PROYECCIONES Y SIMULACIONES DE ALTERNATIVAS DE POLÍTICAS PÚBLICAS

2.5.1 Crystallographic evidence for geochemically-driven aragonite formation in corals

In this study we characterize the crystallography and chemistry of coral aragonites compared to other forms of aragonite in order to better predict the physical nature of these aragonites and how these end-products of coral biomineralization may have formed. Rather than corals exhibiting the same aragonite crystallography as other biogenic aragonites (mollusks), our Rietveld refinement analyses of different aragonite XRD patterns indicate that coral aragonite unit cell parameters are distinct form mollusk aragonite (Figure 2.2, pearl= salmon right-pointing triangles) as well as geologically-formed aragonites (grey stars) and freshwater synthetic aragonite (dark blue left- facing triangles). Instead, coral aragonite is crystallographically indistinguishable from synthetic aragonites precipitated from seawater under a range of controlled pH and Ω conditions (Figure 2.2, blue triangles). Both corals and synthetic aragonites express the same magnitude of anisotropic elongations along all three axes relative to geologically-formed aragonites (Table 2.2). These similarities between coral and seawater synthetic aragonites observed by XRD measurements are supported by Raman spectroscopy measurements of coral aragonites

exhibiting the same FWHM ν1 mode as the f06 synthetic aragonite precipitated at a similar Ω as

54

Our findings that coral aragonite crystallography and bonding-environments resembles that of aragonite crystals inorganically formed from seawater suggests that coral aragonite is similarly formed via precipitation from aragonite-supersaturated seawater. A crystal formation mechanism that depends on seawater chemistry agrees with previous studies which suggest that corals draw in seawater as the initial ingredient to create aragonite (Gagnon et la., 2007;

Tambutté et al., 2011). This is supported by Rayleigh fractionation models which observe similarities between coral and synthetic aragonite trace element incorporation (Cohen et al., 2006; Gaetani and Cohen, 2006). Our observations that coral aragonite crystallography resembles seawater synthetic aragonites but not freshwater synthetic aragonite (Figure 2.2) further serves as evidence that corals likely precipitate aragonite that reflect seawater chemistry. Finally, juvenile scleractinian corals have been shown to reflect their seawater geochemical environments by precipitating calcite skeletons over aragonite skeletons when grown in Cretaceous-like, “calcite sea” seawater with lower Mg/Ca ratios (Higuchi et al., 2014). Based on their crystallographic dissimilarity, the material properties and mode of formation for coral aragonites are likely different from that of mollusk aragonites (Figure 2.4). Crystallographic distinctions between coral and mollusk aragonites reflect the clear

morphological differences between the acicular mineral habit of coral aragonite versus the tabular habit of mollusk aragonite (Holcomb et al., 2009; Gilbert et al., 2015). Mollusk aragonite formation is well-known to be biologically-controlled via ACC precursors (Weiss et al., 2002; Pokroy et al., 2006; 2007; Gilbert et al., 2015). In contrast, our crystallographic analyses corroborate previous crystal habit, carbonate bonding environment, and geochemical

observations comparing the similarities between synthetic and coral aragonites (Constantz, 1986; Holcomb et al. 2009; Cohen et al., 2009; DeCarlo et al., 2018) that point to coral aragonite formation as a geochemically-driven process. Our crystallography results do not corroborate results by Stolarski et al., (2007) which observe the same crystallographic trends in coral

aragonite lattice distortions as mollusk aragonite results reported by Pokroy et al., (2006; 2007). Instead, we suggest that the physical response of coral skeletal aragonite to surrounding ocean conditions and stressors, such as ocean acidification, should follow similar responses as synthetic seawater aragonites. As the end-products of coral biomineralization, a dominant geochemical control over coral aragonite mineral formation may similarly indicate a strong geochemical influence on coral skeleton growth.

