Abstract
Despite their proven reliability for revealing ‘acceptable’ degrees of toxicity in waste- and reclaimed waters, bioassays are rarely used to assess the toxicity of hazardous contaminants present in natural waters. In this study, we used organisms from different trophic levels to assess the toxicity of water samples collected from four different South Korean rivers. The main objective was to develop a multi-descriptor index of toxicity for undiluted river water. The responses of six test organisms (Aliivibrio fischeri, Pseudokirchneriella subcapitata, Heterocypris incongruens, Moina macrocopa, Danio rerio and Lemna minor) after laboratory exposure to water samples were considered for this index, as well as the frequency of teratologies in diatom assemblages. Each individual test was attributed a toxicity class and score (three levels; no toxicity = 0, low toxicity = 1, confirmed toxicity = 2) based on the organism’s response after exposure and a total score was calculated. The proposed index also considers the number of test organisms that received the highest toxicity score (value = 2). An overall toxicity category was then attributed to the water sample based on those two metrics: A = no toxicity, B = slight toxicity, C = moderate toxicity; D = toxicity and E = high toxicity. The susceptibility of the test organisms varied greatly and the sensitivity of their response also differed among bioassays. The combined responses of organisms from different trophic levels and with different life strategies provided multi-level diagnostic information about the intensity and the nature of contamination.
Similar content being viewed by others
References
Ahlf, W., Hollert, H., Neumann-Hensel, H., & Ricking, M. (2002). A guidance for the assessment and evaluation of sediment quality: a German approach based on ecotoxicological and chemical measurements. Journal of Soils and Sediments, 2, 37–42.
Angerville, R. (2009). Evaluation des risques écotoxicologiques liés au déversement de rejets urbains par temps de pluie (RUTP) dans les cours d’eau : application à une ville française et à une ville haïtienne. Chemical Sciences. INSA de Lyon, in French.
Angerville, R., Perrodin, Y., Bazin, C., & Emmanuel, E. (2013). Evaluation of ecotoxicological risks related to the discharge of combined sewer overflows (CSOs) in a periurban river. International Journal of Environmental Research and Public Health, 10, 2670–2687.
Ankley, G. T., Schubauer-Berigan, M. K., & Hoke, R. A. (1992). Use of toxicity identification evaluation techniques to identify dredged material disposal options: a proposed approach. Environmental Management, 16, 1–6.
Arini, A., Feurtet-Mazel, A., Maury-Brachet, R., Pokrovsky, O. S., Coste, M., & Delmas, F. (2012). Recovery potential of periphytic biofilms translocated in artificial streams after industrial contamination (Cd and Zn). Ecotoxicology, 21, 1403–1414.
Backhaus, T., Froehner, K., Altenburger, R., & Grimme, L. H. (1997). Toxicity testing with Vibrio fischeri: a comparison between the long term (24 h) and the short term (30 min) bioassay. Chemosphere, 35, 2925–2938.
Becouze-Lareure, C., Thiebaud, L., Bazin, C., Namour, P., Breil, P., & Perrodin, Y. (2016). Dynamics of toxicity within different compartments of a peri-urban river subject to combined sewer overflow discharges. Science of the Total Environment, 539, 503–514.
Bresch, H. (1991). Early life-stage in zebrafish versus a growth test in rainbow trout to evaluate toxic effects. Bulletin of Environmental Contamination and Toxicology, 46, 641–648.
Calabrese, E. J. (2005). Paradigm lost, paradigm found: The re-emergence of hormesis as a fundamental dose response model in the toxicological sciences. Environmental Pollution, 138, 378–411.
Canesi, L., & Corsi, I. (2016). Effects of nanomaterials on marine invertebrates. Science of the Total Environment, 565, 933–940.
Cerisier, A., Vedrenne, J., Lavoie, I., & Morin, S. (2018). Assessing the severity of diatom deformities using geometric morphometry. Botany Letters, 1–9.
Chial, Z. B., & Persoone, G. (2002a). Cyst-based toxicity tests XII—development of a short chronic sediment toxicity test with the ostracod crustacean Heterocypris incongruens: selection of test parameters. Environmental Toxicology, 17, 520–527.
