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1.
PLoS Pathog ; 19(3): e1011262, 2023 03.
Artigo em Inglês | MEDLINE | ID: mdl-36947551

RESUMO

Microorganisms living in and on macroorganisms may produce microbial volatile compounds (mVOCs) that characterise organismal odours. The mVOCs might thereby provide a reliable cue to carnivorous enemies in locating their host or prey. Parasitism by parasitoid wasps might alter the microbiome of their caterpillar host, affecting organismal odours and interactions with insects of higher trophic levels such as hyperparasitoids. Hyperparasitoids parasitise larvae or pupae of parasitoids, which are often concealed or inconspicuous. Odours of parasitised caterpillars aid them to locate their host, but the origin of these odours and its relationship to the caterpillar microbiome are unknown. Here, we analysed the odours and microbiome of the large cabbage white caterpillar Pieris brassicae in relation to parasitism by its endoparasitoid Cotesia glomerata. We identified how bacterial presence in and on the caterpillars is correlated with caterpillar odours and tested the attractiveness of parasitised and unparasitised caterpillars to the hyperparasitoid Baryscapus galactopus. We manipulated the presence of the external microbiome and the transient internal microbiome of caterpillars to identify the microbial origin of odours. We found that parasitism by C. glomerata led to the production of five characteristic volatile products and significantly affected the internal and external microbiome of the caterpillar, which were both found to have a significant correlation with caterpillar odours. The preference of the hyperparasitoid was correlated with the presence of the external microbiome. Likely, the changes in external microbiome and body odour after parasitism were driven by the resident internal microbiome of caterpillars, where the bacterium Wolbachia sp. was only present after parasitism. Micro-injection of Wolbachia in unparasitised caterpillars increased hyperparasitoid attraction to the caterpillars compared to untreated caterpillars, while no differences were found compared to parasitised caterpillars. In conclusion, our results indicate that host-parasite interactions can affect multi-trophic interactions and hyperparasitoid olfaction through alterations of the microbiome.


Assuntos
Borboletas , Vespas , Animais , Odorantes , Larva , Borboletas/parasitologia , Vespas/parasitologia , Interações Hospedeiro-Parasita
2.
Plant Cell Environ ; 46(3): 931-945, 2023 03.
Artigo em Inglês | MEDLINE | ID: mdl-36514238

RESUMO

Soil composition and herbivory are two environmental factors that can affect plant traits including flower traits, thus potentially affecting plant-pollinator interactions. Importantly, soil composition and herbivory may interact in these effects, with consequences for plant fitness. We assessed the main effects of aboveground insect herbivory and soil amendment with exuviae of three different insect species on visual and olfactory traits of Brassica nigra plants, including interactive effects. We combined various methodological approaches including gas chromatography/mass spectrometry, spectroscopy and machine learning to evaluate changes in flower morphology, colour and the emission of volatile organic compounds (VOCs). Soil amended with insect exuviae increased the total number of flowers per plant and VOC emission, whereas herbivory reduced petal area and VOC emission. Soil amendment and herbivory interacted in their effect on the floral reflectance spectrum of the base part of petals and the emission of 10 VOCs. These findings demonstrate the effects of insect exuviae as soil amendment on plant traits involved in reproduction, with a potential for enhanced reproductive success by increasing the strength of signals attracting pollinators and by mitigating the negative effects of herbivory.


Assuntos
Solo , Compostos Orgânicos Voláteis , Animais , Compostos Orgânicos Voláteis/análise , Polinização , Flores/anatomia & histologia , Insetos , Herbivoria
3.
Proc Natl Acad Sci U S A ; 115(20): 5205-5210, 2018 05 15.
Artigo em Inglês | MEDLINE | ID: mdl-29712841

RESUMO

Symbiotic relationships may provide organisms with key innovations that aid in the establishment of new niches. For example, during oviposition, some species of parasitoid wasps, whose larvae develop inside the bodies of other insects, inject polydnaviruses into their hosts. These symbiotic viruses disrupt host immune responses, allowing the parasitoid's progeny to survive. Here we show that symbiotic polydnaviruses also have a downside to the parasitoid's progeny by initiating a multitrophic chain of interactions that reveals the parasitoid larvae to their enemies. These enemies are hyperparasitoids that use the parasitoid progeny as host for their own offspring. We found that the virus and venom injected by the parasitoid during oviposition, but not the parasitoid progeny itself, affected hyperparasitoid attraction toward plant volatiles induced by feeding of parasitized caterpillars. We identified activity of virus-related genes in the caterpillar salivary gland. Moreover, the virus affected the activity of elicitors of salivary origin that induce plant responses to caterpillar feeding. The changes in caterpillar saliva were critical in inducing plant volatiles that are used by hyperparasitoids to locate parasitized caterpillars. Our results show that symbiotic organisms may be key drivers of multitrophic ecological interactions. We anticipate that this phenomenon is widespread in nature, because of the abundance of symbiotic microorganisms across trophic levels in ecological communities. Their role should be more prominently integrated in community ecology to understand organization of natural and managed ecosystems, as well as adaptations of individual organisms that are part of these communities.


