Biological activity and specificity of Miridae-induced plant volatiles

The ability of zoophytophagous predators to produce defensive plant responses due to their phytophagous behavior has been recently demonstrated. In the case of tomatoes, the mirids Nesidiocoris tenuis and Macrolophus pygmaeus are able to attract or repel pests and/or natural enemies in different ways. Nevertheless, the herbivore-induced plant volatiles (HIPVs) released by the phytophagy of both mirids, which are responsible for these behaviors, are unknown. In this work, the HIPVs produced by the plant feeding of N. tenuis and M. pygmaeus were characterized. In addition, the role of each HIPV in the repellence or attraction of two tomato pests, Bemisia tabaci and Tuta absoluta, and of the natural enemy Encarsia formosa was evaluated. Six green leaf volatiles (GLVs) plus methyl salicylate and octyl acetate clearly stood out as major differential peaks on the chromatogram in a directed analysis. The six GLV and methyl salicylate were repellent for B. tabaci and attractive to E. formosa, whereas they showed no effect on T. absoluta. Octyl acetate, which was significantly present only in the M. pygmaeus-punctured plants, was significantly attractive to T. absoluta, repellent to E. formosa and indifferent to B. tabaci. Unlike the remaining HIPVs, octyl acetate was emitted directly by M. pygmaeus and not by the plant. Our results showed that mirid herbivory could modulate the pest and natural plant enemy locations, since tomato plants release a blend of volatiles in response to this activity. These results could serve as a basis for future development of plant protection.     

What signals do herbivore-induced plant volatiles provide conspecific herbivores?

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 EAG-active 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.     

Responses of a predatory bug to a mixture of herbivore-induced plant volatiles from multiple plant species

The attractiveness of herbivore-induced plant volatiles (HIPVs) from a specific plant species to natural enemies has been well established. However, under natural conditions and polycultural agriculture systems, the interactions among trophic levels are thought to be more complex. For instance, complex mixtures of volatiles emitted from diverse host plant species infested by polyphagous herbivores might affect responses of natural enemies. In this study, we investigated whether a mixture of HIPVs emitted from herbivore-damaged multiple host plant species affect responses of a predatory bug. Therefore, we report (1) olfactory responses of the predatory bug (Orius strigicollis) to volatiles emitted from cotton bollworm (Helicoverpa armigera) first instar larvae-damaged multiple plant species (tomato, French bean and sweet corn), (2) chemical analyses of volatiles emitted from the three plant species exposed to different treatments and (3) olfactory responses of the predators to a reconstituted HIPV blend from multiple plant species based on chemical analyses. O. strigicollis significantly preferred volatiles emanating from H. armigera-damaged multiple plant species to volatiles emanating from a single plant species. In all the three plant species, H. armigera-damaged seedlings emitted significantly a greater amount of volatiles as well as a larger number of volatile compounds than an undamaged or a mechanically injured seedling. The predators preferred the reconstituted HIPVs from multiple plant species to the reconstituted HIPVs from a single plant species. Thus, the mixture of HIPVs from multiple plant species enhanced the attractiveness to the predators.     

A mixture of herbivore-induced plant volatiles from multiple host plant species enhances the attraction of a predatory bug under field-cage conditions

Plants respond to herbivore attack by emitting a blend of volatiles called herbivore-induced plant volatiles (HIPVs), which attract arthropod natural enemies. Under natural conditions and multiple cropping agriculture systems, natural enemies are thought to encounter a mixture of HIPVs emanating from multiple plant species. The effect of such a mixture of HIPVs on the responses of natural enemies under field conditions has not been explored. Our study assessed whether a mixture of HIPVs from multiple host plant species influenced predator responses in field-cage conditions. We investigated (1) foraging behaviors of a predatory bug, Orius strigicollis, on cotton bollworm (Helicoverpa armigera) larvae-infested multiple host plant species, and (2) the attractiveness of a mixture of reconstituted HIPVs from multiple plant species to O. strigicollis in outdoor cages. Significantly, greater numbers of predators were attracted to H. armigera-infested multiple plant species. The predators exterminated significantly greater numbers of H. armigera larvae with the multiple versus single plant species treatments. Significantly, greater numbers of O. strigicollis were captured on traps baited with the mixture of reconstituted HIPVs from multiple versus single plant species. The enhanced attractiveness of a mixture of HIPVs from multiple plant species to O. strigicollis might be the result of an additive effect of HIPVs from the three plant species when combined in a mixture.     

