The interactions between nematode and microbial communities offer significant insights into the impact of organic amendments on the productivity of Miscanthus × giganteus cultivated on marginal lands
Abstract
The investigation is devoted to the analysis of the impact of organic fertilisers, in particular biochar derived from sewage sludge, on the productivity of the energy crop Miscanthus × giganteus and soil health on marginal lands. The results of long-term observations show that among organic additives, biochar demonstrates the most pronounced stabilising effect on the structure of the nematode community, although its impact on the total number of nematodes is limited. The application of biochar increased the diversity of trophic groups and modified the soil trophic network, which was dose-dependent. The experiment also revealed a significant impact of organic additives on the ecological indicators of nematode communities. In particular, the use of biochar significantly increased the Maturity Index (MI) and the Structural Index (SI), which indicates an improvement in the stability and complexity of the soil ecosystem. Reducing the number of migratory endoparasites and other plant-parasitic nematodes, such as Pratylenchus spp. was crucial in increasing the yield of M. × giganteus. The most pronounced changes were observed when biochar was applied at 10% (BD2). The field trial also assessed the impact of organic amendments on soil microbiological characteristics. Although the total number of bacteria and fungi did not change significantly, there was an increase in the number of Pseudomonas bacteria in the biochar-treated samples. This confirms the role of biochar as a stimulator of the growth of beneficial microorganisms and improvement of soil microbial activity. At the same time, the activity of dehydrogenase, which is an indicator of microbial activity, did not change significantly under the influence of additives. The test findings indicate that the addition of biochar has a beneficial effect on the yield of M. × giganteus, contributing to an increase in green mass at harvest. The impact of organic amendments was long-lasting, demonstrating the potential to increase the productivity of energy crops on marginal lands. Reducing the number of plant-parasitic nematodes, especially migratory endoparasites, was a key factor in improving yields. The outcomes of the study confirm the significance of an integrated approach to the application of organic amendments to improve soil health and increase the productivity of energy crops. The dose-dependent effects of biochar indicate the need to adapt application strategies to specific agroecosystems. Further research should focus on analysing the long-term effects of organic fertilisers on the functioning of trophic networks and microbiological processes in the soil.References
Ajema, L. (2018). Effects of biochar application on beneficial soil organism – Review. International Journal of Research Studies in Science, Engineering and Technology, 5(5), 9–18.
Alef, K., & Nannipieri, P. (1995). Enzyme activities. In: Alef, K., & Nannipieri, P. (Eds.). Methods in applied soil microbiology and biochemistry. Elsevier, London, New York, San Francisco. Pp. 311–373.
Andrássy, I. (2007). Free-living nematodes of Hungary (Nematoda Errantia). Budapest.
Andriuzzi, W. S., & Wall, D. H. (2018). Grazing and resource availability control soil nematode body size and abundance-mass relationship in semi-arid grassland. Journal of Animal Ecology, 87(5), 1407–1417.
Andrusiv, U., Zelinska, H., Kupalova, H., Bezuhla, L., & Bieloborodova, M. (2024). The influence of the ecological situation in Ukraine on the life expectancy and health of the population. Ekológia (Bratislava), 43(2), 219–226.
Anuroopa, N., Ram, A. B., Ranadev, P., Bagyaraj, D. J., & Ashwin, R. (2021). Pseudomonas species in soil as a natural resource for plant growth promotion and biocontrol characteristics – An overview. Madras Agricultural Journal, 108(10–12), 1–14.
Bilandžija, N., Voća, N., Leto, J., Jurišić, V., Grubor, M., Matin, A., Geršić, A., & Krička, T. (2018). Yield and biomass composition of Miscanthus x giganteus in the mountain area of Croatia. Transactions of Famena, 42(S1), 51–60.
Bolan, S., Hou, D., Wang, L., Hale, L., Egamberdieva, D., Tammeorg, P., Li, R., Wang, B., Xu, J., Wang, T., Sun, H., Padhye, L. P., Wang, H., Siddique, K. H. M., Rinklebe, J., Kirkham, M. B., & Bolan, N. (2023). The potential of biochar as a microbial carrier for agricultural and environmental applications. Science of the Total Environment, 886(163968), 127–186.
Bongers, T. (1990). The maturity index: An ecological measure of environmental disturbance based on nematode species composition. Oecologia, 83(1), 14–19.
Brzeski, M. W. (1998). Nematodes of Tylenchina in Poland and temperate Europe. Muzeum i Instytutu Zoologii, Polska Akademia Nauk, Warsaw, Poland.
