Comprehensive assessments of ecological states of Songhua River using chemical analysis and bivalves as bioindicators

  • Victoria V. Zarykhta
  • Zhaohan ZhangEmail author
  • Sergey V. Kholodkevich
  • Tatiana V. Kuznetsova
  • Andrey N. Sharov
  • Yu Zhang
  • Kai Sun
  • Miao Lv
  • Yujie Feng
Research Article


The aim of this study was to compare environmental pollution and ecological states of two different areas of the Songhua River areas: near Harbin City and Tongjiang City, located at a distance of about 500 km downstream. The anthropogenic pollution concentrations of heavy metals (HM) were determined. The results showed that concentrations of eight metals (Cd, Cr, Cu, Fe, Mn, Ni, Pb, and Zn) in the water were in the range of 0.001–0.588 mg/L for Tongjiang and 0.001–0.508 mg/L for Harbin, while that in sediments were in the range of 0.67–1575.37 mg/kg for Tongjiang and 0.07–5617.13 mg/kg for Harbin, respectively. Bivalves from tested sites exposed to environmental pollution exhibited significantly different physiological states. The latter was assessed using the method of physiological loading, based on measuring the recovery time (Trec) of heart rate (HR) after removal of the load. Trec in mussels from Harbin was recorded in the range of 151 to 234 min, while that from Tongjiang was only 115 min. Cd, Cu, Pb, and Zn in mollusk soft tissues were also determined for Harbin and Tongjiang, respectively. The metal pollution index (MPI) and bioconcentration factor (BCF) in the mollusks were calculated for each metal. BCF in the mussels from the Tongjiang area was lower than that from the Harbin area. Physiological testing, as well as the concentration of HM in water, and sediment, and also the bioaccumulation of HM in tissue showed that the ecological state of the Tongjiang area was better than that of Harbin. Apparently, after more extensive studies, a methodological approach of assessing the ecological state of water areas, based on physiological state testing of aboriginal mollusks, could be used in the monitoring of pollution effects in water bodies and streams.


Environmental quality Heavy metals Mussels as bioindicators Cardiac activity Metal pollution index 



This project was supported by National Key Research and Development Program of China (2017YFA0207204), Heilongjiang Province Natural Science Foundation (LH2019E042), and the Nanqi Ren Studio, Academy of Environment and Ecology, Harbin Institute of Technology (HSCJ201707). The authors also acknowledged the support of the Innovation Team in Key Areas of the Ministry of Science and Technology.

