Biogeosciences www.biogeosciences.net 1726-4170 1726-4189 6 10 2009 10.5194/bg-6-2313-2009 http://www.biogeosciences.net/6/2313/2009/ http://www.biogeosciences.net/6/2313/2009/bg-6-2313-2009.html http://www.biogeosciences.net/6/2313/2009/bg-6-2313-2009.pdf 2313 2331 2009-10-30 Physiological basis for high CO₂ tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny? F. Melzner fmelzner@ifm-geomar.de M. A. Gutowska M. Langenbuch S. Dupont M. Lucassen M. C. Thorndyke M. Bleich H.-O. Pörtner Biological Oceanography, Leibniz-Institute of Marine Sciences (IFM-GEOMAR), Kiel, Germany Institute of Physiology, Christian-Albrechts-University, Kiel, Germany Department of Marine Ecology, Göteborg University, The Sven Lovén Centre for Marine Sciences, Kristineberg, Sweden Integrative Ecophysiology, Alfred-Wegener-Institute for Polar and Marine Research, Bremerhaven, Germany Royal Swedish Academy of Sciences, The Sven Lovén Centre for Marine Sciences, Kristineberg, Sweden 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 <i>p</i>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 <i>p</i>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 <i>p</i>CO₂ therefore only represents a 10% change in extracellular <i>p</i>CO₂ in some marine teleosts. High extracellular <i>p</i>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 <i>p</i>CO₂. Compensation of extracellular acid-base status in turn may be important in avoiding metabolic depression. So far, maintained "performance" at higher seawater <i>p</i>CO₂ (&gt;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 <i>p</i>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. <br><br> 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. Abele, D., Strahl, J., Brey, T., and Philipp, E. E. R.: Imperceptible senescence: Ageing in the ocean quahog Arctica islandica, Free Radical Res., 42, 474–480, 2008. Baldwin, J. and Lee, A. K.: Contributions of aerobic and anaerobic energy-production during swimming in the bivalve mollusk \textitLimaria-fragilis (Family Limidae), J. Comp. Physiol., 129, 361–364, 1979. Batterton, C. V. and Cameron, J. N.: Characteristics of resting ventilation and response to hypoxia, hypercapnia, and emersion in blue-crab \textitCallinectes-sapidus (Rathbun), J. Exp. Zool., 203, 403–418, 1978. Bernier, N. J., Brauner, C. J., Heath, J. W., and Randall, D. J.: Oxygen and carbon dioxide transport during sustained exercise in diploid and triploid chinook salmon (\textitOncorhynchus tshawytscha), Can. J. Fish. Aquat. Sci., 61, 1797–1805, 2004. Bertorello, A. M., and Katz, A. I.: Short-term regulation of renal Na$^+$-K$^+$-ATPase activity: physiological relevance and cellular mechanisms, Am. J Physiol., 265, F743–F755, 1993. Booth, C. E., McMahon, B. R., and Pinder, A. W.: Oxygen-uptake and the potentiating effects of increased hemolymph lactate on oxygen-transport during exercise in the blue-crab, \textitCallinectes-sapidus, J. Comp. Physiol., 148, 111–121, 1982. Booth, C. E., McDonald, D. G., and Walsh, P. J.: Acid-base balance in the sea mussel, \textitMytilus edulis, L, Effects of hypoxia and air exposure on hemolymph acid-base status, Mar. Biol. Lett., 5, 347–358, 1984a. Booth, C. E., McMahon, B. R., Defur, P. L., and Wilkes, P. R. H.: Acid-base regulation during exercise and recovery in the blue crab, \textitCallinectes sapidus, Resp. Physiol., 58, 359–376, 1984b. Boron, W. F.: Regulation of intracellular pH, Adv. Physiol. Educ., 28, 160–179, 2004. Boutilier, R. G., Heming, T. A., and Iwama, G. K.: Appendix – Physicochemical parameters for use in fish respiratory physiology, Fish Physiol., 10, 403–430, 1984. Brauner, C. J., Thorarensen, H., Gallaugher, P., Farrell, A. P., and Randall, D. J.: CO₂ transport and excretion in rainbow trout (\textitOncorhynchus mykiss) during graded sustained exercise, Resp. Physiol., 119, 69–82, 