Impact of metal polluted sewage water on soil nematode assemblages in agricultural settings of Aligarh, India

Mohammed F.S.A. Ghanem, Shahid Afzal, Humira Nesar, Zarrin Imran, Wasim Ahmad

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Soil Ecology Letters ›› 2024, Vol. 6 ›› Issue (1) : 230193. DOI: 10.1007/s42832-023-0193-3
RESEARCH ARTICLE
RESEARCH ARTICLE

Impact of metal polluted sewage water on soil nematode assemblages in agricultural settings of Aligarh, India

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Highlights

● Sewage water in agriculture threatens human health and soil ecosystems through metal pollution.

● Nematodes show promise as bioindicators of soil health due to their abundance and position in soil food webs.

● Metal-polluted water decreased abundance of certain nematode groups and Sigma Maturity Index.

● Metal pollution positively affected nematode groups with r-selected life cycles.

Abstract

Sewage water has been inappropriately used in agriculture, posing possible threats to human health and the soil ecosystems by its constituent pollutants, especially heavy metals. Correct evaluation of its influences on soil biomes needs to consider the response of soil fauna. Among soil organisms, nematodes are seen as the best promising candidates for bioindicators of soil health. Here in, we collected soil samples from fresh water irrigated field from three sites (S1, S2 and S3) and sewage water irrigated distance gradient (5 m−40 m), to assess the influence of metal (Cu, Zn, Cd, Mn, Pb) polluted water on various characteristics of nematode communities. The results indicated that the heavy metals decreased the abundance of C-p3 nematodes, herbivores, and predatory nematodes as well as sigma maturity index, whereas, C-p1, C-p2, bacterivore and fungivore nematodes abundance and diversity positively responded to the metal pollution. Generally, nematode genera with r-selected life cycle were positively affected and those with K-selected life cycle were negatively affected by metal pollution. Overall nematode community has potential to be used as indicator of pollution stress in agricultural soils to check soil health and sustainability.

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Keywords

heavy metals / sewage irrigation / agriculture / nematodes / bioindicators

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Mohammed F.S.A. Ghanem, Shahid Afzal, Humira Nesar, Zarrin Imran, Wasim Ahmad. Impact of metal polluted sewage water on soil nematode assemblages in agricultural settings of Aligarh, India. Soil Ecology Letters, 2024, 6(1): 230193 https://doi.org/10.1007/s42832-023-0193-3

