Plant defences limit herbivore population growth by changing predator–prey interactions

Kersch-Becker, Mônica F.; Kessler, André; Thaler, Jennifer S.

doi:10.1098/rspb.2017.1120

Cited by 22 publications

(31 citation statements)

References 41 publications

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“…On jasmonate-insensitive plants, for instance, aphids induce higher amounts of methyl salicylate, a SA-dependent secondary compound, compared to jasmonate-overexpressor plants (Kersch-Becker et al, 2017). Our findings differed from Kersch-Becker et al (2017), and we attributed this variation to differences in field and greenhouse experimental set-up. On wild type plants, aphid population also showed negative density-dependent growth, which might be a response to both constitutive and induced resistance expressed by these plants.…”

Section: Discussioncontrasting

confidence: 67%

“…While evidence for a trade-off between induced and constitutive resistance is still evasive, it is often suggested that the level of induced resistance expressed by plants with high levels of constitutive resistance should be lower than those expressed by plants with low levels of constitutive resistance (Karban & Baldwin, 1997). In our study, jasmonate-overexpressing plants show high JA-dependent constitutive levels of resistance (Figure 3a, McGurl et al, 1994) and were unable to activate the SA pathway ( Figure 3b, Kersch-Becker et al, 2017). We provide empirical evidence for this hypothesis by showing that high constitutive levels of resistance caused low population growth regardless of the initial density of aphids and thus did not cause negative density-dependent population growth.…”

Section: Discussionmentioning

confidence: 46%

“…We took an experimental approach by conducting herbivore density manipulations, using a model plant in which resistance has been genetically altered to elevate or suppress jasmonate plant defences. Prosystemin;McGurl, Orozco-Cardenas, Pearce, & Ryan, 1994), and therefore has constitutively high levels of JA-dependent defences conferring high resistance to aphids (Kersch-Becker et al, 2017;Kersch-Becker & Thaler, 2015). We used three genetically modified tomato lines that vary in the expression of JA pathway: (a) jasmonate-insensitive-a mutant tomato line (cv.…”

Section: Introductionmentioning

confidence: 99%

“…We hypothesized weak density-dependent population growth on jasmonate-overexpressing plants because these plants show high constitutive levels of resistance, but low inducibility. These plants induce high amounts of methyl salicylate (Kersch-Becker et al, 2017), a compound expressed in response to SA production. On the wild type, inducible plants, we expect defences to increase with increasing aphid density, promoting density-dependent population growth.…”

Section: Introductionmentioning

confidence: 99%

“…We used three genetically modified tomato lines that vary in the expression of JA pathway: (a) jasmonate-insensitive-a mutant tomato line (cv. Jai-1; Li, Li, Lee, & Howe, 2002) 1994), and therefore has constitutively high levels of JA-dependent defences conferring high resistance to aphids (Kersch-Becker et al, 2017;Kersch-Becker & Thaler, 2015). We evaluated the effects of jasmonate-mediated defences on the performance of the potato aphid, Macrosiphum euphorbiae, in terms of fecundity, developmental time and amount of feeding (honeydew production).…”

Section: Introductionmentioning

confidence: 99%

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Constitutive and herbivore‐induced plant defences regulate herbivore population processes

Kersch-Becker

Thaler

2019

Journal of Animal Ecology

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Herbivore‐induced plant defences regulated by the phytohormones jasmonic acid (JA) and salicylic acid (SA) are predicted to influence herbivore population dynamics, in part because they can operate in a density‐dependent manner. While there is ample evidence that herbivore‐induced plant responses affect individual performance and growth of herbivores, whether they scale‐up to regulate herbivore population dynamics is still unclear. We evaluated the consequences of variation in plant defences and herbivore density on herbivore development, reproduction and density‐dependent population growth. We investigated potential mechanisms affecting the strength of herbivore density‐dependent processes by manipulating jasmonate expression, quantifying plant defensive traits (phytohormones JA and SA and serine proteinase inhibitors) and adding aphids (Macrosiphum euphorbiae) at different densities to plants to simulate different initial population density and herbivore load. We manipulated jasmonate defences by using genetically modified lines of tomato plants (Solanum lycopersicum) with elevated or suppressed jasmonate‐dependent defences. Jasmonate‐insensitive plants cannot induce the defences regulated by the JA pathway, while jasmonate‐overexpressing plants constitutively express jasmonate‐dependent defences. We found that jasmonate defences provided resistance against aphids and influenced density‐dependent processes. Jasmonate‐overexpressing plants reduced aphid reproduction, prolonged developmental time, dampened aphid populations across all aphid densities and caused density‐independent aphid population growth. Jasmonate‐overexpressing plants showed high JA‐dependent constitutive levels of resistance and were unable to activate the SA pathway in response to aphid feeding. In contrast, jasmonate‐insensitive plants increased aphid reproduction, shortened developmental time, reduced population growth only at high initial densities and promoted strong negative density‐dependent population growth. Aphid feeding on jasmonate‐insensitive plants did not induce jasmonate‐dependent defences, but induced the SA pathway in a density‐dependent manner, which resulted in negative density‐dependent aphid population growth. Aphid feeding on jasmonate‐insensitive and jasmonate‐overexpressing plants differentially activated the salicylate pathway, revealing a negative crosstalk between the defensive phytohormones JA and SA. By muting or enhancing jasmonate‐mediated responses and quantifying SA phytohormone induction, we demonstrated that plant defences are a key factor driving not only the performance, but also the density dependence processes and population growth of herbivores.

