Environmental Science and Pollution Research

, Volume 25, Issue 21, pp 21127–21137 | Cite as

Evaluating a 5-year metal contamination remediation and the biomonitoring potential of a freshwater gastropod along the Xiangjiang River, China

  • Deliang Li
  • Jie Pi
  • Ting ZhangEmail author
  • Xiang Tan
  • Dylan J. Fraser
Research Article


Effective remediation of heavy metal pollution in aquatic systems is desired in many regions, but it requires integrative assessments of sediments, water, and biota that can serve as robust biomonitors. We assessed the effects of a 5-year metal contamination remediation along the Xiangjiang River, China, by comparing concentrations of trace metals in water and surface sediments between 2010–2011 and 2016. We also explored the trace metal biomonitoring potential of a freshwater gastropod (Bellamya aeruginosa). Metal concentrations in water (means and ranges) dropped over time to within permissible limits of drinking water guidelines set by China, USEPA, and WHO in 2016. Although sediment means and ranges of Cd, Pb, Zn, and Mn also diminished with remediation, those for Cr and Cu slightly increased, and all six metals retained concentrations higher than standards set by China. All metals in sediments could also be associated with anthropogenic inputs using a hierarchical clustering analysis, and they generate high potential ecological risks based on several indices, especially for Cd and As. The bio-sediment accumulation factors of all measured trace metals in gastropod soft tissues and shells were lower than 1.0, except for Ca. Trace metal contents in gastropods were positively correlated with those in water and surface sediments for As (soft tissues) and Cr (shells). Collectively, our results do not yet highlight strong beneficial effects of 5-year remediation and clearly illustrate the heavy metal pollution remaining in Xiangjiang River sediment. Additional physical, chemical, and biological measurements should be implemented to improve sediment quality. We further conclude that gastropod soft tissues and shells can be suitable biomonitors of spatial differences in some heavy metals found within river sediments (e.g., As, Cr).


Bellamya aeruginosa Bioaccumulation Risk assessment Sediment Trace metals 



This study was supported by the Special Fund for Agro-Scientific Research in the Public Interest of China (No. 201503108), A Project Supported by Scientific Research Fund of Hunan Provincial Education Department (No. 17A099) and Open Funding Project of the Key Laboratory of Aquatic Botany and Watershed Ecology, Chinese Academy of Sciences (No. Y752711s03).