Invasive insect herbivores as disrupters of chemically-mediated tritrophic interactions: effects of herbivore density and parasitoid learning

Invasive insect herbivores have the potential to interfere with native multitrophic interactions by affecting the chemical cues emitted by plants and disrupting the attraction of natural enemies mediated by herbivore-induced plant volatiles (HIPVs). In a previous study, we found that the presence of the exotic herbivore Spodoptera littoralis on Brassica rapa plants infested by the native herbivore Pieris brassicae makes these dually-infested plants unattractive to the main parasitoid of P. brassicae, the braconid wasp Cotesia glomerata. Here we show that this interference by S. littoralis is strongly dependent on the relative densities of the two herbivores. Parasitoids were only deterred by dually-infested plants when there were more S. littoralis larvae than P. brassicae larvae on a plant. Furthermore, the blend of HIPVs emitted by dually-infested plants differed the most from HIPVs emitted by Pieris-infested plants when S. littoralis density exceeded P. brassicae density. We further found that associative learning by the parasitoid affected its preferences: attraction to dually-infested plants increased after parasitoids were presented a P. brassicae caterpillar (rewarding experience) in presence of the odor of a dually-infested plant, but not when presented a S. littoralis caterpillar (non-rewarding experience). A non-rewarding experience prior to the bioassays resulted in a general decrease in parasitoid motivation to respond to plant odors. We conclude that herbivore density and associative learning may play an important role in the foraging behavior of natural enemies in communities, and such effects should not be overlooked when investigating the ecological impact of exotic species on native food webs.     

Phenolic compounds induced by <Emphasis Type="Italic">Bemisia tabaci</Emphasis> and <Emphasis Type="Italic">Trialeurodes vaporariorum</Emphasis> in <Emphasis Type="Italic">Nicotiana tabacum</Emphasis> L. and their relationship with the salicylic acid signaling pathway

Changes in the levels of secondary compounds can trigger plant defenses. To identify phenolic compounds induced by Bemisia tabaci Middle East-Asia Minor 1 (MEAM1) in tobacco (Nicotiana tobacco L.), the content changes of 11 phenolic compounds in plants infested by B. tabaci MEAM1 or Trialeurodes vaporariorum were compared. The chlorogenic acid, catechin, caffeic acid, p-coumaric acid, rutin, and ferulic acid contents in B. tabaci MEAM1-infested tobacco plants increased significantly, having temporal and spatial effects, compared with uninfested control and T. vaporariorum infested plants. The contents were 4.10, 2.84, 2.25, 3.81, 1.46, and 1.91 times higher, respectively, than those in the control. However, a T. vaporariorum nymphal infestation just caused smaller chlorogenic acid, catechin, caffeic acid, and rutin contents increase, which were 2.33, 2.13, 1.59, and 3.19 times higher, respectively, than those in the control. In B. tabaci MEAM1 third-instar nymph-infested plants, chlorogenic acid, catechin, caffeic acid, and rutin increased more significantly in systemic than in local leaves. Salicylate-deficient plants inhibited the induction of the content of 10 phenolic compounds, but not caffeic acid, after a B. tabaci MEAM1 nymphal infestation. Thus, the elevated levels of phenolic compounds induced by B. tabaci MEAM1 were correlated with the salicylic acid signaling pathway and induced the responses of defense-related phenolic compounds.     

