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Agricultural management and pesticide use reduce the functioning of beneficial plant symbionts

Abstract

Phosphorus (P) acquisition is key for plant growth. Arbuscular mycorrhizal fungi (AMF) help plants acquire P from soil. Understanding which factors drive AMF-supported nutrient uptake is essential to develop more sustainable agroecosystems. Here we collected soils from 150 cereal fields and 60 non-cropped grassland sites across a 3,000 km trans-European gradient. In a greenhouse experiment, we tested the ability of AMF in these soils to forage for the radioisotope 33P from a hyphal compartment. AMF communities in grassland soils were much more efficient in acquiring 33P and transferred 64% more 33P to plants compared with AMF in cropland soils. Fungicide application best explained hyphal 33P transfer in cropland soils. The use of fungicides and subsequent decline in AMF richness in croplands reduced 33P uptake by 43%. Our results suggest that land-use intensity and fungicide use are major deterrents to the functioning and natural nutrient uptake capacity of AMF in agroecosystems.

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Fig. 1: Experimental set-up using Plantago lanceolata as model plant.
Fig. 2: Comparison of grassland and cropland soils.
Fig. 3: Relative importance of predictors.
Fig. 4: Recovery of 33P in grassland sites.
Fig. 5: Recovery of 33P in cropland sites.

Data availability

The data that support the findings of this study are available here: https://doi.org/10.6084/m9.figshare.15134328.

Code availability

The code used to analyse the data is available here: https://doi.org/10.6084/m9.figshare.15134670.

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Acknowledgements

We thank all the farmers and farm managers for allowing us to sample their fields and for completing our detailed questionnaires. We also thank A. Bonvicini, L. Schönholzer, M. Macsai, F. Tamburini, H. Gamper, S. Müller, D. Bürge, M. Zuber, S. Zhao, V. Somerville, A. Brugger, O. Scholz, D. Bugmann, R. Heiz, B. Seitz and M. Roser for help with field work, the design and execution of the greenhouse experiment and lab analyses. We also thank J. Helfenstein and the anonymous reviewers for valuable feedback on the manuscript. The Digging Deeper project was funded through the 2015–2016 BiodivERsA COFUND call for research proposals, with the national funders Swiss National Science Foundation (grant 31BD30-172466), Deutsche Forschungsgemeinschaft (317895346), Swedish Research Council Formas (contract 2016-0194), Ministerio de Economía y Competitividad (Digging_Deeper, Ref. PCIN-2016-028) and Agence Nationale de la Recherche (ANR, France; grant ANR-16-EBI3-0004-01).

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Authors and Affiliations

Authors

Contributions

M.G.A.v.d.H., S.H., F.T.M., L.P. and M.C.R. designed the study and obtained research funding. A.E., G.G., K.H., S.B., A.V.-H., C.H., E.K., D.S.P., S.R., A. Saghaï, F.D., P.G.-P. and A. Spor contributed to data collection and analysis. J.J. and E.F. supported the design and execution of the greenhouse experiment. A.E. conducted data analysis. A.E., G.G., M.G.A.v.d.H. and J.J. were involved in the interpretation of results. A.E., G.G. and M.G.A.v.d.H. drafted the manuscript with significant contributions to the writing from all co-authors. All authors commented on and approved the final manuscript.

Corresponding author

Correspondence to Marcel G. A. van der Heijden.

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Nature Ecology & Evolution thanks Minxia Liang, Katie Field and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Sampling locations of the grassland and cropland soils in Europe.

Grassland sites comprised both extensively used grasslands in the vicinity of sampled croplands, as well as marginal land (field strips next to the croplands).

Extended Data Fig. 2 Relationship between the soil microbial biomass carbon (a), AMF richness associated with plant roots (b), and soil available P (c) with the 33P recovery in grassland (green) and cropland soils (orange).

Asterisks indicate a significant relationship at p < 0.001 (***). The grey polygon marks a confidence level of 0.95. Since eight sites had to be excluded in the estimation of AMF richness, the no. of observation is smaller in B (n = 142).

Extended Data Fig. 3 The relationship between hyphal 33P transfer activity (measured as 33P recovery in the shoots) and the shoot N:P ratio (scale log-transformed) in grassland (a) and cropland soils (b).

The polygons frame the upper and lower confidence level (0.95). Asterisks indicate the significances of the relationships at p < 0.001 (***) and p < 0.05 (*).

Extended Data Fig. 4 Site-specific variation of AMF communities.

Relative abundances of different families of AMF per site in cropland soils (n = 146) and grassland soils (n = 58).

Extended Data Fig. 5 Structural Equation Models demonstrating the drivers of root AMF richness and 33P recovery in grassland (a and b) and cropland (c and d) soils.

Models a and c assume no direct relationship between AMF richness and 33P recovery. In b and d, a unidirectional relationship between AMF richness and 33P recovery was defined. Solid and dashed lines represent positive and negative associations, respectively. Curved lines indicate co-variances. The line width corresponds to the regression coefficient shown next to the respective line. Numbers next to the response variables represent the coefficients of variance. Significances are indicated by ***. **, * (p < 0.001, p < 0.01, p < 0.05) and non-significant relationships are coloured in grey. P-values of the Chi-square parameter for model a, b, c and d were 0.772, 0.772, 0.799 and 0.829 (p-values higher 0.05 indicate significant models).

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Supplementary Tables 1–5, Figs. 1–5 and Methods.

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Supplementary Tables 6 and 7

Supplementary Tables 6 and 7: correlation matrix showing Spearman’s correlation coefficient between predictors in grassland (Supplementary Table 6) and cropland (Supplementary Table 7) sites. The selected predictors used for the model-selection procedure are marked with an x. Correlation coefficients >0.80 are highlighted in bold. Significant correlations are indicated as *** P < 0.001, ** P < 0.01, * P < 0.05. ‘Location’ refers to the geographic distance from the southwest-most sampling site.

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Edlinger, A., Garland, G., Hartman, K. et al. Agricultural management and pesticide use reduce the functioning of beneficial plant symbionts. Nat Ecol Evol 6, 1145–1154 (2022). https://doi.org/10.1038/s41559-022-01799-8

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