|
|
Cite this paper: |
|
|
Maosheng LIU, Hua XU, Qiang ZOU, Fei FANG, Shan SUN, Yuting ZHAO, Xin HE, Yonghui BO, Lei YAO, Yan FANG. Assessment of heavy metal pollution in Laizhou Bay (China) using the ecological risk index and the integrated biomarker response of the goby Acanthogobius ommaturus[J]. Journal of Oceanology and Limnology, 2023, 41(4): 1519-1536 |
|
|
|
|
|
|
|
Assessment of heavy metal pollution in Laizhou Bay (China) using the ecological risk index and the integrated biomarker response of the goby Acanthogobius ommaturus |
|
Maosheng LIU1, Hua XU2, Qiang ZOU3, Fei FANG1, Shan SUN4, Yuting ZHAO4, Xin HE4, Yonghui BO1, Lei YAO1, Yan FANG1 |
|
1 School of Agriculture, Ludong University, Yantai 264025, China; 2 Yantai Ecological Environment Monitoring Center, Yantai 264010, China; 3 Yantai Branch of Shandong Technology Transfer Center, Chinese Academy of Sciences, Yantai 264003, China; 4 Shandong Provincial Key Laboratory of Restoration for Marine Ecology, Shandong Marine Resource and Environment Research Institute, Yantai 264006, China |
|
Abstract: |
We used the Integrated Biological Responses version 2 (IBRv2) method to evaluate the biological effects of heavy metals in the sediments in Laizhou Bay, China on the benthic goby Acanthogobius ommaturus. In December 2018, gobies and sediments were collected from 15 stations. We measured the activities of defense enzymes and the contents of malondialdehyde (MDA) and metallothionein (MT) in the goby liver as well as the levels of heavy metals in the sediments and goby muscle tissue. Most of the heavy metal concentrations in sediment at each station were below the Class I criteria set by Chinese Standards for Marine Sediment Quality, and the Håkanson ecological risk index suggested low risk for the heavy metals. We found that A. ommaturus could effectively accumulate mercury, cadmium, arsenic, and zinc and that the contents of MT and MDA and the activities of glutathione peroxidase and glutathione reductase were suitable biomarkers of heavy metal pollution in this species. The IBRv2 method integrated these four biomarkers and discriminated stations according to heavy metal pollution. Higher IBRv2 values suggested more adverse effects in gobies, corroborating more serious heavy metal contamination. The stations with high IBRv2 values and high contents of heavy metals were mainly distributed in the west and northeast parts of the bay. These results show that the IBRv2 approach is a feasible strategy for assessing heavy metal pollution through biological response and biological status and that it can be implemented for environmental monitoring in Laizhou Bay. |
|
Key words:
integrated biomarker responses|heavy metal|assessment|goby Acanthogobius ommaturus|Laizhou Bay
|
|
Received: 2021-11-17 Revised: |
|
|
|
|
References:
Arikibe J E, Prasad S. 2020. Determination and comparison of selected heavy metal concentrations in seawater and sediment samples in the coastal area of Suva, Fiji. Marine Pollution Bulletin, 157: 111157, https://doi.org/10.1016/j.marpolbul.2020.111157. Barhoumi B, Clérandeau C, Gourves P Y et al. 2014. Pollution biomonitoring in the Bizerte lagoon (Tunisia), using combined chemical and biomarker analyses in grass goby, Zosterisessor ophiocephalus (Teleostei, Gobiidae).Marine Environmental Research, 101: 184-195, https://doi.org/10.1016/j.marenvres.2014.07.002. Barhoumi S, Messaoudi I, Deli T et al. 2009. Cadmium bioaccumulation in three benthic fish species, Salaria basilisca, Zosterisessor ophiocephalus and Solea vulgaris collected from the Gulf of Gabes in Tunisia. Journal of Environmental Sciences, 21(7): 980-984, https://doi.org/10.1016/S1001-0742(08)62371-2. Baudou F G, Ossana N A, Castañé P M et al. 2019. Use of integrated biomarker indexes for assessing the impact of receiving waters on a native neotropical teleost