Precipitation regulated soil nematode community and footprint in cropland ecosystems
Pingting Guan, Jianan Li, Cao Hao, Jingjing Yang, Lihong Song, Ximei Niu, Ping Wang, Mohammad Mahamood, Donghui Wu
Precipitation regulated soil nematode community and footprint in cropland ecosystems
● Nematode abundance and footprint show unimodal patterns with precipitation levels.
● MAP governed nematode diversity along the precipitation gradient of agroecosystem.
● Soil pH determined nematode abundance and footprint in low precipitation levels.
Precipitation plays a crucial role in global biodiversity change across terrestrial ecosystems. Precipitation is proven to affect soil organism diversity in natural ecosystems. However, how precipitation change affects the function of the soil nematode community remains unclear in cropland ecosystems. Here, we tested soil nematode communities from different precipitation sites (300 mm to 900 mm) of the agricultural ecosystem. The abundance of total nematodes, fungivores, and plant parasites, together with the footprint of fungivores was significantly affected by mean annual precipitation (MAP) in cropland ecosystem. Plant parasites diversity and footprint showed negative relationships with MAP. The random forest suggested plant parasite footprint was the most responsive to MAP. The structural equation model revealed that MAP affected nematode abundance and footprint indirectly via soil pH; nematode diversity was affected by MAP directly. We conclude that precipitation could act as the main selection stress for nematode diversity among the large gradient of agricultural ecosystems. However, the soil pH may act as a stress factor in determining nematode community and carbon flow in the soil food web. Our study emphasized that using nematode value by trophic group would provide a deep understanding of nematode response to precipitation in cropland ecosystems.
soil nematode community / nematode carbon flux / the Northeast China Transect / agricultural ecosystem / precipitation
[1] |
Andrés, P., Moore, J.C., Cotrufo, F., Denef, K., Haddix, M.L., Molowny–Horas, R., Riba, M., Wall, D.H., 2017. Grazing and edaphic properties mediate soil biotic response to altered precipitation patterns in a semiarid prairie. Soil Biology & Biochemistry113, 263–274.
CrossRef
Google scholar
|
[2] |
Ankrom, K.E., Franco, A.L.C., Fonte, S.J., Gherardi, L.A., de Tomasel, C.M., Wepking, C., Guan, P., Cui, S., Sala, O.E., Wall, D.H., 2022. Ecological maturity and stability of nematode communities in response to precipitation manipulations in grasslands. Applied Soil Ecology170, 104263.
CrossRef
Google scholar
|
[3] |
Arbuckle, J.L., 2006, Amos (Version 70) [Computer Program] SPSS Chicago.
|
[4] |
Bakonyi, G., Nagy, P., Kovács-Láng, E., Kovács, E., Barabás, S., Répási, V., Seres, A., 2007. Soil nematode community structure as affected by temperature and moisture in a temperate semiarid shrubland. Applied Soil Ecology37, 31–40.
CrossRef
Google scholar
|
[5] |
Bellard, C., Bertelsmeier, C., Leadley, P., Thuiller, W., Courchamp, F., 2012. Impacts of climate change on the future of biodiversity. Ecology Letters15, 365–377.
CrossRef
Google scholar
|
[6] |
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
|
[7] |
Cesarz, S., Ciobanu, M., Wright, A.J., Ebeling, A., Vogel, A., Weisser, W.W., Eisenhauer, N., 2017. Plant species richness sustains higher trophic levels of soil nematode communities after consecutive environmental perturbations. Oecologia184, 715–728.
CrossRef
Google scholar
|
[8] |
Cesarz, S., Reich, P.B., Scheu, S., Ruess, L., Schaefer, M., Eisenhauer, N., 2015. Nematode functional guilds not trophic groups reflect shifts in soil food webs and processes in response to interacting global change factors. Pedobiologia58, 23–32.
