Physiological basis for high CO2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny? (original) (raw)

30 Oct 2009

| 30 Oct 2009

F. Melzner, M. A. Gutowska, M. Langenbuch, S. Dupont, M. Lucassen, M. C. Thorndyke, M. Bleich, and H.-O. Pörtner

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 _p_CO2. 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 _p_CO2 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 _p_CO2 therefore only represents a 10% change in extracellular _p_CO2 in some marine teleosts. High extracellular _p_CO2 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 _p_CO2. Compensation of extracellular acid-base status in turn may be important in avoiding metabolic depression. So far, maintained "performance" at higher seawater _p_CO2 (>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 _p_CO2 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 CO2 perturbation experiments suggests that several taxa might react quite sensitively to ocean acidification, others seem to be surprisingly tolerant. However, there is little mechanistic understanding on what physiological traits are responsible for the observed differential sensitivities (see reviews of Seibel and Walsh, 2003; Pörtner et al., 2004; Fabry et al., 2008; Pörtner, 2008). This leads us to the first very basic question of how to define general CO2 tolerance on the species level.

Received: 09 Apr 2009

–

Discussion started: 05 May 2009

–

Revised: 04 Sep 2009

–

Accepted: 06 Oct 2009

–

Published: 30 Oct 2009