Abstract
This study used the integrated biomarker response (IBR) index approach to assess the ecological risks of heavy metals in different regions of Dianchi Lake, combined with active monitoring and passive monitoring. The contents of five heavy metals (Cu, As, Cd, Hg, and Pb) and six biomarkers (acetylcholinesterase, sodium-potassium ATPase, metallothionein, superoxide dismutase, glutathione peroxidase, and malondialdehyde) in the muscles of crucians (Carassius auratus) were measured to calculate the IBR value. The results indicate that the contents of heavy metal in the fish under active monitoring and passive monitoring were rather low and did not exceed the National Food Safety Standards of China. The IBR value of day 14 of active monitoring correlated with the heavy metal Cd content in the fish, suggesting a potential risk of Cd pollution in the aquatic environment of Dianchi Lake. The IBR values obtained for different regions of the lake on day 14 can be arranged in the following order: West S3 (9.24) > East S1 (3.97) > South S2 (2.39) > North S4 (0.36). These results suggest a potential risk of heavy metal contamination in the western part of Dianchi Lake.
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References
Andral B, Stanisiere JY, Sauzade D, Damier E, Thebault H, Galgani F, Boissery P (2004) Monitoring chemical contamination levels in the mediterranean based on the use of mussel caging. Mar Pollut Bull 49(9-10):704–712. https://doi.org/10.1016/j.marpolbul.2004.05.008
Baudou FG, Ossana NA, Castane PM, Mastrangelo MM, Gonzalez Nunez AA, Palacio MJ, Ferrari L (2019) Use of integrated biomarker indexes for assessing the impact of receiving waters on a native neotropical teleost fish. Sci Total Environ 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. Environ Toxicol Chem 21:1316–1322. https://doi.org/10.1002/etc.5620210629
Bervoets L, Voets J, Covaci A, Chu SG, Qadah D, Smolders R, Schepens P, Blust R (2005) Use of transplanted zebra mussels (Dreissena polymorpha) to assess the bioavailability of microcontaminants in Flemish surface waters. Environ Sci Technol 39:1492–1505. https://doi.org/10.1021/es049048t
Besse JP, Geffard O, Coquery M (2012) Relevance and applicability of active biomonitoring in continental waters under the Water Framework Directive. Trac-Trends Anal Chem 36:113–127. https://doi.org/10.1016/j.trac.2012.04.004
Brooks S, Harman C, Zaldibar B, Izagirre U, Glette T, Marigomez I (2011) Integrated biomarker assessment of the effects exerted by treated produced water from an onshore natural gas processing plant in the North Sea on the mussel Mytilus edulis. Mar Pollut Bull 62(2):327–339
Cheng H, Li M, Zhao C, Yang K, Li K, Peng M, Yang Z, Liu F, Liu Y, Bai R, Cui Y, Huang Z, Li L, Liao Q, Luo J, Jia S, Pang X, Yang J, Yin G (2015) Concentrations of toxic metals and ecological risk assessment for sediments of major freshwater lakes in China. J Geochem Explor 157:15–26. https://doi.org/10.1016/j.gexplo.2015.05.010
Chowdhury S, Mazumder MAJ, Attas OA, Husain T (2016) Heavy metals in drinking water: occurrences, implications, and future needs in developing countries. Sci Total Environ 569:476–488. https://doi.org/10.1016/j.scitotenv.2016.06.166
Da C, Petry CT, Droste A (2016) Active versus passive biomonitoring of air quality: genetic damage and bioaccumulation of trace elements in flower buds of Tradescantia pallida var. purpurea. Water Air Soil Pollut 227(7). https://doi.org/10.1007/s11270-016-2923-y
Dabrowska H, Kopko O, Lehtonen KK, Lang T, Waszak I, Balode M, Strode E (2017) An integrated assessment of pollution and biological effects in flounder, mussels and sediment in the southern Baltic Sea coastal area. Environ Sci Pollut Res 24(3):3626–3639. https://doi.org/10.1007/s11356-016-8117-8
Devin S, Burgeot T, Giamberini L, Minguez L, Pain DS (2014) The integrated biomarker response revisited: optimization to avoid misuse. Environ Sci Pollut Res 21(4):2448–2454. https://doi.org/10.1007/s11356-013-2169-9
