Intrashell Variability of Trace Elements in Benthic Foraminifera Grown Under High CO2 Levels
- 1Institute of Earth Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel
- 2Department of Earth Sciences, Royal Holloway University of London, Egham, United Kingdom
- 3Institute of Geosciences, Goethe-University, Frankfurt, Germany
A Corrigendum on
Intrashell Variability of Trace Elements in Benthic Foraminifera Grown Under High CO2 Levels
by Levi, A., Müller, W., and Erez, J. (2019). Front. Earth Sci. 7:247. doi: 10.3389/feart.2019.00247
In our original article an error occurred during its preparation. While the subject and the content of our paper is very different to that of Not et al. (2018), we used their introduction initially to obtain recent references on the effects of pCO2. By act of technical mistake, their introduction was copied into our manuscript during the initial writing process and then was not removed. We are deeply sorry for this mistake and would like to convey our sincere apologies to C. Not, B. Thibodeau, and Y. Yokoyama and to the journal for our oversight. We completely rewrote the introduction. We confirm that our experimental data and subsequent interpretation are original and genuine and only the introductory text was affected, which is now remedied.
(Not, C., Thibodeau, B., and Yokoyama, Y. (2018). Incorporation of Mg, Sr, Ba, U, and B in high-Mg calcite benthic foraminifers cultured under controlled pCO2. Geochem. Geophys. Geosyst. 19, 83–98. doi: 10.1002/2017GC007225)
A correction has been made to the introduction:
“Foraminifera shells are well-known archives for paleoceanography and paleoclimate reconstructions. In addition to the use of foraminifera for biostratigraphy and paleoecology (e.g., CLIMAP project, 1976; Crowley, 2000), stable isotopes (δ18O and δ13C), trace elements and their isotopes (Cd/Ca, Mg/Ca, U/Ca, δ11B, and more) are successfully used for studying past ocean chemistry and paleocirculation (e.g., Emiliani and Shackleton, 1974; Sanyal et al., 1996; Lea, 1999; Nürnberg, 2000; Barker and Elderfield, 2002; Lear et al., 2002; Katz et al., 2010; Allen et al., 2016; Foster and Rae, 2016). Recently it has been proposed that Na/Ca could be used to reconstruct past ocean calcium concentrations (Hauzer et al., 2018). However, different species of foraminifera at the same location show different shell chemistries and isotopic compositions, which are attributed to “vital effects” representing deviations from expected thermodynamic equilibrium (e.g., Erez, 1978). These deviations are mostly associated with the calcification process that is biologically controlled and thus may affect the incorporation of trace and minor elements and their isotopes into the calcite shells (e.g., Erez, 1978, 2003; Elderfield et al., 1996; Bentov and Erez, 2006; Zeebe et al., 2008; de Nooijer et al., 2014; Gussone et al., 2016). One of the main factors that control foraminiferal calcification is the carbonate system in seawater (e.g., ter Kuile et al., 1989; Spero et al., 1997; Erez, 2003). It is therefore expected that the increase in atmospheric CO2 (pCO2), causing ocean acidification, may reduce foraminiferal calcification as well as affect their shell chemistry (e.g., Erez, 2003; Kuroyanagi et al., 2009; Dias et al., 2010; Fujita et al., 2011; Vogel and Uthicke, 2012; McIntyre-Wressnig et al., 2013). For example Mg/Ca in planktic foraminifera shows species-specific sensitivity to the carbonate system (e.g., Russell et al., 2004; Kisakürek et al., 2008; Allen et al., 2016; Evans et al., 2016, 2018; Holland et al., 2017; Gray and Evans, 2019).
An additional complication in the study of foraminiferal proxies is the intra-shell compositional variability (or banding) within individual specimens of both planktic and benthic foraminifera. This has been demonstrated in both trace elements and stable isotopes (e.g., Erez, 2003; Eggins et al., 2004; Rollion-Bard et al., 2008; Hathorne et al., 2009; Branson et al., 2015; Spero et al., 2015; Jonkers et al., 2016; Fehrenbacher et al., 2017; van Dijk et al., 2017, 2019; Geerken et al., 2019; Davis et al., 2020). Intensive experimental work (Eggins et al., 2004; Spero et al., 2015; Jonkers et al., 2016; Fehrenbacher et al., 2017) on planktic foraminifera demonstrated that Mg-rich bands are deposited during the night hours while low-Mg bands are precipitated during the daytime, perhaps connected with mitochondrial activity. Erez (2003) proposed that in large benthic foraminifera banding occurs when a new chamber is created in a two-step process: the first layer of organic-rich matrix (primary calcite) is associated with high concentrations of trace elements, while the secondary thick layer, often termed lamination, covers the existing exposed chambers and is composed of low trace element calcite (secondary calcite). The alteration between high and low elemental bands may thus be attributed to the process of sequential chamber formation (Erez, 2003; Bentov and Erez, 2005, 2006). While this may explain the daily banding in planktic foraminifera that add a chamber every day, the banding phenomena overall are not well-understood. Furthermore, the effect of ocean acidification on the element banding is not known.
