Invasive Species Compendium

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Datasheet

Eriosoma lanigerum
(woolly aphid)

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Datasheet

Eriosoma lanigerum (woolly aphid)

Summary

  • Last modified
  • 03 January 2018
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Preferred Scientific Name
  • Eriosoma lanigerum
  • Preferred Common Name
  • woolly aphid
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Metazoa
  •     Phylum: Arthropoda
  •       Subphylum: Uniramia
  •         Class: Insecta

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Pictures

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PictureTitleCaptionCopyright
Wooly aphid life stages (right) and infestation on apple, causing galls on stem (left).
TitleColour illustration
CaptionWooly aphid life stages (right) and infestation on apple, causing galls on stem (left).
CopyrightAgrEvo
Wooly aphid life stages (right) and infestation on apple, causing galls on stem (left).
Colour illustrationWooly aphid life stages (right) and infestation on apple, causing galls on stem (left).AgrEvo

Identity

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Preferred Scientific Name

  • Eriosoma lanigerum (Hausmann, 1802)

Preferred Common Name

  • woolly aphid

Other Scientific Names

  • Aphis lanigera (Hausmann, 1802)
  • Aphis lanigerum Hausmann, 1802
  • Coccus mali Bingley, 1803
  • Eriosoma lanata (Salisbury, 1816)
  • Eriosoma mali Leach, 1818
  • Mimaphidus lanata (Salisbury, 1816)
  • Mimaphidus lanigerum (Hausmann, 1802)
  • Mimaphidus mali ((Leach, 1818)
  • Myzoxyles lanigerum (Hausmann, 1802)
  • Myzoxyles mali (Leach, 1918)
  • Myzoxylos lanata (Salisbury, 1816)
  • Myzoxylus laniger
  • Myzoxylus lanigerus (Hausmann, 1802)
  • Myzoxylus mali Blot, 1831
  • Schizoneura lanigera Gillette, 1908

International Common Names

  • English: American blight; aphid, elm rosette; aphid, woolly apple; apple root aphid; blight, American; elm rosette aphid; woolly apple aphid
  • Spanish: afido de sangre; pulgón lanigero; pulgón lanigero del manzano
  • French: puceron lanigère; puceron lanigère du pommier
  • Portuguese: pulgao lanigero (Brazil); pulgao lanigero da macieira (Brazil)

Local Common Names

  • Brazil: pulgao lanigero; pulgao lanigero da macieira
  • Denmark: blodlus
  • Finland: verikirva
  • Germany: Blutlaus, Wollige Apfel-; Wollige Apfelblutlaus
  • Israel: knimat hadam
  • Italy: Afide lanigero del melo; Pidocchio rosso del melo; Pidocchio sanguigno
  • Japan: Ringo-watamusi
  • Netherlands: Appelbloedluis; Bloedluis, wollige
  • Norway: blodlus
  • Sweden: blodlus
  • Turkey: elma kabuklu biti

EPPO code

  • ERISLA (Eriosoma lanigerum)

Taxonomic Tree

Top of page
  • Domain: Eukaryota
  •     Kingdom: Metazoa
  •         Phylum: Arthropoda
  •             Subphylum: Uniramia
  •                 Class: Insecta
  •                     Order: Hemiptera
  •                         Suborder: Sternorrhyncha
  •                             Unknown: Aphidoidea
  •                                 Family: Aphididae
  •                                     Genus: Eriosoma
  •                                         Species: Eriosoma lanigerum

Notes on Taxonomy and Nomenclature

Top of page E. lanigerum (Hausmann) is one of 20 species in the genus Eriosoma, in the tribe Eriosomatini of the subfamily Pemphiginae (Blackman and Eastop, 1994). The diploid chromosome number is 2n = 12, although male sexuales are apparently 2n = 11 (Gautam and Verma, 1983a).

Description

Top of page Relatively small to medium-sized aphids, characterized by a reddish-brown body, a blood-red stain when crushed and a fluffy, flocculent wax covering (Palmer, 1952; Blackman and Eastop, 1984). Specialized dermal glands produce the characteristic fluffy or powdery wax, which gives E. lanigerum its characteristic 'woolly' appearance.

Hibernating apterous virginoparae occurring on roots of apple over winter are very dark dusky green. They appear nearly black, especially on the head and thorax, although sometimes a dingy yellowish-brown, and lack the white waxy covering of other virginoparae. Appendages and the distal end of the rostrum are dusky brown (Palmer, 1952).