Chial, Z. B., & Persoone, G. (2002b). Cyst-based toxicity tests XIV—application of the ostracod solid-phase microbiotest for toxicity monitoring of river sediments in Flanders (Belgium). Environmental Toxicology, 17, 533–537.
Cho, E., Khim, J., Chung, S., Seo, D., & Son, Y. (2014). Occurrence of micropollutants in four major rivers in Korea. Science of the Total Environment, 491-492, 138–147.
Chu, K. W., & Chow, K. L. (2002). Synergistic toxicity of multiple heavy metals is revealed by a biological assay using a nematode and its transgenic derivative. Aquatic Toxicology, 6, 53–64.
Coste, M., Boutry, S., Tison-Rosebery, J., & Delmas, F. (2009). Improvements of the Biological Diatom Index (BDI): description and efficiency of the new version (BDI-2006). Ecological Indicators, 9, 621–650.
Davis, J. A. (1981). Comparison of static-replacement and flow through bioassays using duckweed, Lemna gibba G3.EPA 560/6-81-003. Washington, DC: United States Environmental Protection Agency.
Elendt, B.-P. (1990). Selenium deficiency in Crustacea; an ultrastructural approach to antennal damage in Daphnia magna Straus. Protoplasma, 154, 25–33.
Environment Canada. (1992). Biological test method: growth inhibition test using the freshwater alga Selenastrum capricornutum. Report EPS 1/RM/25. Ottawa: Environment Canada.
Fulladosa, E., Murat, J. C., & Villaescusa, I. (2005). Effect of cadmium(II), chromium(VI), and arsenic(V) on long-term viability and growth-inhibition assays using Vibrio fischeri marine bacteria. Archives of Environmental Contamination and Toxicology, 49, 299–306.
Fulladosa, E., Murat, J. C., Bollinger, J. C., & Villaescusa, I. (2007). Adverse effects of organic arsenical compounds towards Vibrio fischeri bacteria. Science of the Total Environment, 377, 207–213.
Geiszinger, A., Bonnineau, C., Faggiano, L., Guasch, H., López-Doval, J. C., Proia, L., Ricart, M., Ricciardi, F., Romaní, A., Rotter, S., Muñoz, I., Schmitt-Jansen, M., & Sabater, S. (2009). The relevance of the community approach linking chemical and biological analyses in pollution assessment. Trends in Analytical Chemistry, 28, 619–626.
Gonzalez-Merchan, C., Perrodin, Y., Barraud, S., Sébastian, C., Becouze-Lareure, C., & Bazin, C. (2014a). Spatial variability of sediment ecotoxicity into a large storm water detention basin. Environmental Science and Pollution Research, 21, 5357–5366.
Gonzalez-Merchan, C., Perrodin, Y., Sébastian, C., Bazin, C., Winiarski, T., & Barraud, S. (2014b). Ecotoxicological characterization of sediments from storm water retention basins. Water Science and Technology, 69, 1045–1051.
Gopalapillai, Y., Vigneault, B., & Hale, B. A. (2014). Root length of aquatic plant, Lemna minor L., as an optimal toxicity endpoint for biomonitoring of mining effluents. Integrated Environmental Assessment and Management, 10, 493–497.
Hassan, I., Jabir, N. R., Ahmad, S., Shah, A., & Tabrez, S. (2015). Certain phase I and phase II enzymes as toxicity biomarker: an overview. Water, Air, and Soil Pollution, 226, 153.
Hsieh, C.-Y., Tsai, M.-H., Ryan, D. K., & Pancorbo, O. C. (2004). Toxicity of the 13 priority pollutant metals to Vibrio fisheri in the Microtox chronic toxicity test. Science of the Total Environment, 320, 37–50.
Hwang, S.-J., Lee, S.-W., & Park, Y.-S. (2011). Ecological monitoring, assessment, and restoration of running waters in Korea. International Journal of Limnology: Annales de Limnologie, 47, S1–S2.
ISO. (2009). Water quality—determination of the inhibitory effect of water samples on the light emission of Vibrio fischeri (Luminescent bacteria test)—part1: method using freshly prepared bacteria. ISO 11348-1.
ISO. (2012). Water quality—determination of fresh watersediment toxicity to Heterocypris incongruens (Crustacea, Ostracoda). ISO 14371.
