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Precipitation of Aragonite by Calcitic Bivalves in Mg-Enriched Marine Waters

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Precipitation of Aragonite by Calcitic Bivalves in Mg-Enriched Marine Waters Mar Biol DOI 10.1007/s00227-006-0411-4 RESEARCH ARTICLE Precipitation of aragonite by calcitic bivalves in Mg-enriched marine waters Antonio G. Checa · Concepción Jiménez-López · Alejandro Rodríguez-Navarro · Jorge P. Machado Received: 30 March 2006 / Accepted: 22 June 2006 © Springer-Verlag 2006 Abstract To understand the relative importance of (the scallop Chlamys varia, the oyster Ostrea edulis, the biological versus physicochemical control over biomin- saddle oyster Anomia ephippium and the mussel eralization, we have tested if the chemical composition Mytilus edulis) survived long enough to secrete signiW- of the medium (i.e., the Mg/Ca ratio) can change the cant amounts of calcium carbonate. The deposits mineralogy of mollusk shells. The shells of mollusks (sometimes extensive) formed on the interior shell sur- are made of calcite and/or aragonite, which are by far faces were predominantly aragonitic. Three individuals the most common CaCO3 polymorphs. Several species of C. varia also increased their length by adding new of bivalves with predominantly calcitic shells have been shell at the margin. Contrary to the internal shell cultivated in artiWcial seawater with a Mg/Ca molar deposits, these margins were high-Mg calcite. This ratio within the range of 8.3–9.2, well above the present implies that the marginal mantle is able to exert a more value for seawater (5.2). Four out of six species used strict control on the secreted mineral phase than the mantle facing the internal shell surface. This is the Wrst report on an in vivo experimentally forced switch in Communicated by O. Kinne, Oldendorf/Luhe bivalve shell mineralogy, from calcite to aragonite due to a change in water chemistry. A. G. Checa (&) Departamento de Estratigrafía y Paleontología, Facultad de Ciencias, Universidad de Granada, Avenida Fuentenueva s/n, 18002 Granada, Spain Introduction e-mail: [email protected] Although the mineralogy and microstructure of mol- C. Jiménez-López Departamento de Microbiología, Facultad de Ciencias, lusk shells is mainly biologically controlled (Watabe Universidad de Granada, Avenida Fuentenueva s/n, and Wilbur 1960; Addadi and Weiner 1992; Belcher 18002 Granada, Spain et al. 1996) the chemistry of the environment can also e-mail: [email protected] aVect to some degree the chemical and mineral compo- A. Rodríguez-Navarro sition of the shell. Nevertheless, little is known on the Departamento de Mineralogía y Petrología, eVect of the chemistry of the medium on shell composi- Facultad de Ciencias, Universidad de Granada, tion and mineralogy in mollusks (and other organ- Avenida Fuentenueva s/n, 18002 Granada, Spain isms). In the case of bivalves, there are only a few e-mail: [email protected] studies that report the inXuence of environmental J. P. Machado parameters on the shell mineralogy. In Mytilus, Laboratorio de Fisiologia Aplicada, increasing water temperature increases the aragonite/ Instituto de Ciências Biomédicas, calcite proportion in the shells (Lowenstam 1954a, b), Universidade de Porto, Largo Profesor Abel Salazar 2, 4099-003 Porto, Portugal while salinity reduces such proportion (Dodd 1964, e-mail: [email protected] 1966; Eisma 1966). 123 Mar Biol There are also a few experimental studies on the and Piggot (1981) that changes were the result of tec- V e ect of Mg on chemical composition of the carbonate tonically induced changes in atmospheric partial CO2 skeletons. In particular, Lorens and Bender (1980) pressure (pCO2), rather than oceanic Mg/Ca, following demonstrate that the magnesium content in the calcite mid oceanic ridge activity cycles (Mackenzie and secreted by Mytilus edulis in artiWcial seawaters Morse 1992; Hallock 1997). Stanley and Hardie (1998) increases exponentially with the Mg/Ca ratio in the cul- reviewed the inadequacies of the CO2 model and, in ture medium. Moreover, Stanley et al. (2002) found a accordance with Morse et al. (1997), proposed instead strong correlation between the aqueous magnesium that the Mg/Ca ratio controls carbonate mineralogy. +2 (Mg (aq)) contents in a relatively magnesium depleted Stanley and Hardie (1998) followed Hardie (1996) and culture medium and in the carbonate precipitated by a linked variations of Mg/Ca ratios in marine waters dur- coralline alga. Following a similar experimental line, ing the Phanerozoic to Mg removal following conver- Ries (2005) determined that the aragonitic codiacean sion of basalt into greenstone due to mid oceanic ridge alga Penicillus capitatus is able to precipitate about hydrothermalism. Consequently, increasing rates of 22 § 3% of low-Mg calcite in waters with Mg/Ca < 2. ocean crust production lowers the Mg/Ca ratio of sea- To our knowledge, this is the only previous experimen- water. Stanley and Hardie (1998) presented an tal study that focus on the change of the carbonate updated curve of variation of the mineralogy of