Can plants betray the presence of multiple herbivore species to predators and parasitoids? The role of learning in phytochemical information networks (original) (raw)
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Ecology …, 2008
The attraction of natural enemies of herbivores by volatile organic compounds as an induced indirect defence has been studied in several plant systems. The evidence for their defensive function originates mainly from laboratory studies with trained parasitoids and predators; the defensive function of these emissions for plants in natural settings has been rarely demonstrated. In native populations and laboratory Y-tube choice experiments with transgenic Nicotiana attenuata plants unable to release particular volatiles, we demonstrate that predatory bugs use terpenoids and green leaf volatiles (GLVs) to locate their prey on herbivore-attacked plants. By attracting predators with volatile signals, this native plant reduces its herbivore loaddemonstrating the defensive function of herbivore-induced volatile emissions. However, plants producing GLVs are also damaged more by flea beetles. The implications of these conflicting ecological effects for the evolution of induced volatile emissions and for the development of sustainable agricultural practices are discussed.
What signals do herbivore-induced plant volatiles provide conspecific herbivores?
Arthropod-Plant Interactions, 2017
Herbivore-induced plant volatiles (HIPVs) have been opined as 'indirect or direct defenses' of plants and are extensively studied. In contrast, HIPVs may also indicate that plant defenses have been overcome by herbivores infesting the plant; however, studies on this aspect have so far received little attention. Using the interaction of Capsicum annum (Bell pepper) with its pest Scirtothrips dorsalis (Chilli thrips) as a model system, we studied the role of HIPVs in this selected insect-plant interaction. Multiple-choice olfactometer assays with headspace volatiles collected from different growth stages of un-infested C. annum plants represented by pre-flowering (PF), flowering (FL) and fruiting stages (FR) proved FR volatiles to be highly attractive to S. dorsalis. Further, FR plants were infested with S. dorsalis adults and HIPVs released by infested plants were collected and subjected to multiple-choice olfactometer bioassays. Thrips were significantly attracted to HIPVs than to headspace volatiles of un-infested FR plants or thrips body odour. Coupled GC-EAG with S. dorsalis and HIPVs or FR plant volatile revealed specific compounds that elicited an EAG response. Individual EAG-active compounds were less attractive to thrips, however, synthetic blends of EAGactive compounds at the ratio similar to headspace samples were found to be highly attractive. However, when given a choice between synthetic blends of HIPVs and FR, thrips were significantly attracted to synthetic blend of HIPVs. Our study provides empirical data on signals HIPVs may provide to conspecific herbivores and suggests that the role of HIPVs, mostly generalized as defense, may vary based on the interaction and must be studied closely to understand their ecological functions.
Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context
Entomologia Experimentalis et Applicata, 2000
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.
Physiological Entomology, 2000
We investigated how the plant-inhabiting, anthocorid predator, Anthocoris nemoralis, copes with variation in prey, host plant and associated herbivore-induced plant volatiles and in particular whether the preference for these plant odours is innate or acquired. We found a marked difference between the olfactory response of orchard-caught predators and that of their ®rst generation reared on¯our moth eggs in the laboratory, i.e. under conditions free of herbivoryinduced volatiles. Whereas the orchard-caught predators preferred odour from psyllid-infested pear leaves, when offered against clean air in a Y-tube olfactometer, the laboratory-reared ®rst generation of (naive) predators did not. The same difference was found when a single component (methyl salicylate) of the herbivore-induced plant volatiles was offered against clean air. After experiencing methyl salicylate with prey, however, the laboratory-reared predators showed a pronounced preference for this volatile. This acquired preference did not depend on whether the volatile had been experienced in the juvenile period or in the adult phase, but it did depend on whether it had been offered in presence or absence of prey. In the ®rst case, they were attracted to the plant volatile in subsequent olfactometer experiments, but when the volatile had been offered during a period of prey deprivation, the predators were not attracted. We conclude that associative learning is the most likely mechanism underlying acquired odour preference.
Volatile signaling in plant–plant–herbivore interactions: what is real?
Current Opinion in Plant Biology, 2002
Plants release volatiles after herbivore attack in a highly regulated fashion. These compounds attract natural enemies and function as indirect defenses. Whether neighboring plants 'eavesdrop' on these volatile signals and tailor their defenses accordingly remains controversial. Recent laboratory studies have identified transcriptional changes that occur in plants in response to certain volatiles. These changes occur under conditions that enhance the probability of signal perception and response. Field studies have demonstrated repeatable increases in the herbivore resistance of plants growing downwind of damaged plants.
