Macrolophus caliginosus (Wagner) as an Intraguild Prey for the Zoophytophagous Dicyphus tamaninii Wagner (Heteroptera: Miridae)

The zoophytophagous predator Macrolophus caliginosus (Wagner) (Heteroptera: Miridae) has previously been identified as a potential prey for the intraguild zoophytophagous predator Dicyphus tamaninii Wagner. Its value as an intraguild prey was tested for D. tamaninii nymphal development and adult survival. In the laboratory, plant (red tomato fruit, green tomato fruit, tomato leaf) and animal (aphids, whiteflies, pyralid eggs) resources were compared to frozen nymphs of M. caliginosus as an intraguild resource for D. tamaninii. M. caliginosus nymphs allowed complete and rapid development of D. tamaninii nymphs and generated low mortality of nymphal and adult stages. Performances were higher with the intraguild M. caliginosus resource than with plant resources. Tomato leaves did not allow the complete nymphal development of D. tamaninii. Tomato fruit generated lighter adults and doubled the nymphal developmental time compared with the M. caliginosus resource. In the animal resource group, there were no differences between the M. caliginosus and the other treatments (aphids, whiteflies, pyralid eggs) for nymphal mortality, average number of molts, nymphal developmental time, adult weight, and adult survival. M. caliginosus should be considered a high-quality resource for D. tamaninii.     

Development and survival ofOrius albidipennis andO. levigatus (Het.: Anthocoridae) on various diets

The effect of various diets on nymphal development and survival of two predaceous anthocorid bugs,Orius albidipennis (Reuter) andO. laevigatus (Fieber) was investigated in the laboratory. Five different diets were compared: eggs ofEphestia kuehniella Zeller; eggs ofE. kuehniella plus mixed flower pollen; only mixed flower pollen; pollen from sweet pepper (Capsicum annuum L. cv. Mazurka) flowers; and sweet pepper plants. A high percentage of predators successfully completed nymphal development on those diets containing lepidopterous eggs. When fed on sweet pepper pollen, the survival percentages were 65% forO. laevigatus and 38% forO. albidipennis. No nymphs of either species completed the nymphal stage on mixed flower pollen or on sweet pepper plants. Development was significantly faster on diets containing eggs ofE. kuehniella. Results are discussed in relation to the capability of the bugs to survive periods of prey scarcity and to the optimization of release strategies for these predators in the greenhouse.     

Intraguild predation by the generalist predator Orius majusculus on the parasitoid Encarsia formosa

Intraguild predation of Orius majusculus (Reuter) (Heteroptera: Anthocoridae) on Encarsia formosa (Gahan) (Hymenoptera: Aphelinidae), both natural enemies of Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae), was studied under laboratory conditions. The experiments quantified prey consumption by 5th instar nymphs and adults of O. majusculus offered unparasitised 3rd, early 4th or 4th instar B. tabaci nymphs or parasitised nymphs containing 2nd or 3rd larval instar or pupal parasitoids. In addition, prey preference of the two stages of O. majusculus for parasitised or unparasitised whitefly nymphs was studied using nine different prey combinations. Both predator stages readily preyed upon on both unparasitised and parasitised B. tabaci. In no-choice experiments, predation on 3rd instar E. formosa by adult predators was the highest, while predator nymphs preyed most on unparasitised 3rd instar B. tabaci and 2nd instar parasitoids. Predation of predator stages was lowest on 4th instar B. tabaci and E. formosa pupae. In all prey combinations, both stages of O. majusculus showed a significant preference for parasitised over unparasitised whitefly nymphs except for the combination of 5th instars of O. majusculus with early 4th instar whiteflies and E. formosa pupae. The results indicate that intraguild interactions between O. majusculus and E. formosa may have negative effects on biological control of B. tabaci.     

