Elsevier

Geochimica et Cosmochimica Acta

Volume 192, 1 November 2016, Pages 318-337
Geochimica et Cosmochimica Acta

Impacts of seawater saturation state (ΩA = 0.4–4.6) and temperature (10, 25 °C) on the dissolution kinetics of whole-shell biogenic carbonates

https://doi.org/10.1016/j.gca.2016.07.001Get rights and content

Abstract

Anthropogenic increase of atmospheric pCO2 since the Industrial Revolution has caused seawater pH to decrease and seawater temperatures to increase—trends that are expected to continue into the foreseeable future. Myriad experimental studies have investigated the impacts of ocean acidification and warming on marine calcifiers’ ability to build protective shells and skeletons. No studies, however, have investigated the combined impacts of ocean acidification and warming on the whole-shell dissolution kinetics of biogenic carbonates. Here, we present the results of experiments designed to investigate the effects of seawater saturation state (ΩA = 0.4–4.6) and temperature (10, 25 °C) on gross rates of whole-shell dissolution for ten species of benthic marine calcifiers: the oyster Crassostrea virginica, the ivory barnacle Balanus eburneus, the blue mussel Mytilus edulis, the conch Strombus alatus, the tropical coral Siderastrea siderea, the temperate coral Oculina arbuscula, the hard clam Mercenaria mercenaria, the soft clam Mya arenaria, the branching bryozoan Schizoporella errata, and the coralline red alga Neogoniolithon sp. These experiments confirm that dissolution rates of whole-shell biogenic carbonates decrease with calcium carbonate (CaCO3) saturation state, increase with temperature, and vary predictably with respect to the relative solubility of the calcifiers’ polymorph mineralogy [high-Mg calcite (mol% Mg > 4)  aragonite > low-Mg calcite (mol% Mg < 4)], consistent with prior studies on sedimentary and inorganic carbonates. Furthermore, the severity of the temperature effects on gross dissolution rates also varied with respect to carbonate polymorph solubility, with warming (10–25 °C) exerting the greatest effect on biogenic high-Mg calcite, an intermediate effect on biogenic aragonite, and the least effect on biogenic low-Mg calcite. These results indicate that both ocean acidification and warming will lead to increased dissolution of biogenic carbonates in future oceans, with shells/skeletons composed of the more soluble polymorphs of CaCO3 being the most vulnerable to these stressors. The effects of saturation state and temperature on gross shell dissolution rate were modeled with an exponential asymptotic function (y=B0B2·eB1Ω) that appeals to the general Arrhenius-derived rate equation for mineral dissolution [r=(C·e-Ea/RT)(1  Ω)n]. Although the dissolution curves for the investigated biogenic CaCO3 exhibited exponential asymptotic trends similar to those of inorganic CaCO3, the observation that gross dissolution of whole-shell biogenic CaCO3 occurred (albeit at lower rates) even in treatments that were oversaturated (Ω > 1) with respect to both aragonite and calcite reveals fundamental differences between the dissolution kinetics of whole-shell biogenic CaCO3 and inorganic CaCO3. Thus, applying stoichiometric solubility products derived for inorganic CaCO3 to model gross dissolution of biogenic carbonates may substantially underestimate the impacts of ocean acidification on net calcification (gross calcification minus gross dissolution) of systems ranging in scale from individual organisms to entire ecosystems (e.g., net ecosystem calcification). Finally, these experiments permit rough estimation of the impact of CO2-induced ocean acidification on the gross calcification rates of various marine calcifiers, calculated as the difference between net calcification rates derived empirically in prior studies and gross dissolution rates derived from the present study. Organisms’ gross calcification responses to acidification were generally less severe than their net calcification response patterns, with aragonite mollusks (bivalves, gastropods) exhibiting the most negative gross calcification response to acidification, and photosynthesizing organisms, including corals and coralline red algae, exhibiting relative resilience.