Assuntos
Borboletas/parasitologia , Interações Hospedeiro-Parasita , Larva/parasitologia , Plantas/metabolismo , Polydnaviridae/fisiologia , Peçonhas/administração & dosagem , Vespas/parasitologia , Animais , Borboletas/fisiologia , Borboletas/virologia , Ecossistema , Regulação da Expressão Gênica de Plantas , Larva/fisiologia , Larva/virologia , Plantas/parasitologia , Plantas/virologia , Simbiose , Vespas/fisiologia , Vespas/virologia
4.
New Phytol ; 220(3): 739-749, 2018 11.
Artigo em Inglês | MEDLINE | ID: mdl-28256726

RESUMO

Chemical communication is ubiquitous. The identification of conserved structural elements in visual and acoustic communication is well established, but comparable information on chemical communication displays (CCDs) is lacking. We assessed the phenotypic integration of CCDs in a meta-analysis to characterize patterns of covariation in CCDs and identified functional or biosynthetically constrained modules. Poorly integrated plant CCDs (i.e. low covariation between scent compounds) support the notion that plants often utilize one or few key compounds to repel antagonists or to attract pollinators and enemies of herbivores. Animal CCDs (mostly insect pheromones) were usually more integrated than those of plants (i.e. stronger covariation), suggesting that animals communicate via fixed proportions among compounds. Both plant and animal CCDs were composed of modules, which are groups of strongly covarying compounds. Biosynthetic similarity of compounds revealed biosynthetic constraints in the covariation patterns of plant CCDs. We provide a novel perspective on chemical communication and a basis for future investigations on structural properties of CCDs. This will facilitate identifying modules and biosynthetic constraints that may affect the outcome of selection and thus provide a predictive framework for evolutionary trajectories of CCDs in plants and animals.


Assuntos
Evolução Biológica , Vias Biossintéticas , Animais , Fenótipo , Compostos Orgânicos Voláteis/metabolismo
5.
J Exp Biol ; 221(Pt 22)2018 11 16.
Artigo em Inglês | MEDLINE | ID: mdl-30297513

RESUMO

Anthropophilic mosquitoes are effective vectors of human disease because of their biting preferences. To find their host, these mosquitoes are guided by human odours, primarily produced by human skin bacteria. By analysing the skin bacterial and skin volatile profiles of humans, bonobos, chimpanzees, gorillas, lemurs and cows, we investigated whether primates that are more closely related to humans have a skin bacterial community and odour profile that is similar to that of humans. We then investigated whether this affected discrimination between humans and closely related primates by anthropophilic and zoophilic mosquitoes that search for hosts. Humans had a lower skin bacterial diversity than the other animals and their skin bacterial composition was more similar to that in other primates than it was to the skin bacteria of cows. Like the skin bacterial profiles, the volatile profiles of the animal groups were clearly different from each other. The volatile profiles of cows and lemurs were more closely related to the human profiles than expected. Human volatiles were indeed preferred above cow volatiles by anthropophilic mosquitoes and no preference was observed when tested against non-human primate odour, except for bonobo volatiles, which were preferred over human volatiles. Unravelling the differences between mosquito hosts and their effect on host selection is important for a better understanding of cross-species transmission of vector-borne diseases.


Assuntos
Anopheles/fisiologia , Bactérias/isolamento & purificação , Quimiotaxia , Pele/metabolismo , Pele/microbiologia , Compostos Orgânicos Voláteis/metabolismo , Animais , Bovinos , Comportamento Alimentar , Feminino , Humanos , Masculino , Odorantes/análise , Primatas , Olfato
6.
Oecologia ; 187(3): 873-874, 2018 07.
Artigo em Inglês | MEDLINE | ID: mdl-29728766

RESUMO

One of the main abiotic stresses that strongly affects plant survival and the primary cause of crop loss around the world is drought.

