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Effects of waterborne Cu and Cd on anti-oxidative response, lipid peroxidation and heavy metals accumulation in abalone Haliotis discus hannai ino

Abstract

The aim of this study was to compare the effects of waterborne copper (Cu) and cadmium (Cd) on survival, anti-oxidative response, lipid peroxidation and metal accumulation in abalone Haliotis discus hannai. Experimental animals (initial weight: 7.49 g ± 0.01 g) were exposed to graded concentrations of waterborne Cu (0.02, 0.04, 0.06, 0.08 mg L−1) or Cd (0.025, 0.05, 0.25, 0.5 mg L−1) for 28 days, respectively. Activities of the anti-oxidative enzymes (catalase, CAT; superoxide dismutase, SOD; glutathione peroxidases, GPx; glutathione S-transferase, GST), contents of the reduced glutathione (GSH) and malondiadehyde (MDA) in the hepatopancreas, and metal accumulation in hepatopancreas and muscles were analyzed after 0, 1, 3, 6, 10, 15, 21, 28 days of metal exposure, respectively. Results showed that 0.04 mg L−1, 0.06 mg L-−1 and 0.08 mg L−1 Cu caused 100% death of abalone on the 21st, 10th and 6th day, respectively. However, no dead abalone was found during the 28-day waterborne Cd exposure at all experimental concentrations. Generally, activities of SOD and GST in hepatopancreas under all Cu concentrations followed a decrease trend as the exposure time prolonged. However, these activities were firstly increased and then decreased to the control level and increased again during Cd exposure. Activities of CAT in all Cu exposure treatments were higher than those in the control. These activities were firstly increased and then decreased to the control level and increased again during Cd exposure. Contents of MDA in hepatopancreas in all Cu treatments significantly increased first and then decreased to the control level. However, the MDA contents in hepatopancreas were not significantly changed during the 28-day Cd exposure. The metals accumulation in both hepatopancreas and muscles of abalone significantly increased with the increase of waterborne metals concentration and exposure time. These results indicated that H. discus hannai has a positive anti-oxidative defense against Cu or Cd. In conclusion, anti-oxidative mechanism in abalone to resist waterborne Cu did not follow the same pattern as that for waterborne Cd.

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References

  • Almeida, E. A., Miyamoto, S., Bainy, A. C. D., Medeiros, M. H., and Mascio, P., 2004. Protective effect of phospholipid hydroperoxide glutathione peroxidase (PHGPx) against lipid peroxidation in mussels Pernaperna exposed to different metals. Marine Pollution Bulletin, 49: 386–392.

    Article  Google Scholar 

  • Almeida, J. A., Diniz, Y. S., Marques, S. F. G., Faine, L. A., Ribas, B. O., Burneiko, R. C., and Novelli, E. L. B., 2002. The use of the oxidative stress responses as biomarkers in Nile tilapia (Oreochromis niloticus) exposed to in vivo Cd contamination. Environment International, 27: 673–679.

    Article  Google Scholar 

  • Al-Subiai, S. N., Jha, A. N., and Moody, A. J., 2009. Contamination of bivalve haemolymph samples by adductor muscle components: Implications for biomarker studies. Ecotoxicology, 18: 334–342.

    Article  Google Scholar 

  • Anderson, M. E., 1985. Determination of glutathione and glutathione disulfide in biological samples. Methods in Enzymology, 113: 548–555.

    Article  Google Scholar 

  • Asagba, S. O., Eriyamremu, G. E., and Igberaese, M. E., 2008. Bioaccumulation of cadmium and its biochemical effect on selected tissues of the catfish (Clarias gariepinus). Fish Physiology and Biochemistry, 34: 61–69.

    Article  Google Scholar 

  • Bagchi, D., Bacghi, M., Hassoun, E. A., and Stohs, S. J., 1996. Cadmium induced excretion of urinary lipid metabolites, DNA damage, glutathione depletion and hepatic lipid peroxidation in Sprague-Dawley rats. Biological Trace Element Research, 52: 143–154.

    Article  Google Scholar 

  • Basha, P. S., and Rani, A. U., 2003. Cadmium-induced antioxidant defense mechanismin freshwater teleost Oreochromis mossambicus (Tilapia). Ecotoxicology Environmental Safety, 56: 218–221.

