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Original Research ARTICLE

Front. Earth Sci., 04 October 2019 | https://doi.org/10.3389/feart.2019.00247

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

Two species of Amphistegina were cultured under four variable DIC concentrations (2340–2570 μM). The variability of trace elements within the foraminiferal shells was measured in the knob area of three individuals for each DIC treatment using LA-ICPMS. In individuals that showed significant growth (identified via 135Ba-enriched seawater), B, Na, and Sr showed an increase with DIC, while K and Mg were slightly lower or unchanged. Sharp transition zones between natural 135Ba and the ∼10-fold increased 135Ba in the shells represent one quarter of a new additional chamber, which occurs roughly once a week. The shape of the transition zone is best described by a logistic equation for population growth. We propose that this reflects the dynamics of seawater vacuoles that serve the biomineralization process and provide Ca and DIC for calcification of Amphistegina as described in previous publications (e.g., Bentov et al., 2009). LA-ICPMS profiles in the central knob (∼70 μm depth) also revealed previously described cyclical changes in concentration of Mg, each apparently representing a growth of a new chamber. Additional elements such as K, Na and U showed similar cycles with the same frequency and phase as the Mg cycles. Sr showed variability with similar frequency but not in-phase to those of the Mg. These multi-element cycles were found both in the newly grown calcite (elevated-135Ba) and in the natural skeleton regardless of the DIC treatments. These high Mg and multi-element cycles seem to be an essential part of the calcification process. They may originate from the interaction with the organic matrix resulting in elevated Mg and other elements in primary calcite while secondary calcite of the lamination process shows lower concentrations. It is also possible that primary calcite is enriched in trace elements if an Amorphous CaCO3 (ACC) or vaterite precursors are involved. In addition, Rayleigh fractionation from a semi-closed reservoir, the presence of high Mg in the lattice or any combination of the previous causes may explain the trace elements enrichment. Changes in the DIC did not affect the pattern of elemental cycles in these foraminifera, suggesting that this variability is inherent to the biomineralization process.