Olfactory response of four aphidophagous insects to aphid- and caterpillar-induced plant volatiles

Plants damaged by herbivores emit blends of volatile organic compounds (VOCs) that attract the herbivore’s natural enemies. Most work has focussed on systems involving one plant, one herbivore and one natural enemy, though, in nature, plants support multiple herbivores and multiple natural enemies of these herbivores. Our study aimed to understand how different aphid natural enemies respond to aphid-induced VOCs, and whether attraction of the natural enemies that responded to aphid-induced VOCs was altered by simultaneous damage by a chewing herbivore. We used a model system based on Brassica juncea (Brassicaceae), Myzus persicae (Hemiptera: Aphididae) and Plutella xylostella (Lepidoptera: Plutellidae). Ceraeochrysa cubana (Neuroptera: Chrysopidae) did not show preferences for any plant odour, while Cycloneda sanguinea (Coleoptera: Coccinellidae) responded to undamaged plants over air but not to aphid-damaged plants over undamaged plants. Therefore, no further tests were carried out with these two species. Chrysoperla externa (Neuroptera: Chrysopidae) preferred aphid-damaged plants, but not caterpillar-damaged plants, over undamaged plants, and preferred plants damaged by both herbivores over both undamaged plants and aphid-damaged plants. When tested for responses against undamaged plants, Aphidius colemani (Hymenoptera: Braconidae) preferred aphid-damaged plants but not plants damaged by caterpillars. Plants damaged by both herbivores attracted more parasitoids than undamaged plants, but not more than aphid-damaged plants. Thus, multiply damaged plants were equally attractive to A. colemani and more attractive to C. externa than aphid-damaged plants, while C. cubana and C. sanguinea did not respond to aphid-induced VOCs, highlighting how different natural enemies can have different responses to herbivore-damaged plants.     

A functional response evaluation of pre-infestation with <Emphasis Type="Italic">Bemisia tabaci</Emphasis> cryptic species MEAM1 on predation by <Emphasis Type="Italic">Propylea japonica</Emphasis> of <Emphasis Type="Italic">Myzus persicae</Emphasis> on host plant tomatoes

Herbivore feeding on host plants may induce defense responses of the plant which influence other herbivores and interacting species in the vicinity, such as natural enemies. The present work evaluated the impact of pre-infestation with the tobacco whitefly Bemisia tabaci cryptic species MEAM 1, on the predation ability of the ladybird Propylea japonica, to the green peach aphid Myzus persicae, on tomato plants. The results show that B. tabaci pre-infestation density, duration, and leaf position, can impact prey consumed by P. japonica under various aphid densities. The aphids consumed by P. japonica in each treatment were fit using the Holling type II functional response equation. The predatory efficiency (a/T _h) of P. japonica was the highest in the treatment with 60 aphids and 48-h infestation directly on damaged leaves. The predatory efficiencies of P. japonica decreased with a reduction of pre-infestation density and duration. We also observed that pre-infestation on young and undamaged leaves increased predation by P. japonica.     

Effects of insecticide application on parasitism rates of pollen beetle larvae (<Emphasis Type="Italic">Brassicogethes aeneus</Emphasis> (Fabricius)) by tersilochine parasitoids

Larval parasitoids can substantially reduce the population density of the pollen beetle [Brassicogethes aeneus (Fabricius), syn. Meligethes aeneus (Fabricius)]. The most abundant tersilochine parasitoids of pollen beetle are Tersilochus heterocerus, Phradis interstitialis and P. morionellus. The main activity of these parasitoids was observed in the period shortly before flowering to full flowering of oilseed rape. Insecticide applications during this period may have negative effects on parasitoids. In the present study, the effects of the insecticides Biscaya (a.i. thiacloprid), Mavrik (a.i. tau-fluvalinate) and Karate Zeon (a.i. lambda-cyhalothrin) applied during the bud or flowering stage of winter oilseed rape on parasitization of pollen beetle larvae by T. heterocerus were studied in 12 field trials at different locations in Germany in 2013–2015. The effects on parasitism by Phradis spp. were assessed in 2015. Parasitism of pollen beetle larvae by T. heterocerus was found in all field trials in all experimental years, but in most trials not before full flowering. Maximum percentage of parasitized larvae at different locations ranged between 3.4 and 16.8% in 2013, 8.3 and 22.4% in 2014 and from 11.1 to 29.1% in 2015. Levels of parasitism were not significantly different between the untreated control and insecticide treatments within each location. In contrast to T. heterocerus, Phradis spp. was not detected at all locations and not before flowering declining. In field trials at Lucklum and Puch, the maximum level of parasitism by Phradis spp. was 9.4 and 18.3%, respectively. No significant effect of insecticide application on parasitism by Phradis spp. was observed between the treatments. The results of this study showed that the insecticides used in the field trials did not affect parasitization of pollen beetle larvae by T. heterocerus and Phradis spp., regardless whether applied at the bud stage, at the beginning of flowering or full flowering.     