2000. Brix, O., Bardgard, A., Cau, A., Colosimo, A., Condo, S. G., and Giardina, B.: Oxygen-binding properties of cephalopod blood with special reference to environmental temperatures and ecological distribution, J. Exp. Zool., 252, 34–42, 1989. Brown, A. C. and Terwilliger, N. B.: Developmental changes in oxygen uptake in \textitCancer magister (Dana) in response to changes in salinity and temperature, J. Exp. Mar. Biol. Ecol., 241, 179–192, 1999. Budelmann, B. U., Schipp, R., and von Boletzky, S.: Cephalopoda, in: Microscopic Anatomy of Invertebrates, Mollusca~II, Wiley-Liss, New York, Volume 6A, 1997. Burnett, L., Terwilliger, N., Carroll, A., Jorgensen, D., and Scholnick, D.: Respiratory and acid-base physiology of the purple sea urchin, \textitStrongylocentrotus purpuratus, during air exposure: Presence and function of a facultative lung, Biol. Bull., 203, 42–50, 2002. Brewer, P. G. and Peltzer, E. T.: Limits to Marine Life, Science, 324, 347–348, 2009. Caldeira, K. and Wickett, M. E.: Anthropogenic carbon and ocean pH, Nature, 425, 365, 2003. Caldeira, K. and Wickett, M. E.: Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean, J. Geophys. Res., 110, 110, C09S04, doi:10.1029/2004JC002671, 2005. Camacho, A. P., Labarta, U., and Navarro, E.: Energy balance of mussels \textitMytilus galloprovincialis: the effect of length and age, Mar. Ecol.-Prog. Ser., 199, 149–158, 2000. Cameron, J. N. and Polhemus, J. A.: Theory of CO₂ exchange in trout gills, J. Exp. Biol., 60, 183–194, 1974. Chatelier, A., McKenzie, D., and Claireaux, G.: Effects of changes in water salinity upon exercise and cardiac performance in the European seabass (\textitDicentrarchus labrax), Mar. Biol., 147, 855–862, 2005. Claiborne, J. B., Edwards, S. L., and Morrison-Shetlar, A. I.: Acid-base regulation in fishes: cellular and molecular mechanisms, J. Exp. Zool., 293, 302–319, 2002. Decleir, W., Lemaire, J., and Richard, A.: The differentiation of blood proteins during ontogeny in \textitSepia officinalis L., J. Comp. Biochem. Physiol., 40, 923–930, 1971. Dejours P.: Principles of comparative respiratory physiology: North. Holl. Publ. Comp. Amsterdam, New York, 1975. Deigweiher, K., Koschnick, N., Portner, H. O., and Lucassen, M.: Acclimation of ion regulatory capacities in gills of marine fish under environmental hypercapnia, Am. J. Physiol.-Reg I., 295, R1660–R1670, 2008. Desforges, P. R., Harman, S. S., Gilmour, K. M., and Perry, S. F.: Sensitivity of CO₂ excretion to blood flow changes in trout is determined by carbonic anhydrase availability, Am. J. Physiol.-Reg. I., 282, R501–R508, 2002. Dickson, K. A., Donley, J. M., Sepulveda, C., and Bhoopat, L.: Effects of temperature on sustained swimming performance and swimming kinematics of the chub mackerel \textitScomber japonicus, J. Exp. Biol., 205, 969-980, 2002. Diez, J. M. and Davenport, J.: Embryonic respiration in the dogfish (\textitScyliorhinus canicula L), J. Mar. Biol. Ass. UK, 67, 249–261, 1987. Dupont, S., Havenhand, J., Thorndyke, W., Peck, L., and Thorndyke, M.: Near-future level of CO₂-driven ocean acidification radically affects larval survival and development in the brittlestar \textitOphiothrix fragilis, Mar. Ecol.-Prog. Ser., 373, 285–294, 2008. Dupont, S. and Thorndyke, M.: Ocean acidification and its impact on the early life-history stages of marine animals, CIESM Monographs, 36, 124~pp., 2009. Dwyer, J. J. and Burnett, L. E.: Acid-base status of the oyster \textitCrassostrea virginica in response to air exposure and to infections by \textitPerkinsus marinus, Biol. Bull., 190, 139–147, 1996. Elkin, C. E. and Marshall, D. J.: Desperate larvae: the influence of deferred costs and habitat requirements on habitat selection, Mar. Ecol.