Herbivore performance and plant defense after sequential attacks by inducing and suppressing herbivores

Abstract

It is well known that herbivore-induced plant defenses alter host plant quality and can affect the behavior and performance of later arriving herbivores. Effects of sequential attacks by herbivores that either suppress or induce plant defenses are less well studied. We sequentially infested leaves of tomato plants with a strain of the phytophagous spider mite Tetranychus urticae that induces plant defenses and the closely related Tetranychus evansi, which suppresses plant defenses. Plant quality was quantified through oviposition of both spider mite species and by measuring proteinase inhibitor activity using plant material that had been sequentially attacked by both herbivore species. Spider-mite oviposition data show that T. evansi could suppress an earlier induction of plant defenses by T. urticae, and T. urticae could induce defenses in plants previously attacked by T. evansi in 1 day. Longer attacks by the second species did not result in further changes in oviposition. Proteinase inhibitor activity levels showed that T. evansi suppressed the high activity levels induced by T. urticae to constitutive levels in 1 day, and further suppressed activity to levels similar to those in plants attacked by T. evansi alone. Attacks by T. urticae induced proteinase inhibitor activity in plants previously attacked by T. evansi, eventually to similar levels as induced by T. urticae alone. Hence, plant quality and plant defenses were significantly affected by sequential attacks and the order of attack does not affect subsequent performance, but does affect proteinase inhibitor activity levels. Based on our results, we discuss the evolution of suppression of plant defenses.

Poplar protease inhibitor expression differs in an herbivore specific manner

“…In soybean, damage by fall armyworm caterpillars increased the activity of PIs, whereas thrips damage did not [43]. De Oliveira et al [11] even observed varying response of tomato PIs to damage by herbivores of the same genus. They showed that PI activity was induced by the spider mite Tetranychus urticae, but was suppressed by T. evansi [11].…”

“…De Oliveira et al [11] even observed varying response of tomato PIs to damage by herbivores of the same genus. They showed that PI activity was induced by the spider mite Tetranychus urticae, but was suppressed by T. evansi [11]. Interestingly, feeding damage by lepidopteran and coleopteran herbivores in tomato yielded opposite results to our study in black poplar.…”

Changes in plant responses induced by an arthropod influence the colonization behavior of a subsequent herbivore

“…T. urticae feeds on the epidermis and punctures parenchyma cells, leaving light‐colored stipples on the leaf surface and injecting phytotoxic compounds that reduce photosynthesis and decrease yield 37,38 . T. urticae activates both the JA and SA signaling pathways, which function differently in plant–arthropod interactions 15,28,39–41 . For instance, up‐regulation of plant defenses such as proteinase inhibitors and allelochemicals caused by T. urticae is correlated with significantly poor performances of the cucumber moth, Diaphania indica (Saunders) (Lepidoptera: Pyralidae), and the red spider mite, T. evansi Baker (Acari: Tetranychidae).…”

Multiple Infestations Induce Direct Defense of Maize to Tetranychus urticae (Acari: Tetranychidae)

“…Thus, the ecological interactions between maize and T. urticae may be insufficient to make selection pressure to input evaluation of plant defense mechanisms. Furthermore, previous studies showed that 1 d of infestation is sufficient for the T. urticae to induce plant defenses (Kant et al 2004;Oliveira et al 2016Oliveira et al , 2017.…”

“…The treatments were 2 versions of Bt maize and non Bt; uninfested (= clean) plants; single infestation with spider mite; and dual species infestation with spider mite and fall armyworm for each maize version. Two d after the first infestation, all plants were re-infested with spider mite to evaluate the impact of previous infestations, because 1 d of infestation is sufficient for T. urticae to induce defense in other plants (Kant et al 2004;Oliveira et al 2016;Oliveira et al 2017). For initial infestation or re-infestation with T. urticae, 10 female T. urticae were introduced to the abaxial surface of a leaf within a barrier made with entomological glue Biocontrole® (Indaiatúba, São Paulo, Brazil) to avoid escape or wandering off.…”