossil lipid biomarkers, which are commonly preserved in ancient marine sediments, in providing estimates of past ocean temperatures. The group of lipids concerned show compositional changes across the modern oceans that are correlated, to some extent, with local surface ocean temperatures. Here we present new machine learning approaches to improve our understanding of this temperature sensitivity and its application to reconstructing past climates.
This article is included in the Encyclopedia of Geosciences
Gordon N. Inglis, Fran Bragg, Natalie J. Burls, Marlow Julius Cramwinckel, David Evans, Gavin L. Foster, Matthew Huber, Daniel J. Lunt, Nicholas Siler, Sebastian Steinig, Jessica E. Tierney, Richard Wilkinson, Eleni Anagnostou, Agatha M. de Boer, Tom Dunkley Jones, Kirsty M. Edgar, Christopher J. Hollis, David K. Hutchinson, and Richard D. Pancost
Clim. Past, 16, 1953–1968, https://doi.org/10.5194/cp-16-1953-2020, https://doi.org/10.5194/cp-16-1953-2020, 2020
Short summary
Short summary
This paper presents estimates of global mean surface temperatures and climate sensitivity during the early Paleogene (∼57–48 Ma). We employ a multi-method experimental approach and show that i) global mean surface temperatures range between 27 and 32°C and that ii) estimates of
This article is included in the Encyclopedia of Geosciences
bulkequilibrium climate sensitivity (∼3 to 4.5°C) fall within the range predicted by the IPCC AR5 Report. This work improves our understanding of two key climate metrics during the early Paleogene.
Cited articles
Adebayo, M. B., Bolton, C. T., Marchant, R., Bassinot, F., Conrod, S., and de Garidel-Thoron, T.: Environmental controls of size distribution of modern planktonic foraminifera in the tropical Indian Ocean, Geochem. Geophy. Geosy., 24, e2022GC010586, https://doi.org/10.1029/2022GC010586, 2023.
Alma, L., Kram, K. E., Holtgrieve, G. W., Barbarino, A., Fiamengo, C. J., and Padilla-Gamiño, J. L.: Ocean acidification and warming effects on the physiology, skeletal properties, and microbiome of the purple-hinge rock scallop, Comp. Biochem. Phys. A, 240, 110579, https://doi.org/10.1016/j.cbpa.2019.110579, 2020.
Andersen, K. H., Blanchard, J. L., Fulton, E. A., Gislason, H., Jacobsen, N. S., and van Kooten, T.: Assumptions behind size-based ecosystem models are realistic, ICES J. Mar. Sci., 73, 1651–1655, https://doi.org/10.1093/icesjms/fsv211, 2016.
Anderson, O. R. and Be, A. W. H.: The ultrastructure of a planktonic foraminifer, Globigerinoides sacculifer (Brady), and its symbiotic dinoflagellates, J. Foramin. Res., 6, 1–21, https://doi.org/10.2113/gsjfr.6.1.1, 1976.
Anderson, O. R., Spindler, M., Bé, A. W. H., and Hemleben, C.: Trophic activity of planktonic foraminifera, J. Mar. Biol. Assoc. UK, 59, 791–799, https://doi.org/10.1017/S002531540004577X, 1979.
Andres, K. J., Lodge, D. M., and Andrés, J.: Environmental DNA reveals the genetic diversity and population structure of an invasive species in the Laurentian Great Lakes, P. Natl. Acad. Sci. USA, 120, e2307345120, https://doi.org/10.1073/pnas.2307345120, 2023.
Armbrecht, L. H., Coolen, M. J. L., Lejzerowicz, F., George, S. C., Negandhi, K., Suzuki, Y., Young J., Foster N. R., Armand, L. K., Cooper, A., Ostrowski, M., Focardi, A., Stat, M., Moreau, J. W., and Weyrich, L. S.: Ancient DNA from marine sediments: precautions and considerations for seafloor coring, sample handling and data generation, Earth-Sci. Rev., 196, 102887, https://doi.org/10.1016/j.earscirev.2019.102887, 2019.
Aze, T., Ezard, T. H., Purvis, A., Coxall, H. K., Stewart, D. R., Wade, B. S., and Pearson, P. N.: A phylogeny of Cenozoic macroperforate planktonic foraminifera from fossil data, Biol. Rev. Camb. Philos. Soc., 86, 900–927, https://doi.org/10.1111/j.1469-185X.2011.00178.x, 2011.
Barker, S. and Elderfield, H.: Foraminiferal calcification response to glacial-interglacial changes in atmospheric CO2, Science, 297, 833–836, https://doi.org/10.1126/science.1072815, 2002.
Barrenechea Angeles, I., Lejzerowicz, F., Cordier, T., Scheplitz, J., Kucera, M., Ariztegui, J., and Morard, R.: Planktonic foraminifera eDNA signature deposited on the seafloor remains preserved after burial in marine sediments, Sci. Rep., 10, 20351, https://doi.org/10.1038/s41598-020-77179-8, 2020.
Barrett, R., de Vries, J., and Schmidt, D. N.: What controls planktic foraminiferal calcification?, Biogeosciences, 22, 791–807, https://doi.org/10.5194/bg-22-791-2025, 2025.
Barton, A. D., Pershing, A. J., Litchman, E., Record, N. R., Edwards, K. F., Finkel, Z. V., Kiørboe, T., and Ward, B. A.: The biogeography of marine plankton traits, Ecol. Lett., 16, 522–534, https://doi.org/10.1111/ele.12063, 2013.
Barton, A. D., Irwin, A. J., Finkel, Z. V., and Stock, C. A.: Anthropogenic climate change drives shift and shuffle in North Atlantic phytoplankton communities, P. Natl. Acad. Sci. USA, 113, 2964–2969, https://doi.org/10.1073/pnas.1519080113, 2016.
Beer, C. J., Schiebel, R., and Wilson, P. A.: Technical Note: On methodologies for determining the size-normalised weight of planktic foraminifera, Biogeosciences, 7, 2193–2198, https://doi.org/10.5194/bg-7-2193-2010, 2010.
Berberich, D.: Die planktische Foraminifere Neogloboquadrina pachyderma (Ehrenberg) im Weddellmeer, Antarktis, Berichte zur Polarfroschung, 195, 1–193, https://doi.org/10.2312/BzP_0195_1996, 1996.
Berger, W. H.: Planktonic foraminifera; sediment production in an oceanic front, J. Foramin. Res., 1, 95–118, https://doi.org/10.2113/gsjfr.1.3.95, 1971.
