Eriosoma Lanigerum Research Articles

DISTRIBUTION, BIOLOGY, NATURE OF DAMAGE AND MANAGEMENT OF WOOLLY APPLE APHID, ERIOSOMA LANIGERUM (HAUSMANN), (HEMIPTERA: APHIDIDAE) IN APPLE ORCHARD: A REVIEW

Eriosoma lanigerum (Hausmann), the woolly apple aphid (WAA), is a major worldwide pest that feeds on Malus species. It is one of the most important invasive apple pests in the world, having spread from eastern North America to almost every apple-growing region on the planet. The crown and root systems of apple trees are infested by this aphid species. This aphid’s crawlers migrate up and down an apple tree continually, and the root colonies serve as a persistent source of infestation on aerial portions The WAA’s salivary gland secretions drive the injured tissues to create abnormal growths or galls that obstruct the transport of water and nutrients within the plant, weakening the tree. On the above-ground portions and on the roots of apple trees, the aphid develops tightly packed colonies coated with white, waxy, filamentous secretions. The use of resistant rootstocks, chemical, and biological control, or a combination of all three, are the mainstays of WAA management. Aphid resistance has emerged as a result of decades of pesticide usage, necessitating research to find alternatives to chemicals for pest control. This study has merely highlighted the information on the biology of the woolly apple aphid, the sorts of damage it produces, and management approaches for reducing it.

Biljne vaši (Hemiptera: Aphididae) - štetočine jabuke

Aphids are often present in apple orchards in Serbia. They represent a significant group of pests for which insecticides are regularly used. The most important species are: Aphis pomi, Aphis spiraecola, Dysaphis devecta, Dysaphis plantaginea, Dysaphis spp., Rhopalosiphum insertum and Eriosoma lanigerum. The paper provides basic data on the development of aphids and the most important data on their morphology, biology, distribution and harmfulness on apple plants. A species identification key is attached.

Diversity and relative abundance of insect fauna of apple (Malus domestica borkh) in high density plantation

During the course of study appearance of insect-pests started in the month of March coinciding with pink bud stage of apple. Insects belonging to orders Lepidoptera, Coleoptera, Hemiptera, Thysanoptera, Aracnida and Cucurlionoidae were identified. The relative abundance of insects belonging to order Hemiptera was maximum (32.44 and 32.88) followed by Acarina (23.66 and 22.42%) during 2018 and 2019, respectively. Major insect-pests recoded were Panonychus ulmi, Eriosoma lanigerum and Thrips flavus appeared as major pests in this crop. Maximum population of P. ulmi (5.30/leaf was reported on apple leaves during the month of September. However, the highest percent mean density i.e. 471 and the relative density i.e. 23.05% was reported in P. ulmi followed by T. flavus (385) under high density apple plantation. The Simpson’s Diversity Index were calculated as 0.85 and 0.84, respectively, during 2018 and 2019, which signifies the number of species present, as well as the relative abundance of each species under high density apple plantation.

Prirodni neprijatelji krvave vaši Eriosoma lanigerum (Hemiptere: Aphididae) u zasadima jabuke (Malus domestica)

Wooly apple aphid Eriosoma lanigerum Hausmann, 1802 (Hemiptera: Aphididae) is a significant pest of apple. Modern agriculture rapidly favors biological protection of plants and the introduction of certain beneficial organisms is becoming an increasingly frequent and promising way to control agricultural pests. In addition, the trend of withdrawing numerous active substances from the market has triggered an increasing interest of the agricultural public for predator, parasitoids and pathogens in the control of E. lanigerum. The parasitic wasp Aphelinus Mali Haldeman, 1851 (Hymenoptera: Aphelinidae) is considered the most important natural enemy of the wooly apple aphid. Although the application of this parasitic wasp is widely present in the integrated apple production, many studies indicate that the effectiveness of A. Mali is significantly increased when this species is used together with other beneficial insects, primarily with certain predatory species. The latest research indicates the frequent commercial use of predatory species in the control of wooly apple aphid, primarily representatives of the families Syrphidae, Chrysopidae and Coccinellidae. Also, for the successful suppression of the wooly apple aphid, it is very important to determine the optimal strategy that will ensure the successful integration of applied predators and other natural enemies of this pest.

