Biogeosciences
www.biogeosciences.net
1726-4170
1726-4189
6
10
2009
10.5194/bg-6-2207-2009
http://www.biogeosciences.net/6/2207/2009/
http://www.biogeosciences.net/6/2207/2009/bg-6-2207-2009.html
http://www.biogeosciences.net/6/2207/2009/bg-6-2207-2009.pdf
2207
2215
2009-10-15
Impact of anthropogenic ocean acidification on thermal tolerance of the spider crab <i>Hyas araneus</i>
K. Walther
kathleen.walther@awi.de
F. J. Sartoris
C. Bock
H. O. Pörtner
Alfred-Wegener-Institute for Polar and Marine Research, Department Integrative Ecophysiology, Am Handelshafen 12, 27570 Bremerhaven, Germany
Future scenarios for the oceans project combined developments of CO<sub>2</sub>
accumulation and global warming and their impact on marine ecosystems. The
synergistic impact of both factors was addressed by studying the effect of
elevated CO<sub>2</sub> concentrations on thermal tolerance of the
cold-eurythermal spider crab <i>Hyas araneus</i> from the population around Helgoland. Here
ambient temperatures characterize the southernmost distribution limit of
this species. Animals were exposed to present day normocapnia (380 ppm
CO<sub>2</sub>), CO<sub>2</sub> levels expected towards 2100 (710 ppm) and beyond (3000 ppm).
Heart rate and haemolymph PO<sub>2</sub> (P<sub>e</sub>O<sub>2</sub>) were measured
during progressive short term cooling from 10 to 0°C and during warming
from 10 to 25°C. An increase of P<sub>e</sub>O<sub>2</sub> occurred during
cooling, the highest values being reached at 0°C under all three
CO<sub>2</sub> levels. Heart rate increased during warming until a critical
temperature (<i>T<sub>c</sub></i>) was reached. The putative <i>T<sub>c</sub></i> under normocapnia
was presumably >25°C, from where it fell to 23.5°C under 710 ppm
and then 21.1°C under 3000 ppm. At the same time, thermal
sensitivity, as seen in the <i>Q<sub>10</sub></i> values of heart rate, rose with
increasing CO<sub>2</sub> concentration in the warmth. Our results suggest a
narrowing of the thermal window of <i>Hyas araneus</i> under moderate increases in CO<sub>2</sub>
levels by exacerbation of the heat or cold induced oxygen and capacity
limitation of thermal tolerance.
Ahsanullah, M. and Newell, R. C.: Factors affecting the heart rate of the shore crab \textitCarcinus \textitmaenas (L.), Comp. Biochem. Physiol., 39A, 277–287, 1971.
Bernárdez, C., González-Gurriarán, E., García-Calvo, B., Corgos, A., and Freire, J.: Movements of juvenile and adult spider crab (\textitMaja squinado) in the Ria da Coruna (N-W Spain), Aquatic telemetry: advances and applications, Proceedings of the Fifth Conference on Fish Telemetry held in Europe, Ustica, Italy, 9–13 June 2003, Rome, FAO/COISPA, 295 pp., 2005.
Bock, C., Frederich, M., Wittig, R.-M., and Pörtner, H. O.: Simultaneous observations of haemolymph flow and ventilation in marine spider crabs at different temperatures: a flow weighted MRI study, Magn. Reson. Imaging, 19, 1113–1124, 2001.
Brevard, M. E., Duong, T. Q., King, J. A., and Ferris, C. F.: Changes in MRI signal intensity during hypercapnic challenge under conscious and anesthetized conditions, Magn. Reson. Imaging, 21, 995–1001, 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, C09S04, doi:10.1029/2004JC002671, 2005.
Cameron, J. N.: Effects of Hypercapnia on Blood Acid-Base Status, NaCl Fluxes, and Trans-Gill Potential in Freshwater Blue crabs, \textitCallinectes sapidus, J. Comp. Physiol., 123, 137–141, 1978.