References

[1]
Afzal, S., Nesar, H., Imran, Z., Ahmad, W., 2021. Altitudinal gradient affect abundance, diversity and metabolic footprint of soil nematodes in Banihal-Pass of Pir-Panjal mountain range. Scientific Reports11, 1–13.
CrossRef Google scholar
[2]
Afzal, S., Nesar, H., Imran, Z., Ahmad, W., 2022. Change in land-use from natural forest impacts functional composition and metabolic footprint of soil nematode community in Western Himalayas. Acta Ecologica Sinica doi:10.1016/j.chnaes.2022.12.004
[3]
Agoro, M.A., Adeniji, A.O., Adefisoye, M.A., Okoh, O.O., 2020. Heavy metals in wastewater and sewage sludge from selected municipal treatment plants in Eastern Cape Province, South Africa. Water (Basel)12, 2746.
CrossRef Google scholar
[4]
Ahmad, W., Jairajpuri, M.S., 2010. Mononchida: The Predaceous Nematodes. Nematology Monographs and Perspectives 7. E. J. Brill, Leiden, The Netherlands. pp. 299
[5]
Alghobar, M.A., Suresha, S., 2017. Evaluation of metal accumulation in soil and tomatoes irrigated with sewage water from Mysore city, Karnataka, India. Journal of the Saudi Society of Agricultural Sciences16, 49–59.
CrossRef Google scholar
[6]
Amin, A., Naik, A.R., Azhar, M., Nayak, H., 2013. Bioremediation of different waste waters−a review. Continental Journal of Fisheries and Aquatic Science7, 7–17.
[7]
Andrássy, I., 1956. The determination of volume and weight of nematodes. Acta Zoologica Academiae Scientiarum Hungaricae2, 1–15.
[8]
Andrássy, I., 2005. Free-living nematodes of Hungary: Nematoda Errantia (Vol. 1). Budapest, Hungary: Hungarian Natural History Museum
[9]
Awasthi, S.K., 2000. Prevention of food adulteration act no 37 of 1954: Central and State rules as amended for 1999. Ashoka, New Delhi
[10]
Bakonyi, G., Nagy, P., Kádár, I., 2003. Long-term effects of heavy metals and microelements on nematode assemblage. Toxicology Letters140, 391–401.
CrossRef Google scholar
[11]
Balkhair, K.S., Ashraf, M.A., 2016. Field accumulation risks of heavy metals in soil and vegetable crop irrigated with sewage water in western region of Saudi Arabia. Saudi Journal of Biological Sciences23, S32–S44.
CrossRef Google scholar
[12]
Bardgett, R.D., Speir, T.W., Ross, D.J., Yeates, G.W., Kettles, H.A., 1994. Impact of pasture contamination by copper, chromium, and arsenic timber preservative on soil microbial properties and nematodes. Biology and Fertility of Soils18, 71–79.
CrossRef Google scholar
[13]
Bharose, R., Lal, S.B., Singh, S.K., Srivastava, P.K., 2013. Heavy metals pollution in soil-water-vegetation continuum irrigated with ground water and untreated sewage. Bulletin of Environmental and Scientific Research2, 1–8.
[14]
Bongers, T., 1990. The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia83, 14–19.
CrossRef Google scholar
[15]
Bongers, T., 1999. The Maturity Index, the evolution of nematode life history traits, adaptive radiation and cp-scaling. Plant and Soil212, 13–22.
CrossRef Google scholar
[16]
Bongers, T., Bongers, M., 1998. Functional diversity of nematodes. Applied Soil Ecology10, 239–251.
CrossRef Google scholar
[17]
Bongers, T., Ferris, H., 1999. Nematode community structure as a bioindicator in environmental monitoring. Trends in Ecology & Evolution14, 224–228.
CrossRef Google scholar
[18]
Bongers, T., van der Meulen, H., Korthals, G., 1997. Inverse relationship between the nematode maturity index and plant parasite index under enriched nutrient conditions. Applied Soil Ecology6, 195–199.
CrossRef Google scholar
[19]
Borrelli, P., Robinson, D.A., Fleischer, L.R., Lugato, E., Ballabio, C., Alewell, C., Panagos, P., 2017. An assessment of the global impact of 21st century land use change on soil erosion. Nature Communications8, 1–13.
CrossRef Google scholar
[20]
Bünemann, E.K., Bongiorno, G., Bai, Z., Creamer, R.E., De Deyn, G., de Goede, R., Brussaard, L., 2018. Soil quality–A critical review. Soil Biology & Biochemistry120, 105–125.