Supplementary material

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  1. Ahn IY, Kang J, Kim KW (2001) The effect of body size on metal accumulations in the bivalve Laternula elliptica. Antarct Sci 13:355–362CrossRefGoogle Scholar
  2. Aouini F, Trombini C, Volland M, Elcafsi M, Blasco J (2018) Assessing lead toxicity in the clam Ruditapes philippinarum: bioaccumulation and biochemical responses. Ecotoxicol Environ Saf 158:193–203CrossRefGoogle Scholar
  3. Arini A, Daffe G, Gonzalez P, Feurtet-Mazel A, Baudrimont M (2014) Detoxification and recovery capacities of Corbicula fluminea after an industrial metal contamination (Cd and Zn): a one-year depuration experiment. Environ Pollut 192:74–82CrossRefGoogle Scholar
  4. Bakhmet IN, Sazhin A, Maximovich N, Ekimov D (2018): In situ long-term monitoring of cardiac activity of two bivalve species from the White Sea, the blue mussel Mytilus edulis and horse mussel Modiolus modiolus. Journal of the Marine Biological Association of the United Kingdom, 1–8Google Scholar
  5. Bamber SD, Depledge MH (1997) Evaluation of changes in the adaptive physiology of shore crabs (Carcinus maenas) as an indicator of pollution in estuarine environments. Mar Biol 129:667–672CrossRefGoogle Scholar
  6. Belabed S, Soltani N (2018): Effects of cadmium concentrations on bioaccumulation and depuration in the marine bivalve Donax trunculus. Euro-Mediterranean Journal for Environmental Integration 19Google Scholar
  7. Ben-Khedher S, Jebali J, Kamel N, Banni M, Rameh M, Jrad A, Boussetta H (2013) Biochemical effects in crabs (Carcinus maenas) and contamination levels in the Bizerta lagoon: an integrated approach in biomonitoring of marine complex pollution. Environ Sci Pollut R 20:2616–2631CrossRefGoogle Scholar
  8. Company R, Serafim A, Cosson RP, Fiala-Medioni A, Camus L, Colaco A, Serrao-Santos R, Bebianno MJ (2008) Antioxidant biochemical responses to long-term copper exposure in Bathymodiolus azoricus from Menez-Gwen hydrothermal vent. Sci Total Environ 389:407–417CrossRefGoogle Scholar
  9. Depledge MH, Galloway TS (2005) Healthy animals, healthy ecosystems. Front Ecol Environ 3:251–258CrossRefGoogle Scholar
  10. El-Shenawy NS, Loutfy N, Soliman MF, Tadros MM, Abd El-Azeez AA (2016) Metals bioaccumulation in two edible bivalves and health risk assessment. Environ Monit Assess 188:139CrossRefGoogle Scholar
  11. Fedotov VP, Kholodkevich SV, Strochilo AG (2000) Study of contractile activity of the crayfish heart with the aid of a new non-invasive technique. J Evol Biochem Physiol 36:288–293CrossRefGoogle Scholar
  12. Fu J, Zhao CP, Luo YP, Liu CS, Kyzas GZ, Luo Y, Zhao DY, An SQ, Zhu HL (2014) Heavy metals in surface sediments of the Jialu River, China: their relations to environmental factors. J Hazard Mater 270:102–109CrossRefGoogle Scholar
  13. Habte G, Choi JY, Nho EY, Oh SY, Khan N, Choi H, Park KS, Kim KS (2015) Determination of toxic heavy metal levels in commonly consumed species of shrimp and shellfish using ICP-MS/OES. Food Sci Biotechnol 24:373–378CrossRefGoogle Scholar
  14. Handy RD, Depledge MH (1999) Physiological responses: their measurement and use as environmental biomarkers in ecotoxicology. Ecotoxicology 8:329–349CrossRefGoogle Scholar
  15. Jarvis KE, Gray AL, Houk RS (1997): Handbook of inductively coupled plasma mass spectrometry. United Kingdom Google Scholar
  16. Jia YY, Wang L, Qu ZP, Yang ZG (2018) Distribution, contamination and accumulation of heavy metals in water, sediments, and freshwater shellfish from Liuyang River, southern China. Environ Sci Pollut R 25:7012–7020CrossRefGoogle Scholar
  17. Jones WG, Walker FK (1979) Accumulation of Iron, manganese, zinc and cadmium by the Australian freshwater mussel Velesunio ambiguus (Phillipi) and its potential as a biological monitor. Mar Freshw Res 30:741–751CrossRefGoogle Scholar
  18. Kesavan K, Murugan A, Venkatesan V, Kumar V (2013) Heavy metal accumulation in molluscs and sediment from uppanar estuary, southeast coast of India. Int J Mar Sci 29:15–21Google Scholar
  19. Khlebovich VV (2007): Levels of homeostasis. Priroda (Moscow), 61–65 (in Russian, English summary)Google Scholar
  20. Kholodkevich SV, Kuznetsova TV, Trusevich VV, Kurakin AS, Ivanov AV (2009) Peculiarities of valve movement and of cardiac activity of the bivalve Mollusc Mytilus galloprovincialis at various stress actions. J Evol. Biochem Phys+ 45:524–526Google Scholar
  21. Kholodkevich SV, Kuznetsova TV, Lehtonen KK, Kurakin AS (2011):Experiences on ecological status assessment of the Gulf of Bothnia different sites based on cardiac activity biomarkers of caged mussels (Mytilusedulis) ICES Annual Science Conference 2011, 12 pGoogle Scholar
  22. Kholodkevich SV, Ivanov AV, Trusevich VV, Kuznetsova TV (2012): Ecotoxicological biomarker for bioindication of aquatic ecosystem state based on evaluation of adaptive capacity of bivalve mollusks living there Doklady National Academy of Sciences of Ukraine, P.138-142 (in Russian) Google Scholar
  23. Kholodkevich SV, Ivanov AV, Kornienko EL, Kurakin AS (2013): Method of biological environment monitoring (versions) and a system for realization thereof : US Pat. № 8442809. — 05.14.2013Google Scholar
  24. Kholodkevich SV, Sharov AN, Kuznetsova TV (2015): Perspectives and problems of application of bioelectronic systems for monitoring of environmental safety state in the Gulf of Finland aquatoria. Regional ecology, 16–26Google Scholar