7.
Plant Cell ; 26(12): 4991-5008, 2014 Dec.
Artigo em Inglês | MEDLINE | ID: mdl-25490915

RESUMO

A pathogen may cause infected plants to promote the performance of its transmitting vector, which accelerates the spread of the pathogen. This positive effect of a pathogen on its vector via their shared host plant is termed indirect mutualism. For example, terpene biosynthesis is suppressed in begomovirus-infected plants, leading to reduced plant resistance and enhanced performance of the whiteflies (Bemisia tabaci) that transmit these viruses. Although begomovirus-whitefly mutualism has been known, the underlying mechanism is still elusive. Here, we identified ßC1 of Tomato yellow leaf curl China virus, a monopartite begomovirus, as the viral genetic factor that suppresses plant terpene biosynthesis. ßC1 directly interacts with the basic helix-loop-helix transcription factor MYC2 to compromise the activation of MYC2-regulated terpene synthase genes, thereby reducing whitefly resistance. MYC2 associates with the bipartite begomoviral protein BV1, suggesting that MYC2 is an evolutionarily conserved target of begomoviruses for the suppression of terpene-based resistance and the promotion of vector performance. Our findings describe how this viral pathogen regulates host plant metabolism to establish mutualism with its insect vector.


Assuntos
Proteínas de Arabidopsis/metabolismo , Arabidopsis/virologia , Fatores de Transcrição de Zíper de Leucina e Hélice-Alça-Hélix Básicos/metabolismo , Geminiviridae/genética , Hemípteros/fisiologia , Nicotiana/virologia , Terpenos/metabolismo , Fatores de Virulência/fisiologia , Animais , Arabidopsis/imunologia , Arabidopsis/metabolismo , Proteínas de Arabidopsis/genética , Fatores de Transcrição de Zíper de Leucina e Hélice-Alça-Hélix Básicos/genética , Vias Biossintéticas/genética , Resistência à Doença/genética , Hemípteros/virologia , Insetos Vetores/fisiologia , Insetos Vetores/virologia , Transdução de Sinais , Nicotiana/metabolismo , Fatores de Virulência/genética , Fatores de Virulência/metabolismo
8.
Oecologia ; 185(4): 699-712, 2017 Dec.
Artigo em Inglês | MEDLINE | ID: mdl-29052769

RESUMO

One of the responses of plants to insect attack is the production of volatile organic compounds that mediate indirect defence of plants by attracting natural enemies of the attacking herbivores. Herbivore-induced plant volatiles (HIPVs) include terpenoids that play key roles in the attraction of natural enemies. Crosstalk between phytohormonal signalling pathways is well known to affect the regulation of plant defences, including the emission of HIPVs. Thus, simultaneous feeding on the same plant by caterpillars and aphids, can affect the attraction of parasitoids by the plant compared to single insect attack. The role of aphid density in the regulation of HIPV emission by plants under dual attack has not been studied previously. Here, we investigated the attraction of Diadegma semiclausum, a parasitoid of the Diamondback moth Plutella xylostella, to volatiles emitted by Arabidopsis thaliana plants, simultaneously attacked by host caterpillars, and by the non-host aphid Brevicoryne brassicae. Our study shows that the effect of aphid infestation on parasitoid attraction is influenced by the density of the aphids. Biosynthesis and emission of (E,E)-α-farnesene could be linked to the observed preference of D. semiclausum parasitoids for the HIPV blend emitted by plants dually infested by caterpillars and aphids at a high density compared to dually infested plants with a low aphid density. Parasitoids such as D. semiclausum are important enemies of herbivorous insects and a better understanding of how plants express indirect defence mechanisms in response to multiple insect attack will provide important knowledge on plant-herbivore-parasitoid interactions under multiple stress conditions.


Assuntos
Afídeos/fisiologia , Arabidopsis/fisiologia , Arabidopsis/parasitologia , Larva/fisiologia , Animais , Herbivoria/efeitos dos fármacos , Interações Hospedeiro-Parasita , Himenópteros , Mariposas/fisiologia , Reguladores de Crescimento de Plantas/farmacologia , Terpenos , Compostos Orgânicos Voláteis/farmacologia
9.
J Chem Ecol ; 43(5): 493-505, 2017 May.
Artigo em Inglês | MEDLINE | ID: mdl-28405915

