Document Type: ORIGINAL RESEARCH PAPER

Authors

Department of Marine and Costal Studies, School of Energy Sciences, Madurai Kamaraj University, Madurai 625021, Tamilnadu, India

Abstract

A laboratory level microcosm analysis of the impacts of ocean acidification on the environmental stress biomarkers in Portunus pelagicus (Linneaus 1758)exposed to a series of pH regimes expected in the year 2100 (pH 7.5 and 7.0) and leakage from a sub-seabed carbon dioxide storage site (pH 6.5 - 5.5) was carried out. Levels of the antioxidant enzyme catalase, the phase II detoxification enzyme, glutathione S. transferase, the lipid peroxidation biomarker, malondialdehyde, acetylcholinesterase, and reduced glutathione were estimated in the tissues of the exposed animals to validate theses enzymes as biomarkers of Hypercapnia. The integrated biomarkers indicated a stress full environment in all animals except those exposed to the control seawater (pH 8.1). The reducing pH was also observed to be highly lethal to the animals exposed to lower pH levels which were obvious from the rate of mortality in a short term of exposure. The present study substantiates the role of biomarkers as an early warning of ocean acidification at a sub-lethal level.

Graphical Abstract

Highlights

  • Hypercapnia induces oxidative stress in animals exposed to low pH / high pCO2 conditions
  • Biomarkers are cost effective and sensitive tools to detect the sub-lethal impacts of ocean acidification
  • Low pH levels are highly lethal to sensitive crustaceans.

Keywords

Main Subjects

Andersson, A.J.; Mackenzie, F.T.; Lerman, A., (2005). Coastal ocean and carbonate systems in the high CO2 world of the Anthropocene. Am. J. Sci., 305(9): 875–918 (44 pages).

Andersson, A.J.; Gledhill, D., (2013). Ocean acidification and coral reefs: effects on breakdown, dissolution, and net ecosystem calcification. Ann. Rev. Mar. Sci., 5: 321-348 (28 pages).

Anthony, K.R.; Kline, D.I.; Diaz-Pulido, G.; Dove, S.; Hoegh-Guldberg, O., (2008). Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc. Natl. Acad. Sci., 105(45): 17442-17446 (5 pages).

Atkinson, M.J.; Cuet, P., (2008). Possible effects of ocean acidification on coral reef biogeochemistry: topics for research. Mar. Ecol. Prog. Serv., 373: 249-256 (8 pages).

Bacastow, R.O.; Keeling, C.D., (1973). Atmospheric carbon dioxide and radiocarbon in the natural carbon cycle: II. Changes from A.D. 1700 to 2070 as deduced from a geochemical model. In: Woodwell GM, Pecan EV (eds), Carbon and the biosphere. US Atomic Energy Commission,  Washington DC, 86-135 (50 pages).

Bandibas, M.;  Hilomen, V., (2016). Crab biodiversity under different management schemes of mangrove  cosystems. Global J. Environ. Sci. Manage., 2(1): 19-30 (12 pages).

Bebianno, M.J.; Company, R.; Serafim, A.; Camus, L.; Cosson, R.P.; Fiala-Médoni, A., (2005). Antioxidant systems and lipid peroxidation in Bathymodiolus azoricus from Mid-Atlantic Ridge hydrothermal vent fields. Aquat. Toxicol., 75(4): 354-373 (19 pages).

Broecker, W.S.; Li, Y.H.; Peng, T.H., (1971). Carbon dioxide- man’s unseen artifact. In: Hood DW (ed), Impingement of man on the oceans. John Wiley & Sons, New York, 287–324 (37 pages).

Browman, H.I.; Alain F.V.; Guldberg, O.H., (2008). Effects of Ocean Acidification on Marine Ecosystem. Mar. Ecol. Prog. Serv.., 373:199-201 (3 pages).

Cajaraville, M.P.; Bebianno, M.J.; Blasco, J.; Porte, C.; Sarasquete, C.; Viarengo, A., (2000). The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian Peninsula: a  practical approach. Sci. Total Environ., 247(2): 295-311 (16 pages).

Caldeira, K.; Wickett, M.E., (2003). Oceanography: anthropogenic carbon and ocean pH. Nature, 425(6956): 365 (1 page).

Caldeira, K.; Wickett, M.E., (2005). Ocean model predictions of chemistry changes from carbon dioxide  emissions to the atmosphere and ocean. J. Geophys. Res. C: Oceans, 110: (C09S04). 