  1. Allison PG, Seiter JM, Diaz A, Lindsay JH, Moser RD, Tappero RV, Kennedy AJ (2015) Gastropod (Otala lactea) shell nanomechanical and structural characterization as a biomonitoring tool for dermal and dietary exposure to a model metal. J Mech Behav Biomed Mater 53:142–150CrossRefGoogle Scholar
  2. Anacleto P, Maulvault AL, Nunes ML, Carvalho ML, Rosa R, Marques A (2015) Effects of depuration on metal levels and health status of bivalve molluscs. Food Control 47:493–501CrossRefGoogle Scholar
  3. AQSIQ (2001) Safety qualification for agricultural product—environmental requirements for origin of non-environmental population aquatic products. General Administration of Quality Supervision, Inspection and Quarantine of People’s Republic of China, BeijingGoogle Scholar
  4. Benito D, Niederwanger M, Izagirre U, Dallinger R, Soto M (2017) Successive onset of molecular, cellular and tissue-specific responses in midgut gland of Littorina littorea exposed to sub-lethal cadmium concentrations. Int J Mol Sci 18:1815CrossRefGoogle Scholar
  5. Bo L, Wang D, Li T, Li Y, Zhang G, Wang C, Zhang S (2015) Accumulation and risk assessment of heavy metals in water, sediments, and aquatic organisms in rural rivers in the Taihu Lake region, China. Environ Sci Pollut Res 22:6721–6731CrossRefGoogle Scholar
  6. Bonnail E, Sarmiento AM, DelValls TA, Nieto JM, Riba I (2016) Assessment of metal contamination, bioavailability, toxicity and bioaccumulation in extreme metallic environments (Iberian Pyrite Belt) using Corbicula fluminea. Sci Total Environ 544:1031–1044CrossRefGoogle Scholar
  7. Cheung Y, Wong M (1992) Comparison of trace metal contents of sediments and mussels collected within and outside Tolo Harbour, Hong Kong. Environ Manag 16:743–751CrossRefGoogle Scholar
  8. Fu J, Zhao C, Luo Y, Liu C, Kyzas GZ, Luo Y, Zhao D, An S, Zhu H (2014) Heavy metals in surface sediments of the Jialu River, China: their relations to environmental factors. J Hazard Mater 270:102–109CrossRefGoogle Scholar
  9. Gnatyshyna LL, Fal'fushinskaya GI, Golubev OP, Dallinger R, Stoliar OB (2011) Role of metallothioneins in adaptation of Lymnaea stagnalis (Mollusca: Pulmonata) to environment pollution. Hydrobiol J 47:56–66CrossRefGoogle Scholar
  10. Hakanson L (1980) An ecological risk index for aquatic pollution control. A sedimentological approach. Water Res 14:975–1001CrossRefGoogle Scholar
  11. Hu Z, Liu J, Fu X, Yan H (2007) Study on mollusca of Xiang River trunk stream. Acta Hydrobiol Sin 31:524–531Google Scholar
  12. Kong M, Hang X, Wang L, Yin H, Zhang Y (2016) Accumulation and risk assessment of heavy metals in sediments and zoobenthos (Bellamya aeruginosa and Corbicula fluminea) from Lake Taihu. Water Sci Technol 73:203–214CrossRefGoogle Scholar
  13. Kumar V, Sinha AK, Rodrigues PP, Mubiana VK, Blust R, De Boeck G (2015) Linking environmental heavy metal concentrations and salinity gradients with metal accumulation and their effects: a case study in 3 mussel species of Vitória estuary and Espírito Santo bay, Southeast Brazil. Sci Total Environ 523:1–15CrossRefGoogle Scholar
  14. Li J, Zeng B, Yao Y, Zhang L, Qiu C, Qian X (1986) Studies on environmental background levels in waters of Doting Lake system. Chin J Environ Sci 7:62–68Google Scholar
  15. Li J, Peng F, Ding D, Zhang S, Li D, Zhang T (2011) Characteristics of the phytoplankton community and bioaccumulation of heavy metals during algal blooms in Xiangjiang River (Hunan, China). Sci China Life Sci 54:931–938CrossRefGoogle Scholar
  16. 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 324:105–113CrossRefGoogle Scholar
  17. Liu J, Hu Z (2007) The species composition and diversity of mollusca in the middle reaches of Xiang River. Acta Ecol Sin 27:1153–1160Google Scholar
  18. Liu H, Yang J, Gan J (2010) Trace element accumulation in bivalve mussels Anodonta woodiana from Taihu Lake, China. Arch Environ Contam Toxicol 59:593–601CrossRefGoogle Scholar
  19. Ma T, Gong S, Zhou K, Zhu C, Deng K, Luo Q, Wang Z (2010) Laboratory culture of the freshwater benthic gastropod Bellamya aeruginosa (Reeve) and its utility as a test species for sediment toxicity. J Environ Sci 22:304–313Google Scholar
  20. Ma L, Sun J, Yang Z, Wang L (2015) Heavy metal contamination of agricultural soils affected by mining activities around the Ganxi River in Chenzhou, southern China. Environ Monit Assess 187:1–9CrossRefGoogle Scholar
  21. Ma L, Yang Z, Li L, Wang L (2016) Source identification and risk assessment of heavy metal contaminations in urban soils of Changsha, a mine-impacted city in southern China. Environ Sci Pollut Res 23:17058–17066CrossRefGoogle Scholar
  22. MacDonald DD, Ingersoll CG, Berger TA (2000) Development and evaluation of consensus-based sediment quality guidelines for freshwater ecosystems. Arch Environ Contam Toxicol 39:20–31CrossRefGoogle Scholar
  23. MacFarlane GR, Markich SJ, Linz K, Gifford S, Dunstan RH, O'Connor W, Russell RA (2006) The Akoya pearl oyster shell as an archival monitor of lead exposure. Environ Pollut 143:166–173CrossRefGoogle Scholar
  24. Maher W, Maher N, Taylor A, Krikowa F, Ubrihien R, Mikac KM (2016) The use of the marine gastropod, Cellana tramoserica, as a biomonitor of metal contamination in near shore environments. Environ Monit Assess 188:1–15CrossRefGoogle Scholar
  25. Mao L, Mo D, Guo Y, Fu Q, Yang J, Jia Y (2013) Multivariate analysis of heavy metals in surface sediments from lower reaches of the Xiangjiang River, southern China. Environ Earth Sci 69:765–771CrossRefGoogle Scholar
