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Plant mediated tritrophic interaction and biological pest control
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Herbivore-induced plant volatiles have been suggested to function as indirect defence signals that attract natural enemies of herbivores. Several insect parasitoids are known to exploit such plant-provided cues to locate hosts. It is unclear if individual plants benefit from the action of parasitoids. We investigated this question in maize plants under attack by Spodoptera littoralis larvae and found that parasitization by the endoparasitoids Cotesia marginiventris and Campoletis sonorensis significantly reduced feeding and weight gain in the host larvae. As a result, young maize plants attacked by a single parasitized larva suffered much less feeding damage and, at maturity, produced about 30% more seed than plants that were attacked by an unparasitized larva. Such fitness benefits may have contributed to selection pressures that shaped the evolution of herbivore-induced indirect defence signals in plants.
Herbivorous and carnivorous arthropods use plant volatiles when foraging for food. In response to herbivory, plants emit a blend that may be quantitatively and qualitatively different from the blend emitted when intact. This induced volatile blend alters the interactions of the plant with its environment. We review recent developments regarding the induction mechanism as well as the ecological consequences in a multitrophic and evolutionary context. It has been well established that carnivores (predators and parasitoids) are attracted by the volatiles induced by their herbivorous victims. This concerns an active plant response. In the case of attraction of predators, this is likely to result in a fitness benefit to the plant, because through consumption a predator removes the herbivores from the plant. However, the benefit to the plant is less clear when parasitoids are attracted, because parasitisation does usually not result in an instantaneous or in a complete termination of consumption by the herbivore. Recently, empirical evidence has been obtained that shows that the plant's response can increase plant fitness, in terms of seed production, due to a reduced consumption rate of parasitized herbivores. However, apart from a benefit from attracting carnivores, the induced volatiles can have a serious cost because there is an increasing number of studies that show that herbivores can be attracted. However, this does not necessarily result in settlement of the herbivores on the emitting plant. The presence of cues from herbivores and/or carnivores that indicate that the plant is a competitor- and/or enemy-dense space, may lead to an avoidance response. Thus, the benefit of emission of induced volatiles is likely to depend on the prevailing faunal composition. Whether plants can adjust their response and influence the emission of the induced volatiles, taking the prevalent environmental conditions into account, is an interesting question that needs to be addressed. The induced volatiles may also affect interactions of the emitting plant with its neighbours, e.g., through altered competitive ability or by the neighbour exploiting the emitted information.Major questions to be addressed in this research field comprise mechanistic aspects, such as the identification of the minimally effective blend of volatiles that explains the attraction of carnivores to herbivore-infested plants, and evolutionary aspects such as the fitness consequences of induced volatiles. The elucidation of mechanistic aspects is important for addressing ecological and evolutionary questions. For instance, an important tool to address ecological and evolutionary aspects would be to have plant pairs that differ in only a single trait. Such plants are likely to become available in the near future as a result of mechanistic studies on signal-transduction pathways and an increased interest in molecular genetics.
Specialist herbivores are known to alter their host's wound-induced responses but the beneficiaries of these alterations are unknown. Nicotiana attenuata plants release a burst of ethylene specifically in response to feeding by Manduca sexta larvae, which is known to suppress wound- and methyl jasmonate (MeJA)-inducible nicotine accumulation. The ethylene burst may be a mechanism by which M. sexta larvae feed "stealthily" on their host plants or, alternatively, it may allow the plant to optimize its defense response against this specialist herbivore by reducing costs of induction. We examined the impact of the ethylene burst on defense-related fitness costs that are readily observed when plants are treated with MeJA and grown in competition with untreated plants. We elicited nicotine induction (with MeJA), the ethylene burst (with the ethylene releasing compound, ethephon) and inhibited the plant's ability to perceive ethylene (with applications of an antagonist of ethylene receptors, 1-methylcyclopropene, 1-MCP). By simultaneously applying MeJA and ethephon we mimicked the plant's hormonal response to larval attack. We hypothesized that if the ethylene burst benefited the plant, the fitness costs of MeJA induction should be reduced by ethephon and restored if the plants were additionally treated with 1-MCP. In a second experiment, we applied larval oral secretion (OS) to elicit endogenous hormone production and predicted that the 1-MCP treatment should reduce the fitness of OS-treated plants. Our measures of plant fitness, namely the rate of stalk elongation and lifetime capsule production, supported these predictions. We conclude that the ethylene burst elicited by this specialist herbivore can reduce MeJA-induced fitness costs and increase the competitive strength of OS-treated plants. Suppressed nicotine production is likely to contribute to, but is not sufficient to explain, the observed fitness outcomes. The intensity of intra-specific competition and herbivore attack will likely determine the adaptive value of the M. sexta-elicited ethylene response.