  25. Kholodkevich SV, Kuznetsova TV, Sharov AN, Kurakin AS, Lips U, Kolesova N, Lehtonen KK (2017) Applicability of a bioelectronic cardiac monitoring system for the detection of biological effects of pollution in bioindicator species in the Gulf of Finland. J Mar Syst 171:151–158CrossRefGoogle Scholar
  26. Kuklina I, Kouba A, Kozak P (2013) Real-time monitoring of water quality using fish and crayfish as bio-indicators: a review. Environ Monit Assess 185:5043–5053CrossRefGoogle Scholar
  27. Kuznetsova TV (2013) Change of salinity of medium as a function loading in estimating functional state of the crayfish Astacus leptodactylus. J Evol Biochem Physiol 49:498–502CrossRefGoogle Scholar
  28. Kuznetsova TV, Kholodkevich SV (2015): Comparative assessment of surface water quality through evaluation of physiological state of bioindicator species: searching a new biomarkers. 4th Mediterranean conference on embedded computing (Meco), 339-344Google Scholar
  29. Kuznetsova TV, Kholodkevich SV, Kurakin AS (2018): Experience on ecological status assessment based on adaptive potential diagnostics in selected invertebrates of the Baltic Sea sub-regions. Fundamental and Applied Hydrophysics, 75-85Google Scholar
  30. Makarenko TV, Koval YV (2014): Heavy metals in the soft tissues and shells of freshwater mollusks of different classes. Actual problems of ecology and preservation of bloodiest in Russia and adjacent countries, 129–132Google Scholar
  31. Mendoza-Carranza M, Sepulveda-Lozada A, Dias-Ferreira C, Geissen V (2016) Distribution and bioconcentration of heavy metals in a tropical aquatic food web: a case study of a tropical estuarine lagoon in SE Mexico. Environ Pollut 210:155–165CrossRefGoogle Scholar
  32. Moor C, Lymberopoulou T, Dietrich VJ (2001): Determination of heavy metals in soils, Sediments and Geological Materials by ICP-AES and ICP-MS Mikrochim Acta, 123–128Google Scholar
  33. Ponnusamy K, Sivaperumal P, Suresh M, Arularasan S, Munilkumar S, Pal AK (2014): Heavy metal concentration from biologically important edible species of bivalves (Perna viridis and Modiolus metcalfei) from Vellar Estuary, South East Coast of India. Journal of aquaculture Research and Development, 258Google Scholar
  34. Pourang N, Dennis JH, Ghourchian H (2005) Distribution of heavy metals in Penaeus Semisulcatus from Persian gulf and possible role of metallothionein in their redistribution during storage. Environ Monit Assess 100:71–88CrossRefGoogle Scholar
  35. Sarmiento AM, Bonnail E, Nieto JM, DelValls A (2016) Bioavailability and toxicity of metals from a contaminated sediment by acid mine drainage: linking exposure-response relationships of the freshwater bivalve Corbicula fluminea to contaminated sediment. Environ Sci Pollut R 23:22957–22967CrossRefGoogle Scholar
  36. Sohail M, Khan MN, Chaudhry AS, Qureshi NA (2016) Bioaccumulation of heavy metals and analysis of mineral element alongside proximate composition in foot, gills and mantle of freshwater mussels (Anodonta anatina). Rend Lincei-Sci Fis 27:687–696CrossRefGoogle Scholar
  37. Soldatov AA, Gostyukhina OL, Golovina IV (2014) Functional states of antioxidant enzymatic complex of tissues of Mytillus galloprovincialis Lam. Under conditions of oxidative stress. J Evol Biochem Physiol 50:206–214CrossRefGoogle Scholar
  38. Tanabe S, Subramanian A (2003): Biomarkers and analytical methods for the analysis of POPs in developing countries. STAP/GEF and Ministry of Environment, Government of Japan (sponsored) STAP workshop on the use of bioindicators, 1Google Scholar
  39. Turja R, Hoher N, Snoeijs P, Barsiene J, Butrimaviciene L, Kuznetsova T, Kholodkevich SV, Devier MH, Budzinski H, Lehtonen KK (2014) A multibiomarker approach to the assessment of pollution impacts in two Baltic Sea coastal areas in Sweden using caged mussels (Mytilus trossulus). Sci Total Environ 473:398–409CrossRefGoogle Scholar
  40. Usero J, GonzalezRegalado E, Gracia I (1997) Trace metals in the bivalve molluscs Ruditapes decussatus and Ruditapes philippinarum from the Atlantic Coast of Southern Spain. Environ Int 23:291–298CrossRefGoogle Scholar
  41. Usero J, Morillo J, Gracia I (2005) Heavy metal concentrations in molluscs from the Atlantic coast of southern Spain. Chemosphere 59:1175–1181CrossRefGoogle Scholar
  42. Wang WX, Lu GY (2017): Heavy metals in bivalve mollusks. Chemical contaminants and residues in food, 553–594Google Scholar
  43. White SL, Rainbow PS (1986): A preliminary study of Cu-, Cd- and Zn- binding components in the Hepatopancreas of Palaeman elegans (Crustacea: Decapoda). Compar Biochem Physiol, 111-116Google Scholar
  44. Wu SD, Zhao HF (2006): The analytical methods in the monitoring of water and wastewater. China Environmental Science PressGoogle Scholar
  45. Zhou QF, Zhang JB, Fu JJ, Shi JB, Jiang GB (2008) Biomonitoring: An appealing tool for assessment of metal pollution in the aquatic ecosystem. Anal Chim Acta 606:135–150CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.State Key Laboratory of Urban Water Resource and Environment, School of EnvironmentHarbin Institute of TechnologyHarbinChina
  2. 2.St.Petersburg State UniversitySt. PetersburgRussia
  3. 3.St.Petersburg Scientific-Research Center for Ecological Safety RASSt. PetersburgRussia

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