fish.Science of the Total Environment, 650: 1779-1786, https://doi.org/10.1016/j.scitotenv.2018.09.342. Beliaeff B, Burgeot T. 2002. Integrated biomarker response: a useful tool for ecological risk assessment. Environmental Toxicology and Chemistry, 21(6): 1316-1322, https://doi.org/10.1002/etc.5620210629. Bradford M M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Analytical Biochemistry, 72(1-2): 248-254, https://doi.org/10.1016/0003-2697(76)90527-3. De Araújo M C, De Assis C R D, Silva K C C et al. 2018.Characterization of brain acetylcholinesterase of bentonic fish Hoplosternum littorale: perspectives of application in pesticides and metal ions biomonitoring. Aquatic Toxicology, 205: 213-226, https://doi.org/10.1016/j.aquatox.2018.10.017. De Jesus W B, Andrade T D S D O M, Soares S H et al. 2021. Biomarkers and occurrences of heavy metals in sediment and the bioaccumulation of metals in crabs(Ucides cordatus) in impacted mangroves on the Amazon coast, Brazil. Chemosphere, 271: 129444, https://doi.org/10.1016/j.chemosphere.2020.129444. Devin S, Burgeot T, Giambérini L et al. 2014. The integrated biomarker response revisited: optimization to avoid misuse. Environmental Science and Pollution Research, 21(4): 2448-2454, https://doi.org/10.1007/s11356-013-2169-9. Di Toro D M, Mahony J D, Hansen D J et al. 1990. Toxicity of cadmium in sediments: The role of acid volatile sulfide.Environmental Toxicology and Chemistry, 9(12): 1487-1502, https://doi.org/10.1002/etc.5620091208. Duarte I A, Reis-Santos P, França S et al. 2017. Biomarker responses to environmental contamination in estuaries: a comparative multi-taxa approach.AquaticToxicology,189:31-41, https://doi.org/10.1016/j.aquatox.2017.05.010. El-Sorogy A S, Youssef M, Al-Kahtany K. 2021. Evaluation of coastal sediments for heavy metal contamination, Yanbu area, Red Sea coast, Saudi Arabia. Marine Pollution Bulletin, 163: 111966, https://doi.org/10.1016/j.marpolbul.2020.111966. Fang Y, Yang H S, Liu B Z. 2012. Tissue-specific response of metallothionein and superoxide dismutase in the clam Mactra veneriformis under sublethal mercury exposure.Ecotoxicology, 21(6): 1593-1602, https://doi.org/10.1007/s0646-012-0938-8. Fatima M, Usmani N, Firdaus F et al. 2015. In vivo induction of antioxidant response and oxidative stress associated with genotoxicity and histopathological alteration in two commercial fish species due to heavy metals exposure in northern India (Kali) river. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 176-177: 17-30, https://doi.org/10.1016/j.cbpc.2015.07.004. Filipović V, Raspor B. 2003. Metallothionein and metal levels in cytosol of liver, kidney and brain in relation to growth parameters of Mullus surmuletus and Liza aurata from the Eastern Adriatic Sea. Water Research, 37(13): 3253-3262, https://doi.org/10.1016/S0043-1354(03)00162-3. General Administration of Quality Supervision, Inspection and Quarantine of the People’s Republic of China. 2004. GB 18668-2002 Marine Sediment Quality. Standards Press of China, Beijing. (in Chinese) General Administration of Quality Supervision, Inspection and Quarantine of the People’s Republic of China, China National Standardization Administration. 2008a. GB/T 12763.1-2007 Specifications for Oceanographic Survey—Part 1: General. Standards Press of China, Beijing. (in Chinese) General Administration of Quality Supervision, Inspection and Quarantine of the People’s Republic of China, China National Standardization Administration. 2008b. GB 17378.1-2007 The Specification for Marine Monitoring—Part 1: General Rules. Standards Press of China, Beijing.