Skip to main content

Advertisement

Log in

Intercropping cereals with faba bean reduces plant disease incidence regardless of fertilizer input; a meta-analysis

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Ecological intensification of agriculture calls for ecological mechanisms to replace anthropogenic inputs. Cereal/legume intercropping increases yields due to species complementarities, it produces high protein food and feed, and it reduces the need for artificial N fertilizer because legumes fix N biologically. In addition, intercropping has the potential to suppress plant diseases, but its efficacy for disease suppression in cereal/legume mixtures has not been well characterized quantitatively. Here we conducted meta-analysis to quantify the disease suppressive effect of intercropping cereals with legumes at different levels of N fertilizer. Intercropping reduced disease incidence (measured by the odds ratio of disease occurrence) by 45% on average. This reduction was significant (P < 0.01) for four out of six studied pathogens: yellow rust (Puccinia striiformis f.sp. tritici) and mildew (Blumeria graminis) in wheat (Triticum aestivum), and chocolate spot (Botrytis fabae) and Fusarium wilt (Fusarium oxysporum) in faba bean (Vicia faba). Disease reduction was marginally significant for yellow rust in barley (Puccinia striiformis f.sp. hordei) (P < 0.10) and not significant for bean rust (Uromyces fabae). The reduction in disease incidence was greatest during the early stages of epidemics. N fertilizer strongly increased the incidence of powdery mildew of wheat, but it did not affect the incidence of the other diseases and it did not affect the effectiveness of intercropping as a management strategy for disease control. While nitrogen input increased powdery mildew incidence in both sole and intercropped wheat, the incidence was lower in the intercropped than sole wheat at all levels of N input. The disease suppressive effect of intercropping on wheat powdery mildew or any other disease was not affected by the amount of nitrogen fertilizer. The results show that intercropping has a substantial and consistent effect on disease incidence in cereal/faba bean mixtures across studies, but is not sufficient to provide complete disease control. Intercropping is therefore best used as a component in an integrated approach for managing plant diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Agresti A. 2002. Categorical data analysis. Wiley. 2nd edition.

  • Bedoussac, L., Journet, E., Hauggaard-Nielsen, H., Naudin, C., Corre-Hellou, G., Jensen, E. S., Prieur, L., & Justes, E. (2015). Ecological principles underlying the increase of productivity achieved by cereal-grain legume intercrops in organic farming. A review. Agronomy Sustainable Development, 35, 911–935.

    Article  Google Scholar 

  • Bommarco, R., Kleijn, D., & Potts, S. G. (2013). Ecological intensification: Harnessing ecosystem services for food security. Trends in Ecology and Evolution, 28(4), 230–238.

    Article  PubMed  Google Scholar 

  • Borenstein, M., Hedges, L. V., Higgins, J. P. T., & Rothstein, H. R. (2009). Introduction to meta-analysis. Wiley.

  • Boudreau, M. A. (2013). Diseases in intercropping systems. Annual Review of Phytopathology, 51, 499–519.

    Article  CAS  PubMed  Google Scholar 

  • Chakraborty, S., & Newton, A. C. (2011). Climate change, plant diseases and food security: An overview. Plant Pathology, 60, 2–14.

    Article  Google Scholar 

  • Chen, Y. X., Zhang, F. S., Tang, L., Zheng, Y., Li, Y. J., Christie, P., & Li, L. (2007). Wheat powdery mildew and foliar N concentrations as influenced by N fertilization and belowground interactions with intercropped faba bean. Plant and Soil, 291, 1–13.

    Article  CAS  Google Scholar 

  • Cong, W. F., Hoffland, E., Li, L., Six, J., Sun, J. H., Bao, X. G., Zhang, F. S., & van der Werf, W. (2015). Intercropping enhances soil carbon and nitrogen. Global Change Biology, 21, 1715–1726.

    Article  PubMed  Google Scholar 

  • Dassou, A. G., & Tixier, P. (2016). Response of pest control by generalist predators to local-scale plant diversity: A meta-analysis. Ecology and Evolution, 6(4), 1143–1153.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dordas, C. (2008). Role of nutrients in controlling plant diseases in sustainable agriculture. A review. Agronomy Sustainable Development, 28, 33–46.

