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Identification & Distribution:

On their secondary host (apple) Eriosoma lanigerum wingless females are purple, red or brown and are covered in thick white flocculent wax. This is produced by distinct wax glands on the head and along the thorax and abdomen. The six segmented antennae are 0.17-0.24 times the length of the body. The body length of Eriosoma lanigerum apterae is 1.2-2.6 mm.

The fourth instar alatiform nymph of Eriosoma lanigerum (shown in the first picture below) is reddish brown with very small wax glands and consequently much less wax. Winged viviparous females (shown in the second picture below) have a brown-black head and thorax and a brown abdomen. Their antennae are about 0.4 times the length of the body. The siphunculi are reduced to a pair of rings on the posterior dorsum of the abdomen.

 

The pictures below show (first) a dorsal view of an Eriosoma lanigerum adult aptera in alcohol and (second) a dorsal view showing wax glands on the head.

 

The clarified slide mounts below are of adult viviparous female Eriosoma lanigerum : wingless, and winged.

 

Micrograph of clarified mounted  aptera (first image) courtesy PaDIL.  Copyright Alice Ames (Department of Primary Industries, Victoria) under Commons Attribution 3.0 Australian License. Alate micrograph (second image) courtesy Favret, C. & G.L. Miller, AphID.  Identification Technology Program, CPHST, PPQ, APHIS, USDA; Fort Collins, CO.

Wingless females of woolly apple aphids live in dense colonies (see picture top) on the roots, trunk or branches of the (secondary) host apple (Malus) where it is a serious pest, often causing deformation and cancer-like swellings of bark. Eriosoma lanigerum is also found on related species, such as hawthorn (Crataegus) and Cotoneaster.

In most parts of the world, sexual forms have never been found, and overwintering is in fissures on the lower part of the trunk and on the roots. Sexuparae producing oviparae and males on apple have been reported in a few countries, with eggs laid on apple, but no resultant fundatrices have been found. In North America aphids of the Eriosoma lanigerum group (which includes several species closely-related to Eriosoma lanigerum, in USA) induce leaf-rosette galls on American elm (Ulmus americana). Some authorities classify such aphids as Eriosoma lanigerum. Others believe that Eriosoma lanigerum (in the strict sense) has lost its primary host and classify the (elm-feeding) host-alternating species as different species within the Eriosoma lanigerum species group.

 

Biology & Ecology:

Wax

Woolly apple aphids, as their common name suggests, have a dense wax covering. This is secreted afresh after each moult, so newly-moulted individuals have little or no wax, whilst adults often have long tendrils of accumulated wax (see picture below). Smith (1999)  looked at the structural details of wax glands and the physical form of the secreted wax for the apterae of woolly apple aphid. The glands are composed of greatly enlarged epidermal cells underlying a modified cuticle that forms distinctive wax gland plates. Secreted wax in the form of threads passes out of the cuticle as filaments. The arrangement of these filaments in the cuticle above each epidermal cell gives rise to the distinctive wax skein found in each wax-producing species (hollow, solid or honeycombed).

Smith suggests that the primary role of the secreted wax is to prevent the aphids becoming contaminated by their own honeydew (see picture above of wax-coated honeydew droplets) and that of other members of the colony, a view supported by Pike et al. (2002).  Other secondary roles of wax may include individual microclimate isolation, protection from fungi, parasites and predators plus waterproofing and frost protection.

Life cycle

Gautam & Verma (1983)  studied the life history and reproductive behaviour of apterous virginoparae (wingless parthenogenetic females, that give birth to same) of Eriosoma lanigerum in Himachal Pradesh, India, in the summer and winter seasons. The aphids underwent 4 moults resulting in 5 instars. The pre-reproductive and reproductive stages were longer in winter than in summer, while fecundity was greater in summer than in winter. During summer, the maximum infestation occurred on the aerial parts of the tree, while in winter the roots suffered severe attack. Migration from roots to shoots in summer and from shoots to roots in winter was observed. No nymphal overwintering was observed. Alate sexuparae (winged parents of sexula forms) appeared from late July to early November; their offspring was also sexuparous.

Asante (1994)  looked at the seasonal occurrence, development and reproductive biology of the different morphs of Eriosoma lanigerum in New South Wales, Australia. As with many other aphids, Eriosoma lanigerum is polymorphic, this despite the fact that in Australia its life cycle is restricted to apple trees and it has no herbaceous secondary host. The different morphs are: (1) apterous virginoparae; (2) alate sexuparae or virginoparae; and (3) sexuales (males and oviparae). The apterous virginoparae occur on apple trees throughout the year. The alate aphids are the offspring of apterous virginoparae and they occur first in November and then from late January to late April. Alate aphids appearing in early November produce only virginoparae, alates appearing from late November to late January produce a mixture of virginoparae and sexuales, whereas those appearing from February to April produce exclusively sexuales. Sexuales are apterous, have degenerate mouth parts and oviparae produce non-viable eggs. Although males and oviparae of this aphid appear seasonally, perpetuation of the species appears to be entirely parthenogenetic, and overwintering is accomplished in the form of cold-hardy apterous virginoparae. Apterous virginoparae attain a rapid rate of nymphal development, large adult size, high fecundity and high population growth rate in the spring compared to summer, autumn and winter. Populations peak in February-March each year.

