Abstract
The aim of this study was to assess the ecological state of the soil of a megalopolis (St. Petersburg) located in the North-West of the Russian Federation using bioassay in order to create a set of the most sensitive biotests. For this, 4-year monitoring studies of the soil quality in different functional zones of the city were carried out using the bioassay, physicochemical, and chemical analyses. A set of express biotests that allow for an integral ecotoxicological assessment of urban soils was developed and tested for the first time. The developed block of biotests consists of test organisms that are representatives of the main levels of the trophic chain: higher plants (Triticum vulgare L.) for producers, hydrobionts (Paramecium caudatum) for consumers, and natural soil microbiocenosis for decomposers. All the test cultures revealed the toxicity of urban soils; they were characterized by different sensitivities to toxicants. Our result showed that a correct assessment of the ecological state of urban soils is possible on the basis of the combined use of eluate (water extract) and contact bioassays. Biotests make it possible to record negative phenomena in urban soils, which occur even under low human-induced loads. The research data confirm the necessity and effectiveness of the study of the soils’ state using a battery of bioassays for inclusion in the monitoring system of urban soils.













Similar content being viewed by others
References
Ajmone-Marsan, F., Padoan, E., Madrid, F., Vrščaj, B., Biasioli, M., & Davidson, C. M. (2019). Metal release under anaerobic conditions of urban soils of four European cities. Water, Air, and Soil Pollution, 230, 53. https://doi.org/10.1007/s11270-019-4101-5
Alef, K. (1995). Soil respiration. In K. Alef, & P. Nannipieri, (Eds.), Methods in applied soil microbiology and biochemistry. (pp. 214–219). Academic Press, Harcourt Brace & Company.
Alvarenga, P., Palma, P., de Varennes, A., & Cunha-Queda, A. C. (2012). A contribution towards the risk assessment of soils from the São Domingos mine (Portugal): chemical, microbial and ecotoxicological indicators. Environment and Pollution, 161, 50–56. https://doi.org/10.1016/j.envpol.2011.09.044
Aparin, B. F., Sukhacheva, Ye. Yu. (2015). Classification of urban soils in Russian soil classification system and international classification of soils. Dokuchaev Soil Bulletin, 79, 53–73. https://doi.org/10.19047/0136-1694-2015-79-53-72
Baderna, D., Colombo, A., Amodei, G., Cantù, S., Teoldi, F., Cambria, F., Rotella, G., Natolino, F., Lodi, M., & Benfenati, E. (2013). Chemical-based risk assessment and in vitro models of human health effects induced by organic pollutants in soils from the Olona Valley. Science Total Environment, 463–464, 790–801. https://doi.org/10.1016/j.scitotenv.2013.06.088
Baderna, D., Lomazzi, E., Pogliaghi, A., Ciaccia, G., Lodi, M., & Benfenati, E. (2015). Acute phytotoxicity of seven metals alone and in mixture: Are Italian soil threshold concentrations suitable for plant protection? Environmental Research, July 2015. Elsevier, p.102–111. https://doi.org/10.1016/j.envres.2015.03.023
Bardina, T. V., Chugunova, M. V., Kulibaba, V. V., & Bardina, V. I. (2020). The use of biological testing approaches to assessing the ecological conditions of soils in a reclaimed surface mine. Biosfera, 12(1), 51–62. https://doi.org/10.24855/biosfera.v12i1.539 (in Russian)
Bardina, T. V., Chugunova, M. V., Kulibaba, V. V., Polyak, Yu. M., Bardina, V. I., & Kapelkina, L. P. (2017). Applying bioassay methods for ecological assessment of the soils from the brownfield sites. Water, Air, & Soil Pollution, 228(9), 351. https://doi.org/10.1007/s11270-017-3521-3
Bardina, T.V., Chugunova, M.V., Bakina, L.G., & Bardina, V.I. (2013). Application of express methods of biotesting in assessing the ecological state of urban soils in St. Petersburg. Unsolved problems of climatology and ecology of megacities. Materials of the international forum, St. Petersburg. P. 16–21. Retrieved January 19, 2020, from http://thegreencity.ru/images/publikacia/sbonik_nereshennye_problemy_klimatologii...2013.pdf. (in Russian)
