Abstract
A trait-based approach is adopted to understand the responses of the soil nematode food web following cover crops incorporated into the soil, i.e., afterlife effect of plant. We conducted an in situ microcosm experiment with two cover crops including leguminous Astragalus sinicus L. (A. sinicus), characterized by high nutrient content, and gramineous Lolium multiflorum Lam (L. multiflorum), characterized by high C and lignin content, representing the acquisitive and conservative side of the economic spectrum, respectively. Furthermore, two incorporation rates were set to represent low and high biomass production of cover crops that could be incorporated into the soil. Soil main microbial groups, nematode food web, and physicochemical properties were analyzed at weeks 4 and 18 after cover crops incorporated into the soil. Results showed that, regardless of time, cover crops affected the abundance and composition of the soil nematode food web. L. multiflorum supported higher nematode abundance and more complex nematode food web than A. sinicus, charactering with higher fungivore/bacterivore, predator/prey, maturity index, and structure index, particularly under the high incorporation rates. In addition, A. sinicus improved much more resource availability (mineral N and dissolved organic C) than L. multiflorum. Together, the quantity and quality of plant residues jointly drive soil food web structure, and a trait-based framework facilitates the mechanical understanding of afterlife effect of plant on soil ecosystems.
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References
Allison SD (2012) A trait-based approach for modelling microbial litter decomposition. Ecol Lett 15:1058–1070
Bardgett RD, Wardle DA (2010) Aboveground-belowground linkages: biotic interactions, ecosystem processes, and global change. Oxford University Press, Oxford
Barel JM, Kuyper TW, de Boer W, Douma JC, De Deyn GB (2018) Legacy effects of diversity in space and time driven by winter cover crop biomass and nitrogen concentration. J Appl Ecol 55:299–310
Bates D, Sarkar D, Bates MD, Matrix L (2007) The lme4 package. R Package Version 2:74
Beltrán M, Galantini JA, Salvagiotti F, Tognetti P, Bacigaluppo S, Sainz Rozas HR, Barraco M, Barbieri PA (2021) Do soil carbon sequestration and soil fertility increase by including a gramineous cover crop in continuous soybean? Soil Sci Soc Am J 85:1380–1394
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Physiol Pharm 37:911–917
Bongers T (1990) The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83:14–19
Carmona CP, Bueno CG, Toussaint A, Träger S, Díaz S, Moora M, Munson AD, Pärtel M, Zobel M, Tamme R (2021) Fine-root traits in the global spectrum of plant form and function. Nature 597:683–687
Chauvin C, Dorel M, Villenave C, Roger-Estrade J, Thuries L, Risède J-M (2015) Biochemical characteristics of cover crop litter affect the soil food web, organic matter decomposition, and regulation of plant-parasitic nematodes in a banana field soil. Appl Soil Ecol 96:131–140
Cheng L, Booker FL, Tu C, Burkey KO, Zhou L, Shew HD, Rufty TW, Hu S (2012) Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2. Science 337:1084–1087
Coleman DC, Wall DH (2015) Soil fauna: occurrence, biodiversity, and roles in ecosystem function. In: Paul EA (ed) Soil microbiology, ecology and biochemistry, 4th edn. Academic, Boston, pp 111–149
De Deyn GB, Cornelissen JH, Bardgett RD (2008) Plant functional traits and soil carbon sequestration in contrasting biomes. Ecol Lett 11:516–531
Dias ATC, Cornelissen JHC, Berg MP (2017) Litter for life: assessing the multifunctional legacy of plant traits. J Ecol 105:1163–1168