Predators and parasitoids of the harlequin ladybird, <Emphasis Type="Italic">Harmonia axyridis</Emphasis>, in its native range and invaded areas

The harlequin ladybird Harmonia axyridis (Coleoptera: Coccinellidae) has rapidly spread in several continents over the past 30 years and is considered an invasive alien species. The success of H. axyridis as an invader is often attributed to weak control by natural enemies. In this paper, we provide an overview of current knowledge on predators and parasitoids of H. axyridis. The common feature of predators and parasitoids is that they directly kill exploited organisms. Currently available data show that H. axyridis, displaying a variety of chemical, mechanical, and microbiological anti-predator defenses, is usually avoided by predators. However, some birds and invertebrates can eat this ladybird without harmful consequences. The primary defenses of H. axyridis against parasitoids include immune response and physiological and nutritional unsuitability for parasitoid development. These defenses are probably relatively efficient against most ladybird parasitoids, but not against flies of the genus Phalacrotophora. The latter are idiobiont parasitoids and hence can evade the host’s immune response. Indeed, rates of parasitism of H. axyridis by Phalacrotophora in the Palaearctic region (both in the native range in Asia and in Europe) are relatively high. While strong evidence for enemy release on the invasive populations of H. axyridis is lacking, several cases of parasitoid acquisition have been recorded in Europe, North America, and South America. We conclude that enemy release cannot be excluded as a possible mechanism contributing to the spread and increase of H. axyridis in the early stages of invasion, but adaptation of parasitoids may lead to novel associations which might offset previous effects of enemy release. However, further work is required to elucidate the population-level effects of such interactions.     

New evidence for a multi-functional role of herbivore-induced plant volatiles in defense against herbivores

