Abstract
Purpose
Intercropping is an important agricultural management that has been applied worldwide. Although intercropping improves soil nutrients and crop productivity, its effects on the microbial-mediated belowground processes and main drivers remain unclear.
Methods
We performed the same field study at two sites (Site1, Youyu; Site2, Zhangbei) by growing soybean and oat in monoculture and intercropping to investigate their effects on rhizosphere soil properties, enzyme stoichiometry, and soil ecosystem multifunctionality (EMF).
Results
Intercropping increased available phosphorus (Avail-P) by 87% and 16% for oat and soybean compared to the corresponding monoculture in site1, respectively. We also found that intercropping increased the C-acquiring and N-acquiring enzyme activities by 18%-48% in site1. Moreover, intercropping enhanced soil EMF and alleviated microbial P limitations for both oat and soybean compared to the corresponding monoculture in site1. However, all observed parameters were not affected by intercropping in site2, which may be due to the lower Avail-P, mineral nitrogen (Nmin), and precipitation in site2 compared to site1. Moreover, the soil EMF was strongly positively correlated with soil Nmin, Avail-P, air temperature, and precipitation.
Conclusion
Therefore, intercropping improves soil ecosystem multifunctionality by increasing available nutrients, which are regulated by regional factors.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Allan E, Manning P, Alt F, Binkenstein J, Blaser S, Bluthgen N, Bohm S, Grassein F, Holzel N, Klaus VH, Kleinebecker T, Morris EK, Oelmann Y, Prati D, Renner SC, Rillig MC, Schaefer M, Schloter M, Schmitt B, Schoning I, Schrumpf M, Solly E, Sorkau E, Steckel J, Steffen-Dewenter I, Stempfhuber B, Tschapka M, Weiner CN, Weisser WW, Werner M, Westphal C, Wilcke W, Fischer M (2015) Land use intensification alters ecosystem multifunctionality via loss of biodiversity and changes to functional composition. Ecol Lett 18:834–843. https://doi.org/10.1111/ele.12469
Allison SD, Weintraub MN, Gartner TB, Waldrop MP (2010) Evolutionary-economic principles as regulators of soil enzyme production and ecosystem function. Soil Enzymology. Springer, pp. 229–243
Bao S (2000) Soil agro-chemistries analysis, 3rd eds. Agricultural Press, Beijing
Brooker RW, Bennett AE, Cong WF, Daniell TJ, George TS, Hallett PD, Hawes C, Iannetta PP, Jones HG, Karley AJ, Li L, McKenzie BM, Pakeman RJ, Paterson E, Schob C, Shen J, Squire G, Watson CA, Zhang C, Zhang F, Zhang J, White PJ (2015) Improving intercropping: a synthesis of research in agronomy, plant physiology and ecology. New Phytol 206:107–117. https://doi.org/10.1111/nph.13132
Bybee-Finley KA, Mirsky SB, Ryan MR (2016) Functional diversity in summer annual grass and legume intercrops in the Northeastern United States. Crop Sci 56:2775–2790. https://doi.org/10.2135/cropsci2016.01.0046
Cui YX, Fang LC, Guo XB, Wang X, Zhang YJ, Li PF, Zhang XC (2018) Ecoenzymatic stoichiometry and microbial nutrient limitation in rhizosphere soil in the arid area of the northern Loess Plateau, China. Soil Biol Biochem 116:11–21. https://doi.org/10.1016/j.soilbio.2017.09.025
Cui YX, Fang LC, Deng L, Guo XB, Han F, Ju WL, Wang X, Chen HS, Tan WF, Zhang XC (2019) Patterns of soil microbial nutrient limitations and their roles in the variation of soil organic carbon across a precipitation gradient in an arid and semi-arid region. Sci Total Environ 658:1440–1451. https://doi.org/10.1016/j.scitotenv.2018.12.289
Curtright AJ, Tiemann LK (2021) Intercropping increases soil extracellular enzyme activity: a meta-analysis. Agric Ecosyst Environ 319. https://doi.org/10.1016/j.agee.2021.107489
