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.     

Response of the zoophytophagous predators Macrolophus pygmaeus and Nesidiocoris tenuis to volatiles of uninfested plants and to plants infested by prey or conspecifics

Knowledge about the orientation mechanisms used by two important predaceous mirids (Macrolophus pygmaeus Rambour and Nesidiocoris tenuis (Reuter)) in finding their prey (whitefly Bemisia tabaci (Gennadius) and the tomato borer Tuta absoluta (Meyrick)) is limited. In a Y-tube olfactometer, we tested the behavioral responses of naïve and experienced predators to uninfested plants, herbivore-induced plant volatiles (HIPVs) from plants infested with T. absoluta and/or B. tabaci, the sex pheromone of T. absoluta, and volatiles produced by plants injured by the predators. Nesidiocoris tenuis responds to volatiles produced by uninfested plants only after experience with the plant, whereas naïve and experienced M. pygmaeus show positive chemotaxis. Both predators are attracted to volatiles from prey-infested plants, and we provide the first evidence that experience affects this response in M. pygmaeus. Infestation of the same plant by both prey species elicited similar responses by the two predators as plants infested by either herbivore singly. Neither predator responded to sex pheromones of T. absoluta. Macrolophus pygmaeus avoided plants injured by conspecifics, while N. tenuis females were attracted by such plants. The implications of these results for augmentative biological control are discussed.     

Intraguild predation and cannibalism among Dicyphini: Dicyphus cerastii vs. two commercialized species

Dicyphine mirids are one of the most important groups of predators on tomato. In the Mediterranean region, several species in the genera Dicyphus, Macrolophus, and Nesidiocoris (Hemiptera: Miridae, Bryocorinae, Dicyphini) colonize protected horticultural crops. In Portugal, Nesidiocoris tenuis (Reuter) is increasingly abundant in the mirid species complex of tomato crops and appears to be displacing the native Dicyphus cerastii Wagner. In order to know whether intraguild predation (IGP) can explain the decreasing abundance of D. cerastii, we evaluated predatory interactions between adult females and first instars of D. cerastii vs. N. tenuis but also D. cerastii vs. Macrolophus pygmaeus (Rambur), as this species is also naturally present in horticultural crops in Portugal. Cannibalistic interactions were also tested for the same three species. All experiments were performed under laboratory conditions, in Petri dish arenas, in the presence or absence of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) eggs as alternative prey. Predation on both heterospecific and conspecific nymphs occurred only in the absence of alternative food. Intraguild predation was mutual and symmetrical between D. cerastii and M. pygmaeus. However, IGP was asymmetrical between D. cerastii and N. tenuis, favouring the first. Cannibalism was not significantly different among these mirid species. Our results show that D. cerastii has a greater capacity to feed on intraguild prey than N. tenuis. Therefore, IGP on small nymphs does not explain the abundance shift between D. cerastii and N. tenuis.     

Nesidiocoris tenuis as a pest in Northwest Europe: Intervention threshold and influence of Pepino mosaic virus

The use of Nesidiocoris tenuis (Hemiptera: Miridae) as a biocontrol agent is controversial as it is considered a pest in Northwest European tomato greenhouses, due to its tendency to damage the plant and fruit. Necessary chemical plant protection products to control N. tenuis have toxic side effects on important beneficials like Macrolophus pygmaeus (Hemiptera: Miridae), which jeopardizes the whole IPM programme. In this study, several commercial tomato greenhouses were monitored for mirid populations. The relationship between the number of N. tenuis individuals and plant damage was assessed in function of availability of prey and interaction with M. pygmaeus. These greenhouse data were used to determine a practical density intervention threshold. Next, the hypothesis that a Pepino mosaic virus (PepMV) infection increases plant and fruit damage by N. tenuis (as has been shown for M. pygmaeus) was tested. Plant damage occurred when the average number of predatory bugs in the head of the plant exceeded 16 per ten plants. Plant damage increased in severity at increasing predatory bug densities, independent of the availability of prey and M. pygmaeus presence. Plant and fruit damage were not affected by the presence of PepMV, as was shown for fruit damage in previous studies for M. pygmaeus. Our study provides a practical density intervention threshold for growers in greenhouse crops. Simple monitoring of the number of predatory bugs in the head of the plant can be used to take specific biocontrol actions. It was also shown that only the predatory bug N. tenuis itself causes damage, and there is no interaction with PepMV.     