The female parasitic waspCotesia kariyai discriminated between the volatiles of corn leaves infested by younger host larvaePseudaletia separata (first to fourth instar) and uninfested leaves in a Y-tube olfactometer; the wasps were attracted to the infested leaves. In contrast, when corn plants were infested by the later stages (fifth and sixth instar) of the armyworm, the wasps did not distinguish between infested corn leaves and uninfested corn leaves in the olfactometer. Mechanically damaged leaves were no more attractive than undamaged leaves, and host larvae or their feces were not attractive to the parasitoid. Through chemical analysis, the herbivore-induced plant volatiles were identified in the headspace of infested corn leaves. The herbivore-induced volatiles (HIVs) constituted a larger proportion of the headspace of corn leaves infested by early instar armyworms than of corn leaves infested by late instar armyworms. Application of third-instar larval regurgitant onto artificially damaged sites of leaves resulted in emission of parasitoid attractants from the leaf, whereas leaves treated with sixth-instar regurgitant did not. The function of this herbivore-stage related specificity of herbivore-induced synomones is discussed in a tritrophic context.
Abstract. To examine the hypothesis that intra-plant oviposition preferences of Manduca
quinquemaculata on Nicotiana attenuate optimize predation risk and nutritional needs
of developing larvae and eggs, we measured oviposition behavior of adults and larval
mortality, movement, performance, and body temperatures at different leaf positions in a
natural population. Nearly 70% of the eggs were oviposited on young central stem leaves
of elongated plants. Intra-plant movement was very rare in the first and common in the
second to fourth larval instars. The oviposition preference for, and larval movement toward,
younger leaves was correlated with a 40% lower predation risk and a 6.3-fold greater mass
gain, suggesting higher nutritive value despite 2. 1-fold higher nicotine concentrations and
4.6-fold higher polyphenol oxidase activities. The predatory bug, Geocoris pallens, which
consumed eggs and larvae with instar- and leaf position-specific preferences, was responsible
for the vast majority of M. quinquemaculata mortality and may shape the moth's
oviposition preference.
After herbivore attack, plants launch a suite of direct and indirect defense responses that must be coordinated if plants
are to realize a fitness benefit from these responses. Here we characterize the volatile emissions in the native tobacco plant, Nicotiana attenuata Torr. ex Wats., that are elicited by tobacco hornworm (Manduca sexta L.) attack and are known to function as attractants for parasitoids. To provide the first ecophysiological comparison of
examples of both types of defense in the same species, we characterize the elicitation and signaling mechanisms, the resources
required, and the potential costs and benefits of the volatile release and compare these traits with those of the well-described
induced direct defense in this species, nicotine production. The release of (E)-β-ocimene, cis-α-bergamotene and linalool is dramatically induced within 24 h by application of methyl jasmonate (MeJA), caterpillar feeding,
and the treatment of mechanical wounds with larval oral secretions (OS), but not by mechanical damage alone. Plants from different
geographic locations produce volatile blends that differ in composition. The most consistently released component from all
genotypes, cis-α-berga-motene, is positively related to the amount of MeJA and the level of wounding if OS are applied to the wounds. The
volatile release is strongly light dependent, dropping to undetectable quantities during dark periods, even when temperatures
are elevated to match those of the light period. Inhibitors of wound-induced jasmonate accumulation (salicylates and auxins),
which are known to inhibit wound-induced nicotine production, do not inhibit the release of volatiles. By individually inducing
different leaf positions with OS and, on other plants, excising them after induction, we demonstrate that the emission is
largely a systemic, whole-plant response, which is maximally triggered when the second fully expanded leaf is induced. We
conclude that while both are whole-plant, systemic responses that utilize recently acquired resources for their production
and are activated by the jasmonate cascade, the elicitation of the volatile release exhibits greater tissue sensitivity and
utilizes additional signaling components than does nicotine production. In contrast to the large investment of fitness-limiting
resources required for induced nicotine production or the resources used in benzyl acetone release from flowers for pollinator
attraction, the resource requirements for the volatile release are minor. Hence the argument that the volatile release incurs
comparatively large physiological costs cannot be supported in this system.
