Abstract
Cephalopods have evolved strong acid–base regulatory abilities to cope with CO2 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. The present work used adult squid Sepioteuthis lessoniana to investigate the effects of short-term (few hours) to medium-term (up to 168 h) seawater acidification on pelagic squids. Routine metabolic rates, NH4+ excretion, extracellular acid–base balance were monitored during exposure to control (pH 8.1) and acidified conditions of pH 7.7 and 7.3 along a period of 168 h. Metabolic rates were significantly depressed by 40% after exposure to pH 7.3 conditions for 168 h. Animals fully restored extracellular pH accompanied by an increase in blood HCO3− levels within 20 hours. This compensation reaction was accompanied by increased transcript abundance of branchial acid–base transporters including V-type H+-ATPase (VHA), Rhesus protein (RhP), Na+/HCO3− cotransporter (NBC) and cytosolic carbonic anhydrase (CAc). Immunocytochemistry demonstrated the sub-cellular localization of Na+/K+-ATPase (NKA), VHA in basolateral and Na+/H+-exchanger 3 (NHE3) and RhP in apical membranes of the ion-transporting branchial epithelium. Branchial VHA and RhP responded with increased mRNA and protein levels in response to acidified conditions indicating the importance of active NH4+ transport to mediate acid–base balance in cephalopods. The present work demonstrated that cephalopods have a well developed branchial acid–base regulatory machinery. However, pelagic squids that evolved a lifestyle at the edge of energetic limits are probably more sensitive to prolonged exposure to acidified conditions compared to their more sluggish relatives including cuttlefish and octopods.
Highlights
CO2 induced acid–base disturbances are a unifying physiological phenomenon that all animals are confronted with
Acid–base transporters potentially involved in both, HCO3− accumulation and H+ equivalent secretion were identified and localized in gill epithelia suggesting that this represents the major site for acid–base regulatory in cephalopods
Significant HCO3− buffering capacities to control extracellular pH were only described for few marine species proton or proton equivalent secretion mechanisms may represent a more direct and ubiquitious pH regulatory pathway
Summary
CO2 induced acid–base disturbances are a unifying physiological phenomenon that all animals are confronted with. Medium- to long-term (several days) acidification experiments using squids with a pelagic lifestyle are rare as these animals are extremely difficult to keep under laboratory conditions Such experiments require large-scale experimental facilities with access to natural, high quality seawater. A large body of knowledge is available for teleosts, a comparatively small number of studies investigated acid–base and ion regulatory mechanisms in non-model invertebrates like mollusks, echinoderms and crustaceans. For the latter a number of studies exist with osmotic and acid–base regulatory mechanisms recently summarized by Henry et al. Cephalopods have evolved strong acid–base regulatory abilities to cope with CO2 induced pH fluctuations in their extracellular compartments to protect gas transport via highly pH sensitive hemocyanins. 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
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