(in Chinese) Grbin D, Sabolić I, Klobučar G et al. 2019. Biomarker response of Mediterranean mussels Mytilus galloprovincialis regarding environmental conditions, pollution impact and seasonal effects. Science of the Total Environment, 694:133470, https://doi.org/10.1016/j.scitotenv.2019.07.276. Håkanson L. 1980. An ecological risk index for aquatic pollution control. A sedimentological approach. Water Research, 14(8): 975-1001, https://doi.org/10.1016/0043-1354(80)90143-8. Han B, Liu A, Wang S et al. 2020. Concentration level, distribution model, source analysis, and ecological risk assessment of polycyclic aromatic hydrocarbons in sediments from Laizhou Bay, China. Marine Pollution Bulletin, 150: 110690, https://doi.org/10.1016/j.marpolbul.2019.110690. Javed M, Abbas K, Ahmed T et al. 2020. Metal pollutants induced peroxidase activity in different body tissues of freshwater fish, Labeo rohita. Environmental Chemistry and Ecotoxicology, 2: 162-167, https://doi.org/10.1016/j.enceco.2020.09.001. Jeong H, Choi J Y, Choi D H et al. 2021. Heavy metal pollution assessment in coastal sediments and bioaccumulation on seagrass (Enhalus acoroides) of Palau. Marine Pollution Bulletin, 163: 111912, https://doi.org/10.1016/j.marpolbul.2020.111912. La Colla N S, Botté S E, Marcovecchio J E. 2018. Metals in coastal zones impacted with urban and industrial wastes:insights on the metal accumulation pattern in fish species.Journal of Marine Systems, 181: 53-62, https://doi.org/10.1016/j.jmarsys.2018.01.012. Li M K, Zhu S Y, Ouyang T P et al. 2021. Magnetic properties of the surface sediments in the Yellow River Estuary and Laizhou Bay, Bohai Sea, China: implications for monitoring heavy metals. Journal of Hazardous Materials, 410: 124579, https://doi.org/10.1016/j.jhazmat.2020.124579. Li S Y, Liu G X, Miao F M. 1994. The distribution and environmental background values of the heavy metals in sediment of the Bohai sea. China Environmental Science, 14(5): 370-376. (in Chinese with English abstract) Li X, Chi W Q, Tian H et al. 2019. Probabilistic ecological risk assessment of heavy metals in western Laizhou Bay, Shandong Province, China. PLoS One, 14(3): e0213011, https://doi.org/10.1371/journal.pone.0213011. Lin Y F, Liu Q Q, Meng F P et al. 2018. Integrated toxicity evaluation of metals in sediments of Jiaozhou Bay(China): based on biomarkers responses in clam Ruditapes philippinarum exposed to sediment extracts.Marine Pollution Bulletin, 131: 180-190, https://doi.org/10.1016/j.marpolbul.2018.04.024. Liu J H, Cao L, Dou S Z. 2019. Trophic transfer, biomagnification and risk assessments of four common heavy metals in the food web of Laizhou Bay, the Bohai Sea. Science of the Total Environment, 670: 508-522, https://doi.org/10.1016/j.scitotenv.2019.03.140. Liu Q, Su Z M, Zeng X Q et al. 1997. Studies on ichthyofauna and ecology of goby fishes in the Bohai Sea. Journal of Ocean University of Qingdao, 27(2): 29-37, https://doi.org/10.16441/j.cnki.hdxb.1997.02.004. (in Chinese with English abstract) Liu R, Jiang W W, Li F J et al. 2021. Occurrence, partition, and risk of seven heavy metals in sediments, seawater, and organisms from the eastern sea area of Shandong Peninsula, Yellow Sea, China. Journal of Environmental Management, 279: 111771, https://doi.org/10.1016/j.jenvman.2020.111771. Lü D W, Zheng B, Fang Y et al. 2015. Distribution and pollution assessment of trace metals in seawater and sediment in Laizhou Bay. Chinese Journal of Oceanology and Limnology, 33(4): 1053-1061, https://doi.org/10.1007/s00343-015-4226-3. Lv J S, Xia Q, Yan T et al. 2018. Identifying the sources, spatial distributions, and pollution status of heavy metals in soils from the southern coast of Laizhou Bay, eastern China.Human and Ecological Risk Assessment: An International Journal, 25(8): 1953-1967, https://doi.org/10.1080/10807 039.2018.1478275. McDonald S, Hassell K, Cresswell T. 2021. Effect of short-term dietary exposure on metal assimilation and metallothionein induction in the estuarine fish Pseudogobius sp. Science of the Total Environment, 772: 145042, https://doi.org/10.1016/j.scitotenv.2021.145042. Migliarini B, Campisi A M, Maradonna F et al. 2005.Effects of cadmium exposure on testis apoptosis in the marine teleost Gobius niger. General and Comparative Endocrinology, 142(1-2): 241-247, https://doi.org/10.1016/j.ygcen.2004.12.012. Ministry of Ecology and Environment of the People’s Republic of China. 