A diverse, often species-specific, array of herbivore-induced plant volatiles (HIPVs) are commonly emitted from plants after herbivore attack. Although research in the last 3 decades indicates a multi-functional role of these HIPVs, the evolutionary rationale underpinning HIPV emissions remains an open question. Many studies have documented that HIPVs can attract natural enemies, and some studies indicate that neighboring plants may eavesdrop their undamaged neighbors and induce or prime their own defenses prior to herbivore attack. Both of these ecological roles for HIPVs are risky strategies for the emitting plant. In a recent paper, we reported that most branches within a blueberry bush share limited vascular connectivity, which restricts the systemic movement of internal signals. Blueberry branches circumvent this limitation by responding to HIPVs emitted from neighboring branches of the same plant: exposure to HIPVs increases levels of defensive signaling hormones, changes their defensive status, and makes undamaged branches more resistant to herbivores. Similar findings have been reported recently for sagebrush, poplar and lima beans, where intra-plant communication played a role in activating or priming defenses against herbivores. Thus, there is increasing evidence that intra-plant communication occurs in a wide range of taxonomically unrelated plant species. While the degree to which this phenomenon increases a plant’s fitness remains to be determined in most cases, we here argue that withinplant signaling provides more adaptive benefit for HIPV emissions than does between-plant signaling or attraction of predators. That is, the emission of HIPVs might have evolved primarily to protect undamaged parts of the plant against potential enemies, and neighboring plants and predators of herbivores later co-opted such HIPV signals for their own benefit.Key words: intra-plant signaling, plantplant communication, eavesdropping, systemic wound signals, plant defense, tri-trophic interactionsPlants often emit a unique blend of volatiles in response to herbivore attack. The emission of these herbivore-induced plant volatiles (HIPVs) is an active response to herbivore feeding, producing a blend of volatiles that is distinct from those emitted following mechanical injury alone.¹ Their emission can be variable; while some compounds follow a diurnal pattern with increasing amounts during the time of high photosynthesis,^2,3 others are emitted primarily at night.⁴ In some cases, the HIPV blend produced also differs depending on the species of herbivore feeding on the plant.⁵ This specificity is thought to be due to chemicals in the herbivore’s regurgitant, such as the fatty-acid amino-acid conjugate volicitin, that activate the emission of volatiles in plants.^6,7 Furthermore, HIPVs are emitted not only from the site of damage, but also at times from systemically undamaged parts of the plant.⁸ This and other systemic responses are, however, restricted within a plant such that only parts of the plant that share vascular connections with the damaged tissue receive wound signals and have the potential to respond.^9,10The ecological role of HIPVs has been a subject of fascination and the evolutionary advantage gained for plants by emitting HIPVs remains an unresolved topic of discussion. While some HIPV compounds, and some of their precursors, have sufficient volatility that their release is essentially inevitable after synthesis,¹¹ most tend to be tightly regulated. Assuming that HIPV emissions evolved as a result of trophic interactions among plants, herbivores, and natural enemies, there are four general ecological roles that HIPVs may play: (1) a direct negative effect on the herbivore, (2) a signal to alert natural enemies of the herbivore, (3) a warning signal to nearby undamaged plants, and (4) a systemic warning signal within the damaged plant (Fig. 1). The first two potential roles involve the manipulation of animal behavior, while the last two may alter plant “behavior”.Open in a separate windowFigure 1Herbivore-induced plant volatiles (HIPVs) play multiple roles in interactions among plants, herbivores, and natural enemies (possible interactions are depicted by arrows). Some of them benefit the HIPV-emitting plant (Emitter); these positive interactions include repellent effects on herbivores, attraction of natural enemies of herbivores, activation or priming of defenses in unwounded parts within the emitting plant (within-plant signaling), and growth inhibitory effects on neighboring plants (Receiver) through allelopathy. On the other hand, HIPVs may negatively affect the emitting plant by attracting herbivores or natural enemies (e.g., certain parasitoids) that result in increased damage. Finally, neighboring plants may “eavesdrop” from the emitting plant by responding to HIPVs (between-plant signaling). This latter interaction may be negative to the emitter if it is outcompeted by neighbors who receive wound signals, but beneficial to the receiving plant. Drawing by Robert Holdcraft.Scents can have a demonstrable effect on animal behavior. With respect to plant-herbivore interactions, scents can provide information about the status of a plant to herbivores and their natural enemies. For example, HIPVs may repel adults moths searching for oviposition sites,³ which has been interpreted from the perspective of either a plant minimizing damage or, perhaps more realistically, an adult moth searching for an undamaged, high quality resource for her offspring. Conversely, HIPV-emitting plants may increase their chance of being injured if herbivores are attracted to these volatiles.