Comparison of prey consumption by Dicyphus tamaninii reared conventionally, and on a meat-based diet

The zoophytophagous predator Dicyphustamaninii Wagner (Heteroptera: Miridae) hasbeen successfully reared for more than fivegenerations on a meat-based diet, and in theabsence of a plant as a substrate foroviposition and feeding. We compared thepredation efficiency of D. tamaniniiproduced on this diet with those rearedconventionally on Ephestia kuehniellaeggs (Zeller) (Lepidoptera: Pyralidae) andtobacco plants. Their performances wereevaluated on two prey, the greenhouse whiteflyTrialeurodes vaporariorum Westwood(Homoptera: Aleyrodidae) and the cotton aphidAphis gossypii Glover (Homoptera: Aphididae). Their tendency to cannibalisticbehaviour was also evaluated.Nymphs of D. tamaninii produced on themeat diet consumed a similar number ofgreenhouse whitefly pupae after 24 and 48 hoursto nymphs reared by the conventional method.Diet-reared females consumed significantly morewhitefly pupae after 24 and 48 hours thancontrol females. When the cotton aphid wasoffered, diet-reared D. tamaninii nymphsand females consumed similar numbers of prey tocontrol D. tamaninii. There was nosignificant increase in cannibalistic behaviourof diet-reared D. tamaninii after 3 and 5days of interaction.These results show that, after fivegenerations, the predation efficiency and thetendency to cannibalism of meat-reared D.tamaninii is similar to that ofconventionally-reared individuals.     

Prey-mediated effects of mCry51Aa2-producing cotton on the predatory nontarget bug Orius majusculus (Reuter)

Genetically engineered (GE) cotton, MON 88702, is protected against certain sucking pests, such as plant bugs and thrips, by producing mCry51Aa2, a modified protein from Bacillus thuringiensis (Bt). Predatory pirate bugs (Orius spp.), natural enemies contributing to biological pest control, are also sensitive to the insecticidal protein when exposed continuously to high concentrations. We evaluated effects of MON 88702 on Orius majusculus when fed prey types with different mCry51Aa2 concentrations. When neonates were provided exclusively Tetranychus urticae spider mites reared on MON 88702 (high mCry51Aa2 content), adverse effects on predator survival and development were confirmed, compared with specimens fed prey from near-isogenic non-Bt cotton. When fed a mixture of T. urticae and Ephestia kuehniella eggs (mCry51Aa2-free), predator life table parameters were similar to the treatment where eggs were fed exclusively. When mCry51Aa2-containing spider mites were provided for a limited time at the beginning or the end of juvenile development, effects were less pronounced. While pirate bug nymphs showed similar consumption rates for prey from Bt and non-Bt cotton, choice experiments revealed a preference for E. kuehniella eggs over spider mites. Lepidopteran larvae (Spodoptera littoralis, high mCry51Aa2 content) or cotton aphids (Aphis gossypii, mCry51Aa2-free) reared on MON 88702 as alternative prey did not result in adverse effects on O. majusculus. Our study suggests limited risk of mCry51Aa2-producing cotton for O. majusculus, because its sensitivity for the Bt protein is relatively low and its natural food consists of diverse prey species with varying concentrations of Bt protein.     

Alaboratory evaluation ofAnthocoris nemorum andA. nemoralis [Hem.: Anthocoridae] as predators ofPhorodon humuli [Hom.: Aphididae]

Anthocoris nemorum (L.) andA. nemoralis (F.) were reared on apterous hop aphids,Phorodon humuli (Schrank), at 20±0.5°C.A. nemorum andA. nemoralis killed an average of 255 and 174 aphids respectively during nymphal development, and the adults killed 37 and 33 per day respectively. Small anthocorid nymphs selectively killed small aphids but adult anthocorids and 5th instar nymphs killed aphids of every size. Mean development times from emergence to final moult were 22 and 16 days forA. nemorum andA. nemoralis respectively.     