    Article  Google Scholar 

  • Bopp, S. F., Abicht, H. K., and Knauer, K., 2008. Copper-induced oxidative stress in rainbow trout gill cells. Aquatic Toxicology, 86: 197–204.

    Article  Google Scholar 

  • Bouraoui, Z., Banni, M., Ghedira, J., Clerandeau, C., Guerbej, H., Narbonne, J. F., and Boussetta, H., 2008. Acute effects of cadmium on liver phase I and phase II enzymes and metallothionein accumulation on sea bream Sparusaurata. Fish Physiology Biochemistry, 34: 201–207.

    Article  Google Scholar 

  • Bradford, M. M., 1976. A rapid method for the quantification of microgram quantities of proteins utilizing the principle of protein-dye binding. Analytical Biochemistry, 72: 248–254.

    Article  Google Scholar 

  • Cao, L., Huang, W., Liu, J., Yin, X., and Dou, S., 2010. Accumulation and oxidative stress biomarkers in Japanese flounder larvae and juveniles under chronic cadmium exposure. Comparative Biochemistry Physiology (C), 151: 386–392.

    Google Scholar 

  • Chandran, R., Sivakumar, A. A., Mohandass, S., and Aruchami, M., 2005. Effect of cadmium and zinc on antioxidant enzyme activity in the gastropod Achatina fulica. Comparative Biochemistry Physiology (C), 140: 422–426.

    Google Scholar 

  • Chelomin, V. P., and Belcheva, N. N., 1991. Alterations of microsomal lipid synthesis in gill cells of bivalve mollusk Mizuhopecten yessoensisin response to cadmium accumulation. Comparative Biochemistry Physiology (C), 99: 1–5.

    Article  Google Scholar 

  • Chelomin, V. P., and Belcheva, N. N., 1992. The effect of heavy metals on processes of lipid peroxidation in microsomal membranes from the hepatopancreas of bivalve mollusk Mizuhopectin yessoensis. Comparative Biochemistry Physiology (C), 103: 419–422.

    Google Scholar 

  • Chen, J. L., Liu, W. X., Liu, S. Z., Lin, X. M., and Tao, S., 2004. An evaluation on heavy metal contamination in the surface sediments in Bohai Sea. Marine Sciences, 28: 16–21.

    Google Scholar 

  • Cheung, C. C. C., Zheng, G. J., Lam, P. K. S., and Richardson, B. J., 2002. Relationships between tissue concentrations of chlorinated hydrocarbons (polychlorinated biphenyls and chlorinated pesticides) and antioxidative responses of marine mussels, Perna viridis. Marine Pollution Bulletin, 45: 181–191.

    Article  Google Scholar 

  • Company, R., Serafim, A., Bebianno, M. J., Cosson, R., Shillito, B., and Fiala-Médioni, A., 2004. Effect of cadmium, copper and mercury on antioxidant enzyme activities and lipid peroxidation in the gills of the hydrothermal vent mussel Bathymodiolus azoricus. Marine Environmental Research, 58: 377–381.

    Article  Google Scholar 

  • Cunha, I., Mangas-Ramirez, E., and Guilhermino, L., 2007. Effects of copper and cadmium on cholinesterase and glutathione S-transferase activities of two marine gastropods (Monodonta lineata and Nucella lapillus). Comparative Biochemistry Physiology (C), 145: 648–657.

    Google Scholar 

  • Dautrememepuits, C., Betoulle, S., and Vernet, G., 2002. Antioxidant response modulated by copper in healthy and parasitized carp (Cyprinus carpio L.) by Ptychobothrium sp. (Cestoda). Biochimica et Biophysica Acta, 1573: 4–8.

    Article  Google Scholar 

  • De la Torre, F. R., Salibián, A., and Ferrari, L., 2000. Biomarkers assessment in juvenile Cyprinus carpio exposed to waterborne cadmium. Environmental Pollution, 109: 277–282.

    Article  Google Scholar 

  • Devi, V. U., 1997. Heavy metal toxicity to an intertidal gastropod Morula granulata (Duclos): Tolerance to copper, mercury, cadmium and zinc. Journal Environment Biology, 18: 287–290.