Apterous summer virginoparae are 1.2-2.6 mm in length, purple, red or brown and covered with a thick white flocculent wax. Antennae are dusky brown; tibiae yellowish to slightly dusky brown. They have a relatively small cornical pore size (0.06-0.07 mm). Apterae body length 1.2-2.6 mm (Palmer, 1952; Blackman and Eastop, 1984).

Alate virginoparae are 1.8-2.3 mm long and have a reddish-brown abdomen with a covering of woolly white wax posteriorly. There are two or three sensoria on antennal segment VI. They have a relatively small cornical pore size (around 0.05 mm) (Blackman and Eastop, 1984).

Oviparae are apterous, and rusty yellow to rusty brown. Males are apterous, and yellowish to dusky brown to dark green (Palmer, 1952).

Distribution

Top of page E. lanigerum probably originated in eastern North America, but it now has a worldwide distribution (CIE, 1975), having been distributed mainly via apple rootstocks.

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Continent/Country/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Asia

AfghanistanPresentMohammad, 1988
ArmeniaPresentCIE, 1975
AzerbaijanPresentCIE, 1975
BangladeshPresentCIE, 1975
BhutanPresentCIE, 1975
ChinaPresentPresent based on regional distribution.
-Hong KongPresentAPPPC, 1987
-LiaoningPresentCIE, 1975
-ShandongPresentCIE, 1975
-XinjiangPresentYu et al., 2008
-YunnanPresentRongping et al., 1991
Georgia (Republic of)PresentCIE, 1975
IndiaPresentPresent based on regional distribution.
-AssamPresentCIE, 1975
-Himachal PradeshPresentCIE, 1975
-Indian PunjabPresentCIE, 1975
-Jammu and KashmirPresentCIE, 1975
-KarnatakaPresentCIE, 1975
-MeghalayaPresentSachan and Gangwar, 1980
-SikkimPresentCIE, 1975
-Tamil NaduPresentCIE, 1975
-Uttar PradeshPresentCIE, 1975
-West BengalPresentGhosh and Raychaudhuri, 1981
IranPresentCIE, 1975
IraqPresentCIE, 1975
IsraelPresentCIE, 1975
JapanWidespreadCIE, 1975
-HokkaidoPresentCIE, 1975
-HonshuPresentCIE, 1975
-KyushuPresentCIE, 1975
-Ryukyu ArchipelagoPresentCIE, 1975
-ShikokuPresentCIE, 1975
JordanPresentCIE, 1975
Korea, DPRPresentCIE, 1975
Korea, Republic ofPresentLee et al., 1997
KyrgyzstanPresentCIE, 1975
LebanonPresentCIE, 1975
MyanmarPresentCIE, 1975
NepalPresentCIE, 1975
PakistanPresentCIE, 1975
Saudi ArabiaPresentCIE, 1975
Sri LankaPresentCIE, 1975
SyriaPresentCIE, 1975
TajikistanPresentBoldyreva, 1970
TurkeyPresentCIE, 1975
YemenPresentCIE, 1975

Africa

AlgeriaPresentCIE, 1975
AngolaPresentCIE, 1975
EgyptPresentCIE, 1975
EritreaPresentCIE, 1975
EthiopiaPresentCIE, 1975
KenyaPresentCIE, 1975
LibyaPresentCIE, 1975
MadagascarPresentCIE, 1975
MoroccoPresentCIE, 1975
RéunionPresentCIE, 1975
South AfricaPresentCIE, 1975
TunisiaPresentCIE, 1975
ZimbabwePresentCIE, 1975

