Extracellular acid–base regulation during short-term hypercapnia is effective in a shallow-water crab, but ineffective in a deep-sea crab

Abstract

Rising levels of atmospheric carbon dioxide could be curbed by large-scale sequestration of CO 2 in the deep sea. Such a solution requires prior assessment of the impact of hypercapnic, acidic seawater on deep-sea fauna. Laboratory studies were conducted to assess the short-term hypercapnic tolerance of the deep-sea Tanner crab Chionoecetes tanneri, collected from 1000 m depth in Monterey Canyon off the coast of central California, USA. Hemolymph acidbase parameters were monitored over 24 h of exposure to seawater equilibrated with ~1% CO 2 (seawater P CO 2 6 torr or 0.8 kPa, pH 7.1), and compared with those of the shallow-living Dungeness crab Cancer magister. Short-term hypercapnia-induced acidosis in the hemolymph of Chionoecetes tanneri was almost uncompensated, with a net 24 h pH reduction of 0.32 units and a net bicarbonate accumulation of only 3 mM. Under simultaneous hypercapnia and hypoxia, short-term extracellular acidosis in Chionoecetes tanneri was completely uncompensated. In contrast, Cancer magister fully recovered its hemolymph pH over 24 h of hypercapnic exposure by net accumulation of 12 mM bicarbonate from the surrounding medium. The data support the hypothesis that deep-sea animals, which are adapted to a stable environment and exhibit reduced metabolic rates, lack the short-term acid -base regulatory capacity to cope with the acute hypercapnic stress that would accompany large-scale CO 2 sequestration. Additionally, the data indicate that sequestration in oxygen-poor areas of the ocean would be even more detrimental to deep-sea fauna.KEY WORDS: CO 2 · Deep sea · Physiology · Decapod crustacea · Acid-base regulation ·Chionoecetes tanneri · Cancer magister Resale or republication not permitted without written consent of the publisherThe ocean's large-scale absorption, as well as possible future anthropogenic sequestration of atmospheric CO 2 , will result in long-term acidification of the water. The deep-sea crab Chionoecetes tanneri (collected from Monterey Canyon at 1000 m depth) is unable to regulate extracellular pH during short-term CO 2 exposure. The results of Pane & Barry support the hypothesis that hypercapnia will have a profound physiological impact on deep-sea organisms.

Sensitivity to ocean acidification parallels natural pCO 2 gradients experienced by Arctic copepods under winter sea ice

“…18,19), with the hypothesis being that organisms will have more effective mechanisms to cope with stress if they frequently experience a more variable environment. One example of this hypothesis for pelagic zooplankton comes from knowledge of mesozooplankton (20) distributions in relation to oxygen minimum zones (OMZs), and thus their sensitivity to low oxygen (20).…”

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

“…20,21 Studies using decapod crustaceans demonstrated that these invertebrates can also fully compensate hypercapnia induced pH e disturbances through active bicarbonate accumulation in body fluids. [22][23][24][25] For example, in response to 1 kPa water pCO 2 Cancer magister increased its blood [HCO 3 ¡ ] by 12 mM within 24 h to fully compensate pH e . 25 Studies on Carcinus maenas and Callinectes sapidus also indicated comparable high acid-base regulatory abilities.…”

“…[22][23][24][25] For example, in response to 1 kPa water pCO 2 Cancer magister increased its blood [HCO 3 ¡ ] by 12 mM within 24 h to fully compensate pH e . 25 Studies on Carcinus maenas and Callinectes sapidus also indicated comparable high acid-base regulatory abilities. [26][27][28][29] Although less active marine invertebrates were generally shown to have lower capabilities to compensate for extracellular acid-base disturbances, some echinoderms including sea urchins (Strongylocentrotus droebachiensis) and brittle stars (Amphiura filiformis) were demonstrated to be able to control extracellular pH to a certain degree.…”

Physiological effects of environmental acidification in the deep-sea urchin <i>Strongylocentrotus fragilis</i>

“…Samples of PCF were drawn anaerobically through the oral membrane into ice-cold gas-tight Hamilton syringes rinsed with a modified Crab Ringer comprised of NaCl (460 mM), KCl (10 mM), CaCl 2 (20 mM), MgCl 2 (9.5 mM), adjusted to pH 7.8 (Lang and Gainer, 1969;Pane and Barry, 2007). Fluid samples were then centrifuged aerobically at 4000 × g at 5 • C for 1 min to remove debris, added (200 µL) to round-bottom flasks for equilibration with humidified gas mixtures of CO 2 and nitrogen from preanalyzed cylinders (Airgas), and allowed to equilibrate for 90 min in a shaking cooler at 5 • C. Samples were then drawn into gas-tight syringes and pH (total scale) was measured using a microelectrode and in-line reference electrode (Microelectrodes) thermostatted to 5 • C and coupled to an Accumet (Fisher Scientific) pH meter.…”

“…The high amount of genetic diversity and/or plasticity presumably required for a population to persist throughout a bathymetric range including an OMZ suggests we should expect fairly high tolerance to at least the extent of conditions seen within its bathymetric range. We expect the apparent limitation in tolerance of OMZ taxa to global climate change is not a product of evolutionary constancy, but rather is a product of the limited energy (food and oxygen) available to cope with the stress of environmental change (Barry et al, 2011;Pane and Barry, 2007;Seibel and Walsh, 2003). Taking these considerations into account, we aim to investigate the physiological effects of elevated pCO 2 on a calcifying OMZ taxon, the deep-sea fragile urchin Strongylocentrotus fragilis.…”