Investigating the Impacts of Heavy Metals and the Environmental on the Soil Biodiversity (Hexapoda: Collembola)

Document Type : Research Article

Authors

• Ensieh Saberi Pour ¹
• Fatemeh Tabatabaei Yazdi ²
• Morteza Kahrarian ³

¹ MA Student in Sciences and Environmental Engineering, Department of Environment, Faculty of Natural Resources and Environment, Ferdowsi University of Mashhad , Mashhad, Iran

² Department of Environment, Faculty of Natural Resources and Environment, Ferdowsi University of Mashhad , Mashhad, Iran

³ Department of Agronomy and Plant Breeding, Faculty of Agriculture, Kermanshah branch, Islamic Azad University, Kermanshah, Iran

10.22067/geoeh.2023.79797.1308

Abstract

The increasing population, the expansion of industrial and urban wastewater, and the lack of proper treatment have significantly contributed to the existance heavy metals in the soil ecosystem. Preventing the impacts of heavy metals on the quality and health of the soil ecosystem requires selecting appropriate bioindicators. Thus, this study aims to investigate the impacts of heavy metals and the effective environmental parameters of the soil on Collembola, at genus level. For this purpose, in two stages, soil samples were taken from the stations around Charmshahr industrial wastewater treatment plant and Khin Arab and Parkandabad municipal wastewater treatment plants in Mashhad, Iran. Twenty-eight soil samples, each obtained by mixing four sub-samples, were collected from 14 stations. Statistical analysis was performed using R software. In the studied area, a total of 15 genera of Collembola were identified. All these genera were reported for the first time from Mashhad. The results of comparing the concentration of chemical parameters and the genera richness in Collembola showed that there is a significant correlation between them. The results show that the number of genera has a negative correlation with two metals, iron and chromium, and among the measured elements in soil, only total carbon has a positive correlation with the number of genera (p<0.05). The results of the canonical correspondence analysis showed that the response of the abundance of each Collembola genera to the concentrations of heavy metals and the environmental parameters is different. Thus, even if Collembola is advising as a proper bioindicator, we should mention that the response of the biodiversity to the abiotic parameters in soil is various, which must be deliberated in the ecosystem management.

Graphical Abstract

Keywords

• Biodiversity
• Bioindicator
• Environment
• Heavy Metals
• Pollution

20.1001.1.23221682.1402.12.2.10.1

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References

اسماعیلیان، حسین؛ تفضلی، سید محمد؛ قاسمی­زاده آزرمی، سید علیرضا؛ خاتمی، فرزانه؛ رجب­زاده، ناهید؛ 1399. واگذاری بهره‌برداری بلندمدت و نتیجه محور تصفیه‌خانه‌های فاضلاب به بخش خصوصی مطالعه موردی تصفیه‌خانه‌های فاضلاب خین­عرب و التیمور مشهد. هشتمین کنفرانس ملی مدیریت منابع آب ایران، مشهد، https://civilica.com/doc/1171954.

جعفری، فاطمه؛ مهرناد، حمید؛ حافظی مقدس، ناصر؛ قزی، اعظم؛ 1394. بررسی تغییرات جانبی رودخانه کشف­رود. کنگره بین­المللی تخصصی علوم و زمین، 34، SID. https://sid.ir/paper/840405/fa.

حسینی بهلولی، مهدیه؛ قشلاقی، افشین؛ محمودی، محمدحسین؛ 1396. بررسی غلظت فلزات سنگین در خاک‌های آبیاری شده با فاضلاب تصفیه نشده در منطقه التیمور مشهد. پنجمین کنفرانس ملی پژوهش­های کاربردی در مهندسی عمران، معماری و مدیریت شهری، https://civilica.com/doc/760154.

صابری کرهرودی، ه؛ گلچین، ا؛ و علمداری، پ؛ 2020. ارزیابی آلودگی خاک‌های اطراف کارخانه آلومینیوم‌سازی اراک به عناصر آلومینیوم، آهن، منگنز و سرب. فصلنامه علوم و تکنولوژی محیط‌زیست، 22(2)، 315–332. https://doi. rg/10.22034/jest.2020.9340.

علیزاده اقدم، محمدباقر؛ بنی­فاطمه، حسین؛ عباس­زاده، محمد؛ سلطانی بهرام، سعید؛ 2017. شهروندی بوم شناختی و هوش معنوی (مورد مطالعه: شهروندان شهر تبریز). جامعه شناسی کاربردی، 28(3)، 79–98،  https://doi.org/10.22108/jas.2017.21715

کهراریان، مرتضی؛ 1392. جمع­آوری و شناسایی حشرات بی­بال راسته Collembola در استان کرمانشاه (شهرستان­های کرمانشاه، صحنه، هرسین). گزارش نهایی طرح پژوهشی. دانشگاه آزاد اسلامی کرمانشاه.

