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Consequences of combined herbivore feeding and pathogen infection for fitness of Barbarea vulgaris plants

  • Plant-microbe-animal interactions - Original research
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Abstract

Plants are often attacked by pathogens and insects. Their combined impact on plant performance and fitness depends on complicated three-way interactions and the plant’s ability to compensate for resource losses. Here, we evaluate the response of Barbarea vulgaris, a wild crucifer, to combined attack by an oomycete Albugo sp., a plant pathogen causing white rust, and a flea beetle, Phyllotreta nemorum. Plants from two B. vulgaris types that differ in resistance to P. nemorum were exposed to Albugo and P. nemorum alone and in combination and then monitored for pathogen infection, herbivore damage, defence compounds, nutritional quality, biomass and seed production. Albugo developed infections in the insect-resistant plants, whereas insect-susceptible plants were scarcely infected. Concentrations of Albugo DNA were higher in plants also exposed to herbivory; similarly, flea beetle larvae caused more damage on Albugo-infected plants. Concentrations of saponins and glucosinolates strongly increased when the plants were exposed to P. nemorum and when the insect-susceptible plants were exposed to Albugo, and some of these compounds increased even more in the combined treatment. The biomass of young insect-susceptible plants was lower following exposure to flea beetles, and the number of leaves of both plant types was negatively affected by combined exposure. After flowering, however, adult plants produced similar numbers of viable seeds, irrespective of treatment. Our findings support the concept that pathogens and herbivores can affect each other’s performance on a host plant and that the plant reacts by inducing specific and general defences. However, plants may be able to compensate for biomass loss from single and combined attacks over time.

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Acknowledgments

We are grateful to the Barbarea group at University of Copenhagen for fruitful discussions and support. We thank L. Munk and E. B. Holub for advice on Albugo inoculation. M-B. Sauer, C. Heimes, S. Christensen and H. Olsen helped with the practical work, J. K. Schjoerring and A.H. Ivø with the nitrogen analyses, and R. A. de Graaf with the glucosinolate analyses. This work was funded by the Danish Agency for Science, Technology and Innovation (grant no. 274-08-0462); the authors declare that they have no conflict of interest with this Agency. All experiments comply with current Danish laws.

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Authors and Affiliations

  1. Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg, Denmark

    Tamara van Mölken, Vera Kuzina, Karen Rysbjerg Munk, Carl Erik Olsen, Thomas Sundelin & Thure P. Hauser

  2. Department of Ecogenomics, Radboud University Nijmegen, Nijmegen, The Netherlands

    Nicole M. van Dam

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  1. Tamara van Mölken
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  2. Vera Kuzina
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Correspondence to Thure P. Hauser.

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Communicated by Corné Pieterse.

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van Mölken, T., Kuzina, V., Munk, K.R. et al. Consequences of combined herbivore feeding and pathogen infection for fitness of Barbarea vulgaris plants. Oecologia 175, 589–600 (2014). https://doi.org/10.1007/s00442-014-2928-4

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