Damavandian & Pringle (2000)  studied the field biology of subterranean Eriosoma lanigerum on two farms in the Elgin apple growing area from October 1995 to January 1999. There were two peaks of activity in subterranean Eriosoma lanigerum populations, one during early summer and one during autumn. Nitrogen levels in the roots also peaked at these times of the year. All developmental stages were recorded on the roots of apple trees throughout the year. Peak numbers of first instar aphids were recorded during spring. Embryos were present in all instars throughout the year. More embryos were recorded in fourth instar and adult aphids than in the other developmental stages. Peak numbers of embryos were also recorded in the final two developmental stages (fourth instar and adults) during spring. Nitrogen levels were higher in healthy roots and in roots adjacent to galls than in galls.

Sandanayaka & Bus (2005)  suggest that their observations on oviparae in New Zealand are evidence of sexual reproduction of Eriosoma lanigerum in New Zealand. Reproduction of the woolly apple aphid can take place parthenogenetically or sexually when both host plants, apple (Malus domestica) and elm (Ulmus americana) are available. Since elm is not commonly grown in New Zealand, Eriosoma lanigerum is thought to reproduce there only parthenogenetically. During their studies between 1999 and 2003, different morphs of Eriosoma lanigerum were observed on apple trees, which were studied in more detail in 2003 and 2004. In the laboratory, alates produced mainly sexual morphs with degenerate mouthparts. Oviparous females lived for about 9 days and males lived for 7 days. Both went through 4 moults, without feeding or changing body size. Oviparous females laid a single egg and died soon after oviposition. In addition to sexual morphs, shiny brown, oblong eggs were seen on apple leaves grown outside - as well as in the glasshouse. As the numbers of eggs and sexual morphs on trees grown outside were less than on those grown in the glasshouse, the authors suggested that alates disperse into the natural environment searching for an apple or elm tree to continue the sexual reproduction while spreading the population.

Movement

Hoyt & Madsen (1960)  looked at the dispersal behaviour of the first instar nymphs ('crawlers') of woolly apple aphid. The first-instar apterae are the forms important in dispersion. Older apterous forms are more or less sessile, and, in California, alates apparently produce sterile sexual forms, so that infestation is confined to apple. Laboratory investigations were carried out with aphids reared on seedling apple trees and removed to a temperature gradient. Gradients round the tree trunk were greater than those up the trunk, but there were no correlations between them and aphid movement. Most of the aphids showed negative phototropism in the laboratory, the percentage to do so increasing as the temperature was raised. When a light source was combined with a temperature gradient, high temperatures and light were highly repellent to the aphids. Low temperatures and a light source together reduced the attractant effect of temperatures between 60 and 70°F. and also reduced the repellent effect of a light source. Many of the laboratory-reared aphids showed positive geotropism, but aphids collected while moving up a tree trunk in the field showed no obvious geotropic response. The latter aphids appeared to respond to light as a stimulus. Air movement over a smooth surface in the laboratory caused most of the aphids to orient themselves with or against the flow of air. In the field, the surface of the ground was not smooth, and wind direction was variable; as a result, the orientation of the aphids did not appear to be affected by air movements.

Studies of seasonal movements showed that the number of aphids moving up the tree increased during May and June, reached a high level during July and August and declined during September, October and November. A second peak of upward movement occurred during December, followed by a rapid decline in January, after which activity remained at a low level until mid-April. The number of aphids moving down showed a rapid increase during May, June and July, reaching a high peak during August and September. A rapid decline in movement occurred during October and November, and the number of aphids moving down remained at a low level until the following June. The amount of rainfall affected the number of aphids moving up, heavy rains causing a reduction in movement. Light was also important, since, in its absence, very few aphids moved up out of the soil. Low temperatures and parasites were the major factors that brought about a reduction in the amount of downward movement. The greatest amount of movement occurred in the late afternoon, and very little occurred during the hours of darkness. Adhesive bands placed immediately above and below single colonies to determine the direction of movement showed that 60 per cent. of the aphids leaving these colonies went downwards; 10 per cent. of the aphids moving down a limb were found to reverse their direction on encountering another limb. Infestation of apple cores occurred during late summer, when the number of aphids in movement was very high, and was probably due to accidental entry into the calyx.

Bhardwaj (1995)  carried out a field study during 1991 and 1992 on apple trees in Himachal Pradesh, India, to investigate the movement of Eriosoma lanigerum. The movement was confined to the first-instar nymphs and continued throughout the year except in severe winters. The movement was significantly greater from the root to the shoot zone than from the shoot to the root zone. Ambient temperature (> 10.3°C) and soil temperature (> 11.5°C) triggered the aphid movement towards both zones. Increase in ambient temperature from 13.2 to 26°C favoured maximum movement unless interrupted by other factors. Two simultaneous upward and downward movement peaks were recorded each year, first during mid-June and second during October-November. The net correlation between movement and mean maximum temperature was positive and significant, whereas it was insignificant for mean minimum temperature and rainfall.

Genetics

Landscape genetics have been particularly relevant when assessing the influence of landscape characteristics on the genetic variability and the identification of barriers to gene flow. Linking current practices of area-wide pest management information on pest population genetics and geographical barriers would increase the efficiency of these programs. Lavandero et al. (2008) collected data on genetic diversity and flow for the woolly apple aphid on apple trees from different locations in a 400 km north-south transect through central Chile. The percentage of molecular variation among locations was 18%. Using a Bayesian  clustering method they inferred the presence of four genetic clusters in the study region. Clustering of individuals followed a pattern explained by some geographical barriers. Barriers to gene flow other than distance were detected, created by a combination of main rivers and mountains.