Introduction

Daily mean atmospheric carbon dioxide (pCO2) exceeded 400 ppm at the Mauna Loa (Hawaii) observatory in May 2013 (Tans and Keeling, 2013), an approximate 43% increase from the pre-Industrial-Revolution level of 280 ppm (IPCC, 2013). This increase in atmospheric pCO2 has caused surface seawater pH to decline by approximately 0.1 units (Brewer, 1997, Caldeira and Wickett, 2003, Orr et al., 2005, IPCC, 2013) and surface seawater temperatures to increase by approximately 1 °C (Kleypas et al., 2005, IPCC, 2013). Atmospheric pCO2 is predicted to increase to between 700 and 900 ppm by the end of the 21st century, which should cause sea surface pH to decrease by an additional 0.3–0.4 units (Brewer, 1997, Caldeira and Wickett, 2003, Orr et al., 2005, Raven et al., 2005, Füssel, 2009, Egleston et al., 2010, IPCC, 2013) and surface seawater temperatures to increase by 2–4 °C (Eakin et al., 2008, Donner, 2009, IPCC, 2013) over the same timeframe. This decrease in seawater pH will reduce the seawater concentration of carbonate ions ([CO32−]), which marine calcifiers use to build their calcium carbonate (CaCO3) shells and skeletons.

Myriad experimental studies (too numerous to mention here) have demonstrated that CO2-induced ocean acidification impairs calcification within many species of marine calcifiers. Review articles by Kleypas et al., 1999, Kleypas et al., 2005, Langdon (2002), Hoegh-Guldberg et al., 2007, Fabry et al., 2008, Doney et al., 2009, Hendricks et al., 2010, and Kroeker et al. (2013) provide excellent summaries of the many studies conducted to date. Several studies also suggest that calcification within some species of marine calcifiers is not negatively impacted and, in some cases, is actually enhanced by moderate elevations in atmospheric pCO2 (e.g., Iglesias-Rodriguez et al., 2008, Wood et al., 2008, Ries et al., 2009, Rodolfo-Metalpa et al., 2010, Rodolfo-Metalpa et al., 2011, Fabricius et al., 2011, Castillo et al., 2014).

The process of shell-building (i.e., ‘net calcification’) within marine calcifiers inhabiting near-undersaturated waters results from the balance of forming new shell through active calcification (i.e., ‘gross calcification’) and losing old shell through dissolution (i.e., ‘gross dissolution’; e.g., Ries, 2011a, Ries, 2011b, Rodolfo-Metalpa et al., 2011). Benthic marine calcifiers inhabiting restricted coastal waters can experience seawater pCO2 that is higher than equilibrium pCO2 for surface seawater in the open ocean due to seasonal cycles in the respiration of organic carbon and/or upwelling and/or water mixing (e.g., Feely et al., 2008, Andersson and Mackenzie, 2012, Andersson and Gledhill, 2013). Calcifiers inhabiting these restricted coastal environments are already experiencing seawater that is undersaturated or nearly undersaturated with respect to their shell mineralogy, which supports the gross dissolution of existing shell (either exposed, distal to calcifying tissue, and possibly covered by calcifying tissue; e.g., Andersson et al., 2005, Andersson et al., 2006, Andersson et al., 2008, Andersson et al., 2011; Morse et al., 2006, Andersson and Mackenzie, 2012, Andersson and Gledhill, 2013) and biologically mediated gross calcification beneath healthy calcifying tissue (e.g., Wood et al., 2008, Ries et al., 2009, Ries, 2011a, Rodolfo-Metalpa et al., 2010, Rodolfo-Metalpa et al., 2011, Fabricius et al., 2011). Furthermore, this dissolution of biogenic carbonates is predicted to increase by more than 200% by year 2300 under business-as-usual scenarios (Kleypas et al., 2005, Andersson et al., 2005, Andersson et al., 2006, Andersson et al., 2008, Andersson et al., 2011; Morse et al., 2006; IPCC, 2013; Andersson and Mackenzie, 2012, Andersson and Gledhill, 2013, Pickett and Andersson, 2015).