Fang T, Ao HY, Liu JT, Cai QH, Liu YD (2004) The spatio-temporal of water environmental status in Dianchi lake. Acta Hydrobiol Sin 28:124–130. https://doi.org/10.3321/j.issn:1000-3207.2004.02.003 (in Chinese)
Ferreira CP, Lima D, Paiva R, Vilke JM, Mattos JJ, Almeida EA, Grott SC, Alves TC, Correa JN, Jorge MB, Uczay M, Vogel CIG, Gomes CHAM, Bainy ACD, Luchmann KH (2019) Metal bioaccumulation, oxidative stress and antioxidant responses in oysters Crassostrea gasar transplanted to an estuary in southern Brazil. Sci Total Environ 685:332–344. https://doi.org/10.1016/j.scitotenv.2019.05.384
Fu J, Hu X, Tao XC, Yu HX, Zhang XW (2013) Risk and toxicity assessments of heavy metals in sediments and fishes from the Yangtze River and Taihu Lake, China. Chemosphere 93(9):1887–1895. https://doi.org/10.1016/j.chemosphere.2013.06.061
Goldberg ED (1975) The mussel watch — A first step in global marine monitoring. Marine Pollution Bulletin 6 (7):111–114. https://doi.org/10.1016/0025-326X(75)90271-4
Hagger JA, Galloway TS, Langston WJ, Jones MB (2009) Application of biomarkers to assess the condition of European Marine Sites. Environ Pollut 157:2003–2010. https://doi.org/10.1016/j.envpol.2009.02.038
Handy RD, Galloway TS, Depledge MH (2003) A proposal for the use of biomarkers for the assessment of chronic pollution and in regulatory toxicology. Ecotoxicology 12:331–343. https://doi.org/10.1023/A:1022527432252
Hou Y, Li B, Muller F, Chen WP (2016) Ecosystem services of human-dominated watersheds and land use influences: a case study from the Dianchi Lake watershed in China. Environ Monit Assess 188:652–671. https://doi.org/10.1007/s10661-016-5629-0
Hu B, Jia X, Hu J, Xu D, Xia F, Li Y (2017) Assessment of heavy metal pollution and health risks in the soil-plant-human system in the Yangtze River Delta, China. Int J Environ Res Public Health 14:1042–1060. https://doi.org/10.3390/ijerph14091042
Huang C, Wang X, Yang H, Li Y, Wang Y, Chen X, Xu L (2014) Satellite data regarding the eutrophication response to human activities in the plateau lake Dianchi in China from 1974 to 2009. Sci Total Environ 486:1–11. https://doi.org/10.1016/j.scitotenv.2014.03.031
Iturburu FG, Bertrand L, Mendieta JR, Ame MV, Menone ML (2018) An integrated biomarker response study explains more than the sum of the parts: oxidative stress in the fish Australoheros facetus exposed to imidacloprid. Ecol Indic 93:351–357. https://doi.org/10.1016/j.ecolind.2018.05.019
Jaiswal A, Verma A, Jaiswal P (2018) Detrimental effects of heavy metals in soil, plants, and aquatic ecosystems and in humans. J Environ Pathol Toxicol Oncol 37:183–197. https://doi.org/10.1615/jenvironpatholtoxicoloncol.2018025348
Jebali J, Banni M, Guerbej H, Almeida EA, Bannaoui A, Boussetta H (2006) Effects of malathion and cadmium on acetylcholinesterase activity and metallothionein levels in the fish Seriola dumerilli. Fish Physiol Biochem 32:93–98. https://doi.org/10.1007/s10695-006-0041-2
Ji Y, Wu P, Zhang J, Zhang J, Zhou Y, Peng Y, Zhang S, Cai G, Gao G (2018) Heavy metal accumulation, risk assessment and integrated biomarker responses of local vegetables: a case study along the Le’an river. Chemosphere 199:361–371. https://doi.org/10.1016/j.chemosphere.2018.02.045
Kim WK, Lee SK, Jung J (2010) Integrated assessment of biomarker responses in common carp (Cyprinus carpio) exposed to perfluorinated organic compounds. J Hazard Mater 180:395–400. https://doi.org/10.1016/j.jhazmat.2010.04.044
Li RY, Yang H, Zhou ZG, Lu JJ, Shao XH, Jin F (2007) Fractionation of heavy metals in sediments from Dianchi Lake, China. Pedosphere 17:265–272. https://doi.org/10.1016/s1002-0160(07)60033-2
Li L, Hu XZ, Liu PT, Zhou BH, Jin XC (2010) Heavy metals distribution characteristics and potential ecological risk evaluation in the sediment of outer area of Lake Dianchi. Environ Sci 30:46–51 (in Chinese)
Li X, Wang M, Chen W, Jiang R (2019) Evaluation of combined toxicity of siduron and cadmium on earthworm (Eisenia fetida) using Biomarker Response Index. Sci Total Environ 646:893–901. https://doi.org/10.1016/j.scitotenv.2018.07.380