Brzezińska, M., & Włodarczyk, T. (2005). Enzymes of intracellular redox metabolism (oxidoreductases). Acta Agrophysica, 3, 11–26.
Burland, A., & von Cossel, M. (2023). Towards managing biodiversity of European marginal agricultural land for biodiversity-friendly biomass production. Agronomy, 13(6), 16–51.
Chauhan, P., Sharma, N., Tapwal, A., Kumar, A., Verma, G. S., Meena, M., Seth, C. S., & Swapnil, P. (2023). Soil microbiome: Diversity, benefits and snteractions with plants. Sustainability, 15(19), 14–43.
Cole, E. J., Barker, A. V., Zandvakili, O. R., Sadeghpour, A., Xing, B., Hashemi, M., Allan-Perkins, E., & Jung, G. (2021). Soil nutrient and nematode community changes in response to hardwood charcoal application. Communications in Soil Science and Plant Analysis, 52(9), 917–925.
Cui, J., Yang, B., Zhang, M., Song, D., Xu, X., Ai, C., Liang, G., & Zhou, W. (2023). Investigating the effects of organic amendments on soil microbial composition and its linkage to soil organic carbon: A global meta-analysis. Science of the Total Environment, 894(164899), 45–84.
Dauber, J., & Miyake, S. (2016). To integrate or to segregate food crop and energy crop cultivation at the landscape scale? Perspectives on biodiversity conservation in agriculture in Europe. Energy, Sustainability and Society, 6(1), 25–48.
De Laporte, A. V., & Ripplinger, D. G. (2019). Economic viability of perennial grass biomass feedstock in northern climates. Industrial Crops and Products, 128, 213–220.
Diacono, M., & Montemurro, F. (2011). Long-term effects of organic amendments on soil fertility. Sustainable Agriculture, 2, 761–786.
Dignam, B. E. A., O’Callaghan, M., Condron, L. M., Raaijmakers, J. M., Kowalchuk, G. A., & Wakelin, S. A. (2019). Impacts of long-term plant residue management on soil organic matter quality, Pseudomonas community structure and disease suppressiveness. Soil Biology and Biochemistry, 135, 396–406.
Domene, X., Mattana, S., & Sánchez-Moreno, S. (2021). Biochar addition rate determines contrasting shifts in soil nematode trophic groups in outdoor mesocosms: An appraisal of underlying mechanisms. Applied Soil Ecology, 158(103788), 15–37.
Du Preez, G., Daneel, M., De Goede, R., Du Toit, M. J., Ferris, H., Fourie, H., Geisen, S., Kakouli-Duarte, T., Korthals, G., Sánchez-Moreno, S., & Schmidt, J. H. (2022). Nematode-based indices in soil ecology: Application, utility, and future directions. Soil Biology and Biochemistry, 169, 10–40.
Dubis, B., Szatkowski, A., & Jankowski, K. J. (2022). Sewage sludge, digestate, and mineral fertilizer application affects the yield and energy balance of Amur silvergrass. Industrial Crops and Products, 175, 11–35.
Eche, C. O., Oluwatayo, J. I., Esang, D. M., Madina, P., & Uloko, A. (2021). Antihelminthic effects of sawdust mixed with eucalyptus biochar against plant-parasitic nematodes associated with Beniseed (Sesamum indicum L.) crop in Makurdi, North-Central Nigeria. Pakistan Journal of Nematology, 39(2), 99–105.
Felten, D., & Emmerling, C. (2012). Accumulation of Miscanthus-derived carbon in soils in relation to soil depth and duration of land use under commercial farming conditions. Journal of Plant Nutrition and Soil Science, 175(5), 661–670.
George, C., Kohler, J., & Rillig, M. C. (2016). Biochars reduce infection rates of the root-lesion nematode Pratylenchus penetrans and associated biomass loss in carrot. Soil Biology and Biochemistry, 95, 11–18.
Gould, W. D., Hagedorn, C., Bardinelli, T. R., & Zablotowicz, R. M. (1985). New selective media for enumeration and recovery of fluorescent pseudomonads from various habitats. Applied and Environmental Microbiology, 49(1), 28–32.
Gurmessa, B., Cocco, S., Ashworth, A. J., Udawatta, R. P., Cardelli, V., Ilari, A., Serrani, D., Fornasier, F., Del Gatto, A., Pedretti, E. F., & Corti, G. (2024). Short term effects of digestate and composted digestate on soil health and crop yield: Implications for sustainable biowaste management in the bioenergy sector. Science of the Total Environment, 906, 167208.