    Article  CAS  Google Scholar 

  • Garrett, K. A., Zúniga, L. N., Roncal, E., Forbes, G. A., Mundt, C. C., Su, Z., & Nelson, R. J. (2009). Intraspecific functional diversity in hosts and its effect on disease risk across a climatic gradient. Ecological Applications, 19(7), 1868–1883.

    Article  CAS  PubMed  Google Scholar 

  • Hoffland, E., van Beusichem, M. L., & Jeger, M. J. (1999). Nitrogen availability and susceptibility of tomato leaves to Botrytis cinerea. Plant and Soil, 210, 263–272.

    Article  CAS  Google Scholar 

  • Hong, Y., Heerink, N. B. M., Jin, S. Q., Berentsen, P. B. M., Zhang, L., & van der Werf, W. (2017). Intercropping and agroforestry in China; current state and trends. Agriculture, Ecosystems and Environment, 244, 52–61.

    Article  Google Scholar 

  • Jensen, B., & Munk, L. (1997). Nitrogen-induced changes in colony density and spore production of Erysiphe graminis f.sp. hordei on seedlings of six spring barley cultivars. Plant Pathology, 46, 191–202.

    Article  Google Scholar 

  • Jiang, Y. N., Wang, W. X., Xie, Q. J., Liu, N., Wang, D. P., Zhang, X. W., Yang, C., Chen, X. Y., Tang, D. Z., & Wang, E. T. (2017). Plant transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science, 356, 1172–1175.

    Article  CAS  PubMed  Google Scholar 

  • Keesing, F., Belden, L. K., Daszak, P., Dobson, A., Harvell, C., Holt, R. D., Hudson, P., Jolles, A., Jones, K. E., Mitchell, C. E., Myers, S. S., Bogich, T., & Ostfeld, R. S. (2010). Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature, 468, 647–652.

    Article  CAS  PubMed  Google Scholar 

  • Li, C. Y., He, X. H., Zhu, S. S., Zhou, H. P., Wang, Y. Y., Li, Y., Yang, J., Fan, J. X., Yang, J. C., Wang, G. B., Long, Y. F., Xu, J. Y., Tang, Y. S., Zhao, G. H., Yang, J. R., Liu, L., Sun, Y., Xie, Y., Wang, H. N., & Zhu, Y. Y. (2009). Crop diversity for yield increase. PLoS One, 4(11), e8049. https://doi.org/10.1371/journal.pone.0008049.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lithourgidis, A. S., Dordas, C. A., Damalas, C. A., & Vlachostergios, D. N. (2011). Annual intercrops: An alternative pathway for sustainable agriculture. Australian Journal of Crop Science, 5, 396–410.

    Google Scholar 

  • Lv, Z. X., Yu, X. P., Heong, K. L., & Hu, C. (2005). Effects of nitrogenous fertilization in rice fields on the predatory function of Cytorhinus lividipennis Reuter to Nilaparvata lugens stål. Acta Entomologica Sinica, 48, 48–56 (In Chinese).

    Google Scholar 

  • Martin-Guay, M.-O., Paquette, A., Dupras, J., & Rivest, D. (2018). The new green revolution: Sustainable intensification of agriculture by intercropping. Science of the Total Environment, 615, 767–772.

    Article  CAS  PubMed  Google Scholar 

  • Mitchell, C. E., Reich, P. B., Tilman, D., & Groth, J. V. (2003). Effects of elevated CO2, nitrogen deposition, and decreased species diversity on foliar fungal plant disease. Global Change Biology, 9, 438–451.

    Article  Google Scholar 

  • Mundt, C. C. (2002). Use of multiline cultivars and cultivar mixtures for disease management. Annual Review of Phytopathology, 40, 381–410.

    Article  CAS  PubMed  Google Scholar 

  • Neumann, S., Paveley, N. D., Beed, F. D., & Sylvester-Bradely, R. (2004). Nitrogen per unit leaf area affects the upper asymptote of Puccinia striiformis f.sp. tritici epidemics in winter wheat. Plant Pathology, 53, 725–732.