Ji, K., Kim, Y., Oh, S., Ahn, B., Jo, H., & Choi, K. (2008). Toxicity of Perfluorooctanoic acid on freshwater macro invertebrates (Daphnia magna and Moina macrocopa) and fish (Oryzia slatipes). Environmental Toxicology and Chemistry, 27, 2159–2168.
Joy, M. K., & Death, R. G. (2002). Predictive modelling of freshwater fish as a biomonitoring tool in New Zealand. Freshwater Biology, 47, 2261–2275.
Katsumata, M., Koike, T., Nishikawa, M., Kazumura, K., & Tsuchiya, H. (2006). Rapid ecotoxicological bioassay using delayed fluorescence in the green alga Pseudokirchneriella subcapitata. Water Research, 40, 3393–3400.
Kelly, M. (2013). Building capacity for ecological assessment using diatoms in UK rivers. Journal of Ecology and Environment, 36, 89–94.
Kim Tiam, S., Fauvelle, V., Morin, S., & Mazzella, N. (2016). Improving toxicity assessment of pesticide mixtures: the use of polar passive sampling devices extracts in microalgae toxicity tests. Frontiers in Microbiology, 7, 1388.
Kim, S. B., Kim, W. K., Chounlamany, V., Seo, J., Yoo, J., Jo, H. J., & Jung, J. (2012). Identification of multi-level toxicity of liquid crystal display wastewater toward Daphnia magna and Moina macrocopa. Journal of Hazardous Materials, 227–228, 327–333.
Kim, Y.-J., Han, Y.-S., Kim, E., Jung, J., Kim, S.-H., Yoo, S.-J., Shin, G.-S., Oh, J.-J., Park, A., Choi, H., Kim, M.-S., Brown, M. T., & Han, T. (2015). Application of the Ulva pertusa bioassay for a toxicity identification evaluation and reduction of effluent from a wastewater treatment plant. Frontiers in Environmental Science, 3, 1–9.
Lainé, M., Morin, S., & Tison-Rosebery, J. (2014). A multicompartment approach—diatoms, macrophytes, benthic macro-invertebrates and fish-to assess the impact of toxic industrial releases on a small French river. PLoS One, 9, e102358.
Lavoie, I., Campeau, S., Zugic-Drakulic, N., Winter, J. G., & Fortin, C. (2014). Using diatoms to monitor stream biological integrity in Eastern Canada: an overview of 10years of index development and ongoing challenges. Science of the Total Environment, 475, 187–200.
Lavoie, I., Hamilton, P., Morin, S., Kim Tiam, S., Gonçalves, S., Falasco, E., Fortin, C., Gontero, B., Heudre, D., Kahlert, M., Kojadinovic-Sirinelli, M., Manoylov, K., Pandey, L. K., & Taylor, J. (2017). Diatom teratologies as biomarkers of contamination: are all deformities ecologically meaningful? Ecological Indicators, 82, 539–550.
Lavoie, I., Lavoie, M., & Fortin, C. (2012). A mine of information: benthic algal communities as biomonitors of metal contamination from abandoned tailings. Science of the Total Environment, 425, 231–241.
Lento, J., Dillon, P. J., Somers, K. M., & Reid, R. A. (2008). Changes in littoral benthic macroinvertebrate communities in relation to water chemistry in 17 Precambrian Shield lakes. Canadian Journal of Fisheries and Aquatic Sciences, 65, 906–918.
Li, L., Zheng, B., & Liu, L. (2010). Biomonitoring and bioindicators used for river ecosystems: definitions, approaches and trends. Procedia Environmental Sciences, 2, 1510–1524.
Macken, A., Giltrap, M., Ryall, K., Foley, B., McGovern, E., McHugh, B., & Davoren, M. (2009). A test battery approach to the ecotoxicological evaluation of cadmium and copper employing a battery of marine bioassays. Ecotoxicology, 18, 470–480.
Mankiewicz-Boczek, J., Naɭecz-Jawecki, G., Drobniewska, A., Kaza, M., Sumorok, B., Izydorczyk, K., Zalewski, M., & Sawicki, J. (2008). Application of a microbiotests battery for complete toxicity assessment of rivers. Ecotoxicology and Environmental Safety, 71, 830–836.
