Abstract
The effects of cadmium (Cd) on metal accumulation, microelements contents, and antioxidant responses in Hexagrammos otakii were studied. The fish were exposed to 0.2, 2.5, or 10 µg L−1 Cd for 12 or 24 days. Then, the concentration of Cd and microelements (Ca, Fe, Zn, and Se) were determined in the liver and kidney. Moreover, the activities of antioxidant enzymes including superoxide dismutase (SOD), catalase (CAT), and glutathione-S-transferase (GST), and the content of malondialdehyde (MDA) in the liver and kidney were also measured. A continuous accumulation of Cd was observed throughout the experimental period. Cd accumulation was higher in liver than that in the kidney, while Ca and Fe contents were lower in liver than those in the kidney. Cd exposure resulted in a decrease of Ca and Fe concentrations in the kidney, while there was no effect on the liver. Zn and Se remained unaffected with exposure to Cd. Cd exposure induced severe oxidative stress in H. otakii, as indicated by significant induction of the activities of SOD, CAT, and GST, and a simultaneous increase of MDA content. These data show that antioxidant enzymes and microelements contents can be used as potential biomarkers to monitor environmental health in fish.
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Asagba, A. 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.
Atli, G., Alptekin, Ö., Tükel, S., and Canli, M., 2006. Response of catalase activity to Ag+, Cd2+, Cr6+, Cu2+ and Zn2+ in five tissues of freshwater fish Oreochromis niloticus. Comparative Biochemistry and Physiology C, 143: 218–224.
Atli, G., and Canli, M., 2008. Enzymatic responses to metal exposures in a freshwater fish Oreochromis niloticus. Comparative Biochemistry and Physiology C, 145: 282–287.
Basha, P. S., and Rani, A. U., 2003. Cadmium-induced antioxidant defense mechanism in freshwater teleost Oreochromis mossambicus (Tilapia). Ecotoxicology and Environmental Safety, 56: 218–221.
Benavides, M. P., Gallego, S. M., and Tomaro, M. L., 2005. Cadmium toxicity in plants. Brazilian Journal of Plant Physiology, 17: 21–34.
Brandão, F., Cappello, T., Raimundo, J., Santos, M. A., Maisano, M., Mauceri, A., et al., 2015. Unravelling the mechanisms of mercury hepatotoxicity in wildfish (Liza aurata) through a triad approach: Bioaccumulation, metabolomic profiles and oxidative stress. Metallomics, 7: 1352–1363.
Capillo, G., Silvestro, S., Sanfilippo, M., Fiorino, E., Giangrosso, G., Ferrantelli, V., et al., 2018. Assessment of electrolytes and metals profile of the Faro Lake (Capo Peloro Lagoon, Sicily, Italy) and its impact on Mytilus galloprovincialis. Chemestry & Biodiversity, 15 (5): e1800044, DOI: https://doi.org/10.1002/cbdv.201800044.
Cui, W. T., Cao, L., Liu, J. H., Ren, Z. H., Zhao, B., and Dou, S. Z., 2020. Effects of seawater acidification and cadmium on the antioxidant defense of flounder Paralichthys olivaceus larvae. Science of the Total Environment, 718: 137234.
Dang, F., Wang, W. X., and Rainbow, P. S., 2012. Unifying prolonged copper exposure, accumulation, and toxicity from food and water in a marine fish. Environmental Science and Technology, 46: 3465–3471.
Durou, C., Poirier, L., Amiard, J. C., Budzinski, H., Gnassia-Barelli, M., Lemenach, K., et al., 2007. Biomonitoring in a clean and a multi-contaminated estuary based on biomarkers and chemical analyses in the endobenthic worm Nereis diversicolor. Environmental Pollution, 148: 445–458.
Freitas, R., Pires, A., Velez, C., Almeida, Â., Moreira, A., Wrona, F. J., et al., 2016. Effects of seawater acidification on Diopatra neapolitana (Polychaete, Onuphidae): Biochemical and regenerative capacity responses. Ecological Indicators, 60: 152–161.