-Prog. Ser., 335, 143–153, 2007. Evans, D. H., Piermarini, P. M., and Choe, K. P.: The multifunctional fish gill: Dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste, Physiol. Rev., 85, 97–177, 2005. Fabry, V. J., Seibel, B. A., Feely, R. A., and Orr, J. C.: Impacts of ocean acidification on marine fauna and ecosystem processes, ICES J. Mar. Sci., 65, 414–432, 2008. Feely, R. A., Sabine, C. L., Hernandez-Ayon, J. M., Ianson, D., and Hales, B.: Evidence for upwelling of corrosive "acidified" water onto the continental shelf, Science, 320, 1490–1492, 2008. Feraille, E. and Doucet, A.: Na$^+$-K$^+$-ATPase dependent sodium transport in the kidney: hormonal control, Physiol. Rev., 81, 345–418, 2001. Fernandez, M., Bock, C., and Pörtner, H. O.: The cost of being a caring mother: the ignored factor in the reproduction of marine invertebrates, Ecol. Lett., 3, 487–494, 2000. Fernandez, M., Pardo, L. M., and Baeza, J. A.: Patterns of oxygen supply in embryo masses of brachyuran crabs throughout development: the effect of oxygen availability and chemical cues in determining female brooding behavior, Mar. Ecol.-Prog. Ser., 245, 181–190, 2002. Fivelstad, S., Haavik, H., Lovik, G., and Olsen, A. B.: Sublethal effects and safe levels of carbon dioxide in seawater for Atlantic salmon postsmolts (\textitSalmo salar L.): ion regulation and growth, Aquaculture, 160, 305–316, 1998. Fivelstad, S., Olsen, A. B., Asgard, T., Baeverfjord, G., Rasmussen, T., Vindheim, T., and Stefansson, S.: Long-term sublethal effects of carbon dioxide on Atlantic salmon smolts (\textitSalmo salar L.): ion regulation, haematology, element composition, nephrocalcinosis and growth parameters, Aquaculture, 215, 301–319, 2003. Foss, A., Rosnes, B. A., and Oiestad, V.: Graded environmental hypercapnia in juvenile spotted wolffish (\textitAnarhichas minor Olafsen): effects on growth, food conversion efficiency and nephrocalcinosis, Aquaculture, 220, 607–617, 2003. Franke, A.: Effects of elevated seawater $p$CO₂ on embryonic and larval development of Baltic herring, Diploma thesis, Univ. Kiel, 69~pp. 2008. Frankignoulle, M., Bourge, I., and Wollast, R.: Atmospheric CO₂ fluxes in a highly polluted estuary (the Scheldt), Limnol. Oceanogr., 41, 365–369, 1996. Frankignoulle, M., Abril, G., Borges, A., Bourge, I., Canon, C., Libert, E., and Theate, J.-M.: Carbon dioxide emission from european estuaries, Science, 282, 434–436, 1998. Fry, F. E. J.: Effects of the environment on animal activity, Univ. Toronto Studies Biology Series, 55, 1–62, 1947. Gazeau, F., Quiblier, C., Jansen, J. M., Gattuso, J.-P., Middelburg, J. J., and Heip, C. H. R.: Impact of elevated CO₂ on shellfish calcification, Geophys. Res. Lett., 34, L07603, doi:10.1029/2006GL028554, 2007. Gibbs, A. and Somero, G. N.: Na$^+$-K+-Adenosine triphosphatase activities in gills of marine teleost fishes – changes with depths, size and locomotory acitvitiy level, Mar. Biol., 106, 315–321, 1990. Gilmour, K. M. and MacNeill, G. K.: Apparent diffusion limitations on branchial CO₂ transfer are revealed by severe experimental anaemia in brown bullhead (\textitAmeiurus nebulosus), Comp. Biochem. Physiol., 135, 165–175, 2003. Guppy, M. and Withers, P.: Metabolic depression in animals: physiological perspectives and biochemical generalizations, Biol. Rev., 74, 1–40, 1990. Gutowska, M. A., Pörtner, H. O., and Melzner, F.: Growth and calcification in the cephalopod \textitSepia officinalis under elevated seawater $p$CO₂, Mar. Ecol.