Díaz S, Kattge J, Cornelissen JH, Wright IJ, Lavorel S, Dray S, Reu B, Kleyer M, Wirth C, Colin Prentice I (2016) The global spectrum of plant form and function. Nature 529:167–171
Djigal D, Chabrier C, Duyck P-F, Achard R, Quénéhervé P, Tixier P (2012) Cover crops alter the soil nematode food web in banana agroecosystems. Soil Biol Biochem 48:142–150
Dornbush ME, Isenhart TM, Raich JW (2002) Quantifying fine-root decomposition: An alternative to buried litterbags. Ecology 83:2985–2990
DuPont ST, Ferris H, Van Horn M (2009) Effects of cover crop quality and quantity on nematode-based soil food webs and nutrient cycling. Appl Soil Ecol 41:157–167
Du Preez G, Daneel M, De Goede R, Du Toit MJ, Ferris H, Fourie H, Geisen S, Kakouli-Duarte T, Korthals G, Sánchez-Moreno S, Schmidt JH (2022) Nematode-based indices in soil ecology: application, utility, and future directions. Soil Biol Biochem 169:108640
Ettema CH, Bongers T (1993) Characterization of nematode colonization and succession in disturbed soil using the Maturity Index. Biol Fertil Soils 16:79–85
Ferris H, Bongers T, de Goede RG (2001) A framework for soil food web diagnostics: extension of the nematode faunal analysis concept. Appl Soil Ecol 18:13–29
Freschet GT, Aerts R, Cornelissen JH (2012) A plant economics spectrum of litter decomposability. Funct Ecol 26:56–65
Freschet GT, Cornelissen JH, Van Logtestijn RS, Aerts R (2010) Evidence of the ‘plant economics spectrum’ in a subarctic flora. J Ecol 98:362–373
Freschet GT, Roumet C, Comas LH, Weemstra M, Bengough AG, Rewald B, Bardgett RD, De Deyn GB, Johnson D, Klimešová J (2021) Root traits as drivers of plant and ecosystem functioning: current understanding, pitfalls and future research needs. New Phytol 232:1123–1158
Fujii S, Berg MP, Cornelissen JH (2020) Living litter: dynamic trait spectra predict fauna composition. Trends Ecol Evol 35:886–896
Franco ALC, Gherardi LA, de Tomasel CM, Andriuzzi WS, Ankrom KE, Shaw EA, Bach EM, Sala OE, Wall DH (2019) Drought suppresses soil predators and promotes root herbivores in mesic, but not in xeric grasslands. Proc Natl Acad Sci USA 116:12883–12888
Garland G, Edlinger A, Banerjee S, Degrune F, García-Palacios P, Pescador DS, Herzog C, Romdhane S, Saghai A, Spor A (2021) Crop cover is more important than rotational diversity for soil multifunctionality and cereal yields in European cropping systems. Nat Food 2:28–37
Garnier E, Navas M-L (2012) A trait-based approach to comparative functional plant ecology: concepts, methods and applications for agroecology. A Review Agron Sustain Dev 32:365–399
Gravel D, Albouy C, Thuiller W (2016) The meaning of functional trait composition of food webs for ecosystem functioning. Philos T R Soc B 371:20150268
Grime JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111:1169–1194
Hansen TH, Laursen KH, Persson DP, Pedas P, Husted S, Schjoerring JK (2009) Micro-scaled high-throughput digestion of plant tissue samples for multi-elemental analysis. Plant Methods 5:1–11
Hobbie SE (2015) Plant species effects on nutrient cycling: revisiting litter feedbacks. Trends Ecol Evol 30:357–363
Joergensen RG (2022) Phospholipid fatty acids in soil-drawbacks and future prospects. Biol Fertil Soils 58:1–6
Kuo S, Jellum E (2000) Long-term winter cover cropping effects on corn (Zea mays L.) production and soil nitrogen availability. Biol Fertil Soils 31:470–477
Kurze S, Engelbrecht BM, Bilton MC, Tielbörger K, Álvarez-Cansino L (2021) Rethinking the plant economics spectrum for annuals: a multi-species study. Front Plant Sci 12:640862
Lamichhane JR, Alletto L (2022) Ecosystem services of cover crops: a research roadmap. Trends Plant Sci 27:758–768
