Susceptibility of the woolly apple aphid parasitoid,Aphelinus mali (Hym.: Aphelinidae), to common pesticides used in apple orchards in Israel

The effects of one acaricide (cyhexatin), two fungicides (penconazole and sulfur), and six insecticides (azinphos-methyl, chlorpyrifos, imidacloprid, pirimicarb, triazamate and vamidothion) on the adult stage of the parasitoidAphelinus mali (Haldeman), a parasite of the woolly apple aphidEriosoma lanigerum (Hausmann), were investigated under laboratory conditions. Chlorpyrifos (an organophosphorus insecticide-OP) was found to be highly toxic to the adult wasps. Vamidothion (OP) was more toxic to the parasitoid than azinphos-methyl (OP). On the other hand, both chlorpyrifos and azinphos-methyl were found to be harmless to the immature stages of the parasitoid in a test conducted under semi-field conditions. Of the other insecticides, imidacloprid was more toxic to the adult parasitoid than pirimicarb and triazamate. Neither cyhexatin nor penconazole had a considerable toxic effect upon the parasitoid. In contrast, sulfur was found to be moderately toxic to the parasitoid under laboratory conditions, as well as in a field survey in which we followed populations ofE. lanigerum andA. mali parasitization in sulfur-treated plots, and in a plot treated withAmpelomyces quisqualis Ces., a fungus antagonist to powdery mildew. The implications of these results to IPM programs of apple orchards in Israel are discussed     

Isolation and characterization of nine microsatellite loci from Aphelinus mali (Hymenoptera: Aphelinidae), a parasitoid of Eriosoma lanigerum (Hemiptera: Aphididae)

Abstract Nine novel microsatellite markers are presented for Aphelinus mali, a parasitoid of the woolly apple aphid Eriosoma lanigerum. Loci were characterized for 28 individuals from a single orchard in central Chile. Seven loci were polymorphic within A. mali (3–6 alleles per locus; observed heterozygosity ranging from 0.04 to 0.57) and are therefore useful for population genetic studies within this species.     

Effect of trap color and orientation on the capture of Aphelinus mali (Hymenoptera: Aphelinidae), a parasitoid of woolly apple aphid (Hemiptera: Aphididae)

The factors affecting trap capture of adult Aphelinus mali (Haldeman) (Hymenoptera: Aphelinidae) were studied in 2010-2011 in eastern Washington apple (Malus spp.) orchards infested with its host woolly apple aphid, Eriosoma lanigerum (Hausmann) (Hemiptera: Aphididae). The initial study of white sticky cards indicated that traps stapled to the trunk in a vertical orientation had the highest capture. A factorial experiment of three colors (clear, white, and yellow) by three orientations (trunk, scaffold, and hanging) indicated that yellow traps and traps on trunks caught higher numbers ofA. mali. For this reason, the recommended trap for this natural enemy is a yellow trap stapled to the trunk. Having a readily available and effective sampling method for this species may be helpful in implementing biological control programs and assessing the impact of different spray regimes.     

鲁西南地区苹果绵蚜(Eriosoma lanigerum)及其天敌种群动态与群落结构特征

通过田间蚜块计数、黄色粘虫板诱集、室内镜检等方法统计苹果绵蚜Eriosoma lanigerum (Hausmann)及其寄生性天敌日光蜂Aphelinus mali Haldeman种群数量,分析比较了它们的消长动态.利用群落结构特征指数研究比较了不同时期苹果绵蚜及其天敌群落多样性.连续2a调查发现,苹果绵蚜种群在鲁西南地区全年发生两个高峰,其中5月中、下旬～7月上旬为第一高峰期,8月下旬～10月中旬为第二高峰期.有翅蚜发生在4月上旬～6月上旬和9月上旬～10月上旬.不同时期,苹果绵蚜在苹果树体不同部位的种群数量存在差异,上半年,苹果绵蚜在根、树干及主枝部位分布密集,发生危害较重;7月中、下旬之后,苹果绵蚜在根及树干部位基本不再发生或发生较轻,而在枝干部位,包括主枝、侧枝和新梢,发生危害较重.7月份之前,日光蜂滞后于苹果绵蚜的发生高峰,其控制作用不很明显,7月份以后日光蜂跟随现象才比较明显,与苹果绵蚜的第二个发生高峰前期基本吻合,可以很好地控制苹果绵蚜的危害.鲁西南地区苹果绵蚜及其天敌群落多样性低,群落稳定性差,发现天敌23种,捕食性天敌亚群落中七星瓢虫Coccinella septempunctata Linnaeus、二星瓢虫Adalia bipunctata (Linnaeus)和叶色草蛉Chrysopa phyllochroma Waesmael等为优势种,特别是4、5月份,七星瓢虫和叶色草蛉可以很好地弥补因日光蜂跟随滞后而对苹果绵蚜控制作用的影响.这为保护利用自然天敌、可持续控制苹果绵蚜危害奠定了理论基础.     