Although numerous studies have investigated the impact of CO2-induced ocean acidification on organisms’ rates of net calcification (gross calcification minus gross dissolution), relatively few studies have endeavored to isolate the effects of ocean acidification on the gross dissolution (e.g., Morse et al., 1979, Keir, 1980, Kennish and Lutz, 1999, Cubillas et al., 2005, Bednaršek et al., 2012, Pickett and Andersson, 2015) or gross calcification (e.g., Comeau et al., 2010, Rodolfo-Metalpa et al., 2011, Cohen and Fine, 2012) of marine calcifiers’ shells and skeletons. And none has investigated the combined impacts of warming and acidification on these processes. Indeed, it is presently unclear which of these two processes (gross dissolution vs. gross calcification) is most directly impacted by ocean acidification (e.g., Andersson et al., 2008, Andersson et al., 2011; Ries et al., 2009, Ries, 2011a, Ries, 2012, Rodolfo-Metalpa et al., 2011, Andersson and Gledhill, 2013, Pickett and Andersson, 2015).

Here we present the results of 47-day laboratory experiments investigating the independent and combined effects of seawater saturation state (ΩA = 0.4–4.6) and temperature (10, 25 °C) on rates of whole-shell gross dissolution for 10 species of marine calcifiers that span a range of carbonate polymorph mineralogies (low-Mg calcite, high-Mg calcite, and/or aragonite): the oyster Crassostrea virginica, the ivory barnacle Balanus eburneus, the blue mussel Mytilus edulis, the conch Strombus alatus, the tropical coral Siderastrea siderea, the temperate coral Oculina arbuscula, the hard clam Mercenaria mercenaria, the soft clam Mya arenaria, the branching bryozoan Schizoporella errata, and the coralline red alga Neogoniolithon sp. Gross calcification rates for a subset of these species are also roughly estimated from the difference between their previously determined net calcification rates (Ries et al., 2009, Castillo et al., 2014) and their empirically derived gross dissolution rates (this study).

The dissolution kinetics of calcium carbonate minerals comprise a vast body of theoretical and empirical research that has now been explored for more than half a century. The field has received such widespread attention because of its relevance to a broad range of industries and scientific disciplines. Industrial applications relevant to CaCO3 dissolution include antifouling of marine and freshwater structures (e.g., turbines, boat hulls), descaling of pipes and industrial reactors, art conservation, ceramics, dentistry, vascular and soft-tissue decalcification, mineralogical sequestration of fossil-fuel derived CO2, the development of oil and gas reservoirs, and the mineralogical sealing of oil and gas wells. Calcium carbonate dissolution is also relevant to countless scientific subjects, including the global carbon cycle, sedimentary diagenesis, the formation, abundance and distribution of limestones, the evolution of ocean chemistry, fossil preservation, lysocline dynamics, buffering of the seawater carbonate system, and the biological and sedimentary responses to ocean acidification and warming. Because many natural waters exist near the CaCO3 precipitation–dissolution divide, the CaCO3–CO2–H2O system has become a model for the empirical exploration of mineral dissolution kinetics.

Although a thorough review of prior studies investigating the dissolution kinetics of CaCO3 minerals is beyond the scope of the present contribution, a brief overview of the field is presented below. Readers seeking a more comprehensive treatment of the subject are directed to reviews by Plummer et al., 1979, Morse, 1983, Mackenzie et al., 1983, Morse and Mackenzie, 1990, Morse and Arvidson, 2002, Morse et al., 2006, Morse et al., 2007, and Andersson and Gledhill (2013).

