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Parasitic plants indirectly regulate below-ground properties in grassland ecosystems

Abstract

Parasitic plants are one of the most ubiquitous groups of generalist parasites in both natural and managed ecosystems, with over 3,000 known species worldwide1,2,3. Although much is known about how parasitic plants influence host peformance1,2,3,4, their role as drivers of community- and ecosystem-level properties remains largely unexplored5. Parasitic plants have the potential to influence directly the productivity and structure of plant communities because they cause harm to particular host plants, indirectly increasing the competitive status of non-host species6,7,8,9,10. Such parasite-driven above-ground effects might also have important indirect consequences through altering the quantity and quality of resources that enter soil, thereby affecting the activity of decomposer organisms3,11,12,13. Here we show in model grassland communities that the parasitic plant Rhinanthus minor, which occurs widely throughout Europe and North America14, has strong direct effects on above-ground community properties, increasing plant diversity and reducing productivity. We also show that these direct effects of R. minor on the plant community have marked indirect effects on below-ground properties, ultimately increasing rates of nitrogen cycling. Our study provides evidence that parasitic plants act as a major driver of both above-ground and below-ground properties of grassland ecosystems.

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Figure 1: Mean (± s.e.m.) values for plant community parameters as affected by the presence of R. minor after three years.
Figure 2: Mean (± s.e.m.) values for fungal-to-bacterial biomass ratio, calculated using PLFA, after three years.
Figure 3: Mean (± s.e.m.) values for soil N cycling parameters as affected by the presense of R. minor after three years.

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Acknowledgements

We are grateful to the UK Department for Environment, Food and Rural Affairs (DEFRA) for funding this work under their species-rich grassland programme. We thank D. Wardle, L. Walker, E. Ayres, R. Van der Wal, K. Harrison, N. Ostle and K. Wilson for their comments on the manuscript, and R. Brand Hardy of DEFRA for his continued support of this work. Author Contributions R. S. Smith was the project leader, responsible for the experimental design and the vegetation aspects, with S.P. and J.M.S. responsible for most of the data collection and management of the mesocosm experiment. R.D.B. was responsible for below-ground aspects of the study, with assistance from H.Q. and P.J.H. R. S. Shiel provided statistical support.

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Correspondence to Richard D. Bardgett.

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Supplementary information

Supplementary Table 1

This table shows mean soil nutrient concentrations (mg l-1), pH, and percent organic matter of each residual soil fertility treatments at the start of the experiment.

Supplementary Table 2

This table shows the effect of residual soil fertility and farmyard manure (FYM) application treatments on total aboveground biomass (kg ha-1), excluding Rhinanthus minor, after one (2001) and three years (2003).

Supplementary Table 3

This table shows the effects of residual soil fertility on phosphorus content of plant tissues and root mycorrhizal colonisation for Lolium perenne, Geranium sylvaticum and Ranunculus acris in 2003.

Supplementary Table 4

This table shows mean and range of total nitrogen, phosphorus and potassium content of mesocosm plant species tissue (mg g-1).

Supplementary Figure 1

This image shows the test species Rhinanthus minor in agricultural grassland in northern England.

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Bardgett, R., Smith, R., Shiel, R. et al. Parasitic plants indirectly regulate below-ground properties in grassland ecosystems. Nature 439, 969–972 (2006). https://doi.org/10.1038/nature04197

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