Impact of Macrolophus caliginosus presence on damage production by Dicyphus tamaninii (Heteroptera: Miridae) on tomato fruits

In northeast Spain, the most common predators found in tomato fields and greenhouses are the mirids Macrolophus caliginosus Wagner and Dicyphus tamaninii Wagner. Natural colonization occurs during the growing season and both species prey on whiteflies. Because D. tamaninii can damage tomato fruits during periods of prey scarcity, a semifield experiment was carried out to evaluate whether the presence of M. caliginosus affects damage produced by D. tamaninii. In a tomato greenhouse, 60 plants were individually caged and distinct predator treatments were introduced: D. tamaninii, D. tamaninii + eggs of Ephestia kuehniella Zeller, D. tamaninii + M. caliginosus, M. caliginosus alone, and a control without any insect. Damage to tomato fruits was recorded (>25% of the fruit) in all the treatments with D. tamaninii, whereas no significant damage was detected with M. caliginosus alone. Finally, no intraguild predation was detected between both mirid species.     

Residual toxicity of some insecticides on the predatory bugs Dicyphus tamaninii and Macrolophus caliginosus

Chlorpyrifos, formetanate, methamidophos, imidacloprid and endosulfan were tested in the laboratory for their effects upon the mirid bugs Dicyphus tamaninii and Macrolophus caliginosus, which are polyphagous predators used for IPM programs in some vegetable crops. The mortality of third-fourth instar nymphs was checked 24 and 48 hours and 7 days after exposure to 1-, 3-, 8-, 21- and 30-day residues of the treatments on tomato leaflets. The reproductive capacity of surviving females also was evaluated for 15 days and compared with females that had not been exposed to insecticides. Chlorpyrifos, formetanate and methamidophos are considered persistent because they remained toxic to both mirid species for 30 days. Imidacloprid is moderately persistent, becoming harmless by 21 days after treatment for M. caliginosus and by 30 days after treatment for D. tamaninii. Endosulfan is moderately persistent for M. caliginosus, becoming harmless by 21 days after treatment, and is short lived for D. tamaninii, becoming harmless by 3 days after treatment. There were no effects on the reproductive capacity of females that were exposed as nymphs to the insecticides tested. Of all the insecticides, only endosulfan is marginally compatible with the use of D. tamaninii.     

Feeding preference of Macrolophus caliginosus (Heteroptera: Miridae) on Bemisia tabaci and Trialeurodes vaporariorum (Homoptera: Aleyrodidae)

A study of predation choices of Macrolophus caliginosus Wagner (Heteroptera: Miridae) late instars and adults, when offered various developmental stages (eggs and nymphs) of the recently established whitefly Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae), was made based on two preference indices. In addition, prey choices of late instars when presented with three ratios of Trialeurodes vaporariorum (Westwood) (Homoptera: Aleyrodidae) and B. tabaci at a similar developmental stage (eggs, young or late instars) were assessed. M. caliginosus preferred older nymphs of B. tabaci than any other stage. It also chose T. vaporariorum over B. tabaci, unless the latter consisted of > 75% of the available prey. These results suggested that M. caliginosus might interfere with parasitoids such as Encarsia, Eretmocerus, or Amitus spp. because all three species emerge from the host pupal case. Furthermore, in mixed infestations, M. caliginosus preference for T. vaporariorum might either negatively affect the control of B. tabaci, or, contrarily, enhance the predator population, before a B. tabaci outbreak occurs in the greenhouse.     

Interactions Between Two Polyphagous Predators, Orius majusculus (Hemiptera: Anthocoridae) and Macrolophus caliginosus (Heteroptera: Miridae)

The mutual predation between two polyphagous predators, Orius majusculus (Reuter) (Hemiptera, Anthocoridae) and Macrolophus caliginosus Wagner (Heteroptera: Miridae), was examined in laboratory experiments with and without presence of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). Adults of O. majusculus preyed upon M. caliginosus in the absence and in some circumstances also in the presence of F. occidentalis, whereas neither nymphs nor adults of M. caliginosus preyed upon O. majusculus. Orius majusculus nymphs did not prey upon M. caliginosus. The predation of O. majusculus on F. occidentalis was unaffected by the presence of M. caliginosus suggesting that the presence of this mirid will not hamper biological control of F. occidentalis.     