Introduction

The geochemistry of foraminifer shells often reflects the environmental conditions in which foraminifers calcified and offers an opportunity to reconstruct past environmental changes (Lea and Boyle, 1989; Nürnberg et al., 1996). Multiple elements incorporated into the shells have been used to reconstruct oceanographic parameters (Mg for temperature, Na for salinity), seawater chemistry (B for carbonate chemistry), biogeochemical cycling and ocean circulation (Lear et al., 2002, 2003; Yu and Elderfield, 2007, 2008; Wit et al., 2013). However, the mechanisms by which trace elements are incorporated into the shell and associated with carbonate are still controversial as contradictory behaviors have been observed (Elderfield, 1996; de Nooijer et al., 2009; Nehrke et al., 2013; Evans and Müller, 2018). It has been widely accepted that the endocytosis of seawater is required for the calcification process to happen (Erez, 2003; Bentov and Erez, 2006). The ensuing evolution of the encapsulated seawater is different according to the foraminifer structure. In foraminifers from porcelaneous/miliolid species, which form imperforate shells, the encapsulated seawater is modified and subsequently transported in the cell to create a unique internal pool containing dissolved inorganic carbon (DIC), calcium and trace elements for calcification (Bentov and Erez, 2006; de Nooijer et al., 2009, 2014). The high-Mg calcite needles produced during calcification are transported and released out of the test to form the new chamber wall (de Nooijer et al., 2009). In hyaline species, which form perforate shells, the encapsulated seawater is modified and transported in the cell to create distinct internal pools for DIC and cations such as Ca2+ or Mg2+ (Erez, 2003). Thus, in both type of calcification, the encapsulated seawater is chemically modified. Elderfield (1996) suggested that this modification is a response to Rayleigh distillation and the element to calcium ratio of the shell is a function of the calcium remaining in the internal pool. The existence of a metastable carbonate phase from which planktonic foraminifers form their shell was recently demonstrated (Jacob et al., 2017). Thus, the processes by which trace elements are incorporated to foraminifer shell and the rationale for the species-specific aspect of E/Ca is still equivocal. In addition, experimental data set on the incorporation processes of trace elements in foraminifers focus mainly on the incorporation of Mg and Sr (Erez, 2003; Nehrke et al., 2013; Geerken et al., 2018; Hori et al., 2018) although other trace element ratios (Ba/Ca, U/Ca, B/Ca, etc.) are described in foraminifer shells. Unfortunately, most of the studies focus on one or two ratios separately and only a limited number of studies (Gussone et al., 2016; van Dijk et al., 2017) have tried to find incorporation processes that would explain the ratio of several trace elements in foraminifer shells. However, strong relationships between empirical data and trace element ratios in benthic foraminifer shells have been widely observed and used to reconstruct environmental conditions. While Mg/Ca is widely used as a temperature proxy (Rosenthal et al., 1997; Rathmann et al., 2004), and carbonate geochemistry (Dissard et al., 2010), Sr/Ca has been linked to different parameters such as DIC (Keul et al., 2017), temperature and/or CO2–3 concentration (Reichart et al., 2003; Rosenthal et al., 2006), hydrostatic pressure (Elderfield, 1996), and Sr/Ca of seawater (Lear et al., 2003; Yu et al., 2014). The strong correlation between Ba concentration in deep water and alkalinity allowed the estimation of past ocean alkalinity using Ba/Ca in benthic foraminifers (Hall and Chan, 2004). U/Ca in foraminifers is thought to be negatively correlated to carbonate ion concentrations (Keul et al., 2013) and carbonate ion saturation state (Raitzsch et al., 2011b). B/Ca has been used to reconstruct the carbonate ion concentration and pH of water masses (Yu and Elderfield, 2007; Raitzsch et al., 2011a). In this study, we measured a variety of trace elements (B, Mg, Na, K, Sr, Ba, and U) relative to calcium in two benthic foraminifera species: Amphistegina lobifera and Amphistegina lessonii. The foraminifera cultured at four DIC (2340, 2420, 2440, and 2570 μM) treatments corresponding to four pCO2 levels (430, 560, 740, and 1390 μatm), in order to document the trace element behavior of these two symbiont bearing, high-Mg calcite, benthic foraminifera. These two species are commonly found in coral-reef environments in the Gulf of Eilat, as such they are an important component in the contribution to the creation of the carbonate sediment in this marine environment (Erez, 2003) and play a key role on the carbonate production of the reef. In addition, at similar pCO2, high-Mg calcite has been found to exceed the solubility of aragonite, and therefore of calcite, which means that high-Mg calcite foraminifers could be highly sensitive to change of pCO2. Thus, we investigated the influence of carbonate chemistry (pCO2) to the incorporation of trace elements.

Materials and Methods

Two sediment-producing benthic foraminifera A. lobifera and A. lessonii were selected for this study. These two species are common in the Gulf of Eilat, and are an important component in carbonate sediment in this marine environment (Erez, 2003) particularly in the area of the coral reef. Both species produce high-Mg calcite shells at approximately 3–4 mol% MgCO3 (Erez, 2003). The foraminifera were collected from stones covered with turf algae in the Gulf of Eilat (Aqaba) at 3–5 m water depth. They were sieved and the 400–600 μm fraction of approximately 1400 live individuals of each species was used for the experiment. Initially the foraminifera were cultured in seawater with Calcein dye (Sigma-Aldrich, 40 μM/L) for 3 days and then washed with seawater (Eilat seawater) and divided to six groups (four experimental groups and two control groups). Both species were cultured in seawater sealed 120 ml Erlenmeyer flasks in four different DIC treatments. During the experiment (14 weeks) the Erlenmeyer flasks were kept at constant temperature of 25°C and light intensity of 60 μmol photons m–2 s–1, with a diurnal cycle of 12 h light. Once a week water was exchanged and sampled for oxygen, DIC, alkalinity, and pH measurements (methods and results will be reported in a separate publication). The salinity was constant at 40.6%, the normal salinity of Eilat seawater.