Bijma, J., Erez, J., and Hemleben, C.: Lunar and semi-lunar reproductive cycles in some spinose planktonic foraminifers, J. Foramin. Res., 20, 117–127, https://doi.org/10.2113/gsjfr.20.2.117, 1990.
Birch, H. S., Coxall, H. K., Pearson, P. N., Kroon, D., and Schmidt, D. N.: Partial collapse of the marine carbon pump after the Cretaceous-Paleogene boundary, Geology, 44, 287–290, https://doi.org/10.1130/g37581.1, 2016.
Bird, C., Darling, K. F., Russell, A. D., Davis, C. V., Fehrenbacher, J., Free, A., Wyman, M., and Ngwenya, B. T.: Cyanobacterial endobionts within a major marine planktonic calcifier (Globigerina bulloides, Foraminifera) revealed by 16S rRNA metabarcoding, Biogeosciences, 14, 901–920, https://doi.org/10.5194/bg-14-901-2017, 2017.
Bornemann, A. and Norris, R. D.: Size-related stable isotope changes in Late Cretaceous planktic foraminifera: Implications for paleoecology and photosymbiosis, Mar. Micropaleontol., 65, 32–42, https://doi.org/10.1016/j.marmicro.2007.05.005, 2007.
Boscolo-Galazzo, F., Crichton, K. A., Ridgwell, A., Mawbey, E. M., Wade, B. S., and Paul N., and Pearson, P. N.: Temperature controls carbon cycling and biological evolution in the ocean twilight zone, Science, 371, 1148–1152, https://doi.org/10.1126/science.abb6643, 2021.
Boyd, C. E. and Goodyear, C. P.: Nutritive quality of food in ecological systems, Arch. Hydrobiol., 69, 256–270, 1971.
Brandão, M. C., Benedetti, F., Martini, S., Soviadan, Y. D., Irisson, J.-O., Romagnan, J.-B., Elineau, A., Desnos, C., Jalabert, L., Freire, A. S., Picheral, M., Guidi, L., Gorsky, G., Bowler, C., Karp-Boss, L., Henry, N., de Vargas, C., Sullivan, M. B., Acinas, S. G., Babin, M., Bork, P., Boss, E., Bowler, C., Cochrane, G., de Vargas, C., Sullivan, M. B., Tara Oceans Consortium, Coordinators, Stemman, L., and Lombard, F.: Macroscale patterns of oceanic zooplankton composition and size structure, Scientific Reports, 11, 15714, https://doi.org/10.1038/s41598-021-94615-5, 2021.
Brasier, M. D. and Armstrong, H.: Foraminifera, in: Microfossils, Blackwell Publishing, 142–187, ISBN 0-632-05279-1, https://doi.org/10.1002/9781118685440, 2004.
Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M., and West, G. B.: Toward a metabolic theory of ecology, Ecology, 85, 1771–1789, https://doi.org/10.1890/03-9000, 2004.
Brummer, G.-J. A., Hemleben, C., and Spindler, M.: Ontogeny of extant spinose planktonic foraminifera (Globigerinidae): A concept exemplified by Globigerinoides sacculifer (Brady) and G. ruber (d'Orbigny), Mar. Micropaleontol., 12, 357–381, https://doi.org/10.1016/0377-8398(87)90028-4, 1987.
Brummer, G.-J. A. and Kučera, M.: Taxonomic review of living planktonic foraminifera, J. Micropalaeontol., 41, 29–74, https://doi.org/10.5194/jm-41-29-2022, 2022.
Buitenhuis, E. T., Hashioka, T., and Quéré, C. L.: Combined constraints on global ocean primary production using observations and models, Global Biogeochem. Cy., 27, 847–858, https://doi.org/10.1002/gbc.20074, 2013.
Bé, A. W. H.: An ecological, zoogeographic and taxonomic review of Recent planktonic foraminifera, in: Oceanic Micropaleontology, edited by: Ramsay, A. T. S., Academic Press, London, 1–100, ISBN 0125773013, 1977.
Bé, A. W. H. and Anderson, O. R.: Gametogenesis in planktonic foraminifera, Science, 192, 890–892, https://doi.org/10.1126/science.946914, 1976.
Bé, A. W. H. and Tolderlund, D. S.: Distribution and ecology of living planktonic foraminifera in surface waters of the Atlantic and Indian oceans, in: The Micropaleontology of Oceans, edited by: Funnel, B. M. and Riedel, W. R., Cambridge University Press, Cambridge, 105–149, ISBN-10: 0521076420, 1971.
Bé, A. W. H., Caron, D. A., and Anderson, O. R.: Effects of feeding frequency on life processes of the planktonic foraminifer Globigerinoides sacculifer in laboratory culture, J. Mar. Biol. Assoc. UK, 61, 257–277, https://doi.org/10.1017/S002531540004604X, 1981.
Bé, A. W. H., Spero, H. J., and Anderson, O. R.: Effects of symbiont elimination and reinfection on the life processes of the planktonic foraminifer Globigerinoides sacculifer, Mar. Biol., 70, 73–86, https://doi.org/10.1007/BF00397298, 1982.
Bé, A. W. H., Anderson, O. R., Faber Jr., W. W., and Caron, D. A.: Sequence of morphological and cytoplasmic changes during gametogenesis in the planktonic foraminifer Globigerinoides sacculifer (Brady), Micropaleontology, 29, 310–325, 1983.
Béjard, T. M., Rigual-Hernández, A. S., Tarruella, J. P., Flores, J.-A., Sanchez-Vidal, A., Llamas-Cano, I., and Sierro, F. J.: Planktonic foraminifera assemblage composition and flux dynamics inferred from an annual sediment trap record in the central Mediterranean Sea, Biogeosciences, 21, 4051–4076, https://doi.org/10.5194/bg-21-4051-2024, 2024.
Bentov, S. and Erez, J.: Impact of biomineralization processes on the Mg content of foraminiferal shells: A biological perspective, Geochem. Geophy. Geosys., 7, Q01P08, https://doi.org/10.1029/2005GC001015, 2006.
Bentov, S., Brownlee, C., and Erez, J.: The role of seawater endocytosis in the biomineralization process in calcareous foraminifera, P. Natl. Acad. Sci. USA, 106, 21500–21504, https://doi.org/10.1073/pnas.0906636106, 2009.
Bertlich, J., Gussone, N., Berndt, J., Arlinghaus, H. F., and Dieckmann, G. S.: Salinity effects on cultured Neogloboquadrina pachyderma (sinistral) from high latitudes: new paleoenvironmental insights, Geo-Mar. Lett, 41, 2, https://doi.org/10.1007/s00367-020-00677-1, 2021.