Effect of diet and mating status on ovarian development and oviposition in the polyphagous predator Macrolophus caliginosus (Heteroptera: Miridae)

The mirid bug Macrolophus caliginosus is commercially reared on eggs of Ephestia kuehniella, constituting an effective but expensive factitious food. Artificial diets can decrease the rearing costs of this natural enemy, but developing and evaluating an artificial diet is a very time-consuming activity. In the current study, development and reproduction of M. caliginosus on two artificial diets based on egg yolk were investigated. The artificial diets resulted in longer development and lower adult weights, but survival was comparable with that of control insects fed E. kuehniella eggs. Reproductive potential of the predator reared on factitious and artificial foods was assessed using a dissection method. The influence of nymphal food on fecundity was less important than that of adult food. Adults fed E. kuehniella eggs had a preoviposition period of about 4 days, whereas adults offered only plant material started laying eggs about 7 days after emergence. Ovarian scores at day 7 were higher for females fed E. kuehniella eggs than for those given access only to a tobacco leaf. Ovarian scores were not significantly affected by mating status. In a final test, a parallel comparison of two methods for assessing reproductive response to diet was made. Here, adult couples were offered one of four diets: E. kuehniella eggs, one of two artificial diets or no food. Half of the females were dissected and the other half was held for determining lifetime oviposition. Females fed E. kuehniella eggs had superior ovarian scores and laid more eggs than those fed either artificial diet or those given no extra food. A good correlation (r = 0.97) was obtained between ovarian scores and oviposition data, indicating that dissecting females after 1 week provides a reliable estimate of fecundity as affected by diet quality. Rapid reproductive assessments as used in the current study will help to increase the rate of development of artificial diets and may contribute to more cost effective production methods for augmentative biological control agents.     

Side-effects of three neem (Azadirachta indica A. Juss) products on the predator Macrolophus caliginosus Wagner (Het., Miridae)

The side-effects of three neem formulations (Neem-Amin EC, Stardoor and B.P. 20/S) were tested on the mirid predator Macrolophus caliginosus Wagner in the laboratory. Direct toxicity tests on 1st instar nymphs exposed to fresh dry residues on glass plates at different doses demonstrated that all the products are harmful to the insects with LD₅₀ values much lower than the maximum recommended rate (1.217, 0.264, 1.083 mg a.i./l instead of 15, 31.5 and 80 mg a.i./l for Neem-Amin EC, Stardoor and B.P. 20/S, respectively). Moreover a reduction of fecundity of the surviving females was assessed with Neem-Amin EC and B.P. 20/S. Persistence tests were carried out on sharp pepper plants treated at the maximum recommended rate. High mortality was recorded when the insects were introduced onto the plants just after the treatment, but no significant differences compared with the controls were observed 5 days after the treatment and any consequence on the fecundity of surviving females was detected. Our experiments showed how azadirachtin can be noxious to M. caliginosus , but the short persistence makes this active ingredient a promising solution in integrated pest management programmes, when a lapse of time is guaranteed between the treatment and the introduction of the predator.     

Photoperiodic Control of Pre-Adult Development and Adult Diapause Induction in Zoophytophagous Bug Dicyphus errans (Wolff) (Heteroptera,Miridae)

Zoophytophagous plant bugs (Heteroptera, Miridae) increasingly attract interest as agents of biological plant protection. In the laboratory experiment, the effects of the day length and temperature on the duration of the pre-adult period and on induction of facultative winter adult diapause were studied in Dicyphus errans (Wolff, 1804) collected in Italy. The experiment demonstrated that at 20°C the duration of the pre-adult period of D. errans significantly depended on the day length. On average, females developed 1.3 days longer than males and, at the same time, the day length equally influenced the duration of the pre-adult period in both sexes. The pre-adult period was the shortest under short-day conditions (10 to 12 h of light per day), reached its maximum at day length of 14 h, but then decreased at 15 h, and at day length of 16 h it was as short as under short-day conditions. Also, a pronounced long-day type photoperiodic response of adult diapause induction was recorded in females of D. errans at 20°C: under short-day conditions (10 to 14 h of light per day) almost all females entered diapause, whereas under long-day conditions (15 and 16 h of light per day) about 90% of females were mature. The threshold of this photoperiodic response was close to 14 h 30 min. The mean (± S.D.) egg load of mature females was 6.3 ± 4.0 eggs per female and did not depend on the day length at which the female was reared before and after the final molt. When photoperiodic response of adult diapause induction was observed at two constant temperatures (20 and 25°C), the proportion of mature females depended significantly on the day length but not on the temperature: the shapes of the photoperiodic response curves of diapause induction were almost the same within the near-threshold zone at 20 and 25°C, i.e., the photoperiodic response was thermostable. The set of two photoperiodic responses manifested at different stages of the species’ life cycle has an obvious adaptive significance. In Central Europe, D. errans has 2 or 3 generations per year and hibernates at the adult stage. Due to the thermostable photoperiodic response, females enter diapause always at the same time at the end of summer, regardless of the weather conditions of a particular year. When oviposition and pre-adult development are extended over a prolonged period in summer, nymphs from the later eggs might not be able to molt to adults in due time and then fully prepare for stable winter diapause. Under such circumstances, the photoperiodic response controlling the rates of pre-adult development acquires apparent adaptive meaning: with an autumnal shortening of the day length to 10–12 h, even under conditions of seasonal decrease in temperature, the rates of nymphal development increase and, thus, the chances of nymphs from the later eggs to molt to adults and properly prepare for overwintering also increase. The new data should be taken into account when analyzing the seasonal cycle of D. errans and developing the programs of mass rearing of this zoophytophagous mirid as an agent of biological plant protection.