Water Preparation

Initially 20 liters of Eilat seawater was filtered throughout a 0.22-μm filter and spiked with 135Ba (Oak Ridge National Laboratory, United States) to reach a concentration of factor of ∼10 from seawater that unequivocally allows the identification of post-culture growth segments by LA-ICPMS (Laser Ablation Inductively Coupled Plasma Mass Spectrometry). Five liters were transferred to a CO2 bubbling system to prepare four pCO2 concentrations, 430, 560, 740, and 1390 ppm. The prepared waters were transferred to sealed bags (Supelco 30229-U) from which the actual experimental water were used for periodic water exchange (∼ once per week). The alkalinity, pH, oxygen and DIC of the reservoirs were measured four times during the experiment. During the experiment, the DIC in the sealed reservoirs increased in all bags (in part due to microbial oxidation of DOM with oxygen depletion). The alkalinity values remained constant and averaged 2411 ± 17 μmol kg–1 while the pH decreased. The exact values and their effect on the physiology (photosynthesis, calcification and respiration) of these foraminifera will be described elsewhere. The average DIC valued for the whole experiment are 2340 μmol (low DIC marked as L), 2420 μmol (intermediate low, IL), 2440 μmol (intermediate high, IH) and 2570 μmol (high, H). Here we report mainly on the shell chemistry recorded in the knob area of these foraminifera.

Sample Preparation and Analysis

At the end of the experiments, the cleaning process was done in two phases. The foraminifera from each treatment were washed five times with distilled water and dried in the oven (50°C, 24 h) then counted, weighted (total weight) and transferred to the organic matter cleaning procedure, by soaking the specimens in sodium hypochlorite (Sigma-Aldrich, 1:10) overnight while shaking gently. Specimens were washed five times again in distilled water, dried, and weighed again (shell weight).

LA-ICPMS

From each treatment, three foraminifers of each species were selected for laser ablation ICPMS analyses. We selected specimens of approximately equal shell size and close to the mean size of each treatment in order to limit the size dependency of the shell chemistry (Elderfield et al., 2002; Friedrich et al., 2012). In addition we examined their growth (the presence of several non-fluorescent chambers past the Calcein stain, see SI). Foraminifers were loosely fixed on top of Blu-Tak inside 1 inch stainless steel rings and analyzed using the RESOlution M-50 LA system coupled to an Agilent 8800 triple-quadrupole ICPMS at Royal Holloway University of London (Müller et al., 2009). The analytical method was optimized for the determination of trace elements via slow depth-profiling (for details see Griffiths et al., 2013 and Evans et al., 2015). Laser spot size of 74 μm for A. lessonii and 96 μm for A. lobifera with repetition rate of 2 Hz was used to ablate into the knob with an approximate vertical drill rate of ∼0.15 μm/pulse. To improve sensitivity, 6 ml min–1 H2 was used as an additional diatomic gas, added to He downstream of the LA cell. Each specimen was ablated once for 240 s, which reached an ablation depth of ∼50–70 μm (Figure 1).

FIGURE 1
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Figure 1. (a) Schematic diagram of Amphistegina lobifera vertical cross section (Adapted from Reiss and Hottinger, 1984). The knob is an imperforated structure build like multi layers concentric dome. (b) Back scatter SEM image of a polished vertical section through the knob of A. lobifera (see Erez, 2003), note the thin dark layers representing ∼weekly chamber growth lines. These dark layers are rich in Mg and K as well as other trace elements (see Figs below). The laser drilling marked in red is roughly 70 mm deep. (c) Images of the actual ablation hole in the knob of A. lessonii (left) and A. lobifera (right).

Data Analysis

Data reduction was done with Iolite software (Paton et al., 2011), trace element DRS method (Woodhead et al., 2007) with NIST SRM 612 (Jochum et al., 2011) as external standard. Data processing performed off-line using a commercial software package (MATLAB R2017a, The MathWorks Inc., Natick, MA, 2000).

Results

Growth of Foraminifera

All four groups showed a positive growth based both on weekly alkalinity depletions and on final weighing as follows: Groups L, IL, IH, H (2340, 2420, 2440, 2570 μM DIC) increased their CaCO3 weight by ∼100, ∼70, ∼78, and ∼30%, respectively. As mentioned previously, a detailed report on the calcification and symbionts photosynthesis will be reported elsewhere. Here we concentrate on the variability of the internal shell chemistry as observed mainly with the LA-ICPMS.