Earwig (Forficula auricularia) predation on the woolly apple aphid, Eriosoma lanigerum

Woolly apply aphid predation by the common earwig, Forficula auricularia L., and other predators was compared in high, intermediate and low earwig density plots of mature apple trees at an experimental orchard in the Netherlands. Aphid colonies were discovered and exterminated primarily by earwigs much more rapidly in the high and intermediate earwig density plots than in the low density plots. Where earwigs were excluded from trees by Tanglefoot bands around the trunks, woolly apple aphids infested 30–35% of new growth shoots whereas less than 10% of the shoots were infested where earwigs were relatively abundant.Several factors including the availability of alternate prey (e.g. Aphis pomi De Geer), earwig developmental phenology and weather probably influenced the outcome of the predation experiments. Nevertheless earwigs play an important role in suppressing woolly apple aphid populations and are potentially important, naturally occurring biological control agents for this pest.

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Résumé L'action prédatrice exercée sur le puceron lanigère par le perceoreille commun, Forficula auricularia, et par d'autres prédateurs, a été comparée dans des parcelles d'un verger expérimental de pommiers adultes aux Pays-Bas. Ces parcelles étaient caractérisées par des densités fortes, intermédiaires, et basses en perce-oreilles. Les colonies de pucerons ont été découvertes et exterminées principalement par les perce-oreilles beaucoup plus rapidement dans les parcelles à forte et moyenne densité de perce-oreilles que dans celles à faible densité. Les pucerons lanigères ont colonisé 30 à 35% des nouvelles pousses lorsque les perce-oreilles étaient exclus par une barrière mécanique (Tanglefoot), alors que moins de 10% des pousses ont été infestées lorsque les perce-oreilles étaient relativement abondants.Plusieurs facterus ont probablement influencé le résultat des expériences de prédation, notamment la présence de proies alternatives (par exemple Aphis pomi), la phénologie du développement des perce-oreilles et le climat. Néanmoins, les perce-oreilles ont joué un rôle important en limitant les populations du puceron lanigère, et constituent potentiellement d'importants agents de contrôle naturel de ce ravageur.

     

Isolation and characterization of microsatellite loci from the woolly apple aphid Eriosoma lanigerum (Hemiptera: Aphididae: Eriosomatinae)

Eight novel microsatellite primer pairs are presented for Eriosoma lanigerum, representing the first microsatellite markers available for this genus. Loci were characterized for 27 individuals from one single orchard in Central Chile. All loci were polymorphic within E. lanigerum (three to 11 alleles per locus; observed heterozygosity ranging from 0.41 to 0.93), and are therefore useful for population genetic studies within the species.     

Genetic diversity of woolly apple aphid Eriosoma lanigerum (Hemiptera: Aphididae) populations in the Western Cape, South Africa

The woolly apple aphid Eriosoma lanigerum (Hausmann) is one of the most damaging apple pests in South Africa. Information on its genetic diversity is lacking and this study, in which the genetic structure of parthenogenetic E. lanigerum populations was characterized in the Western Cape Province of South Africa, represents the first local study of its kind. A total of 192 individuals from four different regions were collected and analysed using amplified fragment length polymorphism (AFLP). Using five selective AFLP primer pairs, 250 fragments were scored for analysis. Results indicated that a low level of genetic variation was apparent in E. lanigerum populations in the Western Cape (H = 0.0192). Furthermore, populations collected from geographically distant regions were very closely related, which can partly be explained by the fact that agricultural practices were responsible for dissemination of populations from a common ancestor to geographically distant areas. The low level of variation found indicated that the possibility of controlling E. lanigerum in the Western Cape using host plant resistance is favourable. This is the first report of AFLP being used to characterize the genetic structure of an aphid species. Results indicate that this marker may be useful for analysis of other aphid species.     

