Assessing foraminifera biomineralisation models through trace element data of cultures under variable seawater chemistry
Introduction
Geochemical proxy data from foraminifera forms the basis of much of our knowledge of palaeoceanography and past changes in Earth’s climate (e.g. Lear et al., 2000, Elderfield et al., 2012, Rosenthal et al., 2013). Furthermore, this group of unicellular organisms is responsible for a large proportion of oceanic CaCO3 production (Schiebel, 2002), and thus has resulted in a virtually continuous archive of planktonic and benthic species throughout the Cenozoic and beyond. As such, a considerable amount of research has focused on understanding the biomineralisation process in foraminifera (e.g. Erez, 2003, Bentov and Erez, 2006, de Nooijer et al., 2014, Toyofuku et al., 2017, Fehrenbacher et al., 2017). One principal goal of this work is to underpin empirical proxy calibrations between environmental conditions and shell geochemistry with a theoretical basis. Understanding how and why foraminifera modify the chemistry of seawater prior to calcification may improve the accuracy of foraminifera-derived palaeoclimate reconstructions and enable the identification of environmental conditions under which empirical calibrations may require adjustment. For example, the incorporation of Mg in planktonic foraminifera is sensitive to both temperature and the carbonate system (Russell et al., 2004, Evans et al., 2016b, Gray et al., 2018), yet correcting fossil Mg/Ca measurements for secular shifts in ocean carbonate chemistry remains challenging because it is unclear which carbonate system parameter(s) modulate calcification rate and shell Mg uptake (Bach, 2015, Allen et al., 2016, Henehan et al., 2017). Constraining how different foraminifera source and concentrate the inorganic carbon necessary for calcification may address this problem, whilst also providing invaluable information regarding the likely response of this important group of marine calcifiers to ocean acidification.
There is currently no consensus within the community on the fundamental mechanism by which foraminifera source the calcium and carbon necessary for mineralisation, highlighting the challenge of observing and analysing organisms typically less than a millimetre in diameter. Moreover, it indicates that different foraminifera may have evolved different biomineralisation strategies (ter Kuile et al., 1989, de Nooijer et al., 2014), especially between the very diverse benthic species which produce CaCO3 with a wide range of Mg/Ca ratios and chamber wall structures (e.g. Reiss, 1958, Bentov and Erez, 2006, Evans et al., 2015b, van Dijk et al., 2017). This contribution focuses on the rotaliid (hyaline or perforate) foraminifera, on which most palaeoceanic reconstructions are based.
Direct observation of intracellular processes poses obvious challenges, and as such much recent work has focused on inferences from the isotopic and elemental composition of foraminifera shells (e.g. Segev and Erez, 2006, Zeebe et al., 2008, Raitzsch et al., 2010, Vigier et al., 2015, Evans et al., 2016b). The justification for such studies is a relatively large body of literature on trace element and isotope incorporation into inorganic calcite, which forms the basis of inverse modelling the conditions at the site of calcification. A simple illustration of this is the observation that the Mg/Ca ratio of planktonic foraminifera is approximately twenty times lower than inorganic calcite precipitated from seawater (Mucci and Morse, 1983), providing strong evidence that some species possess a mechanism of excluding Mg before final precipitation of the shell. Based on both direct observation of cellular processes, and inferences such as this, two principal biomineralisation mechanisms have been proposed, briefly summarised here.