     

Prey‐mediated changes in the selectivity of the predator Macrolophus pygmaeus (Heteroptera: Miridae)

When foraging in communities with mixed prey, generalist predators may be confronted with prey species that differ in quality, size and mobility and interact with one another. To examine prey selection, predation by Macrolophus pygmaeus (Heteroptera: Miridae) was recorded by providing a diet of either one or two prey species of Myzus persicae (third‐instar nymphs), Aphis gossypii (fourth‐instar nymphs), Trialeurodes vaporariorum (third‐instar nymphs) and Ephestia kuehniella (eggs). In the experiments, prey mobility, prey quality and prey biomass were considered. The biomass consumed by the predator was dependent on the combination of prey species and the quantity of biomass offered. In choice experiments with diets mixed of two prey species at equal densities, the predation to A. gossypii was significantly reduced in the presence of E. kuehniella but the rate of consumption of M. persicae, T. vaporariorum and E.kuehniella was not significantly affected by the coexistence of any other species in the mixed prey diet. When equal amounts of biomass from two prey species were provided in combination, the total consumed biomass was significantly reduced in the mixed prey diets composed of E. kuehniella eggs and aphid nymphs. Thus, under the mixed‐prey situation, prey selection by predators may be affected by interactions among prey species differing in traits such as quality, mobility and size.     

Evaluation of Dicyphus hersperus (Heteroptera: Miridae) for biological control of Frankliniella occidentalis (Thysanoptera: Thripidae) on greenhouse tomato

The effectiveness of inoculative releases of the mirid predator Dicyphus hesperus Knight for control of Frankliniella occidentalis (Pergande) on greenhouse tomatoes was evaluated in terms of suppression of the population densities of F. occidentalis and associated fruit damage in the presence of the predator over two seasonal trials. An inoculative release of one D. hesperus per plant (approximately 0.1:10 predator:prey ratio) at a high F. occidentalis population density (140 thrips per plant) suppressed the thrips population density to a significantly lower level, compared with the nonrelease greenhouse, but not below a thrips level that caused economic fruit damage. As the predator:prey ratio increased to approximately 0.5:10 D. hesperus:F. occidentalis, the mean percentage of the thrips-damaged fruit in the D. hesperus release greenhouse decreased to 1.6%. However, the amount of fruit feeding by D. hesperus was highly correlated to the availability of prey (or predator:prey ratio) under greenhouse conditions. D. hesperus-induced fruit damage occurred when the predator:prey ratio was >1:10 D. hesperus:F. occidentalis. Considering the potential risk of fruit damage by D. hesperus and the need for effective control of F. occidentalis, a 0.5-1:10 D. hesperus:F. occidentalis ratio is recommended when the thrips population density is in the range of 60-150 thrips per plant.     

Microbial community of predatory bugs of the genus Macrolophus(Hemiptera: Miridae)

Background

The predatory mirids of the genus Macrolophus are key natural enemies of various economically important agricultural pests. Both M. caliginosus and M. pygmaeus are commercially available for the augmentative biological control of arthropod pests in European greenhouses. The latter species is known to be infected with Wolbachia -inducing cytoplasmic incompatibility in its host- but the presence of other endosymbionts has not been demonstrated. In the present study, the microbial diversity was examined in various populations of M. caliginosus and M. pygmaeus by 16S rRNA sequencing and denaturing gradient gel electrophoresis.

Results

Besides Wolbachia, a co-infection of 2 Rickettsia species was detected in all M. pygmaeus populations. Based on a concatenated alignment of the 16S rRNA gene, the gltA gene and the coxA gene, the first is phylogenetically related to Rickettsia bellii, whereas the other is closely related to Rickettsia limoniae. All M. caliginosus populations were infected with the same Wolbachia and limoniae-like Rickettsia strain as M. pygmaeus, but did not harbour the bellii-like Rickettsia strain. Interestingly, individuals with a single infection were not found. A PCR assay on the ovaries of M. pygmaeus and M. caliginosus indicated that all endosymbionts are vertically transmitted. The presence of Wolbachia and Rickettsia in oocytes was confirmed by a fluorescence in situ hybridisation. A bio-assay comparing an infected and an uninfected M. pygmaeus population suggested that the endosymbionts had minor effects on nymphal development of their insect host and did not influence its fecundity.