A chromosome‐level genome assembly of the woolly apple aphid,Eriosoma lanigerum Hausmann (Hemiptera: Aphididae)

Woolly apple aphid (WAA, Eriosoma lanigerum Hausmann) (Hemiptera: Aphididae) is a major pest of apple trees (Malus domestica, order Rosales) and is critical to the economics of the apple industry in most parts of the world. Here, we generated a chromosome‐level genome assembly of WAA—representing the first genome sequence from the aphid subfamily Eriosomatinae—using a combination of 10X Genomics linked‐reads and in vivo Hi‐C data. The final genome assembly is 327 Mb, with 91% of the assembled sequences anchored into six chromosomes. The contig and scaffold N50 values are 158 kb and 71 Mb, respectively, and we predicted a total of 28,186 protein‐coding genes. The assembly is highly complete, including 97% of conserved arthropod single‐copy orthologues based on Benchmarking Universal Single‐Copy Orthologs (busco ) analysis. Phylogenomic analysis of WAA and nine previously published aphid genomes, spanning four aphid tribes and three subfamilies, reveals that the tribe Eriosomatini (represented by WAA) is recovered as a sister group to Aphidini + Macrosiphini (subfamily Aphidinae). We identified syntenic blocks of genes between our WAA assembly and the genomes of other aphid species and find that two WAA chromosomes (El5 and El6) map to the conserved Macrosiphini and Aphidini X chromosome. Our high‐quality WAA genome assembly and annotation provides a valuable resource for research in a broad range of areas such as comparative and population genomics, insect–plant interactions and pest resistance management.     

Age-specific survival and fecundity and their effects on the intrinsic rate of increase of Aphelinus gossypii (Hym., Aphelinidae), a parasitoid of Aphis gossypii (Hom., Aphididae)

Abstract: The age-specific survival and fecundity of female adults of the aphidophagous parasitoid, Aphelinus gossypii Timberlake (Hym., Aphelinidae), were determined at a host density of 50 Aphis gossypii Glover (Hom., Aphididae) per leaf of Ageratum houstonianum Mill each day at 25°C. The age-specific mummy production, emergence rate and sex ratio of progeny were calculated. The implication of these results in terms of potential population growth of A. gossypii and related species is discussed. The age-specific survival curve ( l _x ) of females exhibited a Type I pattern, which resulted in little difference between Σ m _x and Σ l _x   m _x . The l _x curve of males exhibited a Type II pattern, and their survival time was much shorter than that of females. Each mated female produced on average 598.9 ± 64.0 aphid mummies, and preyed on 87.9±6.2 aphids. Most of the biological performance parameters were not different significantly between mated and virgin females. The highly female-biased sex ratio of offspring produced by mated females soon after their emergence resulted in a high fecundity rate ( m _x ) during the early reproductive period. Therefore, although the sex ratio of progeny was male-biased during the entire reproductive period, the intrinsic rate of increase estimated using age-specific sex ratios was larger than that estimated using a constant sex ratio of 0.5. These results indicate that the high survival and the adaptation of producing mostly female offspring during the early reproductive period contribute much to the population increase potential of this parasitoid.     

Effect of temperature and host stage on performance of Aphelinus varipes Förster (Hym., Aphelinidae) parasitizing the cotton aphid, Aphis gossypii Glover (Hom., Aphididae)

Development time, mummification, pupal mortality, host feeding and sex ratio of a Norwegian strain of Aphelinus varipes Förster parasitizing the cotton aphid, Aphis gossypii Glover were studied at 20, 25 and 30°C in controlled climate cabinets. Petri dishes with cucumber ( Cucumis sativus L) leaves on agar were used as experimental units. Cotton aphids in different larval instars and as adults, reared at the three different temperatures, were presented to A. varipes in a `no-choice' situation for 6 h. These presentations were done at 25°C in each experiment to avoid an influence of temperature on parasitization rate. More first instar aphids were parasitized than third and fourth instars among the aphids reared at 20°C. Pupal mortality of the parasitoid was not influenced by temperature. It was lower in aphids parasitized as adults than in aphids parasitized in second instar. The sex ratio of A. varipes was female-biased, and varied between 92% females developed from aphids reared at 25°C and 70% from aphids reared at 20°C. The sex ratio was not significantly influenced by host stage. The development time of A. varipes ranged from 17.5 days at 20°C to 9.8 days at 30°C.     