RESUMO

Attraction of parasitoids to plant volatiles induced by multiple herbivory depends on the specific combinations of attacking herbivore species, especially when their feeding modes activate different defense signalling pathways as has been reported for phloem feeding aphids and tissue feeding caterpillars. We studied the effects of pre-infestation with non-host aphids (Brevicoryne brassicae) for two different time periods on the ability of two parasitoid species to discriminate between volatiles emitted by plants infested by host caterpillars alone and those emitted by plants infested with host caterpillars plus aphids. Using plants originating from three chemically distinct wild cabbage (Brassica oleracea) populations, Diadegma semiclausum switched preference for dually infested plants to preference for plants infested with Plutella xylostella hosts alone when the duration of pre-aphid infestation doubled from 7 to 14 days. Microplitis mediator, a parasitoid of Mamestra brassicae caterpillars, preferred dually-infested plants irrespective of aphid-infestation duration. Separation of the volatile blends emitted by plants infested with hosts plus aphids or with hosts only was poor, based on multivariate statistics. However, emission rates of individual compounds were often reduced in plants infested with aphids plus hosts compared to those emitted by plants infested with hosts alone. This effect depended on host caterpillar species and plant population and was little affected by aphid infestation duration. Thus, the interactive effect of aphids and hosts on plant volatile production and parasitoid attraction can be dynamic and parasitoid specific. The characteristics of the multi-component volatile blends that determine parasitoid attraction are too complex to be deduced from simple correlative statistical analyses.


Assuntos
Brassica/química , Animais , Afídeos/efeitos dos fármacos , Afídeos/crescimento & desenvolvimento , Afídeos/fisiologia , Comportamento Animal/efeitos dos fármacos , Brassica/metabolismo , Cromatografia Gasosa , Interações Hospedeiro-Parasita/efeitos dos fármacos , Larva/fisiologia , Compostos Orgânicos Voláteis/análise , Compostos Orgânicos Voláteis/farmacologia
10.
J Chem Ecol ; 43(1): 53-65, 2017 Jan.
Artigo em Inglês | MEDLINE | ID: mdl-28050733

RESUMO

Plants release a variety of volatile organic compounds that play multiple roles in the interactions with other plants and animals. Natural enemies of plant-feeding insects use these volatiles as cues to find their prey or host. Here, we report differences between the volatile blends of tomato plants infested with the whitefly Bemisia tabaci or the tomato borer Tuta absoluta. We compared the volatile emission of: (1) clean tomato plants; (2) tomato plants infested with T. absoluta larvae; and (3) tomato plants infested with B. tabaci adults, nymphs, and eggs. A total of 80 volatiles were recorded of which 10 occurred consistently only in the headspace of T. absoluta-infested plants. Many of the compounds detected in the headspace of the two herbivory treatments were emitted at different rates. Plants damaged by T. absoluta emitted at least 10 times higher levels of many compounds compared to plants damaged by B. tabaci and intact plants. The multivariate separation of T. absoluta-infested plants from those infested with B. tabaci was due largely to the chorismate-derived compounds as well as volatile metabolites of C18-fatty acids and branched chain amino acids that had higher emission rates from T. absoluta-infested plants, whereas the cyclic sesquiterpenes α- and ß-copaene, valencene, and aristolochene were emitted at significantly higher levels from B. tabaci-infested plants. Our findings imply that feeding by T. absoluta and B. tabaci induced emission of volatile blends that differ quantitatively and qualitatively, providing a chemical basis for the recently documented behavioral discrimination by two generalist predatory mirid species, natural enemies of T. absoluta and B. tabaci employed in biological control.


Assuntos
Hemípteros/fisiologia , Interações Hospedeiro-Parasita , Lepidópteros/fisiologia , Compostos Fitoquímicos , Solanum lycopersicum , Compostos Orgânicos Voláteis , Animais , Feminino , Herbivoria , Solanum lycopersicum/metabolismo , Solanum lycopersicum/parasitologia , Compostos Fitoquímicos/análise , Compostos Fitoquímicos/metabolismo , Compostos Orgânicos Voláteis/análise , Compostos Orgânicos Voláteis/metabolismo
11.
J Chem Ecol ; 43(10): 1007-1022, 2017 Oct.
Artigo em Inglês | MEDLINE | ID: mdl-28951999

RESUMO

In response to herbivory by insects, various plants produce volatiles that attract enemies of the herbivores. Although ants are important components of natural and agro-ecosystems, the importance of herbivore-induced plant volatiles (HIPVs) as cues for ants for finding food sources have received little attention. We investigated responses of the ant Formica pratensis to volatiles emitted by uninfested and insect-infested cucumber (Cucumis sativus) and potato (Solanum tuberosum) plants. Cucumber plants were infested by the phloem-feeding aphid Aphis gossypii, the leaf chewer Mamestra brassicae or simultaneously by both insects. Potato plants were infested by either Aphis gossypii, by the leaf chewer Chrysodeixis chalcites or both. In olfactometer experiments, ants preferred volatile blends emitted by cucumber plants infested with M. brassicae caterpillars alone or combined with A. gossypii to volatiles of undamaged plants or plants damaged by A. gossypii only. No preference was recorded in choice tests between volatiles released by aphid-infested plants over undamaged plants. Volatiles emitted by potato plants infested by either C. chalcites or A. gossypii were preferred by ants over volatiles released by undamaged plants. Ants did not discriminate between potato plants infested with aphids and caterpillars over plants infested with aphids only. Plant headspace composition showed qualitative and/or quantitative differences between herbivore treatments. Multivariate analysis revealed clear separation between uninfested and infested plants and among herbivore treatments. The importance of HIPVs in indirect plant defence by ants is discussed in the context of the ecology of ant-plant interactions and possible roles of ants in pest management.