Burke, J. E., Elder, L. E., Maas, A. E., Gaskell, D. E., Clark, E. G., Hsiang, A. Y., Foster, G. L., and Hull, P. M.: Physiological and morphological scaling enables gigantism in pelagic protists, Limnol. Oceanogr., 70, 461–476, https://doi.org/10.1002/lno.12770, 2025.
Cao, Y., Lei, Y., Fang, J. K. H., and Li, T.: Molecular diversity of foraminiferal eDNA in sediments and their correlations with environmental factors from the Yellow Sea, Ecol. Indic., 142, 109294, https://doi.org/10.1016/j.ecolind.2022.109294, 2022.
Caromel, A. G. M., Schmidt, D. N., Phillips, J. C., and Rayfield, E. J.: Hydrodynamic constraints on the evolution and ecology of planktic foraminifera, Mar. Micropaleontol., 106, 69–78, https://doi.org/10.1016/j.marmicro.2014.01.002, 2014.
Caromel, A. G. M., Schmidt, D. N., Fletcher, I., and Rayfield, E. J.: Morphological Change During The Ontogeny Of The Planktic Foraminifera, J. Micropalaeontol., 35, 2–19, https://doi.org/10.1144/jmpaleo2014-017, 2016.
Caron, D. A., Bé, A. W. H., and Anderson, O. R.: Effects of variations in light intensity on life processes of the planktonic foraminifer Globigerinoides sacculifer in laboratory culture, J. Mar. Biol. Assoc. UK, 62, 435–451, https://doi.org/10.1017/S0025315400057374, 1982.
Caron, D. A., Faber, W. W., and Bé, A. W. H.: Effects of temperature and salinity on the growth and survival of the planktonic foraminifer Globigerinoides sacculifer, J. Mar. Biol. Assoc. UK, 67, 323–341, https://doi.org/10.1017/S0025315400026643, 1987.
Chernihovsky, N., Torfstein, A., and Almogi-Labin, A.: Daily timescale dynamics of planktonic foraminifera shell-size distributions, Front. Mar. Sci., 10, 1126398, https://doi.org/10.3389/fmars.2023.1126398, 2023.
Darling, K. F. and Wade, C. M.: The genetic diversity of planktic foraminifera and the global distribution of ribosomal RNA genotypes, Mar. Micropaleontol., 67, 216–238, https://doi.org/10.1016/j.marmicro.2008.01.009, 2008.
Davis, C. V., Livsey, C. M., Palmer, H. M., Hull, P. M., Thomas, E., Hill, T. M., and Benitez-Nelson, C. R.: Extensive morphological variability in asexually produced planktic foraminifera, Science Advances, 6, eabb8930, https://doi.org/10.1126/sciadv.abb8930, 2020.
Decelle, J., Romac, S., Stern, R. F., Bendif, E. M., Zingone, A., Audic, S., Guiry, M. D., Guillou, L., Tessier, D., Le Gall, F., Gourvil, P., Dos Santos, A. L., Probert, I., Vaulot, D., de Vargas, C., and Christen, R.: PhytoREF: a reference database of the plastidial 16S rRNA gene of photosynthetic eukaryotes with curated taxonomy, Mol. Ecol. Resour., 15, 1435–1445, https://doi.org/10.1111/1755-0998.12401, 2015.
del Campo, J., Carlos-Oliveira, M., Čepička, I., Hehenberger, E., Horák, A., Karnkowska, A., Kolisko, M., Lara, E., Lukeš, J., Pánek, T., Piwosz, K., Richter, D. J., Škaloud, P., Sutak, R., Tachezy, J., and Hampl, V.: The protist cultural renaissance, Trends Microbiol., 32, 128–131, https://doi.org/10.1016/j.tim.2023.11.010, 2024.
de Nooijer, L. J., Langer, G., Nehrke, G., and Bijma, J.: Physiological controls on seawater uptake and calcification in the benthic foraminifer Ammonia tepida, Biogeosciences, 6, 2669–2675, https://doi.org/10.5194/bg-6-2669-2009, 2009.
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.
de Nooijer, L. J., Pacho Sampedro, L., Jorissen, F. J., Pawlowski, J., Rosenthal, Y., Dissard, D., and Reichart, G. J.: 500 million years of foraminiferal calcification, Earth-Sci. Rev., 243, 104484, https://doi.org/10.1016/j.earscirev.2023.104484, 2023.
Deuser, W. G., Ross, E. H., Hemleben, C., and Spindler, M.: Seasonal changes in species composition, numbers, mass, size, and isotopic composition of planktonic foraminifera settling into the deep sargasso sea, Palaeogeogr. Palaeocl., 33, 103–127, https://doi.org/10.1016/0031-0182(81)90034-1, 1981.
Deutsch, C., Penn, J. L., and Seibel, B.: Metabolic trait diversity shapes marine biogeography, Nature, 585, 557–562, 2020.
de Vargas, C., Renaud, S., Hilbrecht, H., and Pawlowski, J.: Pleistocene adaptive radiation in Globorotalia truncatulinoides: genetic, morphologic, and environmental evidence, Paleobiology, 27, 104–125, https://doi.org/10.1666/0094-8373(2001)027<0104:PARIGT>2.0.CO;2, 2001.
de Vargas, C., Audic, S., Henry, N., Decelle, J., Mahé, F., Logares, R., Lara, E., Berney, C., Le Bescot, N., Probert, I., Carmichael, M., Poulain, J., Romac, S., Colin, S., Aury, J.-M,, Chaffron, S., Dunthorn, M., Engelen, S., Flegontova, O., Guidi, L., Horák, A., Jaillon, O., Lima-Mendez, G., Lukeš, J., Malviya, S., Morard, R., Mulot, M., calco, E., Siano, R., Vincent, F., Zingone, A., Dimier, C., Picheral, M,., Searson, S., Kandels-Lewis, S., Tara Oceans, Acinas, S.G., Bork, P., Bowler, C., Gorsky, G., Grimsley, N., Hingamp, P., Iudicone, D., Not, F., Ogata, H., Pesant, S., Raes, J., Sieracki, M.E., Speich, S., Stemmann, L., Sunagawa, S., Weissenbach, J., Wincker, P., and Karsenti, E.: Ocean plankton. Eukaryotic plankton diversity in the sunlit ocean, Science, 348, 1261605, https://doi.org/10.1126/science.1261605, 2015.
Dieckmann, G. S., Spindler, M., Lange, M. A., Ackley, S. F., and Eicken, H.: Antarctic sea ice; a habitat for the foraminifer Neogloboquadrina pachyderma, J. Foramin. Res., 21, 182–189, https://doi.org/10.2113/gsjfr.21.2.182, 1991.