non- polymorph (aragonite or calcite) induced by the mag- skeletal carbonates throughout the Phanerozoic and nesium content in the culture medium. These results showed that there is a good match between the skeletal are supported by numerous inorganic studies showing mineralogy of major sediment producing algae and that the presence of dissolved magnesium in the dominant reef builders during the Phanerozoic and the medium favours the precipitation of CaCO3 as arago- aragonitic and calcitic periods. They hypothesized that nite from supersaturated seawater and other Mg-rich skeletal mineralogies of anatomically simple organisms aqueous solutions instead of calcite (Kitano and Kana- were directly inXuenced by seawater chemistry. mori 1966; Lippman 1973; Berner 1975; Deleuze and To determine whether the chemistry of the media is Brantley 1997; Morse et al. 1997) and also decreases able to inXuence the mineralogy of mollusk shells and calcite growth rate (Reddy and Wang 1980; Mucci and if so to what extend, we have cultivated bivalves with Morse 1983; Jiménez-Lopez et al. 2004). The inhibitory predominantly calcitic shells in two mediums with ini- eVect of magnesium in calcite nucleation and growth is tial Mg/Ca molar ratios of (a) 8.4, well above the pres- probably related to the smaller size, the higher charge ent ratio in normal (euhaline) seawaters (t 5.2 molar density and the greater hydration energy of Mg2+, ratio), here referred to as high-Mg experiment, and (b) which impedes calcite nucleation and growth until the 5.0, referred to as control experiment. The main idea of dehydration of Mg2+ occurs (Lippmann 1973). Arago- these experiments was to force bivalves to switch from nite probably forms because Mg adsorption and dehy- precipitating calcite to aragonite by introducing mag- dration slows the growth kinetics of calcite compared nesium in the medium in higher proportions. These to that of aragonite (BischoV and Fyfe 1968). experiments will also help us to understand the relative The study of the eVect of the chemistry of the inXuence of biological versus physicochemical pro- medium on skeletal mineralogy has macroevolutionary cesses on shell formation. implications. Water chemistry has changed over geo- logical time and in particular with respect to the Mg to Ca ratio (Hardie 1996; Stanley and Hardie 1998). In Material and methods this respect, the main discussion is on whether secular changes in certain chemical components of marine Species and shell composition waters may have induced changes in the polymorph from which the skeleton is made. Sandberg (1975) orig- The following species were used in the experiments: inally proposed that ancient oolites shifted from being the Pectinidae Aequipecten opercularis (Linnaeus), calcitic to aragonitic in the Mesozoic due to an increase Chlamys varia (Linnaeus) and Pecten maximus (Linna- in the Mg/Ca ratio. Wilkinson (1979) suggested that eus), the Anomiidae Anomia ephippium Linnaeus, the the mineralogical evolution in marine invertebrates Ostreidae Ostrea edulis Linnaeus and the Mytilidae follows that relationship, with increasing oceanic Mg/ Mytilus galloprovincialis Lamarck. Except for M. gallo- Ca inhibiting calcite deposition. Sandberg (1983) provincialis, that has an outer prismatic calcitic layer divided the Phanerozoic Eon into two calcitic and and an inner nacreous layer, all the other species have three aragonitic sea periods and, together with Wilkin- a predominantly calcitic (mostly foliated) shell. In son et al. (1985), he adhered to the idea of MacKenzie these bivalves aragonite is restricted to muscle inser- 123 Mar Biol Experimental setting Specimens were collected from the Mediterranean Sea at Centro OceanográWco de Fuengirola (Ministerio de Ciencia y Tecnología, Málaga) and placed in aquaria in aerated conditions at 18 § 1°C. We selected young individuals, with growth potential. The range of rela- tive sizes (compared to adult sizes) varied from P. max- imus (mean § SD = 21 § 6.37, mean adult size in the sampling area = 65 mm) to A. ephippium (mean § SD =35§ 7.5, adult mean size = 43 mm). Both the high- Mg and control experiments were run for 56 days, though living specimens began to be collected for anal- yses beginning on the 48th day. The high-Mg medium was prepared by mixing 10 l of sea water (Mediterranean Sea, pH = 8.42) and 10 l of a master solution with the following composition: MgCl2 (Panreac, Barcelona, Spain) 127 mM, CaCl2 (Aldrich, St. Louis, MO, USA) 10 mM and NaCl (Sigma–Aldrich) 460 mM. The Wnal solution (20 l) had 2+ the following chemical composition: Mg (aq) 83.6 mM, 2+ + ¡ Ca (aq) 10.0 mM, Na (aq)460 mM and Cl (aq) 599 mM, pH = 7.90. For the control experiment we mixed 8 l of sea water (Mediterranean Sea) and 8 l of a master solu- tion with the following composition: MgCl2 50.0 mM, W CaCl2 10.0 mM and NaCl 460.0 mM. The nal solution 2+ (16 l) had the following chemical composition: Mg (aq) 2+ + ¡ 83.6 mM, Ca (aq) 10.0 mM, Na (aq) 460 mM and Cl (aq) Fig. 1 Spatial distribution of aragonite produced by calcitic biv- 565 mM, pH = 8.37.
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