Constitutive exposure to the volatile methyl salicylate reduces per‐capita foraging efficiency of a generalist predator to learned prey associations

Understanding the factors that influence the ability of predators to find and kill herbivores is central to enhancing their impact on prey populations, but few studies have tested the impact of these factors on predation rates in realistic foraging environments. Using the tri‐trophic system consisting of tomato, Solanum lycopersicum L. (Solanaceae), hornworm caterpillars, Manduca sexta L. (Lepidoptera: Sphingidae), and the predaceous stink bug Podisus maculiventris (Say) (Hemiptera: Pentatomidae), we measured the effects of associative learning and plant volatile camouflage on predator behavior and foraging efficiency in field enclosures. To do so, we compared experienced vs. naive individuals under varying environmental contexts. Experienced predators were those with prior exposure to induced volatiles from the tomato–caterpillar association, whereas naive predators had not experienced tomato, only prey (caterpillars). We varied their environmental foraging matrix using either (1) tomato surrounded by basil (Ocimum basilicum L.; Lamiaceae) or (2) tomato exposed to the synthetic volatile, methyl salicylate (MeSA). We found that (1) experienced predators were more efficient than naive predators, capturing 28% more prey; (2) the tomato–basil combination did not affect predator–prey interactions; and (3) constitutive emission of synthetic MeSA caused a 22% reduction in P. maculiventris predation rate. These differences corresponded with distinct shifts in predator foraging; for example, experienced individuals were less stationary and exhibited unique behaviors such as stylet extension. Taken together, these results suggest that it is possible to improve the function of generalist predators in suppressing prey by coupling odors with food. However, constitutive emission of volatiles to attract natural enemies may ultimately camouflage neighboring plants, reducing the benefits of orientation to learned stimuli such as induced volatiles.     

Intraguild predation and sublethal interactions between two zoophytophagous mirids,Macrolophus pygmaeus and Nesidiocoris tenuis

The omnivorous predators Macrolophus pygmaeus and Nesidiocoris tenuis (Hemiptera: Miridae) are important biological control agents of pests on tomato crops. In this study, potential intraguild predation (IGP) interactions between the two species were investigated on tomato. We examined: (a) the within plant distribution of both species in the field, (b) the within plant distribution of each predatory species when co-occurred at high densities on tomato caged plants, (c) their behavioral interactions when enclosed in experimental arenas and (d) the development young and old nymphs of M. pygmaeus when enclosed together with N. tenuis adults. Results revealed that the two predators showed a different distribution pattern on the plants, with N. tenuis exploiting mostly the upper part, whereas M. pygmaeus were mostly observed on the 5th to the 7th leaf from the top. However, when the predators co-occurred, N. tenuis or M. pygmaeus individuals were recorded with increased numbers on the lower or the higher part of the plant, respectively. In the presence of N. tenuis adult young nymphs of M. pygmaeus completed their development to the adult stage, when alternative prey (lepidopteran eggs) was present on the plant, however failed to reach adulthood in the absence of alternative prey. A high percentage of the dead nymphs found with their body fluids totally sucked indicating predation by N. tenuis. However, large 4th instar nymphs of M. pygmaeus were much less vulnerable to N. tenuis than younger. The behavior of N. tenuis was affected by the presence of M. pygmaeus, but at a rate similar to that when two individuals of N. tenuis were enclosed together. Contacts between the predators were recorded in a similar frequency in mono- and heterospecific treatments, whereas aggressive behavior was not observed. This study shows that intraguild interactions between M. pygmaeus and N. tenuis occur but are not intensive. The potential implications of the outcomes for biological control are discussed.     

Suitability of the tomato borer Tuta absoluta as prey for Macrolophus pygmaeus and Nesidiocoris tenuis

The tomato borer, Tuta absoluta (Meyrick) (Lep.: Gelechiidae), is an important tomato pest native to South America, which appeared in eastern Spain at the end of 2006. Prey suitability of T. absoluta eggs and larval instars was examined under laboratory conditions to evaluate whether two indigenous predators, Macrolophus pygmaeus (Rambur) and Nesidiocoris tenuis Reuter (Hem.: Miridae), can adapt to this invasive pest. Both predators preyed actively on T. absoluta eggs and all larval stages, although they preferred first‐instar larvae. Our results demonstrate that both mirids can adapt to this invasive pest, contributing to their value as biological control agents in tomato crops.     

