Positive effects of root-knot nematodes (Meloidogyne incognita) on nitrogen availability do not outweigh their negative effects on fitness in Nicotiana attenuata

Abstract

Aims

Root herbivory incurs fitness costs, but herbivory by nematodes can additionally increase nutrient availability mediated by enhanced root exudation and soil microbial activity and change plant susceptibility to aboveground herbivores due to systemic changes in plant defence. We hypothesized that such positive indirect effects may outweigh the negative direct effects of root herbivory by nematodes on plant performance.

Methods

We tested the effects of transient (3 weeks) and continuous (11 weeks) belowground herbivory by root-knot nematodes (Meloidogyne incognita) on the biomass, nitrogen levels, and reproductive output of Nicotiana attenuata, and its interaction with a specialist aboveground herbivore (Manduca sexta) in a greenhouse study.

Results

Continuous nematode herbivory caused an increase in shoot biomass and enhanced nitrogen levels in roots, shoots and seeds, but reduced the reproductive output of N. attenuata. Short-term, transient nematode herbivory had no effects. Feeding by the aboveground herbivore reduced reproductive output and increased seed nitrogen content. Nicotine levels in leaves and the plant interaction with M. sexta were not influenced by nematode herbivory.

Conclusion

In summary, only continuous nematode herbivory indirectly increased nitrogen availability and caused resource sequestration to the shoots; however, this effect was not strong enough to outweigh the direct fitness costs of nematode herbivory.

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Acknowledgments

We wish to thank Anke Steppuhn and Michèle Bandoly for providing N. attenuata seeds and for their advice and help with nicotine measurements. The diligent technical assistance of Monika Fünning, Anne Plank and Cynthia Kienzle is also gratefully acknowledged. This study was funded by the Deutsche Forschungsgemeinschaft (Collaborative Research Centre 973 “Priming and Memory of Organismic Responses to Stress” – Project B3).

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Correspondence to Caspar Schöning.

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Responsible Editor: Juha Mikola.

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Schöning, C., Wurst, S. Positive effects of root-knot nematodes (Meloidogyne incognita) on nitrogen availability do not outweigh their negative effects on fitness in Nicotiana attenuata . Plant Soil 400, 381–390 (2016). https://doi.org/10.1007/s11104-015-2738-4

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Keywords

  • Root exudation
  • Resource allocation
  • Root herbivory