Delgado-Baquerizo M, Maestre FT, Reich PB, Jeffries TC, Gaitan JJ, Encinar D, Berdugo M, Campbell CD, Singh BK (2016) Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat Commun 7:10541. https://doi.org/10.1038/ncomms10541
Dodor DE, Amanor YJ, Attor FT, Adjadeh TA, Neina D, Miyittah M (2018) Co-application of biochar and cattle manure counteract positive priming of carbon mineralization in a sandy soil. Environ Syst Res 7:5. https://doi.org/10.1186/s40068-018-0108-y
Frankena J, Van Verseveld HW, Stouthamer AH (1988) Substrate and energy costs of the production of exocellular enzymes by Bacillus licheniformis. Biotechnol Bioeng 32:803–812. https://doi.org/10.1002/bit.260320612
Geyer KM, Kyker-Snowman E, Grandy AS, Frey SD (2016) Microbial carbon use efficiency: accounting for population, community, and ecosystem-scale controls over the fate of metabolized organic matter. Biogeochemistry 127:173–188. https://doi.org/10.1007/s10533-016-0191-y
Gong XW, Liu CJ, Li J, Luo Y, Yang QH, Zhang WL, Yang P, Feng BL (2019) Responses of rhizosphere soil properties, enzyme activities and microbial diversity to intercropping patterns on the Loess Plateau of China. Soil Tillage Res 195:104355. https://doi.org/10.1016/j.still.2019.104355
Han HJ, Hwang J, Kim G (2021) Characterizing the origins of dissolved organic carbon in coastal seawater using stable carbon isotope and light absorption characteristics. Biogeosciences 18:1793–1801. https://doi.org/10.5194/bg-18-1793-2021
Hong Y, Heerink N, Jin S, Berentsen P, Zhang L, van der Werf W (2017) Intercropping and agroforestry in China – current state and trends. Agric Ecosyst Environ 244:52–61. https://doi.org/10.1016/j.agee.2017.04.019
Jia R, Zhou J, Chu JC, Shahbaz M, Yang YD, Jones D, Zang HD, Razavi B, Zeng ZH (2022) Insights into the associations between soil quality and ecosystem multifunctionality driven by fertilization management: a case study from the North China Plain. J Clean Prod 362:132265. https://doi.org/10.1016/j.jclepro.2022.132265
Jing X, Sanders NJ, Shi Y, Chu H, Classen AT, Zhao K, Chen L, Shi Y, Jiang Y, He JS (2015) The links between ecosystem multifunctionality and above- and belowground biodiversity are mediated by climate. Nat Commun 6:8159. https://doi.org/10.1038/ncomms9159
Kumar A, Blagodaskaya E, Dippold MA, Temperton VM (2021) Positive intercropping effects on biomass production are species-specific and involve rhizosphere enzyme activities: evidence from a field study. Soil Ecol Lett. https://doi.org/10.1007/s42832-021-0108-0
Kuzyakov Y, Hill PW, Jones DL (2007) Root exudate components change litter decomposition in a simulated rhizosphere depending on temperature. Plant Soil 290:293–305. https://doi.org/10.1007/s11104-006-9162-8
Li B, Li YY, Wu HM, Zhang FF, Li CJ, Li XX, Lambers H, Li L (2016) Root exudates drive interspecific facilitation by enhancing nodulation and N2 fixation. Proc Natl Acad Sci U S A 113:6496–6501. https://doi.org/10.1073/pnas.1523580113
Li CJ, Hoffland E, Kuyper TW, Yu Y, Zhang CC, Li HG, Zhang FS, van der Werf W (2020) Syndromes of production in intercropping impact yield gains. Nature Plants 6:653–660. https://doi.org/10.1038/s41477-020-0680-9
Liao D, Zhang C, Li H, Lambers H, Zhang FS (2020) Changes in soil phosphorus fractions following sole cropped and intercropped maize and faba bean grown on calcareous soil. Plant Soil 448:587–601. https://doi.org/10.1007/s11104-020-04460-0
Liu M, Qiao N, Zhang Q, Xu XL (2018) Cropping regimes affect NO3− versus NH4+ uptake by Zea mays and Glycine max. Plant Soil 426:241–251. https://doi.org/10.1007/s11104-018-3625-6
Luo GW, Li L, Friman VP, Guo JJ, Guo SW, Shen QR, Ling N (2018) Organic amendments increase crop yields by improving microbe-mediated soil functioning of agroecosystems: a meta-analysis. Soil Biol Biochem 124:105–115. https://doi.org/10.1016/j.soilbio.2018.06.002