(1) The seawater vacuolisation model (SWV), in which ions are predominantly sourced from seawater vacuoles. This model is based on the observation that hyaline foraminifera, in particular Amphistegina lobifera, endocytose large quantities of seawater that are transported to the site of chamber formation in vacuoles (e.g. Bentov et al., 2009). Numerous experiments culturing foraminifera in seawater containing membrane-impermeable fluorescent markers such as calcein (623 Da) and FITC-dextran (10 kDa) demonstrates that seawater is present at the site of calcification (e.g. Erez, 2003, Dissard et al., 2009, Evans et al., 2015b). Furthermore, ‘pulse-chase’ experiments have been conducted by placing foraminifera into seawater containing FITC-dextran or calcein for a period of time, followed by a chase period in normal seawater (Bentov et al., 2009). Material precipitated during the chase period was strongly labelled, demonstrating that the seawater present at the site of biomineralisation must be derived (in part or entirely) from internal seawater vacuoles. Research utilising fluorescent pH indicators has shown that the pH of these vacuoles is increased to 1 unit above seawater (Bentov et al., 2009, de Nooijer et al., 2009), suggesting that they play an important role in concentrating carbon. Providing support for this is earlier experimental work using 14C tracer uptake to demonstrate that the hyaline species A. lobifera does indeed have a large inorganic carbon pool (ter Kuile and Erez, 1987, ter Kuile and Erez, 1988). The mechanism of the foraminifera carbon concentrating mechanism was later revealed through confocal microscope observations. Specifically, raising the pH of the vacuole would increase the DIC and by promoting CO2 diffusion directly from acidic vesicles in the cytosol, or possibly from the surrounding seawater (Bentov et al., 2009). Variations of this model invoke vacuole pH elevation through Na+-H+ active transport (pumps), which would also modify the vacuole [Li] and 7Li given that Na pumps are unlikely to be completely selective for Na+ over Li+ (Erez, 2003, Vigier et al., 2015). Therefore, this process may be associated with a minor modification in seawater elemental chemistry. A long-standing challenge of the model is that seawater vacuolisation alone does not explain how many species of foraminifera are able to form calcite shells with a Mg/Ca ratio 1–2 order of magnitude lower than inorganic calcite (e.g. Lea et al., 1999, Erez, 2003, Rosenthal et al., 2011). Therefore, an additional mechanism is required to remove Mg in the seawater vacuolisation model before final precipitation of the shell. This process has been variously suggested to relate to (i) active Mg removal through channelling and pumping (Erez, 2003, Bentov and Erez, 2006), (ii) uptake by mitochondria (Bentov and Erez, 2006, Spero et al., 2015), (iii) precipitation and removal of Mg-rich phases (Bentov and Erez, 2005, Khalifa et al., 2016), (iv) precipitation through an amorphous or metastable precursor phase (Jacob et al., 2017). Of course, two or several of these processes may act together.
(2) The Ca trans-membrane transport (TMT) model posits that the majority of the calcium required for calcification is channelled and pumped to the site of biomineralisation. The model is based on the example of coccolithophore calcification, in which Ca is indeed channelled and pumped to the calcifying vesicle. In order to explain the higher Mg/Ca ratio of foraminifera compared to coccolithophore calcite and the incorporation of membrane impermeable markers, the model requires a degree of passive seawater transport (Nehrke et al., 2013). It has been argued that this model avoids the requirement for foraminifera to cycle several times their own volume in seawater in order to source calcium exclusively through vacuolisation. For example, a hypothetical spherical foraminifera with a radius of 150 m has an internal volume of 0.014 l. In order to precipitate a chamber with a mass of 1 g it must cycle 1 l of seawater in order to source enough calcium. This is 70 times the volume of the foraminifer, which means that each individual must vacuolise its own volume of seawater every few hours, assuming chamber formation takes place a few times per week. Proponents of the TMT model argue that this is infeasible, and therefore that some proportion of the calcium must be pumped directly to the calcification site.
Both models require the concentration and conversion of carbon into a form useful for CaCO3 precipitation, given that calcification from seawater is ostensibly carbon limited ([] = 10.3 mM, DIC = 2 mM). This may be achieved through a carbon concentrating mechanism which creates an internal DIC pool (ter Kuile and Erez, 1987, Erez, 2003, de Nooijer et al., 2009), and diffusion of CO2 from the cytosol into vacuoles as described above. Recently, in the case of Ammonia, it has been suggested that acidification of the foraminifer microenvironment via proton pumping shifts seawater DIC from to CO2 (aq), a form that is readily diffused over cell membranes (Toyofuku et al., 2017).
We present new laser-ablation trace element data of two rotaliid foraminifera with contrasting Mg/Ca ratios, the low-Mg planktonic species Globigerinoides ruber (white) and the high-Mg benthic Operculina ammonoides, grown in modified seawater with variable Mg/Ca ratios and carbonate chemistries. We explore the contrasting control of the carbonate system and temperature on Mg incorporation between these species, and assess a variety of other trace elements (Li, Na, Mn, Sr, Ba) within the context of existing biomineralisation models. Along with a synthesis of data from key experiments conducted over the last few decades, we outline a set of observations that any such model must be able to explain.