Herbivore-Induced Plant Volatiles Mediate In-Flight Host Discrimination by Parasitoids
Journal of Chemical Ecology, 2005
Herbivore feeding induces plants to emit volatiles that are detectable and reliable cues for foraging parasitoids, which allows them to perform oriented host searching. We investigated whether these plant volatiles play a role in avoiding parasitoid competition by discriminating parasitized from unparasitized hosts in flight. In a wind tunnel set-up, we used mechanically damaged plants treated with regurgitant containing elicitors to simulate and standardize herbivore feeding. The solitary parasitoid Cotesia rubecula discriminated among volatile blends from Brussels sprouts plants treated with regurgitant of unparasitized Pieris rapae or P. brassicae caterpillars over blends emitted by plants treated with regurgitant of parasitized caterpillars. The gregarious Cotesia glomerata discriminated between volatiles induced by regurgitant from parasitized and unparasitized caterpillars of its major host species, P. brassicae. Gas chromatography-mass spectrometry analysis of headspace odors revealed that cabbage plants treated with regurgitant of parasitized P. brassicae caterpillars emitted lower amounts of volatiles than plants treated with unparasitized caterpillars. We demonstrate (1) that parasitoids can detect, in flight, whether their hosts contain competitors, and (2) that plants reduce the production of specific herbivoreinduced volatiles after a successful recruitment of their bodyguards. As the induced volatiles bear biosynthetic and ecological costs to plants, downregulation of their production has adaptive value. These findings add a new level of intricacy to plantYparasitoid interactions.
Information arms race explains plant-herbivore chemical communication in ecological communities
Science
Plants emit an extraordinary diversity of chemicals that provide information about their identity and mediate their interactions with insects. However, most studies of this have focused on a few model species in controlled environments, limiting our capacity to understand plant-insect chemical communication in ecological communities. Here, by integrating information theory with ecological and evolutionary theories, we show that a stable information structure of plant volatile organic compounds (VOCs) can emerge from a conflicting information process between plants and herbivores. We corroborate this information “arms race” theory with field data recording plant-VOC associations and plant-herbivore interactions in a tropical dry forest. We reveal that plant VOC redundancy and herbivore specialization can be explained by a conflicting information transfer. Information-based communication approaches can increase our understanding of species interactions across trophic levels.
Natural Enemy Attraction to Plant Volatiles
2008
Leaves normally release low levels of volatile chemicals. However, when a plant is damaged by herbivorous insects, the emission of volatile organic compounds increases. The chemical composition varies with the herbivorous insect species as well as the plant species. Volatile phytochemicals can serve as airborne semiochemicals, deterring or promoting interactions between plants and insect herbivores. For example, moths (Heliothis virescens) are repelled by herbivore induced volatiles released from tobacco plants at night; such odor cues may allow females to avoid oviposition on previously damaged plants. For swallowtail butterflies, volatiles from host plants enhance the effect of contact stimulants, increasing landing rates and oviposition relative to non-host plants. Volatile plant signals may also induce defense responses in neighboring plants. Such semiochemicals that function in communication between and among species are emitted from a diverse group of plants and mediate key processes in the behavior of specific insects.
Induced response against herbivory by chemical information transfer between plants
Brazilian Journal of Plant Physiology, 2008
Plants respond to herbivores and pathogens attack with increased emission of volatile organic compounds. These molecules act as indirect defences when attracting natural enemies of herbivores and thus benefit the plant. It remains controversial whether undamaged plants capture chemicals released by damaged neighbouring plants and respond to them by increasing their defensive barriers against an imminent attack. In spite of public appeal and of this being the 25th year of the Talking Trees Hypothesis, only recently have the most sceptical scientists been convinced. The induced response to herbivory by interplant information transfer has been found in two plant-herbivore systems. However, the universality of the phenomenon and its ecological and evolutionary relevance remain unclear. The integration of Molecular Biology, Biochemistry, Physiology, and Ecology begin to shed light on the mechanisms of the signal transfer. This integrative approach has developed new and more sensitive too...