    Google Scholar 

  • Fernández, B., Campillo, J. A., Martínez-Gómez, C., and Benedicto, J., 2010. Antioxidant responses in gills of mussel (Mytilus galloprovincialis) as biomarkers of environmental stress along the Spanish Mediterranean coast. Aquatic Toxicology, 99: 186–197

    Article  Google Scholar 

  • Firat, O., Cogun, H. Y., Aslanyavrusu, S., and Kargin, F., 2009. Antioxidant responses and metal accumulation in tissues of Nile tilapia Oreochromis niloticus under Zn, Cd and Zn+Cd exposures. Journal of Applied Toxicology, 29: 295–301.

    Article  Google Scholar 

  • Franco, R., Sanchez-Olea, R., Reyes-Reyes, E. M., and Panayiotidis, M. I., 2009. Environmental toxicity, oxidative stress and apoptosis: Ménage à trois. Mutation Research, 674: 3–22.

    Article  Google Scholar 

  • Giguere, A., Peter, G. C., Campbell, L. H., and Cosu-Leguille, C., 2005. Metal bioaccumulation and oxidative stress in yellow perch (Perca flavescens) collected from eight lakes along a metal contamination gradient (Cd, Cu, Zn, Ni). Canadian Journal Fisheries and Aquatic Sciences, 62: 563–577.

    Article  Google Scholar 

  • Goering, P. I., Waalkes, M. P., and Klassen, C. D., 1995. Toxicology of cadmium. In: Toxicology of Metal Biochemical Aspects: Handbook of Experimental Pharmacology. Goyer, R. A., and Cherian, M. G., eds., Springer-Verlag, New York, 189–213.

    Chapter  Google Scholar 

  • Gorski, J., and Nugegoda, D., 2006. Toxicity of trace metals to juvenile abalone, Haliotis rubra following short-term exposure. Bulletin Environmental Contamination and Toxicology, 77: 732–740.

    Article  Google Scholar 

  • Goth, L., 1991. A simple method for determination of serum catalase activity and revision of reference range. Clinica Chimica Acta, 196: 143–151.

    Article  Google Scholar 

  • Habig, W. H., Pabst, M. J., and Jakoby, W. B., 1974. Glutathione S-transferases. The first step in mercapturic acid formation. The Journal of Biological Chemistry, 249: 7130–7139.

    Google Scholar 

  • Halliwell, B., and Gutteridge, M. C., 1984. Oxygen toxicity, oxygen radicals, transition metals and disease. Biochemical Journal, 219: 1–14.

    Google Scholar 

  • Handy, R. D., 2003. Chronic effects of copper exposure versus endocrine toxicity: Two sides of the same toxicological process? Comparative Biochemistry Physiology (A), 135: 25–38.

    Article  Google Scholar 

  • Huang, X., Guo, F., Ke, C., and Wang, W. X., 2010. Responses of abalone Haliotis diversicolor to sublethal exposure of waterborne and dietary silver and cadmium. Ecotoxicology and Environmental Safety, 73: 1130–1137.

    Article  Google Scholar 

  • Huang, X. X., Zhou, H. Q., and Zhang, H., 2006. The effect of Sargassum fusiforme polysaccharide extracts on vibriosis resistance and immune activity of the shrimp Fenneropenaeus chinensis. Fish and Shellfish Immunology, 20: 750–757.

    Article  Google Scholar 

  • Jiang, W. D., Wu, P., Kuang, S. Y., Liu, Y., Jiang, J., Hu, K., Li, S. H., Tang, L., Feng, L., and Zhou, X. Q., 2011. Myo-inositol prevents copper-induced oxidative damage and changes in antioxidant capacity in various organs and the enterocytes of juvenile Jian carp (Cyprinus carpio var. Jian). Aquatic Toxicology, 105: 543–551.

    Article  Google Scholar 

  • Jorge, M. B., Loro, V. L., Bianchini, A., Wood, C. M., and Gillis, P. L., 2013. Mortality, bioaccumulation and physiological responses in juvenile freshwater mussels (Lampsilis siliquoidea) chronically exposed to copper. Aquatic Toxicology, 126: 137–147.

    Article  Google Scholar 

  • Kaland, T., Andersen, T., and Hylland, K., 1992. Accumulation and subcellular distribution of metals in the marine gastropod Nassarius reticulates L. In: Ecotoxicology of Metals in Invertebrates. Dallinger, R., and Rainbow, P. S., eds., Lewis, London, 37–53.