Caterpillar‐induced plant volatiles attract conspecific herbivores and a generalist predator

Plants release volatiles in response to caterpillar feeding that attracts natural enemies of the herbivores, a tritrophic interaction which has been considered to be an indirect plant defence against herbivores. On the other hand, the caterpillar‐induced plant volatiles have been reported to either repel or attract conspecific adult herbivores. This work was undertaken to investigate the response of both herbivores and natural enemies to caterpillar‐induced plant volatiles in apple orchards. We sampled volatile compounds emitted from uninfested apple trees, and apple trees infested with generalist herbivore the pandemis leafroller moth, Pandemis pyrusana (Lepidoptera, Tortricidae) larvae using headspace collection and analysed by gas chromatography/mass spectrometry. Infested apple trees uniquely release six compounds (benzyl alcohol, phenylacetonitrile, phenylacetaldehyde, 2‐phenylethanol, indole and (E)‐nerolidol). These compounds were tested on two species of herbivores and one predator in apple orchards. Binary blends of phenylacetonitrile + acetic acid or 2‐phenylethanol + acetic acid attracted a large number of conspecific male and female adult herbivores. The response of pandemis leafroller to herbivore‐induced plant volatiles (HIPVs) was so pronounced that over one thousand and seven hundred conspecific male and female adult herbivores were caught in traps baited with HIPVs in three‐day trapping period. In addition, significantly higher number of male and female obliquebanded leafroller, Choristoneura rosaceana (Lepidoptera, Tortricidae), was caught in traps baited a binary blend of 2‐phenylethanol + acetic acid, or a ternary blend contains 2‐phenylethanol and phenylacetonitrile + acetic acid. This result challenges the current paradigm hypothesized that HIPVs repel herbivores and question the indirect defensive function proposed for these compounds. On the other hand, a ternary blend of phenylacetonitrile and 2‐phenylethanol + acetic acid attracted the largest numbers of the general predator, the common green lacewing, Chrysoperla plorabunda. To our knowledge, this is the first record of the direct attraction of conspecific adult herbivores as well as a predator to the caterpillar‐induced plant volatiles in the field.     

Zoophytophagy in the plantbug Nesidiocoris tenuis

1 The zoophytophagy of Nesidiocoris tenuis (Reuter) (Heteroptera: Miridae) was characterized in relation to prey availability and environmental factors by: (i) monitoring its population dynamics in tomato greenhouses; (ii) analysis of the influence of N. tenuis and whitefly density, temperature and humidity on the intensity of N. tenuis plant feeding; and (iii) laboratory assays under controlled conditions to determine the intensity of plant feeding in relation to prey availability, temperature and humidity. 2 A negative relationship was found between plant feeding and predated whiteflies in tomato greenhouses. Plant feeding was directly related to N. tenuis density and temperature and inversely related to whitefly density. The significance of prey availability and temperature was corroborated in laboratory assays. The intensification of plant feeding at low prey density indicates switching from zoophagy to phytophagy as prey become scarce. 3 Nesidiocoris tenuis showed a typical predator dynamic in relation to variance in prey density. Populations increased after whitefly outbreaks and decreased after whitefly had been depleted. The rapid decrease of N. tenuis populations after whitefly decreased, however, suggests that plants are a poorer nutrient source than whitefly for this species.     

How does a predator find its prey? Nesidiocoris tenuis is able to detect Tuta absoluta by HIPVs

The Zoophytophagous predator, Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae) is one of the most important candidates for controlling Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in tomato crops. This predator uses different signals including morphological plant traits, prey insects, and volatile substances produced by the infested plants and prey signals to find its suitable prey. These signals are different in each cultivar of a plant. We aimed to understand how N. tenuis finds its prey using volatiles from tomato plants damaged or infested with T. absoluta. The predator’s responses to various plant treatments on two cultivars of tomato plants were tested in a flight tunnel and a four-choice olfactometer. The volatile compounds released from the treatments were also collected and identified. The results of the olfactory experiments showed that the predators even in the absence of light chose the plants bearing their insect prey. This behavior was not the same in both cultivars, and N. tenuis had a tendency toward mechanically damaged of Early Urbana Y cultivar more than Cal JN3 cultivar. The differences in the amount of monoterpenes, sesquiterpenes, and eugenol between cultivars may play a role in the differential attraction of N. tenuis towards infested plants. The difference in the volatile compounds was evident in two cultivars, and this was consistent with our bioassay results. Therefore, the choice of appropriate cultivar and use of herbivore-infested plant volatiles are important for developing a control strategy against T. absoluta and attract its predators.     