Conclusion

Two species of the palaearctic mirid genus Macrolophus are infected with multiple endosymbionts, including Wolbachia and Rickettsia. Independent of the origin, all tested populations of both M. pygmaeus and M. caliginosus were infected with three and two endosymbionts, respectively. There was no indication that infection with endosymbiotic bacteria had a fitness cost in terms of development and fecundity of the predators.

     

A method for laboratory studies on the polyphagous predator Macrolophus pygmaeus (Hemiptera: Miridae)

A method for studying the life history parameters of Macrolophus pygmaeus Rambur was developed and described. Fecundity of the predator was studied by placing one female and one male in a plastic cylinder in which a stem piece was used as an ovipositional substrate. Smaller cylinders were used to study the percentage of egg hatch of M. pygmaeus. Results demonstrated that this method is suitable for studying the fecundity and egg eclosion of M. pygmaeus. Allowing for easy modification, the method offers suitable conditions for maintenance of both insect and plant material and can be inexpensively modified for different experiments and the parts are easily constructed. The proposed method could also be employed for similar studies on other predatory hemipterans such as mirids and anthocorids and very likely on other phytophagous insect species that lay their eggs in or on plant stems.     

Intraguild predation of water scorpion Laccotrephes japonensis (Nepidae: Heteroptera)

Previous work on community structure of the invertebrate fauna of Japanese wetlands indicates the presence of intraguild predation between the heteropterans Laccotrephes japonensis (Nepidae) and Kirkaldyia deyrolli (Belostomatidae). We designed a series of experiments to understand the biotic interactions of several species of sympatric heteroptera and their shared prey. Adult Laccotrephes japonensis (Nepidae), first-instar nymph of Kirkaldyia (=Lethocerus) deyrolli (Belostomatidae), Hyla japonica tadpole, and fourth-instar nymph of Appasus japonicus (Belostomatidae) have been shown to be intraguild predator, intraguild prey, common prey, and prey of L. japonensis, respectively. To further understand the factors affecting prey preference by L. japonensis, we also examined the comparison of swimming speed in the three prey animals (K. deyrolli first-instar nymph, A. japonicus fourth-instar nymph, and H. japonica tadpole), and effects of prey animals on weight gain of L. japonensis adult. Despite there being no significant difference in weight gain or swimming speed of the three prey species, L. japonensis exhibited a strong preference for the 1st-instar nymph of K. deyrolli. We suggested that this may be evidence for one of elimination of a potential competitor, K. deyrolli, by L. japonensis through intraguild predation.     

Salivary amino acids in Lygus species (Heteroptera:Miridae)

Free and protein-bound amino acids were investigated in the phytophagous bug Lygus rugulipennis and its salivary gland. Over 38 substances were separated. The total content of amino compounds in the insects was about 1400 μmol/g fr. wt (16% by weight), of which 97% was amino acid residues in proteins.The salivary glands, which comprise about 1.5% of the live weight of the insects, contain 3.5% of the total free amino acids and 1% of the whote insect. Free and protein-bound amino acids comprise, respectively, about 1.4 and 11.6% of the fresh weight of the gland. The total concentration of free amino acids in the saliva was estimated to range from 0.5 to 2.2% by weight (ca. 0.1 M).The composition of free amino acids in the salivary gland of Lugus varies markedly. In four studied species (L. rugulipennis, L. gemellatus, L. pratensis, L. punctatus), the most abundant compounds were proline, arginine, lysine, leucine, glutamic acid, methionine sulphoxide and glycerophosphoethanolamine. In whole specimens of L. rugulipennis the predominant free amino acids were proline, alanine, taurine, glutamic acid, glutamine and methionine sulphoxide. The most abundant amino acids in proteins were glutamic and aspartic acid, glycine, alanine and leucine. The results indicate that the amino acid composition in the salivary glands of Lygus species does not differ markedly from that of the whole insect. The functions of salivary amino acids are discussed.     