    Google Scholar 

  • Kappus, H., 1985. Lipid peroxidation: Mechanisms, analysis, enzymology and biological relevance. In: Oxidative Stress. Sies, H., ed., Academic Press, London, 273–310.

    Chapter  Google Scholar 

  • Langston, W. J., Bebianno, M. J., and Burt, G. R., 1998. Metal handling strategies in molluscs. In: Metal Metabolism in Aquatic Environments. Langston, W. J., and Bebianno, M. J., eds., Chapman and Hall, London, 219–283.

    Chapter  Google Scholar 

  • Li, L. J., Zhang, F., and Liu, X. M., 2005. Oxidative stress related enzymes in response to chromium (VI) toxicity in Oxya chinensis (Orthoptera: Acridoidae). Journal of Environmental Science (China), 17: 823–826.

    Google Scholar 

  • Maria, V. L., and Bebianno, M. J., 2011. Antioxidant and lipid peroxidation responses in Mytilus gallopro vincialis exposed to mixtures of benzo (a) pyrene and copper. Comparative Biochemistry and Physiology (C), 154: 56–63.

    Google Scholar 

  • Marr, J. C. A., Lipton, J., Cacela, D., Hansen, J. A., Bergman, H. L., Meyer, J. S., and Hogstrand, C., 1996. Relationship between copper exposure duration, tissue copper concentration, and rainbow trout growth. Aquatic Toxicology, 36: 17–30.

    Article  Google Scholar 

  • Mazon, A. F., Nolan, D. T., Lock, R. A. C., Fernandes, M. N., and Wendelaar Bonga, S. E., 2004. A short-term in vitro gill culture system to study the effects of toxic (copper) and non-toxic (cortisol) stressors on the rainbow trout, Oncorhynchus mykiss (Walbaum). Toxicology in Vitro, 18: 691–701.

    Article  Google Scholar 

  • McGeer, J. C., Szebedinszky, C., McDonald, D. G., and Wood, C. M., 2000. Effects of sublethal exposure to waterborne Cu, Cd or Zn in rainbow trout 1: Ionoregulatory disturbance and metabolic costs. Aquatic Toxicology, 50: 231–243.

    Article  Google Scholar 

  • Meng, W., Qin, Y. W., Zheng, B. H., and Zhang, L., 2008. Heavy metal pollution in Tianjin Bohai Bay, China. Journal of Environmental Sciences, 20: 814–819.

    Article  Google Scholar 

  • Mosleh, Y. Y., Paris-Palacios, S., and Biagianti-Risbourg, S., 2005. Metallothioneins induction and antioxidative response in aquatic worms Tubifex tubifex (Oligochaeta, tubificiadae) exposed to copper. Chemosphere, 64: 121–128.

    Article  Google Scholar 

  • Ohkawa, H., Ohish, I. N., and Yagi, K., 1979. Assay for lipid peroxidation in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry, 95: 351–363.

    Article  Google Scholar 

  • Palace, V. P., and Klaverkamp, J. F., 1993. Variation of hepatic enzymes in three species of freshwater fish from Precambrian shield lakes and the effect of cadmium exposure. Comparative Biochemistry and Physiology (C), 104: 147–154.

    Article  Google Scholar 

  • Reddy, P. S., 1997. Modulations in antioxidant enzymes in the gill and hepatopancreas of the edible crab Scylla serrata during exposure to cadmium and copper. Fresenius Environmental Bulletin, 6: 589–597.

    Google Scholar 

  • Reddy, P. S., and Bhagyalakshmi, A., 1994. Lipid peroxidation in the gill and hepatopancreas of Oziotelphusa senex senex fabricius during cadmium and copper exposure. Bulletin of Environmental Contamination and Toxicology, 53: 704–710.

    Google Scholar 

  • Reméo, D., Bennani, N., Gnassia-Barelli, M., Lafaurie, M., and Girard, J. P., 2000. Cadmium and copper display different responses towards oxidative stress in the kidney of the sea bass Dicentrarchus labrax. Aquatic Toxicology, 48: 185–194.