Dutkiewicz, S., Follows, M. J., and Bragg, J. G.: Modeling the coupling of ocean ecology and biogeochemistry, Global Biogeochem. Cy., 23, GB4017, https://doi.org/10.1029/2008GB003405, 2009.
Dutkiewicz, S., Cermeno, P., Jahn, O., Follows, M. J., Hickman, A. E., Taniguchi, D. A. A., and Ward, B. A.: Dimensions of marine phytoplankton diversity, Biogeosciences, 17, 609–634, https://doi.org/10.5194/bg-17-609-2020, 2020.
Edgar, K. M., Bohaty, S. M., Gibbs, S. J., Sexton, P. F., Norris, R. D., and Wilson, P. A.: Symbiont “bleaching” in planktic foraminifera during the Middle Eocene Climatic Optimum, Geology, 41, 15–18, https://doi.org/10.1130/g33388.1, 2013.
Eiane, K. and Ohman, M. D.: Stage-specific mortality of Calanus finmarchicus, Pseudocalanus elongatus and Oithona similis on Fladen Ground, North Sea, during a spring bloom, Mar. Ecol. Prog. Ser., 268, 183–193, 2004.
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.
Faber, W. W., Anderson, O. R., and Caron, D. A.: Algal-foraminiferal symbiosis in the planktonic foraminifer Globigerinella aequilateralis; II, Effects of two symbiont species on foraminiferal growth and longevity, J. Foramin. Res., 19, 185–193, https://doi.org/10.2113/gsjfr.19.3.185, 1989.
Fenchel, T.: The Ecology of Heterotrophic Microflagellates, in: Advances in Microbial Ecology, edited by: Marshall, K. C., Springer US, Boston, MA, 57–97, https://doi.org/10.1007/978-1-4757-0611-6_2, 1986.
Fenton, I. S., Woodhouse, A., Aze, T., Lazarus, D., Renaudie, J., Dunhill, A. M., Young, J. R., and Saupe, E. E.: Triton, a new species-level database of Cenozoic planktonic foraminiferal occurrences, Sci. Data, 8, 160, https://doi.org/10.1038/s41597-021-00942-7, 2021.
Fenton, I. S., Aze, T., Farnsworth, A., Valdes, P., and Saupe, E. E.: Origination of the modern-style diversity gradient 15 million years ago, Nature, 614, 708–712, https://doi.org/10.1038/s41586-023-05712-6, 2023.
Follows, M. J., Dutkiewicz, S., Grant, S., and Chisholm, S. W.: Emergent biogeography of microbial communities in a model ocean, Science, 315, 1843–1846, https://doi.org/10.1126/science.1138544, 2007.
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, https://doi.org/10.2113/gsjfr.49.4.390, 2019.
Gast, R. J. and Caron, D. A.: Molecular phylogeny of symbiotic dinoflagellates from planktonic foraminifera and radiolaria, Mol. Biol. Evol., 13, 1192–1197, https://doi.org/10.1093/oxfordjournals.molbev.a025684, 1996.
Gaylord, B., Kroeker, K. J., Sunday, J. M., Anderson, K. M., Barry, J. P., Brown, N. E., Connell, S. D., Dupont, S., Fabricius, K. E., Hall-Spencer, J. M., Klinger, T., Milazzo, M., Munday, P. L., Russell, B. D., Sanford, E., Schreiber, S. J., Thiyagarajan, V., Vaughan, M. L. H., Widdicombe, S., and Harley, C. D. G.: Ocean acidification through the lens of ecological theory, Ecology, 96, 3–15, https://doi.org/10.1890/14-0802.1, 2015.
Gibbs, S. J., Bown, P. R., Ward, B. A., Alvarez, S. A., Kim, H., Archontikis, O. A., Sauterey, B., Poulton, A. J., Wilson, J., and Ridgwell, A.: Algal plankton turn to hunting to survive and recover from end-Cretaceous impact darkness, Sci. Adv., 6, eabc9123, https://doi.org/10.1126/sciadv.abc9123, 2020.
Goldstein, S. T.: Foraminifera: A biological review in Modern Foraminifera, edited by: Sen Gupta, B. K., Kluwer Academic Publishers, Dordrecht, 37–55, https://doi.org/10.1007/0-306-48104-9_3, 1999.
Greco, M., Morard, R., and Kucera, M.: Single-cell metabarcoding reveals biotic interactions of the Arctic calcifier Neogloboquadrina pachyderma with the eukaryotic pelagic community, J. Plankton Res., 43, 113–125, https://doi.org/10.1093/plankt/fbab015, 2021.
Greco, M., Westgård, A., Sykes, F. E., Ezat, M. M., and Meilland, J.: Uncovering hidden structures: previously undescribed pseudopodia and ectoplasmic structures in planktonic foraminifera, J. Plankton Res., 45, 652–660, https://doi.org/10.1093/plankt/fbad031, 2023.
Grice, G. D. and Hart, A. D.: The Abundance, Seasonal Occurrence and Distribution of the Epizooplankton between New York and Bermuda, Ecol. Monogr., 32, 287–309, https://doi.org/10.2307/1942377, 1962.
Grigoratou, M., Monteiro, F. M., Schmidt, D. N., Wilson, J. D., Ward, B. A., and Ridgwell, A.: A trait-based modelling approach to planktonic foraminifera ecology, Biogeosciences, 16, 1469–1492, https://doi.org/10.5194/bg-16-1469-2019, 2019.
Grigoratou, M., Monteiro, F. M., Ridgwell, A., and Schmidt, D. N.: Investigating the benefits and costs of spines and diet on planktonic foraminifera distribution with a trait-based ecosystem model, Mar. Micropaleontol., 166, 102004, https://doi.org/10.1016/j.marmicro.2021.102004, 2021.
Grigoratou, M., Monteiro, F. M., Wilson, J. D., Ridgwell, A., and Schmidt, D. N.: Exploring the impact of climate change on the global distribution of non-spinose planktonic foraminifera using a trait-based ecosystem model, Glob. Change Biol., 28, 1063–1076, https://doi.org/10.1111/gcb.15964, 2022.
Haldane, J. B. S.: On Being the Right Size, Harper's Magazine, 152, 424–427, 1926.
Hemleben, C., Spindler, M., Breitinger, I., and Deuser, W.: Field and laboratory studies on the ontogeny and ecology of some globorotaliid species from the Sargasso Sea off Bermuda, J. Foramin. Res., 15, 254–272, https://doi.org/10.2113/gsjfr.15.4.254, 1985.