Marzin, A., Archaimbault, V., Belliard, J., Chauvin, C., Delmas, F., & Pont, D. (2012). Ecological assessment of running waters: Do macrophytes, macroinvertebrates, diatoms and fish show similar responses to human pressures? Ecological Indicators 23,56–65.
M.O.E. Korea. (2007). Toxicity identification of ecological risk hazards in the waste waters around the industrial complex from 2015. Osong: Ministry of Environment.
Moreira-Santos, M., Soares, A. M. V. M., & Ribeiro, R. (2004). An in situ bioassay for freshwater environments with the microalga Pseudokirchneriella subcapitata. Ecotoxicology and Environmental Safety, 59, 164–173.
Morin, S., Duong, T. T., Dabrin, A., Coynel, A., Herlory, O., Baudrimont, M., Delmas, F., Durrieu, G., Schäfer, J., Winterton, P., Blanc, G., & Coste, M. (2008a). Long-term survey of heavy-metal pollution, biofilm contamination and diatom community structure in the Riou Mort watershed, South-West France. Environmental Pollution, 151, 532–542.
Morin, S., Duong, T. T., Boutry, S., & Coste, M. (2008b). Mitigation of metal toxicity to freshwater biofilms development (Decazeville watershed, SW France). Cryptogamie Algologie, 29, 201–216.
Morin, S., Cordonier, A., Lavoie, I., Arini, A., Blanco, S., Duong, T. T., Tornés, E., Bonet, B., Corcoll, N., Faggiano, L., Laviale, M., Pérès, F., Becares, E., Coste, M., Feurtet-Mazel, A., Fortin, C., Guasch, H., & Sabater, S. (2012). Consistency in diatom response to metal-contaminated environments. In H. Guasch, A. Ginebreda, & A. Geiszinger (Eds.), Emerging and priority pollutants in rivers (pp. 117–146). Berlin: Springer-Verlag.
Nedeau, E. J., Merritt, R. W., & Kaufman, M. G. (2003). The effect of an industrial effluent on an urban stream benthic community: water quality vs. habitat quality. Environmental Pollution, 123, 1–13.
Nichols, H. W. (1973). Growth media. Freshwater. In J. R. Stein (Ed.), Handbook of phycological methods. Culture Methods and Growth measurements (pp. 7–24). London: Cambridge University Press.
Niemirycz, E., Nichthauser, J., Staniszewska, M., Nałęcz-Jawecki, G., & Bolałek, J. (2007). The Microtox® biological test: application in toxicity evaluation of surface waters and sediments in Poland. Oceanological and Hydrobiological Studies, 36, 151–163.
Ntengwe, F. W., & Maseka, K. K. (2006). The impact of effluents containing zinc and nickel metals on stream and river waterbodies: the case of Chambishi and Mwambashi streams in Zambia. Physics and Chemistry of the Earth, 31, 814–820.
Oberdorff, T., Pont, D., Hugeny, B., & Porcher, J. P. (2002). Development and validation of a fish-based index (FBI) for the assessment of “river health” in France. Freshwater Biology, 47, 1720–1734.
OECD. (1984). Alga, growth inhibition test. In: OECD guideline for testing of chemicals, Vol. 201, Paris.
OECD. (2012). Daphnia magna reproduction test. In: OECD guideline for the testing of chemicals, Vol. 211, Paris.
OECD. (2013). Fish embryo acute toxicity (FET) test. In: OECD guidelines for the testing of chemicals, Vol. 236, Paris.
Panda, S. K., & Upadhyay, R. K. (2003). Salt stress injury induces oxidative alteration and antioxidative defense in the roots of Lemna minor. Biologia Plantarum, 48, 249–253.
Pandard, P., Devillers, J., Charissou, A.-M., Poulsen, V., Jourdain, M.-J., Férard, J.-F., Grand, C., & Bispo, A. (2006). Selecting a battery of bioassays for ecotoxicological characterization of wastes. Science of the Total Environment, 363, 114–125.
Pandey, L. K., & Bergey, E. A. (2016). Exploring the status of motility, lipid bodies, deformities and size reduction in periphytic diatom community from chronically metal (Cu, Zn) polluted waterbodies as a biomonitoring tool. Science of the Total Environment, 550, 372–381.
