This study was conducted to investigate the effects of multiple stresses on physiological parameters in the hepatopancreas and hemolymph of a Pacific abalone, Haliotis discus hannai. The alteration of antioxidant enzymes including catalase (CAT), superoxide dismuatase (SOD) and immunological indicators such as phenoloxidase (PO), lysozyme activity and total hemocyte count (THC) were measured in a Pacific abalone exposed to nickel chloride solution of sublethal concentrations (200 and 400 μg/L) under higher thermal conditions (22 and 26℃) for 2 weeks. In this study, the hepatopancreas enzymes, CAT and SOD activity were significantly increased in the Pacific abalone exposed to NiCl2 compared to those of the control condition(18℃) at both 22 and 26℃. PO activity in the Pacific abalone exposed to NiCl2 also significantly increased at 26℃ thermal stress. But, THC decreased in the Pacific abalone exposed to NiCl2 at 26℃ (P < 0.05). Lysozyme activity was markedly elevated at 22℃ for 1 weeks and at 18℃ for 2 weeks after NiCl2 exposure. Our results showed that NiCl2 concentrations upper 200 μg/L were able to stimulate immune responses in Pacific abalones. Furthermore, complex stress, thermal stress, or NiCl2 can modify the immunological response and can lead to changes in the physiology of host-pollutant interactions in H. discus hannai. From these results, these biochemical parameters may represent a convenient indicator of monitoring heavy metal pollution in coastal areas.
Abele, D. and Puntarulo, S. (2004) Formation of reactive species and induction of antioxidant defense systems in polar and temperature marine invertebrates and fish. Comparative Biochemistry Physiology, 138(A):405-415.
Asokan, R., Arumugam, M. and Mullainadha, P. (1997)Activation of prophenoloxidase in the plasma and hemocytes of the marine mussel Perna viridis Linnaeus. Developmental and Comparative Immunology, 21: 1-12.
Blewett, T.A. and Leonard, E.M. (2017) Mechanisms of nickel toxicity to fish and invertebrates in marine and estuarine waters. Environmental Pollution, 223:311-322.
Blewett, T.A. and Wood, C.M. (2015a) Low salinity enhances Ni-mediated oxidative stress and sub-lethal toxicity to the green shore crab (Carcinus maenas). Ecotoxicology and Environmental Safety, 122:159-170.
Blewett, T.A., Glover, C.N., Fehsenfeld, S., Lawrence, M.J., Niyogi, S., Goss, G.G. and Wood, C.M. (2015b). Making sense of nickel accumulation and sub-lethal toxic effects in saline waters: Fate and effects of nickel in the green crab, Carcinus maenas. Aquatic Toxicology, 164: 23-33.
Cheng, T.C. (1981) Bivalves. In; Invertebrate blood cell (ed. by Ratcliffe, N.A., Rowley, A.F.), London Academic Press, London. pp. 233-299.
Cheng, W., Li, C.H. and Chen, J.C. (2004a) Effect of dissolved oxygen on the immune responses of Haliotis diversicolor supertexta and its susceptibility to Vibrio parahaemolyticus. Aquaculture, 232:103-115.
Cheng, W., Hsiao, I.S. and Chen, J.C. (2004b) Effect of nitrite on the immune response of Taiwan abalone Haliotis diversicolor supertexta and its susceptibility to Vibrio parahaemolyticus. Disease Aquatic Organism, 60: 157-64.
Cheng, W., Hsiao, I.S., Hsu, C.H. and Chen, J.C. (2004c)Change in water temperature on the immune response of Taiwan abalone Haliotis diversicolor supertexta and its susceptibility to Vibrio parahaemolyticus. Fish and Shellfish Immunology, 17: 235-243.
Cheng, W., and Chen, J.C. (2000) Effects of pH, salinity on immune parameters of the freshwater prawn Macrobrachium rosenbergii. Fish and Shellfish Immunology, 10: 387-391.
Chowdhury, M.J., Bucking, C., and Wood, C.M. (2008)Pre-exposure to waterborne nickel downregulations gastrointestinal nickel uptake in rainbow trout:indirect evidence for nickel essentiality. Environmental Science Technology, 42: 1359-1364.
Cong, R., Sun, W., Liu, G., Fan, T., Meng, X., Yang, L. and Zhu, L. (2005) Purification and characterization of phenoloxidase form clam Ruditapes philippinarum. Fish and Shellfish Immunology, 18: 61-70.