Lavorel S, Storkey J, Bardgett RD, De Bello F, Berg MP, Le Roux X, Moretti M, Mulder C, Pakeman RJ, Díaz S (2013) A novel framework for linking functional diversity of plants with other trophic levels for the quantification of ecosystem services. J Veg Sci 24:942–948
Leslie AW, Wang K-H, Meyer SLF, Marahatta S, Hooks CRR (2017) Influence of cover crops on arthropods, free-living nematodes, and yield in a succeeding no-till soybean crop. Appl Soil Ecol 117–118:21–31
Li Z, Wang F, Su F, Wang P, Li S, Bai T, Wei Y, Liu M, Chen D, Zhu W (2021) Climate change drivers alter root controls over litter decomposition in a semi-arid grassland. Soil Biol Biochem 158:108278
Liu M, Chen X, Qin J, Wang D, Griffiths B, Hu F (2008) A sequential extraction procedure reveals that water management affects soil nematode communities in paddy fields. Appl Soil Ecol 40:250–259
Lu R (2000) Analysis methods of soil agricultural chemistry. China Agricultural Science and Technology Press, Beijing 107:147–150
Mariotte P, Mehrabi Z, Bezemer TM, De Deyn GB, Kulmatiski A, Drigo B, Veen GC, Van der Heijden MG, Kardol P (2018) Plant-soil feedback: bridging natural and agricultural sciences. Trends Ecol Evol 33:129–142
Martin AR, Isaac ME (2018) Functional traits in agroecology: advancing description and prediction in agroecosystems. J Appl Ecol 55:5–11
Neher DA (2001) Role of nematodes in soil health and their use as indicators. J Nematol 33:161
Neher DA (2010) Ecology of plant and free-living nematodes in natural and agricultural soil. Annu Rev Phytopathol 48:371–394
Neutel A-M, Heesterbeek JA, Van de Koppel J, Hoenderboom G, Vos A, Kaldeway C, Berendse F, De Ruiter PC (2007) Reconciling complexity with stability in naturally assembling food webs. Nature 449:599–602
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szöcs E, Wagner H (2020) Vegan: community ecology package. Version 2.5–7. https:// CRAN.R- proje ct. org/ packa ge= vegan
Otfinowski R, Coffey V (2020) Can root traits predict communities of soil nematodes in restored northern prairies? Plant Soil 453:459–471
Prieto I, Roumet C, Cardinael R, Dupraz C, Jourdan C, Kim JH, Maeght JL, Mao Z, Pierret A, Portillo N (2015) Root functional parameters along a land-use gradient: evidence of a community-level economics spectrum. J Ecol 103:361–373
R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Reich PB (2014) The world-wide ‘fast-slow’ plant economics spectrum: a traits manifesto. J Ecol 102:275–301
Roumet C, Birouste M, Picon-Cochard C, Ghestem M, Osman N, Vrignon-Brenas S, Kf C, Stokes A (2016) Root structure–function relationships in 74 species: evidence of a root economics spectrum related to carbon economy. New Phytol 210:815–826
Rousk J, Frey SD (2015) Revisiting the hypothesis that fungal-to-bacterial dominance characterizes turnover of soil organic matter and nutrients. Ecol Monogr 85:457–472
Sharma P, Singh A, Kahlon CS, Brar AS, Grover KK, Dia M, Steiner RL (2018) The role of cover crops towards sustainable soil health and agriculture—a review paper. Am J Plant Sci 9:1935–1951
Sikora RA, Coyne D, Hallmann J, Timper P (2018) Reflections and challenges: nematology in subtropical and tropical agriculture. In: Sikora RA, Coyne D, Hallmann J, Timper P (eds) Plant parasitic nematodes in subtropical and tropical agriculture. CAB International, Wallingford, pp 1–19
Soil Survey Staff (1999) Soil taxonomy: a basic system of soil classification for making and interpreting soil surveys. Natural Resources Conservation Service. U.S. Department of Agriculture Handbook, Washington
