Proceedings of the Royal Society B: Biological Sciences
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Synergistic effects of direct and indirect defences on herbivore egg survival in a wild crucifer

Nina E. Fatouros

Nina E. Fatouros

Laboratory of Entomology, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands

[email protected]

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Ana Pineda

Ana Pineda

Laboratory of Entomology, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands

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Martinus E. Huigens

Martinus E. Huigens

Laboratory of Entomology, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands

Dutch Butterfly Conservation, Mennonietenweg 10, 6702 AD Wageningen, The Netherlands

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Colette Broekgaarden

Colette Broekgaarden

Department of Plant Breeding, Wageningen University and Research Centre, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands

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Methew M. Shimwela

Methew M. Shimwela

Plant Pathology Department, University of Florida, PO Box 110680, Gainesville, FL, USA

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Ilich A. Figueroa Candia

Ilich A. Figueroa Candia

Fundación PROINPA, Avenida Elias Meneces Km 4, El Paso, Cochabamba, Bolivia

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Patrick Verbaarschot

Patrick Verbaarschot

Laboratory of Entomology, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands

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Tibor Bukovinszky

Tibor Bukovinszky

Resource Ecology Group, Wageningen University, Droevendaalsesteeg 3a, 6708 PB Wageningen, The Netherlands

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    Evolutionary theory of plant defences against herbivores predicts a trade-off between direct (anti-herbivore traits) and indirect defences (attraction of carnivores) when carnivore fitness is reduced. Such a trade-off is expected in plant species that kill herbivore eggs by exhibiting a hypersensitive response (HR)-like necrosis, which should then negatively affect carnivores. We used the black mustard (Brassica nigra) to investigate how this potentially lethal direct trait affects preferences and/or performances of specialist cabbage white butterflies (Pieris spp.), and their natural enemies, tiny egg parasitoid wasps (Trichogramma spp.). Both within and between black mustard populations, we observed variation in the expression of Pieris egg-induced HR. Butterfly eggs on plants with HR-like necrosis suffered lower hatching rates and higher parasitism than eggs that did not induce the trait. In addition, Trichogramma wasps were attracted to volatiles of egg-induced plants that also expressed HR, and this attraction depended on the Trichogramma strain used. Consequently, HR did not have a negative effect on egg parasitoid survival. We conclude that even within a system where plants deploy lethal direct defences, such defences may still act with indirect defences in a synergistic manner to reduce herbivore pressure.

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