Life‐history parameters and predation capacity of Macrolophus pygmaeus and Nesidiocoris tenuis (Hemiptera: Miridae) on eggs of Plutella xylostella (Lepidoptera: Plutellidae)

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Sugars as complementary alternative food for the establishment of Nesidiocoris tenuis in greenhouse tomato

Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae) is an omnivorous generalist predator which is augmentatively released and conserved for control of whiteflies (Hemiptera: Aleyrodidae) and Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in tomato crops. Eggs of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) are often provided as factitious prey to improve the establishment of N. tenuis after its release. We first tested different amounts of E. kuehniella eggs per plant to optimize N. tenuis establishment and then investigated whether the amount of eggs that optimized N. tenuis establishment might be reduced by adding sugars (hydrocapsules filled with 0.5 m sucrose) under walk‐in cage and commercial greenhouse conditions. These experiments demonstrated that the addition of sugar to the diet of N. tenuis could half the amount of E. kuehniella eggs required to establish N. tenuis. Under greenhouse conditions, the progeny of N. tenuis per plant did not differ significantly between E. kuehniella alone or the half amount of E. kuehniella plus hydrocapsules. These results demonstrated that the sugar could partially substitute for E. kuehniella eggs improve establishment of N. tenuis and suggest that natural sugars such as nectar and honeydew might also beneficial.     

Can the pheromones of predators modulate responses to herbivore‐induced plant volatiles?

Biological control of greenhouse pests has been successfully developed and applied. In greenhouse crops, several entomophagous species (predators and parasitoids) are used simultaneously in the crop cycle. One important aspect of these crops, which represent modified ecosystems, is the interactions among complexes of species, including plants, phytophagous insects, and predators. The chemical relationships (semiochemicals: pheromones and kairomones) among these species likely play an important role in greenhouse crops; however, few studies have focused on these relationships. The aim of this study was to analyse the importance of semiochemicals. Three groups of laboratory trials were conducted with two predatory species: Nabis pseudoferus and Nesidiocoris tenuis (Hemiptera: Nabidae and Miridae, respectively). The results of the first group of trials indicated that the adult females of both species were more attracted to herbivore‐induced plant volatiles (HIPVs) than they were to the control plants or plants with artificial damage. Based on the second group of trials, pheromones triggered an attraction in adult females of both species for conspecifics. Finally, based on the interactions of the adult females of the same species, pheromones changed or modulated the predatory responses to HIPVs. The implications of these results for the biological control of pest species in greenhouses are further discussed.     

Over what distance are plant volatiles bioactive? Estimating the spatial dimensions of attraction in an arthropod assemblage

As studies demonstrating attraction of natural enemies to synthetic herbivore‐induced plant volatiles (HIPVs) accumulate, it is becoming increasingly important to investigate how deployment of these compounds influences arthropod behavior and distribution in the field. There is currently an unexplained dichotomy in the literature regarding the distance over which HIPVs are thought to be effective. It is assumed that these compounds increase recruitment of natural enemies into fields, whereas experiments have found the effects of attraction to dissipate as little as 1.5 m from lures. Through the use of the common HIPV phenylethyl alcohol in soybean [Glycine max (L.) Merr (Fabaceae)] fields, we used replicated mini plots to test the spatial scale and consequences of attraction by analyzing the response of a complex arthropod community to HIPVs along a distance gradient from the HIPV source. Although repellent effects were more common than attractive ones, we found that insect responses to HIPVs are generally consistent out to a range of 8 m, corroborating the idea that volatiles can influence a wide area and are capable of increasing arthropod recruitment at a field scale. Evidence of redistribution (i.e., depletion of patches surrounding HIPV‐augmented plots) was found for a single taxon, braconid wasps, for which augmentation occurred around the lure, but with a reciprocal decline in abundance at greater distances from the emission site. These results are both encouraging and cautionary. Although broad‐scale diffusion of HIPVs appears to be common, redistribution of key predators and/or parasitoids may complicate natural enemy management on a landscape scale by aggravating pest outbreaks in areas robbed of their normal carnivore assemblage.     