While previous studies have demonstrated how coral aragonite resembles synthetic aragonites both morphologically and chemically (Holcomb et al., 2009; Gaetani and Cohen, 2006), this study goes beyond mineral morphology to prove that coral aragonite is identical to seawater synthetic aragonites from a quantitative crystallographic perspective. Based on this information, we suggest that coral aragonite formation is geochemically controlled and speculate that coral biomineralization is dependent on calcifying fluid chemistry and is sensitive to

seawater chemistry.

2.5.2 Differences in crystallography between corals and geological aragonites not driven by incorporation of organics

Recent studies on the nature of organics in coral skeletons have presented conflicting assumptions about the role of organics in biomineralization and how organics become incorporated into the skeleton as a skeletal organic matrix (SOM) (DeCarlo et al., 2018; Von

55

Euw et al., 2017). In this study we present a mineralogical perspective to addressing the role of organics in coral crystallography, which complements a recent Raman spectroscopy study, which observed no clear differences in organic content in coral aragonite and seawater synthetic

aragonites by measuring the background fluorescence signal in these aragonites (DeCarlo et al., 2018).

In previous study, the nature of coral aragonite has been assumed to follow the same crystallographic trends as other biogenic aragonites, where the difference in lattice parameters between mollusk aragonite and geologically-formed aragonite has been attributed to the 0.1–5 wt% incorporation of intercrystalline organic molecules in aragonite known to make up mollusk composite biominerals (Pokroy et al., 2004). This organic content in mollusk aragonite is

evidenced in our study by the very high fluorescence signal in the pearl sample as observed with Raman spectroscopy, whereas coral aragonites exhibit the same low levels of fluorescence as synthetic and geologically-formed aragonites (Figure 2.4). When we plot the background

fluorescence signals of all of the aragonite samples (except for the pearl sample) in this study, we observe a weak trend of decreasing fluorescence as a function of increasing unit cell volumes, due to the slightly higher fluorescent signals observed in geological aragonites compared to the corals (Supplementary Materials, Figure S2.3). This trend is the opposite of what we would expect if the larger unit cell volumes of corals compared to geological aragonites were due to the incorporation of organic molecules, as qualitatively assessed by increased fluorescent

background signals. As for the nature of mollusk aragonite, our XRD results do confirm

observations by Pokroy et al., (2004) on the crystallographic nature of mollusk nacre, that overall unit cell volume increases are due to an elongation along the c-axis and a-axis as well as a

shortening along the b-axis relative to geological aragonites (Figure 2.2). This is very different from our observations of coral aragonite, which expands along all axes relative to geological aragonite (Figure 2.2). This likely points to a different cause for anisotropic lattice distortions observed in corals relative to geological aragonites. We pwculate that lattice fistortions in coral with respect to geologically-formed aragonites could be driven by crystal growth parameters, such as crystal growth rate, which may introduce crystallographic distortions and incorporate more trace elements in faster-forming coral aragonite crystals, which would increase overall aragonite unit cell volumes. Our mollusk nacre sample also has a marked lower frequency Raman shift compared to our coral and geological aragonite samples (Figure 2.4), likely due to the organic content, however these values may not be entirely accurate because of the

abnormally high fluorescence background. In the future we would have to quantitatively measure the organic content of all of the aragonites in order to confirm that mollusk aragonite has higher organic contents than coral and other aragonites, but our findings do align with previous studies that estimate at least a 5× higher organic content in mollusk nacre versus coral skeletons (Gilbert et al., 2005; Pokroy et al., 2004). Finally, our organics-removal treatment to dissolve excess intercrystalline organic material from our biogenic aragonite samples did not have a significant effect on the background fluorescence or crystallography of our coral samples, but did have a marked effect on the mollusk pearl sample (Supplementary Materials, Figure S2.2), indicating that organics play a larger role in mollusk aragonite than they do in coral aragonite. While corals may use still use biomolecules to template skeletal architecture and aragonite precipitation by lowering the Gibbs free energy barrier with heterogeneous nucleation (De Yoreo et al., 2015), coral crystallography does not support the presence of significant inter- or intra-crystalline organics in skeletal aragonite (Pokroy et al., 2004; 2007). This has important implications for the

56

material nature of skeletal aragonite and how sensitive it may be to changing ocean chemistry and coral growth dynamics.