مهرآوران، بابک؛ انصاری، حسین؛ بهشتی، علی­اصغر؛ اسماعیلی، کاظم؛ 1394. بررسی امکان استفاده از پساب تصفیه شده در آبیاری با توجه به اثرات زیست‌محیطی آن (مطالعه موردی پساب خروجی تصفیه خانه پرکندآباد مشهد). مجله آبیاری و زهکشی ایران، 9(3)، 440-447. SID. https://sid.ir/paper/131692/fa

 

Alengebawy, A., Abdelkhalek, S. T., Qureshi, S. R., & Wang, M.-Q., 2021. Heavy metals and pesticides toxicity in agricultural soil and plants: Ecological risks and human health implications. Toxics, 9(3), 42, https://doi.org/10.3390/toxics9030042.

Amanze, C., Zheng, X., Man, M., Yu, Z., Ai, C., Wu, X., Xiao, S., Xia, M., Yu, R., & Wu, X., 2022. Recovery of heavy metals from industrial wastewater using bioelectrochemical system inoculated with novel Castellaniella species. Environmental Research, 205, 112467, https://doi.org/10.1016/j.envres.2021.112467.

Arbea, J., & Kahrarian, M., 2015. The genus Folsomides Stach (Collembola, Isotomidae) in Kermanshah Province (W Iran) with the descriptionof two new species. Zootaxa, 3925(2), 281–290, http://dx.doi.org/10.11646/zootaxa.3925.2.9.

Ashraf, S., Ali, Q., Zahir, Z. A., Ashraf, S., & Asghar, H. N., 2019. Phytoremediation: Environmentally sustainable way for reclamation of heavy metal polluted soils. Ecotoxicology and Environmental Safety, 174, 714–727, https://doi.org/10.1016/j.ecoenv.2019.02.068

Austruy, A., Laplanche, C., Mombo, S., Dumat, C., Deola, F., & Gers, C., 2016. Ecological changes in historically polluted soils: Metal (loid) bioaccumulation in microarthropods and their impact on community structure. Geoderma, 271, 181–190,

     https://doi.org/10.1016/j.geoderma.2016.02.011

Baratzadeh Poustchi, F., Yazdi, F. T., Heidari, A., & Moosavi, Z., 2020. Evaluation of chromium accumulation and resulting histopathological changes in Libyan jirds (Mammals, Rodentia), affected by effluent from Ghazghan leather industrial town, Iran. Environmental Science and Pollution Research, 27(31), 39343–39353, https://doi.org/10.1007/s11356-020-09801-1.

Bretfeld, G., 1999. Synopses on palaearctic collembola: symphypleona. Abhandlungen Und Berichte Des Naturkundemuseums Gorlitz, 71, 1–318.

https://cir.nii.ac.jp/crid/1571980074212653696.

Calabrese, E. J., & Baldwin, L. A., 2003. Toxicology rethinks its central belief. Nature, 421(6924), 691–692, https://doi.org/10.1038/421691a.

Coulibaly, S. F. M., Coudrain, V., Hedde, M., Brunet, N., Mary, B., Recous, S., & Chauvat, M., 2017. Effect of different crop management practices on soil Collembola assemblages: A 4-year follow-up. Applied Soil Ecology, 119, 354–366.

 https://doi.org/10.1016/j.apsoil.2017.06.013.

Crouau, Y., & Cazes, L., 2005. Unexpected reduction in reproduction of collembola exposed to an arsenic‐contaminated soil. Environmental Toxicology and Chemistry: An International Journal, 24(7), 1716–1720, https://doi.org/10.1897/04-265R.1.

Errington, I., King, C. K., Houlahan, S., George, S. C., Michie, A., & Hose, G. C., 2018. The influence of vegetation and soil properties on springtail communities in a diesel-contaminated soil. Science of the Total Environment, 619, 1098–1104.

 https://doi.org/10.1016/j.scitotenv.2017.11.186.

Farias, D. R., Hurd, C. L., Eriksen, R. S., & Macleod, C. K., 2018. Macrophytes as bioindicators of heavy metal pollution in estuarine and coastal environments. Marine Pollution Bulletin, 128, 175–184, https://doi.org/10.1016/j.marpolbul.2018.01.023.

Fiera, C., 2009. Biodiversity of Collembola in urban soils and their use as bioindicators for pollution. Pesquisa Agropecuária Brasileira, 44, 868–873, https://doi.org/10.1590/S0100-204X2009000800010.