Timm et al. (2005)  studied the genetic diversity of Eriosoma lanigerum populations in the Western Cape, South Africa. A total of 192 individuals from four different regions were collected and analysed. Results indicated that a low level of genetic variation in Eriosoma lanigerum populations in the Western Cape. 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 a good possibility of controlling woolly apple aphid in the Western Cape using host plant resistance.

Population dynamics

Pringle & Heunis (2008)   describe the development of a sampling system for monitoring population levels of the Eriosoma lanigerum in apple orchards in the Western Cape Province of South Africa. Colonies were counted on half of each of 25 apple trees per 2 ha block. Sampling error was affected by whether the colonies were found in wounds or in leaf axils. Parasitism of colonies in leaf axils had a slight effect on sampling error. Sampling error for colonies in leaf axils was high at just over 40%. However, decisions regarding intervention were not markedly compromised by simply classifying the 25 trees as infested or uninfested, as opposed to counting colonies in leaf axils. The presence-absence system greatly reduced the time spent monitoring Eriosoma lanigerum population levels, making it an attractive system for assessing woolly apple aphid infestations in commercial orchards.

Asante et al. (1993)  analyzed the spatial distribution patterns of Eriosoma lanigerum in an established apple orchard using the negative binomial  parameter k, Taylor's power law,  and Iwao's regression technique. All three indices indicated a highly aggregated distribution of the aphid in the apple orchard. There was a weak but significant linear relationship between the negative binomial k and the mean density for the individual aphids but not for aphid colonies. Compared with Iwao's regression, Taylor's power law provided a better description of the relationship between the variance and mean density. Woolly apple aphid occurred on the apple trees mainly as apterous virginoparae throughout the year and showed a preference for the lower part of the canopy and the trunk. At low infestations, the aphid is confined to the trunk and large branches but disperses to establish colonies on twigs or new lateral growths during peak populations. Woolly apple aphid has a limited ability to disperse between trees. Population density appears to increase mainly within trees. The relationship between the proportion of infested trees and mean aphid density had an asymptotic upper limit of 33% infestation level.

Alspach & Bus (1999)  investigated the spatial distribution of woolly apple aphid using local trend surfaces to examine large scale patterns, and point process analyses to check for the presence of small scale clumping. Large scale patterns in woolly apple aphid distribution were found which could be attributed to the degree of exposure of the trees, and clumping was also detectable. The experimental design was found to adequately accommodate these spatial patterns.

Brown & Schmitt (1994)  studied the population dynamics of Eriosoma lanigerum in sprayed and unsprayed apple orchards in West Virginia, USA. In an unsprayed orchard, peak abundance of arboreal populations was 22-24 colonies per tree in early June each year. Spraying the orchard with a pyrethroid three times during 1989 had little effect on the population behavior, demonstrating the resilience of the woolly apple aphid and its natural enemy guild. Nearly 20% of the aphid colonies in June had syrphid larvae present, and parasitism by Aphelinus mali was more than 50% in July. The age structure of arboreal woolly apple aphid colonies varied through the summer with a significant reduction in first instars in July, signalling a return of aphids to the underground from the arboreal environment at that time. Samples of arboreal populations were not useful for predicting year-to-year population abundance or the extent of root infestations in a managed orchard. Microhabitat preference of arboreal colonies during the spring was for wound sites and other protected feeding sites on the tree branches and trunk. Leaf axils were the predominant microhabitat from the end of May through August. Cicada oviposition sites were also highly preferred. Woolly apple aphid colonies were observed more often in wounds and protected sites on branches in sprayed orchards and in high density populations than in unsprayed or low density populations. The authors suggested that these protected sites act as refuges for woolly apple aphid populations in apple orchards.

Lordan et al. (2015)  used a multilateral approach that included both biotic and climatic data to detect the main variables that affected the ecology and population dynamics of woolly apple aphid Eriosoma lanigerum. Crawlers (first instar nymphs) migrated up and down the trunk mainly from spring to autumn and horizontal migration through the canopy was observed from May to August. Winter temperatures did not kill the canopy colonies, and both canopy and root colonies are the source of reinfestations in Mediterranean areas. Thus, control measures should simultaneously address roots and canopy. European earwigs (Forficula auricularia) were found to reduce the survival of overwintering canopy colonies up to June, and this can allow their later control by the parasitoid Aphelinus mali from summer to fall.

Asante et al. (1997)  reviewed the world literature on the natural enemies of Eriosoma lanigerum. Five species of hymenopterous parasitoids and two species of Acarina (ectoparasites) were reported to attack Eriosoma lanigerum. Altogether, 73 species of predatory insects belonging to five orders and seven families (i.e. Coccinellidae, Chrysopidae, Hemerobiidae, Forficulidae, Lygaeidae, Syrphidae, and Cecidomyiidae) have been reported to feed on this aphid species. Verticillium lecanii is the only fungal pathogen reported to infect Eriosoma lanigerum. Although the aphelinid Aphelinus mali has been widely acclaimed as the most important natural enemy of this aphid species, a review of the literature, however, revealed a number of other natural enemies which should be considered in biological control or integrated pest management programs of Eriosoma lanigerum.