Hemleben, C., Spindler, M., Anderson, R. O.: Modern Planktonic Foraminifera, Springer-Verlag, Ney York, Berlin, Heidelberg, 363 pp., ISBN-13: 978-1-4612-8150-4, 1989.
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.
Hill, T. S. and Hoogenboom, M. O.: The indirect effects of ocean acidification on corals and coral communities, Coral Reefs, 41, 1557–1583, https://doi.org/10.1007/s00338-022-02286-z, 2022.
Hoadley, K. D., Lewis, A. M., Wham, D. C., Pettay, D. T., Grasso, C., Smith, R., Kemp, D. W., LaJeunesse, T. C., and Warner, M. E.: Host–symbiont combinations dictate the photo-physiological response of reef-building corals to thermal stress, Scientific Reports, 9, 9985, https://doi.org/10.1038/s41598-019-46412-4, 2019.
Hoppit, G. and Schmidt, D. N.: A Regional View of the Response to Climate Change: A Meta-Analysis of European Benthic Organisms' Responses, Front. Mar. Sci., 9, 896157, https://doi.org/10.3389/fmars.2022.896157, 2022.
Horne, C. R., Hirst, A. G., and Atkinson, D.: Seasonal body size reductions with warming covary with major body size gradients in arthropod species, P. Roy. Soc. B-Biol. Sci., 284, 20170238, https://doi.org/10.1098/rspb.2017.0238, 2017.
Hoshino, T. and Inagaki, F.: Distribution of eukaryotic environmental DNA in global subseafloor sediments, Progress in Earth and Planetary Science, 11, 19, https://doi.org/10.1186/s40645-024-00621-2, 2024.
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, https://doi.org/10.4319/lo.2011.56.2.0562, 2011.
Jonkers, L. and Kučera, M.: Global analysis of seasonality in the shell flux of extant planktonic Foraminifera, Biogeosciences, 12, 2207–2226, https://doi.org/10.5194/bg-12-2207-2015, 2015.
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.
Ketten, D. and Edmond, J.: Gametogenesis and calcification of planktonic Foraminifera, Nature 278, 546–548, https://doi.org/10.1038/278546a0, 1979.
Kimoto, K.: The “unusual” reproduction of planktonic foraminifera: an Asexual reproductive phase of Neogloboquadrina pachyderma (Ehrenberg), Anuario do Instituto de Geociencias, Universidade Federal do Rio de Janeiro, 29, 461, https://doi.org/10.11137/2006_1_461-461, 2006.
Kiørboe, T.: How zooplankton feed: mechanisms, traits and trade-offs, Biol. Rev., 86, 311–339, https://doi.org/10.1111/j.1469-185X.2010.00148.x, 2011.
Kiørboe, T., Visser, A., and Andersen, K. H.: A trait-based approach to ocean ecology, ICES J. Mar. Sci., 75, 1849–1863, https://doi.org/10.1093/icesjms/fsy090, 2018.
Knoll, A. H. and Follows, M. J.: A bottom-up perspective on ecosystem change in Mesozoic oceans, P. Roy. Soc. B-Biol. Sci., 283, 20161755, https://doi.org/10.1098/rspb.2016.1755, 2016.
Köhler-Rink, S. and Kühl, M.: The chemical microenvironment of the symbiotic planktonic foraminifer Orbulina universa, Mar. Biol. Res., 1, 68–78, https://doi.org/10.1080/17451000510019015, 2005.
Kucera, M.: Chapter Six Planktonic Foraminifera as Tracers of Past Oceanic Environments, Developments in Marine Geology, 1, 213–262, https://doi.org/10.1016/S1572-5480(07)01011-1, 2007.
LeKieffre, C., Spero, H. J., Russell, A. D., Fehrenbacher, J. S., Geslin, E., and Meibom, A.: Assimilation, translocation, and utilization of carbon between photosynthetic symbiotic dinoflagellates and their planktic foraminifera host, Mar. Biol., 165, 104, https://doi.org/10.1007/s00227-018-3362-7, 2018.
Leung, J. Y. S., Zhang, S., and Connell, S. D.: Is Ocean Acidification Really a Threat to Marine Calcifiers? A Systematic Review and Meta-Analysis of 980+ Studies Spanning Two Decades, Small, 18, 2107407, https://doi.org/10.1002/smll.202107407, 2022.
Litchman, E., Ohman, M. D., and Kiørboe, T.: Trait-based approaches to zooplankton communities, J. Plankton Res., 35, 473–484, https://doi.org/10.1093/plankt/fbt019, 2013.
Litchman, E., Edwards, K. F., and Boyd, P. W.: Toward trait-based food webs: Universal traits and trait matching in planktonic predator–prey and host–parasite relationships, Limnol. Oceanogr., 66, 3857–3872, https://doi.org/10.1002/lno.11924, 2021.
Lombard, F., Labeyrie, L., Michel, E., Spero, H. J., and Lea, D. W.: Modelling the temperature dependent growth rates of planktic foraminifera, Mar. Micropaleontol., 70, 1–7, https://doi.org/10.1016/j.marmicro.2008.09.004, 2009.
Lombard, F., da Rocha, R. E., Bijma, J., and Gattuso, J.-P.: Effect of carbonate ion concentration and irradiance on calcification in planktonic foraminifera, Biogeosciences, 7, 247–255, https://doi.org/10.5194/bg-7-247-2010, 2010.
Lombard, F., Labeyrie, L., Michel, E., Bopp, L., Cortijo, E., Retailleau, S., Howa, H., and Jorissen, F.: Modelling planktic foraminifer growth and distribution using an ecophysiological multi-species approach, Biogeosciences, 8, 853–873, https://doi.org/10.5194/bg-8-853-2011, 2011.
Lončarić, N., Brummer, G.-J. A., and Kroon, D.: Lunar cycles and seasonal variations in deposition fluxes of planktic foraminiferal shell carbonate to the deep South Atlantic (central Walvis Ridge), Deep-Sea Res. Pt. I, 52, 1178–1188, https://doi.org/10.1016/j.dsr.2005.02.003, 2005.
Lynch, M.: The Genetic interpretation of inbreeding depression and outbreeding depression, Evolution, 45, 622–629, https://doi.org/10.1111/j.1558-5646.1991.tb04333.x, 1991.
Malviya, S., Scalco, E., Audic, S., Vincent, F., Veluchamy, A., Poulain, J., Wincker, P., Iudicone, D., de Vargas, C., Bittner, L., Zingone, A., and Bowler, C.: Insights into global diatom distribution and diversity in the world's ocean, P. Natl. Acad. Sci. USA, 113, E1516–E1525, 2016.