Blaise, C. (2000) Canadian application of microbiotests to assess the toxic potential of complex liquid and solid media. In: Persoone G., Janssen C., De Coen W. (eds) New microbiotests for routine toxicity screening and biomonitoring. Springer, Boston, MA. 3–12. https://doi.org/10.1007/978-1-4615-4289-6_1
Burghardt, W., Morel, J. L., & Zhang, G.-L. (2015). Development of the soil research about urban, industrial, traffic, mining and military areas (SUITMA). Soil Science and Plant Nutrition, 61(1), 3–21. https://doi.org/10.1080/00380768.2015.1046136
Cachada, A., da Silva, E. F., Duarte, A. C., & Pereira, R. (2016). Risk assessment of urban soils contamination: The particular case of polycyclic aromatic hydrocarbons. Science of the Total Environment, 551–552, 271–284. https://doi.org/10.1016/j.scitotenv.2016.02.012
Coldsnow, K. D., & Relyea, R. A. (2018). Toxicity of various road-deicing salts to Asian clams (Corbicula fluminea). Environmental toxicology and Chemistry, 37, 1839–1845. https://doi.org/10.1002/etc.4126
Critto, A., Torresan, S., Semenzin, E., Giove, S., Mesman, M., Schouten, A. J., Rutgers, M., & Marcomini, A. (2007). Development of a site-specific ecological risk assessment for contaminated sites: Part I. A multi-criteria based system for the selection of ecotoxicological tests and ecological observations. Science of the Total Environment, 379, 16–33. https://doi.org/10.1016/j.scitotenv.2007.02.035
Dobrovol’skaya, T. G., Zvyagintsev, D. G., Chernov, I. Y., Golovchenko, A. V., Zenova, G. M., Lysak, L. V., Manucharova, N. A., Marfenina, O. E., Polyanskaya, L. M., Stepanov, A. L., & Umarov, M. M. (2015). The role of microorganisms in the ecological functions of soils. Eurasian Soil Science, 48, 959–967. https://doi.org/10.1134/S1064229315090033
Environmental risk assessment of soil contamination (2014), Editors: Maria C. Hernandez-Soriano, Publisher: IntechOpen. https://doi.org/10.5772/57086
FR.1.39.2015.19243. (2015). Methods for determining the toxicity of soil samples, bottom sediments and sewage sludge by the express method using a device of the “Biotester” series. Saint Petersburg. 22
Friedman, S. P. (2005). Soil properties influencing apparent electrical conductivity: A review. Computers and Electronics in Agriculture, 46(1–3), 45–70. https://doi.org/10.1016/j.compag.2004.11.001
Galitskaya, PYu., & Selivanovskaya, SYu. (2009). Biological assessment of soil toxicity by bioassay. Agrochemistry, 3, 84–88. (in Russian).
van Gestel, C. A., van der Waarde, J. J., Derksen, J. G., van der Hoek, E. E., Veul, M. F., Bouwens, S., Rusch, B., Kronenburg, R., & Stokman, G. N. (2001). The use of acute and chronic bioassays to determine the ecological risk and bioremediation efficiency of oil-polluted soils. Environmental Toxicology and Chemistry, 20(7), 1438–1449. https://doi.org/10.1002/etc.5620200705
Gorbov, S. N., Bezuglova, O. S., Varduni, T. V., Gorovtsov, A. V., Tagiverdiev, S. S., & Hildebrant, Y. A. (2015). Genotoxicity and contamination of natural and anthropogenically transformed soils of the city of Rostov-on-Don with heavy metals. Eurasian Soil Science, 48(12), 1383–1392. https://doi.org/10.1134/S106422931512008X
Gorobtsova, O. N., Gedgafova, F. V., Uligova, T. S., & Tembotov, R. K. (2016). A comparative assessment of the biological properties of soils in the cultural and native cenoses of the Central Caucasus (using the example of the Terskii variant of altitudinal zonality in Kabardino-Balkaria). Eurasian Soil Science, 49(1), 89–94. https://doi.org/10.1134/S1064229316010063
GOST 26423–85. Soils. Methods for determination of specific electric conductivity, pH and solid residue of water extract. USSR Gosstandart 283.
GOST 54650–2011. Soils. Determination of mobile phosphorus and potassium compounds by the Kirsanov method modified by CINAO.