  26. Markich SJ, Jeffree RA, Burke PT (2002) Freshwater bivalve shells as archival indicators of metal pollution from a copper-uranium mine in tropical northern Australia. Environ Sci Technol 36:821–832CrossRefGoogle Scholar
  27. MOH (2006) Standards for drinking water quality (GB 5749-2006). Ministry of health of the People's Republic of China.Google Scholar
  28. Niederwanger M, Calatayud S, Zerbe O, Atrian S, Albalat R, Capdevila M, Palacios Ò, Dallinger R (2017) Biomphalaria glabrata metallothionein: lacking metal specificity of the protein and missing gene upregulation suggest metal sequestration by exchange instead of through selective binding. Int J Mol Sci 18:1457CrossRefGoogle Scholar
  29. Pi J, Li X, Zhang T, Li D (2016) Effects of acute exposure to sublethal waterborne cadmium on energy homeostasis in silver carp (Hypophthalmichthys molitrix). Bull Environ Contam Toxicol 97:497–503CrossRefGoogle Scholar
  30. Protasowicki M, Dural M, Jaremek J (2008) Trace metals in the shells of blue mussels (Mytilus edulis) from the Poland Coast of Baltic sea. Environ Monit Assess 141:329–337CrossRefGoogle Scholar
  31. Rainbow, Dallinger (1993) Metal uptake, elimination and regulation in freshwater invertebrates. In: Dallinger R, Rainbow PS (eds) Ecotoxicology of metals in invertebrates. Lewis Publishers, Boca Raton, pp 119–131Google Scholar
  32. Rzymski P, Niedzielski P, Klimaszyk P, Poniedziałek B (2014) Bioaccumulation of selected metals in bivalves (Unionidae) and Phragmites australis inhabiting a municipal water reservoir. Environ Monit Assess 186:3199–3212CrossRefGoogle Scholar
  33. Shoults-Wilson WA, Elsayed N, Leckrone K, Unrine J (2014) Zebra mussels (Dreissena polymorpha) as a biomonitor of trace elements along the southern shoreline of Lake Michigan. Environ Toxicol Chem 34:412–419CrossRefGoogle Scholar
  34. Szefer P, Ali AA, Ba-Haroon AA, Rajeh AA, Geldon J, Nabrzyski M (1999) Distribution and relationships of selected trace metals in molluscs and associated sediments from the Gulf of Aden, Yemen. Environ Pollut 106:299–314CrossRefGoogle Scholar
  35. Szefer P, Frelek K, Szefer K, Lee CB, Kim BS, Warzocha JW, Zdrojewska I, Ciesielski T (2002) Distribution and relationships of trace metals in soft tissue, byssus and shells of Mytilus edulis trossulus from the southern Baltic. Environ Pollut 120:423–444CrossRefGoogle Scholar
  36. Taylor AM, Edge KJ, Ubrihien RP, Maher WA (2017) The freshwater bivalve Corbicula australis as a sentinel species for metal toxicity assessment: an in situ case study integrating chemical and biomarker analyses. Environ Toxicol Chem 36:709–719CrossRefGoogle Scholar
  37. Ubrihien RP, Taylor AM, Maher WA (2017) Bioaccumulation, oxidative stress and cellular damage in the intertidal gastropod Bembicium nanum exposed to a metal contamination gradient. Mar Freshw Res 68:922–930CrossRefGoogle Scholar
  38. USEPA (2009) Drinking water standards and health advisories. EPA 822-R-09-011 office of water. U.S. Environmental Protection Agency, Washington.Google Scholar
  39. WHO (2008) Guidelines for drinking-water quality, recommendations incorporating 1st and 2nd Addenda, 13th edn. World Health Organization, Geneva.Google Scholar
  40. Yap CK, Ismail A, Tan SG, Abdul Rahim I (2003) Can the shell of the green-lipped mussel Perna viridis from the west coast of Peninsular Malaysia be a potential biomonitoring material for Cd, Pb and Zn ? Estuar Coast Shelf Sci 57:623–630CrossRefGoogle Scholar
  41. Yap CK, Cheng WH, Karami A, Ismail A (2016) Health risk assessments of heavy metal exposure via consumption of marine mussels collected from anthropogenic sites. Sci Total Environ 553:285–296CrossRefGoogle Scholar
  42. Zeng X, Liu Y, You S, Zeng G, Tan X, Hu X, Hu X, Huang L, Li F (2015) Spatial distribution, health risk assessment and statistical source identification of the trace elements in surface water from the Xiangjiang River, China. Environ Sci Pollut Res 22:9400–9412CrossRefGoogle Scholar
  43. Zhang Q, Li Z, Zeng G, Li J, Fang Y, Yuan Q, Wang Y, Ye F (2009) Assessment of surface water quality using multivariate statistical techniques in red soil hilly region: a case study of Xiangjiang watershed, China. Environ Monit Assess 152:123–131CrossRefGoogle Scholar
  44. Zhang T, Zhang Y, Li DL, Xiao TY, Li J (2013) Exposure of silver carp (Hypophthalmichthys molitrix) to environmentally relevant levels of cadmium: hematology, muscle physiology, and implications for stock enhancement in the Xiangjiang River (Hunan, China). Sci China Life Sci 56:66–72CrossRefGoogle Scholar
  45. Zhou Q, Zhang J, Fu J, Shi J, Jiang G (2008) Biomonitoring: an appealing tool for assessment of metal pollution in the aquatic ecosystem. Anal Chim Acta 606:135–150CrossRefGoogle Scholar
  46. Zuykov M, Pelletier E, Harper DAT (2013) Bivalve mollusks in metal pollution studies: from bioaccumulation to biomonitoring. Chemosphere 93:201–208CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Collaborative Innovation Center for Efficient and Health Production of Fisheries in Hunan Province, Hunan Engineering Technology Research Center of Featured Aquatic Resources Utilization, College of Animal Science and TechnologyHunan Agricultural UniversityChangshaPeople’s Republic of China
  2. 2.College of Chemistry and Chemical EngineeringCentral South UniversityChangshaPeople’s Republic of China
  3. 3.Key Laboratory of Aquatic Botany and Watershed EcologyWuhan Botanical Garden the Chinese Academy of SciencesWuhanPeople’s Republic of China
  4. 4.Department of BiologyConcordia UniversityMontréalCanada

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