CrossRef
Google scholar
|
[9] |
Crotty, F.V., Fychan, R., Scullion, J., Sanderson, R., Marley, C.L., 2015. Assessing the impact of agricultural forage crops on soil biodiversity and abundance. Soil Biology & Biochemistry91, 119–126.
CrossRef
Google scholar
|
[10] |
Cui, S., Han, X., Xiao, Y., Wu, P., Zhang, S., Abid, A., Zheng, G., 2022. Increase in rainfall intensity promotes soil nematode diversity but offset by nitrogen addition in a temperate grassland. Science of the Total Environment825, 154039.
CrossRef
Google scholar
|
[11] |
Decraemer, W., Hunt, D.J., 2006. Structure and classification. Plant Nematology, CAB International, Wallingford, pp. 3–32
|
[12] |
Demeure, Y., Freckman, D.W., Van Gundy, S.D., 1979. Anhydrobiotic coiling of nematodes in soil. Journal of Nematology11, 189–195.
|
[13] |
Deng, L., Liu, G.B., Shangguan, Z.P., 2014. Land-use conversion and changing soil carbon stocks in China’s ‘Grain-for-Green’ Program: a synthesis. Global Change Biology20, 3544–3556.
CrossRef
Google scholar
|
[14] |
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
|
[15] |
Ferris, H., Bongers, de Goede, R.G.M. 2001. A framework for soil food web diagnostics: extension of the nematode faunal analysis concept. Applied Soil Ecology18, 13–29.
|
[16] |
Ferris, H., Sánchez–Moreno, S., Brennan, E.B., 2012. Structure functions and interguild relationships of the soil nematode assemblage in organic vegetable production. Applied Soil Ecology61, 16–25.
CrossRef
Google scholar
|
[17] |
Ferris, H., Venette, R.C., Lau, S.S., 1997. Population energetics of bacterial-feeding nematodes: Carbon and nitrogen budgets. Soil Biology & Biochemistry29, 1183–1194.
CrossRef
Google scholar
|
[18] |
Feyissa, A., Yang, F., Wu, J., Chen, Q., Zhang, D., Cheng, X., 2021. Soil nitrogen dynamics at a regional scale along a precipitation gradient in secondary grassland of China. Science of the Total Environment781, 146736.
CrossRef
Google scholar
|
[19] |
Franco, A.L.C., Gherardi, L.A., De Tomasel, C.M., Andriuzzi, W.S., Ankrom, K.E., Shaw, E.A., Bach, E.M., Guan, P., Sala, O.E., Wall, D.H., 2020. Root herbivory controls the effects of water availability on the partitioning between above- and below-ground grass biomass. Functional Ecology34, 2403–2410.
CrossRef
Google scholar
|
[20] |
Franco, A.L.C., Gherardi, L.A., De Tomasel, C.M., Andriuzzi, W.S., Ankrom, K.E., Shaw, E.A., Bach, E.M., Sala, O.E., Wall, D.H., 2019. Drought suppresses soil predators and promotes root herbivores in mesic but not in xeric grasslands. Proceedings of the National Academy of Sciences of the United States of America116, 12883–12888.
CrossRef
Google scholar
|
[21] |
Franco, A.L.C., Guan, P., Cui, S., De Tomasel, C.M., Gherardi, L.A., Sala, O.E., Wall, D.H., 2022. Precipitation effects on nematode diversity and carbon footprint across grasslands. Global Change Biology28, 2124–2132.
CrossRef
Google scholar
|
[22] |
Gao, Q., Zhang, X., 1997. A simulation study of responses of the northeast China transect to elevated CO2 and climate change. Ecological Applications7, 470–483.
|
[23] |
Global Soil Data Task Group, 2000. Global Gridded Surfaces of Selected Soil Characteristics (IGBP-DIS). ORNL DAAC, Oak Ridge, Tennessee, USA
|
[24] |
Gong, X., Chen, X., Geisen, S., Zhang, J., Zhu, H., Hu, F., Liu, M., 2021. Agricultural habitats are dominated by rapidly evolving nematodes. Soil Biology & Biochemistry155, 108183.
