Abstract
Fourteen aquatic organism samples were collected from Bohai Bay, and concentrations of five heavy metals were measured to evaluate the pollution levels in aquatic organisms and the potential risk to human health. The concentrations of Zn and Cu were much higher than those of Cd, Cr, and Pb in all the organisms. In general, the heavy metal concentration levels were in the order phytoplankton < zooplankton < fish < shrimp < shellfish. Heavy metal concentrations in higher trophic-level aquatic organisms in Bohai Bay were compared to those in the organisms from other worldwide coastal waters. The concentration levels of most heavy metals were higher than the 75th percentile, except that Pb concentration was between the 25th and 50th percentiles. The calculated bioconcentration factors (BCF) of Cr, Cu, and Pb for phytoplankton were less than 100, indicating no accumulation in primary producers. The bioaccumulation factor (BAF) of Pb for zooplankton was the highest, indicating significant Pb accumulation in zooplankton. For higher trophic-level aquatic organisms, the order of BAF values was fish < shrimp < shellfish for most metals except for Pb. The human health risk assessment suggests that strict abatement measures of heavy metals must be taken to decrease the health risk caused by consuming aquatic products.
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References
Ahmed Q, Bat L (2015) Heavy metal levels in Euthynnus affinis (Cantor 1849) Kawakawa fish marketed at Karachi Fish Harbour, Pakistan and potential risk to human health. J Black Sea/Mediterr Environ 21:35–44
Alyahya H, El-Gendy AH, Farraj SA, El-Hedeny M (2011) Evaluation of heavy metal pollution in the Arabian Gulf using the clam Meretrix meretrix Linnaeus, 1758. Water Air Soil Poll 214:499–507
Amoozadeh E, Malek M, Rashidinejad R, Nabavi S, Karbassi M, Ghayoumi R, Ghorbanzadeh-Zafarani G, Salehi H, Sures B (2014) Marine organisms as heavy metal bioindicators in the Persian Gulf and the Gulf of Oman. Environ Sci Poll R 21:2386–2395
Baboli MJ, Velayatzadeh M, Branch A (2013) Determination of heavy metals and trace elements in the muscles of marine shrimp, Fenneropenaeus merguiensis from Persian Gulf, Iran. J Anim Plant Sci 23:786–791
Balfour S, Badrie N, Yen IC, Chatergoon L (2012) Seasonal influence and heavy metal analysis in marine shrimp (Penaeus spp.) sold in Trinidad, West Indies. J Food Res 1:193–199
Bat L, Şahin F, Sezgin M, Üstün F, Baki OG, Öztekin HC (2013) Heavy metals in edible tissues of the brown shrimp Crangon crangon (Linnaeus, 1758) from the Southern Black Sea (Turkey). J Black Sea/Mediterr Environ 19:70–81
Canli M, Atli G (2003) The relationships between heavy metal (Cd, Cr, Cu, Fe, Pb, Zn) levels and the size of six Mediterranean fish species. Environ Pollut 121:129–136
Cheng WH, Yap CK (2015) Potential human health risks from toxic metals via mangrove snail consumption and their ecological risk assessments in the habitat sediment from Peninsular Malaysia. Chemosphere 135:156–165
Copat C, Arena G, Fiore M, Ledda C, Fallico R, Sciacca S, Ferrante M (2013) Heavy metals concentrations in fish and shellfish from eastern Mediterranean Sea: consumption advisories. Food Chem Toxicol 53:33–37
Dadar M, Peyghan R, Memari HR (2014) Evaluation of the bioaccumulation of heavy metals in white shrimp (Litopenaeus vannamei) along the Persian Gulf coast. B Environ Contam Tox 93:339–343
Dixit R, Malaviya D, Pandiyan K, Singh UB, Sahu A, Shukla R, Singh BP, Rai JP, Sharma PK, Lade H (2015) Bioremediation of heavy metals from soil and aquatic environment: an overview of principles and criteria of fundamental processes. Sustain 7:2189–2212
Eroglu A, Dogan Z, Kanak E, Atli G, Canli M (2015) Effects of heavy metals (Cd, Cu, Cr, Pb, Zn) on fish glutathione metabolism. Environ Sci Poll R 22:3229–3237