Li Y, Zhou Q, Ren B, Luo J, Yuan J, Ding X, Bian H, Yao X (2020) Trends and health risks of dissolved heavy metal pollution in global river and lake water from 1970 to 2017. Rev Environ Contam Toxicol 251:1–24. https://doi.org/10.1007/398_2019_27
Lin VS (2015) Research highlights: natural passive samplers-plants as biomonitors. Environ Sci Process Impacts 17:1137–1140. https://doi.org/10.1039/c5em90016f
Lischka A, Pook CJ, Pannell JL, Braid HE, Gaw S, Bolstad KSR (2020) Distribution of trace elements in the tissues of arrow squid (Nototodarus sloanii) from the Chatham Rise, New Zealand: human health implications. Fish Res 221:383–390. https://doi.org/10.1016/j.fishres.2019.105383
Liu X (2017) The identification of nutrient limitations on eutrophication in Dianchi Lake, China. Water Environ J 31:592–597. https://doi.org/10.1111/wej.12284
Liu JL, Yang Y, Liu F, Zhang LL (2014) Relationship between periphyton biomarkers and trace metals with the responses to environment applying an integrated biomarker response index (IBR) in estuaries. Ecotoxicology 23:538–552. https://doi.org/10.1007/s10646-014-1234-6
Lu GH, Ji Y, Zhang HZ, Wu H, Qin J, Wang C (2010) Active biomonitoring of complex pollution in Taihu Lake with Carassius auratus. Chemosphere 79:588–594. https://doi.org/10.1016/j.chemosphere.2010.01.053
Lu GH, Qi PD, Qin J, Wang C (2011) Biomarker responses in fish exposed to sediments from Northern Taihu Lake. Bull Environ Contam Toxicol 87:499–505. https://doi.org/10.1007/s00128-011-0398-5
Ma Y, Egodawatta P, McGree J, Liu A, Goonetilleke A (2016) Human health risk assessment of heavy metals in urban stormwater. Sci Total Environ 557:764–772. https://doi.org/10.1016/j.scitotenv.2016.03.067
Marigomez I, Zorita I, Izagirre U, Zarragoitia OM, Navarro P, Etxebarria N, Orbea A, Soto M, Cajaraville MP (2013) Combined use of native and caged mussels to assess biological effects of pollution through the integrative biomarker approach. Aquat Toxicol 137:32–48. https://doi.org/10.1016/j.aquatox.2013.03.008
Peng JF, Song YH, Yuan P, Cui XY, Qiu GL (2009) The remediation of heavy metals contaminated sediment. J Hazard Mater 161:633–640. https://doi.org/10.1016/j.jhazmat.2008.04.061
Qi HX, Li HZ, Ma P, You J (2015) Integrated sediment quality assessment through biomarker responses and bioavailability measurements: application in Tai Lake, China. Ecotoxicol Environ Saf 119:148–154. https://doi.org/10.1016/j.ecoenv.2015.05.007
Qu C, Li B, Wu H, Wang S, Li F (2015) Probabilistic ecological risk assessment of heavy metals in sediments from China’s major aquatic bodies. Stoch Env Res Risk A 30:271–282. https://doi.org/10.1007/s00477-015-1087-4
Ronci L, Meccoli L, Iannilli V, Menegoni P, Matthaeis ED, Setini A (2016) Comparison between active and passive biomonitoring strategies for the assessment of genotoxicity and metal bioaccumulation in Echinogammarus veneris (Crustacea: Amphipoda). Ital J Zool 83:162–172. https://doi.org/10.1080/11250003.2016.1169321
Seo D, Vasconcellos MBA, Catharino MGM, Moreira EG, Sousa ED, Saiki M (2013) Vanadium determination in Perna perna mussels (Linnaeus, 1758: Mollusca, Bivalvia) by instrumental neutron activation analysis using the passive biomonitoring in the Santos coast, Brazil. J Radioanal Nucl Chem 296:459–463. https://doi.org/10.1007/s10967-012-2048-8
Serafim A, Company R, Lopes B, Fonseca VF, Franca S, Vasconcelos RP, Bebianno MJ, Cabral HN (2012) Application of an integrated biomarker response index (IBR) to assess temporal variation of environmental quality in two Portuguese aquatic systems. Ecol Indic 19:215–225. https://doi.org/10.1016/j.ecolind.2011.08.009
Sibal LN, Espino MPB (2018) Heavy metals in lake water: a review on occurrence and analytical determination. Int J Environ Anal Chem 98:536–554. https://doi.org/10.1080/03067319.2018.1481212
Song Q, Li J (2015) A review on human health consequences of metals exposure to e-waste in China. Environ Pollut 196:450–461. https://doi.org/10.1016/j.envpol.2014.11.004
Sturla LJ, Malanga G, Mónica NG (2019) Multiple-biomarker approach in a commercial marine scallop from San Jose gulf (Patagonia, Argentina) for health status assessment. Arch Environ Contam Toxicol 78(3):451–462. https://doi.org/10.1007/s00244-019-00690-1