    Article  Google Scholar 

  • Ruas, C. B. G., Carvalho, C. S., de Araujo, H. S. S., Espindola, E. L. G., and Fernandes, M. N., 2008. Oxidative stress biomarkers of exposure in the blood of cichlid species from a metal-contaminated river. Ecotoxicology and Environmental Safety, 71: 86–93.

    Article  Google Scholar 

  • Sahin, M., Sagdiç, G., Elmas, O., Akpinar, D., Derin, N., Aslan, M., Agar, A., Alicigüzel, Y., and Yargiçoglu, P., 2007. Effect of chronic restraint stress and alpha-lipoic acid on lipid peroxidation and antioxidant enzyme activities in rat peripheral organs. Pharmacological Research, 54: 247–252.

    Article  Google Scholar 

  • Scalbert, A., Johnson, I. T., and Saltmarsh, M., 2005. Polyphenols: Antioxidants and beyond. American Journal of Clinical Nutrition, 81: 215S–217S.

    Google Scholar 

  • Sies, H., 1985. Oxidative stress: Introductory remarks. In: Oxidative Stress. Sies, H., ed., Academic Press, San Diego, 1–8.

    Chapter  Google Scholar 

  • Sies, H., 1999. Glutathione and its role in cellular functions. Free Radical Biology and Medicine, 27: 916–921.

    Article  Google Scholar 

  • Sörensen, E. M., 1991. Metal Poisoning in Fish. CRC Press, Boston, 384pp.

    Google Scholar 

  • Stohs, S. J., Bagchi, D., Hassoun, E., and Bagchi, M., 2000. Oxidative mechanisms in the toxicity of chromium and cadmium ions. Journal of Environmental Pathology, Toxicology and Oncology, 19: 201–213.

    Google Scholar 

  • Tamás, L., Valentovicová, K., Halusková, L., Huttová, J., and Mistrík, I., 2009. Effect of cadmium on the distribution ofhydroxyl radical, superoxide and hydrogen peroxide in barley root tip. Protoplasma, 236: 67–72.

    Article  Google Scholar 

  • Thomas, P., and Juedes, M. J., 1992. Influence of lead on the glutathione status of Atalantic croaker tissues. Aquatic Toxicology, 23: 11–30.

    Article  Google Scholar 

  • Thomas, P., and Wofford, H. W., 1984. Effects of metals and organic compounds on hepatic glutathione, cysteine, and acid soluble thiol levels in mullet (Mugil cephalus L.). Toxicology and Applied Pharmacology, 76: 172–182.

    Article  Google Scholar 

  • Thomas, P., and Wofford, H. W., 1993. Effects of cadmium and Aroclor 1254 on lipid peroxidation, glutathione peroxidase activity, and selected antioxidants in Atlantic croaker tissues. Aquatic Toxicology, 27: 159–178.

    Article  Google Scholar 

  • Thomas, P. T., Wofford, H. W., and Neff, J. M., 1982. Effect of cadmium on glutathione content of mullet (Mugil cephalus) tissues. In: Physiological Mechanisms of Marine Pollutant Toxicity. Vernberg, W. B., et al., eds., Academic Press, New York, 109–125.

    Chapter  Google Scholar 

  • Tort, L., Kargacin, B., Torres, P., Giralt, M., and Hidalgo, J., 1996. The effect of cadmium exposure and stress on plasm cortisol, metallothionein levels and oxidative status in rainbow trout (–) liver. Comparative Biochemistry and Physiology (C), 114: 29–34.

    Google Scholar 

  • Tsai, J. W., Chou, Y. H., Chen, B. C., Liang, H. M., and Liao, C. M., 2004. Growth toxicity bioassays of abalone Haliotis diversicolor supertexta exposed to waterborne zinc. Bulletin of Environmental Contamination and Toxicology, 72: 70–77.

    Article  Google Scholar 

  • Upadhyay, R., and Panda, S. K., 2010. Zinc reduces copper toxicity induced oxidative stress by promoting antioxidant defense in freshly grown aquatic duckweed Spirodela polyrhiza L. Journal of Hazardous Materials, 175: 1081–1084.

    Article  Google Scholar 

  • Verlecar, X. N., Jena, K. B., and Chainy, G. B. N., 2008. Modulation of antioxidant defences in digestive gland of Perna viridis (L.), on mercury exposures. Chemosphere, 71: 1977–1985.