Assuntos
Formigas/fisiologia , Afídeos/fisiologia , Cucumis sativus/fisiologia , Herbivoria , Lepidópteros/fisiologia , Solanum tuberosum/fisiologia , Compostos Orgânicos Voláteis/metabolismo , Animais , Odorantes/análise , Comportamento Predatório , Compostos Orgânicos Voláteis/análise
12.
New Phytol ; 212(4): 1057-1071, 2016 Dec.
Artigo em Inglês | MEDLINE | ID: mdl-27689843

RESUMO

Under conditions of competition for light, which lead to the inactivation of the photoreceptor phytochrome B (phyB), the growth of shade-intolerant plants is promoted and the accumulation of direct anti-herbivore defenses is down-regulated. Little is known about the effects of phyB on emissions of volatile organic compounds (VOCs), which play a major role as informational cues in indirect defense. We investigated the effects of phyB on direct and indirect defenses in tomato (Solanum lycopersicum) using two complementary approaches to inactivate phyB: illumination with a low red to far-red ratio, simulating competition, and mutation of the two PHYB genes present in the tomato genome. Inactivation of phyB resulted in low levels of constitutive defenses and down-regulation of direct defenses induced by methyl jasmonate (MeJA). Interestingly, phyB inactivation also had large effects on the blends of VOCs induced by MeJA. Moreover, in two-choice bioassays using MeJA-induced plants, the predatory mirid bug Macrolophus pygmaeus preferred VOCs from plants in which phyB was inactivated over VOCs from control plants. These results suggest that, in addition to repressing direct defense, phyB inactivation has consequences for VOC-mediated tritrophic interactions in canopies, presumably attracting predators to less defended plants, where they are likely to find more abundant prey.


Assuntos
Herbivoria , Fitocromo B/metabolismo , Comportamento Predatório , Solanum lycopersicum/metabolismo , Solanum lycopersicum/parasitologia , Compostos Orgânicos Voláteis/metabolismo , Animais , Ciclopentanos/farmacologia , Análise Discriminante , Regulação da Expressão Gênica de Plantas/efeitos dos fármacos , Análise dos Mínimos Quadrados , Lepidópteros/fisiologia , Solanum lycopersicum/genética , Solanum lycopersicum/imunologia , Oxilipinas/farmacologia , Folhas de Planta/efeitos dos fármacos , Folhas de Planta/fisiologia , Tricomas/ultraestrutura
13.
Int J Mol Sci ; 17(8)2016 Aug 03.
Artigo em Inglês | MEDLINE | ID: mdl-27527153

RESUMO

Experience of insect herbivores and their natural enemies in the natal habitat is considered to affect their likelihood of accepting a similar habitat or plant/host during dispersal. Growing phenology of food plants and the number of generations in the insects further determines lability of insect behavioural responses at eclosion. We studied the effect of rearing history on oviposition preference in a multivoltine herbivore (Pieris brassicae), and foraging behaviour in the endoparasitoid wasp (Cotesia glomerata) a specialist enemy of P. brassicae. Different generations of the insects are obligatorily associated with different plants in the Brassicaceae, e.g., Brassica rapa, Brassica nigra and Sinapis arvensis, exhibiting different seasonal phenologies in The Netherlands. Food plant preference of adults was examined when the insects had been reared on each of the three plant species for one generation. Rearing history only marginally affected oviposition preference of P. brassicae butterflies, but they never preferred the plant on which they had been reared. C. glomerata had a clear preference for host-infested B. rapa plants, irrespective of rearing history. Higher levels of the glucosinolate breakdown product 3-butenyl isothiocyanate in the headspace of B. rapa plants could explain enhanced attractiveness. Our results reveal the potential importance of flexible plant choice for female multivoltine insects in nature.