Pandey, L. K., Han, T., & Gaur, J. P. (2015). Response of a phytoplanktonic assemblage to copper and zinc enrichment in microcosm. Ecotoxicology 24, 573–582.
Pandey, L. K., Kumar, D., Yadav, A., Rai, J., & Gaur, J. P. (2014). Morphological abnormalities in periphytic diatoms as a tool for biomonitoring of heavy metal pollution in a river. Ecological Indicators, 36, 272–279.
Pandey, L. K., Lavoie, I., Morin, S., Park, J., Jie, L., Choi, S., Lee, H., & Han, T. (2018). River water quality assessment based on a multi-descriptor approach including chemistry, diatom assemblage structure, and non-taxonomical diatom metrics. Ecological Indicators, 84, 140–151.
Park, A., Kim, Y., Choi, E., Brown, M. T., & Han, T. (2013). A novel bioassay using root re-growth in Lemna. Aquatic Toxicology, 140–141, 415–424.
Park, J., Brown, M. T., Depuydt, S., Kim, J. K., Won, D.-S., & Han, T. (2017). Comparing the acute sensitivity of growth and photosynthetic endpoints in three Lemna species exposed to four herbicides. Environmental Pollution, 220, 818–827.
Parvez, S., Venkataraman, C., & Mukherji, S. (2006). A review on advantages of implementing luminescence inhibition test (Vibrio fischeri) for acute toxicity prediction of chemicals. Environment International, 32, 265–268.
Persoone, G., Marsalek, B., Blinova, I., Andrea Tӧrӧkne, A., Zarina, D., Manusadzianas, L., Nalecz-Jawecki, G., Tofan, L., Stepanova, N., Tothova, L., & Kolar, B. (2003). A practical and user-friendly toxicity classification system with microbiotests for natural waters and wastewaters. Environmental Toxicology, 18, 395–402.
Ponader, K. C., Charles, D. F., & Belton, T. J. (2007). Diatom-based TP and TN inference models and indices for monitoring nutrient enrichment of New Jersey streams. Ecological Indicators, 7, 79–93.
Radix, P., Léonard, M., Papantoniou, C., Roman, G., Saouter, E., Gallotti-Schmitt, S., Thiébaud, H., & Vasseur, P. (2000). Comparison of four chronic toxicity tests using algae, bacteria, and invertebrate sassessed with sixteen chemicals. Ecotoxicology and Environmental Safety, 47, 186–194.
Rodrigues, E. S., & Umbuzeiro, G. A. (2011). Integrating toxicity testing in the wastewater management of chemical storage terminals—a proposal based on a ten-year study. Journal of Hazardous Materials, 186, 1909–1915.
Reynoldson, R. H., Norris, V. H., Resh, K. E., Day, D. M., & Rosenberg, T. B. (1997). The reference condition: a comparison of multimetric and multivariate approaches to assess water-quality impairment using benthic macroinvertebrates. Journal of the North American Benthological Society, 16, 833–852.
Ruiz, F., Abad, M., Bodergat, A. M., Carbonel, P., Rodríguez-Lázaro, J., González-Regalado, M. L., Toscano, A., García, E. X., & Prenda, J. (2013). Freshwater ostracods as environmental tracers. International Journal of Environmental Science and Technology, 10, 1115–1128.
Sevilla, J. B., Nakajima, F., & Kasuga, I. (2014). Comparison of aquatic and dietary exposure of heavy metals Cd, Cu, and Zn to benthic ostracod Heterocypris incongruens. Environmental Toxicology and Chemistry, 33, 1624–1630.
Shen, K., Shen, C., Lu, Y., Tang, X., Zhang, C., Chen, X., Shi, J., Lin, Q., & Chen, Y. (2009). Hormesis response of marine and freshwater luminescent bacteria to metal exposure. Biological Research, 42, 183–187.
Şişman, T., İncekara, Ü., & Yıldız, Y. Ş. (2008). Determination of acute and early life stage toxicity of fat-plant effluent using zebrafish (Danio rerio). Environmental Toxicology, 23, 480–486.
Small, A. M., Adey, A. H., Lutz, S. M., Reese, E. G., & Roberts, D. L. (1996). A macrophyte-based rapid biosurvey of stream water quality: Restoration at the watershed scale. Restoration Ecology, 4, 124–145.