Cameron, J. N.: Compensation of hypercapnic acidosis in the aquatic blue crab, \textitCallinectes sapidus: the predominance of external sea water over carapace carbonate as the proton sink, J. Exp. Biol., 114, 197–206, 1985.
Cameron, J. N. and Iwama, G. K.: Compensation of progressive hypercapnia in channel catfish and blue crabs, J. Exp. Biol., 133, 183–197, 1987.
Christiansen, M. E. (Ed.): Crustacea Decapoda Brachyura, in: Marine Invertebrates of Scandinavia, No. 2, Universitetsforlaget, Oslo, 1969.
Cuculescu, M., Hyde, D., amd Bowler, K.: Thermal tolerance of two species of marine crab, \textitCancer pagurus and \textitCarcinus maenas, J. Therm. Biol., 23, 107–110, 1998.
DeFur, P. L. and Mangum, C. P.: The effects of environmental variables on the heart rate of invertebrates, Comp. Biochem. Physiol., 62A, 283–294, 1979.
Derby, C. D., Ache, B. W., and Carr, W. E. S.: Purinergic modulation in the brain of the spiny lobster, Brain Research, 421, 57–64, 1987.
Frederich, M. and Pörtner, H. O.: Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in spider crab, \textitMaja squinado, Am. J. Physiol. Regulatory Integrative Comp. Physiol., 279, R1531–R1538, 2000.
Frederich, M., Sartoris, F. J., Arntz, W. E., and Pörtner, H. O.: Haemolymph Mg$^2+$ regulation in decapod crustaceans: Physiological correlates and ecological consequences in polar areas, J. Exp. Biol., 203, 1383–1393, 2000.
IPCC: Climate Change 2001: Third Assessment Report of the Intergovernmental Panel on Climate Change, Campridge University Press, Campridge, 2001.
IPCC: Climate Change 2007, Fourth Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press, Cambridge, 2007.
Lannig, G., Cherkasov, A. S., Pörtner, H. O., Bock, C., and Sokolovy, I. M.: Cadmium-dependent oxygen limitation affects temperature tolerance in eastern oysters (\textitCrassostrea virginica Gmelin), Am. J. Physiol. Regul. Integr. Comp. Physiol., 294, R1338–R2346, 2008.
Maurer, G., Wilkens, J. L., and Grieshaber, M. K.: Modulatory effects of adenosine and adenine nucleotides on different heart preparations of the American lobster, \textitHomarus americanus, J. Exp. Biol., 211, 661–670, 2008.
Melzner, F., Bock, C., and Pörtner, H. O.: Critical temperatures in the cephalopod \textitSepia officinalis investgated using\textit in vivo $^31$P NMR spectroscopy, J. Exp. Biol., 209, 891–906, 2006.
Metzger, R., Sartoris, F. J., Langenbuch, M., and Pörtner, H. O.: Influence of elevated CO<sub>2</sub> concetrations on thermal tolerance of the edible crab \textitCancer pagurus, J. Therm. Biol., 32, 144–151, 2007.
Orr, J. C., Maier-Reimer, E., Mikolajewicz, U., Monfray, P., Sarmiento, J. L., Toggweiler, J. R., Taylor, N. K., Palmer, J., Gruber, N., Sabine, C. L., Le Quéré, C., Key, R. M., and Boutin, J.: Estimates of anthropogenic carbon uptake from four three-dimensional global ocean models, Global Biogeochem. Cy., 15(1), 43–60, 2001.
Pane, E. F. and Barry, J. P.: Extracellular acid-base regulation during short-term hypercapnia is effective in a shallow-water crab, but uneffective in a deep-sea crab, Mar. Ecol. Prog. Ser., 334, 1–9, 2007.
Pohlmann, T.: Predicting the thermocline in a circulation model of the North Sea – Part I: model description, calibration and verification, Cont. Shelf Res., 16(7), 131–146, 1996.