Assuntos
Brassica rapa/metabolismo , Borboletas/fisiologia , Mostardeira/metabolismo , Vespas/fisiologia , Distribuição Animal , Animais , Borboletas/parasitologia , Feminino , Voo Animal , Preferências Alimentares , Herbivoria , Interações Hospedeiro-Parasita , Masculino , Oviposição
14.
Mol Ecol ; 24(11): 2886-99, 2015 Jun.
Artigo em Inglês | MEDLINE | ID: mdl-25789566

RESUMO

Foraging success of predators profoundly depends on reliable and detectable cues indicating the presence of their often inconspicuous prey. Carnivorous insects rely on chemical cues to optimize foraging efficiency. Hyperparasitoids that lay their eggs in the larvae or pupae of parasitic wasps may find their parasitoid hosts developing in different herbivores. They can use herbivore-induced plant volatiles (HIPVs) to locate parasitized caterpillars. Because different herbivore species induce different HIPV emission from plants, hyperparasitoids may have to deal with large variation in volatile information that indicates host presence. In this study, we used an ecogenomics approach to first address whether parasitized caterpillars of two herbivore species (Pieris rapae and P. brassicae) induce similar transcriptional and metabolomic responses in wild Brassica oleracea plants and, second, whether hyperparasitoids Lysibia nana are able to discriminate between these induced plant responses to locate their parasitoid host in different herbivores under both laboratory and field conditions. Our study revealed that both herbivore identity and parasitism affect plant transcriptional and metabolic responses to herbivory. We also found that hyperparasitoids are able to respond to HIPVs released by wild B. oleracea under both laboratory and field conditions. In addition, we observed stronger attraction of hyperparasitoids to HIPVs when plants were infested with parasitized caterpillars. However, hyperparasitoids were equally attracted to plants infested by either herbivore species. Our results indicate that parasitism plays a major role in HIPV-mediated plant-hyperparasitoid interactions. Furthermore, these findings also indicate that plant trait-mediated indirect interaction networks play important roles in community-wide species interactions.


Assuntos
Borboletas/parasitologia , Herbivoria , Interações Hospedeiro-Parasita , Compostos Orgânicos Voláteis/química , Vespas/fisiologia , Animais , Brassica/química , Brassica/genética , Borboletas/fisiologia , Cadeia Alimentar , Regulação da Expressão Gênica de Plantas , Larva/parasitologia
15.
PLoS Biol ; 10(11): e1001435, 2012.
Artigo em Inglês | MEDLINE | ID: mdl-23209379

RESUMO

Plants respond to herbivory with the emission of induced plant volatiles. These volatiles may attract parasitic wasps (parasitoids) that attack the herbivores. Although in this sense the emission of volatiles has been hypothesized to be beneficial to the plant, it is still debated whether this is also the case under natural conditions because other organisms such as herbivores also respond to the emitted volatiles. One important group of organisms, the enemies of parasitoids, hyperparasitoids, has not been included in this debate because little is known about their foraging behaviour. Here, we address whether hyperparasitoids use herbivore-induced plant volatiles to locate their host. We show that hyperparasitoids find their victims through herbivore-induced plant volatiles emitted in response to attack by caterpillars that in turn had been parasitized by primary parasitoids. Moreover, only one of two species of parasitoids affected herbivore-induced plant volatiles resulting in the attraction of more hyperparasitoids than volatiles from plants damaged by healthy caterpillars. This resulted in higher levels of hyperparasitism of the parasitoid that indirectly gave away its presence through its effect on plant odours induced by its caterpillar host. Here, we provide evidence for a role of compounds in the oral secretion of parasitized caterpillars that induce these changes in plant volatile emission. Our results demonstrate that the effects of herbivore-induced plant volatiles should be placed in a community-wide perspective that includes species in the fourth trophic level to improve our understanding of the ecological functions of volatile release by plants. Furthermore, these findings suggest that the impact of species in the fourth trophic level should also be considered when developing Integrated Pest Management strategies aimed at optimizing the control of insect pests using parasitoids.