North America

CanadaPresentPresent based on regional distribution.
-AlbertaPresentCIE, 1975
-British ColumbiaPresentCIE, 1975
-ManitobaPresentCIE, 1975
-Nova ScotiaPresentCIE, 1975
-OntarioPresentCIE, 1975
-QuebecPresentCIE, 1975
MexicoPresentCIE, 1975
USAPresentPresent based on regional distribution.
-AlabamaPresentCIE, 1975
-ArizonaPresentCIE, 1975
-ArkansasPresentCIE, 1975
-CaliforniaPresentCIE, 1975
-ConnecticutPresentCIE, 1975
-DelawarePresentCIE, 1975
-FloridaPresentCIE, 1975
-GeorgiaPresentCIE, 1975
-HawaiiPresentCIE, 1975
-IdahoPresentCIE, 1975
-IllinoisPresentCIE, 1975
-IndianaPresentCIE, 1975
-IowaPresentCIE, 1975
-KansasPresentCIE, 1975
-KentuckyPresentCIE, 1975
-LouisianaPresentCIE, 1975
-MainePresentCIE, 1975
-MarylandPresentCIE, 1975
-MassachusettsPresentCIE, 1975
-MichiganPresentCIE, 1975
-MinnesotaPresentCIE, 1975
-MississippiPresentCIE, 1975
-MissouriPresentCIE, 1975
-MontanaPresentCIE, 1975
-NebraskaPresentCIE, 1975
-NevadaPresentCIE, 1975
-New JerseyPresentCIE, 1975
-New MexicoPresentCIE, 1975
-North CarolinaPresentCIE, 1975
-North DakotaPresentCIE, 1975
-OhioPresentCIE, 1975
-OklahomaPresentCIE, 1975
-OregonPresentCIE, 1975
-Rhode IslandPresentCIE, 1975
-South CarolinaPresentCIE, 1975
-TennesseePresentCIE, 1975
-TexasPresentCIE, 1975
-UtahPresentCIE, 1975
-VermontPresentCIE, 1975
-WashingtonPresentCIE, 1975; Gontijo et al., 2012
-West VirginiaPresentCIE, 1975
-WisconsinPresentCIE, 1975
-WyomingPresentCIE, 1975

Central America and Caribbean

Costa RicaPresentCIE, 1975
Dominican RepublicPresentCIE, 1975
HaitiPresentCIE, 1975

South America

ArgentinaPresentCIE, 1975
BoliviaPresentCIE, 1975
BrazilPresentPresent based on regional distribution.
-Minas GeraisPresentCIE, 1975
-ParanaPresentCIE, 1975
-Rio de JaneiroPresentCIE, 1975
-Rio Grande do SulPresentCIE, 1975
-Santa CatarinaPresentCIE, 1975
-Sao PauloPresentCIE, 1975
ChilePresentCIE, 1975
ColombiaPresentCIE, 1975
EcuadorPresentCIE, 1975
PeruPresentCIE, 1975
UruguayPresentCIE, 1975
VenezuelaPresentCIE, 1975

Europe

AlbaniaPresentCIE, 1975
AustriaWidespread****CIE, 1975
BelgiumPresentCIE, 1975
BulgariaWidespread****CIE, 1975
CyprusRestricted distributionCIE, 1975
Czechoslovakia (former)Restricted distribution****CIE, 1975
DenmarkPresent, few occurrencesCIE, 1975
FinlandPresentCIE, 1975
FranceRestricted distributionCIE, 1975
GermanyWidespread****CIE, 1975
GreecePresentCIE, 1975
HungaryPresentCIE, 1975
IrelandWidespreadCIE, 1975
ItalyWidespreadCIE, 1975
LatviaPresentRupais, 1989
MaltaPresentCIE, 1975
MoldovaPresentVereshchagin and, 1977
NetherlandsPresentCIE, 1975
PolandPresentCIE, 1975
PortugalWidespreadCIE, 1975
RomaniaPresentCIE, 1975
Russian FederationPresentPresent based on regional distribution.
-Central RussiaPresentCIE, 1975
-Northern RussiaPresentCIE, 1975
-Russian Far EastPresentCIE, 1975
-Southern RussiaPresentCIE, 1975
SlovakiaPresentCIE, 1975
SloveniaPresentModic and ?kerlavaj, 2008
SpainPresentCIE, 1975
SwedenRestricted distribution****CIE, 1975
SwitzerlandWidespreadCIE, 1975
UKWidespread****CIE, 1975
-Channel IslandsPresentCIE, 1975
UkrainePresentCIE, 1975
Yugoslavia (former)PresentCIE, 1975
Yugoslavia (Serbia and Montenegro)PresentCIE, 1975

Oceania

AustraliaPresentPresent based on regional distribution.
-New South WalesPresentCIE, 1975
-QueenslandPresentCIE, 1975
-South AustraliaPresentCIE, 1975
-TasmaniaPresentCIE, 1975
-VictoriaPresentCIE, 1975
-Western AustraliaPresentCIE, 1975
New ZealandPresentCIE, 1975

Risk of Introduction

Top of page E. lanigerum is considered to be a phytosanitary risk in many regions, due to its root-dwelling habitat and its possible presence on imported apple rootstocks. It is listed in the EPPO A2 quarantine list (EPPO, 1979). For example, in Norway, where the aphid is not established, E. lanigerum is considered to be of significant quarantine importance (Edland, 1990).