Note that the natural enemies of the woolly apple aphid have been so widely incorporated into biological and integrated control programmes worldwide, that we include all other research on them in the section below on biological control. 

Other aphids on same host

Blackman & Eastop list about 45 species of aphid  which feed on apples worldwide. Of those aphid species, Baker (2015)  lists 11 as occurring in Britain: Aphis pomi,  Dysaphis anthrisci, Dysaphis brancoi, Dysaphis devecta, Dysaphis chaerophylli, Dysaphis plantaginea,  Eriosoma lanigerum Macrosiphum euphorbiae,  Myzus persicae,  Ovatus crataegarius,  and Rhopalosiphum oxyacanthae.  About six of those species are commonly encountered on the orchard apple (Malus domestica) and crab apple (Malus sylvestris).

 

Damage and control

Damage

The woolly apple aphid is an important economic pest of apple in North America, the Middle East, India, the Far East, South America, Australia and New Zealand, causing severe damage through direct feeding rather than virus transmission. Root damage is usually more severe than stem damage, is harder to detect and more difficult to control.

CABI (2017)  provide an excellent description of the symptoms of Eriosoma lanigerum infestation, and of the damage caused to apple as a result. Eriosoma lanigerum occurs on the both the aerial and subterranean woody tissue of apple. Compounds in aphid saliva can cause deformations, blisters, splitting and cancer-like swellings of the bark on the trunk, branches or twigs. Galling of aerial plant parts can reach the size of a walnut and interfere with sap circulation. Root infestations also cause galling, and damage to roots encourages secondary infection particularly the formation of root canker, a disease caused by the fungal pathogen Nectria ditissima. Feeding disrupts nutrient balance, with reduced foliar nitrogen and phosphorous compared to control trees (Weber and Brown, 1988 ).

Brown et al. (1992)  collected root galls on apple trees created by woolly apple aphid feeding. Root galls, ungalled roots, and ungalled sections of galled roots were analyzed for water conductivity and nitrogen concentration. Water conductivity was significantly reduced through root gall tissue. Root galls had a significantly higher concentration of nitrogen than ungalled roots. Roots of apple trees in the greenhouse were treated with the plant hormones indole-3-acetic acid and 6-benzyl-aminopurine to induce gall formation. Woolly apple aphid galls were characterized by a proliferation of anomalous nonfunctional xylem. Growth anomalies On roots treated with 6-benzyl-aminopurine had typical xylem with a proliferation of phloem tissue. Very little internal or external deformation of roots was observed after treatment with indole-3-acetic acid. Disruption of root xylem, resulting in resistance to water conduction, is one mechanism by which woolly apple aphids reduce the growth of apple trees.

Yield losses due to infestation of apple tree roots were studied in West Virginia, USA, by Brown et al. (1995) . In a year of high fruit production, there was a significant reduction in the number of fruit and weight of fruit per tree, partly because of increased fruit drop and reduced fruit set. Aphids were observed on only 11.5% of terminal branches, suggesting that a reduction in the amount of storage carbohydrates in galled roots may be a partial explanation of how the pest reduces tree growth and production. Damage is particularly severe in young trees, and roots of nursery trees can be particularly affected.

Plant resistance

Knight et al. (1988)  surveyed the world literature on the resistance of cultivated varieties of apple to Eriosoma lanigerum, and provided a list of 18 varieties found immune or highly resistant by at least three independent workers. In addition, 19 varieties were tabulated that have been variously described as immune (or highly resistant) and susceptible in different localities. Well authenticated but conflicting reports on a further 43 varieties confirm that biologic races of the aphid must exist. Despite this, the "Northern Spy" variety has maintained an outstanding level of resistance wherever it has been tested. This resistance is shown to be controlled by a single dominant gene, Er, having little or no minor gene background. This gene appears to be closely linked with an incompatibility gene. The gene Er has considerable potential value in breeding for resistance in rootstock and scion apple varieties.

Bus et al. (1988)  report molecular markers for three genes conferring woolly apple aphid resistance and placing them on two linkage groups on the genetic map of apple. The Er1 and Er2 genes derived from "Northern Spy" and "Robusta 5" respectively, are the two major genes that breeders have used to date to improve the resistance of apple rootstocks to this pest. The gene Er3, from Aotea (an accession classified as Malus sieboldii), is a new major gene for woolly apple aphid resistance. Genetic markers linked to the Er1 and Er3 genes were identified by screening markers from resistant and susceptible plants from populations segregating for these genes. Markers for each of the genes were validated for their usefulness for marker-assisted selection in separate populations. The potential use of the genetic markers for these genes in the breeding of apple cultivars with durable resistance to woolly apple aphid is discussed.

Sandanyaka et al. (2003)  studied the resistance characteristics of the apple resistance genes (Er1, Er2, and Er3) to the woolly apple aphid, according to the performance measured on apple cultivars containing these resistance genes. The resistance characteristics of Northern Spy (Er1), Robusta 5 (Er2), and Aotea (Er3) were compared to the susceptible cultivar Royal Gala, by measuring the aphid settlement, development, and survival rates correlated with electronically monitored probing behaviour. Er1 and Er2 had a higher level of resistance with a significantly shorter period of phloem feeding, suggesting that the resistance factors were present in the phloem tissue. Phenological measurements indicated that the aphids showed poor settlement, development, and survival on Er2. Er1 also showed low settlement and survival, although not as low as Er2. Aphid performance and feeding on Aotea (Er3) were similar to Royal Gala, suggesting that some woolly apple aphids in New Zealand may have recently overcome Er3 resistance. The authors dicussed differences in resistance mechanisms of Er1, Er2, and Er3 in relation to the strategy of pyramiding these genes to give a durable resistance to woolly apple aphid.