CrossRef Google scholar
[21]
Cassidy, E.S., West, P.C., Gerber, J.S., Foley, J.A., 2013. Redefining agricultural yields: from tonnes to people nourished per hectare. Environmental Research Letters8, 034015.
CrossRef Google scholar
[22]
Chauvin, C., Trambolho, M., Hedde, M., Makowski, D., Cérémonie, H., Jimenez, A., Villenave, C., 2020. Soil nematodes as indicators of heavy metal pollution: A meta-analysis. Open Journal of Soil Science10, 579–601.
CrossRef Google scholar
[23]
Chen, G., Qin, J., Shi, D., Zhang, Y., Ji, W., 2009. Diversity of soil nematodes in areas polluted with heavy metals and polycyclic aromatic hydrocarbons (PAHs) in Lanzhou, China. Environmental Management44, 163–172.
CrossRef Google scholar
[24]
Ekschmitt, K., Korthals, G.W., 2006. Nematodes as sentinels of heavy metals and organic toxicants in the soil. Journal of Nematology38, 13.
[25]
European Union, 2002. Heavy Metals in Wastes. European Commission on Environment
[26]
FAO, 2020. State of Knowledge of Soil Biodiversity-Status, Challenges and Potentialities. Rome: FAO
[27]
Ferris, H., 2010. Form and function: metabolic footprints of nematodes in the soil food web. European Journal of Soil Biology46, 97–104.
CrossRef Google scholar
[28]
Ferris, H., Bongers, T., de Goede, R.G., 2001. A framework for soil food web diagnostics: extension of the nematode faunal analysis concept. Applied Soil Ecology18, 13–29.
CrossRef Google scholar
[29]
Ferris, H., Griffiths, B.S., Porazinska, D.L., Powers, T.O., Wang, K.H., Tenuta, M., 2012. Reflections on plant and soil nematode ecology: past, present and future. Journal of Nematology44, 115.
[30]
Fiscus, D.A., Neher, D.A., 2002. Distinguishing sensitivity of free‐living soil nematode genera to physical and chemical disturbances. Ecological Applications12, 565–575.
CrossRef Google scholar
[31]
Foley, J.A., Ramankutty, N., Brauman, K.A., Cassidy, E.S., Gerber, J.S., Johnston, M., Zaks, D.P., 2011. Solutions for a cultivated planet. Nature478, 337–342.
CrossRef Google scholar
[32]
Freckman, D.W., 1988. Bacterivorous nematodes and organic-matter decomposition. Agriculture, Ecosystems & Environment24, 195–217.
CrossRef Google scholar
[33]
Georgieva, S.S., McGrath, S.P., Hooper, D.J., Chambers, B.S., 2002. Nematode communities under stress: the long-term effects of heavy metals in soil treated with sewage sludge. Applied Soil Ecology20, 27–42.
CrossRef Google scholar
[34]
Goodey, T., 1963. Soil and Freshwater Nematodes. London, Methuen and Cooperation Limited
[35]
Gutiérrez, C., Fernández, C., Escuer, M., Campos-Herrera, R., Rodríguez, M.E.B., Carbonell, G., Martín, J.A.R., 2016. Effect of soil properties, heavy metals and emerging contaminants in the soil nematodes diversity. Environmental Pollution213, 184–194.
CrossRef Google scholar
[36]
Heininger, P., Höss, S., Claus, E., Pelzer, J., Traunspurger, W., 2007. Nematode communities in contaminated river sediments. Environmental Pollution146, 64–76.
CrossRef Google scholar
[37]
Höss, S., Reiff, N., Asekunowo, J., Helder, J., 2022. Nematode community of a natural grassland responds sensitively to the broad-spectrum fungicide mancozeb in soil microcosms. Environmental Toxicology and Chemistry41, 2420–2430.
CrossRef Google scholar
[38]
Hou, S., Li, X., Wang, H., Wang, M., Zhang, Y., Chi, Y., Zhao, Z., 2017. Synthesis of core–shell structured magnetic mesoporous silica microspheres with accessible carboxyl functionalized surfaces and radially oriented large mesopores as adsorbents for the removal of heavy metal ions. RSC Advances7, 51993–52000.
CrossRef Google scholar
[39]
Huertos, E. G., Baena, A.R., 2008. Contaminación de suelos por metales pesados. MACLA, revista de la Sociedad Española de Mineralogía10, 48–60.
[40]
Jairajpuri, M.S., Ahmad, W., 1992. Dorylaimida: Free living, Predaceous and Plant Parasitic Nematodes. The Netherlands and Oxford & IBH, New Delhi, pp. 458