Hosts/Species Affected

Top of page E. lanigerum is found on apple (Malus spp.), on which it can be a severe pest, and occasionally on certain other woody host plants in the family Rosaceae. It is restricted to apple in some areas where it has been introduced, for example, parts of Australia (Asante, 1994). It is elsewhere found on species of Crataegus, Sorbus and Cotoneaster, and also rarely on pear and species of Cydonia (Blackman and Eastop, 1984).

Host Plants and Other Plants Affected

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Plant nameFamilyContext
CotoneasterRosaceaeWild host
Crataegus spp.RosaceaeWild host
Cydonia oblonga (quince)RosaceaeWild host
Malus (ornamental species apple)RosaceaeMain
Malus domestica (apple)RosaceaeMain
Malus sylvestris (crab-apple tree)RosaceaeWild host
Prunus domestica (plum)RosaceaeWild host
Pyracantha (Firethorn)RosaceaeWild host
Pyrus (pears)RosaceaeOther
Pyrus communis (European pear)RosaceaeOther
Sorbus americana (American mountainash)RosaceaeWild host
Sorbus spp.RosaceaeWild host

Growth Stages

Top of page Flowering stage, Fruiting stage, Vegetative growing stage

Symptoms

Top of page E. lanigerum occurs on the both the aerial and subterranean woody tissue of apple. It does not feed on the leaves. Aphid colonies on the trunk, branches or twigs can cause deformations, blisters, splitting and cancer-like swellings of the bark (Blackman and Eastop, 1984). Compounds in aphid saliva that are toxic to trees are partly responsible for the severity of this damage. Galling of aerial plant parts can reach the size of a walnut and interfere with sap circulation.

Root infestations also cause galling. Damage to roots encourages secondary infection, particularly the formation of root canker, a disease caused by basidiomycete fungi (Molinari, 1986). In growth chamber experiments, stem splitting and root galling formed as a result of E. lanigerum feeding, 4 and 8 weeks after initial infection, respectively. Feeding resulted in greater shoot and root dry weights and a disruption in nutrient balance, with reduced foliar nitrogen and phosphorous compared to control trees (Weber and Brown, 1988).

List of Symptoms/Signs

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SignLife StagesType
Fruit / honeydew or sooty mould
Roots / galls along length
Roots / galls at junction with stem
Roots / swollen roots
Stems / canker on woody stem
Stems / external feeding
Stems / galls
Stems / honeydew or sooty mould

Biology and Ecology

Top of page E. lanigerum is anholocyclic on apple worldwide, reproducing year-round without host-alternation. Colonies persist on hosts during the winter by living on the plant roots or within bark crevices. Although anholocyclic, an abortive sexual phase occurs in many parts of the world, with sexuales and eggs being produced on apple, but the eggs of this species are not viable and do not hatch (Blackman and Eastop, 1984).

Apterous and alate virginoparae, and sexuales (males and oviparae), appear at particular times during the life cycle on apple. In the USA, overwintering populations start to breed during March to April. Each female can produce over 100 nymphs. Up to 10-12 generations a year can occur in the USA and Europe (for example, France and Italy), from spring to autumn (Molinari, 1986), although in Michigan, USA, and other more northerly parts of North America and Europe, three to four generations may be more usual.

In Australia, Asante (1994) found that alates appearing in early November produced only virginoparae, alates appearing from late November to late January produced a mixture of virginoparae and sexuales, whereas those appearing from February to April produced exclusively sexuales. The sexuales were apterous, had degenerate mouthparts and produced non-viable eggs. The perpetuation of the species appeared to be entirely due to parthenogenesis, with overwintering accomplished in the form of cold-resistant apterous virginoparae.

In India, Gautam and Verma (1983b) observed apterous virginoparae undergoing four moults resulting in five instars. The pre-reproductive and reproductive stages were longer in winter than in summer, whereas fecundity was greater in summer than in winter.

First-instar nymphs are highly mobile and will disperse from crowded populations to establish new colonies (Hoyt and Madsen, 1960) and move between the roots and shoots throughout the year. However, a distinct seasonal migration occurs, from aerial parts to the roots and back, with a pronounced movement of first-instar nymphs at these times (Hoyt and Madsen, 1960). Annual upward and downward movement peaks were recorded in India, for example, during mid-June and October to November, in response to changes in ambient and soil temperatures (Sushma Bhardwaj and Chander, 1995). Differential mortality of aphids on the exposed shoots and sheltered roots also contributes to the seasonal shift in habitat on host plants.