The Host-Plant Origin Affects the Morphological Traits and the Reproductive Behavior of the Aphid Parasitoid Aphelinus mali

Diversifying agroecosystems through habitat management inside or outside production fields can provide alternative hosts and/or prey for natural enemies. In semi-natural habitats, parasitoids may find alternative host-plant complexes (HPC) that could allow their development when pest hosts are scarce in the field. However, morphological and physiological differences between alternative and targeted HPCs could affect the preference and fitness of the parasitoids, possibly altering their efficacy in regulating pests. In the present study, we examined two Aphelinus mali parasitoid populations developing on Eriosoma lanigerum from two host plants (Malus domestica-apple trees and Pyracantha coccinea). We hypothesized that A. mali from both HPCs will show different life history traits and behaviors because primary and alternative host-plants are known to induce variations in parasitoid biological performance. Our findings indicate that A. mali originating from E. lanigerum on P. coccinea parasitized more aphids and are smaller than those originating from E. lanigerum on apple. Furthermore, these parasitoids did not significantly vary their ability to attack and oviposit apple E. lanigerum, suggesting that P. coccinea could function as a suitable banker plant for A. mali. We discuss the potential use of P. coccinea in conservation biological control of E. lanigerum in apple orchards.

Exclusion netting affects apple arthropod communities

Exclusion cages can quantitatively demonstrate the value of natural enemies and the biological control services they provide. Currently, in Washington State, enclosing orchards in netting is being evaluated as a pest control method, but these enclosures may also serve as an exclusion cage to natural enemies, thereby disrupting biological control. To test the effects of net enclosures on apple arthropod communities, we conducted a two-year study comparing apple herbivore, predator, and parasitoid densities in caged and uncaged plots (both receiving insecticides) to an untreated check. Effects on the various groups were influenced by size and motility. Densities of larger motile arthropods, including codling moth (Cydia pomonella (L.)), chrysopids, and syrphids, were lower in the caged plots, demonstrating exclusion. Woolly apple aphid (Eriosoma lanigerum (Hausmann)) and its parasitoid Aphelinus mali (Haldeman) densities in the caged plots were over 100-fold greater and 5-fold greater, respectively, than the other treatments. European earwig (Forficula auricularia (L.)), a generalist predator, was more abundant in the caged plots in 2016 but not in 2017. Spider mites were more abundant in the cage treatments for both years, while predatory mites had higher densities in the cages in 2017 only. These outcomes show that net enclosures change the composition of apple arthropod communities through exclusion of certain herbivores and natural enemies. In the case of some pest herbivores (e.g., codling moth), this exclusion is beneficial, but in the case of predators, it is detrimental. This study further demonstrated that exclusion of only part of the natural enemy complex may be sufficient to cause herbivore outbreaks.

Design, Synthesis, and Study of the Insecticidal Activity of Novel Steroidal 1,3,4-Oxadiazoles.

A series of novel steroidal derivatives with a substituted 1,3,4-oxadiazole structure was designed and synthesized, and the target compounds were evaluated for their insecticidal activity against five aphid species. Most of the tested compounds exhibited potent insecticidal activity against Eriosoma lanigerum (Hausmann), Myzus persicae, and Aphis citricola. Compounds 20g and 24g displayed the highest activity against E. lanigerum, showing LC50 values of 27.6 and 30.4 μg/mL, respectively. Ultrastructural changes in the midgut cells of E. lanigerum were detected by transmission electron microscopy, indicating that these steroidal oxazole derivatives might exert their insecticidal activity by destroying the mitochondria and nuclear membranes in insect midgut cells. Furthermore, a field trial showed that compound 20g exhibited effects similar to those of the positive controls chlorpyrifos and thiamethoxam against E. lanigerum, reaching a control rate of 89.5% at a dose of 200 μg/mL after 21 days. We also investigated the hydrolysis and metabolism of the target compounds in E. lanigerum by assaying the activities of three insecticide-detoxifying enzymes. Compound 20g at 50 μg/mL exhibited inhibitory action on carboxylesterase similar to the known inhibitor triphenyl phosphate. The above results demonstrate the potential of these steroidal oxazole derivatives to be developed as novel pesticides.