Biological control of aphids in the presence of thrips and their enemies

Generalist predators are often used in biological control programs, although they can be detrimental for pest control through interference with other natural enemies. Here, we assess the effects of generalist natural enemies on the control of two major pest species in sweet pepper: the green peach aphid Myzus persicae (Sulzer) and the western flower thrips Frankliniella occidentalis (Pergande). In greenhouses, two commonly used specialist natural enemies of aphids, the parasitoid Aphidius colemani Viereck and the predatory midge Aphidoletes aphidimyza (Rondani), were released together with either Neoseiulus cucumeris Oudemans, a predator of thrips and a hyperpredator of A. aphidimyza, or Orius majusculus (Reuter), a predator of thrips and aphids and intraguild predator of both specialist natural enemies. The combined use of O. majusculus, predatory midges and parasitoids clearly enhanced the suppression of aphids and consequently decreased the number of honeydew-contaminated fruits. Although intraguild predation by O. majusculus on predatory midges and parasitoids will have affected control of aphids negatively, this was apparently offset by the consumption of aphids by O. majusculus. In contrast, the hyperpredator N. cucumeris does not prey upon aphids, but seemed to release aphids from control by consuming eggs of the midge. Both N. cucumeris and O. majusculus did not affect rates of aphid parasitism by A. colemani. Thrips were also controlled effectively by O. majusculus. A laboratory experiment showed that adult predatory bugs feed on thrips as well as aphids and have no clear preference. Thus, the presence of thrips probably promoted the establishment of the predatory bugs and thereby the control of aphids. Our study shows that intraguild predation, which is potentially negative for biological control, may be more than compensated by positive effects of generalist predators, such as the control of multiple pests, and the establishment of natural enemies prior to pest invasions. Future work on biological control should focus on the impact of species interactions in communities of herbivorous arthropods and their enemies.     

Functional responses of two chrysopid predators feeding onHelicoverpa armigera (lep.: noctuidae) and aphis gossypii (hom.: aphididae)

Predation onHelicoverpa armigera (Hubner) eggs andAphis gossypii (Glover) nymphs by 3rd instar larvae ofMallada desjardinsi (Navas) andChrysoperla congrua (Walker) was studied under laboratory conditions. Single predators that had been starved for 24 hours were isolated for 1 hour in 9 cm Petri dishes containing prey at densities of 5, 10, 15, 20 and 25 per dish. A type II functional response model gave a satisfactory fit to the data in case ofM. desiardinsi preying onH. armigera. However, with C.congrua, a type III model gave a slightly better fit. ForA. gossypii, functional responses of both predators did not differ from type II, withM. desjardinsi showing a significantly lower search rate and shorter handling time thanC. congrua. Implications of these findings are discussed     

On the biology of anthocorid bugs (Heteroptera,Anthocoridae), predators of grass aphids in the forest-steppe zone of West Siberia

Four species of the heteropteran family Anthocoridae, Orius niger Wolff., O. majusculus Reut., O. minutus L., and Anthocoris confusus Reut., feeding on grass aphids on grains and bird cherry occur in the foreststeppe zone of Western Siberia. Orius niger and O. majusculus possess the greatest population numbers, with 98% of all the bugs collected in 1987 and 1988 belonging to these species. In 1998–2000, O. niger was predominant (97–100%). Data on the bionomics, seasonal abundance, feeding intensity, and role of anthocorids in the control of aphids are reported. Density of Orius bugs on wheat has been shown to be independent of the preceding culture. Permanent wheat is a preferable habitat of the predatory anthocorids. Mass reproduction of Orius bugs on pea-oat and alfalfa has been recorded.     

Influence des basses températures sur les potentialités biologiques d'Orius laevigatus et d'Orius majusculus (Het.: Anthocoridae)

Résumé Des expérimentations ont permis de comparer l'influence de deux conditions de conservation au froid et de leur durée sur la longévité et la fécondité de deux cspèces d'anthocorides,Orius majusculus (Reuter) etOrius laevigatus (Fieber). La survie des adultes est meilleure dans les conditions thermopériodiques 13°C/3°C qu'à la température constante de 9°C. La longévité des femelles après passage au froid est d'autant plus grande que la durée d'exposition a été courte. La fécondité d'O. laevigatus ne subit pas de réduction significative après 50 jours de conservation en thermopériode alors que celle d'O. majusculus est fortement réduite après 20 jours dans les mêmes conditions.

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Summary Laboratory studies were done to compare the effect of two cold storage conditions on longevity and fecundity of two anthocorids,Orius majusculus (Reuter) andOrius laevigatus (Fieber). Survival of adults is better at a thermoperiodic condition of 13°C/3°C than at a constant temperature of 9°C. Female longevity decreases as the duration of exposure to cold conditions increases. Fecundity ofO. laevigatus is not significantly reduced after 50 days of exposure to thermoperiodic conditions even though those ofO. majusculus is strongly reduced after 20 days.