¹² The more commonly accepted role of HIPVs in manipulating animal behavior is to attract natural enemies of the herbivores. This tri-trophic “cry for help”¹³ has a potential evolutionary benefit for both the plant emitting the volatiles and the natural enemies responding to this emission.^14–16 Although this idea makes sense in an evolutionary perspective, only a few studies have documented the occurrence of this phenomenon in natural systems.¹⁷ Indeed, the effectiveness of a cry for help depends on the presence of a helper and, equally importantly, the ability of the helper to increase plant fitness. In the case of predator attraction, the herbivore may be removed from the plant and consumed, thereby reducing damage for the emitting plant.¹⁸ However, insect herbivores infected by parasitoids, which also use HIPV cues to locate hosts,¹⁹ may also consume less plant material²⁰ but may also in some cases consume more plant material than unparasitized insect herbivores.²¹ Since there is currently no evidence that plants can modify HIPV blends to attract selectively predators versus parasitoids, an answered cry for help may not reliably decrease the total amount of damage to an emitting plant. Thus, the fact that natural enemies respond to HIPVs does not imply that these volatiles evolved for this purpose or that there is an adaptive advantage for a plant to use HIPVs to attract natural enemies. Rather, natural enemies of insect herbivores may have learned to co-opt the HIPV signal emitted by plants and, by doing so, increased their fitness irrespective of the ultimate fitness outcome to the plant.Though more controversial, scents can also have an effect on plant behavior.²² Early work suggested that HIPVs from wounded willows,²³ poplars²⁴ and sugar maples²⁴ could trigger defense responses from other neighboring conspecifics. More recent studies have shown that this signaling can occur between different species of plants.²⁵ While these results are intriguing, they appear to have little adaptive function from the perspective of an emitting plant, which could be facilitating the fitness of potential resource competitors. Further, unless the individual within the same plant species shared some degree of kinship,²⁶ an emitting plant would also be at a disadvantage by providing an HIPV wound signal to a conspecific that, in theory, occupies the same competitive niche space. On the other hand, unwounded conspecific should benefit from being able to ‘eavesdrop’ by detecting HIPVs from wounded plants as they share the same herbivore complex and thus are vulnerable to attack. Moreover, from a heterospecific receiver’s perspective, the benefits of eavesdropping can be confounded by the potential of mounting defenses against a signal generated by incompatible herbivores feeding on a different plant species.²⁷ So, eavesdropping may be adaptive for a receiving plant if it realizes increased fitness relative to a conspecific that did not receive the signal. The emitting plant derives no apparent adaptive benefit of using HIPVs to warn neighboring plants. However, the emitting plant may benefit if their HIPVs have inhibitory allelopathic activity on neighboring plants.²⁸Our recent work¹ highlighted another scenario by which an HIPV-emitting plant would derive a direct benefit from the emissions: when HIPVs act as systemic wound signals within damaged plants. We showed that branches of blueberry shrubs lack effective vascular connections and thus cannot transmit wound signals among branches via the vasculature. To compensate, HIPVs can be transmitted among branches and, in so doing, overcome the vascular constraints of the branching life history strategy. Exposure to HIPVs increased levels of defensive signaling hormones in undamaged branches, changed their defensive chemical status, and made them more resistant to herbivores.¹ This idea that HIPVs may function in intra-plant communication to activate or prime defenses in other parts of the emitting plant against future attack was first suggested separately by Farmer²⁹ and Orians.⁹ The hypothesis was first tested with mechanically clipped wild sagebrush,³⁰ and it was further tested with insect herbivores of wild lima bean³¹ and hybrid poplar.³² Under this scenario, the emitting plant derives a direct benefit from the HIPVs, providing an unambiguous fitness advantage.So, what is the most beneficial factor to a plant for emitting volatiles in response to herbivore feeding? In terms of maximizing the potential benefit and minimizing the potential risk to the emitting plant, the function of HIPVs in mediating systemic wound signaling clearly provides the greatest potential adaptive advantage. Thus, we propose that the primary adaptive benefit for the evolution of HIPVs is to signal and protect unwounded parts of the attacked plant with high risk of infestation against herbivores. Later, these volatiles provided cues that led to adaptive fitness advantages for neighboring plants and natural enemies of herbivores, which may or may not benefit the HIPV-emitting plant. Indeed, ecologically adaptive advantages have emerged and contribute to a diverse, multi-functional chemical ecology mediated by HIPVs.     

