Elevated level of carbon dioxide affects metabolism and shell formation in oysters Crassostrea virginica (Gmelin)

Abstract

Estuarine organisms are exposed to periodic strong fluctuations in seawater pH driven by biological carbon dioxide (CO 2 ) production, which may in the future be further exacerbated by the ocean acidification associated with the global rise in CO 2 . Calcium carbonate-producing marine species such as mollusks are expected to be vulnerable to acidification of estuarine waters, since elevated CO 2 concentration and lower pH lead to a decrease in the degree of saturation of water with respect to calcium carbonate, potentially affecting biomineralization. Our study demonstrates that the increase in CO 2 partial pressure (pCO 2 ) in seawater and associated decrease in pH within the environmentally relevant range for estuaries have negative effects on physiology, rates of shell deposition and mechanical properties of the shells of eastern oysters Crassostrea virginica (Gmelin). High CO 2 levels (pH~7.5, pCO 2~3 500 µatm) caused significant increases in juvenile mortality rates and inhibited both shell and soft-body growth compared to the control conditions (pH ~8.2, pCO 2 380 µatm). Furthermore, elevated CO 2 concentrations resulted in higher standard metabolic rates in oyster juveniles, likely due to the higher energy cost of homeostasis. The high CO 2 conditions also led to changes in the ultrastructure and mechanical properties of shells, including increased thickness of the calcite laths within the hypostracum and reduced hardness and fracture toughness of the shells, indicating that elevated CO 2 levels have negative effects on the biomineralization process. These data strongly suggest that the rise in CO 2 can impact physiology and biomineralization in marine calcifiers such as eastern oysters, threatening their survival and potentially leading to profound ecological and economic impacts in estuarine ecosystems.KEY WORDS: Hypercapnia · Ocean acidification · Calcification · Shell structure · Energy metabolism · Oxygen consumption · Mollusks Resale or republication not permitted without written consent of the publisherMar Ecol Prog Ser 419: [95][96][97][98][99][100][101][102][103][104][105][106][107][108] 2010 between 4 and 5 mo in summer and early fall (Cochran & Burnett 1996; see also long-term water pH data for eastern US estuaries at http://cdmo.baruch.sc.edu/). Given that pH is measured on a log scale, even relatively small changes in pH result in a considerable change in concentrations of hydrogen and hydroxide ions, which may have important physiological consequences for the resident biota.The effects of seasonal and diurnal hypercapnia experienced by estuarine organisms are likely to become exacerbated in the coming years due to global climate change and ocean acidification driven by anthropogenically released CO 2 (Caldeira & Wickett 2003. The uptake of atmospheric CO 2 is especially pronounced in surface ocean waters (< 250 m depth), where nearly 50% of anthropogenic CO 2 is absorbed, making near-shore habitats including estuaries vulnerable to ocean acidification (Feely et al. 2008, Doney e...

Impacts of ocean acidification on marine shelled molluscs

“…However, the mechanical properties of the shells of the juveniles were altered under hypercapnic conditions, resulting in a reduced hardness and fracture resistance. This confirmed the results of Beniash et al (2010) and Welladsen et al (2010) on oysters, showing that the ultrastructure and the mechanical properties of the shells were significantly altered under high CO 2 . Nienhuis et al (2010) have shown that the growth of the rocky intertidal snail Nucella lamellosa decreases with increasing pCO 2 levels as a consequence of increased dissolution rates.…”

“…Both studies showed significant decreased shell growth (as measured by the linear increase of the shells) following pH reductions of -0.75 and -1 pH unit, for Michaelidis et al (2005) and Berge et al (2006), respectively. Similar reductions in shell growth, following medium-term exposures ([2 weeks) to strong pH decrease ([-0.5 pH unit), have been reported by Beniash et al (2010) and Talmage and Gobler (2011) for juvenile Eastern oysters (Crassostrea virginica). Interestingly, in the study of Beniash et al (2010), in contrast to shell mass, the average shell area was not affected by hypercapnic conditions, suggesting that juvenile oysters were depositing thinner shells.…”

“…Similar reductions in shell growth, following medium-term exposures ([2 weeks) to strong pH decrease ([-0.5 pH unit), have been reported by Beniash et al (2010) and Talmage and Gobler (2011) for juvenile Eastern oysters (Crassostrea virginica). Interestingly, in the study of Beniash et al (2010), in contrast to shell mass, the average shell area was not affected by hypercapnic conditions, suggesting that juvenile oysters were depositing thinner shells. This further indicates that shell length or area might not be sufficiently accurate as indicators of the effects of ocean acidification on shelled molluscs as the organisms are potentially able to maintain a normal linear shell growth under low pH conditions.…”

“…In juveniles of the oyster C. virginica, exposure to elevated CO 2 of *3,300 latm (-0.7 pH unit) for 20 weeks, a level much higher than that used in the previous study (and therefore not shown in Fig. 4), caused an increase in SMR which was accompanied by a decrease in both shell and somatic growth and survival (Beniash et al 2010). A number of other shelled mollusc species have also suffered reduced survival following chronic exposure to elevated CO 2 (snail S. lubuanus, Shirayama and Thornton 2005; mussel M. edulis, Berge et al 2006;clam M. mercenaria, Green et al 2009;oyster C. virginica, Dickinson et al 2012;clam T. squamosa, Watson et al 2012b).…”

Adaptation and acclimatization to ocean acidification in marine ectotherms: anin situtransplant experiment with polychaetes at a shallow CO2vent system

“…When exposed to elevated pCO 2 , a number of taxa exhibit a marked downregulation of their metabolic rate or 'metabolic depression' [11,[13][14][15][16][17] but this is not ubiquitous. There are examples of upregulation [18][19][20], and no change in metabolism in response to elevated pCO 2 [11,[21][22][23][24]. It has been proposed that metabolic depression evolved to enable organisms to maintain a balance between energy supply and demand when their physiological machinery may be impaired as a result of environmental challenges [25,26].…”