Gao, X. L., Zhou, F. X., and Chen, C. T. A., 2014. Pollution status of the Bohai Sea: An overview of the environmental quality assessment related trace metals. Environment International, 62: 12–30.
Gaw, S., Northcott, G., Kim, N., Wilkins, A., and Jensen, J., 2012. Comparison of earthworm and chemical assays of the bioavailability of aged 1,1-dichloro-2,2-bis (p-chlorophenyl) ethylene 1,1,1-trichloro-2,2-bis (p-chlorophenyl) ethane, and heavy metals in orchard soils. Environmental Toxicology and Chemistry, 31: 1306–1316.
Gobi, N., Vaseeharan, B., Rekha, R., Vijayakumar, S., and Faggio, C., 2018. Bioaccumulation, cytotoxicity and oxidative stress of the acute exposure selenium in Oreochromis mossambicus. Ecotoxicology and Environmental Safety, 162: 147–159.
Grosell, M., McGeer, J. C., and Wood, C. M., 2001. Plasma copper clearance and biliary copper excretion are stimulated in copper-acclimated trout. American Journal of Physiology, 280: 796–806.
Guardiola, F. A., Chaves-Pozo, E., Espinosa, C., Romero, D., Meseguer, J., Cuesta, A., et al., 2016. Mercury accumulation, structural damages, and antioxidant and immune status changes in the gilthead seabream (Sparus aurata L.) exposed to methylmercury. Archives of Environmental Contamination and Toxicology, 70: 734–746.
Hou, X. Y., 2011. Effect of zeolite on heavy metal accumulation, plasma indicators and liver metallothionein in carps (Cyprinus Carpio) with water cadmium exposure. Master thesis. Nanjing Agricultural University (in Chinese with English abstract).
Huang, X. Z., Liu, Y. M., Liu, Z. K., Zhao, Z. H., Dupont, S., Wu, F. L., et al., 2018. Impact of zinc oxide nanoparticles and ocean acidification on antioxidant responses of Mytilus coruscus. Chemosphere, 196: 182–195.
Jiao, W. Y., 2019. The study on the mechanism of immune injury induced by cadmium and chlorpyrifos exposure in common carp gills. Master thesis. Northeast Agricultural University (in Chinese with English abstract).
Kim, J. H., and Kang, J. C., 2015a. The arsenic accumulation and its effect on oxidative stress responses in juvenile rockfish, Sebastes schlegelii, exposed to waterborne arsenic (As3+). Environmental Toxicology and Pharmacology, 39: 668–676.
Kim, J. H., and Kang, J. C., 2015b. The lead accumulation and hematological findings in juvenile rock fish Sebastes schlegelii exposed to the dietary lead (II) concentrations. Ecotoxicology and Environmental Safety, 115: 33–39.
Kim, J. H., and Kang, J. C., 2016. The chromium accumulation and its physiological effects in juvenile rockfish, Sebastes schlegelii, exposed to different levels of dietary chromium (Cr6+) concentrations. Environmental Toxicology and Pharmacology, 41: 152–158.
Kraal, M. H., Kraak, M. H. S., Degroot, C. J., and Davids, C., 1995. Uptake and tissue distribution of dietary and aqueous cadmium by carp (Cyprinus carpio). Ecotoxicology and Environmental Safety, 31: 179–183.
Li, W., Wang, N. B., Li, Q. B., and Sun, B., 2008. Distribution of dissolved metals in seawater of Jinzhou Bay, China. Environmental Toxicology and Chemistry, 27 (1): 43–48.
Liew, H. J., Chiarella, D., Pelle, A., Faggio, C., Blust, R., and De Boeck, G., 2013. Cortisol emphasizes the metabolic strategies employed by common carp, Cyprinus carpio at different feeding and swimming regimes. Comparative Biochemistry and Physiology-Part A: Molecular & Integrative Physiology, 166 (3): 449–464.
