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.     

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     

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.     

Comparison of a Canadian and a Dutch strain of the parasitoid Aphelinus mali (Hald) (Hym., Aphelinidae) for control of woolly apple aphid Eriosoma lanigerum (Haussmann) (Hom., Aphididae) in the Netherlands: a simulation approach

Woolly apple aphid, Eriosoma lanigerum is one of the important apple pests in the Netherlands. Weather conditions and natural enemies determine whether woolly apple aphid (WAA) will reach pest status. WAA may escape control by natural enemies and therefore it must be controlled using chemical insecticides. To prevent unnecessary applications of insecticides and to promote biological and natural control of WAA more knowledge is needed about the role of natural enemies, weather and their effects on the development of WAA populations. The monophagous parasitoid Aphelinus mali (Hald.) has been introduced into most of apple growing areas to control WAA, but success is variable and depends on climatological conditions. In the Netherlands the level of parasitization is often too low, especially after warm winters. The biological control potential of a strain of A. mali from Nova Scotia (Canada) was compared with a Dutch strain by simulating population growth of both WAA and the Dutch and Canadian strain of the parasitoid for three different years The results indicate that the Canadian strain would perform in general better than the Dutch strain under Dutch weather conditions.     

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.     

Impact of Rag1 aphid resistant soybeans on Binodoxys communis (Hymenoptera: Braconidae), a parasitoid of soybean aphid (Hemiptera: Aphididae)

Multiple strategies are being developed for pest management of the soybean aphid, Aphis glycines Matsumura; however, there has been little published research thus far to determine how such strategies may influence each other, thereby complicating their potential effectiveness. A susceptible soybean (Glycine max L.) variety without the Rag1 gene and a near isogenic resistant soybean variety with the Rag1 gene were evaluated in the laboratory for their effects on the fitness of the soybean aphid parasitoid, Binodoxys communis (Gahan). The presence or absence of the Rag1 gene was verified by quantifying soybean aphid growth. To test for fitness effects, parasitoids were allowed to attack soybean aphids on either a susceptible or resistant plant for 24 h and then aphids were kept on the same plant throughout parasitoid development. Parasitoid fitness was measured by mummy and adult parasitoid production, adult parasitoid emergence, development time, and adult size. Parasitoids that attacked soybean aphids on susceptible plants produced more mummies, more adult parasitoids, and had a higher emergence rate compared with those on resistant plants. Adult parasitoids that emerged from resistant plants took 1 d longer and were smaller compared with those from susceptible plants. This study suggests that biological control by B. communis may be compromised when host plant resistance is widely used for pest management of soybean aphids.     

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.     

Functional responses of aphid parasitoids,Aphidius colemani (Hymenoptera: Braconidae) and Aphelinus asychis (Hymenoptera: Aphelinidae)

We evaluated the functional responses of two aphid parasitoids: Aphidius colemani on the green peach aphid Myzus persicae (Hemiptera: Aphididae), and Aphelinus asychis on M. persicae and the potato aphid, Macrosiphum euphorbiae (Hemiptera: Aphididae). Parasitoid oviposition occurred at host densities of 5, 10, 20, 30, 50, 80 or 100 aphids for A. colemani and 5, 10, 20, 30 or 50 aphids for A. asychis. More M. persicae were parasitized by A. colemani than by A. asychis at an aphid density of 50. Among the three types of functional response, type III best described the parasitoid response to the host densities both in A. colemani and A. asychis. The estimated handling time was shorter for A. colemani than for A. asychis (0.017 and 0.043 d, respectively). The proportion of aphids that were parasitized exhibited the same characteristic curve among the three host-parasitoid combinations: a wave form that appeared to be a composite of a decelerating (as in type II) response at low host density and an accelerating-and-decelerating (as in type III) response at medium to high host density. We hypothesize that the novel host species (and its host plant), density-dependent superparasitism, and/or density-dependent host-killing may have induced the modified type III response.     

Oviposition and host-feeding patterns in Aphelinus asychis (Hymenoptera: Aphelinidae) at different aphid densities

Abstract. 1. The patterns of host-feeding and oviposition were examined in Aphelinus asychis Walker, which had been provided with second-instar pea aphids as hosts.
2. Female wasps responded to increasing host density (between one and forty aphids for 24 h) with an increasing tendency to oviposit rather than to feed. Superparasitism occurred at all aphid densities, even when unparasitized aphids were available.
3. Aphids intended for feeding were paralysed and died. Wasps did not feed on and oviposit in the same aphid.
4. Feeding to satiation lasted between 4 min and 42 min. Females that had starved for ≰18 h generally deposited one or more eggs before feeding again, while the reverse was true in wasps that had starved for 21 h.
5. The host-feeding behaviour of A. asychis is determined by a female's nutritional status. At low rates of host encounter, the anhydropic eggs may be resorbed. This reproductive strategy conforms to the destructive non-concurrent type among the Hymenoptera.     