2021. Bulletin of Marine Ecological Environment in China in 2020, https://www.mee.gov.cn/hjzl/sthjzk/jagb/. (in Chinese) Moniruzzaman M, Kumar S, Das D et al. 2020. Enzymatic, non enzymatic antioxidants and glucose metabolism enzymes response differently against metal stress in muscles of three fish species depending on different feeding niche.Ecotoxicology and Environmental Safety, 202: 110954, https://doi.org/10.1016/j.ecoenv.2020.110954. Müller G. 1969. Index of geoaccumulation in sediments of the Rhine River. GeoJournal, 2(3): 108-118. National Health Commission of the People’s Republic of China, State Administration for Market Regulation. 2017. GB 2762-2017 National Food Safety Standard Maximum Levels of Contaminants in Foods. Standards Press of China, Beijing. (in Chinese) Osher L J, Leclerc L, Wiersma G B et al. 2006. Heavy metal contamination from historic mining in upland soil and estuarine sediments of Egypt Bay, Maine, USA. Estuarine, Coastal and Shelf Science, 70(1-2): 169-179, https://doi.org/10.1016/j.ecss.2006.06.009. Ota Y, Suzuki A, Yamaoka K et al. 2021. Geochemical distribution of heavy metal elements and potential ecological risk assessment of Matsushima Bay sediments during 2012-2016. Science of the Total Environment, 751:141825, https://doi.org/10.1016/j.scitotenv.2020.141825. Pastorino P, Prearo M, Bertoli M et al. 2020. Accumulation of As, Cd, Pb, and Zn in sediment, chironomids and fish from a high-mountain lake: First insights from the Carnic Alps. Science of the Total Environment, 729: 139007, https://doi.org/10.1016/j.scitotenv.2020.139007. Pauletto M, Lopparelli R M, Pegolo S et al. 2019. Significance of the goby Zosterisessor ophiocephalus as a sentinel species for Venice Lagoon contamination: Combining biomarker responses and bioaccumulation. Science of the Total Environment, 660: 959-973, https://doi.org/10.1016/j.scitotenv.2019.01.033. Qi Y J, He Z S, Yuan J J et al. 2021. Comprehensive evaluation of organophosphate ester contamination in surface water and sediment of the Bohai Sea, China. Marine Pollution Bulletin, 163: 112013, https://doi.org/10.1016/j.marpolbul.2021.112013. Rajeshkumar S, Mini J, 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, https://doi.org/10.1016/j.ecoenv.2013.07.029. Raphael S, Aude J, Olivier P et al. 2016. Characterization of a genotoxicity biomarker in three-spined stickleback (G asterosteus aculeatus L.): biotic variability and integration in a battery of biomarkers for environmental monitoring.Environmental Toxicology, 31(4): 415-426, https://doi.org/10.1002/tox.22055. Rebolledo U A, Páez-Osuna F, Fernández R. 2021. Single and mixture toxicity of As, Cd, Cr, Cu, Fe, Hg, Ni, Pb, and Zn to the rotifer Proales similis under different salinities.Environmental Pollution, 271: 116357, https://doi.org/10.1016/J.ENVPOL.2020.116357. Richetti S K, Rosemberg D B, Ventura-Lima J et al. 2011. Acetylcholinesterase activity and antioxidant capacity of zebrafish brain is altered by heavy metal exposure. NeuroToxicology, 32(1): 116-122, https://doi.org/10.1016/j.neuro.2010.11.001. Salgado L D, Marques A E M L, Kramer R D et al. 2021.Sediment contamination and toxic effects on Violet Goby fish (Gobioides broussonnetii-Gobiidae) from a marine protected area in South Atlantic. Environmental Research, 195: 110308, https://doi.org/10.1016/j.envres.2020.110308. Sanchez W, Burgeot T, Porcher J M. 2013. A novel “Integrated Biomarker Response” calculation based on reference deviation concept. Environmental Science and Pollution Research, 20(5): 2721-2725, https://doi.org/10.1007/s11356-012-1359-1. Scheuhammer A M, Cherian M G. 1986. Quantification of metallothioneins by a silver-saturation method.Toxicology and Applied Pharmacology, 82(3): 417-425, https://doi.org/10.1016/0041-008X(86)90277-2. Simonato J D, Mela M, Doria H B et al. 2016. Biomarkers of waterborne copper exposure in the Neotropical fish Prochilodus lineatus. Aquatic Toxicology, 170: 31-41, https://doi.org/10.1016/j.aquatox.2015.11.012. State Environmental Protection Administration of the People’s Republic of China. 