As shown in Figure 1, LA profiles with high vertical resolution of 0.15 mm in the solid CaCO3 of the knob area were performed. 135Ba/Ca ratios in the knob of A. lobifera and in A. lessonii were used as a chemical marker for the start of new shell deposition during the experiment (Figures 2, 3). The transition zone is very clear for most of the specimens and reach a final 135Ba/Ca value of ∼0.2 μmol/mol that is similar in both A. lobifera and A. lessonii. This value is roughly 10 times higher than the natural ratio for this isotope. The transition zone is ∼15–20 μm wide in A. lessonii and ∼5–10 μm in A. lobifera. The new skeleton thickness shows large variability between individuals of the same treatment (i.e,. DIC values) that mask to a large extent the variability between the treatments (see further details in the section “Discussion”).

FIGURE 2
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Figure 2. The transition zone of 135Ba/Ca from natural to experimental calcite as obtained from LA-ICPMS in the knob area of A. lessonii (dotted black). A logistic population function was fitted to the data (red solid line). The correlation coefficients of the fitted lines are very high (R2 > 0.9). The dotted blue line is the Mg/Ca ratio and the high peaks represent new chambers growth. Note that there is no correlation between the newly grown calcite (high 135Ba) and the experimental DIC conditions. Replicates L3 and IL3 stopped growing in the middle of the transition zone and replicate H1 shows only new growth.

FIGURE 3
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Figure 3. The transition zone of 135Ba/Ca from natural to experimental calcite as obtained from LA-ICPMS in the knob area of A. lobifera (dotted black). A logistic function was fitted to the data (red solid line). The correlation coefficients of the fitted lines are very high (R2 > 0.9). The dotted blue line is the Mg/Ca ratios and the high peaks represent new chambers growth. Note that there is no correlation between the newly grown calcite (high 135Ba) and the experimental DIC conditions.

Based on the identity of the newly grown shell we describe below the elemental cycles within the knob and the overall average ratios of several elements in the new and the natural shell.

Element to Ca Variability in the Knob Profiles at Different DIC

For all the specimens we observe the previously described high and low Mg bands in the knob area (Erez, 2003). Most of the profiles (∼70 μm in length) comprise 7–8 bands of Mg rich layers that equals to 60–70% of the last growth circular whorl that contain ∼11–12 chambers in these organisms. Every high-Mg band represents a new chamber and is followed by a low-Mg band (Figures 4, 5). There is no apparent changes in the Mg banding (frequency and phase) as a function of the DIC treatment for both species, i.e., the newly precipitated cycles show continuation of the natural cycles. Here again the variability within treatment as large as the variability between DIC treatments (Figures 4, 5). A. lobifera showed Mg/Ca range of 20–75 mmol/mol, and shows A. lessoni lower range of 14 to 60 mmol/mol. The Mg/Ca cycles were used as a template for comparison to the other elements. The K/Ca cycles throughout the knob are similar to those of the Mg/Ca, both frequency and phase regardless of the DIC treatment (Figure 4). The K/Ca values ranged from 0.45 to 0.35 mmol/mol in A. lobifera and 0.3 to 0.42 mmol/mol in A. lessoni. The Na/Ca (Figure 5) varied from 7 to 14 in A. lobifera and from 6 to 14 mmol/mol in A. lessoni showing a decrease from the old shell (high values) to the new part of the shell (low values), the cycles however, are similar to the Mg/Ca regardless of the DIC treatment. Sr/Ca show the same trend of decreasing values from 1.2 to 2.1 mmol/mol and 1.25 to 2.4 mmol/mol, respectively. The Sr/Ca show the same number of cycles of the Mg/Ca but with a phase shift of ∼1/4 cycle (Figure 6). The U/Ca cycles are very similar to those of the Mg both in frequency and in phase, but has a general trend of increase in the new shell in all treatments (Figure 5).