    Article  Google Scholar 

  • Pelzer, E., Bazot, M., Makowski, D., Corre-Hellou, G., Naudin, C., Rifaï, M. A., Baranger, E., Bedoussac, L., Biarnès, V., Boucheny, P., Corrouée, B., Dorvillez, D., Foissy, D., Gaillard, B., Guichar, L., Mansard, M., Omon, B., Prieur, L., Yvergniaus, M., Justes, E., & Feuffroy, M. (2012). Pea-wheat intercrops in low-input conditions combine high economic performances and low environmental impacts. European Journal of Agronomy, 40, 39–53.

    Article  Google Scholar 

  • Philippot, L., Raaijmakers, J. M., Lemanceau, P., & van der Putten, W. (2013). Going back to the roots: The microbial ecology of the rhizosphere. Nature Reviews Microbiology, 11, 789–799.

    Article  CAS  PubMed  Google Scholar 

  • Pinheiro, J., & Bates, D. (2000). Mixed-effects models in S and S-plus. New York: Springer.

    Book  Google Scholar 

  • R Core Team, 2015. R: A language and Environment for Statistical Computing. Foundation for Statistical Computing, Vienna, Austria.

  • Ren, L. X., Su, S. M., Yang, X. M., Xu, Y. C., Huang, Q. W., & Shen, Q. R. (2008). Intercropping with aerobic rice suppressed Fusarium wilt in watermelon. Soil Biology and Biochemistry, 40, 834–844.

    Article  CAS  Google Scholar 

  • Royston, P. (1982). An extension of Shapiro and Wilk’s W test for normality to large samples. Applied Statstics, 31, 115–124.

    Article  Google Scholar 

  • Savary, S., Ficke, A., Aubertot, J., & Hollier, C. (2012). Crop losses due to diseases and their implications for global food production losses and food security. Food Security, 4, 519–537.

    Article  Google Scholar 

  • Simón, M. R., Cordo, C. A., Perelló, A. E., & Struik, P. C. (2003). Influence of nitrogen supply on the susceptibility of wheat to Septoria tritici. Journal of Phytopathology, 151, 283–289.

    Article  Google Scholar 

  • Skelsey, P., Rossing, W. A. H., Kessel, G. J. T., Powell, J., & van der Werf, W. (2005). Influence of host diversity on development of epidemics: An evaluation and elaboration of mixture theory. Phytopathology, 95, 328–338.

    Article  CAS  PubMed  Google Scholar 

  • Snoeijers, S. S., Pérez-García, A., Joosten, H. A. J., & De Wit, P. J. G. M. (2000). The effect of nitrogen on disease development and gene expression in bacterial and fungal plant pathogens. European Journal of Plant Pathology, 106, 493–506.

    Article  CAS  Google Scholar 

  • Strehmel, N., Bottcher, C., Schmidt, S., & Scheel, D. (2014). Profiling of secondary metabolites in root exudates of Arabidopsis thaliana. Phytochemistry, 108, 35–46.

    Article  CAS  PubMed  Google Scholar 

  • Tilman, D., Cassman, K. G., Matson, P. A., Naylor, R., & Polasky, S. (2002). Agricultural sustainability and intensive production practices. Nature, 418, 671–677.

    Article  CAS  PubMed  Google Scholar 

  • Tooker, J. F., & Frank, S. D. (2012). Genotypically diverse cultivar mixtures for insect pest management and increased crop yields. Journal of Applied Ecology, 49, 974–985.

    Article  Google Scholar 

  • Trenbath, B. R. (1993). Intercropping-bases of productivity intercropping for the management of pests and diseases. Field Crops Research, 34, 381–405.

    Article  Google Scholar 

  • Turnbull, L. A., & Hector, A. (2010). How to get even with pests. Nature, 466, 36–37.

    Article  CAS  PubMed  Google Scholar 

  • van Dam, N. M., & Bouwmeester, H. (2016). Metabolimics in the rhizosphere: Tapping into belowground chemical communication. Trends in Plant Science, 21, 256–265.

    Article  CAS  PubMed  Google Scholar 

  • Vandermeer, J. (1998). Maximizing crop yield in alley crops. Agroforestry Systems, 40, 199–206.