The majority of studies investigating the dissolution kinetics of CaCO3 minerals have focused on synthetic carbonates, primarily calcite (Berner and Morse, 1974, Berner, 1978, Amrhein et al., 1985, Baumann et al., 1985, Busenberg and Plummer, 1986, Arakaki and Mucci, 1995, Alkattan et al., 1998, Arvidson et al., 2003, Arvidson and Luttge, 2010, Chou et al., 1989, Compton et al., 1989, Compton and Pritchard, 1990, Compton and Unwin, 1990, Dreybrodt, 1981, Dreybrodt and Buhmann, 1991, Dreybrodt et al., 1996, Finneran and Morse, 2009, Garrels et al., 1960, Garrels and Wollast, 1978, Gledhill and Morse, 2004, Gledhill and Morse, 2006a, Gledhill and Morse, 2006b, Lafon, 1978, He and Morse, 1993, Kralj and Brečević, 1995, Gutjahr et al., 1996, Hales and Emerson, 1996, Liu and Dreybrod, 1997, Morse and Berner, 1972, Morse et al., 1979, Plath et al., 1980, Plummer and Busenberg, 1982, Plummer and Wigley, 1976, Plummer et al., 1978, Pokrovsky et al., 2005, Pokrovsky et al., 2009, Pokrovsky and Schott, 1999, Pokrovsky and Schott, 2002; Sjöberg and Rickard, 1984, Schott et al., 2009, Sjöberg, 1976, Sjöberg, 1978, Svensson and Dreybrodt, 1992, Thorstenson and Plummer, 1977, Thorstenson and Plummer, 1978, Walter and Morse, 1985, Weyl, 1958, Weyl, 1965, Wollast and Reinhard-Derie, 1977, Wollast, 1990, Xu et al., 2012, Bertram et al., 1991, Bischoff, 1998, Casey and Sposito, 1992). These studies generally support the theoretical assertions that the rate of CaCO3 mineral dissolution can be reliably modeled by the general equation for mineral dissolution rate (cf. Morse and Arvidson, 2002, Gledhill and Morse, 2004, Gledhill and Morse, 2006a, Gledhill and Morse, 2006b):r=k·(1-Ω)n,where r = surface-area-normalized dissolution rate, k = a rate constant, Ω = saturation state of the solution with respect to the CaCO3 mineral of interest, and n = reaction order. The rate constant of the reaction (k) can be modeled from the Arrhenius equation (cf. Morse and Arvidson, 2002, Gledhill and Morse, 2004, Gledhill and Morse, 2006a, Gledhill and Morse, 2006b) as:k=C·e-Ea/RT,where C = a pre-exponential factor, Ea = Arrhenius activation energy of the reaction, R = gas constant, and T = absolute temperature (Kelvin).

Other empirical studies have shown that the dissolution kinetics of synthetic CaCO3 minerals can also be influenced by a range of factors not included in the general equation for mineral dissolution rate, such as inorganic impurities (Garrels et al., 1961, Akin and Lagerwerff, 1965, Berner, 1967, Nestaas and Terjesen, 1969, Mucci and Morse, 1984, Morse, 1986, Buhmann and Dreybrodt, 1987, Mucci et al., 1989, Gutjahr et al., 1996, Eisenlohr et al., 1999, Lea et al., 2001, Alkattan et al., 2002, Arvidson et al., 2006, Harstad and Stipp, 2007; Salem et al., 1994, Terjesen et al., 1961, Walter and Hanor, 1979, Sjöberg and Rickard, 1984, Vinson and Lüttge, 2005), organic impurities (Suess, 1970, Barwise et al., 1990, Compton and Sanders, 1993, Teng and Dove, 1997), crystal surface properties (Compton et al., 1986, Schott et al., 1989, Hillner et al., 1992a, Hillner et al., 1992b, MacInnis and Brantley, 1992, MacInnis and Brantley, 1993, Liang et al., 1996, Liang and Baer, 1997, Jordan and Rammensee, 1998, Shiraki et al., 2000, Lasaga and Luttge, 2001; Sjöberg and Rickard, 1984, White and Peterson, 1990, Van Cappellen et al., 1993, Teng, 2004), and ion transport adjacent to the crystal surface (e.g., Liu and Dreybrod, 1997).

A smaller body of work has investigated the dissolution kinetics of biogenic CaCO3 minerals. The majority of these studies have focused on the dissolution kinetics of bulk CaCO3 sediments, often with the aim of constraining reactions involved in the evolution of sedimentary porewater, early-to-late stage sedimentary diagenesis, lithification, and sedimentary buffering of the seawater carbonate system (Balzer and Wefer, 1981, Archer et al., 1989, Andersson et al., 2007, Andersson et al., 2009, Berger, 1967; Buhmann and Dreybrodt, 1985a, Buhmann and Dreybrodt, 1985b, Burdige et al., 2008, Burdige et al., 2010, Burdige and Zimmerman, 2002, Boucher et al., 1998, Friedman, 1964, Gehlen et al., 2005a, Gehlen et al., 2005b, Honjo and Erez, 1978, Hales et al., 1994, Hales and Emerson, 1996, Jahnke and Jahnke, 2004, Kinsey, 1985, Langdon et al., 2000, Leclercq et al., 2002, Milliman, 1978, Morse, 1978, Morse et al., 2006, Peterson, 1966, Pickett and Andersson, 2015, Rude and Aller, 1991, Silverman et al., 2007a, Silverman et al., 2007b, Schmalz, 1965, Walter and Burton, 1990, Walter et al., 1993, Yates and Halley, 2006, Tynan and Opdyke, 2011). These studies generally investigate bulk mixtures of biogenic CaCO3 minerals that, in some cases, have been substantially altered themselves through neomorphism, diagenetic conversion, laboratory cleaning, and/or natural loss of organic impurities and protective organic layers.

