Calcifying echinoid larvae respond to changes in seawater carbonate chemistry with reduced growth and developmental delay. To date, no information exists on how ocean acidification acts on pH homeostasis in echinoderm larvae. Understanding acid-base regulatory capacities is important because intracellular formation and maintenance of the calcium carbonate skeleton is dependent on pH homeostasis. Using H + -selective microelectrodes and the pHsensitive fluorescent dye BCECF, we conducted in vivo measurements of extracellular and intracellular pH (pH e and pH i ) in echinoderm larvae. We exposed pluteus larvae to a range of seawater CO 2 conditions and demonstrated that the extracellular compartment surrounding the calcifying primary mesenchyme cells (PMCs) conforms to the surrounding seawater with respect to pH during exposure to elevated seawater pCO 2 . Using FITC dextran conjugates, we demonstrate that sea urchin larvae have a leaky integument. PMCs and spicules are therefore directly exposed to strong changes in pH e whenever seawater pH changes. However, measurements of pH i demonstrated that PMCs are able to fully compensate an induced intracellular acidosis. This was highly dependent on Na + and HCO 3 − , suggesting a bicarbonate buffer mechanism involving secondary active Na + -dependent membrane transport proteins. We suggest that, under ocean acidification, maintained pH i enables calcification to proceed despite decreased pH e . However, this probably causes enhanced costs. Increased costs for calcification or cellular homeostasis can be one of the main factors leading to modifications in energy partitioning, which then impacts growth and, ultimately, results in increased mortality of echinoid larvae during the pelagic life stage. pH microelectrode | Strongylocentrotus droebachiensis | acid-base regulation | Na + -HCO 3 − transport | epithelial transport S ea urchin larvae have been shown to react with particular sensitivity to CO 2 -induced reductions in seawater pH (1-4). When larvae are chronically exposed to elevated seawater pCO 2 of >0.1 kPa, e.g., as is predicted to occur during the next century in response to anthropogenic CO 2 emissions or through upwelling of low-pH deep water, this sensitivity is reflected in reduced growth and developmental rates (5, 6). Echinoderm larvae are considered to be especially vulnerable to seawater pH reduction and to the associated changes in calcium carbonate saturation state of seawater (Ω Cal ) because their internal skeleton is composed of high magnesium calcite, a highly soluble form of CaCO 3 (7, 8). However, long-term reductions in growth and development might just as well be evoked by other physiological mechanisms that are also sensitive to hypercapnia and the related acid-base disturbances. Recent studies conducted on several marine taxa including mollusks (9) and echinoderms (10) demonstrated increased metabolic rates in response to elevated seawater pCO 2 . It was concluded that reductions in somatic growth and rate of development were caused by a sh...
Larval stages are considered as the weakest link when a species is exposed to challenging environmental changes 1,2 . Reduced rates of growth and development in larval stages of calcifying invertebrates in response to ocean acidification might be caused by energetic limitations 3 . 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 extra-or intracellular acid-base homeostasis were correlated with energy budget reallocation and decreased scope for somatic growth and development 4,5 . 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 pH of ∼11 for the benefit of digestive enzymes (proteases, phosphatases) with a highly alkaline pH optimum 7 . To maintain high enzyme activities, digestive system pH is regulated by active ion transport processes through the net export or import of acid equivalents 8 .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 ecosystems 9 . Owing to the fact that pluteus larvae cannot regulate the extracellular pH in their primary body cavity 3 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 challenges may be a critical reason for the reported reductions in growth and development of echinoid larvae in response to acidified sea water.Using ion-selective micro-electrodes we found that the stomach pH of sea urchin pluteus l...
In vivo measurements of [Ca2+] and [CO32−] indicate biological control of carbonate chemistry at site of calcification in corals.
The specific transporters involved in maintenance of blood pH homeostasis in cephalopod molluscs have not been identified to date. Using in situ hybridization and immunohistochemical methods, we demonstrate that Na(+)/K(+)-ATPase (soNKA), a V-type H(+)-ATPase (soV-HA), and Na(+)/HCO(3)(-) cotransporter (soNBC) are colocalized in NKA-rich cells in the gills of Sepia officinalis. mRNA expression patterns of these transporters and selected metabolic genes were examined in response to moderately elevated seawater Pco(2) (0.16 and 0.35 kPa) over a time course of 6 wk in different ontogenetic stages. The applied CO(2) concentrations are relevant for ocean acidification scenarios projected for the coming decades. We determined strong expression changes in late-stage embryos and hatchlings, with one to three log2-fold reductions in soNKA, soNBCe, socCAII, and COX. In contrast, no hypercapnia-induced changes in mRNA expression were observed in juveniles during both short- and long-term exposure. However, a transiently increased ion regulatory demand was evident during the initial acclimation reaction to elevated seawater Pco(2). Gill Na(+)/K(+)-ATPase activity and protein concentration were increased by ~15% during short (2-11 days) but not long-term (42-days) exposure. Our findings support the hypothesis that the energy budget of adult cephalopods is not significantly compromised during long-term exposure to moderate environmental hypercapnia. However, the downregulation of ion regulatory and metabolic genes in late-stage embryos, taken together with a significant reduction in somatic growth, indicates that cephalopod early life stages are challenged by elevated seawater Pco(2).
Background: Cephalopods have evolved strong acid-base regulatory abilities to cope with CO 2 induced pH fluctuations in their extracellular compartments to protect gas transport via highly pH sensitive hemocyanins. To date, the mechanistic basis of branchial acid-base regulation in cephalopods is still poorly understood, and associated energetic limitations may represent a critical factor in high power squids during prolonged exposure to seawater acidification.
Understanding mollusk calcification sensitivity to ocean acidification (OA) requires a better knowledge of calcification mechanisms. Especially in rapidly calcifying larval stages, mechanisms of shell formation are largely unexplored—yet these are the most vulnerable life stages. Here we find rapid generation of crystalline shell material in mussel larvae. We find no evidence for intracellular CaCO3 formation, indicating that mineral formation could be constrained to the calcifying space beneath the shell. Using microelectrodes we show that larvae can increase pH and [CO3 2−] beneath the growing shell, leading to a ~1.5-fold elevation in calcium carbonate saturation state (Ωarag). Larvae exposed to OA exhibit a drop in pH, [CO3 2−] and Ωarag at the site of calcification, which correlates with decreased shell growth, and, eventually, shell dissolution. Our findings help explain why bivalve larvae can form shells under moderate acidification scenarios and provide a direct link between ocean carbonate chemistry and larval calcification rate.
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