Hubálek, T., Vosáhlová, S., Mateju, V., Kovácová, N., & Novotný, C. (2007). Ecotoxicity monitoring of hydrocarbon-contaminated soil during bioremediation: A case study. Archives of Environmental Contamination and Toxicology, 52(1), 1–7. https://doi.org/10.1007/s00244-006-0030-6
Hygienic evaluation of soil quality in residential areas (1999). Methodological Instructive Regulations. MIR 2.1.7.730–99, 22
Ivanova, A. E., Nikolaeva, V. V., & Marfenina, O. E. (2015). Changes in the cellulolytic activity of urban soils induced by the removal of plant litter (using Moscow as an example). Eurasian Soil Science, 48(5), 501–508. https://doi.org/10.1134/S1064229315030059
Kapelkina, L. P., Bardina, T. V., Bakina, L. G., Chugunova, M. V., Gerasimov, A. O., Mayachkina, N. V., & Galdiyants, A. A. (2009). Methods for measuring the germination of seeds and the length of the roots of seedlings of higher plants to determine the toxicity of technogenically contaminated soils. FR.1.39.2006.02264. Sankt-Peterburg. 19.
Karczewska, A., & Kabała, C. (2017). Environmental risk assessment as a new basis for evaluation of soil contamination in Polish law. Soil Science Annual, 68(2), 67–80. https://doi.org/10.1515/ssa-2017-0008
Klimkowicz-Pawlas, A., Maliszewska-Kordybach, B., & Smreczak, B. (2019). Triad-based screening risk assessment of the agricultural area exposed to the long-term PAHs contamination. Environmental Geochemistry and Health, 41, 1369–1385. https://doi.org/10.1007/s10653-018-0220-y
Kosheleva, N. E., Vlasov, D. V., Korlyakov, I. D., & Kasimov, N. S. (2018). Contamination of urban soils with heavy metals in Moscow as affected by building development. Science of The Total Environment, 636(15), 854–863. https://doi.org/10.1016/j.scitotenv.2018.04.308
Kostic, D., Arsić, B., Ranđelović, S., Pavlović, A., Tošić, S., & Stojanović, G. (2019). Correlation analysis of heavy metals contents of Malva sylvestris L. plant and its extracts from polluted and non-polluted locations in Niš, Republic of Serbia. Water Air Soil Pollution, 230, 98. https://doi.org/10.1007/s11270-019-4153-6
Kostka, A., Strzebońska, M., Sobczyk, M., Zakrzewska, M., & Bochenek, A. (2019). The effect of de-icing roads with salt on the environment in Krakow (Poland). Geology Geophysics & Environment, 45(3), 195. https://doi.org/10.7494/geol.2019.45.3.195
Leitgib, L., Kálmán, J., & Gruiz, K. (2007). Comparison of bioassays by testing whole soil and their water extract from contaminated sites. Chemosphere, 66(3), 428–434. https://doi.org/10.1016/j.chemosphere.2006.06.024
Mai, T. L., Voronina, L. P., & Cheremnikh, E. G. (2014). Bioassay of soils on rice fields in Vietnam. Moscow University Soil Science Bulletin, 69, 116–123. https://doi.org/10.3103/S0147687414030041
Manzo, S., De Nicola, F., De Luca Picione, F., Maisto, G., & Alfani, A. (2008). Assessment of the effects of soil PAH accumulation by a battery of ecotoxicological tests. Chemosphere, 71(10), 1937–1944. https://doi.org/10.1016/j.chemosphere.2007.12.026
Mertens, J., Degryse, F., Springael, D., & Smolders, E. (2007). Zinc toxicity to nitrification in soil and soilless culture can be predicted with the same biotic ligand model. Environ. Sci. Technol., 41(8), 2992–2997. https://doi.org/10.1021/es061995+
Mills, S. D., Mamo, M., Schacht, W. H., et al. (2020). Soil properties affected vegetation establishment and persistence on roadsides. Water Air Soil Pollut, 231, 568. https://doi.org/10.1007/s11270-020-04930-2
Mónok, D., Kardos, L., Pabar, S. A., & Kotroczó, Zs. (2020). Applying bioassays for investigation of soils from suburban green sites. 5th World Congress on Civil, Structural, and Environmental Engineering (CSEE’20). November. Paper No. ICEPTP 108. https://doi.org/10.11159/iceptp20.108
Nevidomskaya, D., Minkina, T., Fedorov, Y., Nazarenko, O., Kravtsova, N., & Litvinov, Y. (2020). Integral assessment of heavy metal pollution in Don River estuary soils E3S. Web Conf. Vol. 169, art. 01007. Actual Problems of Ecology and Environmental Management: Cooperation for Sustainable Development and Environmental Safety, 5. https://doi.org/10.1051/e3sconf/202016901007
Norikazu, M., Tomonori, K., Miho, T., et al. (2003). Use of Paramecium species in. Journal of Health Science, 46(6), 429–435. https://doi.org/10.1248/jhs.49.429
Oberts, G. L. (2003). Cold climate BMPs: Solving the management puzzle. Water Sci Technol., 48(9), 21–32. https://doi.org/10.2166/wst.2003.0483
Olkova, A. S., Berezin, G. I., & Ashikhmina, T. . Ya. . (2016). Soil status assessment in urban areas by chemical and environmental toxicological methods. Povolzhskiy Journal of Ecology, 4, 411–423. https://doi.org/10.18500/1684-7318-2016-4-411-423