Elia, A.C., Dӧrr, A.J.M., Mastrangelo, C., Prearo, M. and Abete, M.C. (2006) Glutathione and antioxidant enzymes in the hepatophancreas of crayfish Procambarus clarkii (Girard, 1852) of Lake Transimeno (Italy). Bulletin français de la pêche et de la pisciculture, 380-381: 1351-1361.
Ferraris, M., Radice, S., Catalani, P., Francolini, M., Marabini, L. and Chiesara, E. (2002) Early oxidative damage in primary cultured trout hepatocytes: a time course study. Aquatic Toxicology, 59: 283-296.
Fried, G.H. and Levin, N.L. (1973) Enzymatic activity in hepatopancreas of Nassarius obsoletus. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, 45: 153-157.
González, A,L,, Martinez, M.A.N., Albores, F.V., Valle, F.A. and Mungaray, M.R. (2003) Phenoloxidase activity in larval and juvenile homogenates and adult plasma and haemocytes of bivalve mollusks. Fish and Shellfish Immunology, 15: 275-82.
Gopalarishnan, S., Thilagam, H., Huang, W.B. and Wang, K.J. (2009) Immunomodulation in the marine gastropod Haliotis diversicolor exposed to benzo(a)pyrene. Chemospere, 75(3): 389-397.
Gopalarishnan, S., Huang, W.B., Wang, Q.W., Wu, M.L., Liu, J. and Wang, K.J. (2011) Effects of tributyltin and benzo(a)pyrene on the immune-associated activities of hemocytes and recovery responses in the gastropod abalone, Haliotis diversicolor. Comparative Biochemistry and physiology Part C, 154(2): 120-128.
Halliwell, B. and Gutteridge, J.M. (1995) The definition and measurement of antioxidants in biological systems. Free Radical Biology and Medicine, 18:125-126.
Heise, K., Puntarulo, S., Portner, H.O. and Abele D. (2003) Production of reactive oxygen species by isolated mitochondria of the Antarctic bivalve Laternula elliptica (King and Broderip) under heat stress. Comparative Biochemistry Physiology, 134(C):79-90.
Hu, G.F., Li, Z., Liang, H.W., Wang, C.Z., Wu, Q.C., Luo, X.Z. and Zou, G.W. (2009) Effects of cadmium on SOD and CAT in hepatopancreas, antennary gland and gill of Procambarus clarkii. Journal of Agro-Environment Science, 28: 1806-1811.
Hutchinson, T.M. and Manning, M.J. (1996) Seasonal trends in serum lysozyme activity and total protein concentration in dab (Limanda limanda L.) sampled from Lyme Bay, U.K.. Fish Shellfish Immunology, 6:473-482.
Hwang, I.D., Ki, N.S., Lee, J.S. and Lee, S.K. (1989)Effects of Nickel compounds on sister chromatid exchanges and chromosome aberrations in human cultured lymphocytes. The Korean Journal of Occupied Medicine, 1(1): 46-51.
IPCC. (2007) Climate change. 2007. The physical Science Basis. Combride University Press, Cambride, USA.
Johnson, J.K., Rocheleau, T.A., Hillyer, J.F., Chen, C.C., Li, J. and Christernsen, B.M. (2003) A progenital role for phenylalanine hydroxylase in mosquito immune response. Inspection Biochemistry Molecular Biology, 33: 345.354.
Jwa, M.S., Kang, K.P., Choe, M.K. and Yeo, I.K. (2009)Effects of low salinity stresses on the physiology of disc abalone, Haliotis discus discus. Journal of Fish Pathology, 22: 293-303.
Kang, S.W., Lee, J.B. and Lee, J.S. (2003) Morphology and histology of the digestive tract of the Abalone, Haliotis dicsus hannai (Gastropoda: Haliotidae). Korean Journal of Malacology, 19(2): 81-87.
Kasprzak, K.S. (1995) Possible role of oxidative damage in metal induced carcinogenesis. Cancer Investigation, 13: 411-430.
Kim, T.H., Kim, K.J., Choe, M.K. and Yeo, I.K. (2006)Physiological changes of juvenile abalone, Haliotis sieboldii exposed to acute water temperature stress. Journal of Aquaculture, 19: 77-83.
Kim, K.Y., Lee, S.Y., Cho, Y.S., Bang, C., Kim, K.H., Kim, D.S. and Nam, Y.K. (2007) Molecular characterization and mRNA expression during metal exposure and thermal stress of copper/zinc- and managanese superoxide dismutase in disk abalone, Haliotis discus discus. Fish Shellfish of Immunology, 23(5): 1043-1059.