Steinberg, R. (1946). Mineral requirement of Lemna minor. Plant Physiology, 21, 42–48.
Tabrez, S., & Ahmad, M. (2012). Cytochrome P450 system as potential biomarkers of certain toxicants: comparison between plant and animal models. Environmental Monitoring and Assessment, 185(4), 2977–2987.
Tarkpea, M., & Hansson, M. (1989). Comparison between two Microtox test procedures. Ecotoxicology and Environmental Safety, 18, 204–210.
Thiebaut, G., Guérold, F., & Muller, S. (2002). Are trophic and diversity indices based on macrophyte communities pertinent tools to monitor water quality? Water Research, 36, 3602–3610.
Toumi, H., Burga-Perez, K. F., & Ferard, J.-F. (2015). Acute and chronic ecotoxicity of carbaryl with a battery of aquatic bioassays. Journal of Environmental Science and Health, Part B, 51, 57–62.
USEPA (United States Environmental Protection Agency). (1994). Short-term methods for estimating the chronic toxicity of effluents and receiving waters to freshwater organisms, EPA 600/7-91-002, Washington DC.
Vincze, K., Graf, K., Scheil, V., Köhler, H., & Triebskorn, R. (2014). Embryotoxic and proteotoxic effects of water and sediment from the Neckar River (Southern Germany) to zebrafish (Danio rerio) embryos. Environmental Sciences Europe, 26, 1–13.
Vörösmarty, C. J., McIntyre, P. B., Gessner, M. O., Dudgeon, D., Prusevich, A., Green, P., Glidden, S., Bunn, S. E., Sullivan, C. A., Liermann, C. R., & Davies, P. M. (2010). Global threats to human water security and river biodiversity. Nature, 467, 555–561.
Watanabe, H., Nakajima, F., Kasuga, I., & Furumai, H. (2008). Toxicity characterization of urban river sediments using bioassay with ostracod. Journal of Japan Society on Water Environment, 31, 671–676.
Watanabe, H., Nakajima, K., Kasuga, I., & Furumai, H. (2011). Toxicity evaluation of road dust in the runoff process using a benthic ostracod Heterocyprisincongruens. Science of the Total Environment, 409, 2366–2372.
Weyers, A., Sokull-Klüttgen, B., Baraibar-Fentanes, J., & Vollmer, G. (2000). Acute toxicity data: a comprehensive comparison of results of fish, Daphnia, and algae tests with new substances notified in the European Union. Environmental Toxicology and Chemistry, 19, 1931–1933.
Wolska, L., Sagajdakow, A., Kuczyńska, A., & Namieśnik, J. (2007). Application of ecotoxicological studies in integrated environmental monitoring: possibilities and problems. Trends in Analytical Chemistry, 26, 332–344.
Yi, X., Kang, S. W., & Jung, J. (2010). Long-term evaluation of lethal and sublethal toxicity of industrial effluents using Daphnia magna and Moinamacrocopa. Journal of Hazardous Materials, 178, 982–987.
Acknowledgements
This work was partly supported by Post-Doctor Research Program (2016) through Incheon National University and Industrial Strategic Technology Development Program (Grant No. 10079956) funded by the Ministry of Trade, Industry & Energy. We are grateful to Dr. J.C. Taylor (North-West University, South Africa) for his generous donation of Pleurax and to Emilie Saulnier-Talbot for valuable comments on the manuscript and for English revision.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Highlights
- An ecotoxicological assessment of natural waters based on a multi-organism trial was conducted in four South Korean rivers.
- The tested organisms showed distinct levels of performance in their response to natural waters.
- A scoring system is proposed to integrate biological responses into an overall toxicity category.
- This bioassay approach identified more sites as potentially degraded as did water chemistry measurements alone.
Electronic supplementary material
ESM 1
(DOCX 14.3 kb)
Rights and permissions
About this article
Cite this article
Pandey, L.K., Lavoie, I., Morin, S. et al. Towards a multi-bioassay-based index for toxicity assessment of fluvial waters. Environ Monit Assess 191, 112 (2019). https://doi.org/10.1007/s10661-019-7234-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10661-019-7234-5