Sandanyaka et al. (2005)  assessed the resistance of a number of apple accessions to the woolly apple aphid based on the biological parameters of the insect. Two experiments were conducted under glasshouse conditions in two consecutive years. In Expt 1 in 2002, settlement, development and survival of the aphids were assessed on five apple accessions. Royal Gala was the most susceptible and Willie Sharp the most resistant accession to woolly apple aphid. These two were included as references in Expt 2 in 2003, with 11 further accessions. Daily reproductive rate and colony establishment were added to the three parameters assessed in Expt 1. The overall results showed resistance in Geneva, G01-078, Willie Sharp and G01-104 to settlement and development with low survival at the larval stage of the aphid, whereas Raritan showed resistance in all the parameters tested.

Ateyyat & Al-Antary (2009) assessed the susceptibility of nine apple cultivars to woolly apple aphid in Jordan. Fuji was significantly the most infested cultivar during the period of study and it ranked as a highly susceptible cultivar. Prima Rouge, Early Gold, Starking Delicious, Golden Smoothee, and Golden Delicious showed lower susceptibility. Harmony was an immune cultivar as it sustained neither edaphic (root inhabiting) nor arboreal colonies of woolly apple aphid. We propose the development of rootstocks from Harmony cultivar. The latter offers a new gene for resistance to woolly apple aphid that will open the door for plant breeders to produce different resistant rootstocks.

Chemical Control

Bower (1987)  conducted trials to test chlorpyrifos (a crystalline organophosphate) and diazinon (a liquid organophosphate) as alternatives to methidathion (a highly toxic organophosphate) for control of San Jose scale. Methidathion is very effective but disrupts integrated control of two spotted mite by killing the predatory mite Typhlodromus occidentalis. Neither chlorpyrifos nor diazinon disrupted integrated mite control. A single spray of chlorpyrifos or methidathion at the commencement of the first generation of crawlers in late spring gave effective and equivalent control of the scale but diazinon was less effective. One application of 2 or 3 percent dormant oil was as effective as insecticides applied against crawlers. The addition of insecticides to 2 percent dormant oil sprays did not improve scale control. Of the three insecticides and oil evaluated as control agents against woolly aphid, chlorpyrifos was the most effective when used as a dormant or spring application, followed by diazinon and then methidathion, while dormant oil was ineffective.

Nicholas et al. (2003)  used insecticide soil-root drenches to control woolly apple aphid in Australia. Root colonies are protected from the pesticide sprays applied during the growing season, and due to the climatic effects of winter, so they 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 (of systemic neonicotinoid insecticides), 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 (a selective carbamate insecticide) or vamidothion (an organothiophosphate pesticide), 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 authors discussed the potential for imidacloprid in integrated pest management programs.

Beers et al. (2007)  notes that Eriosoma lanigerum has become a more severe pest in Washington (USA) apple production in the past years. Milder winters have promoted overwintering survival on the aerial parts of the tree. A very low percentage of the current apple acreage is planted on resistant rootstocks, nor are such rootstocks used for new plantings. The transition from organophosphate insecticides to either insect growth regulators (hormone analogues) or neonicotinyl insecticides may also be contributing to higher pressure. In addition, this pest became one of quarantine concern in 2006. Alternatives to organophosphate pesticides have been tested for several years. Of these, petroleum oil shows some promise, as does a particle film used for sunburn protection. A neem-based insecticide provided temporary suppression, as did several neonicotinyl insecticides. A second approach to management, that of controlling the root colonies, was explored for the first time in this region. In potted tree assays, several compounds including imidacloprid, spirotetramat and oxamyl showed good root and systemic activity; in field trials, however, results were more variable. A greenhouse test of 8 clonally propagated rootstocks and 2 seedling rootstocks demonstrated that several of the new Geneva rootstocks to have virtual immunity to a Washington strain of woolly apple aphid, whereas the older Malling-Merton rootstocks had a lesser degree of antixenosis.

Carnegie (2007)  carried out insecticide trials in Southern Rhodesia (now Zimbabwe) against Eriosoma lanigerum using methyl-demeton (an organothiophosphate), dimethoate (a widely used organophosphate), diazinon and malathion. As foliar sprays, all insecticides gave good control of infestations above ground, but methyl-demeton and diazinon gave the best control, and treatments were followed by slower rates of repopulation. Injecting the lower part of the trunks of trees 25 to 30 years old with ½ fluid ounce of a concentrate of a systemic insecticide, 50% methyl-demeton or 40% dimethoate, at a single point gave excellent control where that part of the sap stream supplying the aphid colonies was intercepted. By injecting with a spiral of small holes around the trunk using ½ fluid ounce of 50% methyl-demeton, control of all aphids on the tree could generally be achieved. Good control of subterranean aphid colonies on 15-year-old trees was achieved by the application to the soil of 4 gallons per tree of a fluid containing 100 ml of a concentrate containing 75% of V-C 13 (Dichlofenthion, a phosphorothioate organophosphate) diluted with water. Biological control of Eriosoma lanigerum in Southern Rhodesia by the parasitoid Aphelinus mali, which was introduced in 1961, shows great promise.

