Attraction Of Parasitoids Research Articles

Variation in induced responses in volatile and non-volatile metabolites among six willow species: Do willow species share responses to herbivory?

Chemical variation is a critical aspect affecting performance among co-occurring plants. High chemical variation in metabolites with direct effects on insect herbivores supports chemical niche partitioning, and it can reduce the number of herbivores shared by co-occurring plant species. In contrast, low intraspecific variation in metabolites with indirect effects, such as induced volatile organic compounds (VOCs), may improve the attraction of specialist predators or parasitoids as they show high specificity to insect herbivores. We explored whether induced chemical variation following herbivory by various insect herbivores differs between VOCs vs. secondary non-volatile metabolites (non-VOCs) and salicinoids with direct effects on herbivores in six closely related willow species. Willow species identity explained most variation in VOCs (18.4%), secondary non-VOCs (41.1%) and salicinoids (60.7%). The variation explained by the independent effect of the herbivore treatment was higher in VOCs (2.8%) compared to secondary non-VOCs (0.5%) and salicinoids (0.5%). At the level of individual VOCs, willow species formed groups, as some responded similarly to the same herbivores. Most non-VOCs and salicinoids were upregulated by sap-suckers compared to other herbivore treatments and control across the willow species. In contrast, induced responses in non-VOCs and salicinoids to other herbivores largely differed between the willows. Our results suggest that induced responses broadly differ between various types of chemical defences, with VOCs and non-VOCs showing different levels of specificity and similarity across plant species. This may further contribute to flexible plant responses to herbivory and affect how closely related plants share or partition their chemical niches.

Drought aggravates plant stress by favouring aphids and weakening indirect defense in a sugar beet tritrophic system

AbstractClimate change leads to more frequent droughts that may alter multitrophic networks in agroecosystems by changing bottom-up and top-down effects on herbivorous insects. Yet, how bottom-up effects of drought alter tritrophic interactions remains poorly understood. This study investigated two intensities of drought stress in the tritrophic system consisting of sugar beet (Beta vulgaris), an aphid (Aphis fabae), and its parasitoid (Aphidius colemani). We thoroughly investigated each trophic level, examining the performance of plants, pest insects, and parasitoids, as well as the attraction of parasitoids to herbivore-induced plant volatiles (HIPVs). Drought stress negatively affected plant growth but benefited A. fabae, leading to faster development and a higher reproduction rate. Drought-stressed plants also emitted less plant volatiles, which resulted in reduced attraction of A. colemani to aphid-infested plants. Drought indirectly affected parasitoid performance, as evidenced by lower emergence rates and production of fewer females, although mummification rates were higher on drought-stressed plants. Reduced parasitoid attraction and performance on drought-stressed plants may exert lower top-down pressure on aphid populations. Combined with increased aphid performance, this may facilitate aphid outbreaks, which could further weaken drought-stressed plants. Our findings highlight the need to study multiple trophic levels and emphasize the importance of incorporating HIPVs and parasitoid attraction when assessing combined abiotic and biotic stresses in crops.

Differential effects of plant-beneficial fungi on the attraction of the egg parasitoid Trissolcus basalisin response to Nezara viridula egg deposition.

There is increasing evidence that plant-associated microorganisms play important roles in defending plants against insect herbivores through both direct and indirect mechanisms. While previous research has shown that these microbes can modify the behaviour and performance of insect herbivores and their natural enemies, little is known about their effect on egg parasitoids which utilize oviposition-induced plant volatiles to locate their hosts. In this study, we investigated how root inoculation of sweet pepper (Capsicum annuum) with the plant-beneficial fungi Beauveria bassiana ARSEF 3097 or Trichoderma harzianum T22 influences the olfactory behaviour of the egg parasitoid Trissolcus basalis following egg deposition by its host Nezara viridula. Olfactometer assays showed that inoculation by T. harzianum significantly enhanced the attraction of the egg parasitoid, while B. bassiana had the opposite effect. However, no variation was observed in the chemical composition of plant volatiles. Additionally, fitness-related traits of the parasitoids (wasp body size) were not altered by any of the two fungi, suggesting that fungal inoculation did not indirectly affect host quality. Altogether, our results indicate that plant inoculation with T. harzianum T22 can be used to enhance attraction of egg parasitoids, which could be a promising strategy in manipulating early plant responses against pest species and improving sustainable crop protection. From a more fundamental point of view, our findings highlight the importance of taking into account the role of microorganisms when studying the intricate interactions between plants, herbivores and their associated egg parasitoids.