Fan W, Xu Z, Wang WX (2015) Contrasting metal detoxification in polychaetes, bivalves and fish from a contaminated bay. Aquat Toxicol 159:62–68
Gao X, Chen CTA (2012) Heavy metal pollution status in surface sediments of the coastal Bohai Bay. Water Res 46:1901–1911
Gargouri D, Azri C, Serbaji MM, Jedoui Y, Montacer M (2011) Heavy metal concentrations in the surface marine sediments of Sfax Coast, Tunisia. Environ Monit Assess 175:519–530
Ge HL, Liu SS, Su BX, Qin LT (2014) Predicting synergistic toxicity of heavy metals and ionic liquids on photobacterium Q67. J Hazard Mater 268:77–83
Hanna RG (1989) Levels of heavy metals in some Red Sea fish before hot brine pools mining. Mar Pollut Bull 20:631–635
Hu B, Li G, Li J, Bi J, Zhao J, Bu R (2013) Spatial distribution and ecotoxicological risk assessment of heavy metals in surface sediments of the southern Bohai Bay, China. Environ Sci Poll R 20:4099–4110
Hu LG, Diez-Rivas C, Hasan AR, Solo-Gabriele H, Fieber L, Cai Y (2010) Transport and interaction of arsenic, chromium, and copper associated with CCA-treated wood in columns of sand and sand amended with peat. Chemosphere 78:989–995
Kim JH, Kang JC (2015) The lead accumulation and hematological findings in juvenile rock fish Sebastes schlegelii exposed to the dietary lead (II) concentrations. Ecotox Environ Safe 115:33–39
Liang L, He B, Jiang G, Chen D, Yao Z (2004) Evaluation of mollusks as biomonitors to investigate heavy metal contaminations along the Chinese Bohai Sea. Sci Total Environ 324:105–113
Liu C, Wang ZY, He Y (2003) Water pollution in the river mouths around Bohai Bay. Int J Sediment Res 18:326–332
Liu J, Cao L, Huang W, Zhang C, Dou S (2014) Zinc and copper bioaccumulation in fish from Laizhou Bay, the Bohai Sea. Chin J Oceanol Limn 32:491–502
Lu X, Zhang Y, Liu H, **ng M, Shao X, Zhao F, Li X, Liu Q, Yu D, Yuan X (2014) Influence of early diagenesis on the vertical distribution of metal forms in sediments of Bohai Bay, China. Mar Pollut Bull 88:155–161
Martínez M, Intralawan A, Vázquez G, Pérez-Maqueo O, Sutton P, Landgrave R (2007) The coasts of our world: ecological, economic and social importance. Ecolo Eco 63:254–272
McLean C, Miskiewicz A, Roberts E (1991) Effect of three primary treatment sewage outfalls on metal concentrations in the fish Cheilodactylus fuscus collected along the coast of Sydney, Australia. Mar Pollut Bull 22:134–140
Meng W, Qin Y, Zheng B, Zhang L (2008) Heavy metal pollution in Tian** Bohai bay, China. J Environ Sci 20:814–819
MEP (2013) Exposure factors handbook of Chinese population (Adults). Chinese Environment Press (in Chinese), Bei**g
Metian M, Giron E, Borne V, Hédouin L, Teyssié JL, Warnau M (2008) The brown alga Lobophora variegata, a bioindicator species for surveying metal contamination in tropical marine environments. J Exp Mar Biol Ecol 362:49–54
Monikh FA, Maryamabadi A, Savari A, Ghanemi K (2015) Heavy metals’ concentration in sediment, shrimp and two fish species from the northwest Persian Gulf. Toxicol Ind Health 31:554–565
Naser HA (2013) Assessment and management of heavy metal pollution in the marine environment of the Arabian Gulf: a review. Mar Pollut Bull 72:6–13
WHO (2011) Guidelines for drinking water quality, 4th edn. WHO Press, Geneva, Switzerland
Peng S (2015) The nutrient, total petroleum hydrocarbon and heavy metal contents in the seawater of Bohai Bay, China: temporal–spatial variations, sources, pollution statuses, and ecological risks. Mar Pollut Bull 95:445–451
Pini J, Richir J, Watson G (2015) Metal bioavailability and bioaccumulation in the polychaete Nereis (Alitta) virens (Sars): the effects of site-specific sediment characteristics. Mar Pollut Bull 95:565–575
