Associational effects of plant ontogeny on damage by a specialist insect herbivore

Cope, Olivia L.; Becker, Zoe; Ode, Paul J.; Paul, Ryan L.; Pearse, Ian S.

doi:10.1007/s00442-020-04702-z

Cited by 7 publications

(5 citation statements)

References 61 publications

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“…Although the influence of age on traits is understudied in saltmarsh plants, these results follow similar trends to those of a seagrass species and terrestrial studies (seagrasses: Sola et al 2020;forests: Chen and Poland 2009;coastal sage scrub: Funk et al 2021;tallgrass prairies: Henn and Damschen 2021). Further, we saw much greater variation in measured plant traits among new stems than in original stems, supporting others' recent findings that plant age strongly determines intraspecific variation in plant traits (Cope et al 2020, Funk et al 2021, Henn and Damschen 2021.…”

Section: Discussionsupporting

confidence: 90%

“…higher chlorophyll), and reduced defensive traits (e.g. higher nitrogen and protein), than older leaves, and these traits tend to be more plastic and have greater variation in younger plants (Chen and Poland 2009, Cope et al 2020, Sola et al 2020, Funk et al 2021). Thus, increased presence of newer leaves and stems, which grow quicker but are more nutritionally dense, may further shape herbivore preference.…”

Section: Introductionmentioning

confidence: 99%

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Resource availability and plant age drive defense against herbivory in salt marshes

Wittyngham¹,

Carey

Johnson³

2023

Oikos

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The resource‐availability hypothesis (RAH) and the intraspecific RAH (RAHintra), posit that resources, (i.e. nutrients) control plant antiherbivore defenses. Both hypotheses predict that in low‐resource environments, plant growth is slow, and constitutive defense is high. In high‐resource environments, however, the RAH predicts that plant growth is fast, and constitutive defense is low, whereas the RAHintra predicts that increased resources attract more herbivores, and this intensified grazing pressure leads to high constitutive defense. Salt marshes are nutrient‐limited ecosystems threatened by eutrophication and chronic herbivory, yet we know little about how these stressors shape saltmarsh plant antiherbivore defenses, which influence trophic interactions and ecosystem resilience. We manipulated resource availability via nutrient addition and herbivory via the marsh periwinkle Littoraria irrorata, on the saltmarsh foundation species Spartina alterniflora, in mesocosms. Because plant age can also influence trait variation, we measured traits in both original and clonally‐grown new stems. Feeding assays then evaluated how treatments and plant age affected subsequent Littoraria consumption of Spartina. Nutrient addition stimulated growth, while decreasing defensive traits (e.g. fiber and silica content), following the RAH. Herbivory enhanced belowground production and increased stem diameter, yet did not induce defensive traits, contrary to our expectations. Herbivory plus nutrients increased Spartina biomass and reduced phenolics, a defensive trait, further supporting the RAH. Regardless of treatment, clonally‐grown new stems had greater variation in measured traits. Despite altered traits, however, treatments and plant age did not affect Littoraria consumption. Our results support the RAH and part of the RAHintra and suggest: 1) nutrient availability is a primary driver of plant trait change and 2) plant age controls the magnitude of trait variation in Spartina. Further, our findings indicate that eutrophic conditions may not always increase top‒down control by herbivores, and in some instances can enhance saltmarsh resilience against sea‐level rise via stimulated Spartina biomass production.

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Section: Discussionsupporting

confidence: 90%

Section: Introductionmentioning

confidence: 99%

Resource availability and plant age drive defense against herbivory in salt marshes

Wittyngham¹,

Carey

Johnson³

2023

Oikos

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“…For example, in plant communities, so-called associational effects are often observed where the herbivory pressure on a focal plant depends on its neighbours and their traits, e.g. their level of defense or ontogenetic stage (Hahn & Orrock, 2016; Cope et al , 2020). These effects are thought to be mediated by herbivore foraging behaviour.…”

Section: Discussionmentioning

confidence: 99%

Nonlinear averaging in 2D: intraspecific variation in two interacting species and consequences for population dynamics

