Mechanisms, ecological consequences and agricultural implications of tri-trophic interactions

doi:10.1016/S1369-5266(00)00089-3

Current Opinion in Plant Biology

Volume 3, Issue 4, 1 August 2000, Pages 329-335

https://doi.org/10.1016/S1369-5266(00)00089-3 Get rights and content

Abstract

Recent research bridging mechanistic and ecological approaches demonstrates that plant attributes can affect herbivores, natural enemies of herbivores, and their interaction. Such effects may be genetically variable among plants and/or induced in individual plants by herbivore attack, and are mediated by primary plant attributes (i.e. nutritional quality and physical structure) and defense-related products (i.e. secondary chemicals and plant volatiles), and may be modified by human activity (e.g. by the introduction of Bacillus thuringiensis). The study of tri-trophic interactions is important in order to understand natural species interactions and to manipulate these interactions in pest control.

Introduction

For a long time, theoretical predictions have suggested that plants interact in complex ways with herbivores and pathogens that feed on plants, and with natural enemies of herbivores and pathogens [1] (Figure 1). For example, plant traits may be attractive or beneficial to some enemies of herbivores, but the same traits may be poisonous or otherwise detrimental to other enemies of herbivores [2^••]. Studies of tri-trophic interactions aim to identify these interactions, understand their mechanistic basis, and document their consequences. Ultimately, manipulating these interactions may result in better pest control and the reduced use of pesticides. In the past year, rapid advances have been made and four edited books have appeared that cover various aspects of plant–herbivore/pathogen–natural-enemy interactions 3, 4, 5•, 6•. This review focuses on recent empirical advances that have improved our understanding of tri-trophic interactions.

Section snippets

Plant volatiles and natural enemies of herbivores

Plants respond to initial attack by herbivores and pathogens by increasing their levels of defense [7]. For example, volatiles emitted by herbivore-infested plants that are attractive to natural enemies of herbivores are hypothesized to be an evolved response to herbivory. Although the net costs or benefits in plant performance of such induced volatile responses have not been identified, intricate and highly specific interactions between constituents of herbivore saliva and plant responses

Plant morphological traits affect tri-trophic interactions

Aspects of plant morphology may influence the performance of plant parasites, natural enemies of these parasites, and their interactions. Leaf domatia are small hair-tufts or pockets on the abaxial surface of leaves that have been found in nearly 300 plant families and 2000 species [24] (Figure 3). Over a century ago, a Swedish naturalist, Axel Lundströem, proposed that leaf domatia mediated a mutualism between plants (which provide shelter for arthropods) and predatory or fungivorous

Plant effects on omnivores: friend or foe?

Many arthropods are not strictly herbivores or predators, but feed on multiple foods, including leaf tissue, pollen, nectar, and other arthropods [33]. Generalist predators often rely on plants for alternative foods in times of prey scarcity. Big-eyed-bugs survive better and do not disperse when their diet of aphids is supplemented with high-quality plant material [34^•]. The presence of alternative foods increases the retention of predators and may stabilize the interactions between predators

Biotechnology, Bacillus thuringiensis, and beneficial insects

Genetic manipulation of plants can provide potent resistance against pests. Controversy has surrounded the current broad-scale use of transgenic plants with improved resistance to pests in agriculture because of their potential effects on the natural enemies of herbivores, other non-target organisms, gene flow to wild relatives, the rapid evolution of resistance in pests, and human health [39]. The consequences for tri-trophic interactions of expressing Bacillus thuringiensis toxins (Bts) in

Conclusions

In terrestrial environments, strong trophic interactions are modified by the chemistry, morphology, and behavior of each organism involved. Plants recruit natural enemies of herbivores using volatiles. The essential constituents of these interactions ranging from herbivore saliva to plant hormones and regulatory enzymes are now being isolated, and their genes cloned. It is unknown whether plants that are infested with microbial diseases or nematodes attract or facilitate natural enemies of

Acknowledgements

Many thanks to Wilhelm Boland, Mickey Eubanks, Thomas Koch, Richard Mithen, Andrew Norton, and Ken Raffa for sharing unpublished results and discussion. The paper was improved by the comments of Marcel Dicke, Merijn Kant, Rick Karban, Thomas Koch, Jennifer Thaler, and Robin Waugaman. This study was supported by the Section of Population Biology at the University of Amsterdam and the Botany Department at the University of Toronto.

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

• of special interest
•• of outstanding interest

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ReviewMechanisms, ecological consequences and agricultural implications of tri-trophic interactions

Abstract

Introduction

Section snippets

Plant volatiles and natural enemies of herbivores

Plant morphological traits affect tri-trophic interactions

Plant effects on omnivores: friend or foe?

Biotechnology, Bacillus thuringiensis, and beneficial insects

Conclusions

Acknowledgements

References and recommended reading

Biol Control

Biol Control

Biol Control

Biol Control

Interaction between three trophic levels: influence of plants on interactions between insect herbivores and natural enemies

Ann Rev Ecol System

Jasmonate-inducible plant defences cause increased parasitism of herbivores

Nature

The Ecology and Evolution of Inducible Defenses

Induced responses to herbivory and increased plant performance

Science

Induction of plant volatile biosynthesis by jasmonates

Compound effects of induced plant responses on insect herbivores and parasitoids: implications for tritrophic interactions

Ecol Entomol

Jasmonic acid induces the production of gerbera volatiles that attract the biological control agent Phytoseiulus persimilis

Entomologia Experimentalis Applicata

Jasmonic acid and herbivory differentially induce carnivore-attracting plant volatiles in lima bean plants

J Chem Ecol

Channel-forming peptaibols are a novel class of potent elicitors of plant secondary metabolism and tendril coiling

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Differential induction of plant volatile biosynthesis in the lima bean by early and late intermediates of the octadecanoid-signaling pathway

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Spider mite-induced (3S)-(E)-nerolidol synthase activity in cucumber and lima bean. The first dedicated step in acyclic C11-homoterpene biosynthesis

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Induction and systemic release of herbivore-induced plant volatiles mediating in-flight orientation of Aphidius ervi

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Response, of an aphid parasitoid, Aphelinus, asychis to its host, plant, host–plant complex, and to malathion

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Glucosinolate genetics and the attraction of the aphid parasitoid Diaeretiella rapae to Brassica

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Alpha-keto acid elongation and glucosinolate biosynthesis in Arabidopsis thaliana

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Herbivore-induced ethylene suppresses a direct defense but not a putative indirect defense against an adapted herbivore

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Sterilization and canopy modification of a swollen thorn acacia tree by a plant–ant

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Induced responses to herbivory in the Neotropical ant–plant association between Azteca ants and Cecropia trees: response of ants to potential inducing cues

Behav Ecol Sociobiol

Review
Mechanisms, ecological consequences and agricultural implications of tri-trophic interactions