Liew, H. J., Fazio, A., Faggio, C., Blust, R., and De Boeck, G., 2015. Cortisol affects metabolic and ionoregulatory responses to a different extent depending on feeding ration in common carp, Cyprinus carpio. Comparative Biochemistry and Physiology A: Molecular Integrative Physiology, 189: 45–47.
Liew, H. J., Pelle, A., Chiarella, D., Faggio, C., Tang, C. H., Blust, R., et al., 2020. Common carp, Cyprinus carpio, prefer branchial ionoregulation at high feeding rates and kidney ionoregulation when food supply is limited: Additional effects of cortisol and exercise. Fish Physiology and Biochemistry, 46 (1): 451–469.
Matz, C. J., Treble, R. G., and Krone, P. H., 2007. Accumulation and elimination of cadmium in larval stage zebrafish following acute exposure. Ecotoxicology and Environmental Safety, 66: 44–48.
Maulvault, A. L., Barbosa, V., Alves, R., Custódio, A., Anacleto, P., Repolho, T., et al., 2017. Ecophysiological responses of juvenile seabass (Dicentrarchus labrax) exposed to increased temperature and dietary methylmercury. Science of the Total Environment, 586: 551–558.
McRae, N. K., Gaw, S., and Glover, C. N., 2016. Mechanisms of zinc toxicity in the galaxiid fish, Galaxias maculatus. Comparative Biochemistry and Physiology C, 179: 184–190.
Mela, M., Neto, F. F., Yamamoto, F. Y., Almeida, R., Grötzner, S. R., Ventura, D. F., et al., 2014. Mercury distribution in target organs and biochemical responses after subchronic and trophic exposure to Neotropical fish Hoplias malabaricus. Fish Physiology and Biochemistry, 40: 245–256.
Mendil, D., Unal, O. F., Tuzen, M., and Soylak, M., 2010. Determination of trace metals in different fish species and sediments from the River Yesilirmak in Tokat, Turkey. Food and Chemical Toxicology, 48 (5): 1383–1392.
Mohsenpour, R., Mousavi-Sabet, H., Hedayati, A., Rezaei, A., Yalsuyi, A. M., and Faggio, C., 2020. In vitro effects of silver nanoparticles on gills morphology of female Guppy (Poecilia reticulate) after a short-term exposure. Microscopy Research and Technique, 83 (12): 1552–1557, DOI: https://doi.org/10.1002/jemt.23549.
Moyson, S., Liew, H. J., Fazio, A., Van Dooren, N., Delcroix, A., Faggio, C., et al., 2016. Kidney activity increases in copper exposed goldfish (Carassius auratus). Comparative Biochemistry and Physiology C Toxicology & Pharmacology, 190: 32–37.
Nordberg, G. F., 2010. Biomarkers of exposure, effects and susceptibility in humans and their application in studies of interactions among metals in China. Toxicology Letters, 192 (1): 45–49.
OSPAR, 2010. Quality Status Report 2010. OSPAR Head of Delegation Meeting, London, UK, 12–13 November 2009, 176pp.
Pagano, M., Porcino, C., Briglia, M., Fiorino, E., Vazzana, M., Silvestro, S., et al., 2017. The influence of exposure of cadmium chloride and zinc chloride on haemolymph and digestive gland cells from Mytilus galloprovincialis. International Journal of Environmental Research, 11 (2): 207–216.
Qu, R. J., Wang, X. W., Wang, Z. Y., Wei, Z. B., and Wang, L. S., 2014. Metal accumulation and antioxidant defenses in the freshwater fish Carassius auratus in response to single and combined exposure to cadmium and hydroxylated multi-walled carbon nanotubes. Journal of Hazardous Materials, 275: 89–98.
Rajeshkumar, S., Mini, J., and Munuswamy, N., 2013. Effects of heavy metals on antioxidants and expression of HSP70 in different tissues of Milk fish (Chanos chanos) of Kaattuppalli Island, Chennai, India. Ecotoxicology and Environmental Safety, 98: 8–18.
