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Bottom-up and top-down herbivore regulation mediated by glucosinolates in Brassica oleracea var. acephala

  • Plant-microbe-animal interactions - Original research
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Abstract

Quantitative differences in plant defence metabolites, such as glucosinolates, may directly affect herbivore preference and performance, and indirectly affect natural enemy pressure. By assessing insect abundance and leaf damage rate, we studied the responses of insect herbivores to six genotypes of Brassica oleracea var. acephala, selected from the same cultivar for having high or low foliar content of sinigrin, glucoiberin and glucobrassicin. We also investigated whether the natural parasitism rate was affected by glucosinolates. Finally, we assessed the relative importance of plant chemistry (bottom-up control) and natural enemy performance (top-down control) in shaping insect abundance, the ratio of generalist/specialist herbivores and levels of leaf damage. We found that high sinigrin content decreased the abundance of the generalist Mamestra brassicae (Lepidoptera, Noctuidae) and the specialist Plutella xylostella (Lepidoptera, Yponomeutidae), but increased the load of the specialist Eurydema ornatum (Hemiptera, Pentatomidae). Plants with high sinigrin content suffered less leaf injury. The specialist Brevicoryne brassicae (Hemiptera, Aphididae) increased in plants with low glucobrassicin content, whereas the specialists Pieris rapae (Lepidoptera, Pieridae), Aleyrodes brassicae (Hemiptera, Aleyrodidae) and Phyllotreta cruciferae (Coleoptera, Chrysomelidae) were not affected by the plant genotype. Parasitism rates of M. brassicae larvae and E. ornatum eggs were affected by plant genotype. The ratio of generalist/specialist herbivores was positively correlated with parasitism rate. Although both top-down and bottom-up forces were seen to be contributing, the key factor in shaping both herbivore performance and parasitism rate was the glucosinolate concentration, which highlights the impact of bottom-up forces on the trophic cascades in crop habitats.

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Acknowledgments

This research was supported by the National Plan for Research and Development (AGL2012-35539). The authors thank Rosaura Abilleira, Pilar Comesaña, César González, and Tamara Sotelo for their valuable help in field samplings. We also thank David Brown for improving the English. S. Santolamazza-Carbone acknowledges a post-doctoral research contract (JAE-Doc) from the CSIC.

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Authors and Affiliations

  1. Misión Biológica de Galicia, Consejo Superior de Investigaciones Científicas (MBG-CSIC), P.O. Box 28, 36080, Pontevedra, Spain

    Serena Santolamazza-Carbone, Pablo Velasco, Pilar Soengas & María Elena Cartea

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  1. Serena Santolamazza-Carbone
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  2. Pablo Velasco
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  3. Pilar Soengas
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  4. María Elena Cartea
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Correspondence to Serena Santolamazza-Carbone.

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Communicated by Merijn Kant.

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Santolamazza-Carbone, S., Velasco, P., Soengas, P. et al. Bottom-up and top-down herbivore regulation mediated by glucosinolates in Brassica oleracea var. acephala . Oecologia 174, 893–907 (2014). https://doi.org/10.1007/s00442-013-2817-2

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