Marschner P, Crowley D, Yang CH (2004) Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type. Plant Soil 261:199–208. https://doi.org/10.1023/B:PLSO.0000035569.80747.c5
Martin-Guay MO, Paquette A, Dupras J, Rivest D (2018) The new green revolution: sustainable intensification of agriculture by intercropping. Sci Total Environ 615:767–772. https://doi.org/10.1016/j.scitotenv.2017.10.024
Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5:62–71. https://doi.org/10.1006/niox.2000.0319
Moorhead DL, Sinsabaugh RL, Hill BH, Weintraub MN (2016) Vector analysis of ecoenzyme activities reveal constraints on coupled C, N and P dynamics. Soil Biol Biochem 93:1–7. https://doi.org/10.1016/j.soilbio.2015.10.019
Nannipieri P, Giagnoni L, Renella G, Puglisi E, Ceccanti B, Masciandaro G, Fornasier F, Moscatelli MC, Marinari S (2012) Soil enzymology: classical and molecular approaches. Biol Fertil Soils 48:743–762. https://doi.org/10.1007/s00374-012-0723-0
Ohno T, Zibilske LM (1991) Determination of low concentrations of phosphorus in soil extracts using malachite green. Soil Sci Soc Am J 55:892–895. https://doi.org/10.2136/sssaj1991.03615995005500030046x
Qian X, Zang HD, Xu HH, Hu YG, Ren CZ, Guo LC, Wang CL, Zeng ZH (2018) Relay strip intercropping of oat with maize, sunflower and mung bean in semi-arid regions of Northeast China: yield advantages and economic benefits. Field Crops Res 223:33–40. https://doi.org/10.1016/j.fcr.2018.04.004
Rodriguez C, Carlsson G, Englund J-E, Flohr A, Pelzer E, Jeuffroy MH, Makowski D, Jensen ES (2020) Grain legume-cereal intercropping enhances the use of soil-derived and biologically fixed nitrogen in temperate agroecosystems. A meta-analysis. Eur J Agron 118. https://doi.org/10.1016/j.eja.2020.126077
Ryan MR, Crews TE, Culman SW, DeHaan LR, Hayes RC, Jungers JM, Bakker MG (2018) Managing for multifunctionality in perennial grain crops. Bioscience 68:294–304. https://doi.org/10.1093/biosci/biy014
Sanderson MA, Archer D, Hendrickson J, Kronberg S, Liebig M, Nichols K, Schmer M, Tanaka D, Aguilar J (2013) Diversification and ecosystem services for conservation agriculture: outcomes from pastures and integrated crop–livestock systems. Renew Agric Food Syst 28:129–144. https://doi.org/10.1017/s1742170512000312
Sinsabaugh RL, Follstad Shah JJ (2012) Ecoenzymatic stoichiometry and ecological theory. Annu Rev Ecol Evol Syst 43:313–343. https://doi.org/10.1146/annurev-ecolsys-071112-124414
Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop MP, Wallenstein MD, Zak DR, Zeglin LH (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264. https://doi.org/10.1111/j.1461-0248.2008.01245.x
Sinsabaugh RL, Hill BH, Follstad Shah JJ (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–798. https://doi.org/10.1038/nature08632
Solanki MK, Wang FY, Wang Z, Li CN, Lan TJ, Singh RK, Singh P, Yang LT, Li YR (2019) Rhizospheric and endospheric diazotrophs mediated soil fertility intensification in sugarcane-legume intercropping systems. J Soils Sediments 19:1911–1927. https://doi.org/10.1007/s11368-018-2156-3
Tiemann LK, Billings SA (2011) Indirect effects of nitrogen amendments on organic substrate quality increase enzymatic activity driving decomposition in a Mesic Grassland. Ecosystems 14:234–247. https://doi.org/10.1007/s10021-010-9406-6
Tsay JS, FukaiS WGL (1988) Effects of relative sowing time of soybean on growth and yield of cassava in cassava/soybean intercropping. Field Crop Res 19:227–239. https://doi.org/10.1016/0378-4290(88)90045-7
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. https://doi.org/10.1073/pnas.1320054111
Wallenstein MD, Burns RG (2011) Ecology of extracellular enzyme activities and organic matter degradation in soil: a complex community-driven process. Methods Soil Enzymol 2:35–55. https://doi.org/10.2136/sssabookser9.c2