     

Suitability of greenbugs, cotton aphids, andHeliothis virescens eggs for development and reproduction ofOrius insidiosus

Development, fecundity, and longevity of the predator,Orius insidiosus (Say) (Heteroptera: Anthocoridae), when reared on greenbug [Schizaphis graminum (Rondani)], cotton aphid (Aphis gossypii Glover), or eggs of tobacco budworm [Heliothis virescens (F.)] with green beans or water were examined. Developmental time was shortest when predators were reared onH. virescens eggs and beans and longest when reared on cotton aphids and water. Predators were most fecund when fedH. virescens eggs. The inclusion of beans in the nymphal diet further enhanced fecundity when fed eggs. Longevity of both females and males was significantly shorter when reared on aphids than on eggs. Beans in the nymphal diet enhanced longevity of female predators only in combination with budworm eggs. FemaleO. insidiosus were largest when reared onH. virescens eggs. Addition of green beans in aphid treatments resulted in increased size ofO. insidiosus when compared to aphids and free water.     

Change in carbon stable isotope ratios of the predatory bug Orius majusculus after dietary shifts

Orius majusculus Reuter (Hemiptera: Anthocoridae) is an important component of the pest predatory complex in arable crops in Mediterranean areas. It moves between crops searching for prey, and improving knowledge on its dispersal abilities will help to develop conservation biological control strategies. Stable isotope ratios may be used as a tool for tracking insect movements, as the isotopic composition of insect tissues changes to reflect that of their diet when they undergo dietary shifts on moving between isotopically distinct crops. We carried out laboratory diet switch experiments with a stable isotope approach to infer information on dispersal of O. majusculus individuals among C3 and C4 crops to better understand isotopic field data collections. Switching the aphid food source caused a quick change in δ¹³C signatures, regardless of the original and final food source. Changes in the δ¹³C ratio of O. majusculus after diet switching fitted with an exponential model that showed similar turnover rates, and thus half‐lives, between shifting diets up to 20 days. Subsequently, whereas individuals feeding on C4 aphids did not survive, turnover rate decreased in individuals that switched from C4 to C3 aphids. However, δ¹³C traces from the original source remained in the predator until 25 days after switching, and this is enough time to help determine the movement of O. majusculus between crops in the field and to plan the timing of predator sampling and crop practices that may enhance predator ecological services. Orius majusculus that switched to a maize aphid diet showed different turnover rates between sexes, although this did not influence the pattern of switchover.     

Induction and termination of diapause inOrius predatory bugs

Photoperiodic induction of reproductive diapause at 18°C was investigated in fourOrius [Heteroptera: Anthocoridae] species.Orius insidiosus (Say) displayed a long-day response with a critical photoperiod between L11:D13 and L12:D12. Diapause in this species was terminated rapidly when the temperature and/or the daylength were increased.Orius majusculus (Reuter) also displayed a long-day response. The critical photoperiod fell between L14:D10 and L16:D8. Diapause in this species was not terminated within 14 days when both temperature and daylength were increased. InOrius albidipennis (Reuter) no diapause could be induced at photoperiods varying from L8:D16 to L16:D8. InOrius tristicolor (White) a high proportion of diapause was found at all photoperiods tested. The effect of temperature on photoperiodic induction of diapause was studied inO. insidiosus at L10:D14. Diapause occurred at 18°C, 21°C and 25°C, but not at 30°C. Again, diapause was terminated rapidly after transfer to 25°C/L16:D8. Exposing only the nymphal instars 1–5 to short daylength was not enough to induce diapause in the whole population ofO. majusculus. Orius predatory bugs are used as biocontrol agents against western flower thrips,Frankliniella occidentalis (Pergande) [Thysanoptera: Thripidael, in greenhouses. The consequences of photoperiodic induction of diapause for the success of early season releases ofOrius are discussed.     