FIGURE 4
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Figure 4. K/Ca and Mg/Ca ratios in the knob profile of A. lessonii and A. lobifera for one selected specimen from each DIC treatment (data for all the specimens are given in the Supplementary Material). Note that the K bands is following the Mg ones with high fidelity in both frequency and amplitude. These high Mg-K bands represent the dark layers shown in Fig 1b and are associated with the organic rich primary calcite while the thick low Mg-K bands represent the secondary calcite of the lamination process. The DIC treatment did not affect the elemental cycles.

FIGURE 5
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Figure 5. U/Ca and Mg/Ca ratios in the knob profile of A. lessonii and A. lobifera for one selected specimen for the four DIC treatments (all the data are given in the Supplementary Material). The two elements show similar cycles in both frequency and amplitude. In that respect, this is similar to the K/Ca ratio shown in Figure 4. The DIC treatment did not affect the elemental cycles.

FIGURE 6
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Figure 6. Na/Ca and Sr/Ca ratios in the knob profile of A. lessonii and A. lobifera for one selected specimen for each DIC treatments (all the data are given in the Supplementary Material). It should be noted that these two elements show less similarity to the Mg-K-U cycles shown in Figures 4, 5. On the whole, however, the number of cycles (i.e., the frequency) is similar to the those of Mg. The DIC treatment did not affect the elemental cycles.

Average Changes in Shell Composition at Different DIC

The average element to Ca ratios between the newly grown shell and the original natural shell are given in Table 1 and Figure 7 (A. lobifera) and 8 (A. lessoni). Significant differences between the new and natural shells were tested using Two Sample t-test (Table 2). Error bars in Figures 7, 8 represent ± the average standard deviation for the new and natural parts of the shell for each experimental DIC.

TABLE 1
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Table 1. Element to Ca ratios in the new shell precipitated under the experimental conditions and the natural original shell (Figures 7, 8).

FIGURE 7
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Figure 7. Averages of El/Ca ratios of the natural-original shells of Amphistegina lobifera in comparison with the newly grown shell under the DIC modified experimental conditions. For B/Ca, Na/Ca and Sr/Ca the new shell ratios are significantly lower than the original shell. For K/Ca and Mg/Ca the new shells show ratios that are significantly higher than the original shell (see Tables 1, 2 for statistics). 135Ba/Ca show the enrichment of the 135Ba that was added to the culture media to mark the newly precipitated calcite. The numbers on the colored pH bar represent the experimental average DIC measurements during the experiments.

TABLE 2
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Table 2. Two sample t-test P values (using matlab test2 function).

FIGURE 8
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Figure 8. Averages of El/Ca ratios of the natural-original shells Amphistegina lessonii in comparison with the newly grown shell under the DIC modified experimental conditions. For B/Ca, Na/Ca and Sr/Ca the new shell ratios are significantly lower than the original shell. For K/Ca and Mg/Ca the new shells show ratios that are variable, slight lower or similar to the original shell (see Tables 1, 2 for statistics). 135Ba/Ca show the enrichment of the 135Ba that was added to the culture media to mark the newly precipitated calcite. The numbers on the colored pH bar represent the experimental average DIC measurements during the experiments.

B/Ca, Na/Ca and Sr/Ca in the new shell of A. lobifera are significantly lower than the natural shell. For Mg/Ca and K/Ca the new shells show ratios that are significantly higher than the natural shell (Figure 7 and Tables 1, 2). For A. lessoni B/Ca, Na/Ca and Sr/Ca in the new shell ratios are significantly lower than the natural shell. The Mg/Ca and K/Ca of the new shells show ratios that are variable, slightly lower or similar to the natural shell (Figure 8 and Tables 1, 2) thus not affected by the DIC increase.

Discussion

Transition Zone Dynamics

The increase of the 135Ba in the newly precipitated shell due to the spike in the experimental medium, give a marker for the start of the new growing phase. The part of the increase in the 135Ba concentration to a steady state value (i.e., transition zone) can be used to understand the calcification mechanism. The transition shape is rather uniform and can be fitted with a logistic equation (Verhulst, 1938) that investigates a standard model of population growth in a constrained environment.