2.5.3 Relationships between trace element incorporations and crystallography As we suggest that the anisotropic lattice distortions in coral aragonites with respect to geologically-formed aragonites are not caused by the incorporation of organic matter, we measured the trace incorporations of elements (B, Mg, Sr, Ba) into coral skeletons and other aragonites in order to assess whether they may be associated with distortions in coral

crystallography and carbonate bonding environments. We do observe that unit cell volumes increase as functions of B/Ca and Sr/Ca ratios yet decrease as functions of Mg/Ca and Ba/Ca ratios (Figure 2.7) with anisotropic responses along the three axes to these incorporations (Supplementary materials, Figure S2.5). All three unit cell axes respond most strongly to incorporations of B and Sr, which also happen to be significantly more abundant in coral and synthetic aragonites precipitated from seawater than in geological aragonites (Figure 2.6). We also observe a slight decrease in FWHM ν1 and Raman-derived Ωcf as functions of increasing

Ba/Ca incorporations in all samples and a slight increase in FWHM ν1 as a function of increasing

Sr/Ca ratios for corals, seawater synthetic aragonites and geological aragonites (Supplementary materials, Figure S2.6). Thus, it is possible that these B and Sr incorporations may be associated in the process distorting unit cell lattices and driving the larger unit cell volumes and carbonate bonding environment disorder that we observe in coral and synthetic aragonites. Varying trace element incorporations in coral aragonites versus geological aragonites may be a byproduct of crystal growth parameters, such as faster crystal growth rates for coral aragonite crystals, which may lead to increased crystalline disorder accompanied by more trace incorporations of metals trapped during rapid mineral accretion (Watson, 2004; Gabitov et al., 2008; DeCarlo et al., 2015).

In coral aragonites, crystallographic distortions may be linked to Ωcf, which could

influence crystal growth rates. This is supported by our observations of B/Ca ratios trending moderately with both increasing FWHM v1 (R2= 0.44) and b-axis lengths (R2= 0.36), which

suggests that B incorporations may be linked to crystallographic changes along the b-axis and distortions in the v1 carbonate-group stretching mode (Figure 2.8). FWHM v1 is used to derive

estimates for Ωcf using Raman spectroscopy (DeCarlo et al., 2017). As expected from studies

which utilize δ11/10B isotopes to estimate Ωcf, we also observe a relatively strong trend between B

and Ωcf for coral and synthetic seawater aragonites (Figure 2.8, R2= 0.44) (Holcomb et al., 2014;

McCulloch et al., 2014). δ11/10_{B isotope-based estimates of Ω}

cf are derived from δ11/10B isotope-

based estimates of pHcf and assume that salinity, temperature, and the pKB of boric acid are

constant and that δ11/10B of the calcifying fluid is that same as that of seawater (McCulloch et al., 2014). Raman-based estimates for Ωcf are drawn from the relationship between δ11/10B-derived

Ωcf and the FWHM of the ν1 Raman mode (DeCarlo et al., 2017). Note that B/Ca is not the same

as δ11/10B used in boron isotope studies. Similar to how Mg-incorporation in Mg calcites drives disorder in the v1 Raman mode due to out-of-plane rotations of the carbonate groups (Bischoff et

al., 1985), B-incorporations may be involved in causing the Ωcf-driven disorder in coral aragonite

measured by Raman spectroscopy in this study via widening of the FWHM of the ν1 mode.

Further evidence that crystallographic disorder may be tied to Ωcf comes from comparisons of

57

sea corals incorporate more Mg and B into their skeletons while growing in seawater with markedly lower aragonite saturation states and slower growth rates than seawater environments for shallow-water corals. In our plot of decreasing Raman-derived Ωcf (a measure of disorder in

the carbonate bonding environment by FWHM ν1 mode) as a function of increasing B/Ca (Figure

2.8), we confirm that deep sea corals (violet circles) precipitate their skeletons at lower calcifying fluid aragonite saturation states with higher B/Ca ratios compared to shallow-water corals (green squares) (McCulloch et al., 2012b).