Ateyaat et al. (2012)  used a cut-shoot bioassay test to study the efficacy of three flavonoids (which inhibit detoxification organophospate by insects) as aphicides against Eriosoma lanigerum. They were used at three concentrations. Results showed that the three tested flavonoids were active as aphicides against the target species and that mortality to nymphs was higher than that obtained against apterous adults. Increasing the concentration of the flavonoids resulted in a remarkable increase in nymphs mortality. However, rutin hydrate is more toxic to woolly apple aphid than quercetin dehydrate and naringin. The three flavonoids had slight effect on Aphelinus mali compared with the effect caused by imodacloprid insecticide. Quercetin dehydrate, rutin hydrate and naringine can be used as botanical insecticides and incorporated into integrated management programs of the aphid.

Biological & Integrated Control
- USA

Clausen (1956)  describes the biological control of the woolly apple aphid in the United States. The woolly apple aphid is thought to be native to north-east North America, where it used to be fairly well controlled by a chalcid parasitoid Aphelinus mali. When apple production also moved in the north-west USA, the parasite was apparently 'left behind' and heavy infestations of Eriosoma lanigerum developed on the trees. The situation was complicated by a fungus disease, perennial apple canker, caused by the fungal pathogen Nectria ditissima, which caused serious injury to the trees. The wounds in the bark caused by large colonies of the aphids provided optimum conditions for the development of the disease and resulted in large lesions at such points. Aphelinus mali was introduced into the northwest of USA in 1930-31. It spread rapidly and aphid infestations soon subsided to a non-injurious level. Perennial apple canker also virtually disappeared. Control was disrupted in the late 1940s when widespread use of DDT (a persistant organochlorine insecticide) for codling moth control virtually eliminated the parasite from orchards. The picture below shows a codling moth larva in an apple.

Photo by Peggy Grebb. USDA. Public domain.

This led once more to heavy aphid infestations and outbreaks of apple canker. Recent approaches have focused on integrated pest management with use of resistant apple varieties, and more specific insecticides that do not kill the natural enemies.

Brown et al. (1992)  investigated the effects of an entomopathogenic nematode, Steinernema carpocapsae, and an experimental systemic aphicide, on underground populations of Eriosoma lanigerum. Laboratory experiments showed that the presence of the nematode in a colony of Eriosoma lanigerum increased the mortality rate. Nematodes were found inside the body cavity of several aphids with entry possibly being through the anus via a droplet of honeydew. Field trials were carried out in unsprayed apple orchards in West Virginia to test the efficacy of broadcast spray and topdressing applications of nematodes at a rate of 376-600 nematodes/m2. The broadcast spray trees had fewer aphid colonies on roots than the untreated controls, but the topdressing treatment had no effect. Two rates of foliar and soil application of the experimental systemic aphicide were tested, with all treatments significantly reducing arboreal Eriosoma lanigerum populations. Underground populations were also significantly reduced 1 month after treatment, but no difference was found 4 months after treatment. Both control methods were considered promising as potential management options for underground Eriosoma lanigerum populations.

- Chile

Parasitoid populations in agroecosystems can be maintained through the provision of habitat refuges with host resources. However, specialized herbivores that feed on different host plants have been shown to form host-specialized races. Parasitoids may subsequently specialize on these herbivore host races and therefore prefer parasitizing insects from the refuge, avoiding foraging on the crop. Evidence is therefore required that parasitoids are able to move between the refuge and the crop and that the refuge is a source of parasitoids, without being an important source of herbivore pests. Lavandero et al. (2011)  sampled a North-South transect trough the Chilean Central Valley, including apple orchards and surrounding Pyracantha coccinea hedges that were host of the apple pest Eriosoma lanigerum. At each orchard, aphid colonies were collected and taken back to the laboratory to sample the emerging Aphelinus mali. Aphid and parasitoid individuals were genotyped. By studying genetic variation, natural geographic barriers of the aphid pest became evident and some evidence for incipient host-plant specialization was found. However, this had no effect on the population-genetic features of its most important parasitoid. In conclusion, the lack of genetic differentiation among the parasitoids suggests the existence of a single large and panmictic (=random mating) population, which could parasitize aphids on apple orchards and on Pyracantha hedges. The picture below shows a green apple aphid (Aphis pomi ) colony on a Pyracantha hedge in East Sussex.

The latter could thus comprise a suitable and putative refuge for parasitoids, which could be used to increase the effectiveness of biological control. Moreover, the strong geographical differentiation of the aphid suggests local reinfestations occur mainly from other apple orchards with only low reinfestation from Pyracantha hedges. It was proposed that the putative refuge could act as a source of parasitoids without being a major source of aphids.