[41]
Jansson, J.K., Hofmockel, K.S., 2020. Soil microbiomes and climate change. Nature Reviews. Microbiology18, 35–46.
CrossRef Google scholar
[42]
Jaramillo, M.F., Restrepo, I., 2017. Wastewater reuse in agriculture: A review about its limitations and benefits. Sustainability (Basel)9, 1734.
CrossRef Google scholar
[43]
Jiménez, B., Asano, T., 2008. Water Reuse: An International Survey of Current Practice, Issues and Needs. IWA Publishing, London.
[44]
Kammenga, J.E., Van Gestel, C.A.M., Bakker, J., 1994. Patterns of sensitivity to cadmium and pentachlorophenol among nematode species from different taxonomic and ecological groups. Archives of Environmental Contamination and Toxicology27, 88–94.
CrossRef Google scholar
[45]
Karanja, N.N., Mutua, G.K., Ayuke, F., Njenga, M., Prain, G., Kimenju, J., 2010. Dynamics of soil nematodes and earthworms in urban vegetable irrigated with wastewater in the Nairobi river basin, Kenya. Tropical and Subtropical Agroecosystems12, 521–530.
[46]
Kawatra, B.L., Bakhetia, P., 2008. Consumption of heavy metal and minerals by adult women through food in sewage and tube-well irrigated area around Ludhiana city (Punjab, India). Journal of Human Ecology (Delhi, India)23, 351–354.
CrossRef Google scholar
[47]
Kopittke, P.M., Menzies, N.W., Wang, P., McKenna, B.A., Lombi, E., 2019. Soil and the intensification of agriculture for global food security. Environment International132, 105078.
CrossRef Google scholar
[48]
Korthals, G.W., van de Ende, A., van Megen, H., Lexmond, T.M., Kammenga, J.E., Bongers, T., 1996. Short-term effects of cadmium, copper, nickel and zinc on soil nematodes from different feeding and life-history strategy groups. Applied Soil Ecology4, 107–117.
CrossRef Google scholar
[49]
Li, X., Yang, Q., Wang, L., Song, C., Chen, L., Zhang, J., Liang, Y., 2022. Using Caenorhabditis elegans to assess the ecological health risks of heavy metals in soil and sediments around Dabaoshan Mine, China. Environmental Science and Pollution Research International29, 16332–16345.
CrossRef Google scholar
[50]
Marković, M., Cupać, S., Đurović, R., Milinović, J., Kljajić, P., 2010. Assessment of heavy metal and pesticide levels in soil and plant products from agricultural area of Belgrade, Serbia. Archives of Environmental Contamination and Toxicology58, 341–351.
CrossRef Google scholar
[51]
Martinez, J.G., Torres, M.A., dos Santos, G., Moens, T., 2018. Influence of heavy metals on nematode community structure in deteriorated soil by gold mining activities in Sibutad, southern Philippines. Ecological Indicators91, 712–721.
CrossRef Google scholar
[52]
Minhas, P.S., Saha, J.K., Dotaniya, M.L., Sarkar, A., Saha, M., 2022. Wastewater irrigation in India: Current status, impacts and response options. Science of the Total Environment808, 152001.
CrossRef Google scholar
[53]
Monteiro, L.C., Van Butsel, J., De Meester, N., Traunspurger, W., Derycke, S., Moens, T., 2018. Differential heavy-metal sensitivity in two cryptic species of the marine nematode Litoditis marina as revealed by developmental and behavioural assays. Journal of Experimental Marine Biology and Ecology502, 203–210.
CrossRef Google scholar
[54]
Montgomery, D.R., 2007. Soil erosion and agricultural sustainability. Proceedings of the National Academy of Sciences of the United States of America104, 13268–13272.
CrossRef Google scholar
[55]
Nagy, P., Bakonyi, G., Bongers, T., Kadar, I., Fabian, M., Kiss, I., 2004. Effects of microelements on soil nematode assemblages seven years after contaminating an agricultural field. Science of the Total Environment320, 131–143.
CrossRef Google scholar
[56]
Neher, D.A., 2001. Role of nematodes in soil health and their use as indicators. Journal of Nematology33, 161.
[57]