Han, G., Lan, J., Chen, Q., Yu, C., & Bie, S. (2017). Response of soil microbial community to application of biochar in cotton soils with different continuous cropping years. Scientific Reports, 7(1), 10184.
Herbrich, M., Gerke, H. H., & Sommer, M. (2018). Root development of winter wheat in erosion-affected soils depending on the position in a hummocky ground moraine soil landscape. Journal of Plant Nutrition and Soil Science, 181(2), 147–157.
Hu, C., & Qi, Y. (2010). Effect of compost and chemical fertilizer on soil nematode community in a Chinese maize field. European Journal of Soil Biology, 46(3–4), 230–236.
Huang, K., Zhang, J., Tang, G., Bao, D., Wang, T., & Kong, D. (2023). Impacts and mechanisms of biochar on soil microorganisms. Plant, Soil and Environment, 69(2), 45–54.
Karimi, B., Sadet-Bourgeteau, S., Cannavacciuolo, M., Chauvin, C., Flamin, C., Haumont, A., Jean-Baptiste, V., Reibel, A., Vrignaud, G., & Ranjard, L. (2022). Impact of biogas digestates on soil microbiota in agriculture: A review. Environmental Chemistry Letters, 20(5), 3265–3288.
Kekelis, P., Papatheodorou, E. M., Terpsidou, E., Dimou, M., Aschonitis, V., & Monokrousos, N. (2022). The free-living nematodes as indicators of the soil quality in relation to the clay content, when coffee waste is applied. Agronomy, 12(11), 2702.
Khan, M., & Scullion, J. (2000). Effect of soil on microbial responses to metal contamination. Environmental Pollution, 110(1), 115–125.
Khan, S., Zahoor, M., Sher Khan, R., Ikram, M., & Islam, N. U. (2023). The impact of silver nanoparticles on the growth of plants: The agriculture applications. Heliyon, 9(6), e16928.
Kharytonov, M. M., Klimkina, I. I., Martynova, N. V., Rula, I. V., Gispert, M., Pardini, G. M., & Wang, J. V. (2020). The biochar impact on miscanthus and sunflower growth in marginal lands. Agrology, 3(1), 3–11.
Kilowasid, L. M. H., Syamsudin, T. S., Sulystiawati, E., & Susilo, F.-X. (2014). Structure of soil food web in smallholder cocoa plantation, south Konawe District, Southeast Sulawesi, Indonesia. Agrivita Journal of Agricultural Science, 36(1), 33–47.
Kunakh, O. M., Bondarev, D. L., Gubanova, N. L., Domnich, A. V., & Zhukov, O. V. (2022). Multiscale oscillations of the annual course of temperature affect the spawning events of rudd (Scardinus erythrophthalmus). Regulatory Mechanisms in Biosystems, 13(2), 180–188.
Kunakh, O. M., Volkova, A. M., Tutova, G. F., & Zhukov, O. V. (2023). Diversity of diversity indices: Which diversity measure is better? Biosystems Diversity, 31(2), 131–146.
Larsen, S. U., Jørgensen, U., Kjeldsen, J. B., & Lærke, P. E. (2014). Long-term Miscanthus yields influenced by location, genotype, row distance, fertilization and harvest season. Bioenergy Research, 7(2), 620–635.
Lehmann, J., Gaunt, J., & Rondon, M. (2006). Bio-char sequestration in terrestrial ecosystems – A review. Mitigation and Adaptation Strategies for Global Change, 11(2), 403–427.
Lehmann, J., Rillig, M. C., Thies, J., Masiello, C. A., Hockaday, W. C., & Crowley, D. (2011). Biochar effects on soil biota – A review. Soil Biology and Biochemistry, 43(9), 1812–1836.
Li, J., Li, H., Shang, J., Liu, K., He, Y., & Shao, X. (2023). The synergistic effect of biochar and microorganisms greatly improves vegetation and microbial structure of degraded alpine grassland on Qinghai-Tibet Plateau. Agronomy, 13(9), 2203.
Liu, X., Zhang, D., Li, H., Qi, X., Gao, Y., Zhang, Y., Han, Y., Jiang, Y., & Li, H. (2020). Soil nematode community and crop productivity in response to 5-year biochar and manure addition to yellow cinnamon soil. BMC Ecology, 20(1), 39.