Aphid-Induced Volatiles and Subsequent Attraction of Natural Enemies Varies among Sorghum Cultivars.

The production of herbivore-induced plant volatiles (HIPVs) is a type of indirect defense used by plants to attract natural enemies and reduce herbivory by insect pests. In many crops little is known about genotypic variation in HIPV production or how this may affect natural enemy attraction. In this study, we identified and quantified HIPVs produced by 10 sorghum (Sorghum bicolor) cultivars infested with a prominent aphid pest, the sorghum aphid (Melanaphis sorghi Theobald). Volatiles were collected using dynamic headspace sampling techniques and identified and quantified using GC-MS. The total amounts of volatiles induced by the aphids did not differ among the 10 cultivars, but overall blends of volatiles differed significantly in composition. Most notably, aphid herbivory induced higher levels of methyl salicylate (MeSA) emission in two cultivars, whereas in four cultivars, the volatile emissions did not change in response to aphid infestation. Dual-choice olfactometer assays were used to determine preference of the aphid parasitoid, Aphelinus nigritus, and predator, Chrysoperla rufilabris, between plants of the same cultivar that were un-infested or infested with aphids. Two aphid-infested cultivars were preferred by natural enemies, while four other cultivars were more attractive to natural enemies when they were free of aphids. The remaining four cultivars elicited no response from parasitoids. Our work suggests that genetic variation in HIPV emissions greatly affects parasitoid and predator attraction to aphid-infested sorghum and that screening crop cultivars for specific predator and parasitoid attractants has the potential to improve the efficacy of biological control.

Enhanced parasitisation of caterpillars and aphids on field‐grown Brassica oleracea plants upon soil amendment with insect exuviae

Abstract Multitrophic plant–insect interactions are mediated by plant volatiles. The emission of herbivore‐induced plant volatiles is influenced by environmental conditions, such as soil microbes and nutrient composition, with consequences for above‐ground trophic interactions. Here, we investigated whether insect exuviae in the soil alter the plant's volatile blend and attraction of parasitoids in the laboratory and whether this attraction also occurs in the field. We studied the effects of soil amendment with exuviae originating from three insect species, Tenebrio molitor, Acheta domesticus and Hermetia illucens, on the proportion of parasitised Plutella xylostella caterpillars and Brevicoryne brassicae aphids in the field in three consecutive years. In the laboratory, we collected and analysed the volatile blend of amended plants infested with caterpillars or aphids. The attraction of the parasitoids Diadegma semiclausum and Diaeretiella rapae, respectively, towards these volatile blends was assessed in an olfactometer. Our study shows that insect exuviae‐amended soil enhanced the proportion of parasitised herbivores of two species in the field. Relative amounts of several components of the plant volatile blend were affected by soil amendment. Soil amendment with Acheta domesticus or Tenebrio molitor exuviae resulted in an increased attraction of the two parasitoid species in the olfactometer. Soil amendment with insect exuviae altered the plant volatile blend leading to enhanced attraction of parasitoids in laboratory assays. These effects were sustained under the complex and variable biotic and abiotic conditions in the field. Our results underline the importance of belowground processes, such as the decomposition of insect exuviae, on aboveground volatile‐mediated multitrophic interactions. Read the free Plain Language Summary for this article on the Journal blog.

Surviving the serenade: how conflicting selection pressures shape the early stages of sexual signal diversification.

Understanding how the early stages of sexual signal diversification proceed is critically important because these microevolutionary dynamics directly shape species trajectories and impact macroevolutionary patterns. Unfortunately, studying this is challenging because signals involve complex interactions between behavior, morphology, and physiology, much of which can only be measured in real-time. In Hawaii, male Pacific field cricket song attracts both females and a deadly parasitoid fly. Over the past two decades, there has been a marked increase in signal variation in Hawaiian populations of these crickets, including novel male morphs with distinct mating songs. We capitalize on this rare opportunity to track changes in morph composition over time in a population with three novel morphs, investigating how mate and parasitoid attraction (components of sexual and natural selection) may shape signal evolution. We find dramatic fluctuation in morph proportions over the three years of the study, including the arrival and rapid increase of one novel morph. Natural and sexual selection pressures act differently among morphs, with some more attractive to mates and others more protected from parasitism. Collectively, our results suggest that differential protection from parasitism among morphs, rather than mate attraction, aligns with recent patterns of phenotypic change in the wild.