Nesar, H., Afzal, S., Imran, Z., Ahmad, W., 2021. Substratum-dependent moss microhabitat types alter soil nematode community structure in the mixed coniferous forest of Dachigam National Park, Jammu and Kashmir. Global Ecology and Conservation32, e01924.
CrossRef Google scholar
[58]
O’Connor, J., Hoang, S.A., Bradney, L., Dutta, S., Xiong, X., Tsang, D.C., Bolan, N.S., 2021. A review on the valorisation of food waste as a nutrient source and soil amendment. Environmental Pollution272, 115985.
CrossRef Google scholar
[59]
Pen-Mouratov, S., Shukurov, N., Steinberger, Y., 2008. Influence of industrial heavy metal pollution on soil free-living nematode population. Environmental Pollution152, 172–183.
CrossRef Google scholar
[60]
Pérez, A.P., Eugenio, N.R., 2018. Status of Local Soil Contamination in Europe. Publications Office of the European Union, Luxembourg
[61]
Quéré, C., Andrew, R.M., Friedlingstein, P., Sitch, S., Hauck, J., Pongratz, J., Zheng, B., 2018. Global carbon budget 2018. Earth System Science Data10, 2141–2194.
CrossRef Google scholar
[62]
Šalamún, P., Renčo, M., Kucanová, E., Brázová, T., Papajová, I., Miklisová, D., Hanzelová, V., 2012. Nematodes as bioindicators of soil degradation due to heavy metals. Ecotoxicology (London, England)21, 2319–2330.
CrossRef Google scholar
[63]
Sánchez-Moreno, S., Ferris, H., Young-Mathews, A., Culman, S.W., Jackson, L.E., 2011. Abundance, diversity and connectance of soil food web channels along environmental gradients in an agricultural landscape. Soil Biology & Biochemistry43, 2374–2383.
CrossRef Google scholar
[64]
Shao, Y., Zhang, W., Shen, J., Zhou, L., Xia, H., Shu, W., Ferris, H., Fu, S., 2008. Nematodes as indicators of soil recovery in tailings of a lead/zinc mine. Soil Biology & Biochemistry40, 2040–2046.
CrossRef Google scholar
[65]
Sieriebriennikov, B., Ferris, H., de Goede, R.G., 2014. NINJA: an automated calculation system for nematode-based biological monitoring. European Journal of Soil Biology61, 90–93.
CrossRef Google scholar
[66]
Singh, A., Sharma, R.K., Agrawal, M., Marshall, F.M., 2010. Health risk assessment of heavy metals via dietary intake of foodstuffs from the wastewater irrigated site of a dry tropical area of India. Food and Chemical Toxicology48, 611–619.
CrossRef Google scholar
[67]
Singh, K.P., Mohan, D., Sinha, S., Dalwani, R., 2004. Impact assessment of treated/untreated wastewater toxicants discharged by sewage treatment plants on health, agricultural, and environmental quality in the wastewater disposal area. Chemosphere55, 227–255.
CrossRef Google scholar
[68]
Sinha, R.K., Bharambe, G., Chaudhari, U., 2008. Sewage treatment by vermifiltration with synchronous treatment of sludge by earthworms: a low-cost sustainable technology over conventional systems with potential for decentralization. Environmentalist28, 409–420.
CrossRef Google scholar
[69]
Skubała, P., Zaleski, T., 2012. Heavy metal sensitivity and bioconcentration in oribatid mites (Acari, Oribatida): Gradient study in meadow ecosystems. Science of the Total Environment414, 364–372.
CrossRef Google scholar
[70]
Teh, T.L., Rahman, N.N.N.A., Shahadat, M., Wong, Y.S., Syakir, M.I., Omar, A.K., 2016. A comparative study of metal contamination in soil using the borehole method. Environmental Monitoring and Assessment188, 1–16.
CrossRef Google scholar
[71]
Tilman, D., Balzer, C., Hillc, J., Befort, B.L., 2011. Global food demand and the sustainable intensification of agriculture. Proceedings of the National Academy of Sciences of the United States of America108, 20260–20264.
CrossRef Google scholar
[72]
Trivedi, R.K., Goel, P.K., 1986. Chemical and Biological Methods for Water Pollution Studies. Enviromedia Publications, Karad. pp. 209
[73]
Türkdoğan, M.K., Kilicel, F., Kara, K., Tuncer, I., Uygan, I., 2003. Heavy metals in soil, vegetables and fruits in the endemic upper gastrointestinal cancer region of Turkey. Environmental Toxicology and Pharmacology13, 175–179.