Food quality of Ephestia eggs,the aphid Rhopalosiphum padi and mixed diet for Orius majusculus

We studied the food quality of the aphid Rhopalosiphum padi to the pirate bug Orius majusculus using Ephestia eggs as high-quality comparison prey. Several performance parameters were tested on individuals that had been reared and maintained on each of the two single-prey diets or on a mixed diet. All fitness parameters were lower in individuals fed aphids only, indicating poor food quality of this prey. Compared with the pure Ephestia egg diet, the mixed diet enhanced teneral mass, while adult survival and female starvation tolerance were negatively affected and all other traits were unaffected. Body protein proportions were constant across diets, whereas lipid proportion was low in the aphid treatment. Preference for aphids was lower following a monotypic aphid diet than when reared on Ephestia eggs or a mixed diet. The results confirm that R. padi is low-quality food for O. majusculus as it is for other generalist predators, even though O. majusculus may contribute significantly to population suppression of the aphid.     

The functional response and preference ofMacrolophus caliginosus [Heteroptera: Miridae] for two of its prey:Myzus persicae andTetranychus urticae

Functional response studies of females ofMacrolophus caliginosus Wagner for 2 prey speciesMyzus persicae Sulzer andTetranychus urticae Koch showedHolling's type II response (1959). Estimations of handling time (Th) and attack rate (a) obtained for the aphid (Th=.055 day; a=1.035) and for the mite (Th=.025 day; a=.947) enabled the development of a mathematical model which describes the predation rate on the 2 prey simultaneously. This mirid shows a sharp preference for aphids over mites.

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Résumé L'étude en laboratoire des réponses fonctionnelles des femelles adultes deMacrolophus caliginosus Wagner vis-à-vis des deux proiesMyzus persicae Sulzer etTetranychus urticae Koch montre dans les 2 cas une réponse de type II deHolling (1959). L'estimation du temps de manipulation (Th) et du taux d'attaque instantané (a) pour l'aphide (Th=.055 jour; a=1.035) et pour l'acarien (Th=.025 jour; a=.947) permet d'établir un modèle mathématique décrivant la prédation sur les 2 proies présentes simultanément et de préciser ainsi, au regard des résultats expérimentaux, l'existence d'une préférence du miride pour le puceronM. persicae.

     

Density-dependent predation of the antLasius niger (Hymenoptera: Formicidae) on two attended aphidsLachnus tropicalis andMyzocallis kuricola (Homoptera: Aphididae)

The antLasius niger was observed collecting honeydew and preying on the two aphid speciesLachnus tropicalis andMyzocallis kuricola on the chestnut treesCastanea crenata. Observation determined how the antL. niger controlled their predation on the aphids in response to the density and honeydew-productivity of the aphids.Lachnus tropicalis was a better honeydew source thanM. kuricola forL. niger in terms of the amount of honeydew collected per unit time by the ants. The number of foraging workers on a tree increased with the number ofL. tropicalis on the tree, but not with the number ofM. kuricola. The density ofL. tropicalis perL. niger worker on a tree had a positive effect on the predation activity ofL. niger on both aphids, whereas the density ofM. kuricola per ant did not have any significant effect. The predation pressure by the ant which increased withL. tropicalis density, however, directed toM. kuricola rather than toL. tropicalis. These facts suggest (1) thatL. niger control their predation activities on aphids with regards to the densities of the attended aphids per worker, and (2) that the ants prey on the aphid species producing less honeydew. The effects of the ant predation on aphids and the importance of these predation effect in antaphids interactions were discussed.     

Effects of Various Items,Host Plants,and Temperatures on the Development and Survival of Macrolophus pygmaeus Rambur (Hemiptera: Miridae)

Nymphal development and survival of Macrolophus pygmaeus Rambur (Hemiptera: Miridae) on various host plants, in the presence and absence of various insect prey, and on bee pollen and pollen from Ecbalium elaterium L. (Cucurbitaceae) in various combinations were studied. The effect of temperature on the development and mortality of M. pygmaeus nymphs was also studied. Experiments were conducted in temperature cabinets maintained at 65 ± 5% RH, 16L:8D h photoperiod, and constant temperatures, depending on the experiment. Results demonstrated that M. pygmaeus can successfully complete its development on tomato, eggplant, cucumber, pepper, and green beans in the absence of insect prey. In the presence of insect prey, M. pygmaeus had the shortest period of nymphal development on eggplant with Trialeurodes vaporariorum (Westwood) followed by Myzus persicae (Sulzer), Macrosiphum euphorbiae (Thomas), Aphis gossypii Glover, and Tetranychus urticae Koch. Mortality of M. pygmaeus nymphs was relatively higher in the absence than in the presence of prey on various host plants but was not considered a factor restricting predator establishment. M. pygmaeus completed its development, even in the absence of prey, under a range of temperatures from 15 to 30°C on tomato, with optimum development at 30°C. Bee pollen and pollen from E. elaterium, when offered separately, were sufficient to support successful predator nymphal development and survival. Bee pollen contributed considerably to the development and survival of the nymphs when it was included in diets containing other food sources, like eggplant leaves and M. persicae.     

