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