P ( t ) = K 1 + ( K - P 0 P 0 ) e - r t (1)

In the case P is the 135Ba concentration at given time, “K” is the maximum concentration of the 135Ba (∼ 0.2 μM), “P0” is the concentration at time zero, “r” is the rate constant and “t” is time (or depth). This equation represents biological population growth, which approaches a steady state “K” (Table 3). The application of this formulation can be justified if we think about the population of the seawater vacuoles that supply the 135Ba to the calcification site. The first vacuoles containing the spike dilute with the previous older vacuoles and with time the number of the new vacuoles increases (and the old vacuoles decrease) until all the vacuoles contain the Ba spike. The maximum concentration in the skeleton is determined by the distribution coefficient of Ba in the foraminiferal calcite.

TABLE 3
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Table 3. Logistic equation coefficients for the uptake of 135Ba into the skeleton of A. lobifera and A. lessonii.

In Figures 2, 3 (red line) we show the best fit of the logistic function to the 135Ba data (black dots). The correlation coefficients are very high (all above 0.9), suggesting that the model indeed describes well the data, and this supports the seawater vacuolization mechanism proposed by Bentov et al., 2009. In this case the “t” Parameter is distance in μm between the natural 135Ba (P0) and the equilibrium values of the spike (K), obviously, this distance represents the time of saturation of the 135Ba pool, which we assume is equal to the complete replacement of the old seawater vacuoles with the new ones. If we assume that Ba is following Ca during the calcification process, this indicates a very large internal Ca pool roughly equivalent to the amount of Ca in a new chamber (and the lamination process associated with these lamellar species). Such internal Ca pools were described by Erez, 2003 for A. lobifera. Such large concentration (∼ a few Molar) of Ca in this pool is most probably a solid phase, most likely amorphous calcium carbonate (ACC).

There is no clear relationship between the DIC treatments and the thickness of the transition zone possibly because the variability between individuals in each treatment was as large as the variability between treatments. Similarly, there was no significant correlation between the thickness of the transition zone and the new skeleton thickness or the rate constant parameter “r” and the total growth (Figure 9).

FIGURE 9
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Figure 9. The transition zone thickness (based on 135Ba) as a function of DIC. The two intermediate DIC treatments yielded a thicker transition zone. There are no simple relations between the thickness of the transitions zones and the total shell growth (second Y axis) of these treatments.

Trace Element in the Knob Profiles and the Role DIC

The shell (within the knob) is composed of three parts: the natural growth (before collection) the pre experiment (short maintenance of the foraminifera before the experiment while being labeled with Calcein), and finally the part that grew during the experiment labeled with 135Ba.

The Mg banding in these species is different from that observed in the planktonic species (e.g., Eggins et al., 2003, 2004) mainly because A. lobifera and A. lessonii are involute species with a central knob (where the measurements were made) that accumulate skeleton for each new chamber (Figure 1). In addition, Ampnistegina (both species) have a long life cycle (of 6–12 months) as opposed to the short life cycle of the planktonic ones (∼30 days or less).

The Mg in this genus (as well as in other foraminifera) show growth cycles of Mg rich layers that have been described before (Eggins et al., 2003; Erez, 2003; Fehrenbacher et al., 2017; Geerken et al., 2018, 2019). The Mg cycles are observed both in the natural and in the new skeleton (Figures 2, 3, blue dots), regardless of the large variations in the DIC. Surprisingly, the elevated DIC concentrations did not have a significant effect on the patterns of the intrashell variability. This is supported by Geerken et al. (2019) showing that the high and low concentration bands are not effected by salinity and temperature. On the other hand, the averages of the measured trace elements to calcium ratios in the newly calcified shells did show some changes compared to the previous natural shells that may be related to the DIC treatment (see below, Figures 7, 8 and Table 1). Unlike the previous observations on A. lobifera (Erez, 2003), the Mg banding signal from the LA-ICPMS is less regular and the peaks are less sharp. This probably occurs because of three main reasons: (1) The growth lines in the foraminifera shells in the knob area have a topography and are only semi parallel, especially for large ablation area of 4300 μm2 used in this study. (2) The difference between the EPMA 1 μm3 interaction volume (Erez, 2003) and the LA-ICPMS ∼ 700 μm3 ablation volume per shot, which averages out and smooth the sharp peaks that seen by the EPMA. (3) The volume above the laser spot (the cup and tubing leading to the ICPMS) may causes some mixing between the layers and thus smooth out the original signal.