Acute toxicity of lethal and sublethal concentrations of neonicotinoid, insect growth regulator and diamide insecticides on natural enemies of the woolly apple aphid and the obscure mealybug

Acute toxicity of lethal and sublethal concentrations of neonicotinoid, insect growth regulator and diamide insecticides on natural enemies of the woolly apple aphid and the obscure mealybug

EPG analysis of stylet penetration preference of woolly apple aphid on different parts of apple trees.

Woolly apple aphid (WAA), Eriosoma lanigerum (Hausmann), is an important global pest that feeds on Malus species. We studied the feeding preference of WAA on apple trees in the field for two consecutive years and in the laboratory we used electronic penetration graphs (EPG) to record the stylet penetration behavior of WAA on different parts of apple trees. We found that in the field WAA fed primarily on twigs and branches, not on leaves and fruits. Six EPG waveforms were produced during WAA probing on shoots, trunks and leaves of apple trees, including the non-penetration wave (np), the stylet pathway phase wave (C), the intracellular feeding wave (pd), the xylem feeding wave (G), waves indicative of release of saliva into the phloem (E1), and a wave indicative of ingestion from phloem (E2). In the laboratory, aphids only successfully fed on shoots, trunks and leaves, not on fruits. The EPG parameters on the phloem of shoots were significantly higher than those on trunks, indicating WAA prefer to feed on shoots. These laboratory findings explain the relative field feeding preference of WAA on different parts of apple trees, which occurs primarily on branches, barks, and young twigs in orchards, especially on young twigs.

Efficacy and Nontarget Effects of Net Exclusion Enclosures on Apple Pest Management.

Management of direct apple pests, such as codling moth, continues to be problematic despite the widespread implementation of behavioral and chemical controls. Apple growers have increased their use of netting to protect fruit from environmental injury, with some structures enclosing the entire orchard. These enclosures represent a new pest management tactic through physical exclusion. We conducted a two-year trial to examine the effects of full exclusion netting on pests and natural enemies of apples. Insect densities and damage in trees under fully enclosed (net) cages were compared with conventionally (insecticide only) treated and untreated plots. Caged plots had 18.1- and 11.4-fold less codling moth damage than the check, and 4.9- and 4.2-fold less damage than the insecticide-only plots in 2016 and 2017, respectively. However, densities of woolly apple aphid and its parasitoid Aphelinus mali (Haldeman) (Hymenoptera: Aphelinidae) were significantly greater in the caged plots. Densities of earwigs, a typically flightless generalist predator, were not different among treatments, while adults of more mobile flying generalist predators, lacewings and syrphids, were significantly lower in cages compared with uncaged plots. These results demonstrate that although biological control may be partially disrupted, net enclosures have significant potential as a holistic apple management technique.

Towards a Knowledge-Based Decision Support System for Integrated Control of Woolly Apple Aphid, Eriosoma lanigerum, with Maximal Biological Suppression by the Parasitoid Aphelinus mali.