Pörtner, H. O.: Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchies of thermal tolerance in animals, Comp. Biochem. Phys. A, 132, 739–761, 2002.
Pörtner, H. O., Langenbuch, M., and Michaelidis, B.: Synergistic effects of temperature extremes, hypoxia, and increases in CO<sub>2</sub> on marine animals: From Earth history to global change, J. Geophys. Res., 110, C09S10, doi:10.1029/2004JC002561, 2005.
Pörtner, H. O.: Climate-dependent evolution of Antarctic ectotherms: an integrative anaysis, Deep-Sea Res. II, 53, 1071–1104, 2006.
Pörtner, H. O. and Knust, R.: Climate Change Affects Marine Fishes Through the Oxygen Limitation of Thermal Tolerance, Science, 315, 95–97, doi:10.1126/science.1135471, 2007.
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.
Pörtner, H. O. and Farrell, A. P.: Physiology and Climate Change, Science, 322, 690–692, doi:10.1126/science.1163156, 2008.
Reipschläger, A., Nilsson, G. E., and Pörtner, H. O.: A role for adenosine in metabolic depression in the marine invertebrate \textitSipunculus nudus, Am. J. Physiol.-Reg. I., 272, R350–R356, 1997.
Spicer, J. I., Raffo, A., and Widdicombe, S.: Influence of CO<sub>2</sub>-related seawater acidification on extracellular acid-base balance in the velvet swimming crab \textitNecora puber, Mar. Biol., 151, 1117–1125, 2007.
Stegen, E. and Grieshaber, M. K.: Adenosine increases ventilation rate, cardiac performance and haemolymph velocity in the American lobster \textitHomarus americanus, J. Exp. Biol., 204, 947–957, 2001.
Stillman, J. H. and Somero, G. N.: Adaption to temperature stress and aerial exposure in congeneric species of intertidal porcelain crabs (genus \textitPetrolisthes): Correlation of physiology, biochemistry and morphology with vertical distribution, J. Exp. Biol., 199, 1845–1855, 1996.
Svendsen, H., Breszczynska-Møller, A., Hagen, J. O., Lefauconnier, B., Tverberg, V., Gerland, S., Ørbæk, J. B., Bischof, K., Papucci, C., Zajaczkowski, M., Azzolini, R., Bruland, O., Wiencke, C., Winther, J.-G., and Dallmann, W.; The physical environment of Kongsfjorden-Krossfjorden, an Arctic fjord system in Svalbard, Polar Res., 21(1), 133–166, 2002.
Truchot, J.-P.: Water carbonate alkalinity as a determinant of hemolymph acid-base balance in the shore crab, \textitCarcinus maenas: a study at two different ambient $P$CO<sub>2</sub> and $P$O<sub>2</sub> levels, J. Comp. Physiol. B, 154, 601–606, 1984.
Wickins, J. F.: The effect of hypercapnic sea water on growth and mineralization in penaeid prawns, Aquaculture, 41, 37–48, 1984.
Wiltshire, K. H. and Manly, B. F. J.: The warming trend at Helgoland Roads, North Sea: phytoplankton response, Helgoland Mar. Res., 58, 269–273, 2004.
Wittmann, A. C., Schröer, M., Bock, C., Steeger, H.-U., Paul, R. J., and Pörtner, H.-O.: Indicators of oxygen- and capacity-limited thermal tolerance in the lugworm \textitArenicola marina, Climate Res., 37, 227–240, 2008.
Worden, M. K., Clark, C. M., Conaway, M., and Qadri, S. A.: Temperature dependence of cardiac performance in the lobster \textitHomarus americanus, J. Exp. Biol., 209, 1024–1034, 2006.
Zainal, K. A. Y., Taylor, A. C., and Atkinson, R. J. A.: The effect of temperature and hypoxia on the respiratory physiology of the squat lobsters, \textitMunida rugosa and \textitMunida sarsi (Anomura, Galatheidae), Comp. Biochem. Physiol., 101A, 557–567, 1992.