The element concentration between the old and new parts of the shells show trends that may be related to the elevated DIC. B/Ca, Na/Ca and Sr/Ca showing decrease with elevated DIC (Figures 2A–C) while K/Ca, Mg/Ca and showing slight increase in A. lobifera (Figures 2D,E) that are reported before for other Ampnistegina species (van Dijk et al., 2017). In A. lessonii B/Ca, Na/Ca, and Sr/Ca also showing decrease with elevated DIC (Figures 3A–C) and in the K/Ca, Mg/Ca we not see any significant change (Figures 3D,E). The U showing increase with the elevated DIC in both Ampnistegina species but it is not significant because only three specimens per treatment was ablated and there are large variation between specimens inside each group. To address this element properly more work need to be done to gain more statistics on the influence of the DIC on U concentration.

The Effect of DIC on Intra-Shell Variability

While the intrashell variability in foraminifera is widely described both in planktonic and benthic foraminifera, the source of these variations is not well understood. Erez and Bentov suggested that these variations are alternations of primary and secondary calcite (Erez, 2003; Bentov and Erez, 2005, 2006; Geerken et al., 2018) associated with the buildup of every new chamber (Figure 10). The primary calcite is associated with the organic matrix (often termed as the Primary Organic Membrane, POM or Primary Organic Sheet, POS) that forms the shape or scaffold (also called the anlage) for the newly precipitating chamber. The primary calcite is composed of very small nuclei of trace elements-rich crystals that are formed on both sides of the organic matrix (Bentov and Erez, 2005). The secondary calcite represents the well-known process of layering (or lamination) in bilamellar foraminifera (Reiss, 1957, 1959). This involves precipitation of thick low Mg layers of flat semi-hexagonal radially (c-axis) oriented calcite crystals that cover the newly precipitated primary calcite and forms the radial structure all over the exposed chambers, leaving the pores open, in the last exposed whorl of chambers. As such, the layered shell is composed of alternations of primary organic and trace element rich calcite (Erez, 2003; Bentov and Erez, 2005, 2006; Bonnin et al., 2019) and secondary calcite that comprise more than 95% of the shell mass that is lower in organic and trace element content. Note however, that in addition to the primary and secondary calcites there is a third layer termed the inner lining, which precipitates, inside every chamber (Figure 10). This layer is not represented in the knob area (investigated here) and was recently well described for planktonic foraminifera (Fehrenbacher et al., 2017). The reasons for the trace elements enrichment in the primary calcite is not known; however, we speculate that it may result from the interactions with the organic matrix, as suggested also in a by Erez (2003),Geerken et al. (2019). Additionally precipitation of Vaterite and possibly ACC precursors of the primary calcite may be rich in trace elements (Jochum et al., 2011; Jacob et al., 2017). In the planktonic foraminifera that add a new chamber every day (Spero, 1987; Eggins et al., 2004; Fehrenbacher et al., 2017) we propose that the Mg rich primary calcite is precipitated during the night as indeed well documented by these authors. In the large benthic foraminifera, each growth of new chamber with all its layering is occurring at slower rates of roughly once a week to 10 days (age dependent). In the present study we found that in addition to Mg, S, and Na (Erez, 2003; Bentov and Erez, 2005, 2006; Fehrenbacher et al., 2017), there is also enrichment in K and Sr. Another possible explanation for the multi element high bands is that they represent precipitation from a semi-closed reservoir in which Ca is depleted relative to other ions (with distribution coefficient lower than 1) thus leading to an increase in their concentration relative to Ca (Elderfield, 1996). It is also possible that Mg is the key variable that changes its concentrations in the calcifying fluid and other elements are readily incorporated into the lattice due to the distortion of the crystal lattice (Mucci and Morse, 1983; Reeder et al., 1999). We cannot resolve with our data set the causes for these multi elemental cycles, but it should be mentioned that such cycles are also observed in other biomineralizing systems: clams (e.g,. Warter et al., 2018), corals (e.g., Vielzeuf et al., 2018) and others. Our observation that DIC did not affect the pattern of elemental cycles within the shells suggest that these variations are indeed an essential part of the calcification process that may be strongly biologically controlled and therefore are not influenced by the DIC. Recently Geerken et al. (2019) provided similar observations with respect to salinity and temperature. While the patterns of intrashell variability did not change, the average ratios of elemets to calcium did change in response to DIC (Figures 7, 8 and Table 1). Because our observations are based on very few individuals, we do feel that further mechanistic interpretation of these data is beyond the scope of this paper.