Reynders, H., Campenhout, K. V., Bervoets, L., Coen, W. M. D., and Blust, R., 2006. Dynamics of cadmium accumulation and effects in common carp (Cyprinus carpio) during simultaneous exposure to water and food (Tubifex tubifex). Environmental Toxicology and Chemistry, 25: 1558–1567.
Roy, S., and Bhattacharya, S., 2006. Arsenic-induced histopathology and synthesis of stress proteins in liver and kidney of Channa punctatus. Ecotoxicology and Environmental Safety, 65: 218–229.
Savorelli, F., Manfra, L., Croppo, M., Tornambè, A., Palazzi, D., Canepa, S., et al., 2017. Fitness evaluation of Ruditapes philippinarum exposed to nickel. Biological Trace Element Research, 177 (2): 384–393.
Torre, A., Trischitta, F., and Faggio, C., 2013. Effect of CdCl2 on Regulatory Volume Decrease (RVD) in Mytilus galloprovincialis digestive cells. Toxicology in Vitro, 27: 1260–1266.
Tsai, J. W., Ju, Y. R., Huang, Y. H., Deng, Y. S., Chen, W. Y., Wu, C. C., et al., 2013. Toxicokinetics of tilapia following high exposure to waterborne and dietary copper and implications for coping mechanisms. Environmental Science and Pollution Research International, 20: 3771–3780.
Vajargah, M. F., Yalsuyi, A. M., Hedayati, A., and Faggio, C., 2018. Histopathological lesions and toxicity in common carp (Cyprinus carpio L. 1758) induced by copper nanoparticles. Microscopy Research and Technique, 81 (7): 724–729.
Vajargah, M. F., Yalsuyi, A. M., Sattari, M., Prokic, M., and Faggio, C., 2019. Effects of copper oxide nanoparticles (CuO-NPs) on parturition time, survival rate and reproductive success of guppy fish, Poecilia reticulate. Journal of Cluster Science, 31: 499–506, DOI: https://doi.org/10.1007/s10876-019-01664-y.
Vijayakumar, S., Vaseeharan, B., Sudhakaran, R., Jeyakandan, J., Ramasamy, P., Sonawane, A., et al., 2019. Bioinspired zinc oxide nanoparticles using Lycopersicon esculentum for antimicrobial and anticancer applications. Journal of Cluster Science, 30 (6): 1465–1479.
Wu, F. Z., Huang, W., Liu, Q., Xu, X. Q., Zeng, J. N., Cao, L., et al., 2018. Responses of antioxidant defense and immune gene expression in early life stages of large yellow croaker (Pseudosciaena crocea) under methyl mercury exposure. Frontiers in Physiology, 9: 1436.
Zhang, C. N., Zhang, J. L., Ren, H. T., Zhou, B. H., Wu, Q. J., and Sun, P., 2017. Effect of tributyltin on antioxidant ability and immune responses of zebrafish (Danio rerio) Ecotoxicology and Environmental Safety, 138: 1–8.
Zhao, X., Wang, S., Ma, L., Yue, B., Zhao, Y. F., and Shang, X. H., 2016. Analysis of Pb and Cd pollution in marine fish in some sea areas of China. Journal of Hygiene Research, 45 (3): 474–476 (in Chinese with English abstract).
Zhou, Y. Y., Zhang, W., Guo, Z. Q., and Zhang, L., 2017. Effects of salinity and copper co-exposure on copper bioaccumulation in marine rabbitfish Siganus oramin. Chemosphere, 168: 491–500.
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This study was supported by the Key Technology Research and Development Program of Shandong Province (Nos. 2019GHY112071 and 2019GHY112062), and the Major Agricultural Application Technology Innovation Projects in Shandong Province (No. SD2019YY007).
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Hu, F., Sun, M., Li, L. et al. Effects of Environmental Cadmium on Cadmium Accumulation, Oxidative Response, and Microelements Regulation in the Liver and Kidney of Hexagrammos otakii. J. Ocean Univ. China 21, 479–485 (2022). https://doi.org/10.1007/s11802-022-4969-3
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DOI: https://doi.org/10.1007/s11802-022-4969-3