On aerial plant parts, the preference for sheltered sites, including wounds and axil buds, is possibly an adaptation to avoid natural enemies (Brown and Schmitt, 1994).

Natural enemies

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Natural enemyTypeLife stagesSpecificityReferencesBiological control inBiological control on
Anthocoris nemoralis Predator Adults/Nymphs Turkey apples
Aphelinus mali Predator/parasite Nymphs Argentina; Australia; Belgium; Brazil; Chile; Colombia; Costa Rica; Cyprus; Denmark; Ecuador; Egypt; France; Germany; Himachal Pradesh; India; Iraq; Israel; Italy; Japan; Kenya; Malta; Mexico; Netherlands; New Zealand; Pakistan; Peru; Poland; Portugal; Russian Far East; Saudi Arabia; South Africa; Spain; Sweden; Switzerland; Tasmania; UK; Uruguay; USSR; Venezuela; Western Australia; Zimbabwe apples
Areopraon lepelleyi Parasite Adults/Nymphs
Balaustium putmani Predator Adults/Nymphs
Brinckochrysa scelestes Predator Adults/Nymphs Himachal Pradesh
Cheilomenes lunata Predator Adults/Nymphs Ascension apples
Chrysopa pallens Predator Adults/Nymphs Turkey
Chrysoperla carnea Predator Adults/Nymphs Turkey apples
Clitostethus arcuatus Predator Adults/Nymphs
Coccinella septempunctata Predator Adults/Nymphs
Episyrphus balteatus Predator Adults/Nymphs India apples
Eupeodes confrater Predator Adults/Nymphs India; India; Himachal Pradesh apples
Eupeodes corollae Predator Adults/Nymphs India apples
Exochomus melanocephalus Predator Adults/Nymphs Ascension; Australia apples
Exochomus quadripustulatus Predator Adults/Nymphs
Forficula auricularia Predator Adults/Nymphs
Harmonia dimidiata Predator Adults/Nymphs
Harmonia eucharis Predator
Hippodamia convergens Predator Adults/Nymphs South Africa apples
Lioadalia flavomaculata Predator Adults/Nymphs Ascension apples
Oenopia cinctella Predator Adults/Nymphs Ascension apples
Paragus tibialis Predator Adults/Nymphs India apples

Notes on Natural Enemies

Top of page Data for natural enemies of E. lanigerum worldwide were summarized by Asante (1997), who reported that aphid colonies were attacked by five species of hymenopterous endoparasitoids and two species of Acarina (ectoparasites). In addition, 73 species of predatory insects belonging to five orders and seven families (Coccinellidae, Chrysopidae, Hemerobiidae, Forficulidae, Lygaeidae, Syrphidae and Cecidomyiidae) have been reported to feed on E. lanigerum. Verticillium lecanii is the only fungal pathogen known to infect E. lanigerum (Asante, 1997).

E. lanigerum is the preferred host of Aphelinus mali, the only important host-specific natural enemy. This parasitoid, which originates from the USA, is now widespread and has been introduced into many apple-growing regions as a biological control agent. The hyperparasitoids Asaphes vulgaris, A. suspensus, Pachyneuron solitarium and Aphidencyrtus aphidivorus are often associated with A. mali (von Kogler, 1989).

Predation of E. lanigerum by the earwig Forficula auricularia was studied by Mueller et al. (1988). Exclusion and feeding experiments performed in Poland showed that Exochomus quadripustulatus played an important role in controlling E. lanigerum during early spring, whereas during the summer F. auricularia and sometimes Coccinella septempunctata were important (Mols, 1996).

Impact

Top of page E. lanigerum is an important economic pest of apple, causing severe damage through direct feeding, but not as a vector of apple viruses (Blackman and Eastop, 1984). It infests both the canopy and root system of apple trees, although root damage is usually more severe than stem damage. Root damage is also harder to detect and more difficult to control. It is a common and highly injurious apple pest in the USA, particularly in areas of Maryland and Virginia (Weber and Brown, 1988). Thakur and Dogra (1980) cited E. lanigerum as the most important pest of apple in India. It is also a significant apple pest in Europe, the Middle East, the Far East, South America, Australia and New Zealand.

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. Average yield losses were 2.4 kg (13 apples) per tree, representing a gross loss of $465.18/ha. 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.

