Effects of the Timing of Herbivory on Plant Defense Induction and Insect Performance in Ribwort Plantain (Plantago lanceolata L.) Depend on Plant Mycorrhizal Status

Abstract

Plants often are exposed to antagonistic and symbiotic organisms both aboveground and belowground. Interactions between above- and belowground organisms may occur either simultaneously or sequentially, and jointly can determine plant responses to future enemies. However, little is known about time-dependency of such aboveground-belowground interactions. We examined how the timing of a 24 h period of aboveground herbivory by Spodoptera exigua (1–8 d prior to later arriving conspecifics) influenced the response of Plantago lanceolata and the performance of later arriving conspecifics. We also examined whether these induced responses were modulated by the arbuscular mycorrhizal fungus (AMF) Funneliformis mosseae. The amount of leaf area consumed by later arriving herbivores decreased with time after induction by early herbivores. Mycorrhizal infection reduced the relative growth rate (RGR) of later arriving herbivores, associated with a reduction in efficiency of conversion of ingested food rather than a reduction in relative consumption rates. In non-mycorrhizal plants, leaf concentrations of the defense compound catalpol showed a linear two-fold increase during the eight days following early herbivory. By contrast, mycorrhizal plants already had elevated levels of leaf catalpol prior to their exposure to early herbivory and did not show any further increase following herbivory. These results indicate that AMF resulted in a systemic induction, rather than priming of these defenses. AMF infection significantly reduced shoot biomass of Plantago lanceolata. We conclude that plant responses to future herbivores are not only influenced by exposure to prior aboveground and belowground organisms, but also by when these prior organisms arrive and interact.

Response of Brassica oleracea to temporal variation in attack by two herbivores affects preference and performance of a third herbivore

“…b). This contrasts to a study on Plantago lanceolata in which a longer time between the arrival of conspecifics caused a decrease in the consumption of leaf area by the second‐arriving Spodoptera exigua caterpillars (Wang et al ., ). However, in another study with S. exigua caterpillars attacking tomato plants twice, caterpillar bioassays after a short or longer period following the two attacks showed that a short arrival time after repeated attack yielded a lower plant resistance response than that after the first attack only (Underwood, ).…”

“…As plant responses to herbivores from different feeding guilds are often asymmetric (Kaplan & Denno, 2007), and we observed that the timing of herbivore arrival affects the performance of a subsequent herbivore (Wang et al, 2015), we expected an interaction between the effects of order and timing of inducer arrival on M. brassicae performance. Feeding by the aphid B. brassicae was expected to dampen the effect of P. xylostella induction, because of antagonistic effects of plant physiological responses of aphids to responses induced by caterpillars (Thaler et al, 2002;Voelckel & Baldwin, 2004;Stam et al, 2014).…”

“…This indicates that plant responses that mediate indirect interactions between multiple herbivores do not directly translate with the same magnitude and direction into responses of another herbivore (Utsumi et al, 2010;Ohgushi, 2016). The response of a herbivore to an induced-plant phenotype depends on many aspects of plant-herbivore interactions, such as the species and feeding guild of inducing and responding herbivore (Bidart-Bouzat & Kliebenstein, 2011;Ali & Agrawal, 2014), the type of plant responses involved (Howe & Jander, 2008;Rodriguez-Saona et al, 2010), and modifications of the plant response due to timing and order of arrival of multiple herbivores (Erb et al, 2011;Karban, 2011;Stam et al, 2014;Wang et al, 2015). Therefore, going from two to multiple herbivores in more natural situations of plant-herbivore communities cannot be interpreted by simple extrapolations (Stam et al, 2014;Poelman, 2015).…”

Mycorrhizae Alter Toxin Sequestration and Performance of Two Specialist Herbivores

“…We did not find correlations between foliar nutrient content and sequestration, potentially due to low sample sizes, but variation in soil N and P availability has been found to alter the efficiency of monarch caterpillar sequestration and the composition of cardenolides that monarch caterpillars sequester . Alternatively, interactions between AMF and caterpillar feeding may have altered the composition of foliar cardenolides Agrawal et al, 2014;Wang et al, 2015), resulting in the observed, AMF-mediated differences in caterpillar sequestration. However, milkweed responses to monarch caterpillar feeding can take up to 5 days to occur (Agrawal et al, 2014) and monarch caterpillars fed on our experimental plants for only 6 days.…”

Untargeted metabolic profiling reveals geography as the strongest predictor of metabolic phenotypes of a cosmopolitan weed

“…A wide array of environmental factors have been shown to influence the types or concentrations of specialized metabolites produced by the model Plantago species, including plant/leaf age and phenology (Barton, 2008;Hanley et al, 2013;Pankoke et al, 2013;Sutter & Muller, 2011), herbivore and pest damage (Bowers, Collinge, Gamble, & Schmitt, 1992;Sutter & Muller, 2011), genotype (Adler, Schmitt, & Bowers, 1995;Al-Mamun, Abe, Kofujita, Tamura, & Sano, 2008;Barton, 2007;Marak, Biere, & van Damme, 2002;Zubair et al, 2012), habitat type (Adler et al, 1995), plant competition (Barton & Bowers, 2006;Pankoke, Hopfner, Matuszak, Beyschlag, & Muller, 2015;Waschke, Hancock, Hilker, Obermaier, & Meiners, 2015), associations with microorganisms including arbuscular mycorrhizal fungi (Bennett & Bever, 2007;Bennett, Macrae, Moore, Caul, & Johnson, 2013;Fontana, Reichelt, Hempel, Gershenzon, & Unsicker, 2009;Schweiger et al, 2014;Wang, Bezemer, van der Putten, & Biere, 2015), nutrient levels (Darrow & Bowers, 1999;Jarzomski, Stamp, & Bowers, 2000;Miehe-Steier, Roscher, Reichelt, Gershenzon, & Unsicker, 2015;Pankoke et al, 2015), UV levels (McCloud & Berenbaum, 1999;Murai et al, 2009), and variation in geography and climate (Mølgaard, 1986;Murai et al, 2009;Pellissier, Roger, Bilat, & Rasmann, 2014;Reudler & Elzinga, 2015).…”