苹果绵蚜蚜小蜂——对苹果绵蚜有控制潜能的寄生蜂

苹果绵蚜蚜小蜂是苹果绵蚜的重要寄生蜂。本文综述了苹果绵蚜蚜小蜂的研究概况,包括该寄生蜂的引种与分布、寄主范围、生物学特性、控制效果与影响因素、重寄生蜂及合理利用等,指出应加快苹果绵蚜蚜小蜂的规模化生产,充分发挥其对苹果绵蚜的控制作用。     

Effects of bio-pesticides on Eretmocerus warrae (Hym., Aphelinidae), a parasitoid of Bemisia tabaci (Hom., Aleyrodidae)

The sweet potato whitefly Bemisia tabaci (WF) can be controlled by two commercial neem products, NeemAzal-T/S^® (1% azadirachtin) for foliar application, and NeemAzal-U (17% azadirachtin) for soil application, alongwith two biorational products of microbial origin, Abamectin (avermectin) and Success^® (spinosad). Side effects of these products were tested in a laboratory bioassay against a native aphelinid, Eretmocerus warrae (EW). Eggs and early larval instars of the parasitoid, commonly found outside the host body, were highly susceptible to foliar spray of neem with only 8%, 18% and 55% emergences of adults from treated eggs. larval and pupal stages respectively at recommended dose-rates of 5 ml/l and 1%, 8% and 40% at twice recommend dose-rate (10 ml/l). Soil application with NeemAzal-U marginally affected EW. At highest tested dose-rate of 3.0 g/l, 46%, 64% and 81% emergence was recorded after treatement of plants harbouring WF parasitized by egg, larval and pupal stages of EW respectively. In contrast to neem application, Success^® and Abamectin caused high mortality in development stages of the parasitoids. In particular, abamectin was highly toxic to the parasitoids with less than 1% emergence from either of the three development stages if treated with 1–2 ml/l.     

Morphological observations on the preimaginal stages ofAphelinus varipes (Hym., Aphelinidae) and the effects of this parasitoid on the aphidRhopalosiphum padi (Hom., Aphididae)

Three instar larvae could be observed forAphelinus varipes. In the second and third instars, the colon which forms the largest part of the hindgut was composed of secretory cells. There was a reduction in the size and number of embryos produced by parasitized aphids. Fat cells of parasitized aphids also degenerated sooner than those of unparasitized aphids. The number of mycetocytes remained higher in parasitizedRhopalosiphum padi than in non-parasitized aphids. During the last instar ofA. varipes the host aphid developed into a mummy in which black pigments were incorporated into the exocuticle and the integument of the aphid became sclerotized.     

Control of woolly aphid, Eriosoma lanigerum (Hausmann) (Hemiptera: Pemphigidae) on mature apple trees using insecticide soil-root drenches

Abstract Woolly aphid, Eriosoma lanigerum , is an important pest of apples that infests both the aerial and root parts of the tree. Root colonies are protected from the pesticide sprays applied during the growing season and the climatic effects of winter. Consequently, root colonies are a major source of aerial re-infestation in the following spring. Imidacloprid, the first of a new group of insecticides from the chloronicotinyl family, is known to provide excellent control of woolly aphid on trees up to 7-years-old when applied as a root soil drench. This study compared the effects of a single application of chlorpyrifos, imidacloprid, pirimicarb or vamidothion, applied as a root drench over four growing seasons. A soil wetting agent was added to each chemical to improve soil saturation and penetration. Imidacloprid provided excellent control of woolly aphid on the trees that were 17-years-old at the start of the study and continued to do so for four seasons. Pirimicarb appeared to offer some suppression of woolly aphid during the first season but not in subsequent seasons, while chlorpyrifos and vamidothion failed to control woolly aphid in any season. The potential role for imidacloprid in IPM programs is discussed.     

Apple sawfly Hoplocampa testudinea (Hym., Tenthredinidae) and its parasitoid Lathrolestes ensator in Dutch apple orchards (Hym., Ichneumonidae, Ctenopelmatinae)