Diapause induction under greenhouse conditions in two populations of Dicyphus hesperus (Hemiptera: Miridae)

The effects of daylength on induction of reproductive diapause were investigated in two populations of Dicyphus hesperus to determine which was more suitable as a biological control in greenhouses without supplemental light. A population from British Columbia Canada (49°36' N Lat.) had a critical daylength of about 15.5 h, whereas that of a population from California, USA (35°43' N Lat.) was between 14.0 and 13.5 h. Under natural daylengths in greenhouses at 49°N Lat., females of both populations exhibited reproductive diapause at a daylength that was consistent with their respective critical daylengths. In spring, a lower proportion of both populations diapaused when exposed to diapause-inducing conditions than in autumn. Reproductive diapause of the females of the BC population was 100% in autumn, but half of those females laid eggs when held in the greenhouse for 6 weeks. A maximum of 63% of females of the California population diapaused in autumn, and most began to lay eggs after 2 weeks. The differences in response to daylength presumably reflect differences between the two localities in the reliability of the critical daylength as a predictor of conditions unsuitable for growth and reproduction. Under greenhouse conditions the California population is essentially non-diapausing, and would be the more suitable of the two populations for use as a biological control agent.     

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.

     

Morphology of the Phytophagous bug Platyscytus decempunctatus (Carvalho) (Heteroptera: Miridae)

Platyscytus decempunctatus Carvalho is a small mirid living throughout its life cicle plant Solanum cernuum Vell. (Solanaceae). The internal morphology of P. decempunctatus was studied and found that the female has a telotrophic ovary with three ovarioles in the right ovary and five in the left one. In the male reproductive trait there is a well developed tubular accessory gland. The phytophagous feeding habitat of P. decempunctatus was confirmed by the observations of chlorophyll pigments in the gut of all dissected specimens. The tubular salivary glands and the Malpighian tubules were also discussed.     

Percussion signals of Lygus rugulipennis Poppius (Heteroptera: Miridae)

The European tarnished plant bug (Lygus rugulipennis Poppius) is among the most serious pests in the family Miridae, and therefore there is increasing interest in understanding the behaviour of this species. In the present study, laboratory recordings were taken using a laser vibrometer on adult males and females to ascertain whether acoustic signals are involved in intraspecific communication. Recordings were both carried out on plant and loudspeaker membrane substrates. Males and females emitted vibratory signals and the present results indicate that these signals are important during courtship. The basic signal characteristics measured were the dominant frequency, pulse duration, repetition time and number of pulses per group within the signal. Male and female signals did not differ in respect to any of these characteristics. Plant recorded signals were longer because of different mechanical properties of substrates. Additionally, the high frequency components were attenuated due to the low-pass filtering properties of plants. As this is the first study on vibratory communication of the European tarnished plant bug, we believe these findings may contribute considerably to the better understanding of the mating behavior of this important pest species.     

后丽盲蝽属作为属级分类单元的DNA分子证据

用蛋白酶K消化法提取并正反链双向测得半翅目盲蝽科盲蝽族(Mirini)中后丽盲蝽属(Apolygus)和草盲蝽属(Lygus)9个种的线粒体DNA细胞色素b基因片段的序列,应用Mega计算该两个属7个种11个Cyt b 432 bp片段序列的碱基组成、核苷酸的种间变异率、所编码的144个氨基酸的变异率。其核苷酸变异率：后丽盲蝽属内小于0．02,草盲蝽属内小于0．08(个别种例外);两个属种类之间平均变异率都大于0．10,平均为0．15。氨基酸变异率：后丽盲蝽属内种间无变异,而草盲蝽属内只有L．gemellatus与其他种间有13个氨基酸变异,仅占9．03％;两属各种类间却存在8～11个氨基酸的变异。表明在分子水平上两属之间较之于属内种间具有明显的差异,支持将后丽盲蝽从亚属提升为属级分类单元的分类观点。     

盲蝽科一中国新记录属及新记录种

记述盲蝽科Miridae1中国新记录属：薇盲蝽属Monalocoris Dahlbohm,1851及1新记录种,薇盲蝽Monalocoris filicis (Linneaus,1758)。     

Toxicity of some insecticides and acaricides to the predatory bugDicyphus tamaninii (Het.: Miridae)

Several pesticides were tested in the laboratory for their side-effects upon the mirid bugDicyphus tamaninii, a polyphagous predator used for IPM programmes in some vegetable crops. Residual toxicity to 3rd -4th instar nymphs on tomato leaflets was checked 24, 48 hours and seven days after treatment. The acaricides bromopropylate, dicofol+tetradifon and fenpyroximate were harmless to the nymphs. The insect growth regulators azadirachtin, buprofezin, lufenuron and pyriproxyfen were also harmless to nymphs and teflubenzuron was slightly harmful seven days after treatment. Among the conventional insecticides tested, only pirimicarb and tau-fluvalinate were harmless toD. tamaninii nymphs