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Section: Discussioncontrasting

confidence: 67%

Section: Discussionmentioning

confidence: 46%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Constitutive and herbivore‐induced plant defences regulate herbivore population processes

Kersch-Becker

Thaler

2019

Journal of Animal Ecology

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Chemical diversity rather than cultivar diversity predicts natural enemy control of herbivore pests

Hauri

Glassmire

Wetzel

2021

Ecological Applications

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Cultivar mixtures have been studied for decades as a means for pest suppression. The literature, however, shows a large variability in outcomes, suggesting that we are unable to create mixtures that consistently suppress insect pests and attract natural enemies. A key gap in our understanding of how cultivar mixtures influence pest control is that few studies have examined the plant traits or mechanisms by which cultivar diversity affects pests and their interactions with natural enemies. The diversity of plant chemistry in a cultivar mixture is one trait dimension that is likely influential for insect ecology because chemical traits alter how predators and herbivores forage and interact. To understand how plant chemical diversity influences herbivores and their interactions with predators, we fully crossed predator presence or absence with monocultures, bicultures, and tricultures of three chemotypes of tomato that differed in odor diversity (terpenes) or surface chemistry (acyl sugars) in a caged field experiment. We found that the direct effects of plant chemotype diversity on herbivore performance were strongest in bicultures and depended on herbivore sex, and these effects typically acted through growth rather than survival. The effects of chemotype diversity on top-down pest suppression by natural enemies differed between classes of chemical diversity. Odor diversity (terpenes) interfered with the ability of predators to hunt effectively, whereas diversity in surface chemistry (acyl sugars) did not. Our results suggest that phytochemical diversity can contribute to pest suppression in agroecosystems, but that implementing it will require engineering cultivar mixtures using trait-based approaches that account for the biology of the pests and natural enemies in the system.

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Host‐plant sex and phenology of Buddleja cordata Kunth interact to influence arthropod communities

González‐Ramírez,

López‐Gómez,

Cano‐Santana

et al. 2024

Ecology and Evolution

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Intraspecific variation in plants is expected to have profound impacts on the arthropod communities associated with them. Because sexual dimorphism in plants is expected to provide consistent variation among individuals of the same species, researchers have often studied the effect it has on associated arthropods. Nevertheless, most studies have focused on the effect of sexual dimorphism in a single or a few herbivores, thus overlooking the potential effects on the whole arthropod community. Our main objective was to evaluate effects of Buddleja cordata's plant‐sex on its associated arthropod community. We surveyed 13 pairs of male and female plants every 2 months during a year (June 2010 to April 2011). Every sampling date, we measured plant traits (water content and leaf thickness), herbivory, and the arthropod community. We did not find differences in herbivory between plant sex or through time. However, we found differences in water content through time, with leaf water‐content matching the environmental seasonality. For arthropod richness, we found 68 morphospecies associated with female and 72 with male plants, from which 53 were shared by both sexes. We did not observe differences in morphospecies richness; however, we found sex‐associated differences in the diversity of all species and differences on the diversity of the most abundant species with an interesting temporal component. During peak flowering season, male plants showed higher values on both parameters, but during the peak fructification season female plants showed the higher values on both diversity parameters. Our research exemplifies the interaction between plant‐phenology and plant‐sex as drivers of arthropod communities' diversity, even when plant sexual‐dimorphism is inconspicuous, and highlighting the importance of accounting for seasonal variation. We stress the need of conducting more studies that test this time‐dependent framework in other dioecious systems, as it has the potential to reconcile previous contrasting observations reported in the literature.

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Plant defences limit herbivore population growth by changing predator–prey interactions

Cited by 22 publications

References 41 publications

Constitutive and herbivore‐induced plant defences regulate herbivore population processes

Constitutive and herbivore‐induced plant defences regulate herbivore population processes

Chemical diversity rather than cultivar diversity predicts natural enemy control of herbivore pests

Host‐plant sex and phenology of Buddleja cordata Kunth interact to influence arthropod communities

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