A key volatile infochemical that elicits a strong olfactory response of the predatory mite <Emphasis Type="Italic">Neoseiulus californicus</Emphasis>, an important natural enemy of the two-spotted spider mite <Emphasis Type="Italic">Tetranychus urticae</Emphasis>

Herbivore-induced plant volatiles (HIPVs) emitted from lima bean leaves infested with the two-spotted spider mites Tetranychus urticae strongly attract the predatory mites Neoseiulus californicus. Among these HIPVs, methyl salicylate and linalool can attract the predators. Three green-leaf volatiles (GLVs) of (Z)-3-hexen-1-ol, (Z)-3-hexenyl acetate and (E)-2-hexenal, found in the odor blends from T. urticae-infested leaves and physically damaged leaves, can also attract the predators. To search for a strong predator attractant, the olfactory responses of N. californicus to each synthetic compound or their combinations were investigated in a Y-tube olfactometer. When presented a choice between a mixture of the five compounds (i.e. the two HIPVs and the three GLVs) and T. urticae-infested leaves, N. californicus did not discriminate between these odor sources. The same trend was observed when either a mixture of the two HIPVs or methyl salicylate vs. T. urticae-infested leaves were compared. In contrast, the predators preferred T. urticae-infested leaves to linalool, each of the three GLVs, or a mixture of the three GLVs. These results indicated that methyl salicylate is a strong predator attractant, and its potential attractiveness almost equaled that of the blend of HIPVs from T. urticae-infested leaves.     

Functional response of Macrolophus pygmaeus (Rambur) and Nesidiocoris tenuis (Reuter) feeding on two different prey species

Functional response type and predatory parameters of Macrolophus pygmaeus and Nesidiocoris tenuis (Hemiptera: Miridae), the two important predators widely used in IPM programmes at tomato greenhouses, were investigated. The predators fed on Tuta absoluta (Lepidoptera: Gelechiidae) or Ephestia kuehniella (Lepidoptera: Pyralidae) eggs. Different densities of prey eggs including 1, 2, 3, 4, 5, 8, 10, 15, 20, 30 and 40 (latest only for E. kuehniella) were used at laboratory conditions. The results showed that both predatory bugs had type II functional response. Also, predation indices were significantly different between the predators. Although N. tenuis was more efficient against T. absoluta eggs than M. pygmaeus, M. pygmaeus predatory indices showed that this predator was more efficient on E. kuehniella eggs. Thus, minimum and maximum attack rate were observed in N. tenuis fed on E. kuehniella (0.0871 h^?1) and T. absoluta (0.2514 h^?1) eggs, respectively. Whilst, the minimum and maximum handling time were observed in M. pygmaeus fed on E. kuehniella (1.8695 h) and T. absoluta (2.7415 h) eggs, respectively.     

An ecogenomic analysis of herbivore‐induced plant volatiles in Brassica juncea

Upon herbivore feeding, plants emit complex bouquets of induced volatiles that may repel insect herbivores as well as attract parasitoids or predators. Due to differences in the temporal dynamics of individual components, the composition of the herbivore‐induced plant volatile (HIPV) blend changes with time. Consequently, the response of insects associated with plants is not constant either. Using Brassica juncea as the model plant and generalist Spodoptera spp. larvae as the inducing herbivore, we investigated herbivore and parasitoid preference as well as the molecular mechanisms behind the temporal dynamics in HIPV emissions at 24, 48 and 72 h after damage. In choice tests, Spodoptera litura moth preferred undamaged plants, whereas its parasitoid Cotesia marginiventris favoured plants induced for 48 h. In contrast, the specialist Plutella xylostella and its parasitoid C. vestalis preferred plants induced for 72 h. These preferences matched the dynamic changes in HIPV blends over time. Gene expression analysis suggested that the induced response after Spodoptera feeding is mainly controlled by the jasmonic acid pathway in both damaged and systemic leaves. Several genes involved in sulphide and green leaf volatile synthesis were clearly up‐regulated. This study thus shows that HIPV blends vary considerably over a short period of time, and these changes are actively regulated at the gene expression level. Moreover, temporal changes in HIPVs elicit differential preferences of herbivores and their natural enemies. We argue that the temporal dynamics of HIPVs may play a key role in shaping the response of insects associated with plants.     

