Abstract
Plants possess various inducible defences that result in synthesis of specialized metabolites in response to herbivory, which can interfere with the performance of herbivores of the same and other species. Much less is known of the effects of plant feeding by omnivores. We found that previous feeding of the omnivorous predator Macrolophus pygmaeus on sweet pepper plants significantly reduced reproduction of the two-spotted spider mite Tetranychus urticae and western flower thrips Frankliniella occidentalis on the same plants, also on leaves that had not been exposed to the omnivore. In contrast, no effect was found on the reproduction of the green peach aphid Myzus persicae. Juvenile survival and developmental time of T. urticae and M. persicae, and larval survival of F. occidentalis were not affected by plant feeding by M. pygmaeus. Larvae of F. occidentalis feeding on leaves previously exposed to M. pygmaeus required longer to develop into adults. Defence-related plant hormones were produced locally and systemically after exposure to M. pygmaeus. The concentrations of 12-oxo-phytodienoic acid and jasmonic acid–isoleucine in the attacked leaves were significantly higher than in the corresponding leaves on the uninfested plants, and jasmonic acid concentrations showed the same trend, suggesting that jasmonic-acid-related defence pathways were activated. In contrast, similar concentrations of salicylic acid were found in the attacked leaves of M. pygmaeus-infested plants and uninfested plants. Our results show that plant feeding by omnivorous predators decreases the performance of herbivores, suggesting that it induces plant defences.
Highlights
Plants employ different types of defences to resist herbivores
We show that the feeding of M. pygmaeus on sweet pepper plants lowers the performance of two of the three herbivore species feeding on the same plants through induced defences
The reproduction of T. urticae and F. occidentalis on M. pygmaeus-infested plants was significantly lower than on uninfested plants, on the leaves that had been exposed to M. pygmaeus, and on other leaves of the same plants, showing that the effect was systemic
Summary
Plants employ different types of defences to resist herbivores. Such defences can be displayed constitutively or can be induced. Macrolophus pygmaeus is an important omnivorous predator of several agricultural pests such as whiteflies (Montserrat et al 2000), thrips (Riudavets and Castañé 1998), aphids (Alvarado et al 1997), spider mites (Hansen et al 1999), leaf miners (Arnó et al 2003) and Lepidoptera species, including Tuta absoluta (Urbaneja et al 2009) It attacks a wide range of arthropod pests and is commercially used for the biological control of spider mites and whiteflies. We investigated the effects of phytophagy of M. pygmaeus on the performance of three species of its herbivorous prey, the two-spotted spider mite Tetranychus urticae Koch (Acari, Tetranychidae), the green peach aphid Myzus persicae (Hemiptera, Aphididae), and the western flower thrips Frankliniella occidentalis (Pergande) (Thysanoptera, Thripidae) These herbivores species employ different feeding strategies. We quantified the hormone12-oxo-phytodienoic acid (OPDA), which is the precursor of JA (Wasternack and Hause 2013), JA-isoleucine (JA-Ile), which is the main bioactive form of JA and plays a key role in regulating defence gene expression (Fonseca et al 2009), and abscisic acid (ABA) (Bodenhausen and Reymond 2007; Pieterse et al 2009), which plays an important ancillary role in fine-tuning plant defences (Kessler and Baldwin 2002; Vos et al 2013; Kant et al 2015)
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