Ortiz-Martinez et al. (2013)  noted that the presence of a natural enemy in a habitat refuge is no guarantee of emigration by these into crop fields, when pest population outbreaks occur. Parasitoids from a refuge may not prefer foraging on the pest crop, exhibiting host fidelity, and therefore not constituting a source of natural enemies for improving biological control. An effective refuge must not only be a suitable sink for natural enemies, providing an acceptable host when these are not present in the crop, but it must also be a suitable source of parasitoids that readily accept the aphid-host on the crop. Therefore, crop-originated parasitoids would have to accept pests from the refuge as hosts to lay eggs in, and refuge-originated parasitoids would have to accept and lay eggs in pests from the crop. Hence the host fidelity of populations of Eriosoma lanigerum originating from two host plants, firethorn (Pyracantha) and apple, was studied through reciprocal transfer experiments. Thereafter, the host fidelity of parasitoids from populations in the two host plants (firethorn and apple) was assessed. Reciprocal transfer experiments of parasitoids did not show an association between apple-originated parasitoids and their preference for any of the aphid hosts. Conversely, parasitoids from firethorn exhibited a higher number of attacks and in less time when aphids from apple were offered, suggesting a preference for apple-originated aphids. If future field work confirms these findings, firethorn could become an important management tool for enhancing biological control of woolly apple aphid in apple orchards, without being a substantial source of aphids.

- Netherlands

In the Netherlands Mueller et al. (1988)  compared predation by the common earwig, Forficula auricularia (see picture below) and other predators in high, intermediate and low earwig density plots of mature apple trees at an experimental orchard.

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 (a nonsetting adhesive) bands around the trunks. In the low earwig density plots, woolly apple aphids infested 30 to 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), earwig developmental phenology and weather probably influenced the outcome of the predation experiments. Nevertheless Mueller. et al. concluded that earwigs played an important role in suppressing woolly apple aphid populations and are a potentially important, naturally occurring biological control agent for this pest.

Mueller et al. (1992)  showed that the host specific endoparasitoid, Aphelinus mali, will parasitize all stages of woolly apple aphid but apparently prefers third stage nymphs and older hosts. Female parasitoids are generally larger than males, emerge from larger mummies and take about half a day longer to complete development. The sex ratio is strongly male-biased when only small hosts are available for parasitization, and strongly female biased when only large hosts are available. Pre-adult mortality decreases with increasing mummy size suggesting higher mortality for males than females which may explain, in part, the slightly female biased sex ratio in the field. Rates of parasitism are inversely proportional to host colony size because woolly aphids in the centers of large colonies are relatively more protected from parasitoid attack than aphids on colony margins due to the dense crowding of aphids and the white, waxy secretion that covers colonies. In very small woolly aphid colonies few, if any, individuals are protected from Aphelinus mali. Rates of parasitism are greater in long, narrow colonies than in round colonies of the same size because a higher proportion of woolly aphids are located on the colony margins where parasitoids concentrate their attacks. The authors discussed the likelihood of successful biological control in relation to the observed patterns of parasitism.

Asante et al. (1995)  reports that the functional response data obtained in the laboratory for the major predators of woolly apple aphid, namely the earwig Forficula auricularia and the coccinellids Parapriasus australasiae and Harmonia conformis all fitted well to the type II model of the Holling disc equation. These predators consumed larger numbers of early than later instars of Eriosoma lanigerum within the same time period. Adult Harmonia conformis had a lower instantaneous search rate and handling time and could also consume larger numbers of Eriosoma lanigerum than could mature larvae. Overall the earwig was the most efficient predator of Eriosoma lanigerum.

Helsen et al. (2007)  noted apple growers encounter increasing problems controlling Eriosoma lanigerum. Various authors have shown that the common earwig Forficula auricularia plays a role in controlling aphid pests. It was assumed that earwig numbers in orchards had decreased in recent years. Therefore an inventory was made to assess the number of earwigs in apple orchards and to identify factors that determine their presence. The average number of earwigs in cardboard traps varied between 0 and 34 per trap, but in half of the orchards, average trap catches were less than 1 earwig per trap. There was a strong negative correlation  between the numbers of earwigs and woolly apple aphid infestation, which, the authors felt, shows that earwigs play an essential role in controlling woolly apple aphid in commercial orchards. Several factors seem to affect the presence of earwigs in the orchards, the most important one being the drainage of the soil. Organic orchards had slightly more earwigs than integrated pest management orchards.

- Iraq

El Haidari et al. (1978)  studied Aphelinus mali and its host Eriosoma lanigerum in Iraq in 2 unsprayed apple orchards with different cultural practices over two years. The aphid population increased in late March, peaked in April and the first week of May, and then declined sharply and stayed low until September. A second peak occurred in November and December, followed by a decline during January and February. Adult parasites began their activity during the first week of April. Parasitization was high on both branches and trunks in the orchard which had no regular pruning but was planted with clover. Parasitization was higher on branches than on trunks in the orchard with regular pruning but without clover. This study showed that parasite activity was very much synchronized with its host and could be utilized successfully to control the aphid in Iraq.

- Israel

Cohen et al. (1996)  investigated 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 aphid parasitoid Aphelinus mali under laboratory conditions. Chlorpyrifos (an organophosphorus insecticide) was found to be highly toxic to the adult wasps. Vamidothion was more toxic to the parasitoid than azinphos-methyl. On the other hand, both chlorpyrifos and azinphos-methyl were found to be harmless to the immature stages of the parasitoid. 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.

- South Africa

Heunis & Pringle (2006)  studied the seasonal cycles of Eriosoma lanigerum and its natural enemy, Aphelinus mali in the Western Cape Province region of South Africa. Crawlers of Eriosoma lanigerum migrated from the roots into the apple trees during spring to initiate above-ground colonies. Population numbers peaked at the end of summer. Aphelinus mali became active from February until June. Aphid numbers declined with the onset of winter but a few colonies remained on apple trees during winter.