Section snippets
Operculina ammonoides
Benthic foraminifera were collected from the North Beach, Eilat, Israel at a water depth of 20 m by scuba diving and transported to The Hebrew University of Jerusalem. Live foraminifera were identified as being those that climbed the sides of the container into which they were placed. The culturing procedure for Operculina ammonoides is described in detail in Evans et al. (2015b). Briefly, foraminifera were cultured in batches of 50 individuals in 150 ml flasks, sealed with a glass stopper and
Operculina ammonoides Mg/Ca and the carbonate system
Growth rate curves for the different carbonate chemistry experiments, and mean calcite deposited per individual are shown in the supporting material and Table 3 respectively. Growth rate, as monitored by alkalinity depletion (i.e. moles CaCO3 = (Eq. l−1 )/2), was widely divergent between cultures, as previously observed for O. ammonoides (Evans et al., 2015b). Foraminifera in the lowest pH experiment (Table 1) were unsurprisingly characterised by the lowest growth rate, however
Contrasting Mg incorporation in high and low-Mg foraminifera
Much of the geochemical literature on foraminifera in relation to biomineralisation models focuses on Mg incorporation because of the importance of formulating a mechanistic understanding of the Mg/Ca palaeothermometer, and because many species are able to regulate the Mg/Ca ratio of their shell. Of particular concern is the mechanism by which some foraminifera are able to reduce the Mg content of calcite by more than an order of magnitude compared to inorganic calcite precipitated from
Conclusions
Calibrating the relationship between foraminifera shell chemistry with all environmental factors that have undergone secular variation over geological time may represent an insurmountable challenge for the palaeoceanographic community. Given the biological and geochemical overprint that these processes exert on trace element and isotope systems in these tightly biologically-mediated calcites, developing a mechanistic understanding of the biomineralisation process is of fundamental importance.
At
Acknowledgements
We are grateful to Shai Oron (IUI, Eilat) for help with sample collection, and to Tom Barlow and Simon Chenery (BGS, UK) for ICPMS trace element analysis of seawater samples. LA-ICPMS work at RHUL was co-funded by SRIF3 (HEFCE) and NERC (NERC CC073) equipment grants. This research was supported by the Israel Science Foundation grant No. 790/16 to JE. We would like to thank the editor and reviewers for their time and constructive comments, which greatly improved this contribution.
References (92)
- et al.
Trace element proxies for surface ocean conditions: a synthesis of culture calibrations with planktic foraminifera
Geochim. Cosmochim. Acta
(2016) - et al.
Chemical and physical controls on the transformation of amorphous calcium carbonate into crystalline CaCO3 polymorphs
Geochim. Cosmochim. Acta
(2017) - et al.
The effects of PCO2 and temperature on magnesium incorporation in calcite in seawater and MgCl2-CaCl2 solutions
Geochim. Cosmochim. Acta
(1991) - et al.
The distribution of zinc, nickel, manganese, cadmium, copper, and iron in some surface waters from the world ocean
Mar. Chem.
(1974) - et al.
Biomineralization in perforate foraminifera
Earth Sci. Rev.
(2014) - et al.
Li, Sr, Mg, and Na in foraminiferal calcite shells from laboratory culture, sediment traps, and sediment cores
Geochim. Cosmochim. Acta
(1985) - et al.
Mg/Ca variation in planktonic foraminifera tests: implications for reconstructing palaeo-seawater temperature and habitat migration
Earth Planet. Sci. Lett.
(2003) - et al.
A biomineralization model for the incorporation of trace elements into foraminiferal calcium carbonate
Earth Planet. Sci. Lett.
(1996) - et al.
Calibrations for benthic foraminiferal Mg/Ca paleothermometry and the carbonate ion hypothesis
Earth Planet. Sci. Lett.
(2006) - et al.
Planktic foraminifera shell chemistry response to seawater chemistry: Pliocene–Pleistocene seawater Mg/Ca, temperature and sea level change
Earth Planet. Sci. Lett.
(2016)
Mg/Ca-temperature and seawater-test chemistry relationships in the shallow-dwelling large benthic foraminifer Operculina ammonoides
Geochim. Cosmochim. Acta
Eocene seasonality and seawater alkaline earth reconstruction using shallow-dwelling large benthic foraminifera
Earth Planet. Sci. Lett.
Voltage-independent calcium channels: regulation by receptors and intracellular calcium stores
Biochem. Pharmacol.
The effects of temperature, salinity, and the carbonate system on Mg/Ca in Globigerinoides ruber (white): a global sediment trap calibration
Earth Planet. Sci. Lett.
Li/Ca in multiple species of benthic and planktonic foraminifera: thermocline, latitudinal, and glacial-interglacial variation
Geochim. Cosmochim. Acta
Application of calcite Mg partitioning functions to the reconstruction of paleocean Mg/Ca
Geochim. Cosmochim. Acta
Planktic foraminifers as recorders of seawater Ba/Ca
Mar. Micropaleontol.
Uptake of sodium and potassium by calcite
Chem. Geol.
Effect of preservation state of planktonic foraminifera tests on the decrease in Mg/Ca due to reductive cleaning and on sample loss during cleaning
Chem. Geol.
Biomineralization pathways in a foraminifer revealed using a novel correlative cryo-fluorescence–SEM–EDS technique
J. Struct. Biol.
Controls on shell Mg/Ca and Sr/Ca in cultured planktonic foraminiferan, Globigerinoides ruber (white)
Earth Planet. Sci. Lett.