Direct and indirect host‐related volatile compounds attract a fruit fly parasitoid, Diachasmimorpha longicaudata

AbstractFruit fly pests (Diptera: Tephritidae) are a serious problem for fruit production and for local and international trade. Biological control is increasingly included as a pest control tool within integrated pest management (IPM) programmes, seeking to reduce pesticides and improve fruit quality. Ceratitis capitata Wiedemann, the Mediterranean fruit fly (medfly), is probably the most damaging fruit fly pest, with a global distribution and more than 200 host species. The solitary larval endoparasitoid Diachasmimorpha longicaudata Ashmead (Hymenoptera: Braconidae) is a biocontrol agent widely used against Tephritidae fruit fly pests. Previous studies showed that female wasps locate host larvae using visual, mechanical, and chemical cues. Here, we investigated the chemical basis of female parasitoid attraction to cues that guide D. longicaudata to the host, and thus unveil volatile organic compounds that might be used in IPM programmes. Female orientation to chemical cues was tested in a Y‐tube olfactometer, where attraction to C. capitata‐infested oranges, oranges with residues of larval activity, oranges infected with a green mould, and overripe oranges was confirmed. Volatiles from all these types of fruit were collected and used in gas chromatography‐electroantennographic detection (GC‐EAD) and GC‐mass spectrometry (MS) analyses. These studies allowed us to identify six candidate compounds that were present in all treated oranges but not in the control fruit (ripe and uninfested oranges): D‐limonene, acetophenone, linalool, nonanal, decanal, and eugenol. Electroantennography (EAG) showed that acetophenone, nonanal, and decanal triggered dose‐dependent responses, suggesting a relevant role in the process of host finding. Although responses to D‐limonene, linalool, and eugenol were independent of the dose, they could be involved in host location in areas with high probability of host presence. The fact that these six compounds are shared by the four behaviourally attractive sources opens new possibilities for the development of novel tools to improve biocontrol programmes.

Effects of root inoculation of entomopathogenic fungi on olfactory-mediated behavior and life-history traits of the parasitoid Aphidius ervi (Haliday) (Hymenoptera: Braconidae).

Although most biological control programs use multiple biological agents to manage pest species, to date only a few programs have combined the use of agents from different guilds. Using sweet pepper (Capsicum annuum L.), the entomopathogenic fungus Akanthomyces muscarius ARSEF 5128, the tobacco peach aphid Myzus persicae var. nicotianae and the aphid parasitoid Aphidius ervi as the experimental model, we explored whether root inoculation with an entomopathogenic fungus is compatible with parasitoid wasps for enhanced biocontrol of aphids. In dual-choice behavior experiments, A. ervi was significantly attracted to the odor of M. persicae-infested C. annuum plants that had been inoculated with A. muscarius, compared to noninoculated infested plants. There was no significant difference in attraction to the odor of uninfested plants. Myzus persicae-infested plants inoculated with A. muscarius emitted significantly higher amounts of indole, (E)-nerolidol, (3E,7E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene and one unidentified terpene compared to noninoculated infested plants. Coupled gas chromatography-electroantennography, using the antennae of A. ervi, confirmed the physiological activity of these elevated compounds. Inoculation of plants with A. muscarius did not affect parasitism rate nor parasitoid longevity, but significantly increased the speed of mummy formation in parasitized aphids on fungus-inoculated plants. Our data suggest that root inoculation of C. annuum with A. muscarius ARSEF 5128 alters the olfactory-mediated behavior of parasitoids, but has little effect on parasitism efficiency or life-history parameters. However, increased attraction of parasitoids towards M. persicae-infested plants when inoculated by entomopathogenic fungi can accelerate host localization and hence improve biocontrol efficacy. © 2023 Society of Chemical Industry.

The effects of plants domestication on the foraging and performance of parasitoids.