Simple SummaryThe woolly apple aphid Eriosoma lanigerum is an important pest in apple orchards worldwide. At present, effective limitation of woolly aphid populations relies on a good synergy between chemical control treatments and biological suppression by beneficial insects, especially by its main specific natural enemy, the parasitic wasp (parasitoid) Aphelinus mali. In order to reach maximum control levels on woolly apple aphids and avoid negative side effects on A. mali, decision support for the optimal timing and positioning of control treatments is needed. In this study, we developed prediction models that based on the weather conditions (temperature data) can reasonably accurately predict crucial development/activity phases of both insects in the orchard. These prediction models can be utilized to target insecticide sprayings at the most sensitive stage of the pest (woolly apple aphids) and/or to avoid insecticide sprayings with detrimental side effects at the vulnerable stage of the beneficial insect (parasitoid A. mali), as was demonstrated by the outcomes of a field trial in this study.The woolly apple aphid Eriosoma lanigerum (Homoptera: Aphidiae) is an important pest in apple orchards worldwide. Since the withdrawal or restricted use of certain broad-spectrum insecticides, E. lanigerum has become one of the most severe pests in apple growing areas across Western Europe. At present, effective limitation of woolly aphid populations relies on a good synergy between chemical control treatments and biological suppression by beneficial arthropods, especially by its main specific natural enemy, the parasitoid Aphelinus mali (Hymenoptera: Aphelinidae). To develop a knowledge-based decision support system, detailed monitoring data of both species were collected in the field (region of Sint-Truiden, Belgium) for a period of ten years (2010–2020). Aphelinus mali flights were monitored in the field, starting before flowering until the end of the second-generation flight at minimum. The seasonal occurrence of the most important management stages of E. lanigerum, e.g., start of wool production or activity on aerial parts in spring and migration of crawlers from colonies towards flower clusters or shoots, were thoroughly monitored. All obtained data were compared with historical and literature data and analysed in a population dynamics phenological model. Our outcomes showed that the emergence of first-generation A. mali adults (critical for the first parasitation activity and the basis for following A. mali generations in the continuation of the season) can be accurately predicted by the developed model. Hence, this information can be utilized to avoid insecticide sprayings with detrimental side effects at this particular moment as demonstrated by the outcomes of a field trial. In addition, the start of migration of E. lanigerum crawlers towards flower clusters or shoots is accurately predicted by the model. In conclusion, our results demonstrate that the model can be used as decision support system for the optimal timing of control treatments in order to achieve effective control of E. lanigerum with maximal biological suppression by its main natural enemy.

Resistance Evaluation of G, CG, or M Series Apple Rootstocks to Soil-borne Diseases (Phytophthora Root Rot, White Root Rot, and Southern Blight) and Woolly Apple Aphid

Resistance Evaluation of G, CG, or M Series Apple Rootstocks to Soil-borne Diseases (Phytophthora Root Rot, White Root Rot, and Southern Blight) and Woolly Apple Aphid

Resistance performance of four principal apple cultivars to woolly apple aphid, Eriosoma lanigerum (Hemiptera:\xa0Pemphigidae), by simulated seasonal temperature in northern China

Woolly apple aphid (WAA), Eriosoma lanigerum (Hausmann) (Hemiptera: Pemphigidae), is a worldwide quarantine pest of apples. Understanding the resistance mechanism of various cultivars to WAA is important for the selection for durable resistance. Few studies have examined the resistance of different apple cultivars to WAA in China; among common varieties produced in China, Red Fuji is highly sensitive to WAA. In this study, the resistance to WAA of Red Fuji and three other common cultivars—Starkrimson, Jonagold, and Ralls Genet—was assessed based on the developmental and reproductive biological characteristics of aphids, assessed under four fixed temperatures: 20, 25, 30, and 35 ℃. We found the optimal temperature for WAA growth and reproduction to be 20–25 ℃, at which temperature, aphids on Red Fuji showed the highest rate of reproduction, the highest number of colonies, and the greatest area covered by aphid colonies among the four cultivars. These attributes of WAA were significantly higher at 20–25 ℃ than at 30 ℃. On Red Fuji, the most favorable variety, WAA showed its highest net reproductive rate (127.3 ± 13.3), intrinsic growth rate (0.30 ± 0.01), highest growth rate of the colony area (1.35 ± 0.02), and the lowest average generation time (16.1 ± 0.8 day) at 25 ℃. The aphids inoculated onto the four tested cultivars all died within 1 week at 35 ℃. Overall, Red Fuji was highly susceptible, while Starkrimson, Jonagold, and Ralls Genet were partially resistant.