Influence of volatile compounds from herbivore‐damaged soybean plants on searching behavior of the egg parasitoid Telenomus podisi

Parasitoids use herbivore‐induced plant volatiles (HIPVs) to locate their hosts. However, there are few studies in soybean showing the mechanisms involved in the attraction of natural enemies to their hosts and prey. The objective of this study was to evaluate the influence of volatile organic compounds (VOCs) of soybean, Glycine max (L.) Merr. (Fabaceae) (cv. Dowling), that were induced after injury caused by Euschistus heros (Fabricius) (Hemiptera: Pentatomidae), on the searching behavior of the egg parasitoid Telenomus podisi Ashmead (Hymenoptera: Scelionidae). Four HIPVs from soybean, (E,E)‐α‐farnesene, methyl salicylate, (Z)‐3‐hexenyl acetate, and (E)‐2‐octen‐1‐ol, were selected, prepared from standards at various concentrations (10^?6 to 10^?1 m ), and tested individually and in combinations using a two‐choice olfactometer (type Y). Telenomus podisi displayed a preference only for (E,E)‐α‐farnesene at 10^?5 m when tested individually and compared to hexane, but they did not respond to the other compounds tested individually at any concentration or when combinations of these compounds were tested. However, the parasitoids stayed longer in the olfactometer arm with the mixture of (E,E)‐α‐farnesene + methyl salicylate at 10^?5 m than in the arm containing hexane. The results suggest that (E,E)‐α‐farnesene and methyl salicylate might help T. podisi to determine the presence of stink bugs on a plant. In addition, bioassays were conducted to compare (E,E)‐α‐farnesene vs. the volatiles emitted by undamaged and E. heros‐damaged plants, to evaluate whether (E,E)‐α‐farnesene was the main cue used by T. podisi or whether other minor compounds from the plants and/or the background might also be used to locate its host. The results suggest that minor volatile compounds from soybean plants or from its surroundings are involved in the host‐searching behavior of T. podisi.     

A comparative life history study of two mirid bugs preying on Tuta absoluta and Ephestia kuehniella eggs on tomato crops: implications for biological control

The omnivorous predators Nesidiocoris tenuis (Reuter) and Macrolophus pygmaeus Rambur (Hemiptera: Miridae) are indigenous natural enemies that commonly inhabit tomato crops in the Mediterranean basin. Both predators are mass-reared and primarily released to control whiteflies, although recently they have also contributed to the control of the invasive tomato pest Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). The life history traits of these two predators have been studied in the laboratory under the conditions of being fed exclusively the eggs of T. absoluta or the eggs of the factitious prey Ephestia kuehniella (Zeller) (Lepidoptera: Pyralidae). Immature stages of both predator species successfully developed while preying on eggs of T. absoluta. However, the mature M. pygmaeus females produced significantly lower numbers of offspring in comparison to the offspring produced when preying on E. kuehniella eggs. This resulted in higher than expected demographic indexes for N. tenuis when compared to M. pygmaeus (e.g., the intrinsic rates of increase were 0.127 and 0.005, respectively). Our results support previous studies on the potential of N. tenuis has as biological control agent of T. absoluta, and indicate that the role of M. pygmaeus in controlling T. absoluta in the absence of other food sources is possibly limited.     

Olfactory response of a predatory mirid to herbivore induced plant volatiles: multiple herbivory vs. single herbivory

Plants infested with a single herbivore species can attract natural enemies through the emission of herbivore‐induced plant volatiles (HIPVs). However, under natural conditions plants are often attacked by more than one herbivore species. We investigated the olfactory response of a generalist predators Macrolophus caliginosus to pepper infested with two‐spotted spider mites, Tetranychus urticae, or green peach aphid, Myzus persicae, vs. plants infested with both herbivore species in a Y‐tube olfactometer set up. In addition, the constituents of volatile blends from plants exposed to multiple or single herbivory were identified by gas chromatography‐mass spectrometry (GC‐MS). The mirid bugs showed a stronger response to volatiles emitted from plants simultaneously infested with spider mites and aphids than to those emitted from plants infested by just one herbivore, irrespective of the species. Combined with results from previous studies under similar conditions we infer that this was a reaction to herbivore induced plant volatiles. The GC‐MS analysis showed that single herbivory induced the release of 22 additional compounds as compared with the volatiles emitted from clean plants. Quantitative analyses revealed that the amount of volatile blends emitted from pepper infested by both herbivores was significantly higher than that from pepper infested by a single herbivore. Moreover, two unique substances were tentatively identified (with a probability of 94% and 91%, respectively) in volatiles emitted by multiple herbivory damaged plants: α‐zingiberene and dodecyl acetate.