Predatory Mirid Research Articles

Comparative biocontrol potential of three predatory mirids when preying on sweet pepper key pests

Pest management in protected sweet pepper crops mainly rely on biological control (BC) strategies. Recently, the zoophytophagous predatory mirids, Nesidiocoris tenuis, Macrolophus pygmaeus, and Dicyphus maroccanus, proved to be effective in the control of aphids on sweet pepper, for which the current biological control strategies have been meagre. The next step to integrate the possible use of these mirids in sweet pepper BC practices would be to ascertain their potential control on other sweet pepper pests. In this research, a comparative study to assess the establishment and the efficacy of N. tenuis, M. pygmaeus, and D. maroccanus on the two sweet pepper key pests; the thrips, Frankliniella occidentalis, and the whitefly, Bemisia tabaci was conducted. This study was carried out with two different temperature regimes, 20 °C and 27 °C, which simulated the mean temperatures registered in the two main crop cycles in Spain (the winter and summer planting period). Both, N. tenuis and M. pygmaeus were able to establish on sweet pepper and significantly reduced the number of F. occidentalis and B. tabaci adults, larvae and nymphs. Macrolophus pygmaeus had the highest density at 20 °C, whereas N. tenuis was more abundant at 27 °C. In contrast, D. maroccanus was less abundant under both temperatures studied; and did not reduce neither F. occidentalis nor B. tabaci infestations in this crop. None of the three mirids were observed to cause any damage to the pepper plant. The implications of these results applied to the use of mirids in sweet pepper crops are discussed.

Comparative Effectiveness and Injury to Tomato Plants of Three Neotropical Mirid Predators of Tuta absoluta (Lepidoptera: Gelechiidae).

Tuta absoluta (Meyrick; Lepidoptera: Gelechiidae) is a key pest of tomato and is quickly spreading over the world. We conducted an experiment aimed at evaluating the control capacity and risk for plant damage of three Neotropical mirid species, Campyloneuropsis infumatus (Carvalho; Hemiptera: Miridae), Engytatus varians (Distant; Hemiptera: Miridae) and Macrolophus basicornis (Stal; Hemiptera: Miridae) on T. absoluta infested tomato plants in large cages in an experimental greenhouse. During three successive periods of 9 wk each, we followed population development of the three mirids when exposed to T. absoluta, and of T. absoluta alone in separate cages in the greenhouse. We determined weekly the numbers of T. absoluta eggs and larvae per leaf, the number of mirid predators per leaf, the percentage of damaged leaves and fruits by T. absoluta, and the weight of fruits. Two of the mirid predators, C. infumatus and M. basicornis, successfully established on T. absoluta infested tomato plants and significantly reduced T. absoluta numbers, which ultimately resulted in an increased yield. These two mirid species hardly injured tomato plants or fruits as a result of plant feeding. Surprisingly, the species E. varians, which showed high predation rates in laboratory experiments, did not establish and reduce pest populations in any of the tests.

Zoophytophagous mirids provide pest control by inducing direct defences, antixenosis and attraction to parasitoids in sweet pepper plants.

In addition to their services as predators, mirid predators are able to induce plant defences by phytophagy. However, whether this induction occurs in sweet pepper and whether it could be an additional benefit to their role as a biological control agent in this crop remain unknown. Here, these questions were investigated in two model insects, the mirids Nesidiocoris tenuis and Macrolophus pygmaeus. Plant feeding behaviour was observed in both N. tenuis and M. pygmaeus on sweet pepper and occupied 33% and 14% of total time spent on the plant, respectively. The punctures caused by mirid plant feeding induced the release of a blend of volatile organic compounds (VOCs) which repelled the herbivore pests Frankliniella occidentalis and Bemisia tabaci and attracted the whitefly parasitoid Encarsia formosa. The repellent effect on B. tabaci was observed for at least 7 days after initial exposure of the plant to N. tenuis, and attraction of E. formosa remained functional for 14 days. Plant defences induced by the feeding of mirid predators, their subsequent effects on the behaviour of both pests and natural enemies, and the persistence of these observed effects open the door to new control strategies in the sweet pepper crop. Further application of this research is discussed, such as the vaccination of plants by zoophytophagous mirids in the nursery before transplantation. © 2017 Society of Chemical Industry.

