Digestion in sea urchin larvae impaired under ocean acidification

Larval stages are considered as the weakest link when a species is exposed to challenging environmental changes1,2. Reduced rates of growth and development in larval stages of calcifying invertebrates in response to ocean acidification might be caused by energetic limitations3. So far no information exists on how ocean acidification affects digestive processes in marine larval stages. Here we reveal alkaline (∼pH 9.5) conditions in the stomach of sea urchin larvae. Larvae exposed to decreased seawater pH suffer from a drop in gastric pH, which directly translates into decreased digestive efficiencies and triggers compensatory feeding. These results suggest that larval digestion represents a critical process in the context of ocean acidification, which has been overlooked so far. Ocean acidification as it is projected for the next century can affect vital functions of marine organisms. Larval stages are often particularly sensitive to ocean acidification. Decreased survival of larvae can directly affect population stability and could lead to decreased ecosystem integrity. As observed in several species, disturbances of extraor intracellular acid–base homeostasis were correlated with energy budget reallocation and decreased scope for somatic growth and development4,5. However, little attention has been placed on whether digestive processes are impacted by decreased seawater pH, particularly in larval stages of marine invertebrates. According to the preferred sources of nutrients and the necessary catabolic enzymes, digestive systems with distinct pH environments have evolved. For example, stomachs of most vertebrates operate at an acidic pH of ∼2, corresponding to maximum activity of most gastric enzymes at low pH (ref. 6). On the other hand, the midgut of larvae of several insect species operates at a strongly alkaline pHof ∼11 for the benefit of digestive enzymes (proteases, phosphatases) with a highly alkaline pH optimum7. To maintain high enzyme activities, digestive system pH is regulated by active ion transport processes through the net export or import of acid equivalents8. Here we investigated the effects of seawater acidification on digestive processes in green sea urchin pluteus larvae (Strongylocentrotus droebachiensis), which are keystone species in temperate and subpolar kelp ecosystems9. Owing to the fact that pluteus larvae cannot regulate the extracellular pH in their primary body cavity3 the larval digestive system is directly exposed to changes in seawater pH. We reasoned that changes in seawater pH will directly influence the larval physiology by reducing stomach pH, digestive enzyme activity, and thus food assimilation and/or by challenging the acid–base regulatory machinery responsible for stomach pH maintenance. In terms of larval energy budgets, such