CrossRef
Google scholar
|
[25] |
Grace, J.B., 2006. Structural equation modeling and natural systems. Cambridge University Press, Cambridge
|
[26] |
Guo, Y., Fan, R., Zhang, X., Zhang, Y., Wu, D., McLaughlin, N., Zhang, S., Chen, X., Jia, S., Liang, A., 2020. Tillage-induced effects on SOC through changes in aggregate stability and soil pore structure. Science of the Total Environment703, 703134617.
CrossRef
Google scholar
|
[27] |
Ikoyi, I.O., Heuvelink, G.B.M., de Goede, R.G.M., 2021. Geostatistical modelling and mapping of nematode-based soil ecological quality indices in a polluted nature reserve. Pedosphere31, 670–682.
CrossRef
Google scholar
|
[28] |
Kardol, P., Cregger, M.A., Campany, C.E., Classen, A.T., 2010. Soil ecosystem functioning under climate change: plant species and community effects. Ecology91, 767–781.
CrossRef
Google scholar
|
[29] |
Kergunteuil, A., Campos-Herrera, R., Sánchez–Moreno, S., Vittoz, P., Rasmann, S., 2016. The abundance diversity and metabolic footprint of soil nematodes is highest in high elevation alpine grasslands. Frontiers in Ecology and Evolution4, 84.
CrossRef
Google scholar
|
[30] |
Knapp, A.K., Fay, P.A., Blair, J.M., Collins, S.L., Smith, M.D., Carlisle, J.D., Harper, C.W., Danner, B.T., Lett, M.S., McCarron, J.K., 2002. Rainfall variability carbon cycling and plant species diversity in a mesic grassland. Science298, 2202–2205.
CrossRef
Google scholar
|
[31] |
Köhl, L., Oehl, F., van der Heijden, M.G.A., 2014. Agricultural practices indirectly influence plant productivity and ecosystem services through effects on soil biota. Ecological Applications24, 1842–1853.
CrossRef
Google scholar
|
[32] |
Laganiãre, J., Anger, D.A., Pare, D., 2010. Carbon accumulation in agricultural soils after afforestation: a meta-analysis. Global Change Biology16, 439–453.
CrossRef
Google scholar
|
[33] |
Landesman, W.J., Treonis, A.M., Dighton, J., 2011. Effects of a one–year rainfall manipulation on soil nematode abundances and community composition. Pedobiologia54, 87–91.
CrossRef
Google scholar
|
[34] |
Lauenroth, W.K., Bradford, J.B., 2012. Ecohydrology of dry regions of the United States: water balance consequences of small precipitation events. Ecohydrology5, 46–53.
CrossRef
Google scholar
|
[35] |
Legendre, P., Legendre, L., 2012. Numerical Ecology. 3rd English ed. Elsevier
|
[36] |
Li, X., Zhu, H., Geisen, S., Bellard, C., Hu, F., Li, H., Chen, X., Liu, M., 2020. Agriculture erases climate constraints on soil nematode communities across large spatial scales. Global Change Biology26, 919–930.
CrossRef
Google scholar
|
[37] |
Liu, T., Mao, P., Shi, L., Wang, Z., Wang, X., He, X., Tao, L., Liu, Z., Zhou, L., Shao, Y., Fu, S., 2020. Contrasting effects of nitrogen deposition and increased precipitation on soil nematode communities in a temperate forest. Soil Biology & Biochemistry148, 107869.
CrossRef
Google scholar
|
[38] |
Luo, J., Zhang, X., Kou, X., Xie, H., Bao, X., Mahamood, M., Liang, W., 2021. Effects of residue mulching amounts on metabolic footprints based on production and respiration of soil nematodes in a long–term no-tillage system. Land Degradation & Development32, 2383–2392.