Domestication-related changes in the chemical traits of crop plants affect parasitoid foraging success, development, and survival. For example, herbivore-induced changes in the production of volatiles by domesticated plants can enhance or reduce parasitoid attraction. While the trade-off between nutrient content and chemical defense in cultivated plants can increase the suitability of hosts for parasitoids, their increased health and size can positively affect their immune response against parasitoids. Overall, plant domestication is expected to significantly affect their relationship with parasitoids due to altered plant morphology, physical characteristics, chemical defenses, and new plant associations. This review highlights the need for research on the effects of plant domestication on host-parasitoid interactions in the interest of better controlling insect pests.

Mechanical Branch Wounding Alters the BVOC Emission Patterns of Ficus Plants

Tree leaves emit biogenic volatile organic compounds (BVOCs) in response to mechanical wounding by insect folivores. However, BVOCs are also released from leaves in response to damage to other tree organs. In this study, we hypothesized that if trees utilize BVOCs to defend against leaf herbivory, BVOCs emitted in response to leaf wounding would be different from those emitted in response to other types of mechanical damage. To test this hypothesis, we measured BVOCs emitted from the leaves of four Ficus species in response to leaf-cutting, branch-cutting, leaf-branch-cutting, and control (constitutive BVOCs). We found that leaf-cutting triggered the emission of BVOCs, but their emission patterns were species-specific, and the overall BVOC composition did not significantly differ from that of constitutive BVOCs. In contrast, branch-cutting triggered the emission of many BVOCs, some known as parasitoid attractants and herbivore deterrents. Our study suggests that plant defense mediated by BVOCs is highly species-specific and not effective for attracting herbivore enemies when unrelated disturbances such as tree falls and windstorms occur. Additionally, we recommend avoiding ex situ BVOC sampling of cut plants, as this method alters BVOC emission patterns from both intact and damaged leaves.

Tomato Varieties Influence the Performance of Tamarixia triozae (Hymenoptera: Eulophidae) on Bactericera cockerelli (Hemiptera: Triozidae) Nymphs.

Simple SummaryHorticultural crops are often exposed to insect attacks, and insect vectors of plant diseases represent a significant agronomical challenge. The tomato psyllid is a principal vector for bacterial pathogens causing disease and economic losses in crops. In the present study, we evaluated the performance of the parasitoid (T. triozae) against tomato psyllid on tomato varieties. Our results showed that parasitoids selected one commercial variety of tomato plants and attacked the psyllid under greenhouse conditions. We also demonstrated that healthy plants of commercial variety attracted more natural enemies under laboratory conditions. Therefore, these results could help fine-tune the release of natural enemies in greenhouse and field crops.The potato/tomato psyllid Bactericera cockerelli is the Candidatus Liberibacter solanacearum bacterium vector that causes diseases in Solanaceae crops. Pest control is based on synthetic chemical insecticides, plant extracts, and natural enemies such as parasitoids. Tamarixia triozae feeds on nymphs of B. cockerelli, reaching up to 95% parasitism. This work aimed to evaluate the parasitic performance of T. triozae on tomato leaves with B. cockerelli N3 nymphs, using two domesticated (Floradade and Micro-Tom) and one Wild tomato variety. Several assays were completed to identify the parasitoid attraction toward un-infested plants (healthy) and infested plants (damaged) of three varieties. Parasitism preference and “Y” tube olfactometer tests were performed, respectively. The parasitism of Tamarixia triozae showed a preference toward plants of the Floradade variety by 44% compared with the other two varieties (p = 0.0003). T. triozae was more attracted to damaged plants of the Wild variety (p = 0.0523). Healthy plants of Floradade and Micro-Tom varieties attracted a higher proportion of parasitoids, except in the Wild variety, where T. triozae was more attracted to damaged plants. Taken together, the results of this study show that the domestication degree in tomato plants positively influenced the interactions between tomato plants and the parasitoid, T. triozae.

Evaluation and optimization of blends for attracting Trichogramma dendrolimi based on semiochemicals mediating tritrophic interactions in the orchard habitat