- China

Yong et al. (2008)  looked at the population dynamics of Harmonia axyridis (see pictures below on apple in Britain) and its role in controlling Eriosoma lanigerum in China.

 

Harmonia axyridis is one of the important predatory insects for controlling woolly apple aphid in apple orchards in China. First occurrence was observed between February and March and the population peak between March and April. In orchards with cover crops, the adult occurrence of Harmonia axyridis was earlier by one or a half month and lasted longer than in purely apple-cultivated orchards.

- Australia

Nicholas et al. (1988)  monitored Eriosoma lanigerum populations over three growing seasons to assess its abundance and management under apple integrated pest management programs in New South Wales, Australia. Woolly aphid infestations were found to be extremely low in programs utilising mating disruption and fenoxycarb (a carbamate insect growth regulator) for codling moth control. This was the direct result of increased numbers of natural enemies. No insecticides were applied for woolly aphid control. Under the integrated pest management strategies tested the principal control agent was identified as earwigs (Forficula auricularia). Earwigs in combination with Aphelinus mali reduced woolly aphid infestations below the action threshold set by commercial growers. However, Aphelinus mali together with other flying natural enemies, e.g., ladybirds, lacewings and hoverflies, did not provide commercially acceptable control of woolly aphid in the absence of earwigs. Under the conventional spray program, using the broad-spectrum insecticide azinphos-methyl (a broad spectrum organophosphate) for codling moth control, the level of woolly aphid infestation increased with each successive season and biological control was not established. When azinphos-methyl was withdrawn, natural enemies migrated in and provided control of woolly aphid within one season. This was the first study to show that the biological control of woolly aphid can be achieved in a commercially viable integrated pest management program.

 

Images copyright H. Riedl & E. Beers,  Tree Fruit Research & Extension Center, Washington State University.

The images above show an Aphelinus mali adult, and Aphelinus mali adults attacking woolly apple aphids.

- New Zealand

Shaw & Walker (1996)  describe the early development of integrated fruit production in New Zealand incorporating biological control for woolly apple aphid. The parasitoid Aphelinus mali was introduced into New Zealand in 1921, and by 1925 had spread throughout New Zealand, almost eliminating the aphid. However the routine use of broad spectrum organophosphorus sprays for control of leafroller and codling moth subsequently disrupted this control. In 1994 a much more specific insect growth regulator insecticide - tebufenozide - was introduced. The aphid population increased dramatically during the first season in one cultivar from mid February and reached 90% shoot infestation by late summer. Parasitism of the aphid by Aphelinus mali was first recorded in late March 1995 and peaked at 13% by the end of April 1995 when monitoring ceased. In the second season the parasitoid was present from early summer and > 80% parasitism was recorded by late April 1996. Aphid control was achieved without the need for specific aphicide sprays.

Wearing et al. (2010)  monitored woolly apple aphid and its natural enemies from 1994 to 2000 on apples at Central Otago, New Zealand during the transition from conventional fruit production using broad spectrum insecticides, to integrated fruit production using selective insecticides. Populations were compared in orchard blocks under three management regimes: conventional fruit production; transition to integrated fruit production; and a biological fruit production programme. Woolly apple aphid remained at very low levels in the conventional fruit production programme, because of insecticides, and in the biological fruit production programme, primarily because of natural enemies. Transition to integrated control was accompanied by a surge in woolly apple aphid and a slow colonization by natural enemies which took at least four years to reduce the aphid population to acceptable levels. The principal natural enemy that achieved this was the parasitoid Aphelinus mali, assisted by predators whose contribution remained obscure, including the brown lacewing (Micromus tasmaniae) and the European earwig (Forficula auricularia). A single annual application of lufenuron (a benzoylurea pesticide which inhibits chitin production) within the integrated fruit production programme was not detrimental to any of these natural enemies, although further research is needed to confirm its lack of impact on the lacewing. Lufenuron reduced arboreal predator diversity, and this was in part due to decline in the populations of Orius vicinus (Pirate bug, a generalist predator) and Stethorus bifidus (a coccinellid predator of Tetranychus lintearius, a mite used to control Ulex europaeus, common gorse). Pirimicarb was an effective selective aphicide for integration with the action of the natural enemies of woolly apple aphid, but a substitute is required, as its use is no longer permitted on export crops.

Acknowledgements

We especially thank Elizabeth Beers, Tree Fruit Research & Extension Center,  Washington State University, for permission to reproduce the photographs of Aphelinus mali, and Plumpton College at Stanmer Park  for their kind assistance and permission to sample.

We have made provisional identifications from high resolution photos of living specimens, along with host plant identity. In the great majority of cases, identifications have been confirmed by microscopic examination of preserved specimens. We have used the keys and species accounts of Blackman & Eastop (1994)  and Blackman & Eastop (2006)  supplemented with Blackman (1974) , Stroyan (1977) , Stroyan (1984) , Blackman & Eastop (1984) , Heie (1980-1995) , Dixon & Thieme (2007)  and Blackman (2010) . We fully acknowledge these authors as the source for the (summarized) taxonomic information we have presented. Any errors in identification or information are ours alone, and we would be very grateful for any corrections. For assistance on the terms used for aphid morphology we suggest the figure  provided by Blackman & Eastop (2006).

Useful weblinks 

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