Margulis, L.: Origins of species: acquired genomes and individuality, Biosystems, 31, 121–125, https://doi.org/10.1016/0303-2647(93)90039-F, 1993.
McKinney, M. L.: Trends in body-size evolution, in: Evolutionary Trends, edited by: McNamara, K. J., Belhaven Press, London, 75–118, ISBN-10: 0816512345 1990.
Meilland, J., Howa, H., Lo Monaco, C., and Schiebel, R.: Individual planktic foraminifer protein-biomass affected by trophic conditions in the Southwest Indian Ocean, 30° S–60° S, Mar. Micropaleontol., 124, 63–74, https://doi.org/10.1016/j.marmicro.2016.02.004, 2016.
Meilland, J., Ezat, M. M., Westgård, A., Manno, C., Morard, R., Siccha, M., and Kucera, M.: Rare but persistent asexual reproduction explains the success of planktonic foraminifera in polar oceans, J. Plankton Res., 45, 15–32, https://doi.org/10.1093/plankt/fbac069, 2023.
Meilland, J., Siccha, M., Morard, R., and Kucera, M.: Continuous reproduction of planktonic foraminifera in laboratory culture, J. Eukaryot. Microbiol., 71, e13022, https://doi.org/10.1111/jeu.13022, 2024.
Michaels, A. F., Caron, D. A., Swanberg, N. R., Howse, F., and Michaels, C. M.: Planktonic sarcodines (Acantharia, Radiolaria, Foraminifera) in surface waters near Bermuda: abundance, biomass and vertical flux, J. Plankton Res., 17, 131–163, 1995.
Monteiro, F. M., Bach, L. T., Brownlee, C., Bown, P., Rickaby, R. E. M., Poulton, A. J., Tyrrell, T., Beaufort, L., Dutkiewicz, S., Gibbs, S., Gutowska, M. A., Lee, R., Riebesell, U., Young, J., and Ridgwell, A.: Why marine phytoplankton calcify, Science Advances, 2, e1501822, https://doi.org/10.1126/sciadv.1501822, 2016.
Morard, R., Escarguel, G., Weiner, A. K., André, A., Douady, C. J., Wade, C. M., Darling, K. F., Ujiié, Y., Seears, H. A., Quillévéré, F., de Garidel-Thoron, T., de Vargas, C., and Kucera, M.: Nomenclature for the Nameless: A Proposal for an Integrative Molecular Taxonomy of Cryptic Diversity Exemplified by Planktonic Foraminifera, Syst. Biol., 65, 925–940, https://doi.org/10.1093/sysbio/syw031, 2016.
Morard, R., Darling, K. F., Weiner, A. K. M., Hassenrück, C., Vanni, C., Cordier, T., Henry, N., Greco, M., Vollmar, N. M., Milivojevic, T., Rahman, S. N., Siccha, M., Meilland, J., Jonkers, L., Quillévéré, F., Escarguel, G., Douady, C. J., de Garidel-Thoron, T., de Vargas, C., and Kucera, M.: The global genetic diversity of planktonic foraminifera reveals the structure of cryptic speciation in plankton, Biol. Rev., 99, 1218–1241, https://doi.org/10.1111/brv.13065, 2024.
Naidoo-Bagwell, A. A., Monteiro, F. M., Hendry, K. R., Burgan, S., Wilson, J. D., Ward, B. A., Ridgwell, A., and Conley, D. J.: A diatom extension to the cGEnIE Earth system model – EcoGEnIE 1.1, Geosci. Model Dev., 17, 1729–1748, https://doi.org/10.5194/gmd-17-1729-2024, 2024.
Nehrke, G., Keul, N., Langer, G., de Nooijer, L. J., Bijma, J., and Meibom, A.: A new model for biomineralization and trace-element signatures of Foraminifera tests, Biogeosciences, 10, 6759–6767, https://doi.org/10.5194/bg-10-6759-2013, 2013.
Neukermans, G., Bach, L. T., Butterley, A., Sun, Q., Claustre, H., and Fournier, G. R.: Quantitative and mechanistic understanding of the open ocean carbonate pump – perspectives for remote sensing and autonomous in situ observation, Earth-Sci. Rev., 239, 104359, https://doi.org/10.1016/j.earscirev.2023.104359, 2023.
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, https://doi.org/10.1029/95PA02088, 1995.
Otto, S. P. and Lenormand, T.: Resolving the paradox of sex and recombination, Nat. Rev. Genet., 3, 252–261, https://doi.org/10.1038/nrg761, 2002.
Pallacks, S., Ziveri, P., Schiebel, R., Vonhof, H., Rae, J. W. B., Littley, E., Garcia-Orellana, J., Langer, G., Grelaud, M., and Martrat, B.: Anthropogenic acidification of surface waters drives decreased biogenic calcification in the Mediterranean Sea, Communications Earth & Environment, 4, 301, https://doi.org/10.1038/s43247-023-00947-7, 2023.
Palmer, A. R.: Calcification in marine molluscs: how costly is it?, P. Natl. Acad. Sci. USA, 89, 1379–1382, https://doi.org/10.1073/pnas.89.4.1379, 1992.
Pawlowski, J., Lejzerowicz, F., and Esling, P.: Next-Generation Environmental Diversity Surveys of Foraminifera: Preparing the Future, Biol. Bull., 227, 93–106, 2014.
Pearson, P. N., Ditchfield, P. W., Singano, J., Harcourt-Brown, K. G., Nicholas, C. J., Olsson, R. K., Shackleton, N. J., and Hall, M. A.: Warm tropical sea surface temperatures in the Late Cretaceous and Eocene epochs, Nature, 413, 481–487, https://doi.org/10.1038/35097000, 2001.
Peters, R. H.: The Ecological Implications of Body Size, Cambridge Studies in Ecology, Cambridge University Press, Cambridge, https://doi.org/10.1017/CBO9780511608551, 1983.
Rebotim, A., Voelker, A. H. L., Jonkers, L., Waniek, J. J., Schulz, M., and Kucera, M.: Calcification depth of deep-dwelling planktonic foraminifera from the eastern North Atlantic constrained by stable oxygen isotope ratios of shells from stratified plankton tows, J. Micropalaeontol., 38, 113–131, https://doi.org/10.5194/jm-38-113-2019, 2019.
Ridgwell, A. and Zeebe, R. E.: The role of the global carbonate cycle in the regulation and evolution of the Earth system, Earth Planet. Sc. Lett., 234, 299–315, https://doi.org/10.1016/j.epsl.2005.03.006, 2005.
Riebesell, U., Fabry, V.J., Hansson, L., and Gattuso, J.-P. (Eds.): Guide to best practices for ocean acidification research and data reporting, Publications Office of the European Union, Luxembourg, 260 pp., https://doi.org/10.2777/66906, 2010.