Kim, D.W. (2014) Effect on bentic foraminifera of organic pollution in the abalone aquaculture. Master Thesis of Chonnam National University. pp. 66.
Kim, S.J., Kim, K.M., Kang, S.Y. and Lee, J.S. (2015)Oxidative stress response of the Abalone Haliotis discus hannai acute exposed to Nickel Chloride (NiCl2). Korean Journal of Malacology, 31(4):285-290.
Kubrak, O.I., Poigner, H., Husak, V.V., Rovenko, B.M., Meyer, S., Abele, D., Lushchak, V.I. (2014) Glodfish brain and heart are well protected from Ni2+-induced oxidative stress. Comparative Biochemistry and Physiology, 162(C): 43-50.
Kwon, T.K. and Yoo, Y.J. (2010) Structural analysis of thermostable enzymes. Korean Journal of Chemical Engineering, 6(1): 1185.
Leonard, E.M., Marentette, J.R., Balshine, S. and Wood, C.M. (2014) Critical body residues, Michaelis-Menten analysis of bioaccumulation, lethality and behaviour as endpoints of waterborne Ni toxicity in two teleost. Aquatic Toxicology, 23: 147-162.
Liu, H., Zhang, J.F., Shen, H., Wang, X.R. and Wang, W.M. (2005) Impact of copper and Its EDTA complex on the glutathione-dependent antioxidant system in freshwater fish (Carassius auratus). Bulletin of Environmental Contamination and Toxicology, 74:1111–1117.
Lopes, P.A., Pinheiro, T., Santos, M.C., da Luz Mathias, M., Collares-Pereira, M.J. and Viegas-Crespo, A.M. (2001) Response of antioxidant enzymes in freshwater fish population (Leuciscus alburnoides complex) to inorganic pollutants exposure. Science of the Total Environment, 280: 153-163.
Martello, L. and Tjeerdema, R.S. (2001) Combined effects of pentachorophenol and salinity stress on chemiluminescence activity in two species of abalone. Aquatic Toxicology, 51: 351-362.
Mattzzo, V., Ballarin, L. and Marine, M.G. (2002) In vitro effects of tributyltin on functional responses of haemocytes in the clam Tapes philippinarum. Applied Organometallic Chemistry, 16: 169-74.
Mok, J.S., Lee, K.J., Shim, K.B., Lee, T.S., Song, K.C. and Kim, J.H. (2010) Contents of heavy metals in marine invertebrates from the Korean coast. Journal of the Korean Society of Food Science and Nutrition, 39: 894-901.
Moody, C.S. and Hassan, H.M. (1982) Mutagenicity of oxygen free radicals. Proceedings of the National Academy Sciences, 79: 2855-2859.
Nappi, A.J., Vass, E., Frey, F. and Carton, Y. (1995)Superoxide anion generation in Drosophila during melanotic encapsulation of parasites. European Journal of Cell Biology, 68: 450-456.
Nebot, C., Moutet, M., Huet, P., Xu, J.Z., Yadan, J.C. and Chaudiere, J. (1993) Spectrophotometric assay of superoxide dismutase activity based on the activated autoxidation of a tetracyclic catechol. Analytical Biochemistry, 214: 442-451.
Pane, E.F., Haque, A. and Wood. C.M. (2004)Mechanistic analysis of acute, Ni-induced respiratory toxicity in the rainbow trout (Oncorhynchus mykiss):an exclusively branchial phenomenon. Aquatic Toxicology, 69: 11-24.
Parihar, M.S., Javeri, T., Hemnani, T., Dubey, A.K. and Parkash, P. (1997) Responses of superoxide dismutase, glutathione peroxidase and reduced glutathione antioxidant defenses in gills of the freshwater catfish (Heteropneustes fossilis) to short-term elevated temperature. Journal of Thermal Biology, 22: 151-156.
Park, C.J., Min, B.H., Kim, K.S., Lee, J.W., Lee, J.H., Noh, J.K., Kim, H.C., Park, J.W. and Myeong, J.I. (2011) Physiological responses on low water temperature stress of Pacific abalone, Haliotis discus hannai. Korean Journal of Malacology, 27: 317-322.
Park, H.J. and Kang, J.C. (2012) Biochemical changes in the hemolymph and hepatopancreas of abalone Haliotis discus hannai exposed to copper. Korean Journal of Fisheries and Aquatic Sciences, 45:154-160.