CrossRef
Google scholar
|
[39] |
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
|
[40] |
Moore, J.C., McCann, K., de Ruiter, P.C., 2005. Modeling trophic pathways nutrient cycling and dynamic stability in soils. Pedobiologia49, 499–510.
CrossRef
Google scholar
|
[41] |
Murrell, E.G., Barton, B.T., 2017. Warming alters prey density and biological control in conventional and organic agricultural systems. Integrative and Comparative Biology1, 1–13.
CrossRef
Google scholar
|
[42] |
Ni, J., Zhang, X.S., 2000. Climate variability ecological gradient and the Northeast China Transect (NECT). Journal of Arid Environments46, 313–325.
CrossRef
Google scholar
|
[43] |
Nicol, J.M., Turner, S.J., Coyne, D.L., den Nijs, L., Hockland, S., Tahna Maafi, Z., 2011. Current Nematode Threats to World Agriculture. In: Jones, J., Gheysen, G., Fenoll, C., eds. Genomics and Molecular Genetics of Plant-Nematode Interactions. Springer, Dordrecht
|
[44] |
Nie, Q., Xu, J., Ji, M., Cao, L., Yang, Y., Hong, Y., 2012. The vegetation coverage dynamic coupling with climatic factors in Northeast China Transect. Environmental Management50, 405–417.
CrossRef
Google scholar
|
[45] |
Nielsen, U.N., Ayres, E., Wall, D.H., Li, G., Bardgett, R.D., Wu, T., Garey, J.R., 2014. Global-scale patterns of assemblage structure of soil nematodes in relation to climate and ecosystem properties. Global Ecology and Biogeography23, 968–978.
CrossRef
Google scholar
|
[46] |
Oostenbrink, M., 1960. Estimating Nematode Populations by Some Selected Methods. In: Sasser, J.N., Jenkins, W.R., eds. Nematology. University of North Carolina Press, Chapel Hill
|
[47] |
Papatheodorou, E.M., Argyropoulou, M.D., Stamou, G.P., 2004. The effects of large- and small-scale differences in soil temperature and moisture on bacterial functional diversity and the community of bacterivorous nematodes. Applied Soil Ecology25, 37–49.
CrossRef
Google scholar
|
[48] |
Rehman, S., Gupta, V.K., Goyal, A.K., 2016. Identification and functional analysis of secreted effectors from phytoparasitic nematodes. BMC Microbiology16, 48.
CrossRef
Google scholar
|
[49] |
Sánchez–Moreno, S., Ferris, H., 2007. Suppressive service of the soil food web: Effects of environmental management. Agriculture, Ecosystems & Environment119, 75–87.
CrossRef
Google scholar
|
[50] |
Shen, C., Shi, Y., Fan, K., He, J.S., Adams, J.J., Ge, Y., Chu, H., 2019. Soil pH dominates elevational diversity pattern for bacteria in high elevation alkaline soils on the Tibetan Plateau. FEMS Microbiology Ecology95, fiz003.
CrossRef
Google scholar
|
[51] |
Siebert, J., Ciobanu, M., Schädler, M., Eisenhauer, N., 2020. Climate change and land use induce functional shifts in soil nematode communities. Oecologia192, 281–294.
CrossRef
Google scholar
|
[52] |
Slessarev, E.W., Lin, Y., Bingham, N.L., Johnson, J.E., Dai, Y., Schimel, J.P., Chadwick, O.A., 2016. Water balance creates a threshold in soil pH at the global scale. Nature540, 567–569.
CrossRef
Google scholar
|
[53] |
Song, M., Li, X., Jing, S., Lei, L., Wang, J., Wan, S., 2016. Responses of soil nematodes to water and nitrogen additions in an old-field grassland. Applied Soil Ecology102, 53–60.
CrossRef
Google scholar
|
[54] |
Townshend, J.L., 1963. A modification and evaluation of the apparatus for the Oostenbrink direct cottonwool filter extraction method. Nematologica9, 106–110.