Biological properties and influencing factors of woolly apple aphid (Eriosoma lanigerum Hausm) in the condition of orchard agrobiocenosis

This article provides information on the influence of biotic and abiotic factors on the development of the population of orchard agrobiocenosis of woolly apple aphid (Eriosoma lanigerum Hausm), the main sucking pest of seed orchards.

Mitochondrial Genome of Aphelinus mali (Haldeman) (Hymenoptera: Aphelinidae) with a Higher at Percent and the Highest AT-Skew in Hymenoptera

Aphelinus mali (Haldeman) (Hymenoptera: Aphelinidae) is an important specific endoparasitoid of Eriosoma lanigerum (Hausmann) (Hymenoptera: Aphididae) with high natural parasitism in the field. By studying the COI gene of the A. mali mitochondrion, two distinct clades, Shandong and Liaoning clades, were found in China. In this paper, the mitochondrial genome of A. mali populations from Shandong province was sequenced and analyzed. In total, 14415 bp were sequenced, representing 93.5% of the total length of the A. mali mitochondrial genome, with six tRNA, trnY, trnM, trnI, trnQ, trnW, trnS1, not sequenced. The unmeasured area was located in an A+T-rich region of approximately 1000 bp. The AT content in the A+T-rich region was as high as 91.3% and this may be why this region has not been detected until now. The A+T content was 84.4% in the measured region, which is higher than that of other Hymenoptera. The AT skew was 0.1291, the highest AT skew known among Hymenoptera, which might be related to the higher AT content of protein-coding genes, rRNA and RSCU AT content. Transport genes (tRNA) had a secondary clover shaped structure, compared with other Hymenoptera; there is a more incomplete secondary structure, and less base mismatch. The mitochondrial genome of A. mali showed considerable rearrangement when compared with the mitochondrial genome of the most primitive arrangement, mainly concentrated in six tRNA genes and the gene region from cob to trnE and from trnL to nad1. The mitochondrial genome of A. mali is quite different from that of other Hymenoptera as can be demonstrated by constructing a phylogenetic tree. This paper provides a basis for further study of phylogeny, genetic structure, and hybridization of A. mali populations.

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 327Mb, with 91% of the assembled sequences anchored into six chromosomes. The contig and scaffold N50 values are 158kb and 71Mb, 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.

Comparative Analysis of Stylet Penetration Behaviors of Eriosoma lanigerum (Hemiptera: Aphididae) on Main Apple Cultivars in China

The preference and behavioral mechanism of the feeding behavior of the woolly apple aphid, Eriosoma lanigerum (Hausmann), on Chinese apple cultivars was investigated using the electrical penetration graph (EPG) technique. Feeding of adult aphids was assessed for the four main cultivars of apple in China (Red Fuji, Ralls Genet, Starkrimson, and Jonagold) over an 8-h monitoring period, what that of fourth-instar nymphs was assessed for 8 h on Jonagold only. EPG waveforms representing the details of probing behaviors, parameters were measured for analysis. We found that at the nonphloem phase, the total duration of the nonpenetration (np) waveform and the total duration of the stylet pathway phase (the 'C wave') on Ralls Genet and Starkrimson were significantly longer than on Red Fuji. In addition, the phloem-feeding phase, the total duration of 'release of saliva into the phloem', (the E1 waveform) was significantly longer on Ralls Genet and Jonagold than on Red Fuji. The total duration of the 'ingestion from sieve cells' phase (the E2 waveform) on Red Fuji, meanwhile, was significantly longer than on Ralls Genet or Starkrimson. At the same time, when combined with EPG parameters, Red Fuji was found to have no obvious resistance to woolly apple aphid and to be a susceptible cultivar. This experiment also recorded the feeding waveform of fourth-instar aphid nymphs. Based on the phloem and nonphloem parameters recorded in this study, it was inferred that adult aphids are more likely than nymphs to feed on apple trees.