Assuntos
Brassica/química , Borboletas/parasitologia , Herbivoria , Compostos Orgânicos Voláteis/química , Vespas/fisiologia , Animais , Tamanho Corporal , Brassica/fisiologia , Borboletas/fisiologia , Tamanho da Ninhada , Ecossistema , Feminino , Larva/fisiologia , Masculino , Odorantes , Oviposição , Especificidade da Espécie , Volatilização
16.
Oecologia ; 177(3): 701-713, 2015 Mar.
Artigo em Inglês | MEDLINE | ID: mdl-25370387

RESUMO

One of the main abiotic stresses that strongly affects plant survival and the primary cause of crop loss around the world is drought. Drought stress leads to sequential morphological, physiological, biochemical and molecular changes that can have severe effects on plant growth, development and productivity. As a consequence of these changes, the interaction between plants and insects can be altered. Using cultivated Brassica oleracea plants, the parasitoid Microplitis mediator and its herbivorous host Mamestra brassicae, we studied the effect of drought stress on (1) the emission of plant volatile organic compounds (VOCs), (2) plant hormone titres, (3) preference and performance of the herbivore, and (4) preference of the parasitoid. Higher levels of jasmonic acid (JA) and abscisic acid (ABA) were recorded in response to herbivory, but no significant differences were observed for salicylic acid (SA) and indole-3-acetic acid (IAA). Drought significantly impacted SA level and showed a significant interactive effect with herbivory for IAA levels. A total of 55 VOCs were recorded and the difference among the treatments was influenced largely by herbivory, where the emission rate of fatty acid-derived volatiles, nitriles and (E)-4,8-dimethylnona-1,3,7-triene [(E)-DMNT] was enhanced. Mamestra brassicae moths preferred to lay eggs on drought-stressed over control plants; their offspring performed similarly on plants of both treatments. VOCs due to drought did not affect the choice of M. mediator parasitoids. Overall, our study reveals an influence of drought on plant chemistry and insect-plant interactions.


Assuntos
Brassica/parasitologia , Secas , Herbivoria , Mariposas/parasitologia , Reguladores de Crescimento de Plantas/metabolismo , Estresse Fisiológico , Compostos Orgânicos Voláteis/metabolismo , Ácido Abscísico/metabolismo , Animais , Brassica/metabolismo , Brassica/fisiologia , Ciclopentanos/metabolismo , Interações Hospedeiro-Parasita , Himenópteros/fisiologia , Ácidos Indolacéticos/metabolismo , Oxilipinas/metabolismo , Doenças das Plantas/parasitologia , Ácido Salicílico/metabolismo
17.
Oecologia ; 179(1): 163-74, 2015 Sep.
Artigo em Inglês | MEDLINE | ID: mdl-25953114

RESUMO

In response to insect herbivory, plants emit volatile organic compounds which may act as indirect plant defenses by attracting natural enemies of the attacking herbivore. In nature, plants are often attacked by multiple herbivores, but the majority of studies which have investigated indirect plant defenses to date have focused on the recruitment of different parasitoid species in a single-herbivore context. Here, we report our investigation on the attraction of egg parasitoids of lepidopteran hosts (Trichogramma brassicae and T. evanescens) toward plant volatiles induced by different insect herbivores in olfactometer bioassays. We used a system consisting of a native crucifer, Brassica nigra, two naturally associated herbivores [the butterfly Pieris brassicae (eggs and caterpillars) and the aphid Brevicoryne brassicae] and an alien invasive herbivore (eggs and caterpillars of the moth Spodoptera exigua). We found that Trichogramma wasps were attracted by volatiles induced in the plants by P. brassicae eggs, but not by those induced in the plants 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 egg-killing parasitoids.


Assuntos
Borboletas/fisiologia , Herbivoria , Mostardeira/química , Feromônios/química , Spodoptera/parasitologia , Compostos Orgânicos Voláteis/química , Vespas/fisiologia , Animais , Comportamento Alimentar/fisiologia , Interações Hospedeiro-Parasita , Larva/parasitologia , Larva/fisiologia , Mostardeira/parasitologia , Óvulo/parasitologia , Óvulo/fisiologia , Spodoptera/fisiologia
18.
Oecologia ; 178(4): 1169-80, 2015 Aug.
Artigo em Inglês | MEDLINE | ID: mdl-25783487

RESUMO

Beneficial root-associated microbes modify the physiological status of their host plants and affect direct and indirect plant defense against insect herbivores. While the effects of these microbes on direct plant defense against insect herbivores are well described, knowledge of the effect of the microbes on indirect plant defense against insect herbivores is still limited. In this study, we evaluate the role of the rhizobacterium Pseudomonas fluorescens WCS417r in indirect plant defense against the generalist leaf-chewing insect Mamestra brassicae through a combination of behavioral, chemical, and gene-transcriptional approaches. We show that rhizobacterial colonization of Arabidopsis thaliana roots results in an increased attraction of the parasitoid Microplitis mediator to caterpillar-infested plants. Volatile analysis revealed that rhizobacterial colonization suppressed the emission of the terpene (E)-α-bergamotene and the aromatics methyl salicylate and lilial in response to caterpillar feeding. Rhizobacterial colonization decreased the caterpillar-induced transcription of the terpene synthase genes TPS03 and TPS04. Rhizobacteria enhanced both the growth and the indirect defense of plants under caterpillar attack. This study shows that rhizobacteria have a high potential to enhance the biocontrol of leaf-chewing herbivores based on enhanced attraction of parasitoids.