Numerous studies have also investigated the dissolution kinetics of specific types of biogenic CaCO3 shells and skeletons (Plummer and Mackenzie, 1974, Bischoff et al., 1983, Bischoff et al., 1987, Walter and Morse, 1984, Walter and Morse, 1985, Walter, 1985, Cubillas et al., 2005). However, most of these studies involved the heavy treatment, via pulverization and/or chemical cleaning, of the shells and skeletons as the investigators sought to eliminate the effects of organic impurities, protective organic coverings, and shell and/or crystal geometry on the dissolution kinetics of the biogenic mineral (c.f., Morse and Arvidson, 2002). Although studies investigating mechanically and/or chemically treated shells and skeletons provide important insight into the dissolution kinetics of sedimentary biogenic carbonates, they are not ideal for constraining the whole-shell dissolution kinetics that are relevant to predicting organismal responses to CO2-induced ocean acidification and warming.

Pickett and Andersson (2015) have published the most recent and comprehensive investigation of dissolution kinetics of biogenic carbonates. In their seminal study, they evaluated the impact of pCO2 ranging from 3000 to 5500 μatm on the dissolution rates of pulverized shells of 5 species of marine invertebrates that produce calcite of varying Mg-content: a barnacle, a foraminifer, a bryozoan, an urchin, and two species of coralline algae. They found that dissolution rates increased predictably with increasing pCO2, increasing Mg-content of calcite, and increasing microstructural surface area. Like prior studies on biogenic carbonates, this study utilized crushed shells in order to make their results relevant to sedimentary porewater systems and buffering of the seawater carbonate system. Modification of shell geometry and surface area through mechanical grinding, however, makes it challenging to apply their results to whole shell dissolution kinetics and the biological process of shell-building.

A handful of studies have investigated the dissolution kinetics of untreated, whole-shell biogenic carbonates. The earlier of these studies (Friedman, 1964; Schroeder, 1969; Land, 1967) focused mainly on the diagenetic stabilization of high-Mg calcite to form more stable low-Mg calcite and dolomite. As such, these experiments were carried out at temperatures and saturation states that are not relevant to conditions predicted for the future oceans. Moreover, rates of CaCO3 dissolution in these experiments were typically not documented with the precision and accuracy needed for comparing results amongst organisms and/or experiments (Morse and Arvidson, 2002) or for interpreting these results in the context of future oceanic change.

More recent investigations of whole-shell dissolution kinetics (e.g., Morse et al., 1979, Keir, 1980, Bednaršek et al., 2012) were conducted with greater scientific rigor and over solution parameters more relevant to future oceanic change. However, these studies have largely been focused on planktonic calcifiers (e.g., foraminifera, coccolithophores, pteropods) due to their role in shelf, slope and deep-sea sedimentation.

Kennish and Lutz (1999) and Powell et al. (2008) conducted long-term field-based experiments and Glover and Kidwell (1993) conducted controlled laboratory experiments investigating the dissolution kinetics of bivalve shells, mainly from a taphonomic perspective (i.e., to determine the potential for preserving bivalve shells in the fossil record). And in a controlled laboratory experiment investigating dissolution rates of whole oyster shells over the pH range 7.2–7.9, Waldbusser et al. (2011) found that oyster shell dissolution rates increased with decreasing seawater pH, except between pH 7.4 and 7.2, and that fresh shells dissolved faster than weathered shells, which in turn dissolved faster than dredged shells.