We have successfully released phytophagous Willamette mites into Zinfandel vineyards that have had chronic problems with the economically more damaging Pacific spider mites. These release induced resistance in the grapevines, causing smaller populations of Pacific mites and higher berry sugar concentrations. This study addresses the sustainability of our techniques. We define a sustainable technique as one that (1) is effective, (2) requires low inputs of resources, (3) is self-perpetuating, (4) produces minimal pollution, (5) produces minimal effects on non-target organisms, and (6) is compatible with other agronomic practices. Most of these criteria are met by our inoculation techniques; here we seek to determine the persistence of Willamette mites from one season to the next, and to evaluate effects of several commonly used agronomic practices on our vaccinations. Our data suggest that Willamette mites can be introduced a single time into a vineyard; they will reduce populations of Pacific mites and persist from year to year in the absence of miticides or other disruptions. We observed Willamette mites overwintering commonly on the grapevines and on box elder (Acer negundo) foliage adjacent to vineyards. Pacific mites were not observed overwintering in vineyards, and we surmise that they generally blow into vineyards during each growing season. We did not observe Willamette mites overwintering on cover crops although other phytophagous mites and predatory mites were found. In preliminary observations, we found no strong effects (positive or negative) associated with cover-cropping in terms of mite management. Vineyards with Pacific mites are often treated with miticides, either dicofol or propargite. We found that dicofol (but not propargite) was extremely disruptive to mite populations; after an initial kill, applications of dicofol were consistently associated with resurgences of mites that exceeded numbers found in unsprayed controls. Unlike applications of miticides, introductions of Willamette mites to control Pacific mites satisfy our criteria for sustainable agriculture. Here we demonstrated that they are self-perpetuating at low numbers from one season to the next. Furthermore, releasing Willamette mites for control of Pacific mites is compatible with some, but not all, management practices.
Volatile compounds elicited by insect herbivore feeding damage in five cotton cultivars and one naturalized cotton variety were examined by allowing beet armyworm larvae to feed overnight on leaves and collecting volatiles from the plants in situ. Of 23 compounds identified from larval damaged leaves, terpenes and lipoxygenase-hydroperoxide lyase-derived volatiles predominated. No pronounced differences in the levels of volatile emission were noted from leaves of undamaged plants of the different varieties. However, average volatile emission from damaged leaves of the naturalized variety was almost sevenfold higher than from damaged leaves of the commercial cultivars. This was despite the fact that larvae preferred feeding on the leaves of commercial cultivars over those of the naturalized variety in choice tests.
We have successfully released phytophagous Willamette mites into Zinfandel vineyards that have had chronic problems with the economically more damaging Pacific spider mites. These releases induced resistance in the grapevines, causing smaller populations of Pacific mites and higher berry sugar concentrations. This study addresses the sustainability of our techniques. We define a sustainable technique as one that (1) is effective, (2) requires low inputs of resources, (3) is self-perpetuating, (4) produces minimal pollution, (5) produces minimal effects on non-target organisms, and (6) is compatible with other agronomic practices. Most of these criteria are met by our inoculation techniques; here we seek to determine the persistence of Willamette mites from one season to the next, and to evaluate effects of several commonly used agronomic practices on our vaccinations. Our data suggest that Willamette mites can be introduced a single time into a vineyard; they will reduce populations of Pacific mites and persist from year to year in the absence of miticides or other disruptions. We observed Willamette mites overwintering commonly on the grapevines and on box elder (Acer negundo) foliage adjacent to vineyards. Pacific mites were not observed overwintering in vineyards, and we surmise that they generally blow into vineyards during each growing season. We did not observe Willamette mites overwintering on cover crops although other phytophagous mites and predatory mites were found. In preliminary observations, we found no strong effects (positive or negative) associated with cover-cropping in terms of mite management. Vineyards with Pacific mites are often treated with miticides, either dicofol or propargite. We found that dicofol (but not propargite) was extremely disruptive to mite populations; after an initial kill, applications of dicofol were consistently associated with resurgences of mites that exceeded numbers found in unsprayed controls. Unlike applications of miticides, introductions of Willamette mites to control Pacific mites satisfy our criteria for sustainable agriculture. Here we demonstrated that they are self-perpetuating at low numbers from one season to the next. Furthermore, releasing Willamette mites for control of Pacific mites is compatible with some, but not all, management practices.