-Prog. Ser., 373, 303–309, 2008. Gutowska, M. A. and Melzner, F.: Abiotic conditions in cephalopod (\textitSepia officinalis) eggs: embryonic development at low pH and high $p$CO₂, Mar. Biol., 156, 515–519, 2009. Gutowska, M. A., Melzner, F., Langenbuch, M., Bock, C., Claireaux, G., and Pörtner, H. O.: Acid-base regulatory capacity in the cephalopod \textitSepia officinalis exposed to environmental hypercapnia, J. Comp. Phys. B, in press, doi:10.1007/s00360-009-0412-y, 2009. Gutowska, M. A., Melzner, F., Pörtner, H. O., and Meier, S.: Calcification in the cephalopod \textitSepia officinalis in response to elevated seawater $p$CO₂, Mar. Biol., accepted, 2009. Hamdoun, A. and Epel, D.: Embryo stability and vulnerability in an always changing world, P. Natl. Acad. Sci. USA, 104, 1745–1750, 2007. Hamilton, N. M. and Houlihan, D. F.: Respiratory and circulatory adjustments during aquatic treadmill exercise in the european shore crab \textitCarcinus-maenas, J. Exp. Biol., 162, 37–54, 1992. Havenhand, J. N., Buttler, F. R., Thorndyke, M. C., and Williamson, J. E.: Near-future levels of ocean acidification reduce fertilization success in a sea urchin, Curr. Biol., 18, R651–R652, 2008. Heisler, N.: Acid-base regulation in fishes, in: Acid-base regulation in Animals, edited by: Heisler, N., Elsevier Biomedical Press, Amsterdam, 309–356, 1986. Henry, R. P. and Cameron, J. N.: The role of carbonic-anhydrase in respiration, ion regulation and acid-base-balance in the aquatic crab \textitCallinectes-sapidus and the terrestrial crab \textitGecarcinus-lateralis, J. Exp. Biol., 103, 205–223, 1983. Henry, R. P. and Swenson, E. R.: The distribution and physiological significance of carbonic anhydrase in vertebrate gas exchange organs, Resp. Physiol., 121, 1–12, 2000. Hill, A. D., Taylor, A. C., and Strang, R. H. C.: Physiological and metabolic responses of the shore crab \textitCarcinus-maenas (L) during environmental anoxia and subsequent recovery, J. Exp. Mar. Biol. Ecol., 150, 31–50, 1991. Hoegh-Guldberg, O., Mumby, P. J., Hooten, A. J., Steneck, R. S., Greenfield, P., Gomez, E., Harvell, C. D., Sale, P. F., Edwards, A. J., Caldeira, K., et al.: Coral reefs under rapid climate change and ocean acidification, Science, 318, 1737–1742, 2007. Holeton, G. F., Neumann, P., and Heisler, N.: Branchial ion-exchange and acid-base regulation after strenuous exercise in rainbow-trout (\textitSalmo gairdneri), Resp. Physiol., 51, 303–318, 1983. Houlihan, D. F., Innes, A. J., Wells, M. J., and Wells, J.: Oxygen-consumption and blood-gases of \textitOctopus-vulgaris in hypoxic conditions, J. Comp. Physiol., 148, 35–40, 1982. Houlihan, D. F., Duthie, G., Smith, P. J., Wells, M. J., and Wells, J.: Ventilation and circulation during exercise in \textitOctopus-vulgaris, J. Comp. Physiol., 156, 683–689, 1986. Hughes, G. M. and Iwai, T.: Morphometric study of gills in some pacific deep-sea fishes, J. Zool., 184, 155–170, 1978. Hunt, J. C. and Seibel, B. A.: Life history of \textitGonatus onyx (Cephalopoda : Teuthoidea): ontogenetic changes in habitat, \mboxbehavior and physiology, Mar. Biol., 136, 543–552, 2000. Ishimatsu, A., Hayashi, M., Lee, K. S., Kikkawa, T., and Kita, J.: Physiological effects on fishes in a high-CO₂ world, J. Geophys. Res., 110, C09S09, doi:10.1029/2004JC002564, 2005. Ishimatsu, A., Kikkawa, T., Hayashi, M., Lee, K. S., and Kita, J.: Effects of CO₂ on marine fish: larvae and adults, J. Oceanogr., 60, 731–741, 2004. Johansen, K. and Petersen, J. A.: Gas exchange and active ventilation in a starfish, \textitPteraster tesselatus, Z. vergl. Physiol., 70, 1–19, 1971. Johansen, K., Brix, O., and Lykkeboe, G.: Blood gas transport in the cephalopod \textitSepia officinalis, J. Exp. Biol., 99, 331–338, 1982. Kiceniuk, J. W. and Jones, D. R.: Oxygen-transport system in trout (\textitSalmo gairdneri) during sustained exercise, J. Exp. Biol., 69, 247–260, 1977. Kikkawa, T., Ishimatsu, A., and Kita, J.: Acute CO₂ tolerance during the early developmental stages of four marine teleosts, Environ. Toxicol., 18, 375–382, 2003. Knoll, A. H., Barnbach, R. K., Payne, J. L., Pruss, S., and Fischer, W. W.: Paleophysiology and end-Permian mass extinction, Earth Planet. Sci. Lett., 256, 295–313, 2007. Korsmeyer, K. E., Lai, N. C., Shadwick, R. E., and Graham, J. B.: Oxygen transport and cardiovascular responses to exercise in the yellowfin tuna \textitThunnus albacares, J. Exp. Biol., 200, 1987–1997, 1997. Kraffe, E., Tremblay, R., Belvin, S., LeCoz, J. R., Marty, Y., and Guderley, H.: Effect of reproduction on escape responses, metabolic rates and muscle mitochondrial properties in the scallop \textitPlacopecten magellanicus, Mar. Biol., 156, 25–38, 2008. Kurihara, H. and Shirayama, Y.: Effects of increased atmos extracellular pHric CO₂ on sea urchin early development, Mar. Ecol.