The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’

Dicke, Marcel; Baldwin, Ian Thomas

doi:10.1016/j.tplants.2009.12.002

Cited by 963 publications

(846 citation statements)

References 99 publications

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“…glucosinolates) can be constitutively present in plants and be induced to even higher levels in response to herbivore feeding (Wittstock and Halkier 2002). Inducible defenses can directly affect the development or behavior of the attacker (direct defenses), or attract natural enemies of the attacking herbivore, known as indirect defenses (Turlings et al 2002;Schoonhoven et al 2005;Gols et al 2008a;Dicke and Baldwin 2010). Inducible defenses are especially intriguing, as in general, it has been postulated that they reduce production costs and provide a regulatory mechanism that allows plants to trade-off between defense and growth (Herms and Mattson 1992;Karban and Baldwin 1997;Heil and Baldwin 2002).…”

Section: Introductionmentioning

confidence: 99%

Mechanisms and ecological implications of plant‐mediated interactions between belowground and aboveground insect herbivores

Papadopoulou

Dam

2016

Ecological Research

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Plant-mediated interactions between belowground (BG) and aboveground (AG) herbivores have received increasing interest recently. However, the molecular mechanisms underlying ecological consequences of BG-AG interactions are not fully clear yet. Herbivore-induced plant defenses are complex and comprise phytohormonal signaling, gene expression and production of defensive compounds (defined here as response levels), each with their own temporal dynamics. Jointly they shape the response that will be expressed. However, because different induction methods are used in different plant-herbivore systems, and only one or two response levels are measured in each study, our ability to construct a general framework for BG-AG interactions remains limited. Here we aim to link the mechanisms to the ecological consequences of plant-mediated interactions between BG and AG insect herbivores. We first outline the molecular mechanisms of herbivore-induced responses involved in BG-AG interactions. Then we synthesize the literature on BG-AG interactions in two well-studied plant-herbivore systems, Brassica spp. and Zea mays, to identify general patterns and specific differences. Based on this comprehensive review, we conclude that phytohormones can only partially mimic induction by real herbivores. BG herbivory induces resistance to AG herbivores in both systems, but only in maize this involves drought stress responses. This may be due to morphological and physiological differences between monocotyledonous (maize) and dicotyledonous (Brassica) species, and differences in the feeding strategies of the herbivores used. Therefore, we strongly recommend that future studies explicitly account for these basic differences in plant morphology and include additional herbivores while investigating all response levels involved in BG-AG interactions.

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Section: Introductionmentioning

confidence: 99%

Mechanisms and ecological implications of plant‐mediated interactions between belowground and aboveground insect herbivores

Papadopoulou

Dam

2016

Ecological Research

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“…But because HIPVs can be perceived by many other members of the ecological community—from herbivores, pollinators, predators and parasitoids to competing or parasitic plants—it is not clear whether HIPVs increase plant fitness in nature (Dicke and Baldwin, 2010; Kessler and Heil, 2011). The field studies described above have either spanned too short a time to reveal Darwinian fitness benefits, or have not reported fitness data at all (Kessler and Baldwin, 2001; Rasmann et al, 2005; Halitschke et al, 2008; Degenhardt et al, 2009; Allmann and Baldwin, 2010).…”

Section: Introductionmentioning

confidence: 99%

Herbivory-induced volatiles function as defenses increasing fitness of the native plant Nicotiana attenuata in nature

Schuman

Barthel

Baldwin

2012

eLife

167

200

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From an herbivore's first bite, plants release herbivory-induced plant volatiles (HIPVs) which can attract enemies of herbivores. However, other animals and competing plants can intercept HIPVs for their own use, and it remains unclear whether HIPVs serve as an indirect defense by increasing fitness for the emitting plant. In a 2-year field study, HIPV-emitting N. attenuata plants produced twice as many buds and flowers as HIPV-silenced plants, but only when native Geocoris spp. predators reduced herbivore loads (by 50%) on HIPV-emitters. In concert with HIPVs, plants also employ antidigestive trypsin protease inhibitors (TPIs), but TPI-producing plants were not fitter than TPI-silenced plants. TPIs weakened a specialist herbivore's behavioral evasive responses to simulated Geocoris spp. attack, indicating that TPIs function against specialists by enhancing indirect defense.DOI: http://dx.doi.org/10.7554/eLife.00007.001

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“…Therefore, not only intrinsic sap quality, but also foraging kairomones from beetles (Fernandez & Hilker, 2007) or plant volatile induction due to feeding or oviposition (Dicke & Baldwin, 2010) that may change the predator/omnivore behavior need to be considered.…”

Section: Discussionmentioning

confidence: 99%

Consumptive and nonconsumptive effect ratios depend on interaction between plant quality and hunting behavior of omnivorous predators

Stephan

Stenberg

Björkman

2017

Ecology and Evolution

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SummaryPredators not only consume prey but exert nonconsumptive effects in form of scaring, consequently disturbing feeding or reproduction. However, how alternative food sources and hunting mode interactively affect consumptive and nonconsumptive effects with implications for prey fitness have not been addressed, impending functional understanding of such tritrophic interactions. With a herbivorous beetle, two omnivorous predatory bugs (plant sap as alternative food, contrasting hunting modes), and four willow genotypes (contrasting suitability for beetle/omnivore), we investigated direct and indirect effects of plant quality on the beetles key reproductive traits (oviposition rate, clutch size). Using combinations of either or both omnivores on different plant genotypes, we calculated the contribution of consumptive (eggs predated) and nonconsumptive (fewer eggs laid) effect on beetle fitness, including a prey density‐independent measure (c:nc ratio). We found that larger clutches increase egg survival in presence of the omnivore not immediately consuming all eggs. However, rather than lowering mean, the beetles generally responded with a frequency shift toward smaller clutches. However, female beetles decreased mean and changed clutch size frequency with decreasing plant quality, therefore reducing intraspecific exploitative competition among larvae. More importantly, variation in host plant quality (to omnivore) led to nonconsumptive effects between one‐third and twice as strong as the consumptive effects. Increased egg consumption on plants less suitable to the omnivore may therefore be accompanied by less searching and disturbing the beetle, representing a “cost” to the indirect plant defense in the form of a lower nonconsumptive effect. Many predators are omnivores and altering c:nc ratios (with egg retention as the most direct link to prey fitness) via plant quality and hunting behavior should be fundamental to advance ecological theory and applications. Furthermore, exploring modulation of fitness traits by bottom‐up and top‐down effects will help to explain how and why species aggregate.

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The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’

Cited by 963 publications

References 99 publications

Mechanisms and ecological implications of plant‐mediated interactions between belowground and aboveground insect herbivores

Mechanisms and ecological implications of plant‐mediated interactions between belowground and aboveground insect herbivores

Herbivory-induced volatiles function as defenses increasing fitness of the native plant Nicotiana attenuata in nature

Consumptive and nonconsumptive effect ratios depend on interaction between plant quality and hunting behavior of omnivorous predators

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