Benthem

Bagawade

Blüml

et al. 2021

Preprint

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Recent empirical and theoretical work shows that intraspecific trait variation (ITV) is prevalent and ecologically important, and should thus be taken into account in ecological models. What is lacking, however, is a comprehensive understanding of the joint effects of ITV in two interacting species (two-dimensional ITV). Here we address this gap for the cases where interspecific individual-by-individual interactions are affected by the trait values of both participants. Using nonlinear averaging in two dimensions, we show for several interaction functions how ITV affects average predation rates or competition coefficients. We develop an intuition for the direction and magnitude of this effect by using a Taylor approximation based on the local curvatures of the interaction function, the trait means, and the trait variances and covariances. We then incorporate the estimated average interaction parameters into simple competition and predator-prey models to derive the expected population-dynamic consequences. We show that two-dimensional ITV can have quantitative effects on abundances, as well as qualitative effects, such as stabilizing or destabilizing coexistence. Our approach can straightforwardly be applied to other interaction functions and dynamical systems and thus provides a valuable tool for understanding the joint effect of trait variation in two interacting species.

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“…Herbivores encounter variability in defences both spatially and temporally throughout development (Cope et al, 2020;Hakes & Cronin, 2011;Herrera, 2009;Hunter, 2016;Quintero et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

“…Herbivores encounter variability in defences both spatially and temporally throughout development (Cope et al., 2020; Hakes & Cronin, 2011; Herrera, 2009; Hunter, 2016; Quintero et al., 2014). Herbivores can experience variation moving across different parts of the same plant or between individual plants (Ruhnke et al., 2009; Wetzel et al., 2016), through ontogenetic variation in plant defence production (Cope et al., 2020; Ochoa‐López et al., 2020; Quintero et al., 2014), or through induction (Karban et al., 1997). From the perspective of an herbivore, variation in plant defensive traits can occur at radically different scales, and the scale at which variation occurs can have profound consequences for herbivores.…”

Section: Introductionmentioning

confidence: 99%

Fine‐scale plant defence variability increases top‐down control of an herbivore

2021

Self Cite

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Herbivore populations are regulated by a combination of plant defences and natural enemies. While plant defence can suppress herbivore populations, these defences can also adversely affect natural enemies, thereby releasing herbivores from top‐down control. Over their life spans, herbivores and their natural enemies may experience substantial variation in plant defence. Recent studies have demonstrated that individual herbivores feeding on diets containing variable concentrations of plant toxins suffer substantially reduced fitness compared to herbivores feeding on a constant toxin concentration, even when both groups of herbivores experience equivalent means. However, the impacts of defence variability on natural enemies and top‐down control of herbivores are unknown. Using artificial diets, we independently manipulated the mean concentration and variation of a plant toxin experienced by individual Trichoplusia ni caterpillars and its parasitoid Copidosoma floridanum. Additionally, by combining the performance of individual caterpillars on different constant diet concentrations of toxin, we were able to estimate the effect of toxin variability between herbivores using nonlinear averaging. Increases in the mean toxin concentration in the diet of parasitized T. ni hosts decreased the fitness of C. floridanum, while variance in individual diets did not impact parasitoid fitness, even though both mean and variance decreased the fitness of T. ni caterpillars. Increased variability in encountered plant defences suppressed individual herbivore fitness with no perceptible cost to top‐down control. At the population level, however, increased variability between individual herbivore diets decreased the success of parasitoids relative to herbivores, thus reducing the strength of top‐down control. Our study highlights the importance of defence variability at different scales in regulating herbivore performance. Variability in plant defence has the potential to reduce herbivore populations through a combination of bottom‐up and top‐down effects, but only at small spatial scales experienced by individual herbivores. A free Plain Language Summary can be found within the Supporting Information of this article.

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Associational effects of plant ontogeny on damage by a specialist insect herbivore

Cited by 7 publications

References 61 publications

Resource availability and plant age drive defense against herbivory in salt marshes

Resource availability and plant age drive defense against herbivory in salt marshes

Nonlinear averaging in 2D: intraspecific variation in two interacting species and consequences for population dynamics

Fine‐scale plant defence variability increases top‐down control of an herbivore

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