Park, H.S. and Park, K.S. (2004) Nickel toxicity and carcinogenicity. Journal of Environmental Toxicology, 19(2): 119-134.
Pipe, R.K., Coles, J.A., Carissan, F.M.M. and Ramanathan, K. (1999) Copper induced immunomodulation in the marine mussel, Mytilus edulis. Aquatic Toxicology, 46:43-54.
Power, A. and Sheehan, D. (1996) Seasonal variation in the antioxidant defense of gill and digestive gland of the blue mussel, Mytilis edulis. Comparative Biochemistry Physiology, 114(C): 99-103.
Pyle, G. and Couture, P. (2012) Nickel. In; Wood, C.M., Farrell, A.P., Brauner, C.J.(Eds.), Homeostasis and Toxicology of Essential Metals, Fish Physiology, Vol. 31(A). Academic Press, London.
Ragsdale, S.W. (1998) Nickel biochemistry. Current Opinion in Chemical Biology, 2: 208-215.
Seong, K.T., Hwan, D.W., Han, I.S., Go, W.J., Suh, Y.S. and Lee, J.Y. (2010) Characteristic for long-term trends of temperature in the Koreans waters. Journal of Korea Society Marine Environment, 16(4):353-360.
Smith, V.J. and Chisholm, J.R.S. (1992) Non-cellular immnunity in crustaceans. Fish and Shellfish Immunology, 2: 1-31.
Soderhall, K. and Cerenius, J.M. (1996) The prophenoloxidase activating system in invertebrates. In; Soderhall, K., Iwanaga, S., Vasta, G.R., editors. New Directions in Invertebrate Immunity. Fairhaven, N.J.: SOS Publications.
Stohs, S.J., Bagchi, D., Hassoun, E. and Bagchi, M. (2000) Oxidative mechanism in the toxicity of chromium and cadmium ions. Journal of environmental Pathology Toxicology and Oncology, 19: 201-213.
Sugiyama, M. (1994) Role of cellular antioxidant in metal-induced damage. Cell Biology and Toxicology, 10: 1-22.
Szefer, P. (2002) Trace metals in the environment. 5. Metals, metalloids and radionuclides in the Baltic Sea ecosystem; Elsevier: London, pp. 699-703.
Vijayavel, K., Anbuselvam, C. and Balasubramanian, M.P. (2005) Naphthalene-induced hematological distrubances and oxidative stress in an estuarine edible crab, Scylla serrata. Environmental Toxicology, 20: 464-466.
Vijayavel, K., Gopalakrishnan, S., Thiagarajan, R. and Thilagam, H. (2009) Immunotoxic effects of nickel in the mud crab, Scylla serrata. Fish and Shellfish Immunology, 26: 133-139.
Wang, W., Mai, K., Zhang, W., Ai, Q., Yao, C., Li, H. and Liufu, Z. (2009) Effects of dietary copper on survival, growth and immune response of juvenile abalone, Haliotis discus hannai Ino. Aquaculture, 297: 122-127.
Wendel, A. and Feuerstein, S. (1981) Drug-induced lipid peroxidation in mice—I Modulation by monooxegenase activity, glutathione and selenium status. Biochemical Pharmacology, 30: 2513-2520.
Youm, J.H., Oh, G.J. and Yoo, Y.C. (2001) Role of Nitric oxide in the nickel and cobalt induced cytotoxicity in RAW 264.7. Korean Journal of Environmental Medicine, 13(3): 274-285.
Yue, F., Pan, L., Xie, P., Zheng, D. and Li, J. (2010)Immune responses and expression of immune-related genes in swimming crab Portunus trituberculatus exposed to elevated ambient ammonia-N stress. Comparative Biochemistry Physiology, 157(A):246-251.
Zhou, J., Cai, Z.H., Zhu, X.S., Li, L. and Gao, Y.F. (2010) Innate immune parameters and haemolymph protein expression profile to evaluate the immunotoxicity of tributyltin on abalone (Haliotis diversicolor supertexa). Development Comparative Immunology, 34: 1059-1067.
KFIC (2016) 한국해양수산개발원. 해외시장분석센터 해외시장심층분석. 중국 전복 시장 동향, 1: 1-69.
KMI (2016) 한국해양수산개발원. FTA 이행에 따른 어입인등지원센터. 중국 수산 동향, 9: 1-38.
농림수산식품부 (2011) 한국해양수산개발원. 기후변화에 대한 수산업의 정책적 대응전략 수립을 위한 연구보고서, 1-51.