Mamirova, A., & Pidlisnyuk, V. (2024). The economic and environmental aspects of Miscanthus × giganteus phytomanagement applied to non-agricultural land. Agronomy, 14(4), 791.
Martin, J. (1950). Use of acid, rose bengal, and streptomycin in the plate method for estimating soil fungi. Soil Science, 69(3), 215–232.
Molozhon, K. O., Lisovets, O. I., Kunakh, O. M., & Zhukov, O. V. (2023). The structure of beta-diversity explains why the relevance of phytoindication increases under the influence of park reconstruction. Regulatory Mechanisms in Biosystems, 14(4), 634–651.
Mykhailyuk, T., Lisovets, O., & Tutova, H. (2023). Steppe vegetation islands in the gully landscape system: Hemeroby, naturalness and phytoindication of ecological regimes. Regulatory Mechanisms in Biosystems, 14(4), 581–594.
Panchenko, K. (2022). Bioclimatic projection of the ecological niche of curly mallow (Malva verticillata) based on the forecast of the dynamics of the geographical range in the context of global climate change. Regulatory Mechanisms in Biosystems, 13(4), 400–411.
Panchenko, K., Podorozhnyi, S., & Diuzhykova, T. (2024). Predicting organic carbon in European soils: Only in Southern Ukraine can we expect an increase in humus content. Regulatory Mechanisms in Biosystems, 15(1), 24–30.
Pidlisnyuk, V., Newton, R., & Mamirova, A. (2021). Miscanthus biochar value chain – A review. Journal of Environmental Management, 290, 112611.
Pires, D., Orlando, V., Collett, R. L., Moreira, D., Costa, S. R., & Inácio, M. L. (2023). Linking nematode communities and soil health under climate change. Sustainability, 15(15), 11747.
Poveda, J., Martínez-Gómez, Á., Fenoll, C., & Escobar, C. (2021). The use of biochar for plant pathogen control. Phytopathology, 111(9), 1490–1499.
Pressler, Y., Foster, E. J., Moore, J. C., & Cotrufo, M. F. (2017). Coupled biochar amendment and limited irrigation strategies do not affect a degraded soil food web in a maize agroecosystem, compared to the native grassland. GCB Bioenergy, 9(8), 1344–1355.
Puissant, J., Villenave, C., Chauvin, C., Plassard, C., Blanchart, E., & Trap, J. (2021). Quantification of the global impact of agricultural practices on soil nematodes: A meta-analysis. Soil Biology and Biochemistry, 161, 108383.
Rahman, L., Whitelaw-Weckert, M. A., & Orchard, B. (2014). Impact of organic soil amendments, including poultry-litter biochar, on nematodes in a Riverina, New South Wales, vineyard. Soil Research, 52(6), 604.
Raniak, A., & Izakovičová, Z. (2024). Global megatrends impacts on the landscape, analysis based on key drivers of the megatrends and landscape change: Case study of Danubian Lowland, Slovakia. Ekológia (Bratislava), 43(2), 183–191.
Rashid, M. I., Mujawar, L. H., Shahzad, T., Almeelbi, T., Ismail, I. M. I., & Oves, M. (2016). Bacteria and fungi can contribute to nutrients bioavailability and aggregate formation in degraded soils. Microbiological Research, 183, 26–41.
Renčo, M. (2013). Organic amendments of soil as useful tools of plant parasitic nematodes control. Helminthologia, 50(1), 3–14.
Saletnik, B., Zagula, G., Bajcar, M., Czernicka, M., & Puchalski, C. (2018). Biochar and biomass ash as a soil ameliorant: The effect on selected soil properties and yield of giant Miscanthus (Miscanthus x giganteus). Energies, 11(10), 2535.
Schad, P. (2023). World reference base for soil resources – Its fourth edition and its history. Journal of Plant Nutrition and Soil Science, 186(2), 151–163.
Seinhorst, J. W. (1966). Killing nematodes for taxonomic study with hot f.a. 4: 1. Nematologica, 12(1), 178–178.
Shi, G., Luan, L., Zhu, G., Zeng, Z., Zheng, J., Shi, Y., Sun, B., & Jiang, Y. (2023). Interaction between nematodes and bacteria enhances soil carbon sequestration under organic material amendments. Frontiers in Microbiology, 14, 1155088.
Siebielec, G., Siebielec, S., & Lipski, D. (2018). Long-term impact of sewage sludge, digestate and mineral fertilizers on plant yield and soil biological activity. Journal of Cleaner Production, 187, 372–379.