The potential of Dicyphus hesperus as a biological control agent of potato psyllid and sweetpotato whitefly in tomato.

The potential of the mirid predator Dicyphus hesperus Knight (Heteroptera: Miridae) as a biological control agent of the sweetpotato whitefly, Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) and the potato psyllid, Bactericera cockerelli Sulcer (Hemiptera: Psyllidae) in tomato was investigated in two experiments. The first experiment focused on the study of the life history traits of D. hesperus when fed on nymphs of the potato psyllid compared with the factitious prey Ephestia kuehniella Zeller (Lepidoptera: Pyrallidae) eggs. Although reproductive and development rates were higher on E. kuehniella eggs, the predator exhibited a good intrinsic rate of natural increase (rm) when feeding on B. cockerelli nymphs (rm: B. cockerelli 0.069 ± 0.0001; E. kuehniella 0.078 ± 0.0001), thus reflecting good potential as a biocontrol agent of this pest. The second experiment focused on the efficacy of D. hesperus as a biocontrol agent of the potato psyllid and the sweetpotato whitefly in a tomato greenhouse. Prey species were offered individually or together in a series of five treatments in greenhouse cages. Results showed that the predator was able to establish and suppress populations of both pests inhabiting tomato plants when pests occurred alone or together. Thus, D. hesperus was demonstrated to be a suitable biocontrol agent of these two important pests that could be used in tomato greenhouses.

Does Foraging Experience Affect the Responses of the Predator Dicyphus hesperus Knight to Prey-Induced Volatiles?

The predatory mirid bug Dicyphus hesperus Knight (Hemiptera: Miridae) is a native North America species with high potential as biological control agent of the potato psyllid, Bactericera cockerelli Sulcer (Hemiptera: Triozidae), which is a major solanaceous pest. Olfactory responses of D. hesperus to volatiles from plants infested with the potato psyllid and the effect of foraging experience on search efficacy were studied. Using a Y-tube olfactometer, we found that naïve females had no preference in choice tests between either uninfested tomato plants, or Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) eggs-infested plants, and clean air. Naïve females showed an innate positive response to B. cockerelli-infested plants, but no preference when given a choice between uninfested tomato plants and E. kuehniella eggs-infested plants. However, females with experience of foraging on B. cockerelli-infested plants showed a strong preference for B. cockerelli-infested plants (78% response) in choice tests with uninfested tomato plants and E. kuehniella eggs-infested plants. Implications of learning for augmentative biological control are discussed.

Attraction of Three Mirid Predators to Tomato Infested by Both the Tomato Leaf Mining Moth Tuta absoluta and the Whitefly Bemisia tabaci.

Plants emit volatile compounds in response to insect herbivory, which may play multiple roles as defensive compounds and mediators of interactions with other plants, microorganisms and animals. Herbivore-induced plant volatiles (HIPVs) may act as indirect plant defenses by attracting natural enemies of the attacking herbivore. We report here the first evidence of the attraction of three Neotropical mirid predators (Macrolophus basicornis, Engytatus varians and Campyloneuropsis infumatus) toward plants emitting volatiles induced upon feeding by two tomato pests, the leaf miner Tuta absoluta and the phloem feeder Bemisia tabaci, in olfactometer bioassays. Subsequently, we compared the composition of volatile blends emitted by insect-infested tomato plants by collecting headspace samples and analyzing them with GC-FID and GC-MS. Egg deposition by T. absoluta did not make tomato plants more attractive to the mirid predators than uninfested tomato plants. Macrolophus basicornis is attracted to tomato plants infested with either T. absoluta larvae or by a mixture of B. tabaci eggs, nymphs and adults. Engytatus varians and C. infumatus responded to volatile blends released by tomato plants infested with T. absoluta larvae over uninfested plants. Also, multiple herbivory by T. absoluta and B. tabaci did not increase the attraction of the mirids compared to infestation with T. absoluta alone. Terpenoids represented the most important class of compounds in the volatile blends and there were significant differences between the volatile blends emitted by tomato plants in response to attack by T. absoluta, B. tabaci, or by both insects. We, therefore, conclude that all three mirids use tomato plant volatiles to find T. absoluta larvae. Multiple herbivory did neither increase, nor decrease attraction of C. infumatus, E. varians and M. basicornis. By breeding for higher rates of emission of selected terpenes, increased attractiveness of tomato plants to natural enemies may improve the effectiveness of biological control.