Finally, Nash et al. (2013) conducted short-term (10-day) laboratory experiments investigating the dissolution rates of crustose coralline algae over the pH range 7.7–8.3 and found that algal skeletons rich in the less soluble dolomite mineral exhibited slower rates of dissolution than algal skeletons rich in the more-soluble Mg-calcite mineral.

Here, we seek to build upon this foundation of research investigating carbonate dissolution kinetics by conducting the first systematic analysis of whole-shell dissolution kinetics at various saturation states and temperatures for a range of benthic calcifying taxa spanning various polymorph mineralogies (aragonite, low-Mg calcite, high-Mg calcite).

Section snippets

Specimen collection

Live organisms were collected, pursuant to local, state, and federal regulations, from the following localities: M. edulis (blue mussel) and C. virginica (oyster) from Buzzards Bay, Massachusetts; B. eburneus (ivory barnacle), S. errata (branching bryozoan), and S. alatus (conch) from the Gulf of Mexico off the coast of Florida; Neogoniolithon sp. (red alga) from the Atlantic Ocean off the coast of Florida; M. mercenaria (hard clam) and M. arenaria (soft clam) from Nantucket Sound off the coast

Effect of ΩA on gross dissolution

All ten species of calcifiers exhibited gross dissolution curves that were asymptotic in nature. Dissolution rates were relatively constant in the treatments that were oversaturated with respect to organisms’ predominant polymorph, and then predictably increased exponentially in the undersaturated treatments. Notably, gross dissolution of shells and skeletons of all investigated taxa were also observed in each of the oversaturated treatments (ΩA > 1) and at both temperatures (10, 25 °C), albeit at

Effect of Ω on gross dissolution rate

The observation that the gross dissolution curves for the investigated biogenic CaCO3 exhibited trends similar to those of inorganic CaCO3 and could be reasonably modeled with an exponential asymptotic function (y=B0B2·eB1Ω; terms define above) that appeals to the general Arrhenius-derived rate equation for mineral dissolution [r=(C·e-Ea/RT)(1  Ω)n; terms defined above; cf. Gledhill and Morse, 2004, Gledhill and Morse, 2006a, Gledhill and Morse, 2006b, Morse and Arvidson, 2002] suggests that

Conclusions

Whole-shell dissolution experiments conducted across a range of saturation states (0.4 < ΩA < 4.6) and temperatures (10, 25 °C) on ten species of marine calcifiers revealed the following:

  • (1)

    Dissolution rates of whole-shell biogenic carbonates decrease with CaCO3 saturation state, increase with temperature, and vary predictably with respect to the relative solubility of the calcifiers’ shell polymorph mineralogy [high-Mg calcite (mol% Mg > 4)  aragonite > low-Mg calcite (mol% Mg < 4)], consistent with prior

Acknowledgements

We thank K. Horvath and T. Courtney for valuable input and assistance. We thank C. Pelejero and an anonymous referee for their thorough reviews. This research was supported by NOAA awards NA13OAR4310186 (to JBR and KDC) and NA14NMF4540072 (to JBR), the UNC-Chapel Hill IDEA Program (NSF award #1107897, in support of MNG), and NSF awards OCE-1437371 and OCE-1459706 (to JBR). This is contribution number 340 of the Marine Science Center at Northeastern University.

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      2022, Estuarine, Coastal and Shelf Science
      Citation Excerpt :

      Under a reduced CaCO3 saturation state in low saline water, the energetic cost of calcification may be elevated, possibly leading to skeletal growth disorder. Recent studies revealed calcifying species as sensitive to the low CaCO3 saturation state, expressing a lower calcification rate, altered skeletal composition and mineral disorganization (Fitzer et al., 2015; Ramajo et al., 2016; Ries et al., 2016; Watson et al., 2012). A growing number of studies have shown the ability of some species, especially those inhabiting coastal habitats, to cope with unfavourable conditions for calcification (e.g., limiting Ca2+ and aragonite undersaturation; Sanders et al., 2018; Thomsen et al., 2018) through biological skeletal production control mechanisms (Hendriks et al., 2015; Telesca et al., 2019).

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