Herbivore-Induced Plant Volatiles Can Serve as Host Location Cues for a Generalist and a Specialist Egg Parasitoid (original) (raw)
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Animal Behaviour, 2008
Parasitoids of herbivorous larvae are well known to be able to associatively learn a response to feedinginduced plant volatiles. However, little is known of the abilities of egg parasitoids to learn a response to herbivore oviposition-induced plant volatiles (OVIV). The eulophid wasp Chrysonotomyia ruforum is known to be attracted by OVIV from Scots pine released 3 days after host egg deposition. This study aimed to elucidate (1) the impact of the nutritional state of the parasitoid on its response to OVIV and (2) the effect of learning and response to the temporal change of OVIV. Supply of food as a reward during associative learning trials inevitably influences the nutritional state and thus leads to an experimental constraint. Nevertheless, the results indicate that the parasitoids have to associate OVIV with host presence and that they need to be supplied with food to learn and to respond to OVIV. Furthermore, the parasitoids' positive response to OVIV from pine twigs laden with eggs for 3 days was independent of the induction time of pine twigs experienced. However, a positive response was given only to OVIV from pine twigs with 3-day-old eggs, while OVIV from twigs with other induction times (1, 2, 4 days) were not attractive. Thus, our findings indicate an unusual learning process in this specialized egg parasitoid. We suggest that the parasitoid is using a learning strategy by which common information is filtered out of similar odour blends (here: 1-to 4-day-long induced pine twigs), but a behavioural response to this learned information becomes evident only in a specific odour context (here: 3-day-long induced twigs).
Frontiers in Plant Science, 2014
Plants respond to insect oviposition by emission of oviposition-induced plant volatiles (OIPVs) which can recruit egg parasitoids of the attacking herbivore. To date, studies demonstrating egg parasitoid attraction to OIPVs have been carried out in tritrophic systems consisting of one species each of plant, herbivore host, and the associated egg parasitoid. Less attention has been given to plants experiencing multiple attacks by host and non-host herbivores that potentially could interfere with the recruitment of egg parasitoids as a result of modifications to the OIPV blend. Egg parasitoid attraction could also be influenced by the temporal dynamics of multiple infestations, when the same non-host herbivore damages different organs of the same plant species. In this scenario we investigated the responses of egg parasitoids to feeding and oviposition damage using a model system consisting of Vicia faba, the above-ground insect herbivore Nezara viridula, the above-and below-ground insect herbivore Sitona lineatus, and Trissolcus basalis, a natural enemy of N. viridula. We demonstrated that the non-host S. lineatus disrupts wasp attraction toward plant volatiles induced by the host N. viridula. Interestingly, V. faba damage inflicted by either adults (i.e., leaf-feeding) or larvae (i.e., root-feeding) of S. lineatus, had a similar disruptive effect on T. basalis host location, suggesting that a common interference mechanism might be involved. Neither naïve wasps or wasps with previous oviposition experience were attracted to plant volatiles induced by N. viridula when V. faba plants were concurrently infested with S. lineatus adults or larvae. Analysis of the volatile blends among healthy plants and aboveground treatments show significant differences in terms of whole volatile emissions. Our results demonstrate that induced plant responses caused by a non-host herbivore can disrupt the attraction of an egg parasitoid to a plant that is also infested with its hosts.
Journal of Chemical Ecology, 2008
Volatiles emitted by plants in response to feeding by Lygus species were tested in neurophysiological, behavioral, and parasitism trials with Anaphes iole, an egg parasitoid of Lygus. Electroantennogram analyses indicated that A. iole antennae responded to most herbivore-induced plant volatiles (HIPVs) tested and that females were usually more responsive than males. Antennal responses to (Z)-3hexenyl acetate and methyl salicylate were among the strongest. Behavioral assays in a four-arm olfactometer demonstrated that response of female wasps to (Z)-3hexenyl acetate varied greatly depending on preconditioning regime. Preconditioning wasps to complex host-plant odors led to stronger preference than did a single preconditioning stimulus, i.e., (Z)-3-hexenyl acetate. In a horizontal wind tunnel, female wasps were attracted by methyl salicylate and α-farnesene. Parasitism of Lygus lineolaris eggs by A. iole in a cotton field was greater when the eggs were associated with (Z)-3-hexenyl acetate or αfarnesene than with controls. Overall, the results of this study show that A. iole can perceive a variety of plant volatiles released after its host damages plants, that the degree of associative learning in A. iole can be manipulated based on preconditioning regime, and that single synthetic HIPVs are attractive to A. iole and can be used to increase attack rates on host eggs. Therefore, it appears that HIPVs have potential for use in suppression of Lygus population densities.