Attraction of <Emphasis Type="Italic">Telenomus podisi</Emphasis> to volatiles induced by <Emphasis Type="Italic">Euschistus heros</Emphasis> in three different plant species

Specialized natural enemies that forage for polyphagous hosts need to locate hosts on different plants. Telenomus podisi (Hymenoptera: Platygastridae) is a stink bug egg parasitoid with a preference for Euschistus heros (Hemiptera, Pentatomidae), a polyphagous species. The aim of this study was to evaluate the induction of defences in three E. heros host plants: maize (Zea mays), sunflower (Helianthus annuus) and pigeon pea (Cajanus cajan). We hypothesized that E. heros damage to these three plants enhances the attraction of the parasitoid T. podisi as has been observed in other systems. Using Y-tube olfactometer bioassays, we tested parasitoid responses to combinations of the following odour sources: clean air, undamaged plants and plants damaged by stink bug feeding. Volatiles were collected by means of dynamic headspace collection and analysed by gas chromatography coupled to mass spectrometry. T. podisi did not distinguish odours from undamaged plants against air for any of the three plant species. For maize, the parasitoid preferred the odour from herbivore-damaged plants over both clean air and undamaged plants. For sunflower, the parasitoid only preferred the odour of herbivore-damaged plants over the odour of undamaged plants. For pigeon pea, no preferences were observed. Quantitative differences in the volatile profile of damaged and undamaged plants were observed in each plant species. We conclude that sunflower and maize plants, when damaged by E. heros, release volatiles that attract the parasitoid T. podisi; the parasitoid appears to use a different blend composition to distinguish herbivore-damaged plants of each species.     

Oviposition Preferences of <Emphasis Type="Italic">Plutella xylostella</Emphasis> are Influenced by the Type of Plant Induction and Glucosinolate Hydrolysis Profiles

Effects of inducing plants by exposing them to insect herbivory, mechanical damage or damaged neighboring plants were evaluated on the oviposition preferences of Plutella xylostella. The role of plant genotypes differing in their glucosinolate hydrolysis profiles was also evaluated using a wild ecotype (Col-0) and a genetically modified line (tgg1tgg2) of Arabidopsis thaliana. While the Col-0 line has normal production of glucosinolate hydrolysis products, the double myrosinase knockout (tgg1tgg2) is defective in the production of these volatiles. Dual choice oviposition assays were performed using naïve P. xylostella females, and the two A. thaliana lines, which were exposed to the three types of induction treatments. Female oviposition preferences were significantly influenced by both the type of plant induction and the plant genotypes differing in their volatile profiles. Plutella xylostella females significantly preferred to oviposit on herbivore-damaged plants (versus undamaged controls) when Col-0 plants were used, but chose control plants over the double myrosinase knockout tgg1tgg2. However, plant genotype did not influence oviposition choices between plant-plant primed or mechanically damaged plants and paired undamaged controls. Given the prevalent use of genetically modified plants and the potential differences in their responses to different types of induction, these factors may be important to consider in the management of specialist pests such as the diamondback moth P. xylostella.     

In search of secondary plants to enhance the efficiency of cabbage seed weevil management

The infestation rate and parasitoid communities of Ceutorhynchus obstrictus (Marsham) (Coleoptera: Curculionidae) were assessed on seven spring sown brassicaceous plant species to find potential secondary plants that might help increase the parasitism rates of this serious oilseed pest. Over the three-year study, the average infestation rate of pods by C. obstrictus remained below 10 % for each plant species. Despite the low pest abundance, C. obstrictus was parasitized by hymenopteran parasitoids on all plant species, except on Eruca vesicaria subsp. sativa ((Mill.) Thell.). Parasitism rates were remarkably high: between 33.7 and 70.8 % on average and peaked at 94.7 % on Raphanus sativus (L.) var. oleiformis (Pers.). Not only was the parasitism rate high on R. sativus, but it also had a different parasitoid species composition consisting mainly of egg parasitoids (Mymaridae), while on the other plant species larval parasitoids (Pteromalidae) dominated. These findings are important for planning new sustainable pest management approaches.     

Reduced ant defenses in <Emphasis Type="Italic">Macaranga</Emphasis> myrmecophytes (Euphorbiaceae) infested with a winged phasmid <Emphasis Type="Italic">Orthomeria cuprinus</Emphasis>