The brine shrimp Artemia sp. as alternative prey for rearing the predatory bug Macrolophus caliginosus

The predatory bug Macrolophus caliginosus, which is widely used in greenhouse crops, is limited in its application by its high price. An important factor in the cost is the high price of Ephestia kuehniella eggs, the prey used in their mass rearing. In order to reduce their price, alternatives to moth eggs are currently being investigated. The brine shrimp Artemia sp. is produced in large quantities in saline lakes and is fed as live food source to the larvae of a variety of marine and freshwater organisms. In this study, we tested Artemia sp. as prey for rearing M. caliginosus from two strains. We evaluated developmental and reproduction parameters of the predator when fed nauplii, enriched nauplii with a fatty acid, dry cysts and hydrated cysts, and were compared with those obtained when the predator was fed with E. kuehniella eggs. Nauplii had a significant reduction in survivorship, a delay in development of nymphs and a low reproduction of adults. Nauplii enriched with docosahexaenoic acid (DHA, 22:6n − 3), a common practice for larviculture of some marine fish species, resulted toxic to M. caliginosus nymphs and survival was quite low. On the contrary, either dry or hydrated cysts from the two strains tested of the brine shrimp produced the same nymphal survivorship, nymphal development time and weight and fecundity of adults as those obtained with E. kuehniella eggs. Demographic parameters of the eighth generation of the predator reared with cysts of the two strains, either dry or hydrated, were as good as those of moth eggs. We concluded that Artemia sp. cysts were a good substitution prey for the mass rearing of M. caliginosus.     

Stable carbon and nitrogen isotope signatures to determine predator dispersal between alfalfa and maize

The dispersal of Orius majusculus and Coccinella septempunctata between maize and alfalfa during the vegetative and reproductive maize growth periods was investigated, using carbon and nitrogen stable isotope analysis and aphids as herbivore prey at two locations of the NE Iberian Peninsula. The dispersal pattern of O. majusculus and C. septempunctata differs between these crops and also between different moments of the maize growth period. In the vegetative period the pattern was similar for the two predators and alfalfa acted as a source of predators towards maize. During the reproductive period, the dispersal of O. majusculus between the two crops was continuous but biased from maize to alfalfa, which mainly becomes a sink crop. All of the C. septempunctata collected on alfalfa were local and those collected on maize came from alfalfa, but there was no dispersal from maize to alfalfa. The present study increases knowledge of the dispersion of predators between arable crops and can improve habitat and landscape management at the farm scale by enhancing their biological control functions.     

Cannibalism and interspecific predation in two predatory ladybirds in relation to prey abundance in the field

Life tables for two predatory ladybirds,Coccinella septempunctata andHarmonia axyridis, were constructed in two years in which prey abundance differed. The prey aphid,Aphis gossypii, was abundant on its primary host from late May to late June. Females ofH. axyridis andC. septempumctata laid their eggs during the increase and peak in aphid abundance. The oviposition period ofC. septempunctata started before and was shorter than that ofH. axyridis. In both species, intraguild predation and/or cannibalism of the egg and fourth instar stages, but rarely of other developmental stages, were observed. Fourth instar larvae ofH. axyridis had to complete their development when aphids were scarce more frequently than those ofC. septempunctata. The highest frequency of intra- and interspecific predation was of fourth instarH. axyridis larvae. In terms of intraguild predation, the larvae ofH. axyridis preyed on larvae ofC. septempunctata, but the reverse was not observed. Percentage survival from egg to adult inH. axyridis was higher than inC. septempunctata in both years, and least in both species in the year of low aphid abundance. These results suggest that prey abundance influenced the frequency of cannibalism and intraguild predation, which were important in structuring this guild of ladybirds.