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Plant-mediated interactions between shoot-feeding aphids and root-feeding nematodes depend on nitrate fertilization

  • Plant-microbe-animal interactions - Original research
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Abstract

The plant metabolite composition is modulated by various abiotic and biotic factors including nutrient availability and herbivory. In turn, induced changes in plant quality can affect herbivore performance and mediate indirect interactions between spatially separated herbivores sharing a host. Studies on plant-mediated herbivore interactions have been carried out at single fertilization regimes only, but we hypothesized that nutrient availability modifies these interactions. Therefore, we studied the interactions between two vascular tissue herbivores, the aboveground feeding aphid Brevicoryne brassicae and the belowground infesting nematode Heterodera schachtii, on Arabidopsis thaliana grown under two nitrate fertilization conditions (varying by 33 %). Furthermore, we investigated plant growth and primary metabolic responses to fertilization and herbivore treatments, which could potentially mediate these interactions, as the herbivores may act as metabolic sinks. Whereas nematodes had no effects on aphids, aphid presence influenced nematodes in opposite directions, depending on fertilization: at low nitrate supply, aphids had a promoting effect on nematodes, whereas at high nitrate fertilization they lowered the nematode infestation compared to control plants. Plants produced significantly more biomass under high nitrate supply but C and N contents were not altered. Primary metabolite profiles differed only marginally between roots of both fertilization treatments in plants with and without aphids, indicating that nematodes may respond to these or other metabolic modifications, which are caused by minute environmental changes, in a sensitive way. Our results highlight the need to consider the importance of plant nutrient availability on the outcome of interactions between co-occurring herbivores in future studies.

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Acknowledgments

The authors thank Linda Ehlert for assistance with plant cultivation, Jana Niekamp for help with nematode counting, Bianca Kreuzinger for practical help, Dr. Björn Niere for an initial nematode culture, and Prof. Dr. Karsten Niehaus for providing standards of various primary metabolites. This work was supported by the grant MU 1829/9-1 of the Deutsche Forschungsgemeinschaft.

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  1. Department of Chemical Ecology, Bielefeld University, Universitätsstr. 25, 33615, Bielefeld, Germany

    Magdalene Kutyniok & Caroline Müller

  2. Institute for Genome Research and Systems Biology, CeBiTec, 33615, Bielefeld, Germany

    Magdalene Kutyniok & Caroline Müller

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  1. Magdalene Kutyniok
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  2. Caroline Müller
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Correspondence to Caroline Müller.

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Communicated by Russell K Monson.

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442_2013_2712_MOESM1_ESM.docx

Supplementary material: Table S1 Primary metabolites detected in Arabidopsis thaliana roots in plants either fertilized with low (F L) or 33 % higher (F H) nitrate doses and with or without aphid shoot herbivory, respectively. (DOCX 73 kb)

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Kutyniok, M., Müller, C. Plant-mediated interactions between shoot-feeding aphids and root-feeding nematodes depend on nitrate fertilization. Oecologia 173, 1367–1377 (2013). https://doi.org/10.1007/s00442-013-2712-x

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