-Prog. Ser., 274, 161–169, 2004. Kurihara, H. and Ishimatsu, A.: Effects of high CO₂ seawater on the copepod (\textitAcartia tsuensis) through all life stages and subsequent generations, Mar. Pollut. Bull., 56, 1086–1090, 2008. Kurihara, H., Matsui, M., Furukawa, H., Hayashi, M., and Ishimatsu, A.: Long-term effects of predicted future seawater CO₂ conditions on the survival and growth of the marine shrimp \textitPalaemon pacificus, J. Exp. Mar. Biol. Ecol., 367, 41–46, 2008. Kurihara, H.: Effects of CO₂-driven ocean acidification on the early developmental stages of invertebrates, Mar. Ecol-Prog. Ser., 373, 275–284, 2008. Langdon, C., Takahashi, T., Sweeney, C., Chipman, D., Goddard, J., Marubini, F., Aceves, H., Barnett, H., and Atkinson, M. J.: Effect of calcium carbonate saturation state on the calcification rate of an experimental coral reef, Global Biogeochem. Cy., 14, 639–654, 2000. Langenbuch, M. and Pörtner, H. O.: High sensitivity to chronically elevated CO₂ levels in a eurybathic marine sipunculid, Aquat. Toxicol., 70, 55–61, 2004. Larsen, B. K., Pörtner, H. O., and Jensen, F. B.: Extra- and intracellular acid-base balance and ionic regulation in cod (\textitGadus morhua) during combined and isolated exposures to hypercapnia and copper, Mar. Biol., 128, 337–346, 1997. Lee, C. G., Devlin, R. H., and Farrell, A. P.: Swimming performance, oxygen consumption and excess post-exercise oxygen consumption in adult transgenic and ocean-ranched Coho salmon, J. Fish Biol., 62, 753–766, 2003. Legeay, A. and Massabuau, J. C.: Effect of salinity on hypoxia \mboxtolerance of resting green crabs, \textitCarcinus maenas, after feeding, Mar. Biol., 136, 387–396, 2000. Lindinger, M. I., Lauren, D. J., and McDonald, D. G.: Acid-base-balance in the sea mussel, \textitMytilus edulis, 3, Effects of environmental hypercapnia on intracellular and extracellular acid-base-balance, Mar. Biol. Lett., 5, 371–381, 1984. Mangum, C. P.: Gas transport in the blood, in: Squid as Experimental Animals, edited by: Gilbert, D. L., Adelman Jr., E. J., and Arnold, J. M., Plenum, New York, 443–468, 1990. McDonald, D. G., McMahon, B. R., and Wood, C. M.: Analysis of acid-base disturbances in the hemolymph following strenuous activity in the dungeness crab, \textitCancer-magister, J. Exp. Biol., 79, 47–58, 1979. McGaw, I. J.: The interactive effects of exercise and feeding on oxygen uptake, activity levels, and gastric processing in the graceful crab \textitCancer gracilis, Physiol. Biochem. Zool., 80, 335–343, 2007. McKenzie, D. J., Taylor, E. W., Dalla Valle, A. Z., and Steffensen, J. F.: Tolerance of acute hypercapnic acidosis by the European eel (\textitAnguilla anguilla), J. Comp. Physiol., 172, 339–346, 2002. McMahon, B. R., McDonald, D. G., and Wood, C. M.: Ventilation, oxygen-uptake and hemolymph oxygen-transport, following enforced exhausting activity in the dungeness crab \textitCancer magister, J. Exp. Biol., 80, 271–285, 1979. Melzner, F., Mark, F. C., and Pörtner, H. O.: Role of blood-oxygen transport in thermal tolerance of the cuttlefish, \textitSepia officinalis, Integr. Comp. Biol., 47, 645–655, 2007. Melzner, F., Göbel, S., Langenbuch, M., Gutowska, M. A., Pörtner, H. O., and Lucassen, M.: Swimming performance in Atlantic Cod (\textitGadus morhua) following long-term (4–12 months) acclimation to elevated sea water $p$CO₂, Aquat. Toxicol., 92, 30–37, 2009. Michaelidis, B., Ouzounis, C., Paleras, A., and Pörtner, H. O.: Effects of long-term moderate hypercapnia on acid-base balance and growth rate in marine mussels \textitMytilus galloprovincialis, Mar. Ecol.