Cuttlebone calcification increases during exposure to elevated seawater pCO2 in the cephalopod Sepia officinalis

Abstract

Changes in seawater carbonate chemistry that accompany ongoing ocean acidification have been found to affect calcification processes in many marine invertebrates. In contrast to the response of most invertebrates, calcification rates increase in the cephalopod Sepia officinalis during long-term exposure to elevated seawater pCO 2 . The present trial investigated structural changes in the cuttlebones of S. officinalis calcified during 6 weeks of exposure to 615 Pa CO 2 . Cuttlebone mass increased sevenfold over the course of the growth trail, reaching a mean value of 0.71 ± 0.15 g. Depending on cuttlefish size (mantle lengths 44-56 mm), cuttlebones of CO 2 -incubated individuals accreted 22-55% more CaCO 3 compared to controls at 64 Pa CO 2 . However, the height of the CO 2 -exposed cuttlebones was reduced. A decrease in spacing of the cuttlebone lamellae, from 384 ± 26 to 195 ± 38 lm, accounted for the height reduction The greater CaCO 3 content of the CO 2 -incubated cuttlebones can be attributed to an increase in thickness of the lamellar and pillar walls. Particularly, pillar thickness increased from 2.6 ± 0.6 to 4.9 ± 2.2 lm. Interestingly, the incorporation of non-acidsoluble organic matrix (chitin) in the cuttlebones of CO 2 -exposed individuals was reduced by 30% on average. The apparent robustness of calcification processes in S. officinalis, and other powerful ion regulators such as decapod cructaceans, during exposure to elevated pCO 2 is predicated to be closely connected to the increased extracellular [HCO 3 -] maintained by these organisms to compensate extracellular pH. The potential negative impact of increased calcification in the cuttlebone of S. officinalis is discussed with regard to its function as a lightweight and highly porous buoyancy regulation device. Further studies working with lower seawater pCO 2 values are necessary to evaluate if the observed phenomenon is of ecological relevance.

Ocean acidification and temperature rise: effects on calcification during early development of the cuttlefish Sepia officinalis

“…This study corroborates with the observation of Gutowska et al (2010b) where cuttlebones of Sepia officinalis juveniles displayed a significant increase in CaCO 3 mass (hypercalcification) under very high pCO 2 (~6000 µatm for 40 days). Here, using 45 Ca ß-emitting radiotracer, a very sensitive nuclear detection method that allows for calcification rate estimation in early life stages (Fabry and Balch 2010), we demonstrate that such hypercalcification also occurs under realistic scenarios of increased temperature and pCO 2 in early life stages of Sepia.…”

“…Still, 45 Ca incorporation in the cuttlebone was found to be increased even in juveniles under acidified conditions, indicating that similar mechanisms as described must be operative in juveniles as well. In contrary to Gutowska et al (2010b), we were not able to measure a difference in cuttlebone mass in response to pCO 2 or temperature, however our animals were younger and smaller. The cuttlebone is mainly composed of CaCO 3 (92 to 95 % mass) embedded in an organic matrix, giving the organ structure; therefore, in this study, it is not possible to infer conclusion on the impact of the experimental treatments on the organic matrix.…”

“…Nevertheless, it should be mentioned that a high seawater pCO 2 could modify the cuttlebone size, its internal structure, its organization or composition, resulting in an increase of calcium incorporation but no alteration of the weight. For example, under acidified conditions, along with 20-55% increase in the cuttlebone mass, Gutowska et al (2010b) observed a strong increase in the number of shell-chambers constituting the cuttlebone, including an increase in the number of CaCO 3 structure such as pillars and walls. This last study also demonstrated that the mass of the non-acid-soluble organic matrix (or chitin), was significantly decreased under high pCO 2 .…”

“…concentrations from 3.3 to 10.4 mM in the blood to compensate hypercapnia-induced extracellular acidosis (Gutowska et al 2010b). Increases in extracellular [HCO 3 -] raises the calcium carbonate saturation state in extracellular fluids, potentially facilitating calcium precipitation at the site of biomineralization, or increasing HCO 3 -transport into calcifying epithelial cells (Gutowska et al 2010a).…”

“…On the common cuttlefish Sepia officinalis for instance, Gutowska et al (2008) showed maintained calcification and growth in juveniles after 40 days of exposure to high pCO 2 . In a second study, Gutowska et al (2010b) showed a 20-50% increase of the CaCO 3 fraction in juvenile's cuttlebones along with a structural change of the calcified matrix.…”