Macaranga is a tree genus that includes many species of myrmecophytes, which are plants that harbor ant colonies within hollow structures known as domatia. The symbiotic ants (plant–ants) protect their host plants against herbivores; this defense mechanism is called ‘ant defense’. A Bornean phasmid species Orthomeria cuprinus feeds on two myrmecophytic Macaranga species, Macaranga beccariana and Macaranga hypoleuca, which are obligately associated with Crematogaster ant species. The phasmids elude the ant defense using specialized behavior. However, the mechanisms used by the phasmid to overcome ant defenses have been insufficiently elucidated. We hypothesized that O. cuprinus only feeds on individual plants with weakened ant defenses. To test the hypothesis, we compared the ant defense intensity in phasmid-infested and non-infested M. beccariana trees. The number of plant–ants on the plant surface, the ratio of plant–ant biomass to tree biomass, and the aggressiveness of plant–ants towards experimentally introduced herbivores were significantly lower on the phasmid-infested trees than on the non-infested trees. The phasmid nymphs experimentally introduced into non-infested trees, compared with those experimentally introduced into phasmid-infested trees, were more active on the plant surface, avoiding the plant–ants. These results support the hypothesis and suggest that ant defenses on non-infested trees effectively prevent the phasmids from remaining on the plants. Thus, we suggest that O. cuprinus feeds only on the individual M. beccariana trees having decreased ant defenses, although the factors that reduce the intensity of the ant defenses remain unclear.     

Supplemental releases of specialist parasitic wasps improve whitefly and psyllid control by <Emphasis Type="Italic">Dicyphus hesperus</Emphasis> in tomato

Dicyphus hesperus Knight (Heteroptera: Miridae) can contribute to the suppression of populations of Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) and Bactericera cockerelli Sulcer (Hemiptera: Psyllidae) in tomato. Nevertheless, the remaining levels of these pests could still be too high for the crop to tolerate. We thus tested here whether the combination of D. hesperus with the specialist parasitoids Eretmocerus eremicus Rose & Zolnerowich (Hymenoptera: Aphelinidae) (whitefly) and Tamarixia triozae (psyllid) can result in better pest control compared with methods based exclusively on single-species releases in tomato. We conducted two simultaneous experiments in tomato (‘Whitefly’ and ‘Psyllid’ Experiment), where we compared the effectiveness against B. tabaci and B. cockerelli in cages receiving releases of the predator or the specialist parasitoid alone, or in combination. Although all natural enemies reduced pest levels when released separately, the combination of D. hesperus with E. eremicus and D. hesperus with T. triozae resulted in better whitefly and psyllid control, respectively, compared with the separate releases.     

A Bird in the Hand Versus Two in the Bush? The Specialist Leafhopper <Emphasis Type="Italic">Dalbulus maidis</Emphasis> (Hemiptera: Cicadellidae) Does Not Discriminate Against Sub-optimal Host Plants (<Emphasis Type="Italic">Zea</Emphasis> spp.)

The corn leafhopper [Dalbulus maidis (DeLong & Wolcott)] is a specialist on Zea (Poaceae) that coevolved with maize (Zea mays mays) and its teosinte (Zea spp.) relatives. This study tested the hypothesis that host acceptance by females varies among Zea hosts, and is correlated with variation in defensive levels across those hosts. Prior studies revealed differences in plant defenses among Zea hosts and corresponding differences in corn leafhopper performance. Thus, host acceptance was expected to be correlated with defensive levels and offspring performance across Zea hosts, following the hypothesis that offspring performance mediates host preference. In parallel, host acceptance was expected to be correlated with transitions in life history strategy (perennial to annual life cycle), domestication status (wild to domesticated), and breeding intensity (landrace to hybrid variety) in Zea because variation in defensive levels and corn leafhopper performance were shown in prior studies to be correlated with those transitions. The study’s hypotheses were tested by comparing, under no-choice conditions, host acceptance by corn leafhopper of a suite of Zea hosts encompassing those transitions: perennial teosinte (Zea diploperennis), Balsas teosinte (Zea mays parviglumis), and landrace and commercial hybrid maize. The results did not show differences in host acceptance for oviposition or feeding among the hosts. Thus, under no-choice conditions, all Zea hosts may be similarly acceptable for feeding and oviposition, despite marked ovipositional preferences under choice conditions and poorer offspring performance on teosintes relative to maize shown previously. The results suggested also that oviposition frequency per plant by females was not correlated with their offspring’s performance.