Rillo, M. C., Miller, C. G., Kucera, M., and Ezard, T. H. G.: Intraspecific size variation in planktonic foraminifera cannot be consistently predicted by the environment, Ecol. Evol., 10, 11579–11590, https://doi.org/10.1002/ece3.6792, 2020.
Rink, S., Kühl, M., Bijma, J., and Spero, H. J.: Microsensor studies of photosynthesis and respiration in the symbiotic foraminifer Orbulina universa, Mar. Biol., 131, 583–595, https://doi.org/10.1007/s002270050350, 1998.
Ruppert, K. M., Kline, R. J., and Rahman, M. S.: Past, present, and future perspectives of environmental DNA (eDNA) metabarcoding: A systematic review in methods, monitoring, and applications of global eDNA, Global Ecology and Conservation, 17, e00547, https://doi.org/10.1016/j.gecco.2019.e00547, 2019.
Russell, A. D., Hönisch, 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, https://doi.org/10.1016/j.gca.2004.03.013, 2004.
Sanders, T., Schmittmann, L., Nascimento-Schulze, J. C., and Melzner, F.: High Calcification Costs Limit Mussel Growth at Low Salinity, Front. Mar. Sci., 5, 352, https://doi.org/10.3389/fmars.2018.00352, 2018.
Schiebel, R. and Hemleben, C.: Planktic Foraminifers in the Modern Ocean, Springer, Heidelberg, ISBN 978-3-662-50295-2, 2017.
Schiebel, R., Hiller, B., and Hemleben, C.: Impacts of storms on Recent planktic foraminiferal test production and CaCO3 flux in the North Atlantic at 47° N, 20° W (JGOFS), Mar. Micropaleontol., 26, 115–129, https://doi.org/10.1016/0377-8398(95)00035-6, 1995.
Schmidt, D. N., Renaud, S., and Bollmann, J.: Response of planktic foraminiferal size to late Quaternary climate change, Paleoceanography, 18, 1039, https://doi.org/10.1029/2002PA000831, 2003.
Schmidt, D. N., Renaud, S., Bollmann, J., Schiebel, R., and Thierstein, H. R.: Size distribution of Holocene planktic foraminifer assemblages: biogeography, ecology and adaptation, Mar. Micropaleontol., 50, 319–338, https://doi.org/10.1016/S0377-8398(03)00098-7, 2004.
Schmidt, D. N., Lazarus, D., Young, J. R., and Kucera, M.: Biogeography and evolution of body size in marine plankton, Earth-Sci. Rev., 78, 239–266, https://doi.org/10.1016/j.earscirev.2006.05.004, 2006.
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.
Shaked, Y. and de Vargas, C.: Pelagic photosymbiosis: rDNA assessment of diversity and evolution of dinoflagellate symbionts and planktonic foraminiferal hosts, Mar. Ecol. Prog. Ser., 325, 59–71, 2006.
Siccha, M. and Kucera, M.: ForCenS, a curated database of planktonic foraminifera census counts in marine surface sediment samples, Scientific Data, 4, 170109, https://doi.org/10.1038/sdata.2017.109, 2017.
Siebold, E. and Berger, W.: The Sea Floor: An Introduction to Marine Geology, Springer Verlag, Berlin, Heidelberg, New York, 356 pp., ISSN 2510-1307, 1993.
Spero, H. J. and Parker, S. L.: Photosynthesis in the symbiotic planktonic foraminifer Orbulina universa, and its potential contribution to oceanic primary productivity, J. Foramin. Res., 15, 273–281, https://doi.org/10.2113/gsjfr.15.4.273, 1985.
Spindler, M.: On the salinity tolerance of the planktonic foraminifer Neogloboquadrina pachyderma from Antarctic sea ice, Polar Biol., 9, 85–91, 1996.
Spindler, M. and Dieckmann, G. S.: Distribution and abundance of the planktic foraminifer Neogloboquadrina pachyderma in sea ice of the Weddell Sea (Antarctica), Polar Biol., 5, 185–191, https://doi.org/10.1007/BF00441699, 1986.
Spindler, M., Hemleben, C., Bayer, U., Bé, A. W. H., Anderson, O.R.: Lunar Periodicity of Reproduction in the Planktonic Foraminifer Hastigerina pelagica, Mar. Ecol. Prog. Ser., 1, 61–64, 1979.
Spindler, M., Hemleben, C., Salomons, J. B., and Smit, L. P.: Feeding behavior of some planktonic foraminifers in laboratory cultures, J. Foramin. Res., 14, 237–249, https://doi.org/10.2113/gsjfr.14.4.237, 1984.
Stoecker, D. K., Johnson, M. D., deVargas, C., and Not, F.: Acquired phototrophy in aquatic protists, Aquat. Microb. Ecol., 57, 279–310, 2009.
Strack, T., Jonkers, L., C. Rillo, M., Baumann, K.-H., Hillebrand, H., and Kucera, M.: Coherent response of zoo- and phytoplankton assemblages to global warming since the Last Glacial Maximum, Global Ecol. Biogeogr., 33, e13841, https://doi.org/10.1111/geb.13841, 2024.
Swezey, D. S., Boles, S. E., Aquilino, K. M., Stott, H. K., Bush, D., Whitehead, A., Rogers-Bennett, L., Hill, T. M., and Sanford, E.: Evolved differences in energy metabolism and growth dictate the impacts of ocean acidification on abalone aquaculture, P. Natl. Acad. Sci. USA, 117, 26513–26519, https://doi.org/10.1073/pnas.2006910117, 2020.
Sykes, F. E., Meilland, J., Westgård, A., Chalk, T. B., Chierici, M., Foster, G. L., and Ezat, M. M.: Large-scale culturing of the subpolar foraminifera Globigerina bulloides reveals tolerance to a large range of environmental parameters associated to different life-strategies and an extended lifespan, J. Plankton Res., 46, 403–420, https://doi.org/10.1093/plankt/fbae029, 2024.
Takagi, H., Kimoto, K., Fujiki, T., Kurasawa, A., Moriya, K., and Hirano, H.: Ontogenetic dynamics of photosymbiosis in cultured planktic foraminifers revealed by fast repetition rate fluorometry, Mar. Micropaleontol., 122, 44–52, https://doi.org/10.1016/j.marmicro.2015.10.003, 2016.
Takagi, H., Kimoto, K., Fujiki, T., and Moriya, K.: Effect of nutritional condition on photosymbiotic consortium of cultured Globigerinoides sacculifer (Rhizaria, Foraminifera), Symbiosis, 76, 25–39, https://doi.org/10.1007/s13199-017-0530-3, 2018.