FIGURE 10
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Figure 10. Schematic drawing of a horizontal section showing the layering structure in laminated, perforate (calcitic radial) foraminiferal shell. These layers are represented also in the knob area of the two involute species of the genus Amphistegina in this study. Every new chamber contains thin layer of primary calcite (yellow) which precipitates over the primary organic sheet (POS) and is rich in Mg and other elements. The primary calcite is followed by a thick layer of secondary calcite (blue). The secondary calcite has much lower concentrations of Mg and other trace elements, which show radial crystal arrangement, described as “calcitic radial.” While the mechanism of formation of the primary calcite is not well known for this genus, the secondary calcite is precipitated from alkaline seawater vacuoles (Bentov et al., 2009). Each chamber contains another thin layer of calcite, the inner lining (red) which may also have laminations (Fehrenbacher et al., 2017). This scheme was originally suggested by Reiss, 1957, 1959 and here was modified from that of Erez (2003).

Conclusion

Intra-shell chemical variability of the large benthic foraminifera A. lobifera and A. lessonii that were cultured under four high DIC concentrations (2340–2570 μM) was measured in the knob area using LA-ICPMS. The LA profiles (in three specimens for each treatment per species) represent the growth history of last whorl of chambers (∼10) in these two species. The knob displays alterations of Mg-rich and Mg-poor layers. The high Mg layers are also rich in Na, U and K while Sr shows similar variability but out of phase with the Mg. The high Mg layers are associated with the primary calcite while the low-Mg layers of the secondary calcite have lower concentrations of minor and trace elements. The alternations between the high and low element bands in Amphistegina represent new chamber growth at a rate of ∼ once a week for these larger specimens. Furthermore, there is no significant influence of the DIC (pCO2) changes on the alternation bands. On the other hand, the averages of some element to calcium ratios (B, Na, and Sr) are lower than the original shell at higher DIC while Mg and K are similar or slightly higher than the natural shell. 135Ba was added to the culture media to mark the newly precipitated calcite. The dynamics of 135Ba incorporation into the knob area is well describes using the logistic population growth function. We propose that this may represent the population of seawater vacuoles that bring the ions to the calcification site and are inherent to the biomineralization mechanism of these foraminifera. As for the intrashell cycles, we did not observe a correlation between the 135Ba dynamics and the DIC treatments.

Author Contributions

JE designed and directed the study. AL performed the growth experiments and analyzed the data. WM performed LA-ICPMS analysis and processing. AL, JE, and WM wrote the manuscript.

Funding

This work was supported by Israel Science Foundation grants ISF grants 551/10 and 790/16 to JE.

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

We thank Dr. David Evans who helped with the analysis of the foraminifera using the LA-ICPMS. We thank the HUJI students Matan Yona, Hagar Hauzer, and Elana Palaria for their help in the field collections and the laboratory experiments.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/feart.2019.00247/full#supplementary-material

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Keywords: biomineralization, LA-ICPMS, foraminifera, Amphistegina, trace elements, Mg banding, DIC, primary calcite

Citation: Levi A, Müller W and Erez J (2019) Intrashell Variability of Trace Elements in Benthic Foraminifera Grown Under High CO2 Levels. Front. Earth Sci. 7:247. doi: 10.3389/feart.2019.00247

Received: 06 February 2019; Accepted: 04 September 2019;
Published: 04 October 2019.

Edited by:

Alberto Perez-Huerta, The University of Alabama, United States

Reviewed by:

Alexey Kamyshny, Ben-Gurion University of the Negev, Israel
William Patrick Gilhooly III, Purdue University Indianapolis, United States

Copyright © 2019 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, adam.levi@mail.huji.ac.il; adaml1215@gmail.com