Multiannual effects of induced plant defenses: Are defended plants good or bad neighbors?

Abstract

Defenses induced by herbivore feeding or phytohormones such as methyl jasmonate (MeJA) can affect growth, reproduction, and herbivory, not only on the affected individual but also in its neighboring plants. Here, we report multiannual defense, growth, and reproductive responses of MeJA‐treated bilberry (Vaccinium myrtillus) and neighboring ramets. In a boreal forest in western Norway, we treated bilberry ramets with MeJA and water (control) and measured responses over three consecutive years. We observed the treatment effects on variables associated with herbivory, growth, and reproduction in the MeJA‐treated and untreated ramet and neighboring ramets distanced from 10 to 500 cm. MeJA‐treated ramets had fewer grazed leaves and browsed shoots compared to control, with higher effects in 2014 and 2015, respectively. In 2013, growth of control ramets was greater than MeJA‐treated ramets. However, MeJA‐treated ramets had more flowers and berries than control ramets 2 years after the treatment. The level of insect and mammalian herbivory was also lower in untreated neighboring ramets distanced 10–150 cm and, consistent with responses of MeJA‐treated ramets, the stronger effect was also one and 2 years delayed, respectively. The same neighboring ramets had fewer flowers and berries than untreated ramets, indicating a trade‐off between defense and reproduction. Although plant–plant effects were observed across all years, the strength varied by the distance between the MeJA‐treated ramets and its untreated neighbors. We document that induced defense in bilberry reduces both insect and mammalian herbivory, as well as growth, over multiple seasons. The defense responses occurred in a delayed manner with strongest effects one and 2 years after the induction. Additionally, our results indicate defense signaling between MeJA‐treated ramets and untreated neighbors. In summary, this study shows that induced defenses are important ecological strategies not only for the induced individual plant but also for neighboring plants across multiple years in boreal forests.

Molecular and ecological plant defense responses along an elevational gradient in a boreal ecosystem

“…Our results suggest that bilberry plants are more responsive to induced defenses in the suboptimal lower elevation, where the average temperature is higher and the timing of snow melt is earlier, by allocating resources from growth and reproduction to effective herbivory defense for at least one year after induction. This result corroborates with our previous ecological study showing that the induced defense system in low‐land bilberry plants functions in a multiannual manner (Benevenuto et al, ).…”

“…The plant is considered as a key food source for herbivores, pollinators, and fruit eating birds and mammals in northern European boreal forest ecosystems (Hegland et al, ; Hjältén, Danell, & Ericson, ; Jacquemart, ; Selas, ), and has been found to be sensitive to environmental changes. In previous studies, we showed that defenses induced by herbivore feeding or treatment with MeJA reduce herbivory and increase reproduction of the damaged or treated plants (Benevenuto et al, ; Hegland, Seldal, Lilleeng, & Rydgren, ; Seldal, Hegland, Rydgren, Rodriguez‐Saona, & Töpper, ). These studies provide evidence of potential trade‐offs between growth and defense in bilberry plants when coping with herbivore attack.…”

“…Within each block, two ramets (between 10–25 cm height) at least 10 m apart were randomly selected ( N = 120 plants), and each was exposed to one of two different treatments following the same methodology as previous studies (Benevenuto et al, ; Seldal et al, ): (a) 10 mM MeJA application (treated plants), and (b) water/ethanol application (control plants). Several studies have shown that inducible defense responses in plants can be activated by exogenous application of MeJA (Baldwin, ; Benevenuto et al, ; Hegland et al, ; Van Dam & Baldwin, ; Yang, Huihui, Xie, & Rantala, ). To achieve the desired concentration of MeJA, 4.1 M MeJA stock (Bedoukian Research, Danbury, CT) was diluted 1:10 with 95% (v/v) ethanol and rediluted with water to get a final concentration of 10 mM MeJA (Seldal et al, ).…”

“…Induced defense responses can persist from hours and days to years, depending on the plant species, previous herbivory pressure, and life history of the plant (Haukioja, Suomela, & Neuvonen, 1985;Karban & Baldwin, 1997 (Benevenuto et al, 2018).…”

“…We expected MeJA-treated plants to allocate resources from growth and reproduction to defenses at the molecular (i.e., upregulation of defense genes and downregulation of genes related to photosynthesis/nitrogen metabolism) and ecological levels (i.e., reduction of growth, reproduction, and consequently herbivory). As induced defenses are presumed to be energetically costly (Benevenuto et al, 2018;Karban, Yang, & Edwards, 2014;Nabity, Zavala, & DeLucia, 2013;Rodriguez-Saona, Polashock, & Malo, 2013;Seldal et al, 2017) and decline with increasing elevation Pellissier et al, 2016), we predicted that this effect would be most pronounced at the lowest elevation (Prediction I). According to the "optimal defense theory" hypothesis, plants at lower elevations should invest more on defenses due to high risk of herbivory (Rhoades, 1979).…”