CrossRef Google scholar
[74]
Van Bezooijen, J., 2006. Methods and Techniques for Nematology. Wageningen, The Netherlands: Wageningen University. p. 20
[75]
Wagg, C., Bender, S.F., Widmer, F., Van Der Heijden, M.G., 2014. Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proceedings of the National Academy of Sciences of the United States of America111, 5266–5270.
CrossRef Google scholar
[76]
Walkley, A., Black, T.A., 1934. An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Science37, 29–38.
CrossRef Google scholar
[77]
Wang, C., Hu, X., Chen, M.L., Wu, Y.H., 2005. Total concentrations and fractions of Cd, Cr, Pb, Cu, Ni and Zn in sewage sludge from municipal and industrial wastewater treatment plants. Journal of Hazardous Materials119, 245–249.
CrossRef Google scholar
[78]
Weider, S.Z., Nittler, L.R., Starr, R.D., Crapster-Pregont, E.J., Peplowski, P.N., Denevi, B.W., Solomon, S.C., 2015. Evidence for geochemical terranes on Mercury: Global mapping of major elements with MESSENGER’s X-Ray Spectrometer. Earth and Planetary Science Letters416, 109–120.
CrossRef Google scholar
[79]
Wilson, M.J., Kakouli-Duarte, T., eds., 2009. Nematodes as Environmental Indicators. CABI
[80]
Winpenny, J., Heinz, I., Koo-Oshima, S., Salgot, M., Collado, J., Hernández, F., 2013. Reutilización del agua en la agricultura: Beneficios para todos? Informes sobre temas hídricos. Rome, Italy: Food and Agriculture Organization
[81]
Yang, L., Zhang, F., Luo, Y., 2021. A soil nematode community response to reclamation of salinized abandoned farmland. Zoological Studies (Taipei, Taiwan)60, e72.
CrossRef Google scholar
[82]
Yeates, G.W., 2003. Nematodes as soil indicators: functional and biodiversity aspects. Biology and Fertility of Soils37, 199–210.
CrossRef Google scholar
[83]
Yeates, G.W., Orchard, V.A., Speir, T.W., Hunt, J.L., Hermans, M.C.C., 1994. Impact of pasture contamination by copper, chromium, arsenic timber preservative on soil biological activity. Biology and Fertility of Soils18, 200–208.
CrossRef Google scholar
[84]
Zhang, X., Li, Q., Zhu, A., Liang, W., Zhang, J., Steinberger, Y., 2012. Effects of tillage and residue management on soil nematode communities in North China. Ecological Indicators13, 75–81.
CrossRef Google scholar
[85]
Zhang, Z., Hibberd, A., Zhou, J.L., 2008. Analysis of emerging contaminants in sewage effluent and river water: comparison between spot and passive sampling. Analytica Chimica Acta607, 37–44.
CrossRef Google scholar
[86]
Zhou, S., Huang, Y., Yu, B., Wang, G., 2015. Effects of human activities on the eco-environment in the middle Heihe River Basin based on an extended environmental Kuznets curve model. Ecological Engineering76, 14–26.
CrossRef Google scholar

Data availability statement

The data presented in the study are included in the supplementary material. For further inquiries related to data presented in this article corresponding authors can be contacted.

Author contributions

M.F.S.A.G and SA contributed equally to the manuscript. M.F.S.A.G, SA, WA designed the research, M.F.S.A.G performed the soil sampling and analyzed the soil abiotic and biotic community; SA performed the statistical analyses, designed figures and lead the writing of the manuscript, HN corrected the references, HN and ZI corrected the manuscript. All authors contributed to the article and approved the submitted version.

Conflict of interest

The authors declare they have no conflict of interest.

Acknowledgments

The authors would like to thank the farmers who allowed to carry out the soil sampling in their fields. The authors are also thankful to the Aligarh Muslim University for providing the required facilities.

Electronic supplementary material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s42832-023-0193-3 and is accessible for authorized users.

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