CrossRef
Google scholar
|
[55] |
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., Mauro da Cunha Castro, J., Dam, M., Djigal, D., Escuer, M., Griffiths, B.S., Gutiérrez, C., Hohberg, K., Kalinkina, D., Kardol, P., Kergunteuil, A., Korthals, G., Krashevska, V., Kudrin, A.A., Li, Q., Liang, W., Magilton, M., Marais, M., Martín, J.A.R., Matveeva, E., Mayad, E.H., Mulder, C., Mullin, P., Neilson, R., Nguyen, T.A.D., Nielsen, U.N., Okada, H., Rius, J.E.P., Pan, K., Peneva, V., Pellissier, L., Carlos Pereira da Silva, J., Pitteloud, C., Powers, T.O., Powers, K., Quist, C.W., Rasmann, S., Moreno, S.S., Scheu, S., Setälä, H., Sushchuk, A., Tiunov, A.V., Trap, J., van der Putten, W., Vestergård, M., Villenave, C., Waeyenberge, L., Wall, D.H., Wilschut, R., Wright, D.G., Yang, J., Crowther, T.W., 2019. Soil nematode abundance and functional group composition at a global scale. Nature572, 194–198.
CrossRef
Google scholar
|
[56] |
Van Gundy, S.D., 1965. Factors in survival of nematodes. Annual Review of Phytopathology3, 43–68.
CrossRef
Google scholar
|
[57] |
Wang, X., Shen, H., Zhang, W., Cao, J., Qi, Y., Chen, G., Li, X., 2015. Spatial and temporal characteristics of droughts in the Northeast China Transect. Natural Hazards76, 601–614.
CrossRef
Google scholar
|
[58] |
Williamson, V.M., Hussey, R.S., 1996. Nematode pathogenesis and resistance in plants. Plant Cell8, 1735–1745.
|
[59] |
Xiong, D., Wei, C., Wubs, E.R.J., Veen, G.F., Liang, W., Wang, X., Li, Q., Van der Putten, W.H., Han, X., 2020. Nonlinear responses of soil nematode community composition to increasing aridity. Global Ecology and Biogeography29, 117–126.
CrossRef
Google scholar
|
[60] |
Yan D, Li J, Pei J, Cui J, Nie M, Fang C., 2017. The temperature sensitivity of soil organic carbon decomposition is greater in subsoil than in topsoil during laboratory incubation. Scientific Reports7, 5181.
CrossRef
Google scholar
|
[61] |
Yang, B., Banerjee, S., Herzog, C., Ramirez, A.C., Dahlin, P., van der Heijden, M.G.A., 2021. Impact of land use type and organic farming on the abundance, diversity, community composition and functional properties of soil nematode communities in vegetable farming. Agriculture, Ecosystems & Environment318, 107488.
CrossRef
Google scholar
|
[62] |
Yeates, G.W., Bongers, T., 1999. Nematode diversity in agroecosystems. Agriculture, Ecosystems & Environment74, 113–135.
CrossRef
Google scholar
|
[63] |
Yeates, G.W., Bongers, T., De Goede, R.G.M., Freckman, D.W., Georgieva, S.S., 1993. Feeding habits in soil nematode families and genera-an outline for soil ecologists. Journal of Nematology25, 315–331.
|
[64] |
Zhang, G., Sui, X., Li, Y., Jia, M., Wang, Z., Han, G., Wang, L., 2020. The response of soil nematode fauna to climate drying and warming in Stipa breviflora desert steppe in Inner Mongolia, China. Journal of Soils and Sediments20, 2166–2180.
CrossRef
Google scholar
|
[65] |
Zhang, X., Ferris, H., Mitchell, J., Liang, W., 2017. Ecosystem services of the soil food web after long-term application of agricultural management practices. Soil Biology & Biochemistry111, 36–43.
CrossRef
Google scholar
|
/
〈 | 〉 |