    Article  Google Scholar 

  • Viarengo, A., Canesi, L., Pertica, M., Poli, G., Moore, M. N., and Orunesu, M., 1990. Heavy metal effect on lipid peroxidation in the tissues of Mytilus galloprovincialis. Comparative Biochemistry and Physiology (C), 97: 37–42.

    Google Scholar 

  • Vieira, L. R., Gravato, C., Soares, A. M. V. M., Morgado, F., and Guilhermino, L., 2009. Acute effects of copper and mercury on the estuarine fish Pomatoschistus microps: Linking biomarkers to behavior. Chemosphere, 76: 1416–1427.

    Article  Google Scholar 

  • Vincent, R., Boudreau, J., Nadeau, D., Fournier, M., Krrzystyniak, K., Trottier, B., and Chevalier, G., 1989. Lipid peroxidation in rat lungs following an acute inhalation exposure to cadmium chloride. Journal Aerosol Medicine, 2: 349–356.

    Article  Google Scholar 

  • Wang, G. D., Liu, B. Z., Tang, B. J., Zhang, T., and Xiang, J. H., 2006. Pharmacological and immunocytochemical investigation of the role of catecholamineson larval metamorphosis by beta-adrenergic-like receptor in the bivalve Meretrix meretrix. Aquaculture, 258: 611–618.

    Article  Google Scholar 

  • Wang, N., Ingersoll, C. G., Greer, I. E., Hardesty, D. K., Ivey, C. D., Kunz, J. L., Brumbaugh, W. G., Dwyer, F. J., Roberts, A. D., Augspurger, T., Kane, C. M., Neves, R. J., and Barnhart, M. C., 2007a. Chronic toxicity testing of copper and ammonia to juvenile freshwater mussels (Unionidae). Environmental Toxicology and Chemistry, 26: 2048–2056.

    Article  Google Scholar 

  • Wang, N., Ingersoll, C. G., Hardesty, D. K., Ivey, C. D., Kunz, J. L., May, T. W., Dwyer, F. J., Roberts, A. D., Augspurger, T., Kane, C. M., Neves, R. J., and Barnhart, M. C., 2007b. Acute toxicity f copper, ammonia, and chlorine to glochidia and juveniles of freshwater mussels (Unionidae). Environmental Toxicology and Chemistry, 26: 2036–2047.

    Article  Google Scholar 

  • Warner, H. R., 1994. Superoxide dismutase, aging and degenerative disease. Free Radical Biology and Medicine, 17: 249–258.

    Article  Google Scholar 

  • Winterbourn, C. C., 1982. Superoxide-dependent production of hydroxyl radicals in the presence of iron salts (Letter). Biochemical Journal, 205: 463.

    Google Scholar 

  • Xu, H. Z., Zhou, C. G., Ma, Y. A., Shang, L. S., Yao, Z. W., and Li, H., 2000. Environmental quality of deposits in offshore zone of China. Environmental Protection in Transportation, 21: 16–18.

    Google Scholar 

  • Xu, X. D., Lin, Z. H., and Li, S. Q., 2005. The studied of the heavy metal pollution of Jiaozhou Bay. Marine Sciences, 29: 48–53.

    Google Scholar 

  • Yu, B. P., 1994. Cellular defenses against damage from reactive oxygen species. Physiological Reviews, 74: 139–162.

    Google Scholar 

  • Yu, R. L., Yuan, X., Zhao, Y. H., Hu, G. R., and Tu, X. L., 2008. Heavy metal pollution in intertidal sediments from Quanzhou Bay, China. Journal of Environmental Science, 20: 664–669.

    Article  Google Scholar 

  • Yuan, C. G., Shi, J. B., He, B., Liu, J. F., Liang, L. N., and Jiang, G. B., 2004. Speciation of heavy metals in marine sediments from the East China Sea by ICP-MS with sequential extraction. Environment International, 30: 769–783.

    Article  Google Scholar 

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Lei, Y., Zhang, W., Xu, W. et al. Effects of waterborne Cu and Cd on anti-oxidative response, lipid peroxidation and heavy metals accumulation in abalone Haliotis discus hannai ino. J. Ocean Univ. China 14, 511–521 (2015). https://doi.org/10.1007/s11802-015-2464-9

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