Ecology, Worldwide Spread, and Management of the Invasive South American Tomato Pinworm, Tuta absoluta: Past, Present, and Future.

The South American tomato pinworm, Tuta absoluta (Meyrick), is native to the western Neotropics. After invading Spain in 2006, it spread rapidly throughout Afro-Eurasia and has become a major threat to world tomato production. Integrated pest management (IPM) strategies have been developed, but widespread insecticide use has caused selection for insecticide resistance as well as undesirable effects on key beneficial arthropods. Augmentation and conservation biological control relying on omnivorous mirid predators has proved successful for management of T. absoluta, where implementation is dependent on abiotic, biotic (e.g., alternative prey), and anthropogenic factors (e.g., pesticides). Research has been carried out on larval parasitoids, showing potential for further development of sustainable control. The development of resistant tomato varieties is ongoing, but they are not commercially available yet. Knowledge gaps remain to be filled to optimize IPM packages on tomato crops and to help prevent further spread worldwide.

Investigating alternative methods for enhancing the establishment of the zoophytophagous mirid Nesidiocoris tenuis (Reuter) in greenhouse tomato crops

The zoophytophagous mirid Nesidiocoris tenuis (Reuter) (Heteroptera: Miridae) is an effective natural enemy of some major pests of tomatoes in the Mediterranean region. In this area the colonization of protected tomato crops by this biocontrol agent may be hampered by the application of measures aimed at avoiding the transmission to tomato plants of insect-vectored diseases (e.g. TYLCD). Furthermore, various factors, such as the scarce availability of preys on crop plants and the severe deleafing of tomato plants, may affect the population build-up of artificially introduced predatory mirids. Since these natural antagonists have become commercially available in Europe, several methods have been explored to enhance their establishment on greenhouse tomatoes. This work reports the results of experiments carried out to investigate the effects of different release methods on the establishment of N. tenuis in commercial greenhouse tomato crops grown in southern Sardinia (Italy). The techniques tested can be summarized as follows: a) release of mirids before transplanting; b) introduction into release points covered by non-woven films; c) introduction into uncovered feeding points; d) traditional release method. N. tenuis was introduced at a rate of 0.8 individuals per stem grown (2.4-3.2 mirids plant-1) in crops planted during late summer. All methods except the traditional one envisaged the distribution of 0.01 g plant-1 of Ephestia kuehniella Zeller eggs, supplied three times at two-week intervals, as an alternative food source. Two months after planting, pre-plant release and the introduction into covered or uncovered release points allowed the predatory mirid to reach significantly higher densities in comparison with the traditional release method. Under the conditions tested, the anticipation of release and the supply of an artificial food source appear to be decisive factors for enhancing the establishment of N. tenuis in greenhouse tomato crops.

First Record of the South American Leafminer Liriomyzα huidobrensis (Blanchard) (Diptera: Agromyzidae) in Greece