Thakur MP, Reich PB, Fisichelli NA, Stefanski A, Cesarz S, Dobies T, Rich RL, Hobbie SE, Eisenhauer N (2014) Nematode community shifts in response to experimental warming and canopy conditions are associated with plant community changes in the temperate-boreal forest ecotone. Oecologia 175:713–723
Thapa R, Tully KL, Cabrera ML, Dann C, Schomberg HH, Timlin D, Reberg-Horton C, Gaskin J, Davis BW, Mirsky SB (2021) Effects of moisture and temperature on C and N mineralization from surface-applied cover crop residues. Biol Fertil Soils 57:485–498
Tiemann L, Grandy A, Atkinson E, Marin-Spiotta E, McDaniel M (2015) Crop rotational diversity enhances belowground communities and functions in an agroecosystem. Ecol Lett 18:761–771
van den Hoogen J, Geisen S, Routh D et al (2019) Soil nematode abundance and functional group composition at a global scale. Nature 572:194–191
Van Der Krift TA, Berendse F (2001) The effect of plant species on soil nitrogen mineralization. J Ecol 89:555–561
Van Soest PJ, Wine R (1967) Use of detergents in the analysis of fibrous feeds. IV. Determination of plant cell-wall constituents. J Assoc off Anal Chem 50:50–55
Violle C, Navas ML, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007) Let the concept of trait be functional! Oikos 116:882–892
Wagg C, Bender SF, Widmer F, Van Der Heijden MG (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci U S A 111:5266–5270
Wilschut RA, Geisen S (2021) Nematodes as drivers of plant performance in natural systems. Trends Plant Sci 26:237–247
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JH, Diemer M (2004) The worldwide leaf economics spectrum. Nature 428:821–827
Xiong D, Wei C, Wubs ERJ, Veen GF, Liang W, Wang X, Li Q, Putten WH, Han X, Ordonez A (2019) Nonlinear responses of soil nematode community composition to increasing aridity. Glob Ecol Biogeogr 29:117–126
Yeates GW, Bongers T, De Goede RG, Freckman DW, Georgieva S (1993) Feeding habits in soil nematode families and genera—an outline for soil ecologists. J Nematol 25:315
Yeates GW (2003) Nematodes as soil indicators: functional and biodiversity aspects. Biol Fertil Soils 37:199–210
Zhang C, Wang J, Ren Z, Hu Z, Tian S, Fan W, Chen X, Griffiths BS, Hu F, Liu M (2020) Root traits mediate functional guilds of soil nematodes in an ex-arable field. Soil Biol Biochem 151:108038
Zhang C, Xue W, Xue J, Zhang J, Qiu L, Chen X, Hu F, Kardol P, Liu M (2022a) Leveraging functional traits of cover crops to coordinate crop productivity and soil health. J Appl Ecol 59:2627–2641
Zhang J, Hu Z, Zhang C, Tao Y, Chen X, Griffiths BS, Liu M (2022b) Roots with larger specific root length and C: N ratio sustain more complex rhizosphere nematode community. Plant Soil 477:693–706
Zheng W, Zhao Z, Gong Q, Zhai B, Li Z (2018) Effects of cover crop in an apple orchard on microbial community composition, networks, and potential genes involved with degradation of crop residues in soil. Biol Fertil Soils 54:743–759
Acknowledgements
We thank Misses Songjuan Gao, Jingxuan Chen, and Ting Liu who offered valuable help in the maintenance of field experiment and manuscript preparation.
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This work was supported by the National Key R&D program (2021YFD1700202) and National Foundation of Sciences in China (42077047, 41877056).
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Zhang, C., Xue, J., Li, N. et al. Afterlife effect of cover crops on soil nematode food web: Implications from the plant ecological strategy. Biol Fertil Soils 58, 937–947 (2022). https://doi.org/10.1007/s00374-022-01676-3
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DOI: https://doi.org/10.1007/s00374-022-01676-3