Sun X, Xia B, Cui Z, Chen B (2016) Integrated biomarker responses in the hepatopancreas of the bivalve, Mactra veneriformis (Reeve, 1854) from the Yellow River Estuary, China. Indian J Geo-Mar Sci 45:388–398
Tang WZ, Shan BQ, Zhang H, Mao ZP (2010) Heavy metal sources and associated risk in response to agricultural intensification in the estuarine sediments of Chaohu Lake Valley, East China. J Hazard Mater 176:945–951. https://doi.org/10.1016/j.jhazmat.2009.11.131
Tlili S, Minguez L, Giamberini L, Geffard A, Boussetta H, Mouneyrac C (2013) Assessment of the health status of Donax trunculus from the Gulf of Tunis using integrative biomarker indices. Ecol Indic 32:285–293. https://doi.org/10.1016/j.ecolind.2013.04.003
Tsangaris C, Hatzianestis I, Catsiki VA, Kormas KA, Strogyloudi E, Neofitou C, Andral B, Galgani F (2011) Active biomonitoring in Greek coastal waters: application of the integrated biomarker response index in relation to contaminant levels in caged mussels. Sci Total Environ 412:359–365. https://doi.org/10.1016/j.scitotenv.2011.10.028
Ullah AK, Maksud MA, Khan SR, Lutfa LN, Quraishi SB (2017) Dietary intake of heavy metals from eight highly consumed species of cultured fish and possible human health risk implications in Bangladesh. Toxicol Rep 4:574–579. https://doi.org/10.1016/j.toxrep.2017.10.002
Wang Z, Cui Z (2016) Accumulation, biotransformation, and multi-biomarker responses after exposure to arsenic species in the earthworm Eisenia fetida. Toxicol Res 5:500–510. https://doi.org/10.1039/c5tx00396b
Wang C, Lu GH, Song WT, Xu S, Wang PF (2010) Integrated biomarker response index for the assessment of environmental stress of the Yangtze River (Nanjing section). Fish Physiol Biochem 36:1069–1078. https://doi.org/10.1007/s10695-010-9384-9
Wang Z, Yao L, Liu G, Liu W (2014) Heavy metals in water, sediments and submerged macrophytes in ponds around the Dianchi Lake, China. Ecotoxicol Environ Saf 107:200–206. https://doi.org/10.1016/j.ecoenv.2014.06.002
Wepener V, van Vuren JHJ, Chatiza FP, Mbizi Z, Slabbert L, Masola B (2005) Active biomonitoring in freshwater environments: early warning signals from biomarkers in assessing biological effects of diffuse sources of pollutants. Phys Chem Earth 30:751–761. https://doi.org/10.1016/j.pce.2005.08.018
Xiao D, Shi Z, Wu F, Su B, Feng Z (2018) Seasonal and spatial variations of heavy metals in surface sediments collected from the Baoxiang River in the Dianchi Watershed, China. Hum Ecol Risk Assess 24:1916–1929. https://doi.org/10.1080/10807039.2018.1431044
Xie Q, Gui D, Liu W, Wu Y (2020) Risk for Indo-Pacific humpback dolphins (Sousa chinensis) and human health related to the heavy metal levels in fish from the Pearl River Estuary, China. Chemosphere 240:124844. https://doi.org/10.1016/j.chemosphere.2019.124844
Xing K, Guo H, Sun Y, He B, Huang Y (2005) Simulation of non-point source pollution in watershed scale: the case of application in Dianchi Lake Basin. Geogr Res 24(4):549–558 (in Chinese)
Zhang Y, Shi T, Zhang Y, Yu T (2014) Spatial distribution and risk assessment of heavy metals in sediments from a hypertrophic plateau lake Dianchi, China. Environ Monit Assess 186:1219–1234. https://doi.org/10.1007/s10661-013-3451-5
Zhao J, Guo F (2019) Assessment of lake eutrophication recovery: the filtering trajectory method (FTM) and its application to Dianchi Lake, China. Environ Monit Assess 191(6):360. https://doi.org/10.1007/s10661-019-7492-2
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This work was supported by the National Natural Science Foundation of China (Grant No. 21567029).
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Gao, Y., Fang, L., Xiang, Q.Q. et al. Ecological risk assessment of heavy metals in fish from the Dianchi Lake, China using the integrated biomarker response approach. Environ Sci Pollut Res 27, 45712–45721 (2020). https://doi.org/10.1007/s11356-020-10434-7
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DOI: https://doi.org/10.1007/s11356-020-10434-7