In mid autumn 1992 the South American leaf-miner Liriomyza huidobrensis (Blanchard) was firstly recorded on greenhouse cucumbers, melons, beans and outdoor beans, broad beans and lettuce in the following locations of Crete: 1) Mires, Tymbaki, Antiskari at Messara valley of Southern Crete 2) Filissia in the midland and 3) Platanias and Kokini Chani in Northern Crete. The following year L. huidobrensis had spread all over Crete (Ierapetra, Stomion, Koutsoura, Chania etc.) while melon and potato leaves which were sent to our laboratory from mainland Greece, Pirgos (Peloponissos) and Chalkida (Evia island), were found heavily damaged by the same leafmincr. The different types of mines (it usually mines the leaf alongside the veins), the colour of pupae (blackish) and the sudden attack of some plants (lettuce, broad beans, onions) which have never been damaged by the known local leafminers as yet, indicated that it was a newly introduced species. The new leafminer alerted the growers due to the high crop losses on outdoor and greenhouse vegetables (lettuce, broad beans, beans etc) despite the frequent application of registered insecticides. In the following year an extensive survey started to investigate its distribution and host plant in the greenhouses and outdoor vegetables and ornamentals in Crete. L. huidobrensis, a quarantine insect, is a polyphagous leafminer distributed in most biogeographical regions. It is native in South American countries from which it was spread soon in North America, Asia and Europe. In Europe it was first noticed in Holland, England and France in 1989 causing considerable damage to vegetables and ornamentals. It mines the spongy mesophyll reducing the photosynthesis more than the other leafminers. This type of mines is not easily visible, unless the leaf is observed through transmitted sunlight or artificial light. This method was applied to ensure accurate detection of larvae and their parasitoids under a stereoscope. In our observations we found mines in leaves and cucumber fruits as well. Studies of its life cycle on greenhouse beans and melons revealed that most pupae (98%) remain on the bean leaves outside a hole in the autumn, while a few fall on the ground. The number of pupae collected from ten leaves per 24h was: 5.7±1.6 on lettuce, 17.07±4.1 on beans, 24.2±7.3 on melon, 6.0±2 on broad bean leaves. During the survey the following host plants were recorded: Chemical control could be effective by applying certain insecticides (abamectin, triazophos, imidacloprid, heptenophos etc.) while biological control seems to be rather effective by the known parasitoids, which are already used against the tomato leafminer Liriomyza bryoniae Kalt. Biological control of L. huidobrensis was effective on lettuce by means of repeated releases of Dacnusa sibirica Telenga and Diglyphus isaea (Walker) but so far native parasitoids proved to be able to control the pest. Mass trapping with coloured sticky traps seems to be also a potential method in IPM programmes. The mortality of pupae collected from heavily treated greenhouse plants with insecticides varied from 65 to 74% while that of untreated plants was between 18-25%. No pupal parasitoids were recorded but D. isaea and D. sibirica were both recorded as larval parasitoids. D. isaea was abundant all over the year while D. sibirica only in spring-summer period. These two parasitoids were able, in certain cases, to control sufficiently the leaf miner in untreated greenhouse cucumber and bean plants. The neem seed extract (Azadirachta indica) applied on outdoor tomatoes in Antiskari (Southern Crete) proved harmless both on hymenoptera and on the mirid predator Macrolophus caliginogus Wagner. Despite its weak larvicide action on L. huidobrensis it was very effective in conjuction with parasitoids consisting of a promising candidate in IPM programmes.

Thermal effects on the biological parameters of the predatory mirid Pilophorus gallicus (Hemiptera: Miridae)

AbstractPilophorus gallicus Remane (Hemiptera: Miridae) is a predatory mirid reported in deciduous trees in the western Mediterranean area. This work aimed to determine the biological and demographic parameters for this species at different temperatures (15, 20, 25 and 30°C). Egg hatching times shortened from 57.8 days at 15°C to 9.2 days at 30°C, and nymphal development times declined from 62.8 days at 15°C to 11.1 days at 30°C. The hatching and nymphal survival rates were low at 15 and 30°C. The lower thermal thresholds for the egg and nymphal development were 12.4 and 12.0°C, respectively. These high thermal thresholds could be a safety mechanism to avoid the emergence of nymphs in the unfavorable winter period. Female weight increased between 15 and 25°C and decreased at 30°C. The fecundity increased from 70.2 eggs per female at 15°C to 212.4 eggs per female at 25°C, and decreased to 88.5 eggs per female at 30°C. Fertility ranged from 9.4% at 15°C to 40.9% at 25°C, being 24.9% at 30°C. The intrinsic rate of natural increase (rm) rose from 0.001 to 0.081 between 15 and 25°C and decreased to 0.05 at 30°C. In summary, this species performs poorly at low temperatures and has a relative tolerance of high temperatures (30°C); its performance was best at 25°C. Knowledge of the variation in the biological parameters with temperature may be very useful for the understanding of its ecology and population dynamics.