Takagi, H., Kimoto, K., Fujiki, T., Saito, H., Schmidt, C., Kucera, M., and Moriya, K.: Characterizing photosymbiosis in modern planktonic foraminifera, Biogeosciences, 16, 3377–3396, https://doi.org/10.5194/bg-16-3377-2019, 2019.
Takagi, H., Kurasawa, A., and Kimoto, K.: Observation of asexual reproduction with symbiont transmission in planktonic foraminifera, J. Plankton Res., 42, 403–410, https://doi.org/10.1093/plankt/fbaa033, 2020.
Takahashi, K. and Bé, A. W. H.: Planktonic foraminifera: factors controlling sinking speeds, Deep Sea Research Part A. Oceanographic Research Papers, 31, 1477–1500, https://doi.org/10.1016/0198-0149(84)90083-9, 1984.
Thomsen, J., Casties, I., Pansch, C., Körtzinger, A., and Melzner, F.: Food availability outweighs ocean acidification effects in juvenile Mytilus edulis: laboratory and field experiments, Glob. Change Biol., 19, 1017–1027, 2013.
Topa, P., Faber, Ł., Tyszka, J., and Komosinski, M.: Modelling ecology and evolution of Foraminifera in the agent-oriented distributed platform, Journal of Computational Science, 18, 69–84, https://doi.org/10.1016/j.jocs.2016.07.009, 2017.
Vincent, E. and Berger, W. H.: Planktonic foraminifera and their use in paleoceanography, in: The Sea, edited by: Emiliani, C., John Wiley & Sons, New York, 1035–1119, ISBN 9780674017368, 1981.
Violle, C., Navas, M.-L., Vile, D., Kazakou, E., Fortunel, C., Hummel, I., and Garnier, E.: Let the concept of trait be functional!, Oikos, 116, 882–892, https://doi.org/10.1111/j.0030-1299.2007.15559.x, 2007.
Wade, B. S., Al-Sabouni, N., Hemleben, C., and Kroon, D.: Symbiont bleaching in fossil planktonic foraminifera, Evol. Ecol., 22, 253–265, https://doi.org/10.1007/s10682-007-9176-6, 2008.
Ward, B. B.: Oceans. How nitrogen is lost, Science, 341, 352–353, https://doi.org/10.1126/science.1240314, 2013.
Watson, S.-A., Morley, S. A., and Peck, L. S.: Latitudinal trends in shell production cost from the tropics to the poles, Science Advances, 3, e1701362, https://doi.org/10.1126/sciadv.1701362, 2017.
Weinkauf, M. F. G., Kunze, J. G., Waniek, J. J., and Kučera, M.: Seasonal Variation in Shell Calcification of Planktonic Foraminifera in the NE Atlantic Reveals Species-Specific Response to Temperature, Productivity, and Optimum Growth Conditions, PLOS ONE, 11, e0148363, https://doi.org/10.1371/journal.pone.0148363, 2016.
Weinkauf, M. F. G., Siccha, M., and Weiner, A. K. M.: Reproduction dynamics of planktonic microbial eukaryotes in the open ocean, J. R. Soc. Interface, 19, 20210860, https://doi.org/10.1098/rsif.2021.0860, 2022.
Westgård, A., Ezat, M. E., Chalk, T. B., Chierici, M., Foster, G. L., and Meilland, J.: Large-scale culturing of Neogloboquadrina pachyderma, its growth in, and tolerance of, variable environmental conditions, J. Plankton Res., 45, 732–745, 2023.
Westoby, M.: Trait-based ecology, trait-free ecology, and in between, New Phytol., 245, 33–39, https://doi.org/10.1111/nph.20197, 2024.
Wilkinson, M. D., Dumontier, M., Aalbersberg, I. J., Appleton, G., Axton, M., Baak, A., Blomberg, N., Boiten, J.-W., da Silva Santos, L. B., Bourne, P. E., Bouwman, J., Brookes, A. J., Clark, T., Crosas, M., Dillo, I., Dumon, O., Edmunds, S., Evelo, C. T., Finkers, R., Gonzalez-Beltran, A., Gray, A. J. G., Groth, P., Goble, C., Grethe, J. S., Heringa, J., ’t Hoen, P. A. C., Hooft, R., Kuhn, T., Kok, R., Kok, J., Lusher, S. J., Martone, M. E., Mons, A., Packer, A. L., Persson, B., Rocca-Serra, P., Roos, M., van Schaik, R., Sansone, S.-A., Schultes, E., Sengstag, T., Slater, T., Strawn, G., Swertz, M. A., Thompson, M., van der Lei, J., van Mulligen, E., Velterop, J., Waagmeester, A., Wittenburg, P., Wolstencroft, K., Zhao, J., and Mons, B.: The FAIR Guiding Principles for scientific data management and stewardship, Scientific Data, 3, 160018, https://doi.org/10.1038/sdata.2016.18, 2016.
Wirtz, K. W.: Who is eating whom? Morphology and feeding type determine the size relation between planktonic predators and their ideal prey, Mar. Ecol. Prog. Ser., 445, 1–12, https://doi.org/10.3354/meps09502, 2012.
Woodhouse, A., Swain, A., Fagan, W. F., Fraass, A. J., and Lowery, C. M.: Late Cenozoic cooling restructured global marine plankton communities, Nature, 614, 713–718, https://doi.org/10.1038/s41586-023-05694-5, 2023.
Ying, R., Monteiro, F. M., Wilson, J. D., and Schmidt, D. N.: ForamEcoGEnIE 2.0: incorporating symbiosis and spine traits into a trait-based global planktic foraminiferal model, Geosci. Model Dev., 16, 813–832, https://doi.org/10.5194/gmd-16-813-2023, 2023.
Ying, R., Monteiro, F.M., Wilson, J.D., Ödalen, M., and Schmidt, D.N.: Past foraminiferal acclimation capacity is limited during future climate warming, Nature, 636, 385–289, https://doi.org/10.1038/s41586-024-08029-0, 2024.
Short summary
Planktic foraminifera are microscopic marine organisms whose calcium carbonate shells provide valuable insights into past ocean conditions. A promising means of understanding foraminiferal ecology and their environmental interactions is to constrain their key functional traits relating to feeding, symbioses, motility, calcification, and reproduction. Here we review what we know of their functional traits, key gaps in our understanding, and suggestions on how to fill them.
Planktic foraminifera are microscopic marine organisms whose calcium carbonate shells provide...
Altmetrics
Final-revised paper
Preprint