Assuntos
Herbivoria , Mariposas/parasitologia , Raízes de Plantas/microbiologia , Pseudomonas fluorescens/fisiologia , Vespas/fisiologia , Alquil e Aril Transferases/metabolismo , Animais , Arabidopsis , Compostos Bicíclicos com Pontes/metabolismo , Feminino , Larva/parasitologia , Masculino , Folhas de Planta , Simbiose , Compostos Orgânicos Voláteis/metabolismo
19.
Oecologia ; 177(2): 477-86, 2015 Feb.
Artigo em Inglês | MEDLINE | ID: mdl-25273955

RESUMO

Animals use information from their environment while foraging for food or prey. When parasitic wasps forage for hosts, they use plant volatiles induced by herbivore activities such as feeding and oviposition. Little information is available on how wasps exploit specific plant volatiles over time, and which compounds indicate changes in host quality. In experiments investigating the role of herbivore-induced plant volatiles in wasp foraging, induction of plant response is usually achieved by placing larvae on clean plants instead of allowing the natural sequence of events: to let eggs deposited by the herbivore develop into larvae. We compared the attraction of the parasitoid Cotesia glomerata to volatiles emitted by black mustard (Brassica nigra) plants induced by eggs and successive larval stages of the Large Cabbage White butterfly (Pieris brassicae) to the attraction of this parasitoid to black mustard plant volatiles induced only by larval feeding in a wind tunnel setup. We show that wasps are attracted to plants infested with eggs just before and shortly after larval hatching. However, wasp preference changed at later time points towards plants induced only by larval feeding. These temporal changes in parasitoid attraction matched with changes in the chemical compositions of the blends of plant volatiles. Previous studies have shown that host quality/suitability decreases with caterpillar age and that P. brassicae oviposition induces plant defences that negatively affect subsequently feeding caterpillars. We investigated parasitoid performance in hosts of different ages. Wasp performance was positively correlated with preference. Moreover, parasitism success decreased with time and host stage. In conclusion, the behaviour of Cotesia glomerata is fine-tuned to exploit volatiles induced by eggs and early host stages that benefit parasitoid fitness.


Assuntos
Borboletas/parasitologia , Mostardeira/metabolismo , Comportamento Predatório/efeitos dos fármacos , Compostos Orgânicos Voláteis/farmacologia , Vespas/fisiologia , Animais , Borboletas/fisiologia , Feminino , Herbivoria , Interações Hospedeiro-Parasita , Larva/parasitologia , Larva/fisiologia , Mostardeira/química , Oviposição , Compostos Orgânicos Voláteis/química , Compostos Orgânicos Voláteis/isolamento & purificação , Vespas/efeitos dos fármacos , Vespas/crescimento & desenvolvimento
20.
J Chem Ecol ; 41(2): 187-93, 2015 Feb.
Artigo em Inglês | MEDLINE | ID: mdl-25612522

RESUMO

Proximate factors affecting animal behavior include stimuli generated by conspecifics. In spider mites of the genus Tetranychus (Acari: Tetranychidae), males guard pre-reproductive quiescent females, because only the first mating results in fertilization. In a dual-choice experiment, more adult males of T. urticae were attracted to females guarded by a male than to solitary females. Because spider mites are known to perceive volatiles, we hypothesized that guarded and solitary females differ in the volatile blends emitted. To test this hypothesis, headspace volatiles of guarded females, solitary females, and solitary males were collected, respectively. GC/MS analysis detected octanal, methyl salicylate, ethyl 4-ethoxybenzoate, and methyl cis-dihydrojasmonate in all of the groups. Orthogonal Projection to Latent Structures Discriminant Analysis (OPLS-DA) of the blends clearly discriminated guarded females from solitary females, supporting our hypothesis. Individual compounds did not show significant difference in emission rates for guarded females vs. solitary females, suggesting that differences lay in the total blend composition. OPLS-DA did not discriminate between the blends emitted by guarded females and solitary males. In conclusion, the differences in the volatile blends are likely to mediate male discrimination between guarded and solitary females.


Assuntos
Quimiotaxia , Comportamento Sexual Animal , Tetranychidae/fisiologia , Compostos Orgânicos Voláteis/metabolismo , Animais , Feminino , Cromatografia Gasosa-Espectrometria de Massas , Masculino
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