Fjellberg, A., 2007. The Collembola of Fennoscandia and Denmark, Part II: Entomobryomorpha and Symphypleona. Brill.

https://books.google.com/books?id=28ewCQAAQBAJ&lpg=PA1&ots=8cuWolrdDU&dq=Fjellberg%2C%20A.%20(2007).%20The%20Collembola%20of%20Fennoscandia%20and%20Denmark%2C%20Part%20II%3A%20Entomobryomorpha%20and%20Symphypleona.%20Brill.&lr&pg=PA1#v=onepage&q=Fjellberg,%20A.%20(2007).%20The%20Collembola%20of%20Fennoscandia%20and%20Denmark,%20Part%20II:%20Entomobryomorpha%20and%20Symphypleona.%20Brill.&f=false.

Kuznetsova, N. A., 2009. Soil-dwelling Collembola in coniferous forests along the gradient of pollution with emissions from the Middle Ural Copper Smelter. Russian Journal of Ecology, 40(6), 415–423, https://doi.org/10.1134/S106741360906006X.

Kwiatkowska-Malina, J., 2018. Functions of organic matter in polluted soils: The effect of organic amendments on phytoavailability of heavy metals. Applied Soil Ecology, 123, 542–545, https://doi.org/10.1016/j.apsoil.2017.06.021.

Li, S., Li, J., Li, Z., Ke, X., Wu, L., & Christie, P., 2021. Toxic effects of norfloxacin in soil on fed and unfed Folsomia candida (Isotomidae: Collembola) and on gut and soil microbiota. Science of The Total Environment, 788, 147793,

 https://doi.org/10.1016/j.scitotenv.2021.147793.

Liu, M., Xu, J., Krogh, P. H., Song, J., Wu, L., Luo, Y., & Ke, X., 2018. Assessment of toxicity of heavy metal-contaminated soils toward Collembola in the paddy fields supported by laboratory tests. Environmental Science and Pollution Research, 25(17), 16969–16978,

 https://doi.org/10.1007/s11356-018-1864-y.

Manickavasagam, S., Sudhan, C., & Aanand, S., 2019. Bioindicators in aquatic environment and their significance. Journal of Aquaculture in the Tropics, 34(1/2), 73–79,

 http://doi.org/10.32381/JAT.2019.34.1-2.6.

Mirsal, I. A., 2008. Soil pollution. Springer, https://doi.org/10.1007/978-3-540-70777-6.

Nursita, A. I., Singh, B., & Lees, E., 2005. The effects of cadmium, copper, lead, and zinc on the growth and reproduction of Proisotoma minuta Tullberg (Collembola). Ecotoxicology and Environmental Safety, 60(3), 306–314, https://doi.org/10.1016/j.ecoenv.2004.05.001.

Park, J., Lee, S., Lee, E., Noh, H., Seo, Y., Lim, H., Shin, H., Lee, I., Jung, H., & Na, T., 2019. Probabilistic ecological risk assessment of heavy metals using the sensitivity of resident organisms in four Korean rivers. Ecotoxicology and Environmental Safety, 183, 109483, https://doi.org/10.1016/j.ecoenv.2019.109483

Potapov, M., 2002. Synopses on Palaearctic Collembola. Volume 3, Isotomidae. In: Dunger, W. (Ed). Staatliches Museum Fur Naturkunde Gorlitz,

https://www.researchgate.net/publication/284409981_Synopses_on_Palaearctic_Collembola_Isotomidae.

Rekhate, C. V, & Srivastava, J. K., 2021. Effectiveness of O3/Fe2+/H2O2 process for detoxification of heavy metals in municipal wastewater by using RSM. Chemical Engineering and Processing-Process Intensification, 165, 108442,

 https://doi.org/10.1016/j.cep.2021.108442.

Rochefort, S., Therrien, F., Shetlar, D. J., & Brodeur, J., 2006. Species diversity and seasonal abundance of Collembola in turfgrass ecosystems of North America. Pedobiologia, 50(1), 61–68, https://doi.org/10.1016/j.pedobi.2005.10.007.

Santamaría, J. M., Moraza, M. L., Elustondo, D., Baquero, E., Jordana, R., Lasheras, E., Bermejo, R., & Ariño, A. H., 2012. Diversity of Acari and Collembola along a pollution gradient in soils of a pre-Pyrenean forest ecosystem. Environmental Engineering & Management Journal (EEMJ), 11(6), https://dadun.unav.edu/handle/10171/27602.