Comparison of the toxicity and repellency of two conventional neonicotinoids and a coconut-derived insecticide soap toward the parasitoid wasp Aphelinus mali Haldeman, 1851

The parasitoid wasp Aphelinus mali,Haldeman, 1851 (Hymenoptera: Aphelinidae) is the most important biological control agent against the woolly apple aphid, Eriosoma lanigerum (Hausemann, 1802) (Hemiptera: Aphididae), which is an important apple orchards pest throughout the world. Based on the importance of using low-risk compounds to protect beneficial agents, the present study was carried out to evaluate the toxic and repellent effects of two conventional chemicals (imidacloprid and thiacloprid) and coconut-derived biopesticide soap (PalizinÒ) toward A. mali. The results of residual bioassays on apple leaf discs indicated that imidacloprid after 24 h and insecticide soap after 72 h exposure time categorized at the highest and no/little toxicity rates, respectively. Ingestion bioassays on filter papers revealed that imidacloprid and thiacloprid had moderate toxicity rate, while insecticide soap had a low-level toxicity rate. Repellency test at Y-tube olfactometer showed that the repellent effects of both chemicals were more than that of insecticide soap. It is concluded that coconut-derived soap was compatible with the parasitoid activity, and the caution should be paid when including the two neonicotinoid insecticides imidacloprid and thiacloprid for E. lanigerum management.

Influence of invasive pest and natural enemies on entomofauna formation in the Sochi region

The article describes the changes in local entomofauna in the Sochi region. Monitoring for several decades provides information about the spreading and density of invasive species established a long time ago and causing massive damage to agricultural plants during regular outbreaks. This group of species, which includes the Boisduval scale Diaspis boisduvalii, the Japanese planthopper Ricania japonica, and the fall webworm Hyphantria cunea, has had an enormous effect on local insects’ community for the last 50 years. What is most important is that this list of alien species continues to grow. Since the late 1990s, several invaders have been discovered in the Sochi region, including including the sycamore lace bug Corythucha ciliata, the leafhoppers Metcalfa pruinosa and Arboridia kakogawana, the brown marmorated stink bug Halyomorpha halys, the tortoise wax scale Ceroplastes japonicus and the woolly aphid Eriosoma lanigerum. The invasion process causes significant changes in the relationship between newly established populations of invasive pests and their natural enemies, which are partly used as biocontrol agents. So the impact of local and introduced entomophagous species on the fauna is also discussed.

Perceptions and outcomes of conventional vs. organic apple orchard management

Organic farming can improve soil quality and provide effective pest control with reduced inputs compared to conventional farming. Although organic and conventional farming are often viewed as dichotomous, they may overlap in pest management and soil quality goals and outcomes. Here, we assessed similarities and differences between conventional and organic apple orchards in Washington State by quantifying pesticide program risk to natural enemies, soil quality, leaf nitrogen, and abundance of woolly apple aphid (Eriosoma lanigerum) and its natural enemies. We also interviewed orchard owners, managers, and consultants to learn about their practices and opinions of conventional and organic management for aphids and soil quality. Organic orchards used more insecticide applications than conventional orchards, but the insecticides used were rated as less harmful to natural enemies. Conventional and organic orchards had similar soil quality, pest abundance, and natural enemy abundance. Woolly apple aphid abundance was not correlated to soil, plant, or natural enemy measurements. Interviews revealed that management goals were similar in both systems. Overall, our results suggest that both conventional and organic styles of farming are heterogenous. For example, conventional farmers may simply follow recommendations for inputs of synthetic fertilizers and pesticides or go further by using some organic or integrated practices; at the same time, organic farmers can vary in their use of organically certified pesticide sprays and ecologically based management tactics. Our study suggests that integrated management strategies that use a mix of appropriate tactics may be more important than being strictly conventional or organic to achieve superior soil and pest management outcomes.