In this study, we measured the intra-shell variability of trace elements (B, Mg, Na, K, Sr, Ba, and U) in the two benthic foraminifera species Amphistegina lobifera and A. lessonii, cultured at four DIC concentrations (2,340, 2,420, 2,440, and 2,570 μM). These correspond to four pCO2 levels of 430, 560, 740, and 1,390 μatm. These two species are commonly found in coral-reef environments of the Gulf of Eilat, and as such they are an important component of the carbonate sediments in this marine environment (Reiss and Hottinger, 1984).
The authors apologize for this error and state that this does not change the scientific conclusions of the article in any way. The original article has been updated.
References
Allen, K. A., Hönisch, B., Eggins, S. M., Haynes, L. L., Rosenthal, Y., and Yu, J. (2016). Trace element proxies for surface ocean conditions: a synthesis of culture calibrations with planktic foraminifera. Geochim. Cosmochim. Acta 193, 197–221. doi: 10.1016/j.gca.2016.08.015
Barker, S., and Elderfield, H. (2002). Foraminiferal calcification response to glacial-interglacial changes in atmospheric Co2. Science 297, 833–836. doi: 10.1126/science.1072815
Bentov, S., and Erez, J. (2005). Novel observations on biomineralization processes in foraminifera and implications for Mg/Ca ratio in the shells. Geology 33, 841–844. doi: 10.1130/G21800.1
Bentov, S., and Erez, J. (2006). Impact of biomineralization processes on the Mg content of foraminiferal shells: a biological perspective. Geochem. Geophys. Geosyst. 7, 1010–1029. doi: 10.1029/2005GC001015
Branson, O., Kaczmarek, K., Redfern, S. A. T., Misra, S., Langer, G., Tyliszczak, T., et al. (2015). The coordination and distribution of B in foraminiferal calcite. Earth Planet. Sci. Lett. 416, 67–72. doi: 10.1016/j.epsl.2015.02.006
Davis, C. V., Fehrenbacher, J. S., Benitez-Nelson, C., and Thunell, R. C. (2020). Trace element heterogeneity across individual planktic foraminifera from the modern Cariaco basin. J. Foraminifer. Res. 50, 204–218. doi: 10.2113/gsjfr.50.2.204
de Nooijer, L. J., Spero, H. J., Erez, J., Bijma, J., and Reichart, G. J. (2014). Biomineralization in perforate foraminifera. Earth Sci. Rev. 135, 48–58. doi: 10.1016/j.earscirev.2014.03.013
Dias, B. B., Hart, M. B., Smart, C. W., and Hall-Spencer, J. M. (2010). Modern seawater acidification: the response of foraminifera to high-CO2 conditions in the Mediterranean Sea. J. Geol. Soc. Lond. 167, 843–846. doi: 10.1144/0016-76492010-050
Eggins, S. M., Sadekov, A., and De Deckker, P. (2004). Modulation and daily banding of Mg/Ca in Orbulina universa tests by symbiont photosynthesis and respiration: a complication for seawater thermometry? Earth Planet. Sci. Lett. 225, 411–419. doi: 10.1016/j.epsl.2004.06.019
Elderfield, H., Bertram, C. J., and Erez, J. (1996). A biomineralization model for the incorporation of trace elements into foraminiferal calcium carbonate. Earth Planet. Sci. Lett. 142, 409–423. doi: 10.1016/0012-821x(96)00105-7
Emiliani, C., and Shackleton, N. J. (1974). The Brunhes epoch: isotopic paleotemperatures and geochronology. Science 183, 511–514. doi: 10.1126/science.183.4124.511
Erez, J. (1978). Vital effect on stable-isotope composition seen in foraminifera and coral skeletons. Nature 273, 199–202. doi: 10.1038/273199a0
Erez, J. (2003). The Source of ions for biomineralization in foraminifera and their implications for paleoceanographic proxies. Rev. Mineral. Geochem. 54, 115–149. doi: 10.2113/0540115
Evans, D., Müller, W., and Erez, J. (2018). Assessing foraminifera biomineralisation models through trace element data of cultures under variable seawater chemistry. Geochim. Cosmochim. Acta 236, 198–217. doi: 10.1016/j.gca.2018.02.048