Olkova, A. S. (2018). Modern trends in the development of the methodology of bioassay aquatic environments. Theoretical and Applied Ecology, 3, 19–26. https://doi.org/10.25750/1995-4301-2018-3-019-026
Osma, E., Serin, M., Leblebici, Z., & Aksoy, A. (2012). Heavy metals accumulation in some vegetables and soils in Istanbul. Ekoloji, 21(82), 1–8. https://doi.org/10.5053/ekoloji.2011.821
Perrodin, Y., Boillot, C., Angerville, R., Donguy, G., & Emmanual, E. (2011). Ecological risk assessment of urban and industrial systems: A review. Science of the Total Environment, 409(24), 5162–5176. https://doi.org/10.1016/j.scitotenv.2011.08.053
PND. Methods for determining the acute toxicity of drinking, fresh natural and waste waters, water extracts from soils, sewage sludge and waste according to the mortality of daphnia (2014). F T 14.1:2:4.12–06 and T 16.1:2.3:3.9–06, Moscow, 34.
Pouyat, R. V., Yesilonis, I. D., Dombos, M., Szlavecz, K., Setälä, H., Cilliers, S., Hornung, E., Kotze, D. J., & Yarwood, S. (2015). A global comparison of surface soil characteristics across five cities. A test of the Urban Ecosystem Convergence Hypothesis. Soil Science, 180(4–5), 136–145. https://doi.org/10.1097/SS.0000000000000125
Prokof’eva, T. V., Gerasimova, M. I., Bezuglova, O. S., Gorbov, S. N., Bakhmatova, K. A., Matinyan, N. N., Gol’eva, A. A., Zharikova, E. A., Nakvasina, E. N., & Sivtseva, N. E. (2014). Inclusion of soils and soil-like bodies of urban territories into the Russian soil classification system. Eurasian Soil Science, 47(10), 959–967. https://doi.org/10.1134/S1064229314100093
Pukalchik, M. A., Terekhova, V. A., Karpukhin, M. M., & Vavilova, V. M. (2019). Comparison of eluate and direct soil bioassay methods of soil assessment in the case of contamination with heavy metals. Eurasian soil science, 52(4), 464–470. https://doi.org/10.1134/S1064229319040112
Rotting, T. S., Cama, J., Ayora, C., Cortina, J.-L., & de Pablo, J. (2006). Use of caustic magnesia to remove cadmium, nickel, and cobalt from water in passive treatment systems: Column experiments. Environment Science Technology, 40, 6438–6443. https://doi.org/10.1021/es061092g
Rybakov, D. S., & Kevlich, V. I. (2017). Microelements in anthropogenically contaminated soils in the central part of Petrozavodsk. Eurasian Soil Science, 50(6), 708–719. https://doi.org/10.1134/S1064229317060102
SANPIN 1.2.3685–21 (2021). Hygienic standards and requirements for ensuring, safety and (or) harmlessness to humans of environmental factors. Moscow, 736.
Senese, V., Boriani, E., Baderna, D., Mariani, A., Lodi, M., Finizio, A., Testa, S., & Benfenati, E. (2010). Assessing the environmental risks associated with contaminated sites: Definition of an Ecotoxicological Classification index for landfill areas (ECRIS). Chemosphere, 80(1), 60–66. https://doi.org/10.1016/j.chemosphere.2010.03.035
Šerá, B. (2017). Salt-tolerant trees usable for Central European cities – Review. Horticultural Science (Prague), 44(1), 43–48. https://doi.org/10.17221/201/2015-HORTSCI
Shchepeleva, A. S., Vasenev, V. I., Mazirov, I. M., Vasenev, I. I., Prokhorov, I. S., & Gosse, D. D. (2017). Changes of soil organic carbon stocks and CO2 emissions at the early stages of urban turf grasses’ development. Urban Ecosystems, 20(2), 309–321. https://doi.org/10.1007/s11252-016-0594-5
Smagin, A. V., Stepanov, A. L., Azovtseva, N. A., Smagina, M. V., Myagkova, A. D., & Kurbatova, A. S. (2006). Criteria and methods to assess the ecological status of soils in relation to the landscaping of urban territories. Eurasian Soil Science, 39(5), 539–551. https://doi.org/10.1134/S1064229306050115
Sorvari, J., Schultz, E., & Haimi, J. (2013). Assessment of ecological risks at former landfill site using TRIAD procedure and multicriteria analysis. Risk Analysis, 33(2), 203–219. https://doi.org/10.1111/j.1539-6924.2012.01858.x
Steffan, J. J., Brevik, E. C., Burgess, L. C., & Cerdàc, A. (2018). The effect of soil on human health: An overview. European journal of soil science, 69(1), 159–171. https://doi.org/10.1111/ejss.12451
Stoma, G. V., Manucharova, N. A., & Belokopytova, N. A. (2020). Biological activity of microbial communities in soils of some Russian cities. Eurasian Soil Science, 53(6), 760–771. https://doi.org/10.1134/S1064229320060125
Stroganova, M. N., & Agarkova, M. G. (1993). Urban soils: Experimental study and classification (exemplified by the Soils of Southwestern Moscow). Eurasian Soil Science, 25(3), 59–69.
