Disarming the paradox of sublethal plant defense against insects: <i>Trirhabda virgata</i> larval development time and leaf tissue loss on <i>Solidago altissima</i>

Wise, Michael J.; Fox, Rebecca J.; Abrahamson, Warren G.

doi:10.1111/j.1570-7458.2006.00434.x

Cited by 11 publications

(9 citation statements)

References 52 publications

(80 reference statements)

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“…Alternatively, although not mutually exclusively, exposure and damage may induce distinct resistance phenotypes that differentially affect T. virgata's performance and behaviour (Bode, Halitschke & Kessler 2013;Uesugi, Poelman & Kessler 2013)for instance, while both resistance phenotypes may repel T. virgata, they may vary in the amount of toxins or antidigestive resistance compounds they contain. Our herbivore movement and performance data generally seem to support this hypothesis and are consistent with a study showing that 'sublethal' plant defences in S. altissima differentially affect T. virgata's feeding and growth rate (Wise, Fox & Abrahamson 2006). The distinct induction patterns for secondary metabolite production discussed above further support this hypothesis.…”

Section: P L a N T C O M M U N I C A T I O N I N C R E A S E S H E R supporting

confidence: 90%

Plant communication in a widespread goldenrod: keeping herbivores on the move

Morrell

Kessler

2016

Functional Ecology

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Summary Plant communication has been documented in over 35 plant species spanning 16 families to date; however, the underlying mechanisms through which it shapes plants' ecological interactions remain less clear. Using a combination of field/laboratory bioassays, headspace volatile and leaf chemical analyses in tall goldenrod (Solidago altissima), we tested the hypothesis that plant‐to‐plant communication affects the performance, feeding and movement behaviour of herbivores by changing plants' chemical phenotypes. We found that plant communication accelerates herbivore movement between host plants while simultaneously reducing herbivory. This suggests that plant communication can limit herbivore loads by keeping herbivores on the move between host plants. We demonstrate that volatile chemicals emitted from herbivore‐attacked plants are sufficient to explain metabolic responses in and ecological consequences for the exposed neighbour plant. Volatile profiles of beetle (Trirhabda virgata)‐damaged and undamaged plants show substantial compositional differences, especially in sesquiterpene emission, indicating that these differences have the potential to provide neighbouring plants with specific information about herbivores in the vicinity. Despite qualitative and phenological differences in plants' metabolic responses to herbivory‐induced volatile organic compounds (VOCs) and feeding herbivores, herbivores nonetheless respond similarly to directly damaged plants and plants exposed to VOCs from damaged neighbours as if they were of equivalently poor quality. This study suggests that by enlarging the spatial scale at which induced resistance affects the distribution of plant chemical phenotypes in plant populations, VOC‐mediated plant communication alters the movement behaviour and performance of herbivores. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.12793/suppinfo is available for this article.

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Section: P L a N T C O M M U N I C A T I O N I N C R E A S E S H E R supporting

confidence: 90%

Plant communication in a widespread goldenrod: keeping herbivores on the move

Morrell

Kessler

2016

Functional Ecology

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“…An interpretation of the observed differences between host plant species requires some caution because plants used in this experiment represent only a small genotypic variation (if any) within a species, and different plant genotypes are likely to differ in mode of resistance against herbivores (Gols et al, 2008). Further demonstrations of SGHM in relation to plant nutritional quality using plant genotypes that vary in primary, as well as secondary metabolites, could provide new insights into the evolution of low plant quality as mechanisms of direct and indirect plant defences (Wise et al, 2006).…”

Section: Plant Nutritional Quality and Plant Resistancementioning

confidence: 99%

“…The slow-growth high-mortality (SGHM) hypothesis posits that prolonged larval stages among insect herbivores will extend exposure to, and mortality from, their natural enemies (Moran & Hamilton, 1980;Clancy & Price, 1987). This hypothesis has critical implications for the paradoxical evolution of sublethal toxins and low digestibility in plants, which merely retards herbivore growth, thus potentially causing greater tissue loss on plants (Feeny, 1976;Price et al, 1980; but see Wise et al, 2006). Although studies of plant-herbivore interactions often assume the action of SGHM, empirical support for the hypothesis has been equivocal (reviewed in Williams, 1999).…”