Santorufo, L., Van Gestel, C. A. M., Rocco, A., & Maisto, G., 2012. Soil invertebrates as bioindicators of urban soil quality. Environmental Pollution, 161, 57–63, https://doi.org/10.1016/j.envpol.2011.09.042.

Sharma, N., Sodhi, K. K., Kumar, M., & Singh, D. K., 2021. Heavy metal pollution: Insights into chromium eco-toxicity and recent advancement in its remediation. Environmental Nanotechnology, Monitoring & Management, 15, 100388,

 https://doi.org/10.1016/j.enmm.2020.100388.

Sharma, P., Pandey, A. K., Kim, S.-H., Singh, S. P., Chaturvedi, P., & Varjani, S., 2021. Critical review on microbial community during in-situ bioremediation of heavy metals from industrial wastewater. Environmental Technology & Innovation, 101826,

 https://doi.org/10.1016/j.eti.2021.101826.

Sheikh, M. M., Rezaei, M. R., & Nasseri, M. A., 2013. Heavy metals (Hg, Cr and Pb) concentrations in water and sediment of Kashaf Rood River. Toxicology and Environmental Health Sciences, 5(2), 65–70, https://doi.org/10.1007/s13530-013-0159-4.

Sławski, M., & Sławska, M., 2019. Seven decades of spontaneous forest regeneration after large-scale clear-cutting in Białowieża forest do not ensure the complete recovery of collembolan assemblages. Forests, 10(11), 948, https://doi.org/10.3390/f10110948.

Sterzyńska, M., Nicia, P., Zadrożny, P., Fiera, C., Shrubovych, J., & Ulrich, W., 2018. Urban springtail species richness decreases with increasing air pollution. Ecological Indicators, 94, 328–335, https://doi.org/10.1016/j.ecolind.2018.06.063.

Tang, J., Zhang, J., Ren, L., Zhou, Y., Gao, J., Luo, L., Yang, Y., Peng, Q., Huang, H., & Chen, A., 2019. Diagnosis of soil contamination using microbiological indices: A review on heavy metal pollution. Journal of Environmental Management, 242, 121–130,

 https://doi.org/10.1016/j.jenvman.2019.04.061.

Thibaud, J.-M., 2004. Synopses on palaearctic collembola: hypogastruridae. Abhandlungen Und Berichte Des Naturkundemuseums Gorlitz, 75, 1–287,

https://cir.nii.ac.jp/crid/1572543025726348544#citations_container.

Tidona, S., Van Gestel, C. A. M., Morais, P. V, & Sousa, J. P., 2009. The use of Collembola avoidance tests to characterize sewage sludges as soil amendments. Chemosphere, 77(11), 1526–1533, https://doi.org/10.1016/j.chemosphere.2009.09.056.

Wang, Y., Slotsbo, S., & Holmstrup, M., 2022. Soil dwelling springtails are resilient to extreme drought in soil, but their reproduction is highly sensitive to small decreases in soil water potential. Geoderma, 421, 115913, https://doi.org/10.1016/j.geoderma.2022.115913.

Winkler, D., Bidló, A., Bolodár-Varga, B., Erdő, Á., & Horváth, A., 2018. Long-term ecological effects of the red mud disaster in Hungary: Regeneration of red mud flooded areas in a contaminated industrial region. Science of The Total Environment, 644, 1292–1303, https://doi.org/10.1016/j.scitotenv.2018.07.059.

Xu, J., Ke, X., Krogh, P. H., Wang, Y., Luo, Y., & Song, J., 2009. Evaluation of growth and reproduction as indicators of soil metal toxicity to the Collembolan, Sinella curviseta. Insect Science, 16(1), 57–63. file:///C:/Users/Pardis 32623410/Documents/mendpay/j.1744-7917.2009.00254.x(1).pdf, https://doi.org/10.1111/j.1744-7917.2009.00254.x.

Yan, N., & Marschner, P., 2013. Response of soil respiration and microbial biomass to changing EC in saline soils. Soil Biology and Biochemistry, 65, 322–328, https://doi.org/10.1016/j.soilbio.2013.06.008.

Ying, D., Zhu, L. I., Xin, K. E., Longhua, W. U., & Shengpeng, Z. U. O., 2021. Toxicity of lead pollution to the collembolan Folsomia candida in Ferri-Udic Cambosols. Pedosphere, 31(4), 627–637, https://doi.org/10.1016/S1002-0160(21)60008-5.

Zhang, H., Zhang, F., Song, J., Tan, M. L., & Johnson, V. C., 2021. Pollutant source, ecological and human health risks assessment of heavy metals in soils from coal mining areas in Xinjiang, China. Environmental Research, 202, 111702, https://doi.org/10.1016/j.envres.2021.111702.