Qualitative and Quantitative Differences in Herbivore-Induced Plant Volatile Blends from Tomato Plants Infested by Either Tuta absoluta or Bemisia tabaci

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

Life-History Traits of Macrolophus pygmaeus with Different Prey Foods.

Macrolophus pygmaeus Rambur (Hemiptera: Miridae) is a generalist predatory mirid widely used in augmentative biological control of various insect pests in greenhouse tomato production in Europe, including the invasive tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera, Gelechiidae). However, its biocontrol efficacy often relies on the presence of alternative prey. The present study aimed at evaluating the effect of various prey foods (Ephestia kuehniella eggs, Bemisia tabaci nymphs, Tuta absoluta eggs and Macrosiphum euphorbiae nymphs) on some life history traits of M. pygmaeus. Both nymphal development and adult fertility of M. pygmaeus were significantly affected by prey food type, but not survival. Duration of nymphal stage was higher when M. pygmaeus fed on T. absoluta eggs compared to the other prey. Mean fertility of M. pygmaeus females was greatest when fed with B. tabaci nymphs, and was greater when offered M. euphorbiae aphids and E. kuehniella eggs than when offered T. absoluta eggs. Given the low quality of T. absoluta eggs, the efficacy of M. pygmaeus to control T. absoluta may be limited in the absence of other food sources. Experiments for assessing effectiveness of generalist predators should involve the possible impact of prey preference as well as a possible prey switching.

Resilience and robustness of IPM in protected horticulture in the face of potential invasive pests

Recently, various approaches for the biological control of major pests in protected crops have successfully been adopted. These successes have primarily occurred via the selection, release and/or conservation of generalist native predators that naturally colonize Mediterranean crops that are highly adapted to local environmental conditions. These generalist predators have resulted very effective in controlling key pests; as a result, pesticide use has been reduced considerably. In addition, because these predators are typically highly polyphagous, horticultural crops have become more resilient to newly emerging pests, which are preyed upon by these predators. Possibilities to further strengthen pest management in horticultural crops have recently arisen, such as the use of beneficial microbes (BM) to induce plant resilience. In this review, we used a tomato crop as an example to present two new, highly interrelated plant defense induction strategies: the use of Miridae zoophytophagous predators and the use of Trichoderma spp. microbial biological control agents. Both the mirid predators and Trichoderma symbiotic fungi can activate direct and indirect plant defense responses, which may increase the robustness of pest management against invading organisms. The practical use of these new approaches is discussed.

Betraying its presence: identification of the chemical signal released by Tuta absoluta-infested tomato plants that guide generalist predators toward their prey

Plants modify their volatile chemical signature under pest infestation, which might directly or indirectly improve their defence against threats. These chemical signals have potential in integrated pest management strategies. Macrolophus pygmaeus (Rambur) [Heteroptera: Miridae] is a generalist predatory insect widely used to control the tomato leaf miner, Tuta absoluta (Meyrick) [Lepidoptera: Gelechiidae]. Based on a previous study demonstrating the ability of this mirid species to discriminate non-infested versus T. absoluta-infested tomato plants, our objective was to identify plant volatile chemicals (herbivore-induced plant volatiles—HIPVs) guiding the behaviour of such a generalist predator towards its prey. First, we used coupled gas chromatography-mass spectrometry-electroantennographic detection analysis to screen for active antenna components from the volatile blend released by T. absoluta-infested tomato plants. Dose responses associated with each isolated HIPV were also performed using an electroantennograph. Subsequently, behavioural assays were conducted in a double-choice olfactometer to analyse and identify the behaviourally active chemicals eliciting olfactory responses. Twenty-one total compounds induced antennal responses and six of the 21 evoked positive attractions in M. pygmaeus: (E)hex-2-enal, 2-carene, α-pinene, β-phellandrene, hexanal, and linalool. A synthetic blend of active HIPVs induced olfactory responses as well as attraction in the bioassays. Our results provided evidence the generalist mirid predator M. pygmaeus uses chemical cues from infested tomato plants to identify plants infested by prey. We discussed how these results can be used to improve existing biological approaches to control the tomato leaf miner, T. absoluta.