-Prog. Ser., 293, 109–118, 2005. Michaelidis, B., Spring, A., and Pörtner, H. O.: Effects of long-term acclimation to environmental hypercapnia on extracellular acid-base status and metabolic capacity in Mediterranean fish \textitSparus aurata, Mar. Biol., 150, 1417–1429, 2007. Miles, H., Widdicombe, S., Spicer, J. I., and Hall-Spencer, J.: Effects of anthropogenic seawater acidification on acid-base balance in the sea urchin \textitPsammechinus miliaris, Mar. Pollut. Bull., 54, 89–96, 2007. Milligan, C. L. and Wood, C. M.: Regulation of blood-oxygen transport and red-cell pHi after exhaustive activity in rainbow-trout (\textitSalmo gairdneri) and starry flounder (\textitPlatichthys stellatus), J. Exp. Biol., 133, 263–282, 1987. Nixon, M. and Mangold, K.: The early life of \textitSepia officinalis, and the contrast with that of \textitOctopus vulgaris (Cephalopoda), J. Zool., 245, 407–421, 1998. Odor, R. K. and Webber, D. M.: Invertebrate athletes – trade-offs between transport efficiency and power-density in cephalopod evolution, J. Exp. Biol., 160, 93–112, 1991. Otero-Villanueva, M. D. M., Kelly, M. S., and Burnell, G.: How diet influences energy partitioning in the regular echinoid \textitPsammechinus miliaris; constructing an energy budget, J. Exp. Mar. Biol. Ecol., 304, 159–181, 2004. Pane, E. F. and Barry, J. P.: Extracellular acid-base regulation \mboxduring short-term hypercapnia is effective in a shallow-water crab, but ineffective in a deep-sea crab, Mar. Ecol.-Prog. Ser., 334, 1–9, 2007. Perry, S. F.: Carbon-dioxide excretion in fishes, Can. J. Zool., 64, 565–572, 1986. Perry, S. F. and Gilmour, K.: An evaluation of factors limiting carbon-dioxide excretion by trout red-blood-cells in vitro, J. Exp. Biol., 180, 39–54, 1993. Perry, S. F. and Gilmour, K. M.: Acid-base balance and CO₂ excretion in fish: Unanswered questions and emerging models, Resp. Physiol. Neurobiol., 154, 199–215, 2006. Piermarini, P. M., Choi, I. and Boron, W. F.: Cloning and characterization of an electrogenic Na/HCO$_3^-$ cotransporter from the squid giant fiber lobe, Am. J. Physiol., 292, C2032–C2045, 2007. Pörtner, H. O., Webber, D. M., Boutilier, R. G., and O'Dor, R. K.: Acid-base regulation in exercising squid (\textitIllex illecebrosus, \textitLoligo pealei), Am. J. Physiol., 261, R239–R246, 1991. Pörtner, H. O., Reipschlager, A., and Heisler, N.: Acid-base regulation, metabolism and energetics in \textitSipunculus nudus as a function of ambient carbon dioxide level, J. Exp. Biol., 201, 43–55, 1998. Pörtner, H. O., Langenbuch, M., and Reipschlager, A.: Biological impact of elevated ocean CO₂ concentrations: Lessons from animal physiology and earth history, J. Oceanogr., 60, 705–718, 2004. Pörtner, H. O.: Ecosystem effects of ocean acidification in times of ocean warming: a physiologist's view, Mar. Ecol.-Prog. Ser., 373, 203–217, 2008. Ramnanan, C. J. and Storey, K. B.: Suppression of Na$^+$/K$^+$-ATPase activity during estivation in the land snail \textitOtala lacteal, J. Exp. Biol., 209, 677–688, 2006. Randall, D.: The control of respiration and circulation in fish during exercise and hypoxia, J. Exp. Biol., 100, 275–285, 1982. Randall, D. and Daxboeck, C.: Oxygen and carbon-dioxide transport across fish gills, Fish Physiol., 10, 263–314, 1984. Scarabello, M., Heigenhauser, G. J. F., and Wood, C. M.: The oxygen debt hypothesis in juvenile rainbow-trout after exhaustive exercise, Resp. Physiol., 84, 245–259, 1991. Schipp, R., Mollenhauer, S., and Vonboletzky, S.: Electron microscopical and histochemical-studies of differentiation and function of the cephalopod gill (\textitSepia officinalis L), Zoomorphologie, 93, 193–207, 1979. Seibel, B. A., Thuesen, E. V., Childress, J. J., and Gorodezky, L. A.: Decline in pelagic cephalopod metabolism with habitat depth reflects differences in locomotory efficiency, Biol. Bull., 192, 262–278, 1997. Seibel, B. A. and Childress, J. J.: Metabolism of benthic octopods (Cephalopoda) as a function of habitat depth and oxygen concentration, Deep-Sea Res. Pt I, 47, 1247–1260, 2000. Seibel, B. A. and Walsh, P. J.: Carbon cycle – Potential, impacts of CO₂ injection on deep-sea biota, Science, 294, 319–320, 2001. Seibel, B. A. and Walsh, P. J.: Biological impacts of deep-sea carbon dioxide injection inferred from indices of physiological performance, J. Exp. Biol., 206, 641–650, 2003. Shadwick, R. E., Odor, R. K., and Gosline, J. M.: Respiratory and cardiac-function during exercise in squid, Can. J. Zool., 68, 792–798, 1990. Siikavuopio, S. I., Mortensen, A., Dale, T., and Foss, A.: Effects of carbon dioxide exposure on feed intake and gonad growth in green sea urchin, \textitStrongylocentrotus droebachiensis, Aquaculture, 266, 97–101, 2007. Somero, G. N. and Childress, J. J.: A violation of the metabolism-size scaling paradigm – activities of glycolytic-enzymes in muscle increase in larger-size fish, Physiol. Zool., 53, 322–337, 1980. Spicer, J. I., Taylor, A. C., and Hill, A. D.: Acid-base status in the sea-urchins \textitPsammechinus miliaris and \textitEchinus esculentus (Echinodermata: Echinoidea) during emersion, Mar. Biol., 99, 527–534, 1988. Spicer, J. I., Raffo, A., and Widdicombe, S.: Influence of CO₂-related seawater acidification on extracellular acid-base balance in the velvet swimming crab \textitNecora puber, Mar. Biol., 151, 1117–1125, 2007. Steffensen, J. F., Tufts, B. L., and Randall, D. J.: Effect of burst swimming and adrenaline infusion on O₂ consumption and CO₂ excretion in rainbow-trout, \textitSalmo-gairdneri, J. Exp. Biol., 131, 427–434, 1987. Sukhotin, A. A., Abele, D., and Portner, H. O.: Growth, metabolism and lipid peroxidation in \textitMytilus edulis: age and size effects, Mar. Ecol.-Prog. Ser., 226, 223–234, 2002. Taylor, H. H. and Taylor, E. W: Gills and lungs: the exchange of gases, In: Microscopic Anatomy of Invertebrates, Decapod Crustacea: Wiley-Liss, New York, Volume 10, 1997. Thomas, S.: Changes in blood acid-base-balance in trout (\textitSalmo gairdneri) following exposure to combined hypoxia and hypercapnia, J. Comp. Physiol., 152, 53–57, 1983. Thomas, S., Poupin, J., Lykkeboe, G., and Johansen, K.: Effects of graded-exercise on blood-gas tensions and acid-base characteristics of rainbow-trout, Resp. Physiol., 68, 85–97, 1987. Thomsen, J.: Ion and acid-base regulation in marine invertebrates in reponse to altered carbonate system parameters, Diploma Thesis, Univ Kiel, 63~pp., 2009. Thorson, G.: Reproductive and larval ecology of marine bottom invertebrates, Biol. Rev., 25, 1–45, 1950. Thorson, G.: Some factors influencing the recruitment and establishment of marine benthic communities, Neth. J. Sea Res., 3, 267–293, 1966. Torres, J. J., Belman, B. W., and Childress, J. J.: Oxygen-consumption rates of midwater fishes as a function of depth of occurrence, Deep-Sea Res., 26, 185–197, 1979. Truchot, J. P.: Effect of hypercapnia on acid-base status of blood in crab \textitCarcinus maenas (L)(Crustacea-Decapoda), Comptes Rendus Hebdomadaires Des Seances De L Academie Des Sciences Serie~D, 280, 311–314, 1975. Truchot, J. P.: Carbon-dioxide combining properties of blood of shore crab \textitCarcinus maenas L – carbon-dioxide solubility coefficient and carbonic-acid dissociation-constants, J. Exp. Biol., 64, 45–57, 1976. Truchot, J. P.: Mechanisms of the compensation of blood respiratory acid-base disturbances in the shore crab, \textitCarcinus maenas (L), J. Exp. Zool., 210, 407–416, 