Evans, D., Wade, B. S., Henehan, M., Erez, J., and Müller, W. (2016). Revisiting carbonate chemistry controls on planktic foraminifera Mg/Ca: implications for sea surface temperature and hydrology shifts over the Paleocene-Eocene Thermal Maximum and Eocene-Oligocene transition. Clim. Past 12, 819–835. doi: 10.5194/cp-12-819-2016
Fehrenbacher, J. S., Russell, A. D., Davis, C. V., Gagnon, A. C., Spero, H. J., Cliff, J. B., et al. (2017). Link between light-triggered Mg-banding and chamber formation in the planktic foraminifera Neogloboquadrina dutertrei. Nat. Commun. 8, 1–10. doi: 10.1038/ncomms15441
Foster, G. L., and Rae, J. W. B. (2016). Reconstructing ocean pH with boron isotopes in foraminifera. Annu. Rev. Earth Planet. Sci. 44, 207–237. doi: 10.1146/annurev-earth-060115-012226
Fujita, K., Hikami, M., Suzuki, A., Kuroyanagi, A., Sakai, K., Kawahata, H., et al. (2011). Effects of ocean acidification on calcification of symbiont-bearing reef foraminifers. Biogeosciences 8, 2089–2098. doi: 10.5194/bg-8-2089-2011
Geerken, E., de Nooijer, L. J., Roepert, A., Polerecky, L., King, H. E., and Reichart, G. J. (2019). Element banding and organic linings within chamber walls of two benthic foraminifera. Sci. Rep. 9, 1–15. doi: 10.1038/s41598-019-40298-y
Gray, W. R., and Evans, D. (2019). Nonthermal influences on Mg/Ca in planktonic foraminifera: a review of culture studies and application to the last glacial maximum. Paleoceanogr. Paleoclimatol. 34, 306–315. doi: 10.1029/2018PA003517
Gussone, N., Filipsson, H. L., and Kuhnert, H. (2016). Mg/Ca, Sr/Ca and Ca isotope ratios in benthonic foraminifers related to test structure, mineralogy and environmental controls. Geochim. Cosmochim. Acta 173, 142–159. doi: 10.1016/j.gca.2015.10.018
Hathorne, E. C., James, R. H., and Lampitt, R. S. (2009). Environmental versus biomineralization controls on the intratest variation in the trace element composition of the planktonic foraminifera G. inflata and G. scitula. Paleoceanography 24, 1–14. doi: 10.1029/2009PA001742
Hauzer, H., Evans, D., Müller, W., Rosenthal, Y., and Erez, J. (2018). Calibration of Na partitioning in the calcitic foraminifer Operculina ammonoides under variable Ca concentration: toward reconstructing past seawater composition. Earth Planet. Sci. Lett. 497, 80–91. doi: 10.1016/j.epsl.2018.06.004
Holland, K., Eggins, S. M., Hönisch, B., Haynes, L. L., and Branson, O. (2017). Calcification rate and shell chemistry response of the planktic foraminifer Orbulina universa to changes in microenvironment seawater carbonate chemistry. Earth Planet. Sci. Lett. 464, 124–134. doi: 10.1016/j.epsl.2017.02.018
Jonkers, L., Buse, B., Brummer, G. J. A., and Hall, I. R. (2016). Chamber formation leads to Mg/Ca banding in the planktonic foraminifer Neogloboquadrina pachyderma. Earth Planet. Sci. Lett. 451, 177–184. doi: 10.1016/j.epsl.2016.07.030
Katz, M. E., Cramer, B. S., Franzese, A., Hönisch, B., Miller, K. G., Rosenthal, Y., et al. (2010). Traditional and emerging geochemical proxies in foraminifera. J. Foraminifer. Res. 40, 165–192. doi: 10.2113/gsjfr.40.2.165
Kisakürek, B., Eisenhauer, A., Böhm, F., Garbe-Schönberg, D., and Erez, J. (2008). Controls on shell Mg/Ca and Sr/Ca in cultured planktonic foraminiferan, Globigerinoides ruber (white). Earth Planet. Sci. Lett. 273, 260–269. doi: 10.1016/j.epsl.2008.06.026
Kuroyanagi, A., Kawahata, H., Suzuki, A., Fujita, K., and Irie, T. (2009). Impacts of ocean acidification on large benthic foraminifers: results from laboratory experiments. Mar. Micropaleontol. 73, 190–195. doi: 10.1016/j.marmicro.2009.09.003