Stroganova, M. N., Myagkova, A. D., & Prokofieva, T. V. (1997). The role of soils in urban ecosystems. Eurasian Soil Science, 30(1), 82–86.
Swartjes, F. A. (2011). Introduction to contaminated site management. In Dealing with Contaminated Sites (pp. 3–89). Dordrecht: Springer Publishers. https://doi.org/10.1007/978-90-481-9757-6_1
Terekhova, V. A. (2011). Soil bioassay: Problems and approaches. Eurasian Soil Science, 44(2), 173–179. https://doi.org/10.1134/S1064229311020141
Terekhova, V. A., Pukalchik, M. A., & Yakovlev, A. S. (2014). The triad approach to ecological assessment of urban soils. Eurasian Soil Science, 47(9), 952–958. https://doi.org/10.1134/S1064229314090129
Terekhova, V. A., Wadhia, K., Fedoseeva, E. V., & Uchanov, P. V. (2018). Bioassay standardization issues in freshwater ecosystem assessment: Test cultures and test conditions. Knowledge and Management of Aquatic Ecosystems, 419(32), 14. https://doi.org/10.1051/kmae/2018015/
Vasilyeva, G. K., Kondrashina, V. S., Strijakova. E. R., & Pinsky, D. L. (2020). Express-phytotest for choosing conditions and following process of soil remediation. Environmental Geochemistry and Health, 1–13. https://doi.org/10.1007/s10653-020-00727-8
Vodyanitskii, Y. N. (2011). About hazardous heavy metals/metalloids in soils. Dokuchaev Soil Bulletin, 68, 56–82. https://doi.org/10.19047/0136-1694-2011-68-56-82 (in Russian).
Vodyanitskii, Y. N. (2013). Contamination of soils with heavy metals and metalloids and its ecological hazard (analytic review). Eurasian Soil Science, 46, 793–801. https://doi.org/10.1134/S1064229313050153
Wei, B., & Yang, L. (2010). A review of heavy metal contaminations in urban soils, urban road dusts and agricultural soils from China. Microchemical journal, 94(2), 99–107. https://doi.org/10.1016/j.microc.2009.09.014
Westerhoff, B. M., Fairbairn, D. J., Ferrey, M. L., Matilla, A., Kunkel, J., Elliott, S. M., Kiesling, R. L., Woodruff, D., & Schoenfuss, H. L. (2018). Effects of urban stormwater and iron-enhanced sand filtration on Daphnia magna and Pimephales promelas. Environ Toxicol Chem., 37, 2645–2659. https://doi.org/10.1002/etc.4227
Yakovlev, A. S., & Evdokimova, M. V. (2011). Ecological standardization of soil and soil quality control. Eurasian Soil Science, 44, 534–546. https://doi.org/10.1134/S1064229311050152
Yang, J. L., & Zhang, G. L. (2015). Formation, characteristics and eco-environmental implications of urban soils – A review. Soil Science and Plant Nutrition, 61(1), 30–46. https://doi.org/10.1080/00380768.2015.1035622
Acknowledgements
The present study was supported by state research topic of SRCES RAS №0241-2019-0018.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no competing interests.
Rights and Permissions
Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Bardina, T.V., Chugunova, M.V., Kapelkina, L.P. et al. Ecological State Assessment of Urban Soils by Bioassay. Water Air Soil Pollut 233, 7 (2022). https://doi.org/10.1007/s11270-021-05475-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11270-021-05475-8