Wang ZG, Bao XG, Li XF, Jin X, Zhao JH, Sun JH, Christie P, Li L (2015) Intercropping maintains soil fertility in terms of chemical properties and enzyme activities on a timescale of one decade. Plant Soil 391:265–282. https://doi.org/10.1007/s11104-015-2428-2
Wang XY, Gao YZ, Zhang HL, Shao ZQ, Sun BR, Gao Q (2019) Enhancement of rhizosphere citric acid and decrease of NO3−/NH4+ ratio by root interactions facilitate N fixation and transfer. Plant Soil 447:169–182. https://doi.org/10.1007/s11104-018-03918-6
Willey RW (1979) Intercropping-its importance and research needs. Part I, competition and yield advantages. Fields Crops Abstract 32:1–10
Xue YF, Xia HY, Christie P, Zhang Z, Li L, Tang CX (2016) Crop acquisition of phosphorus, iron and zinc from soil in cereal/legume intercropping systems: a critical review. Ann Bot 117:363–377. https://doi.org/10.1093/aob/mcv182
Yan ZJ, Zhou J, Yang L, Gunina A, Yang YD, Peixoto L, Zeng ZH, Zang HD, Kuzyakov Y (2022) Diversified cropping systems benefit soil carbon and nitrogen stocks by increasing aggregate stability: results of three fractionation methods. Sci Total Environ 824:153878. https://doi.org/10.1016/j.scitotenv.2022.153878
Zang HD, Qian X, Wen Y, Hu YG, Ren CZ, Zeng ZH, Guo LC, Wang CL (2018) Contrasting carbon and nitrogen rhizodeposition patterns of soya bean (Glycine max L.) and oat (Avena nuda L.). Eur J Soil Sci 125:34–40. https://doi.org/10.1111/ejss.12556
Zhang WP, Liu GC, Sun JH, Fornara D, Zhang LZ, Zhang FF, Li L, Niels A (2017) Temporal dynamics of nutrient uptake by neighbouring plant species: evidence from intercropping. Funct Ecol 31:469–479. https://doi.org/10.1111/1365-2435.12732
Zhang XC, Kuzyakov Y, Zang HD, Dippold M, Shi LL, Spielvogel S, Razavi B (2020) Rhizosphere hotspots: root hairs and warming control microbial efficiency, carbon utilization and energy production. Soil Biol Biochem 148:107872. https://doi.org/10.1016/j.soilbio.2020.107872
Zhou J, Gui H, Banfield C, Wen Y, Zang HD, Dippold M, Charlton A, Jones D (2021a) The microplastisphere: biodegradable microplastics addition alters soil microbial community structure and function. Soil Biol Biochem 156:108211. https://doi.org/10.1016/j.soilbio.2021.108211
Zhou J, Wen Y, Shi LL, Marshall MR, Kuzyakov Y, Blagodatskaya E, Zang HD (2021b) Strong priming of soil organic matter induced by frequent input of labile carbon. Soil Biol Biochem 152:108069. https://doi.org/10.1016/j.soilbio.2020.108069
Acknowledgements
This study was financially supported by the earmarked fund for the China Agriculture Research System (CARS-07-B-5), the Young Elite Scientists Sponsorship Program by CAST (2020QNRC001), and the Joint Funds of the National Natural Science Foundation of China (U21A20218).
Author information
Authors and Affiliations
Contributions
Huaiying Ma: Methodology, Investigation and Writing—Original Draft; Jie Zhou: Writing—Review & Editing; Junyong Ge: Field management, Soil sample collection and Writing—Review & Editing; Jiangwen Nie: Formal analysis, Writing—Review & Editing; Jie Zhao: Formal analysis, Writing—Review & Editing; Zhiqiang Xue: Field management, Soil sample collection; Yuegao Hu: Project administration, Supervision; Yadong Yang: Writing—Review & Editing; Leanne Peixoto: Writing—Review & Editing; Huadong Zang: Conceptualization, supervision, Writing—Review & Editing and Funding acquisition; Zhaohai Zeng: Writing—Review & Editing and Funding acquisition.
Corresponding author
Additional information
Responsible Editor: Rémi Cardinael.
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ma, H., Zhou, J., Ge, J. et al. Intercropping improves soil ecosystem multifunctionality through enhanced available nutrients but depends on regional factors. Plant Soil 480, 71–84 (2022). https://doi.org/10.1007/s11104-022-05554-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-022-05554-7