Trichogramma dendrolimi Matsumura (Hymenoptera: Trichogrammatidae) is one of the most important parasitic natural enemies of Grapholita molesta (Busck) (Lepidoptera: Tortricidae) in peach and pear orchards. The artificial rearing T. dendrolimi have been widely used in biological control programs in recent years. However, its actual parasitic effect on the pest in the field is less, so it is important to develop attractants to increase the parasitic efficiency of the parasitoids. T. dendrolimi can be easily attracted by semiochemicals derived from flowers, intact plants, herbivore-attacked plants, and insects in its orchard habitats. In this paper, 73 semiochemicals were evaluated as potential attractants at three concentrations (0.1 mg/mL, 1 mg/mL, and 10 mg/mL) to T. dendrolimi by Y-tube olfactometer bioassays and Electroantennogram (EAG) technology, and then the mixtures of active individual compounds were further tested and evaluated in the field. As a result, 17 individual compounds showed attractive bioactivity to T. dendrolimi. Interestingly, when methyl salicylate and benzaldehyde mixed with linalool oxide or cis-3-hexenyl caproate in a volume ratio of 10:3:3 respectively showed excellent attractant bioactivity for T. dendrolimi in the orchard field. Thus, introducing such parasitoid attractants in orchard habitat may improve the biological control effect to pests.

Plant Volatiles and Herbivore Induced Plant Volatiles from Chili Pepper Act as Attractant of the Aphid Parasitoid Aphelinus varipes (Hymenoptera: Aphelinidae).

Plants have evolved a number of different chemical defenses, covering nearly all classes of (secondary) metabolites, that represent a major barrier to herbivory: some are constitutive; others are induced after attacks from herbivores (HIPVs) and may elicit the attraction of predators and parasitoids. Here, we studied how the female solitary endoparasitoid Aphelinus varipes responds to plant and host aphid volatiles in a series of experiments on five commercially important vegetables that were either healthy or infested with the aphid Myzus persicae: chili pepper, eggplant, crown daisy, Chinese cabbage and cabbage. The results for the olfactory responses of A. varipes showed that the presence of M. persicae increased the attraction of the endoparasitoid to the infested plants. In a second experiment, volatiles from highly attractive and repellent plants were obtained via headspace collection to investigate volatiles from healthy and aphid-damaged plants. The results for the differences in volatile profiles in response to aphid infestation in chili pepper cultivar were dominated by the volatile blends, including α-pinene, decanal and phthalic acid, while in cabbage they were dominated by isophorone. Moreover, when HIPVs with different concentrations were compared, α-pinene at a dose rate of 100 ng/μL attracted more parasitoids, and the comparison was useful to understand the mechanisms of plant secondary volatiles during aphid infestation and to provide new resources to control this insect pest. Overall our study shows how HIPVs can bolster tritrophic interactions by enhancing the attractiveness of parasitoids.

UV light attracts Diaphorina citri and its parasitoid

Diaphorina citri Kuwayama (Hemiptera: Psyllidae) transmits the bacteria associated with Huanglongbing, an incurable and lethal disease affecting citrus productivity and fruit quality worldwide. This vector is prominently phototactic and uses visual cues to find host plants. Yellow sticky traps are used for its monitoring, but their efficiency is limited, especially at low population densities. Diaphorina citri can be captured at night when light is provided and it is attracted to UV light. One way to increase the attraction of D. citri is therefore combining sticky traps with LEDs of specific colors at night, but more information about attractiveness of UV and colors combined with UV is needed. Moreover, information on the attraction of the main parasitoid of D. citri, Tamarixia radiata Waterson (Hymenoptera: Eulophidae) to UV and other light colors is lacking. We examined the attraction of males and females of D. citri to LED lights of different colors but comparable intensities separately or combined with ultraviolet (UV). The non-UV colors alone did not differ in attractiveness, whereas green, light blue and red light became more attractive when combined with UV. However, none of these color combinations were more attractive than UV alone. The parasitoid T. radiata was also attracted to UV LEDs. Female parasitoids were equally attracted to UV during day and night, but males were more attracted at night. These results suggest that the effectiveness of the commonly used yellow sticky traps can be increased by combining them with UV LEDs at night, and the parasitoid of D. citri may also be attracted. On the one hand, attraction of parasitoids to the traps may help monitoring their presence, but on the other hand, it may affect biological control by this natural enemy.

A parasitoid's dilemma between food and host resources: the role of volatiles from nectar-providing marigolds and host-infested plants attracting Aphidius platensis.