Dailianis, S.; Domouhtsidou, G.P.; Raftopoulou, E.; Kaloyianni, M.; Dimitriadis, V.K., (2003).  Evaluation of neutral red retention assay, micronucleus test, acetylcholinesterase activity and a signal transduction molecule (cAMP) in tissues of Mytilus galloprovincialis (L.), in pollution monitoring. Mar. Environ. Res., 56(4): 443-470 (27 pages).

De'ath, G.; Lough, J.M.; Fabricius, K.E., (2009). Declining coral calcification on the Great Barrier Reef. Science, 323(5910): 116-119 (4 pages).

Delille, B.; Harlay, J.; Zondervan, I.; Jacquet, S.; Chou, L.; Wollast, R.; Bellerby R.G.J., Frankignoulle, M.; Borges, A.V.; Riebesell, U.; Gattuso, J.P., (2005). Response of primary production and calcification to changes of pCO2 during experimental blooms of the coccolithophorid Emiliania  huxleyi. Global Biogeochem. Cycles, 19(2).

Denman, K.L.; Brasseur, G.P.; Chidthaisong, A.; Ciais, P.; Cox, P.M.; Dickinson, R.E.; Hauglustaine,  D.A.; Heinze, C.; Holland, E.A.; Jacob, D.J.; Lohmann, U.; Ramachandram, S.;  da Silva Dias, P.L.;  Wofsy, S.C.;  Zhang X.,  (2007). Couplings between changes in the climate system and biogeochemistry. In: Climate change: The physical science basis (Eds.: Solomon, S.; Qin, D.; Manning, M.; Chen, Z.; Marquis, M.; Averyt, K.B.; Tignor, M.; Miller, H.L.) Contribution of working  group I to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press. 499-587 (88 pages).

Di Giulio, R. T.; Habig, C.; Gallagher, E. P., (1993). Effects of Black Rock Harbor sediments on indices  of biotransformation, oxidative stress, and DNA integrity in channel catfish. Aquat. Toxicol., 26(1): 1- 2 (22 pages).

Doyotte, A.; Cossu, C.; Jacquin, M.C.; Babut, M.; Vasseur, P., (1997). Antioxidant enzymes, glutathione and lipid peroxidation as relevant biomarkers of experimental or field exposure in the gills and the  digestive gland of the freshwater bivalve Unio tumidus. Aquat. Toxicol., 39(2): 93-110 (17 pages).

Dupont, S.; Havenhand, J.; Thorndyke, W.; Peck, L.;  Thorndyke, M., (2008). Near-future level of CO2- driven ocean acidification radically affects larval survival and development in the brittlestar  Ophiothrix fragilis. Mar. Ecol. Prog. Serv.., 373:285-294 (9 pages).

Ellman, G.L.; Courtney, K.D.; Andres, V.; Featherstone, R.M., (1961). A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol., 7(2): 88-95 (8 pages).

Erez, J.; Reynaud, S.; Silverman, J.; Schneider, K.; Allemand, D., (2011). Coral calcification under ocean acidification and global change. In Coral reefs: an ecosystem in transition (eds Dubinsky, Z., Stambler, N.,). Springer Netherlands. 151-176 (26 pages).

Escartin, E.; Porte, C., (1997). The use of cholinesterase and carboxylesterase activities from Mytilus galloprovincialis in pollution monitoring. Environ. Toxicol. Chem., 16(10): 2090-2095 (6 pages).

Fabry, V.J.; Seibel, B.A.; Feely, R.A.; Orr, J.C., (2008). Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J. Mar. Sci., 65(3): 414-432 (19 pages).

Fulton, M.H.; Key, P.B., (2001). Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorus insecticide exposure and effects. Environ. Toxicol. Chem., 20(1): 37-45 (9 pages).

Gattuso, J.P.; Lavigne, H., (2009). Technical note: approaches and software tools to investigate the  impact of ocean acidification. Biogeosci., 6(10): 2121-2133 (13 pages).

German Advisory Council on Global Change., (2006). The Future Oceans: Warming Up, Rising High, Turning Sour. Berlin.

Guinotte, J.M.; Fabry, V.J., (2008). Ocean acidification and its potential effects on marine ecosystems. Ann. N.Y. Acad. Sci. , 1134(1): 320-342 (23 pages).

Habig, W.H.; Pabst, M.J.; Jakoby, W.B., (1974). Glutathione S-transferases the first enzymatic step in mercapturic acid formation. J. Biol. Chem., 249(22): 7130-7139 (10 pages).