Effects of plant protease inhibitors, oryzacystatin I and soybean Bowman-Birk inhibitor, on the aphid Macrosiphum euphorbiae (Homoptera, Aphididae) and its parasitoid Aphelinus abdominalis (Hymenoptera, Aphelinidae)

Transgenic plants expressing protease inhibitors (PIs) have emerged in recent years as an alternative strategy for pest control. Beneficial insects such as parasitoids may therefore be exposed to these entomotoxins either via the host or by direct exposure to the plant itself. With the objective of assessing the effects of PIs towards aphid parasitoids, bioassays using soybean Bowman-Birk inhibitor (SbBBI) or oryzacystatin I (OCI) on artificial diet were performed on Macrosiphum euphorbiae-Aphelinus abdominalis system. OCI significantly reduced nymphal survival of the potato aphid M. euphorbiae and prevented aphids from reproducing. This negative effect was much more pronounced than with other aphid species. On the contrary, SbBBI did not affect nymphal viability but significantly altered adult demographic parameters. Enzymatic inhibition assays showed that digestive proteolytic activity of larvae and adults of Aphelinus abdominalis predominantly relies on serine proteases and especially on chymotrypsin-like activity. Immunoassays suggested that OCI bound to aphid proteins and accumulated in aphid tissues, whereas SbBBI remained unbound in the gut. Bioassays using M. euphorbiae reared on artificial diets supplemented with both OCI and SbBBI showed a fitness impairment of Aphelinus abdominalis that developed on intoxicated aphids. However, only SbBBI was detected in parasitoid larvae, while no PI could be detected in adult parasitoids that emerged from PI-intoxicated aphids. The potential impact of PI-expressing plants on aphid parasitoids and their combined efficiency for aphid control are discussed.     

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.     

褐带蚜小蜂产卵器刺入对寄主桃蚜存活、生长发育和繁殖力的影响

[目的]褐带蚜小蜂Aphelinus maculatus是2016年的中国新纪录种,是桃蚜Myzus persicae的重要寄生蜂之一.为科学评估褐带蚜小蜂对桃蚜的控制作用,研究了褐带蚜小蜂产卵器刺入对寄主桃蚜存活、生长发育和繁殖力的影响.[方法]培养皿中用油菜叶单头饲养、每天记录被褐带蚜小蜂产卵器刺入1次的桃蚜存活数...     

Microsatellites from Lysiphlebus hirticornis Mackauer (Hymenoptera: Braconidae), a specialist primary parasitoid attacking the specialist tansy aphid, Metopeurum fuscoviride Stroyan (Hemiptera: Aphididae)

Nine polymorphic microsatellite loci were isolated from the specialist aphid parasitoid, Lysiphlebus hirticornis. In addition, two published loci from closely related Lysiphlebus species were also used. Allelic diversity and heterozygosity were quantified in samples collected from eight tansy plants growing in an area of approximately 150 m² in Jena, Germany.     

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.     

苹果绵蚜蚜小蜂发育历期、发育起点温度和有效积温的研究

本文以苹果绵蚜为繁殖寄主,研究了苹果绵蚜蚜小蜂在不同温度下的发育历期、发育起点温度和有效积温。结果显示:苹果绵蚜蚜小蜂的发育历期随温度的升高而缩短,最适发育温度为21℃-27℃。山东地区越冬代苹果绵蚜蚜小蜂打破滞育的发育起点温度为雌蜂8.58℃,雄蜂8.22℃;有效积温为雌蜂148.72日度,雄蜂154.68日度。非越冬代苹果绵蚜蚜小蜂在卵-羽化阶段发育起点温度为雌蜂5.62℃,雄蜂5.55℃;有效积温为雌蜂284.40日度,雄蜂为295.61日度。并推测了2008年济南地区苹果绵蚜蚜小蜂发生代数和越冬代羽化时间,与实测情况基本相符。     

Reproductive compatibility and genetic variation between two strains of Aphelinus albipodus (Hymenoptera: Aphelinidae), a parasitoid of the soybean aphid, Aphis glycines (Homoptera: Aphididae)

Aphelinus albipodus Hayat and Fatima is a potential biological control agent of the soybean aphid, Aphis glycines Matsumura, which is a newly introduced soybean pest in the United States. We compared the reproductive compatibility and molecular genetic variation between two geographic strains of A. albipodus. One strain was collected from soybean aphids in Japan and the other recovered from Russian wheat aphid, Diuraphis noxia (Mordvilko), in the western U.S., populations of which were established with parasitoids imported from Eurasia. We present results of crossing experiments between the two strains, genetic differences based on RAPD-PCR markers, rDNA ITS1 and ITS2 gene sequences, and presence of Wolbachia in the two strains using PCR amplification of the wsp gene. We found no reduction in the production of females in reciprocal crosses between strains, but a significant reduction in fecundity when F₁ females stemming from one of the reciprocal crosses were backcrossed to males from either source. The two strains differed by 3.4% in the rDNA ITS1 sequence and by presence/absence of one RAPD-PCR marker from a total of 20 RAPD primers screened, but their rDNA ITS2 sequences were identical. We used restriction enzyme analysis to separate the strains by differential digestion of the ITS1 PCR product. Wolbachia was present in 100% of males and females of both strains of A. albipodus.