The use of nectar-producing companion plants in crops is a well-known strategy of conserving natural enemies in biological control. However, the role of floral volatiles in attracting parasitoids and effects on host location via herbivore-induced plant volatiles is poorly known. Here, we examined the role of floral volatiles from marigold (Tagetes erecta), alone or in combination with volatiles from sweet pepper plant (Capsicum annuum), in recruiting Aphidius platensis, an important parasitoid of the green peach aphid Myzus persicae. We also investigated whether marigold floral volatiles are more attractive to the parasitoid than those emitted by sweet pepper plants infested by M. persicae. Olfactometry assays indicated that floral volatiles attracted A. platensis to the marigold plant and are more attractive than sweet pepper plant volatiles. However, volatiles emitted by aphid-infested sweet pepper were as attractive to the parasitoid as those of uninfested or aphid-infested blooming marigold. The composition of volatile blends released by uninfested and aphid-infested plants differed between both blooming marigold and sweet pepper, but the parasitoid did not discriminate aphid-infested from uninfested blooming marigold. Volatile released from blooming marigold and sweet pepper shared several compounds, but that of blooming marigold contained larger amounts of fatty-acid derivatives and a different composition of terpenes. We discuss the potential implications of the aphid parasitoid attraction in a diversified crop management strategy.

Cooperative herbivory between two important pests of rice

Normally, when different species of herbivorous arthropods feed on the same plant this leads to fitness-reducing competition. We found this to be different for two of Asia’s most destructive rice pests, the brown planthopper and the rice striped stem borer. Both insects directly and indirectly benefit from jointly attacking the same host plant. Double infestation improved host plant quality, particularly for the stemborer because the planthopper fully suppresses caterpillar-induced production of proteinase inhibitors. It also reduced the risk of egg parasitism, due to diminished parasitoid attraction. Females of both pests have adapted their oviposition behaviour accordingly. Their strong preference for plants infested by the other species even overrides their avoidance of plants already attacked by conspecifics. This cooperation between herbivores is telling of adaptations resulting from the evolution of plant-insect interactions, and points out mechanistic vulnerabilities that can be targeted to control these major pests.

Aphids Facing Their Parasitoids: A First Look at How Chemical Signals May Make Higher Densities of the Pea Aphid Acyrthosiphon pisum Less Attractive to the Parasitoid Aphidius ervi.

Simple SummarySuccessful foraging behavior of parasitoids depends on specific organic information emitted by host-infested plants. For instance, the emission of volatile compounds increases in infested plants, and these are the first indicator of host presence. Parasitoids are attracted by these volatiles in a quite specific way. By combining behavioral and chemical studies, we showed bottom-up effects in a broad bean Vicia faba (Fabaceae)–pea aphid Acyrthosiphon pisum (Homoptera: Aphididae)–parasitoid Aphidius ervi (Hymenoptera: Braconidae) model system. We found that behavioral selection of parasitoid females toward plants with a high density of aphid infestation was reduced, and this can be linked to reduced emission of volatile compounds. In practice, if parasitoids are less attracted to plants with high-density aphid infestations, there may be potential negative impacts on biological control. Therefore, the common recommendation in biological control is to release parasitoids early in the season when aphid density on crop plants is still low.Herbivore-induced plant volatiles constitute the first indicators of insect host presence, and these can affect the foraging behavior of their natural enemies. The density of insect hosts may affect the nature and concentration of these plant-induced volatiles. We tested the impact of infestation density (low, intermediate, and high) of the pea aphid, Acyrthosiphon pisum (Homoptera: Aphididae), feeding on the broad bean Vicia faba, on the attractiveness of the parasitoid Aphidius ervi (Hymenoptera: Braconidae), using a Y-tube olfactometer (infested vs. non-infested plants). The emitted volatile compounds from both infested and non-infested plants were collected and identified. In addition, two series of experiments were carried out to test the impact of the presence of a conspecific female parasitoid within the aphid/plant complex on the attractiveness to other females. Parasitoids were significantly more attracted to the plants with low and intermediate aphid infestation levels. The volatile blend composition of the infested plants changed in relation to aphid density and may explain the low attraction of parasitoids toward high aphid density. The presence of conspecific females on the aphid patch had no apparent impact on the behavioral choices of other parasitoid females. Our study adds a new aspect to understanding plant–aphid–parasitoid interactions, including the possibility that aphids may manipulate chemical cues of host plants affecting the orientation of parasitoids.

The Pupal Parasitoid Trichopria drosophilae Is Attracted to the Same Yeast Volatiles as Its Adult Host.