    Article  Google Scholar 

  • Weston, L. A., & Mathesius, U. (2013). Flavonoids: Their structure, biosynthesis and role in the rhizosphere, including allelopathy. Journal of Chemical Ecology, 39, 283–293.

    Article  CAS  PubMed  Google Scholar 

  • Wiik, L. (2009). Yield and disease control in winter wheat in southern Sweden during 1977-2005. Crop Protection, 28, 82–89.

    Article  Google Scholar 

  • Willey, R. W. (1985). Evaluation and presentation of intercropping advantages. Experimental Agriculture, 21, 119–133.

    Article  Google Scholar 

  • Xu, W. H., Liu, D., Wu, F. Z., & Liu, S. W. (2015). Root exudates of wheat are involved in suppression of Fusarium wilt in watermelon in watermelon-wheat companion cropping. European Journal of Plant Pathology, 141, 209–216.

    Article  Google Scholar 

  • Yu, Y., Stomph, T. J., Makowski, D., & van der Werf, W. (2015). Temporal niche differentiation increases the land equivalent ratio of annual intercrops: A meta-analysis. Field Crops Research, 184, 133–144.

    Article  Google Scholar 

  • Yu, Y., Stomph, T., Makowski, D., Zhang, L. Z., & van der Werf, W. (2016). A meta-analysis of relative crop yields in cereal/legume mixtures suggests options for management. Field Crops Research, 198, 269–279.

    Article  Google Scholar 

  • Zadoks, J. C., & Schein, R. D. (1979). Epidemiology and plant disease management (p. 427). Oxford: Oxford University Press.

    Google Scholar 

  • Zhang, F. S., & Li, L. (2003). Using competitive and facilitative interactions in intercropping systems enhances crop productivity and nutrient-use efficiency. Plant and Soil, 248, 305–312.

    Article  CAS  Google Scholar 

  • Zhang, S., Luo, H. G., Zhang, Q. D., Xu, Y. Y., Zou, C. H., Guo, M. L., He, S. M., Fang, X. W., Zhang, J. X., & Chen, Q. Z. (2008). Effects of nitrogen and potassium fertilizer applications on yield and occurrence of major diseases and insect pests of rice. Journal of Huazhong Agricultural University, 27, 732–735 (In Chinese).

    Article  Google Scholar 

  • Zhu, Y. Y., Chen, H. R., Fan, J. H., Wang, Y. Y., Li, Y., Chen, J. B., Fan, J. X., Yang, S. S., Hu, L. P., Leung, H., Mew, T. W., Teng, P. S., Wang, Z. H., & Mundt, C. C. (2000). Genetic diversity and disease control in rice. Nature, 406, 718–722.

    Article  CAS  PubMed  Google Scholar 

  • Zuur AF, Ieno EN, Walter NJ, Saveliev AA & Smith GM. 2009. Mixed effects models and extensions in ecology with R. Springer, 574 pp.

Download references

Acknowledgments

We are grateful for the financial support from the key project of the Ministry of Science and Technology of China (grant number 2016YFE0101100), the National Natural Science Foundation of China (NO. 31210103906), the Chinese National Basic Research Program (2015CB150405), and the European Union’s Horizon 2020 Programme for Research & Innovation under grant agreement n°727217 “ReMIX”.

Author information

Authors and Affiliations

Authors

Contributions

YD and CZ did the literature search, extracted data and conducted the analysis. CZ, YD, YY, DM and WW designed methods for statistical meta-analysis and interpreted results. All authors contributed to formulation of research aims and overall approach, discussed outcomes and approved the submission. CZ, YD, DM and WW wrote the paper.

Corresponding author

Correspondence to Chaochun Zhang.

Ethics declarations

Conflict of interests

The authors declare no conflicts of interests.

Electronic supplementary material

ESM 1

(DOCX 2856 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, C., Dong, Y., Tang, L. et al. Intercropping cereals with faba bean reduces plant disease incidence regardless of fertilizer input; a meta-analysis. Eur J Plant Pathol 154, 931–942 (2019). https://doi.org/10.1007/s10658-019-01711-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-019-01711-4

Keywords

Navigation