Induced Defenses in Herbivores and Plants Differentially Modulate a Trophic Cascade

Stap, Irene van der; Vos, Matthijs; Verschoor, Antonie M.; Helmsing, Nico R.; Mooij, Wolf M.

doi:10.1890/07-1731.1

Cited by 48 publications

(47 citation statements)

References 44 publications

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“…In addition to reducing prey vulnerability to predators, such inducible defenses can strongly influence community dynamics through trait-mediated cascades (Schmitz et al 1997, 2004, 2003, Van der Stap et al 2007 or habitat modification (Raimondi et al 2000).…”

Section: Introductionmentioning

confidence: 99%

Top‐down effects on antagonistic inducible defense and offense

Kishida

Trussell

Nishimura

2009

Ecology

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Abstract. Antagonistic phenotypic plasticity may strongly influence trait evolution in tightly interacting predator-prey pairs as well as the role that trait plasticity plays in community dynamics. Most work on trait plasticity has focused on single predator-prey pairs, but prey must often contend with multiple predators in natural environments. Hence, a better understanding of the evolutionary and ecological significance of phenotypic plasticity requires experiments that examine how multiple predators shape prey trait plasticity.Here, using a simple food chain consisting of a top predator (dragonfly larvae, Aeshna nigroflava), an intermediate predator (salamander larvae, Hynobius retardatus), and frog (Rana pirica) tadpoles as prey, we show that the presence of dragonfly risk cues substantially modifies the intensity of antagonistic morphological plasticity in both amphibians. In the absence of dragonflies, tadpoles produced bulgier bodies in response to salamanders, and salamanders responded to this defense by enlarging their gape size. However, in the presence of dragonfly risk cues, the expression of both antagonistic traits was significantly reduced because tadpoles and salamanders produced phenotypes that are more effective against dragonfly predators. Thus, the reduced antagonism likely emerged, in part, because the benefits of antagonistic trait expression were outweighed by the potential cost of increased vulnerability to dragonfly predation. In addition, our results suggest that when all three species were present, salamander activity levels, which influence the amount of signals required to induce antagonistic traits, were more strongly affected by dragonfly risk cues than were tadpole activity levels. This species-specific difference in activity levels was likely responsible for the reduced tadpole mortality caused by salamanders in the presence vs. absence of dragonfly risk cues. Hence, dragonflies had a positive trait-mediated indirect effect on tadpoles by modifying both the morphological and behavioral traits of salamanders.

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Section: Introductionmentioning

confidence: 99%

Top‐down effects on antagonistic inducible defense and offense

Kishida

Trussell

Nishimura

2009

Ecology

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“…The recognition that functional traits of species can drive the indirect positive effect of carnivores on plant biomass [trophic cascades broadly defined (4,5)] provides important insight into the causes of variation in these dynamics (1,6). An emerging understanding of the functional traits mediating trophic cascade strength includes traits of herbivores that facilitate predator avoidance (7)(8)(9)(10), or provide constitutive (11,12) or induced resistance to predation (13). These examples identify antipredator traits of herbivores as an important mediator of top-down effects on plants within individual tritrophic food chains.…”

