Variable [Mg²⁺] in seawater forces mineralogy change in Spirobranchus cariniferus calcification

Highlights

• Five Mg/Ca ratios between 1.5 and 5.3 grew three southern hemisphere marine invertebrates.

• Mg/Ca = 1.5 forced blue tubeworm (Spirobranchus cariniferus) to calcify 2–4 wt% MgCO₃.

• Typical blue tubeworm calcite is 8–14 wt% MgCO₃, which was observed in Mg/Ca above 2.5.

Abstract

Environmentally-forced mineralogical change has implications for both strength and solubility of skeletal carbonate. Three marine invertebrates from the southern hemisphere were grown for 50 days in artificial seawater with different Mg/Ca ratios (1.5, 2.5, 3.5, 4.5 and 5.3). Blue mussels (Mytilus edulis) and jingle oysters (Anomia trigonopsis) showed no changes in mineralogy. Blue tubeworms (Spirobranchus cariniferus) were able to maintain their typical mineralogical composition (calcite with 8–12 wt% MgCO₃) at most seawater Mg concentrations. However, at the lowest Mg/Ca ratio (1.5), the tubeworms precipitated calcite with significantly lower amounts of MgCO₃ (2–4 wt% MgCO₃). Current models of passive calcification, based on a linear relationship between seawater Mg/Ca and calcite Mg content, do not accurately reflect this Mg-dependent stepwise change in minerology among organisms with an active calcification strategy. We propose a new “tipping-point” model that better describes the calcification response of blue tubeworms to changing environmental conditions. The boundary of this active/passive tipping point may be species-specific and may have consequences for preservation, alteration, and resilience of marine skeletal carbonate.

Introduction

Marine invertebrates produce shells for a wide variety of reasons, including protection from predation, access to the water column, and excretion of excess calcium. Among the most common biominerals is calcium carbonate (CaCO₃), which can be precipitated as one of several stable polymorphs; most commonly aragonite or calcite (Pokroy et al., 2015; Cusack and Freer, 2008). The orthorhombic structure of aragonite enables Ca-sized and larger (Sr, Ba) ions to substitute into the lattice. Conversely, the hexagonal structure of calcite allows for Ca-sized and smaller ions (Mg, Fe, Mn) to occasionally become incorporated via substitution for calcium (Ca). While Mg substitution into calcite can theoretically reach 45% by weight (wt%) in specific calcite locations, the range found in marine invertebrates is 0–20 wt% MgCO₃ (Long et al., 2014). Adding Mg to calcite (>4 wt% MgCO₃) improves its impact resistance, but also increases its susceptibility to dissolution in seawater (Andersson et al., 2007; Ries, 2010), reaching maximum solubility at about 11 wt% MgCO₃. A broad spectrum of Mg content in calcite occurs naturally in marine invertebrate calcite as biological needs and environments vary.

[Mg²⁺] and [Ca²⁺] in seawater have varied over the geological history of the oceans (Stanley and Hardie, 1998; Hardie, 2003; Roest-Ellis et al., 2020). Ancient minerals and evaporites suggest that the ratio of magnesium to calcium (Mg/Ca) in the open ocean has varied between 1.0 and 5.2. As Mg/Ca changed in seawater, the composition of at least some skeletal carbonates changed both chemically and structurally (Stanley and Hardie, 1998; Dickson, 2002). In the presence of elevated levels of Mg in seawater, aragonite- and high-Mg calcite- (HMC) precipitating organisms are favored, whereas low-Mg seawater conditions resulted in the dominance of low-Mg calcite precipitating (LMC) organisms. Some organisms may increase or decrease their shell Mg/Ca in response to seawater Mg/Ca changes as an adaptive measure, possibly at the sacrifice of shell quality, decreasing fitness and reducing the organisms' capacity to compete.

Marine organisms appear to apply one of two strategies to adapt to changing Mg/Ca seawater conditions. Some organisms employ passive calcification, which mimics abiotic calcification, i.e., when seawater chemistry changes, the calcite produced reflects these environmental changes. These passive calcifiers (such as algae and corals) are able to calcify under a wide variety of seawater conditions (Ries, 2005; Stanley and Hardie, 1998; Stanley et al., 2010), with the [Mg²⁺] in their shells broadly proportional to that of seawater. They respond to changing seawater chemistry with variation in their shell composition, maintaining consistent growth rates (Mewes et al., 2014).

In contrast, some organisms maintain their preferred mineralogy by controlling their internal chemistry to provide localized microenvironments of precipitation (Higuchi et al., 2014). These active calcifiers control the chemistry of calcite formation even when it requires a considerable expenditure of energy, creating the specific mineral they require regardless of ambient conditions (Ries, 2005, Ries, 2010). When active calcifiers encounter unfavourable seawater chemistry, the production cost increases for their preferred calcite, which can decrease their skeletal growth (Stanley et al., 2010; Higuchi et al., 2014). Active calcifiers (such as molluscs and bryozoans) generally have complex biomineralization pathways. Their calcite production either occurs in an internal sublayer that allows for chemical manipulation of the environment and control over the calcite, or has some active mechanism that autoregulates Mg content in calcite (Ries, 2010). In the laboratory, these organisms produce a lower calcification rate in unfavourable Mg/Ca conditions, and show non-linear responses of wt% of Mg to changes in seawater Mg/Ca.

Experimental manipulation of Mg/Ca in artificial seawater to test active and passive calcification mechanisms has focused mainly on tropical species from the Northern Hemisphere (Dissard et al., 2010; Gomes and Asaeda, 2010; Mewes et al., 2014; Stanley et al., 2002). Results have shown that the relationship between Mg/Ca content in seawater and the mineralogy of biogenic carbonate is variable (Table 1) and species-specific. Modelling from calcite data of active calcifiers indicate unique and distinctly different non-linear calcification. Variation is found even within the same organism, e.g., two different locations on crab shells (Ries, 2004). Models of skeletal carbonate from passive calcifiers, often in a lower trophic level, contain linear slopes, i.e., power coefficients closest to 1 (Hasiuk and Lohmann, 2010).

Here we identify the effects of Mg/Ca in seawater on survival and calcification of three common temperate marine organisms from the Southern Hemisphere: blue tubeworms (Spirobranchus cariniferus), blue mussels (Mytilus edulis) and jingle oysters (Anomia trigonopsis). These actively calcifying species are well-suited to such an investigation because the natural skeletal carbonate mineralogy and growth rates are well known (Riedi, 2012; Smith et al., 2013; Bayne and Worrall, 1980; De Witte et al., 2014), but their responses to Mg/Ca in seawater are unknown.