2004. GB 3097-1997 Marine Water Quality Standard. China Environmental Press, Beijing.(in Chinese) Swaleh S B, Banday U Z, Usmani N. 2019. Comparative study of biochemical, histological and molecular biomarkers of heavy metal contamination in Cyprinus carpio collected from warm-monomictic lake and government culture pond. Chemosphere, 236: 124182, https://doi.org/10.1016/j.chemosphere.2019.06.152. Tagliaferro M, Gonçalves A M M, Bergman M et al. 2018.Assessment of metal exposure (uranium and copper) by the response of a set of integrated biomarkers in a stream shredder. Ecological Indicators, 95: 991-1000, https://doi.org/10.1016/j.ecolind.2017.10.065. Tian K, Wu Q M, Liu P et al. 2020. Ecological risk assessment of heavy metals in sediments and water from the coastal areas of the Bohai Sea and the Yellow Sea. Environment International, 136: 105512, https://doi.org/10.1016/j.envint.2020.105512. Vieira C E D, Costa P G, Caldas S S et al. 2019. An integrated approach in subtropical agro-ecosystems:Active biomonitoring, environmental contaminants, bioaccumulation, and multiple biomarkers in fish. Science of the Total Environment, 666: 508-524, https://doi.org/10.1016/j.scitotenv.2019.02.209. Weber A A, Sales C F, Faria F D S et al. 2020. Effects of metal contamination on liver in two fish species from a highly impacted neotropical river: A case study of the Fundão dam, Brazil.EcotoxicologyandEnvironmentalSafety,190:110165, https://doi.org/10.1016/j.ecoenv.2020.110165. WHO. 1993. Biomarkers and risk assessment: concepts and principles. In: Safety I P O C ed. Environmental Health Criteria. United Nations Environment Programme, International Labour Organisation, World Health Organization, Geneva. Xia P, Meng X W, Yin P et al. 2011. Eighty-year sedimentary record of heavy metal inputs in the intertidal sediments from the Nanliu River estuary, Beibu Gulf of South China Sea. Environmental Pollution, 159: 92-99, https://doi.org/10.1016/j.envpol.2010.09.014. Xu G, Liu J, Pei S F et al. 2015. Sediment properties and trace metal pollution assessment in surface sediments of the Laizhou Bay, China. Environmental Science and Pollution Research, 22(15): 11634-11647, https://doi.org/10.1007/s11356-015-4393-y. Zhang L C, Li F, Lv Z B et al. 2019. Stock distribution and community structure of members in Gobioidei in Laizhou Bay. Journal of Dalian Ocean University, 34(4): 588-594, https://doi.org/10.16535/j.cnki.dlhyxb.2019.04.019. (in Chinese with English abstract) Zhang P, Hu R J, Zhu L H et al. 2017. Distributions and contamination assessment of heavy metals in the surface sediments of western Laizhou Bay: Implications for the sources and influencing factors. Marine Pollution Bulletin, 119(1): 429-438, https://doi.org/10.1016/j.marpolbul.2017.03.046. Zhao L, Xu Y F, Hou H et al. 2014. Source identification and health risk assessment of metals in urban soils around the Tanggu chemical industrial district, Tianjin, China.Science of the Total Environment, 468-469: 654-662, https://doi.org/10.1016/j.scitotenv.2013.08.094. Zhu N, Yang Y Y, Xu H et al. 2019. Bioaccumulation of decabromodiphenyl ether affects the antioxidant system in the clam Mactra veneriformis. Environmental Toxicology and Pharmacology, 68: 19-26, https://doi.org/10.1016/j.etap.2019.03.004.
|
|
|