Section: Introductionmentioning

confidence: 99%

The slow‐growth high‐mortality hypothesis: direct experimental support in a leafmining fly

Uesugi

2015

Ecological Entomology

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1. Based on the slow-growth high-mortality (SGHM) hypothesis, which predicts that prolonged larval development increases mortality from their natural enemies, studies have often assumed that low quality of plants that slows larval development would function as a defence against insect herbivores. However, empirical support for the SGHM hypothesis has been limited, especially in natural and ecologically relevant contexts.2. In a leafminer Amauromyza flavifrons Meigen (Agromyzidae, Diptera), the SGHM hypothesis was tested along with four other hypotheses (e.g. prey size, mine appearance, density-dependent parasitism, and plant quality hypotheses) to control for spurious associations between development time and parasitism that are primarily driven by other larval traits. Two host plant species, Saponaria officinalis and Silene latifolia, were grown under varying nitrogen levels, and leafminers developing on these plants were exposed to, or protected from, a natural assembly of parasitoids across the entire course of larval development.3. On both host plant species, leafminers that survived to an adult stage in the presence of parasitoids had a shorter development time than those in the absence of parasitoids, indicating that parasitoids disproportionately kill leafminers with longer larval development. The results provided concrete evidence for the SGHM hypothesis within the natural ecological context for these interacting species. Moreover, reduced plant quality was associated with higher larval mortality on Sa. officinalis only in the presence of parasitoids, suggesting that low quality could function as indirect plant resistance via SGHM under some tri-trophic interactions.

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“…Lethal effects often occur at higher metal concentrations than sublethal effects, and their defensive value may be greater because they can severely impact herbivore populations (Boyd 2012). However, sublethal effects of elemental sequestration may be evolutionarily effective in some cases (Price et al 1980;Boyd and Moar 1999;Wise et al 2006). Determination of both lethal and sublethal levels of elements may provide information helpful to studies of elemental plant defense.…”

Section: Discussionmentioning

confidence: 99%

Elemental defense of nickel hyperaccumulator seeds against a generalist insect granivore

Mincey

Boyd

2018

Ecological Research

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Hyperaccumulation has been proposed as an elemental defense against herbivores; however, few studies have examined seed defense. This study included two annual Streptanthus species (Brassicaceae) from California serpentine soils: a non‐hyperaccumulator (S. insignis) and three populations (representing Y, P, and U morphs) of a Ni hyperaccumulator (S. polygaloides). Adults of the generalist seed herbivore Tribolium confusum (Coleoptera: Tenebrionidae) were fed either whole or cut seeds, survival was recorded for 7 weeks, and Ni concentrations of both beetles and seeds were determined using ICP‐OES. Survival analysis showed significantly more rapid mortality for beetles consuming S. polygaloides seeds compared to those consuming S. insignis. Mortality of beetles fed whole S. polygaloides seeds was more rapid than those fed cut S. polygaloides seeds. Seeds of the S. polygaloides populations contained approximately 300 µg Ni g−1 whereas S. insignis contained approximately 5 µg Ni g−1. Beetles fed whole S. polygaloides seeds contained more than 2.5‐fold greater Ni concentrations than those fed cut seeds (approximately 60 and 25 µg Ni g−1, respectively), whereas beetles fed either cut or whole S. insignis seeds contained < 0.3 µg Ni g−1. An artificial diet study, using Ni‐amended cornmeal, confirmed that diet Ni concentrations greater than 240 µg Ni g−1 were toxic to T. confusum. We conclude that Ni in S. polygaloides seeds can act as an elemental defense against seed herbivores even at 300 µg Ni g−1, a level below the 1000 µg Ni g−1 hyperaccumulation threshold concentration.

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Disarming the paradox of sublethal plant defense against insects: Trirhabda virgata larval development time and leaf tissue loss on Solidago altissima

Cited by 11 publications

References 52 publications

Plant communication in a widespread goldenrod: keeping herbivores on the move

Plant communication in a widespread goldenrod: keeping herbivores on the move

The slow‐growth high‐mortality hypothesis: direct experimental support in a leafmining fly

Elemental defense of nickel hyperaccumulator seeds against a generalist insect granivore

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