There is increasing evidence that microorganisms, particularly fungi and bacteria, emit volatile compounds that mediate the foraging behaviour of insects and therefore have the potential to affect key ecological relationships. However, to what extent microbial volatiles affect the olfactory response of insects across different trophic levels remains unclear. Adult parasitoids use a variety of chemical stimuli to locate potential hosts, including those emitted by the host's habitat, the host itself, and microorganisms associated with the host. Given the great capacity of parasitoids to utilize and learn odours to increase foraging success, parasitoids of eggs, larvae, or pupae may respond to the same volatiles the adult stage of their hosts use when locating their resources, but compelling evidence is still scarce. In this study, using Saccharomyces cerevisiae we show that Trichopria drosophilae, a pupal parasitoid of Drosophila species, is attracted to the same yeast volatiles as their hosts in the adult stage, i.e. acetate esters. Parasitoids significantly preferred the odour of S. cerevisiae over the blank medium in a Y-tube olfactometer. Deletion of the yeast ATF1 gene, encoding a key acetate ester synthase, decreased attraction of T. drosophilae, while the addition of synthetic acetate esters to the fermentation medium restored parasitoid attraction. Bioassays with individual compounds revealed that the esters alone were not as attractive as the volatile blend of S. cerevisiae, suggesting that other volatile compounds also contribute to the attraction of T. drosophilae. Altogether, our results indicate that pupal parasitoids respond to the same volatiles as the adult stage of their hosts, which may aid them in locating oviposition sites.

Multiple Attack to Inflorescences of an Annual Plant Does Not Interfere with the Attraction of Parasitoids and Pollinators

Plants in the flowering stage need to ensure reproduction by protecting themselves from attack and by preserving interactions with mutualist pollinators. When different plant mutualists are using the same type of cues, such as volatile compounds, attraction of parasitoids and pollinators may trade off. To explore this, we compared volatile emission of Brassica nigra plants in response to single or dual attack on their inflorescences. Additionally, we recorded flower visitation by pollinators and the attraction of parasitoids in the greenhouse and/or field. Brassica nigra were exposed in the flowering stage to one or two of the following three attackers: Brevicoryne brassicae aphids, Pieris brassicae caterpillars, and Xanthomonas campestris pv. raphani bacteria. We found that single attack by caterpillars, and dual attack by caterpillars plus aphids, induced the strongest changes in plant volatile emission. The caterpillars’ parasitoid C. glomerata did not exhibit preference for plants exposed to caterpillars only vs. plants exposed to caterpillars plus aphids or plus bacteria. However, the composition of the pollinator community associated with flowers of B. nigra was affected by plant exposure to the attackers, but the total number of pollinators visiting the plants did not change upon attack. We conclude that, when B. nigra were exposed to single or dual attack on their inflorescences, the plants maintained interactions with natural enemies of the insect attackers and with pollinators. We discuss how chemical diversity may contribute to plant resilience upon attack.

Exogenous application of plant hormones in the field alters aboveground plant\u2013insect responses and belowground nutrient availability, but does not lead to differences in plant\u2013soil feedbacks

Plant–soil feedbacks of plants that are exposed to herbivory have been shown to differ from those of plants that are not exposed to herbivores. Likely, this process is mediated by jasmonic acid (JA) and salicylic acid (SA) defense pathways, which are induced by aboveground herbivory. Furthermore, exogenous application of these phytohormones to plants alters belowground communities, but whether this changes plant–soil feedbacks in natural systems is unknown. We applied exogenous sprays of JA and SA individually and in combination to field plots in a restored grassland. Control plots were sprayed with demineralized water. After three repeated application rounds, we transplanted seedlings of the plant–soil feedback model plant Jacobaea vulgaris as phytometer plants to test the effects of potential phytohormone-mediated changes in the soil, on plant performance during the response phase. We further measured how exogenous application of phytohormones altered plant-related ecosystem characteristics (plot-level); soil chemistry, plot productivity, insect communities and predation. Biomass of the phytometer plants only co-varied with plot productivity, but was not influenced by phytohormone applications. However, we did observe compound-specific effects of SA application on insect communities, most notably on parasitoid attraction, and of JA application on soil nitrogen levels. Although we did not find effects on plant–soil feedbacks, the effects of exogenous application of phytohormones did alter other ecosystem-level processes related to soil nutrient cycling, which may lead to legacy effects in the longer term. Furthermore, exogenous application of phytohormones led to altered attraction of specific insect groups.