1979. Truchot, J. P. and Duhameljouve, A.: Oxygen and carbon-dioxide in the marine inter-tidal environment – diurnal and tidal changes in rockpools, Resp. Physiol., 39, 241–254, 1980. Tufts, B. L. and Perry, S. F.: Carbon dioxide transport and excretion, In: Carbon dioxide transport and excretion, Fish Physiology v17 Fish Respiration: Academic Press, San Diego, 229–281~pp., 1998. Tunnicliffe, V., Davies, K. T. A., Butterfield, D. A., Embley, R. W., Rose, J. M., and Chadwick, W. W.: Survival of mussels in extremely acidic waters on a submarine volcano, Nature Geosci., 2, 344–348, 2009. Vahl, O.: The relationship between specific dynamic action (SDA) and growth in the common starfish, \textitAsterias rubens L., Oecologia, 61, 122–125, 1984. Van den Thillart, G. D., Randall, D., and Hoa-Ren, L.: CO₂ and H$^+$ excretion by swimming coho salmon, \textitOncorhynchus kisutch, J. Exp. Biol., 107, 169–180, 1983. Virkki, L. V., Choi, I., Davis, B. A., and Boron, W. F.: Cloning of a Na$^+$-driven Cl/HCO3$^-$ exchanger from squid giant fiber lobe, Am. J. Physiol., 285, C771–C780, 2003. Watt, A. J. S., Whiteley, N. M., and Taylor, E. W.: An in situ study of respiratory variables in three British sublittoral crabs with different routine rates of activity, J. Exp. Mar. Biol. Ecol., 239, 1–21, 1999. Webber, D. M. and Odor, R. K.: Monitoring the metabolic-rate and activity of free-swimming squid with telemetered jet pressure, J. Exp. Biol., 126, 205–224, 1986. Webster, S. K.: Oxygen-consumption in echinoderms from several geographical locations, with particular reference to Echinoidea, Biol. Bull., 148, 157–164, 1975. Weigelt, M. and Rumohr, H.: Effects of wide-range oxygen depletion on benthic fauna and demersal fish in Kiel Bay 1981–1983, Rep. Mar. Res., 31, 124–136, 1986. Wells, M. J., Odor, R. K., Mangold, K., and Wells, J.: oxygen-consumption in movement by octopus, Mar. Behav. Physiol., 9, 289–303, 1983. Wheatly, M. G. and Henry, R. P.: Extracellular and intracellular acid-base regulation in crustaceans, J. Exp. Zool., 263, 127–142, 1992. Widdicombe, S. and Spicer, J. I.: Predicting the impact of ocean acidification on benthic biodiversity: What can animal physiology tell us? J. Exp. Mar. Biol. Ecol., 366, 187–197, 2008. Widdows, J.: Effect of temperature and food on heart beat, ventilation rate and oxygen-uptake of \textitMytilus edulis, Mar. Biol., 20, 269–276, 1973. Willson, L. L., and Burnett, L. E.: Whole animal and gill tissue oxygen uptake in the Eastern oyster, \textitCrassostrea virginica: Effects of hypoxia, hypercapnia, air exposure, and infection with the protozoan parasite \textitPerkinsus marinus, J. Exp. Mar. Biol. Ecol., 246, 223–240, 2000. Wilson, J. M., Laurent, P., Tufts, B. L., Benos, D. J., Donowitz, M., Vogl, A. W., and Randall, D. J.: NaCl uptake by the branchial epithelium in freshwater teleost fish: An immunological approach to ion-transport protein localization, J. Exp. Biol., 203, 2279–2296, 2000. Wood, C. M. and Munger, R. S.: Carbonic-anhydrase injection provides evidence for the role of blood acid-base status in stimulating ventilation after exhaustive exercise in rainbow-trout, J. Exp. Biol., 194, 225–253, 1994. Wood, H. L., Spicer, J. I., and Widdicombe, S.: Ocean acidification may increase calcification rates, but at a cost, P. Roy. Soc. B-Biol. Sci., 275, 1767–1773, 2008. Wootton, J. T., Pfister, C. A., and Forester, J. D.: Dynamic patterns and ecological impacts of declining ocean pH in a high-resolution multi-year dataset, P. Natl. Acad. Sci. USA, 105, 18848–18853, 2008. Yamamoto, K.: Increase of arterial O₂ content in exercised yellowtail (\textitSeriola quinqueradiata), Comp. Biochem. Physiol., 98, 43–46, 1991. Zielinski, S., Sartoris, F. J., and Pörtner, H. O.: Temperature effects on hemocyanin oxygen binding in an Antarctic cephalopod, Biol. Bull., 200, 67–76, 2001.