Hale, R.; Calosi, P.; McNeill, L.; Mieszkowska, N.; Widdicombe, S., (2011). Predicted levels of future  ocean acidification and temperature rise could alter community structure and biodiversity in marine  benthic communities. Oikos, 120(5): 661-674 (14 pages).

Kleypas, J.A.; Buddemeier, R.W.; Archer, D.; Gattuso, J.P.; Langdon, C.; Opdyke, B.N., (1999). Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science, 284(5411): 118-120 (3 pages).

Kurutaş, E.B.; Şahan, A.; Altun, T., (2009). Oxidative Stress Biomarkers in Liver and Gill Tissues of  Spotted Barb (Capoeta Barroisi Lortet, 1894) Living in Ceyhan River, Adana-Turkey. Turk. J. Biol., 33(4): 275-282 (8 pages).

Langer, G.; Geisen, M.; Baumann, K.H.; Kläs, J.; Riebesell, U.; Thoms, S.; Young, J.R., (2006). Species‐specific responses of calcifying algae to changing seawater carbonate chemistry. Geochem. Geophys. Geosyst., 7(9).

Linnaeus C., (1758). Systema Naturae per Regna Tria Naturae, Secundum Classes, Ordines, Genera, Species, cum Characteribus, Differentiis, Synonymis, Locis., 10:(1): 1-824 (824 pages).

Lowry, O.H.; Rosebrough, N.J.; Farr, A.L.; Randall, R.J., (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem., 193(1): 265-275 (11 pages).

Lueker, T.J.; Dickson, A.G.; Keeling, C.D., (2000). Ocean pCO2 calculated from dissolved inorganic carbon, alkalinity, and equations for K1 and K2: validation based on laboratory measurements of CO2 in gas and seawater at equilibrium. Mar. Chem., 70(1): 105-119 (15 pages).

McCulloch, M.; Falter, J.; Trotter, J.; Montagna, P., (2012). Coral resilience to ocean acidification and global warming through pH up-regulation. Nat. Clim. Change., 2(8): 623-627 (5 pages).

Melzner, F.; Gutowska, M.A.; Langenbuch, M.; Dupont, S.; Lucassen, M.; Thorndyke, M.C.; Bleich M.; Pörtner, H.O., (2009). Physiological basis for high CO2 tolerance in marine ectothermic animals: pre-  adaptation through lifestyle and ontogeny?. Biogeosci., 6(10): 2313-2331 (19 pages).

Mora, P.; Michel, X.; Narbonne, J.F., (1999). Cholinesterase activity as potential biomarker in two  bivalves. Environ. Toxicol. Pharmacol., 7(4): 253-260 (8 pages).

Moron, M.S.; Depierre, J.W.; Mannervik, B., (1979). Levels of glutathione, glutathione reductase and  glutathione S-transferase activities in rat lung and liver. Biochim. Biophys. Acta., 582(1): 67-78 (12 pages).

Mostafa, M.G.; Liu, C.Q.; Zhai, W.D.; Minella. M.; Vione, D.;  Gao, K.; Minakata, D.; Arakaki, T.; Yoshioka, T.; Hayakawa, K.; Konohira, E., (2016). Reviews and Syntheses: Ocean acidification and its potential impacts on marine ecosystems. Biogeosci., 13:1767-1786 (20 pages).

Nagarani, N.; Devi, V.J.; Kumaraguru, A.K., (2011). Mercuric chloride induced proteotoxicity and  structural destabilization in marine fish (Therapon jarbua). Toxicol. Environ. Chem., 93(2): 296-306   (11 pages).

Ohkawa, H.; Ohishi, N.; Yagi, K., (1979). Assay for lipid peroxides in animal tissues by thiobarbituric  acid reaction. Anal. Biochem., 95(2): 351-358 (8 pages).

Orr,  J.C.; Fabry, V.J.; Aumont, O.; Bopp, L.; Doney, S.C.; Feely, R.A.; Gnanadesikan, A.; Gruber, N.; Ishida, A.; Joos, F.; Key, R.M., (2005). Anthropogenic ocean acidification over the twenty-first century and its impacts on calcifying organisms. Nature., 437(7059): 681-686 (6 pages).

Pörtner, H. O., (2008). Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view. Mar. Ecol. Prog. Serv.., 373: 203-217 (15 pages).

Priya, R.J.; Muthusamy, A.; Maruthupandy, M., Beevi, A.H.; (2016). Biomarker response of ocean acidification induced hypercapnia on marine bivalve Donax cuneatus, Linnaeus 1758. J. Aquacult. Mar. Biol., 4(2): 00077 (8 pages).

