A tritrophic signal that attracts parasitoids to host-damaged plants withstands disruption by non-host herbivores

Abstract

BackgroundVolatiles emitted by herbivore-infested plants are highly attractive to parasitoids and therefore have been proposed to be part of an indirect plant defense strategy. However, this proposed function of the plant-provided signals remains controversial, and it is unclear how specific and reliable the signals are under natural conditions with simultaneous feeding by multiple herbivores. Phloem feeders in particular are assumed to interfere with plant defense responses. Therefore, we investigated how attack by the piercing-sucking cicadellid Euscelidius variegatus influences signaling by maize plants in response to the chewing herbivore Spodoptera littoralis.ResultsThe parasitoid Cotesia marginiventris strongly preferred volatiles of plants infested with its host S. littoralis. Overall, the volatile emissions induced by S. littoralis and E. variegatus were similar, but higher levels of certain wound-released compounds may have allowed the wasps to specifically recognize plants infested by hosts. Expression levels of defense marker genes and further behavioral bioassays with the parasitoid showed that neither the physiological defense responses nor the attractiveness of S. littoralis infested plants were altered by simultaneous E. variegatus attack.ConclusionsOur findings imply that plant defense responses to herbivory can be more robust than generally assumed and that ensuing volatiles convey specific information about the type of herbivore that is attacking a plant, even in complex situations with multiple herbivores. Hence, the results of this study support the notion that herbivore-induced plant volatiles may be part of a plant's indirect defense stratagem.

Unraveling molecular mechanisms underlying plant defense in response to dual insect attack : studying density-dependent effects

“…For instance, attraction of the predatory mite Phytoseiulus persimilis to volatiles from Lima bean plants (Phaseolus lunatus) infested by spider mites (Tetranychus urticae) and attraction of the parasitoid Cotesia vestalis to volatile blends emitted by P. xylostella-infested cabbage plants (Brassica oleracea) are density-dependent (Gols et al, 2003;Girling et al, 2011). Compared with feeding by only one insect species, herbivory by a second herbivore may influence indirect defense responses (Rodriguez-Saona et al, 2003;Rodriguez-Saona et al, 2005;Heil, 2008;Erb et al, 2010;, which can also be affected by the density of the attacking insects . Simultaneous feeding by phloem-feeding whiteflies and Spodoptera exigua caterpillars on cotton plants (Gossypium hirsutum) reduced the emission of the terpenes DMNT ((E)-4,-8-dimethyl-1, 3,7-nonatriene), TMTT and mycrene compared to plants infested by only S. exigua (Rodriguez-Saona et al, 2003).…”

“…It has been hypothesized that by activating the SA signaling pathway, phloem feeders suppress JA-dependent defenses to which phloem feeders are more sensitive Zarate et al, 2007). Several recent studies have supported the interference of SA with JA-inducible defenses against chewing insects , although phloem-feeding insects do not in all cases interfere with the defenses induced by chewing herbivores (Erb et al, 2010), which may be due to density effects or to differences between species.…”

“…Interactions between multiple insect attackers affect the induction of JA-, SA-, and ET-dependent defense responses and could lead to positive or negative effects on the performance of the attacking herbivores (Rodriguez-Saona et al, 2005;. Similarly, multiple insect attack could also affect indirect defense responses through a change in the emission of HIPVs such that it can affect the attraction of parasitoids and predators Erb et al, 2010;Schwartzberg et al, 2011;Ponzio et al, 2014;. The regulation of plant defense depends on factors such as the number of insect species attacking simultaneously and insect density.…”

“…In addition, it is known that phloem-feeding herbivores such as aphids induce lower levels of HIPV emission compared to chewing herbivores (Turlings et al, 1998;Rodriguez-Saona et al, 2003;Truong et al, 2014). Consequently, multiple herbivores feeding on plants interact indirectly through plant-mediated effects and this may alter emission of HIPVs (Rodriguez-Saona et al, 2003;Ponzio et al, 2013) such that it can affect the attractiveness of the plant to predators and parasitoids compared to single insect attack Erb et al, 2010;. For example, herbivory by the phloem-feeding whitefly Bemisia tabaci interfered with indirect defenses of A. thaliana to P. xylostella caterpillars.…”

“…Multiple insect species feeding on the same plant interact through plant-mediated effects and affect both direct and indirect ) plant defense responses. Recent research reported interference by phloem-feeding insects with induced defenses against chewing herbivores (Rodriguez-Saona et al, 2005;Erb et al, 2010;Schwartzberg et al, 2011;Ponzio et al, 2014;. However, little is known about caterpillar interference with aphid-induced (in)direct defenses (Agbogba and Powell, 2007;.…”