Lea, D. W. (1999). “Trace elements in foraminiferal calcite,” in Modern Foraminifera (Dordrecht: Springer Netherlands), 259–277. doi: 10.1007/0-306-48104-9_15
Lear, C. H., Rosenthal, Y., and Slowey, N. (2002). Benthic foraminiferal Mg/Ca-paleothermometry: a revised core-top calibration. Geochim. Cosmochim. Acta 66, 3375–3387. doi: 10.1016/S0016-7037(02)00941-9
McIntyre-Wressnig, A., Bernhard, J. M., McCorkle, D. C., and Hallock, P. (2013). Non-lethal effects of ocean acidification on the symbiont-bearing benthic foraminifer Amphistegina gibbosa. Mar. Ecol. Prog. Ser. 472, 45–60. doi: 10.3354/meps09918
Nürnberg, D. (2000). Taking the temperature of past ocean surfaces. Science 289, 1698–1699. doi: 10.1126/science.289.5485.1698
Reiss, Z., and Hottinger, L. (1984). The Gulf of Aqaba: Ecological Micropaleontology. Springer Science & Business Media. doi: 10.1007/978-3-642-69787-6
Rollion-Bard, C., Erez, J., and Zilberman, T. (2008). Intra-shell oxygen isotope ratios in the benthic foraminifera genus Amphistegina and the influence of seawater carbonate chemistry and temperature on this ratio. Geochim. Cosmochim. Acta 72, 6006–6014. doi: 10.1016/J.GCA.2008.09.013
Russell, A. D., Hönisch, B., Spero, H. J., and Lea, D. W. (2004). Effects of seawater carbonate ion concentration and temperature on shell U, Mg, and Sr in cultured planktonic foraminifera. Geochim. Cosmochim. Acta 68, 4347–4361. doi: 10.1016/j.gca.2004.03.013
Sanyal, A., Hemming, N. G., Broecker, W. S., Lea, D. W., Spero, H. J., and Hanson, G. N. (1996). Oceanic pH control on the boron isotopic composition of foraminifera: evidence from culture experiments. Paleoceanography 11, 513–517. doi: 10.1029/96PA01858
Spero, H. J., Bijma, J., Lea, D. W., Bemis, B. E., and Bernis, B. E. (1997). Effect of seawater carbonate concentration on foraminiferal carbon and oxygen isotopes. Nature 390, 497–500. doi: 10.1038/37333
Spero, H. J., Eggins, S. M., Russell, A. D., Vetter, L., Kilburn, M. R., and Hönisch, B. (2015). Timing and mechanism for intratest Mg/Ca variability in a living planktic foraminifer. Earth Planet. Sci. Lett. 409, 32–42. doi: 10.1016/j.epsl.2014.10.030
ter Kuile, B., Erez, J., and Padan, E. (1989). Mechanisms for the uptake of inorganic carbon by two species of symbiont-bearing foraminifera. Mar. Biol. 103, 241–251. doi: 10.1007/BF00543354
van Dijk, I., de Nooijer, L. J., Boer, W., and Reichart, G. J. (2017). Sulfur in foraminiferal calcite as a potential proxy for seawater carbonate ion concentration. Earth Planet. Sci. Lett. 470, 64–72. doi: 10.1016/j.epsl.2017.04.031
van Dijk, I., Mouret, A., Cotte, M., Le Houedec, S., Oron, S., Reichart, G. J., et al. (2019). Chemical Heterogeneity of Mg, Mn, Na, S, and Sr in Benthic Foraminiferal Calcite. Front. Earth Sci. 7:281. doi: 10.3389/feart.2019.00281
Vogel, N., and Uthicke, S. (2012). Calcification and photobiology in symbiont-bearing benthic foraminifera and responses to a high CO2 environment. J. Exp. Mar. Biol. Ecol. 424–425, 15–24. doi: 10.1016/j.jembe.2012.05.008
Keywords: biomineralization, LA-ICPMS, foraminifera, Amphistegina, trace elements, Mg banding, DIC, primary calcite
Citation: Levi A, Müller W and Erez J (2021) Corrigendum: Intrashell Variability of Trace Elements in Benthic Foraminifera Grown Under High CO2 Levels. Front. Earth Sci. 9:681294. doi: 10.3389/feart.2021.681294
Received: 16 March 2021; Accepted: 08 April 2021;
Published: 07 May 2021.
Edited and reviewed by: Alexandra V. Turchyn, University of Cambridge, United Kingdom
Copyright © 2021 Levi, Müller and Erez. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Adam Levi, YWRhbS5sZXZpJiN4MDAwNDA7bWFpbC5odWppLmFjLmls