Radenac, G.; Bocquene, D.; Fichet, P.; Miramand, G., (1998). Contamination of a dredged material  disposal site La Rochelle Bay, France. The use of the acetylcholinesterase activity of Mytilus edulis L. as a biomarker of pesticides: the need for a critical approach. Biomarkers, 3(4-5): 305-315 (11 pages).

Regoli, F.; Principato, G., (1995). Glutathione, glutathione-dependent and antioxidant enzymes in mussel, Mytilus galloprovincialis, exposed to metals under field and laboratory conditions: implications for the use of biochemical biomarkers. Aquat. Toxicol., 31(2): 143-164 (22 pages).

Regoli, F.; Winston, G.W.; Gorbi, S.; Frenzilli, G.; Nigro, M.; Corsi, I.; Focardi, S., (2003). Integrating  enzymatic responses to organic chemical exposure with total oxyradical absorbing capacity and DNA damage in the European eel Anguilla anguilla. Environ. Toxicol. Chem., 22(9): 2120-2129 (10 pages).

Ries, J. B.; Cohen, A. L.; McCorkle, D.C., (2009). Marine calcifiers exhibit mixed responses to CO2- induced ocean acidification. Geology, 37(12): 1131-1134 (4 pages).

River Watch Network. (1992). Total alkalinity and pH field and laboratory procedures. Based on University of Massachusetts Acid Rain Monitoring Project.

Rogelj, J.; Hare, B.; Nabel, J.; Macey, K.; Schaeffer, M.; Markmann, K.; Meinshausen, M., (2009). Halfway to Copenhagen, no way to 2 °C. Nature Reports Climate Change., 3: 81-83 (3 pages).

Royal Society., (2005). Ocean acidification due to increasing atmospheric carbon dioxide. Policy  Document 12/05, The Royal Society, London. Available at: www.royalsoc.ac.uk/ displaypagedoc.asp?id=13539. 1-68 (68 pages)

Saliu, J.K.; Bawa-Allah, K.A., (2012). Toxicological effects of lead and zinc on the antioxidant enzyme  activities of post juvenile Clarias gariepinus. Resour. Environ., 2(1): 21-26 (6 pages).

Sinha, A. K., (1972). Colorimetric assay of catalase. Anal. Biochem., 47(2): 389-394 (6 pages).

Stephensen, E.; Svavarsson, J.; Sturve, J.; Ericson, G.; Adolfsson-Erici, M.; Förlin, L., (2000). Biochemical indicators of pollution exposure in shorthorn sculpin (Myoxocephalus scorpius), caught in four harbours on the southwest coast of Iceland. Aquat. Toxicol., 48(4):431-442 (11 pages).

Türkay, M., (2001). Decapoda, In: Costello, M.J., (Ed.). European register of marine species: a check-list  of the marine species in Europe and a bibliography of guides to their identification. Patrim. Nat., 50: 284-292 (9 pages).

Venn, A.A.; Tambutté, E.; Holcomb, M.; Laurent, J.; Allemand, D.; Tambutté, S., (2013). Impact of  seawater acidification on pH at the tissue-skeleton interface and calcification in reef corals. Proc. Natl. Acad. Sci., 110(5): 1634-1639 (6 pages).

Vijayavel, K.; Gomathi, R.D.; Durgabhavani, K.; Balasubramanian, M.P., (2004). Sublethal effect of naphthalene on lipid peroxidation and antioxidant status in the edible marine crab Scylla serrata. Mar. Pollut. Bull., 48(5): 429-433 (5 pages).

Widdicombe, S.; Needham, H.R., (2007). Impact of CO2-induced seawater acidification on the burrowing activity of Nereis virens and sediment nutrient flux. Mar. Ecol. Prog. Ser., 341: 111-122 (12 pages).

Widdicombe, S.; Spicer, J.I., (2008). Predicting the impact of ocean acidification on benthic biodiversity:  what can animal physiology tell us?. J. Exp. Mar. Biol. Ecol., 366(1): 187-197 (11 pages).

 

HOW TO CITE THIS ARTICLE:

Jeevapriya, R.; Anand, M.; Maruthupandy, M.; Hameedha Beevi, A., (2017). Biomarker response of climate change-induced ocean acidification and hypercapnia studies on brachyurian crab Portunus pelagicus. Global J. Environ. Sci. Manage., 3(2): 165-176 (12 pages).


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