Sequential above- and belowground herbivory modifies plant responses depending on herbivore identity

Abstract

BackgroundHerbivore-induced changes in plant traits can cause indirect interactions between spatially and/or temporally separated herbivores that share the same host plant. Feeding modes of the herbivores is one of the major factors that influence the outcome of such interactions. Here, we tested whether the effects of transient aboveground herbivory for seven days by herbivores of different feeding guilds on tomato plants (Solanum lycopersicum) alters their interaction with spatially as well as temporally separated belowground herbivores.Results The transient aboveground herbivory by both chewing caterpillars (Spodoptera exigua) and sucking aphids (Myzus persicae) had significant impacts on plant traits such as plant growth, resource allocation and phytohormone contents. While the changes in plant traits did not affect the overall performance of the root-knot nematodes (Meloidogyne incognita) in terms of total number of galls, we found that the consequences of aboveground herbivory for the plants can be altered by the subsequent nematode herbivory. For example, plants that had hosted aphids showed compensatory growth when they were later challenged by nematodes, which was not apparent in plants that had hosted only aphids. In contrast, plants that had been fed by S. exigua larvae did not show such compensatory growth even when challenged by nematodes.ConclusionThe results suggest that the earlier aboveground herbivory can modify plant responses to subsequent herbivores, and such modifications may depend upon identity and/or feeding modes of the aboveground herbivores.Electronic supplementary materialThe online version of this article (doi:10.1186/s12898-017-0115-2) contains supplementary material, which is available to authorized users.

Aboveground herbivory induced jasmonates disproportionately reduce plant reproductive potential by facilitating root nematode infestation

“…According to our preliminary experiments, this nematode density results in 38.8 ± 7.08 galls/plant within 5 weeks, which corresponds to an intermediate level of infestation and does not affect plant growth drastically (Bridge & Page, ). Similar nematode densities are frequently used in other studies (Arce et al, ; Barker & Weeks, ; Hanounik & Osborne, ; Kafle et al, ).…”

“…Interactions between leaf and root feeders in particular have received much attention (Arce et al, ; Coppola, Soler, Rao, & Corrado, ; Erb et al, ; Erb, Robert, Hibbard, & Turlings, ; Huang et al, ; Kaplan, Sardanelli, & Denno, ; Robert et al, ; Soler et al, ). Several studies demonstrate, for instance, that leaf herbivore attack increases the abundance and performance of root parasitic nematodes (Alston, Schmitt, Bradley Jr, & Coble, ; Kafle, Hänel, Lortzing, Steppuhn, & Wurst, ; Kaplan et al, ; Kaplan et al, ; Russin et al, ; Russin, McGawley, & Boethel, ). Despite the increasing number of studies showing effects of leaf feeders on root herbivores and parasites, the systemic shoot–root signals mediating these effects are unclear.…”

Cumulative herbivory outpaces compensation for early floral damage on a monocarpic perennial thistle

“…Effective compensation depends upon multiple interactions; response capacity, and the range of damage at which tolerance works, varies with ecological context. Plant resource condition, herbivore dynamics, phenological overlap with shared hosts and pollinators or competing predators, and timing of damage can influence the degree of plant tolerance (Kolb et al 2007;Wise and Abrahamson 2007;von Euler et al 2014;Lehndal and Ågren 2015;Krimmel and Pearse 2016;Stieha et al 2016;Kafle et al 2017). Co-occurring stressors may further interact with cumulative herbivory pressure to inhibit successful tolerance (Lay et al 2011;Nguyen et al 2016).…”

Differences in Hormonal Signaling Triggered by Two Root-Feeding Nematode Species Result in Contrasting Effects on Aphid Population Growth

“…Direct measurements of the hormone concentrations in S. lycopersicum showed a lower endogenous SA, but higher JA concentrations in the leaves at 14 d.a.i. with M. incognita (Kafle et al, 2017). Due to a paucity of studies, it is currently not possible to identify general patterns.…”

“…Both ISR and priming may cause interactions between aboveground and belowground herbivores feeding on the same plant (Erb et al, 2011;Mathur et al, 2011;van Dam and Heil, 2011;van Geem et al, 2016). Consequently, aboveground herbivores may be confronted with plant defense responses activated by root herbivores, and vice versa (Kaplan and Denno, 2007;Wurst et al, 2008;Kafle et al, 2017;Papadopoulou and van Dam, 2017). The outcome of aboveground-belowground interactions may depend on the herbivore species that is feeding on either organ, as well as on the time and sequence of infestation (Erb et al, 2011;van Dam and Heil, 2011).…”