Trading direct for indirect defense? Phytochrome B inactivation in tomato attenuates direct anti-herbivore defenses whilst enhancing volatile-mediated attraction of predators.

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

Population genetic structure of the biological control agent Macrolophus pygmaeus in Mediterranean agroecosystems.

Biological control of agricultural pests relies on knowledge of agroecosystem functionality, particularly when affected by the use of mass-produced biological agents. Incorporating pre- and/or post-release information such as genetic diversity and structure on these agents using molecular-based approaches could advance our knowledge of how they perform in agroecosystems. We evaluated the population genetics of Macrolophus pygmaeus, the most widely used predatory mirid against many arthropod pests of greenhouse crops in the Mediterranean region, using the mitochondrial Cytb sequence and microsatellite data, and population genetics and phylogeny approaches. We investigated commercially mass-produced insects (i.e., commercial insects either mass-reared in the laboratory for many generations, or purchased by farmers and released in the greenhouses) and "wild" insects (i.e., that occur naturally outside or are collected in nature for release in the greenhouses). The mirids were mainly collected in agroecosystems in which solanaceous plants are grown in northern Spain, southern France and Greece. Both molecular markers and approaches distinguished 2 genetically differentiated populations. The less genetically diverse population, hereafter named the "commercial" strain included all individuals from laboratory mass-rearings and most releases of commercially bred individuals. The most genetically diverse population mainly comprised individuals originating from noncultivated environments, or from releases of "wild" individuals. Rare examples of hybridization between M. pygmaeus from the 2 populations were observed and asymmetric gene flow was revealed. These findings provide new insights into what happens to M. pygmaeus released in the agroecosystems we studied, and show that it is possible to monitor some commercial strains.

Functional Responses of Three Neotropical Mirid Predators to Eggs of Tuta absoluta on Tomato.

Tuta absoluta (Meyrick) has quickly developed into a significant tomato pest worldwide. While the recently found mirid predators Macrolophus basicornis (Stal), Engytatus varians (Distant) and Campyloneuropsis infumatus (Carvalho) of this pest are able to establish and reproduce on tomato, biological knowledge of these mirids is still limited. Here we describe the functional response of the three mirid predators of the tomato pest T. absoluta when offered a range of prey densities (four, eight, 16, 32, 64, 128 and 256 eggs) during a 24 h period inside cylindrical plastic cages in the laboratory. Engytatus varians and M. basicornis showed a type III functional response, whereas C. infumatus showed a type II functional response. At the highest prey densities, C. infumatus consumed an average of 51.0 eggs, E. varians 91.1 eggs, and M. basicornis 100.8 eggs. Taking all information into account that we have collected of these three Neotropical mirid species, we predict that M. basicornis might be the best candidate for control of the tomato borer in Brazil: it has the highest fecundity, the largest maximum predation capacity, and it reacts in a density-dependent way to the widest prey range.

Local landscape heterogeneity affects crop colonization by natural enemies of pests in protected horticultural cropping systems

