Pathways for plant‐mediated negative feedback to insect herbivores: accounting for non‐linear effects of larval density on plant quality and quantity

McNutt, David W.; Samuelson, Kathryn; Underwood, Nora

doi:10.1111/eea.12515

Cited by 7 publications

(7 citation statements)

References 57 publications

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“…While our study lacks the data to address these predictions, nonlinearities in recruitment curves seem particularly likely, considering that the relationship between larval density and herbivore performance has been shown to be nonlinear (Morris , Underwood ; but see McNutt et al. ).…”

Section: Discussionmentioning

confidence: 98%

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Variation in plant‐mediated intra‐ and interspecific interactions among insect herbivores: effects of host genotype

McNutt

Underwood

2016

Ecosphere

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Abstract. Many studies show that indirect interactions between insect herbivores via shared host plants are common and often mediated by plant-induced responses to damage. However, we lack some types of data that will be needed to model how plant-mediated interactions on individual plants contribute to the population dynamics of interacting herbivores. Specifically, there are few simultaneous characterizations of both the intra-and interspecific effects that are mediated by the host plant, as well as host plant constitutive resistance. Additionally, as herbivores are likely to move among plants that differ in quality, we must consider how this set of intra-and interspecific effects differs among plant genotypes-that is, how plantmediated effects genetically vary or covary. We examined how the set of intra-and interspecific indirect effects involving the insect folivores Leptinotarsa juncta and Manduca sexta varies across different genotypes of a shared host plant, Solanum carolinense. We damaged 12 plant genotypes using both herbivore species, then measured effects on the growth of both con-and heterospecifics, as well as constitutive resistance to each herbivore. We then tested for genetic variation and covariation in plant-mediated effects and constitutive resistance among plant genotypes. We found that on average, there were significant negative intraspecific plant-mediated effects on the growth rate of both herbivores, as well as asymmetric negative interspecific effects of M. sexta on L. juncta. Both intra-and interspecific effects varied across plant genotypes. For example, the interspecific effect of M. sexta on L. juncta ranged from significantly negative to significantly positive. Additionally, there were strong correlations among the individual effects mediated by S. carolinense, particularly between constitutive resistance and both intra-and interspecific effects. We find that these genetic correlations might limit the types and strength of interactions that take place across multiple genotypes of the same plant species. Our results suggest that future models of plant-mediated interactions between herbivores should account for patterns of genetic variation and covariation when scaling from individual interactions to population-level processes.

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Section: Discussionmentioning

confidence: 98%

“…; McNutt et al. ) likely to feed or oviposit on damaged plants, affecting the likelihood of intra‐ or interspecific interactions. Herbivores can also exhibit different movement rates, susceptibility to defenses (van Dam et al.…”

Section: Discussionmentioning

confidence: 99%

Variation in plant‐mediated intra‐ and interspecific interactions among insect herbivores: effects of host genotype

McNutt

Underwood

2016

Ecosphere

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“…Similar to these results, elm leaf beetle larvae feeding upon whole twigs of oviposited elm trees gain more weight than conspecifics on non-oviposited trees and because more larvae die on previously oviposited plants these larvae are also feeding at reduced densities [10]. A previous study showed that growth of S. exigua on another Solanum species (tomato) is density-dependent and attributed this to the result of intraspecific competition and density-dependent changes in plant quality [31] as, for example, differential activation of PI activity [32].…”

Section: Discussionmentioning

confidence: 99%

Oviposition by Spodoptera exigua on Solanum dulcamara Alters the Plant’s Response to Herbivory and Impairs Larval Performance

Geuß

Lortzing

Schwachtje

et al. 2018

IJMS

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Plant resistance traits against insect herbivores are extremely plastic. Plants respond not only to the herbivory itself, but also to oviposition by herbivorous insects. How prior oviposition affects plant responses to larval herbivory is largely unknown. Combining bioassays and defense protein activity assays with microarray analyses and metabolite profiling, we investigated the impact of preceding oviposition on the interaction of Solanum dulcamara with the generalist lepidopteran herbivore Spodoptera exigua at the levels of the plant’s resistance, transcriptome and metabolome. We found that oviposition increased plant resistance to the subsequent feeding larvae. While constitutive and feeding-induced levels of defensive protease inhibitor activity remained unaffected, pre-exposure to eggs altered S. dulcamara’s transcriptional and metabolic response to larval feeding in leaves local and systemic to oviposition. In particular, genes involved in phenylpropanoid metabolism were more strongly expressed in previously oviposited plants, which was reflected by reciprocal changes of primary metabolites upstream and within these pathways. Our data highlight that plants integrate signals from non-threatening life stages of their natural enemies to optimize their response when they become actually attacked. The observed transcriptional and metabolic reshaping of S. dulcamara’s response to S. exigua herbivory suggests a role of phenylpropanoids in oviposition-primed plant resistance.

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“…By altering plant productivity (van der Graaf et al 2005) and/or food quality (Reynolds et al 2012), herbivores can influence the carrying capacity of their environment, resulting in feedback regulation of their population. However, the effects of multiple feedbacks are rarely considered in combination (McNutt et al 2017), despite the fact that they can have nonadditive effects on herbivore dynamics (Abbott et al 2008). …”

Section: Introductionmentioning

confidence: 99%

Unpacking multi-trophic herbivore-grass-endophyte interactions: feedbacks across different scales in vegetation responses to Soay sheep herbivory

Vicari

Puentes

Granath

et al. 2018

Sci Nat

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Grazing can induce changes in both plant productivity and nutritional quality, which may subsequently influence herbivore carrying capacity. While research on Soay sheep (Ovis aries L.) dynamics on Hirta Island in the St. Kilda archipelago has elucidated the complexity of population drivers, including parasites, the role of herbivore-generated feedbacks as an intrinsic regulating factor remains unclear. The sheep lack large predators and every 3–9 years undergo population crashes (overcompensatory mortality). We investigated the effects of grazing on (1) sward productivity and (2) quality (toxicity) of the primary forage species, red fescue (Festuca rubra L.), which is highly infected by an alkaloid-synthesizing fungal endophyte. Grazing had a negative impact on both forage quantity and quality. At higher sheep densities, impacts on sward growth were magnified, resulting in a nonlinear relationship with plant productivity. Simultaneously, endophyte hyphal load (and by inference, toxicity) peaked close to the time of a crash. A greenhouse experiment showed that alkaloid concentration in F. rubra increased in response to artificial defoliation. We conclude that at high sheep densities, grazing-mediated reductions in productivity, together with sustained alkaloid production, are likely to influence sheep dynamics. Future research should consider the interactive effects of forage toxicity, quantity, and nutritional content.

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Pathways for plant‐mediated negative feedback to insect herbivores: accounting for non‐linear effects of larval density on plant quality and quantity

Cited by 7 publications

References 57 publications

Variation in plant‐mediated intra‐ and interspecific interactions among insect herbivores: effects of host genotype

Variation in plant‐mediated intra‐ and interspecific interactions among insect herbivores: effects of host genotype

Oviposition by Spodoptera exigua on Solanum dulcamara Alters the Plant’s Response to Herbivory and Impairs Larval Performance

Unpacking multi-trophic herbivore-grass-endophyte interactions: feedbacks across different scales in vegetation responses to Soay sheep herbivory

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