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confidence: 99%

Herbivore diet breadth mediates the cascading effects of carnivores in food webs

Singer

Lichter‐Marck

Farkas

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

113

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Predicting the impact of carnivores on plants has challenged community and food web ecologists for decades. At the same time, the role of predators in the evolution of herbivore dietary specialization has been an unresolved issue in evolutionary ecology. Here, we integrate these perspectives by testing the role of herbivore diet breadth as a predictor of top-down effects of avian predators on herbivores and plants in a forest food web. Using experimental bird exclosures to study a complex community of trees, caterpillars, and birds, we found a robust positive association between caterpillar diet breadth (phylodiversity of host plants used) and the strength of bird predation across 41 caterpillar and eight tree species. Dietary specialization was associated with increased enemy-free space for both camouflaged (n = 33) and warningly signaled (n = 8) caterpillar species. Furthermore, dietary specialization was associated with increased crypsis (camouflaged species only) and more stereotyped resting poses (camouflaged and warningly signaled species), but was unrelated to caterpillar body size. These dynamics in turn cascaded down to plants: a metaanalysis (n = 15 tree species) showed the beneficial effect of birds on trees (i.e., reduced leaf damage) decreased with the proportion of dietary specialist taxa composing a tree species' herbivore fauna. We conclude that herbivore diet breadth is a key functional trait underlying the trophic effects of carnivores on both herbivores and plants.ecological specialization | host specificity | plant-herbivore interactions | tritrophic interactions | trophic cascade P redicting the strength of trophic interactions is a major goal in ecology. Because most natural ecosystems contain numerous coexisting species at each trophic level, achieving this goal necessarily involves the integration of theory in evolutionary, community, and food web ecology. In this context, evolutionary ecology explains how traits of organisms adapt them to a fundamental trade-off between resource acquisition and mortality risk from natural enemies (1, 2); community ecology theory links the many patterns and consequences of species interactions to the diversity of traits of those species (2); and food web ecology subsumes this diversity into patterns of trophic structure and dynamics, such as a trophic cascade (3). The recognition that functional traits of species can drive the indirect positive effect of carnivores on plant biomass [trophic cascades broadly defined (4, 5)] provides important insight into the causes of variation in these dynamics (1,6). An emerging understanding of the functional traits mediating trophic cascade strength includes traits of herbivores that facilitate predator avoidance (7-10), or provide constitutive (11, 12) or induced resistance to predation (13). These examples identify antipredator traits of herbivores as an important mediator of top-down effects on plants within individual tritrophic food chains. However, the role of antipredator (or other) traits of herbivores is curr...

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“…Such behavioral shifts are clearly important but more attention to the ecological importance of morphological plasticity to the demography of predators and prey is needed. Few studies have explored how morphological plasticity affects the population processes of predators and their prey as well as the strength of trophic cascades (Verschoor et al 2004;Van der Stap et al 2007;Kishida et al 2009b). Using ideal experimental systems, Verschoor and his colleague elegantly showed stabilizing effects of inducible defense on population dynamics, in which inducible morphological defense of algae stabilize the dynamics of bi-and tritrophic planktonic food chains in case of eutrophic environment (Verschoor et al 2004).…”

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confidence: 99%

Evolutionary ecology of inducible morphological plasticity in predator–prey interaction: toward the practical links with population ecology

et al. 2009

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The outcome of species interactions is often strongly influenced by variation in the functional traits of the individuals participating. A rather large body of work demonstrates that inducible morphological plasticity in predators and prey can both influence and be influenced by species interaction strength with important consequences for individual fitness. Much of the past research in this area has focused on the ecological and evolutionary significance of trait plasticity by studying single predatorprey pairs and testing the performance of individuals having induced and non-induced phenotypes. This research has thus been critical in improving our understanding of the adaptive value of trait plasticity and its widespread occurrence across species and community types. More recently, researchers have expanded this foundation by examining how the complexity of organismal design and community-level properties can shape plasticity in functional traits. In addition, researchers have begun to merge evolutionary and ecological perspectives by linking trait plasticity to community dynamics, with particular attention on trait-mediated indirect interactions. Here, we review recent studies on inducible morphological plasticity in predators and their prey with an emphasis on internal and external constraints and how the nature of predatorprey interactions influences the expression of inducible phenotypes. In particular, we focus on multiple-trait plasticity, flexibility and modification of inducible plasticity, and reciprocal plasticity between predator and prey. Based on our arguments on these issues, we propose future research directions that should better integrate evolutionary and population studies and thus improve our understanding of the role of phenotypic plasticity in predator-prey population and community dynamics.3 Keywords

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Induced Defenses in Herbivores and Plants Differentially Modulate a Trophic Cascade

Cited by 48 publications

References 44 publications

Top‐down effects on antagonistic inducible defense and offense

Top‐down effects on antagonistic inducible defense and offense

Herbivore diet breadth mediates the cascading effects of carnivores in food webs

Evolutionary ecology of inducible morphological plasticity in predator–prey interaction: toward the practical links with population ecology

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