Barium partitioning in coccoliths of Emiliania huxleyi
Geochim. Cosmochim. Acta
Controls on magnesium and strontium uptake in planktonic foraminifera determined by live culturing
Geochim. Cosmochim. Acta
Sr, Cd, Mn and Co distribution coefficients in calcite as a function of calcite precipitation rate
Geochim. Cosmochim. Acta
Temperature dependence of 7Li, 44Ca and Li/Ca during growth of calcium carbonate
Earth Planet. Sci. Lett.
Manganese uptake during calcite precipitation from seawater: conditions leading to the formation of a pseudokutnahorite
Geochim. Cosmochim. Acta
The incorporation of and into calcite overgrowths: influences of growth rate and solution composition
Geochim. Cosmochim. Acta
Response of the coccolithophores Emiliania huxleyi and Coccolithus braarudii to changing seawater Mg2+ and Ca2+ concentrations: Mg/Ca, Sr/Ca ratios and 44/40Ca, 26/24Mg of coccolith calcite
Geochim. Cosmochim. Acta
Assessing the reliability of magnesium in foraminiferal calcite as a proxy for water mass temperatures
Geochim. Cosmochim. Acta
Coprecipitation of alkali metal ions with calcium carbonate
Geochim. Cosmochim. Acta
Distribution coefficient of ions between calcite and solution at 10–50 °C
Mar. Chem.
Magnesium and strontium compositions of recent symbiont-bearing benthic foraminifera
Mar. Micropaleontol.
Effects of seawater carbonate ion concentration and temperature on shell U, Mg, and Sr in cultured planktonic foraminifera
Geochim. Cosmochim. Acta
Timing and mechanism for intratest Mg/Ca variability in a living planktic foraminifer
Earth Planet. Sci. Lett.
Lithium isotopes in foraminifera shells as a novel proxy for the ocean dissolved inorganic carbon (DIC)
C.R. Geosci.
Mg/Ca in the benthic foraminifera Cibicidoides wuellerstorfi and Cibicidoides mundulus: temperature versus carbonate ion saturation
Earth Planet. Sci. Lett.
Comparison of two potential strategies of planktonic foraminifera for house building: Mg2+ or H+ removal?
Geochim. Cosmochim. Acta
Two voltage-gated, calcium release channels coreside in the vacuolar membrane of broad bean guard cells
Plant Cell
Dynamic activity-induced manganese-dependent contrast magnetic resonance imaging (DAIM MRI)
Magn. Reson. Med.
Reconsidering the role of carbonate ion concentration in calcification by marine organisms
Biogeosciences
The role of seawater endocytosis in the biomineralization process in calcareous foraminifera
Proc. Nat. Acad. Sci.
Novel observations on biomineralization processes in foraminifera and implications for Mg/Ca ratio in the shells
Geology
Impact of biomineralization processes on the Mg content of foraminiferal shells: a biological perspective
Geochem. Geophys. Geosyst.
Use of the fluorescent calcite marker calcein to label foraminiferal tests
J. Foramin. Res.
Mg/Ca–temperature proxy in benthic foraminifera: new calibrations from the Florida straits and a hypothesis regarding Mg/Li
Paleoceanography
Relationships between bottom water carbonate saturation and element/Ca ratios in coretop samples of the benthic foraminifera Oridorsalis umbonatus
Biogeosciences
Cited by (44)
Controls on potassium incorporation in foraminifera and other marine calcifying organisms
2023, Geochimica et Cosmochimica ActaSodium incorporation in foraminiferal calcite: An evaluation of the Na/Ca salinity proxy and evidence for multiple Na-bearing phases
2023, Geochimica et Cosmochimica ActaThe Mg/Ca proxy for temperature: A Uvigerina core-top study in the Southwest Pacific
2021, Geochimica et Cosmochimica ActaMagnesium partitioning into vaterite and its potential role as a precursor phase in foraminiferal Mg/Ca thermometer
2021, Earth and Planetary Science LettersBenthic foraminifera geochemistry as a monitoring tool for heavy metal and phosphorus pollution — A post fish-farm removal case study
2021, Marine Pollution BulletinCitation Excerpt :Based on Mg/Ca-temperature calibration previously performed on O. ammonoides (Evans et al., 2015), temperatures calculated using our Mg/Ca measurements are generally within range of the real temperatures measured during the month before collection (Table 4). Mg/Ca was previously shown to be significantly positively correlated with CO32− and Ωca and weakly positively correlated with pH over the range 7.46–8.23 (total scale), where in 25 °C mean Mg/Ca dropped below 144 mmol/mol in treatments with pH < 7.84 (Evans et al., 2018). In our study the samples with the highest Zn-Cu/Ca levels were collected in December 2009 (23.0–25.6 °C) and the corresponding Mg/Ca mean was 145.3 (Table 4).