Elevated pCO2 drives lower growth and yet increased calcification in the early life history of the cuttlefish Sepia officinalis (Mollusca: Cephalopoda)

Ocean acidification is an escalating environmental issue and associated changes in the ocean carbonate system have implications for many calcifying organisms. The present study followed the growth of Sepia officinalis from early-stage embryos, through hatching, to 7-week-old juveniles. Responses of cuttlefish to elevated pCO(2) (hypercapnia) were investigated to test the impacts of near-future and extreme ocean acidification conditions on growth, developmental time, oxygen consumption, and yolk utilization as proxies for individual fitness. We further examined gross morphological characteristics of the internal calcareous cuttlebone to determine whether embryonically secreted shell lamellae are impacted by environmental hypercapnia. Embryonic growth was reduced and hatching delayed under elevated pCO(2), both at environmentally relevant levels (0.14 kPa pCO(2) similar to predicted ocean conditions in 2100) and extreme conditions (0.40 kPa pCO(2)). Comparing various metrics from control and intermediate treatments generally showed no significant difference in experimental measurements. Yet, results from the high pCO(2) treatment showed significant changes compared with controls and revealed a consistent general trend across the three treatment levels. The proportion of animal mass contributed by the cuttlebone increased in both elevated pCO(2) treatments. Gross cuttlebone morphology was affected under such conditions and cuttlebones of hypercapnic individuals were proportionally shorter. Embryonic shell morphology was maintained consistently in all treatments, despite compounding hypercapnia in the perivitelline fluid; however, post-hatching, hypercapnic animals developed denser cuttlebone laminae in shorter cuttlebones. Juvenile cuttlefish in acidified environments thus experience lower growth and yet increased calcification of their internal shell. The results of this study support recent findings that early cuttlefish life stages are more vulnerable towards hypercapnia than juveniles and adults, which may have negative repercussions on the biological fitness of cuttlefish hatchlings in future oceans.