Sieriebriennikov, B., Ferris, H., & de Goede, R. G. M. (2014). NINJA: An automated calculation system for nematode-based biological monitoring. European Journal of Soil Biology, 61, 90–93.
Soong, J. L., Dam, M., Wall, D. H., & Cotrufo, M. F. (2017). Below-ground biological responses to pyrogenic organic matter and litter inputs in grasslands. Functional Ecology, 31(1), 260–269.
Stefanovska, T., Skwiercz, A., Pidlisnyuk, V., Zhukov, O., Kozacki, D., Mamirova, A., Newton, R. A., & Ust’ak, S. (2022). The short-term effects of amendments on nematode communities and diversity patterns under the cultivation of Miscanthus × giganteus on marginal land. Agronomy, 12(9), 2063.
Suci Rahayu, D., & Puspita Sari, N. (2017). Development of Pratylenchus coffeae in biochar applied soil, coffee roots and its effect on plant growth. Pelita Perkebunan, 33(1), 24–32.
Szczygieł, A. (1971). Application of the centrifugal method for extraction of nematodes from soil. Journal of Progress in Agricultural Sciences, 12, 169–179.
Tao, C., Li, R., Xiong, W., Shen, Z., Liu, S., Wang, B., Ruan, Y., Geisen, S., Shen, Q., & Kowalchuk, G. A. (2020). Bio-organic fertilizers stimulate indigenous soil Pseudomonas populations to enhance plant disease suppression. Microbiome, 8(1), 137.
van den Hoogen, J., Geisen, S., Routh, D., Ferris, H., Traunspurger, W., Wardle, D. A., de Goede, R. G. M., Adams, B. J., Ahmad, W., Andriuzzi, W. S., Bardgett, R. D., Bonkowski, M., Campos-Herrera, R., Cares, J. E., Caruso, T., de Brito Caixeta, L., Chen, X., Costa, S. R., Creamer, R., … Crowther, T. W. (2019). Soil nematode abundance and functional group composition at a global scale. Nature, 572(7768), 194–198.
Van Sinh, N., Kato, R., Linh, D. T. T., Phuong, N. T. K., & Toyota, K. (2022). Influence of rice husk biochar on soil nematode community under upland and flooded conditions: A microcosm experiment. Agronomy, 12(2), 378.
Verschoor, B. C., de Goede, R. G. M., de Hoop, J.-W., & de Vries, F. W. (2001). Seasonal dynamics and vertical distribution of plant-feeding nematode communities in grasslands. Pedobiologia, 45(3), 213–233.
Vithanage, M., Bandara, T., Al-Wabel, M. I., Abduljabbar, A., Usman, A. R. A., Ahmad, M., & Ok, Y. S. (2018). Soil enzyme activities in waste biochar amended multi-metal contaminated soil; Effect of different pyrolysis temperatures and application rates. Communications in Soil Science and Plant Analysis, 49(5), 635–643.
Wiedener, K., & Glaser, B. (2013). Biochar-fungi interactions in soil. In: Ladygina, N., & Rineau, F. (Eds.). Biochar and soil biota. CRC Press, Boca Raton. Pp. 1–31.
Yan, H., Liu, C., Yu, W., Zhu, X., & Chen, B. (2023). The aggregate distribution of Pseudomonas aeruginosa on biochar facilitates quorum sensing and biofilm formation. Science of the Total Environment, 856, 159034.
Yeates, G. W., Bongers, T., De Goede, R. G., Freckman, D. W., & Georgieva, S. S. (1993). Feeding habits in soil nematode families and genera – an outline for soil ecologists. Journal of Nematology, 25(3), 315–331.
Zhang, R., Zhang, M., Mou, H., An, Z., Fu, H., Su, X., Chen, C., Chen, J., Lin, H., & Sun, F. (2023). Comparation of mesophilic and thermophilic anaerobic co-digestion of food waste and waste activated sludge driven by biochar derived from kitchen waste. Journal of Cleaner Production, 408, 137123.
Zhang, X., Li, Q., Liang, W., Zhang, M., Bao, X., & Xie, Z. (2013). Soil nematode response to biochar addition in a chinese wheat field. Pedosphere, 23(1), 98–103.
Zymaroieva, A., Zhukov, O., Fedoniuk, T., Pinkina, T., & Hurelia, V. (2021). The relationship between landscape diversity and crops productivity: Landscape scale study. Journal of Landscape Ecology, 14(1), 39–58.