Parasitic Wasps Learn and Report Diverse Chemicals with Unique Conditionable Behaviors
Chemical Senses, 2003
Parasitoids exploit numerous chemical cues to locate hosts and food. Whether they detect and learn chemicals foreign to their natural history has not been explored. We show that the parasitoid Microplitis croceipes can associate, with food or hosts, widely different chemicals outside their natural foraging encounters. When learned chemicals are subsequently detected, this parasitoid manifests distinct behaviors characteristic with expectations of food or host, commensurate with prior training. This flexibility of parasitoids to rapidly link diverse chemicals to resource needs and subsequently report them with recognizable behaviors offers new insights into their foraging adaptability, and provides a model for further dissection of olfactory learning related processes. . (2001) Electroantennogram responses of a parasitic wasp, Microplitis croceipes, to host-related volatile and anthropogenic compounds. Physiol. Entomol., 26, 69-77. SAS Institute (1998) SAS User's Guide: Statistics. SAS Institute Inc., Cary, NC. Takasu, K. and Lewis, W.J. (1993) Host-and food-foraging of the parasitoid Microplitis croceipes: learning and physiological state effects. The effect of complete versus incomplete information on odor discrimination in a parasitic wasp. Anim. Behav., 55, 1271-1279. Visser, J.H. (1979) Electroantennogram responses of the Colorado beetle (Leptinotarsa decemlineata), to plant volatiles. Entomol. Exp. Appl., 25, 86-97. von Frisch, K. (1915) Der Farbensinn und formensinn der biene. Zool. Abt. behavior in the Hymenopteran parasitoid Microplitis croceipes. Entomol. Exp. Appl., 103, 135-138. Weatherston, I., Miller, D. and Dohse, L. (1985) Capillaries as controlled release devices for insect pheromones and other volatile substances-a reevaluation. Part I. Kinetics and development of predictive model for glass capillaries. J. Chem. Ecol., 11, 953-965.
BioControl, 2011
The response of the generalist egg parasitoid Ooencyrtus telenomicida (Vassiliev) (Hymenoptera: Encyrtidae) to host-related chemical cues from tomato plants, Solanum lycopersicum L., and adults of Nezara viridula (L.) (Heteroptera: Pentatomidae) was investigated in laboratory-based no-choice and paired-choice tests. In Y-tube olfactometer experiments, when female wasps were exposed to volatiles from plants in different conditions, they were attracted only to volatiles produced by N. viridula adult-infested tomato plants. When female wasps were exposed to adults of N. viridula, they were attracted to volatiles from virgin males, and, at a lower level, to volatiles from mated females in preoviposition state. Finally, studies in open arena showed that chemical footprints left by adults of N. viridula did not induce arrestment responses in wasp females. These results are discussed in terms of extrinsic competition with other beneficial egg parasitoids that in field can compete for the same egg mass, since intraguild interactions may affect the success of a biological control program.
Attraction of egg-killing parasitoids toward induced plant volatiles in a multi-herbivore context
Oecologia, 2015
by S. exigua eggs, indicating the specificity of the plant responses toward lepidopteran herbivores. The results of the chemical analysis revealed significant differences between the volatile blends emitted by plants in response to attack by P. brassicae and S. exigua eggs which were in agreement with the behavioural observations. We investigated the attraction of Trichogramma wasps toward P. brassicae egg-induced volatiles in plants simultaneously attacked by larvae and nymphs of different non-hosts. The two chewing caterpillars P. brassicae and S. exigua, but not the phloem-feeding aphid B. brassicae, can disrupt the attraction of Trichogramma species toward P. brassicae egg-induced volatiles. Indirect plant defenses are discussed in the context of multiple herbivory by evaluating the importance of origin, dietary specialization and feeding guild of different attackers on the recruitment of eggkilling parasitoids.
Parasitic wasps orient to green leaf volatiles
Chemoecology, 1990
Undamaged plants emit low levels of green leaf volatiles (GLVs), while caterpillar-damaged and artificially damaged plants emit relatively higher levels of cerrain GLVs. Female braconid parasitoids, Microplitis croceipes, oriented to both damaged plants and to individual GLVs in no-choice tests in a wind tunnel, but seldom oriented to undamaged plants. Female ichneumonid parasitoids, Netelia heroica, also oriented to individual GLVs in a wind tunnel. Males of both wasp species failed to orient to the GLVs. These data show that leaf-feeding caterpillars can cause the release of GLVs, and that parasitic wasps can respond to these odors by flying upwind (chemoanemotactic response), which brings the wasps to their caterpillar hosts. This supports the hypothesis that plants communicate with members of the third trophic level, i.e., plants under herbivore attack emit chemical signals that guide natural enemies of herbivores to sites of plant damage. In this interaction, the GLVs serve as tritrophic plant-to-parasitoid synomones. That parasitoids from two different wasp families oriented to GLVs suggests that the response may be widespread among the Hymenoptera.
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.
Role of volatile semiochemicals in host location by the egg parasitoid Anagrus breviphragma
Entomologia Experimentalis et Applicata, 2012
Recent investigations conducted on several tritrophic systems have demonstrated that egg parasitoids, when searching for host eggs, may exploit plant synomones that have been induced as a consequence of host oviposition. In this article we show that, in a system characterized by host eggs embedded in the plant tissue, naïve females of the egg parasitoid Anagrus breviphragma Soyka (Hymenoptera: Mymaridae) responded in a Y-tube olfactometer to volatiles from leaves of Carex riparia Curtis (Cyperaceae) containing eggs of one of its hosts, Cicadella viridis (L.) (Hemiptera: Cicadellidae). The wasp did not respond to host eggs or to clean leaves from non-infested plants compared with clean air, whereas it showed a strong preference for the olfactometer arm containing volatiles of leaves with embedded host eggs, compared with the arm containing volatiles of leaves from a non-infested plant or host eggs extracted from the plant. When the eggs were removed from an infested leaf, the parasitoid preference was observed only if eggs were added aside, suggesting a synergistic effect of a local plant synomone and an egg kairomone. The parasitoid also responded to clean leaves from an egginfested plant when compared with leaves from a non-infested plant, indicating a systemic effect of volatile induction.