Physiological basis for high CO₂ 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, metabolic depression 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 pCO2. 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 pCO2 values (0.1 to 0.4 kPa, 1000 to 4000 μatm) than those of unicellular organisms and gametes, for which the ocean (0.04 kPa, 400 μatm) is the extracellular space. A doubling in environmental pCO2 therefore only represents a 10% change in extracellular CO2 in some marine teleosts. High extracellular pCO2 values are to some degree related to high metabolic rates, as diffusion gradients need to be high in order to excrete an amount of CO2 that is directly proportional to the amount of O2 consumed. In active metazoans, such as teleost fish, cephalopods and many brachyuran crustaceans, exercise induced increases in metabolic rate require an efficient ion-regulatory machinery for CO2 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 pCO2. Compensation of extracellular acid-base status in turn may be extremely important in avoiding metabolic depression. So far, maintained "performance" at higher seawater pCO2 (>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 pCO2 during their regular embryonic development, unicellular gametes, which lack specialized ion-regulatory epithelia, may be the true bottleneck for ecological success – even of the more tolerant taxa.