Conservation biological control of crop pests is considered a promising strategy in protected horticultural cropping systems. In Mediterranean regions, crop colonization by native predatory mirid bugs is frequent but highly heterogeneous among crop production sites. The contribution of landscape heterogeneity to the variability in colonization levels remains little explored, although it is a major driver of the abundance of natural enemies of pests in open field cropping systems. The goal of our study was to assess whether landscape heterogeneity (land-cover diversity, percent cover, and spatial configuration) at a local scale (up to 300m) affects colonization of protected crops by Macrolophus and Dicyphus mirids, and whether these effects are significantly greater or lower than those of crop management practices. In southern France (Roussillon) in 2010 and 2011, we collected data on mirid populations, pest infestation levels, crop management practices, and landscape heterogeneity within 300m buffers. We investigated relationships between natural enemies, farming practices, and landscape metrics using an algorithm for random forests combined with GLM analyses. Tomato crops were colonized the most by Macrolophus mirids in landscapes with fallow, suggesting that these semi-natural habitats contribute to mirid movements between protected crops and the surrounding landscape. In contrast, crop colonization by mirids was reduced by nearby orchard, which reflected either sink effects due to intensive management practices or dilution effects linked to herbaceous resources. Landscape composition and configuration had similar effects on mirid populations. Macrolophus and Dicyphus mirids responded the most to lanscape heterogeneity at different spatial scales (200–300 and 100m scales, respectively), possibly reflecting different dispersal abilities. However, effects of landscape heterogeneity on mirids were lower than those of crop management practices. Our study suggests that maintaining large areas of semi-natural habitats with ruderal vegetation typical of fallow is important to ensure colonization of protected crops by natural enemies of pests. Our findings emphasize that converting farms from conventional to organic production systems and adopting integrated plant management practices remain the most promising strategies to enhance populations of natural enemies in protected horticultural crops in Mediterranean regions.

Residual Acute Toxicity of Some Modern Insecticides Toward Two Mirid Predators of Tomato Pests.

The successful integration of chemical and biological control strategies for crop pests depends on a thorough evaluation of the effects of pesticides on the natural enemies of pests. A case-by-case review is difficult to achieve because of the many combinations of pests, natural enemies, and crops that need to be tested. Within this framework, we tested and compared seven insecticides representative of four different modes of action (MoAs) groups on closely related predators (Miridae): flubendiamide, spirotetramat, metaflumizone, and sulfoxaflor on Nesidiocoris tenuis Reuter and flubendiamide, spiromesifen, indoxacarb, and imidacloprid on Macrolophus basicornis (Stal). We follow the standardized methodology of the International Organization for Biological Control, a sequential testing exposure scheme. The lethal effect of each insecticide was evaluated in adults after three days of contact with treated surfaces in the laboratory, extended laboratory, and semifield tests (inert substrate, tomato leaves, and tomato plant as the treated surface, respectively). Flubendiamide, spiromesifen, and spirotetramat were classified as harmless (class 1), metaflumizone was slightly harmful (class 2) but persistent, indoxacarb was harmless (class 1), and sulfoxaflor and imidacloprid were toxic (class 4) and exhibited a long residual activity. Our results suggest similarities in the acute toxicities of insecticides from the same MoA group on related species of natural enemies.

Effects of Sublethal Concentrations of Insecticides on the Functional Response of Two Mirid Generalist Predators

The use of agrochemicals particularly pesticides, can hamper the effectiveness of natural enemies, causing disruption in the ecosystem service of biological control. In the current study, the effects of the insecticides thiacloprid and chlorantraniliprole on the functional response curves were assessed for two mirid predator nymphs, Macrolophus pygmaeus Rambur and Nesidiocoris tenuis Reuter. In the absence of insecticides, both predators exhibited a type II functional response when feeding on eggs of the moth Ephestia kuehniella. N. tenuis seems to be a more efficient predator than M. pygmaeus, as model estimated handling time was significantly lower for the former than for the latter. Residual exposure of M. pygmaeus to sublethal concentrations of either insecticide was associated with a change in the asymptote but not the type of the functional response curve. Thiacloprid seems to be the least compatible with M. pygmaeus, as it led to both a significant reduction of the attack rate and an increase in handling time. In contrast, chlorantraniliprole exposure significantly increased the handling time, but not the attack rate of the predator. Residual exposure of N. tenuis to sublethal concentrations of either insecticide did not have a significant effect on the type nor the parameters of the functional response model. The results show that pesticide residues that do not have lethal effects on beneficial arthropods can reduce prey consumption depending on predator species and on likely risks associated with toxicity.