Qiu YW, Lin D, Liu JQ, Zeng EY (2011) Bioaccumulation of trace metals in farmed fish from South China and potential risk assessment. Ecotox Environ Safe 74:284–293
Romeo M, Siau Y, Zn S, Gnassia-Barelli M (1999) Heavy metal distribution in different fish species from the Mauritania coast. Sci Total Environ 232:169–175
Saleh E A, Sadek K M, Ghorbal S H (2014) Bio-estimation of selected heavy metals in shellfish and their surrounding environmental media[J]. World Academy of Science, Engineering and Technology, International Journal of Biological, Biomolecular, Agricultural, Food and Biotechnological Engineering 8:1208–1212
Sankar T, Zynudheen A, Anandan R, Nair PV (2006) Distribution of organochlorine pesticides and heavy metal residues in fish and shellfish from Calicut region, Kerala, India. Chemosphere 65:583–590
Sapkota A, Sapkota AR, Kucharski M, Burke J, McKenzie S, Walker P, Lawrence R (2008) Aquaculture practices and potential human health risks: current knowledge and future priorities. Environ Int 34:1215–1226
Shafi N, Pandit AK, Kamili AN, Mushtaq B (2015) Heavy metal accumulation by Azolla pinnata of Dal Lake ecosystem, India. Development 1:8–12
Tao Y, Yuan Z, **aona H, Wei M (2012) Distribution and bioaccumulation of heavy metals in aquatic organisms of different trophic levels and potential health risk assessment from Taihu lake, China. Ecotox Environ Safe 81:55–64
USEPA (1991) Technical support document for water quality-based toxics control (EPA/505/2-90-001). Washington, DC.
USEPA (2015) Integrated Risk Information System. URL: http://www.epa.gov/iris
Vicente-Martorell JJ, Galindo-Riaño MD, García-Vargas M, Granado-Castro MD (2009) Bioavailability of heavy metals monitoring water, sediments and fish species from a polluted estuary. J Hazard Mater 162:823–836
Xu FL, Li YL, Wang Y, He W, Kong XZ, Qin N, Liu WX, Wu WJ, Jorgensen SE (2015) Key issues for the development and application of the species sensitivity distribution (SSD) model for ecological risk assessment. Ecolo Indic 54:227–237
Xu J, Zhang M (2012) Primary consumers as bioindicator of nitrogen pollution in lake planktonic and benthic food webs. Ecolo Indic 14:189–196
Yatawara M, Qi S, Owago OJ, Zhang Y, Yang D, Zhang J, Burnet JE (2010) Organochlorine pesticide and heavy metal residues in some edible biota collected from Quanzhou Bay and **nghua Bay, Southeast China. J Environ Sci 22:314–320
Yi Y, Yang Z, Zhang S (2011) Ecological risk assessment of heavy metals in sediment and human health risk assessment of heavy metals in fishes in the middle and lower reaches of the Yangtze River basin. Environ Pollut 159:2575–2585
Yu T, Zhang Y, Meng W, Hu X (2012) Characterization of heavy metals in water and sediments in Taihu Lake, China. Environ Monit Assess 184:4367–4382
Zhang W, Liu X, Cheng H, Zeng EY, Hu Y (2012) Heavy metal pollution in sediments of a typical mariculture zone in South China. Mar Pollut Bull 64:712–720
Zhou R, Qin X, Peng S, Deng S (2014) Total petroleum hydrocarbons and heavy metals in the surface sediments of Bohai Bay, China: long-term variations in pollution status and adverse biological risk. Mar Pollut Bull 83:290–297
Acknowledgments
This work was financially supported by The National Natural Science Fund (41273068), Tian** Research Program of Applied Science and Advanced Technology (11JCZDJC24100), and the EU-funded Environmental Sustainability Program (Contract No. DCI-ASIE/2013/323-550, EuropeAid/133-582/L/ACT/CN).
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Zhang, Y., Lu, X., Wang, N. et al. Heavy metals in aquatic organisms of different trophic levels and their potential human health risk in Bohai Bay, China. Environ Sci Pollut Res 23, 17801–17810 (2016). https://doi.org/10.1007/s11356-016-6948-y
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DOI: https://doi.org/10.1007/s11356-016-6948-y