Plants as green phones

Abstract

Plants can act as vertical communication channels or ‘green phones’ linking soil-dwelling insects and insects in the aboveground ecosystem. When root-feeding insects attack a plant, the direct defense system of the shoot is activated, leading to an accumulation of phytotoxins in the leaves. The protection of the plant shoot elicited by root damage can impair the survival, growth and development of aboveground insect herbivores, thereby creating plant-based functional links between soil-dwelling insects and insects that develop in the aboveground ecosystem. The interactions between spatially separated insects below- and aboveground are not restricted to root and foliar plant-feeding insects, but can be extended to higher trophic levels such as insect parasitoids. Here we discuss some implications of plants acting as communication channels or ‘green phones’ between root and foliar-feeding insects and their parasitoids, focusing on recent findings that plants attacked by root-feeding insects are significantly less attractive for the parasitoids of foliar-feeding insects.

Plants Linking Root and Foliar Insect Interactions: General Introduction

Plants can act as vertical communication channels connecting soil-dwelling organisms and insects that feed on aboveground plant parts.^1–10 When root-feeding insects attack a plant, the direct defense system of the shoot of the plant can be activated, leading to an accumulation of phytotoxins in the leaves (reviewed in refs. ¹⁰ and ¹¹). Aboveground defense responses induced by belowground herbivory have been shown for several plant and insects species,^7,9,12–14 but the ecological implications and evolutionary background of these processes remains largely unknown. The protection of the plant shoot elicited by root damage can markedly impair the survival, growth and development of foliar-feeding insect herbivores, thereby creating plant-based functional links between soil-dwelling insects and biotic components of the aboveground ecosystems. Recent studies show that the interactions between spatially separated insects below- and aboveground are not restricted to plant feeders (root- and foliar-feeding insects), but can extend to higher trophic levels, such as insect parasitoids.^9,15–19 Here we discuss some implications of plants acting as communication channels or ‘green phones’ between root-feeding and foliar-feeding insects and their parasitoids, focusing on recent findings that plants attacked belowground become significantly less attractive for parasitoids of the foliar-feeding insects.^18,20 We restrict this discussion to studies showing that root-feeding insects induce the direct defense system of shoots and interfere negatively with indirect defense signaling to higher trophic levels. It should be noted, however, that a number of case studies have reported positive plant-mediated interactions between root and foliar-feeding insects,^1,2 and higher trophic levels.^15,16,21

Plants as ‘Green Phones’: One Front Attacked—Two Fronts Defended?

Optimal defense theory suggests that plants allocate resources in an economic way, thereby matching the spatio-temporal expression of defense traits to long-term patterns of herbivore threats in natural systems.²² This poses the question why plants should express costly defenses at sites (e.g., aboveground) which are far from the site of attack (e.g., belowground). It has been recently proposed that plants may benefit from the induction of foliar defenses after root herbivory if this response diminishes the intensity of foliar damage of the plants that are already attacked in the roots.¹⁰ It is possible that the strategy of ‘one front attacked—two fronts defended’ is an adaptive response of plants to attenuate simultaneous infestations above- and belowground. For such a response to evolve, belowground herbivory should often be coupled to aboveground herbivore threats, implying that root damage is indicative of impending shoot damage. No data are available to date for testing this hypothesis.

Female parasitoids looking for hosts can discriminate against plant-host complexes infested by root-feeding insects, and preferentially oviposit on insect larvae (hosts) feeding on root-uninfested plants.^18,20 This may represent an adaptive response of female parasitoids to avoid suboptimal growth conditions for their offspring when developing on root-infested plants.⁹ However, such a decrease in the attraction of natural enemies of the herbivore can provide foliar-feeding insects with ‘enemy-free space’, thereby impairing plant performance. From the plant's perspective, the benefits of acting as a communication channel between root- and foliar-feeding herbivores to attenuate simultaneous infestations is thus clearly counterbalanced, and possibly eliminated, by trophic interferences with the indirect defense system of the plant via a reduced attraction of natural enemies of foliar herbivores after root infestation. The balance between ecological costs and benefits of the complex systemic defense signaling in plants awaits further clarification. Nevertheless, the above-mentioned findings provide novel insights into plant-mediated trophic communication, suggesting an important role for parasitoids as users of belowground information channeled through plants. This emphasizes the notion that parasitoids contribute substantially to the structure and organization of plant-based communities through topdown regulation of the insect herbivore populations.^23–28

Implications for the Foliar-Feeding Insects

Root-infested plants may represent a suboptimal food source (i.e., high in levels of phytotoxins) for foliar-feeding insects.^7,9 Similarly, shoot-infested plants may be of suboptimal nutritional value for root-feeding insects.^1,3,29–31 Consequently, root- and foliar-feeding insects should not attack the same plant to avoid fitness costs due to the systemic defense expression activated in the other plant compartment. However, root-infested plants can also offer a refuge to foliar-feeding herbivores through indirect protection from their natural enemies, leading to an ecological ‘dilemma’ for foliar-feeding insects with respect to root-infested host plants. Their choice is between (a) growing more slowly and/or attaining a smaller size, but benefitting from a smaller probability of being found by natural enemies on root-infested plants, or (b) optimizing their performance (larval growth and development) at the cost of running a higher risk of parasitism or predation on root-uninfested healthy plants.

Laboratory experiments and field studies are currently underway to test the hypothesis that foliar-feeding insects discriminate against plants already occupied by their counterparts in the belowground ecosystem, and whether they prefer to feed and oviposit on root-uninfested plants, thereby avoiding competition for the same plant resources. If such avoidance occurs, the strategy of ‘one front attacked—two fronts defended’ will result in benefits for the plant by reducing the probability for root-damaged plants being simultaneously attacked below- and aboveground.

Conclusions and Future Perspectives

It is now clear that interactive effects between above- and belowground organisms cannot be limited to insects directly associated with the plant, because such interactions clearly operate as parts of a much more complex chain of multitrophic communication and cross-interference between different food web levels. Consequently, higher trophic levels need to be incorporated into ecological studies aiming at elucidating plant-mediated communication leading to positive and negative feedbacks between plant-associated organisms. As discussed above, the outcome of trophic interactions and their interpretation in ecological and evolutionary terms may change considerably when diverse natural enemies are considered. A multitrophic approach linking food webs from the soil and the aboveground ecosystem is crucial to enhance our understanding of plant-based communities.