Physiological basis for high CO<sub>2</sub> tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny?

Abstract

Abstract. Future ocean acidification has the potential to adversely affect many marine organisms. A growing body of evidence suggests that many species could suffer from reduced fertilization success, decreases in larval-and adult growth rates, reduced calcification rates, and even mortality when being exposed to near-future levels (year 2100 scenarios) of ocean acidification. Little research focus is currently placed on those organisms/taxa that might be less vulnerable to the anticipated changes in ocean chemistry; this is unfortunate, as the comparison of more vulnerable to more tolerant physiotypes could provide us with those physiological traits that are crucial for ecological success in a future ocean. Here, we attempt to summarize some ontogenetic and lifestyle traits that lead to an increased tolerance towards high environmental pCO 2 . In general, marine ectothermic metazoans with an extensive extracellular fluid volume may be less vulnerable to future acidification as their cells are already exposed to much higher pCO 2 values (0.1 to 0.4 kPa, ca. 1000 to 3900 µatm) than those of unicellular organisms and gametes, for which the ocean (0.04 kPa, ca. 400 µatm) is the extracellular space. A doubling in environmental pCO 2 therefore only represents a 10% change in extracellular pCO 2 in some marine teleosts. High extracellular pCO 2 values are to some degree related to high metabolic rates, as diffusion gradients need to be high in order to excrete an amount of CO 2 that is directly proportional to the amount of O 2 consumed. In active metazoans, such as teleost fish, cephalopods and Correspondence to: F. Melzner (fmelzner@ifm-geomar.de) many brachyuran crustaceans, exercise induced increases in metabolic rate require an efficient ion-regulatory machinery for CO 2 excretion and acid-base regulation, especially when anaerobic metabolism is involved and metabolic protons leak into the extracellular space. These ion-transport systems, which are located in highly developed gill epithelia, form the basis for efficient compensation of pH disturbances during exposure to elevated environmental pCO 2 . Compensation of extracellular acid-base status in turn may be important in avoiding metabolic depression. So far, maintained "performance" at higher seawater pCO 2 (>0.3 to 0.6 kPa) has only been observed in adults/juveniles of active, high metabolic species with a powerful ion regulatory apparatus. However, while some of these taxa are adapted to cope with elevated pCO 2 during their regular embryonic development, gametes, zygotes and early embryonic stages, which lack specialized ion-regulatory epithelia, may be the true bottleneck for ecological success -even of the more tolerant taxa.Our current understanding of which marine animal taxa will be affected adversely in their physiological and ecological fitness by projected scenarios of anthropogenic ocean acidification is quite incomplete. While a growing amount of empirical evidence from CO 2 perturbation experiments suggests that several taxa might react quite se...

Recent advances in understanding trans-epithelial acid-base regulation and excretion mechanisms in cephalopods

“…117 On the other hand substantial acid-base regulatory abilities as found in most cephalopod species represents a common feature that was suggested to make ectothermic marine animals robust to seawater acidification. 45 However, metabolic data from the cuttlefish S. officinalis (acute exposure to 0.6 kPa pCO 2 ) and the squids Dosidicus gigas (acute exposure to 0.1 kPa pCO 2 ) and Sepiteuthis lessoniana (acute; 20 h medium term; 168 h 0.16 and 0.41 kPa pCO 2 ) indicated that these animals respond very differently toward environmental hypercapnia. 12,118,119 Although these studies partly used unrealistically high pCO 2 levels, in the context of environmental hypercania (usually >0.1 kPa), they could indicate a higher sensitivity in active pelagic squids compared to cuttlefish that have a benthic lifestyle.…”

“…45,48,117 Environmental hypercapnia that alters positive diffusion gradients of CO 2 from the animal to the seawater will affect the acid-base physiology of all water breathing animals as intra-and extra-cellular CO 2 concentrations will increase as well to maintain a sufficient diffusion gradient to excrete metabolic CO 2 . 45 Among a range of marine species, some have been identified as more sensitive (e.g. less active calcifying species such as corals or echinoderms) whereas others (many active species such as adult fish and cephalopods) can tolerate relatively high CO 2 concentrations over long exposure times.…”

“…45 Anthropogenic CO 2 emissions are predicted to lead to a rise in surface ocean pCO 2 from 0.04 kPa up to 0.08 -0.14 kPa within this century. 46 The increased hydration of CO 2 changes seawater chemistry, causing a drop in ocean pH.…”

“…49,50 A major hypothesis that had to be tested was, if the ability to compensate for a hypercapnia -induced acidosis by actively accumulating bicarbonate and eliminating protons from their body fluids is a general, unifying feature of tolerant organisms. 45 Thus, a first step was dedicated to the identification of acid-base regulatory structures in marine species and the characterization of the underlying ion-regulatory machinery including ion transporters and channels. The advances in molecular biology and available genomes and transcriptomes of the 21 st century have opened new venues to re-address the mechanisms of ion / pH regulation and excretion in non-model species like cephalopods.…”

Reconsidering the role of carbonate ion concentration in calcification by marine organisms

“…(Keul et al, 2013), and larvae of the Pacific oyster Crassostrea gigas (Gazeau et al, 2011) an inhibitor (Bach et al, 2011(Bach et al, , 2013(Bach et al, , 2015Jokiel, 2011aJokiel, , b, 2013Jokiel et al, 2014 (Bach et al, 2015). Indeed, HCO − 3 uptake is a common mechanism to buffer acidosis and might be facilitated at higher HCO − 3 availability (Boron, 2004;Melzner et al, 2009;Stumpp et al, 2012).…”