Abstract: Changes in population densities of the apple sawfly Hoplocampa testudinea (Klug) and its parasitoid Lathrolestes ensator (Brauns) were monitored in 15 apple orchards for a period of up to 4 years. The parasitoid species was found in all orchards except one, and was more numerous in plantings on sandier soils. Post‐bloom insecticide applications against other pests, and carbaryl for fruit thinning, often decimated both host and parasitoid in integrated pest management orchards. In organic orchards, where synthetic pesticides are banned, and Quassia is the only remedy against sawfly, the pest is more problematic. The low levels of parasitism in all organic orchards, except one, were possibly due to the application of wettable sulphur during the parasitoid flight period. The sawfly usually recovers more quickly than its parasitoid when chemical control is discontinued, because propagation of L. ensator is limited in various ways. The parasitoid is time limited, because suitable second instar host larvae are rarely available for more than a week on a single apple variety. Moreover, parasitism levels stay moderate because the parasitoid females do not avoid superparasitism. Finally, relatively more sawflies than parasitoids emerge after 10 months underground, because the incidence of prolonged diapause is more elevated in L. ensator than in the sawfly. It is suggested that both the high incidence of prolonged diapause and the inability to avoid superparasitism are useful in reducing the risk of local extinction. Elevated sawfly attack in a single early apple variety would reduce exploitation of suitable host larvae in other nearby varieties, in as far as the parasitoid is not able to distinguish fruitlets with accessible second instar host larvae from those with inaccessible older larvae. Although the former are available for a limited time, the latter may keep the parasitoids from moving to the less abundant second instar larvae in late(r) varieties. Reduction of elevated host density in such an early variety by a properly timed application of a short‐lived pesticide, such as Quassia, increases parasitism levels proportionally, and is expected to promote parasitoid movement to host larvae in other varieties nearby.     

Development and parasitism by Aphelinus certus (Hymenoptera: Aphelinidae), a parasitoid of Aphis glycines (Hemiptera: Aphididae)

Since its introduction in 2000, the soybean aphid (Aphis glycines Matsumura) has been a serious pest of soybean in North America. Currently, insecticide application is the only recommended control method. However, a number of natural enemies have the potential to regulate soybean aphid populations. In 2007, Aphelinus certus Yasnosh, a soybean aphid parasitoid native to Asia, was found in commercial soybean fields in Ontario. This is the first record of this species in North America. To evaluate the potential biological control services provided by A. certus for soybean aphid management, temperature-dependent developmental parameters and functional response to soybean aphid were determined. A. certus is capable of completing its development between temperatures of 15.3 and 30.2°C. The lower thresholds of development for the egg-mummy and mummy-adult life stages were determined to be 9.1 and 11.6°C, respectively. The lethal temperature of development for the egg-mummy and mummy-adult life stages were 29.5 and 31.0°C, respectively. In this temperature range, A. certus did not exhibit temperature-dependent mortality; however, parasitism rate increased with temperature. A. certus exhibited a type II functional response to the soybean aphid.     

The phylogenetic relationships of introduced Aphelinus (Hymenoptera: Aphelinidae), biological control agents of the Russian wheat aphid (Homoptera: Aphididae)

Abstract  Several species of Aphelinus have been introduced to the US from the Old World for biological control of the Russian wheat aphid, Diuraphis noxia (Modvilko). Reproductive incompatibility has been observed among populations collected from different geographic areas. We examined whether or not the reproductive incompatibility between strains of A. asychis was caused by distant phylogenetic relationships. Ribosomal DNA sequences of internal transcribed spacers 2 (ITS2) were analyzed in several species of Aphelinus collected from multiple sites of Europe and Asia. The phylogenetic analysis showed that strains within the species A. albipodus and A. asychis are not monophyletic, and two clearly divergent clades were revealed among sequenced samples. Our results suggest that the reproductive incompatibility between three exotic strains of A. asychis was more likely caused by divergence of phylogeny than by symbiotic bacteria.     

Winter ecology of the cabbage aphid Brevicoryne brassicae (L.) (Homo., Aphididae) and its parasitoid Diaeretiella rapae (McIntosh) (Hym., Braconidae: Aphidiidae)

Abstract:  Flower strips near crops may stimulate natural enemies by the provision of nectar and hibernation sites. However, these habitats may also be beneficial for potential pest species. We investigated the dynamics of the cabbage aphid Brevicoryne brassicae (L.) (Homo., Aphididae) and its primary parasitoid Diaeretiella rapae (McIntosh) (Hym., Braconidae) in brussels sprout fields and adjoining flower plots in winter. A wide variety of 14 plant species were included in the study, each established as monoculture plots. Brussels sprout fields and flower plots were established at two sites. One site was located in an open agricultural landscape, the other in a landscape dominated by mixed forest. Brevicoryne brassicae and D. rapae were found on brussels sprout plants but not in the flower plots. Brevicoryne brassicae was initially more abundant in the open landscape, but as their densities declined rapidly in time, no living aphids were recovered at both sites by February. The density of aphids parasitized by D. rapae showed a similar trend, but densities of eight mummies per brussels sprout plant were still present by the end of February. These findings suggest that (i) flower species under investigation do not function as sources of B. brassicae and (ii) brussels sprout plants that are not harvested may not only harbour D. rapae populations that may sustain biological control, but are also likely to act as sources of B. brassicae infestation.