Brown et al. (1991) found that root galls caused by E. lanigerum were characterized by a proliferation of anomalous non-functional xylem. Disruption of root xylem, resulting in resistance to water conduction, is one mechanism by which E. lanigerum reduces the growth of apple trees. Heavy infestations may result in the formation of swellings and wounds that permit the entry of the fungi Nectria ditissima and N. galligena, which produce cankers (Molinari, 1986). Heavily infested trees lack vigour, due to disturbances in nutrient balance, but it is usually difficult to separate the various direct and indirect effects of aphid feeding.

Fruit can be directly affected, through the deposition of honeydew from colonies feeding on adjacent branches or twigs. These can cause cosmetic damage and lead to the growth of sooty moulds on the apples. Weber and Brown (1988) reported that aphids can sometimes infest the cores of some cultivars.

Damage is particularly severe in young trees. Roots of nursery trees, for example, can be particularly affected. Mature trees are often little affected, even though levels of infestation are generally greatest in orchards over 25 years old (Molinari, 1986).

Detection and Inspection

Top of page E. lanigerum is found on the stems and roots of apple. Inspect for aphid presence on aerial plant parts by looking for whitish colonies on branches, especially around healing pruning cuts or wounds in the bark, throughout mid- to late-summer. Microhabitat preferences of arboreal colonies during the spring is for wound and other protected feeding sites on the tree branches and trunk, whereas leaf axils were the predominant microhabitat (51% of the colonies observed) from the end of May to August (Brown and Schmitt, 1994).

In Massachusetts, USA, standard inspection involves examining five prunings per tree, on one tree per 3.5 acres, whereas a provisional threshold for treatment is 50% of pruning cuts infected. Aphids generally show a preference for the lower part of the canopy and the trunk. At low infestations, E. lanigerum is confined to the trunk and large branches, but disperses to establish colonies on twigs or new lateral growths during peak populations (Asante et al., 1993).

Similarities to Other Species/Conditions

Top of page In North America, E. lanigerum was once thought to overwinter on elm (Ulmus spp.) and utilize apple as a secondary host plant. However, E. lanigerum is now considered to be a separate species from closely related species that live on elm. Previous records of E. lanigerum on elm are most likely to have been E. herioti, which induces rosette galls on species of Ulmus and migrates from Ulmus americana to the roots of species of Crataegus, apple and Sorbus americana (Blackman and Eastop, 1984, 1994). Records describing E. lanigerum on U. americana may also be misidentifications of E. crataegi or the woolly elm aphid, E. americanum (CIE, 1975).

Prevention and Control

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Biological Control

The chalcidoid parasite Aphelinus mali has been introduced into many countries in attempts to control E. lanigerum. It was originally native to the USA, but has become acclimatized in Europe and has now been introduced into apple-growing regions worldwide. Where aboveground infestations dominate, control of E. lanigerum has been very successful, but where root-feeding populations are important, the results have been less good. A review of the history and results of biological control of this pest is provided by Clausen (1978).

In laboratory studies performed by Mueller et al. (1992), A. mali parasitized all stages of E. lanigerum, but preferred third-instar nymphs, whereas rates of parasitism were inversely proportional to host colony size, with small colonies and long, thin colonies having a greater proportion of individuals parasitized.

A. mali was first introduced into India during the 1930s, and 98% control was soon achieved in the Kullu Valley, Himachal Pradesh (Thakur and Dogra, 1980).

In field studies undertaken in New Zealand, Shaw et al. (1996) reported that parasitism of E. lanigerum by A. mali exceeded 80% by late April, and control was achieved without the need for specific aphicide sprays. High levels of parasitism by A. mali (80%) were also recorded at low population densities of E. lanigerum in Mexico (Tejada and Rumayor, 1986), whereas parasitism rates of over 50% were recorded during the summer in West Virginia, USA (Brown and Schmitt, 1994). E. lanigerum was controlled by A. mali in pesticide-free apple orchards in Israel (Oppenheim et al., 1997).

In the Netherlands, the predatory coccinellid Exochomus quadripustulatus is the most common and most widespread coccinellid in apple orchards, and contributes to aphid control alongside A. mali in the spring (Bogya, 1996). In India, releases of A. mali have been accompanied by releases of the predators Brinckochrysa scelestes and Eupeodes confrater as a biological control for E. lanigerum (Thakur and Dogra, 1980; Thakur et al., 1992). In Europe, the earwig Forficula auricularia could be an important supplementary biological control agent against E. lanigerum (Mueller et al., 1988). Predators are not effective against subterranean aphid populations.

The use of entomopathogenic nematodes to control root-dwelling populations of E. lanigerum was described by Brown et al. (1992).


Host-Plant Resistance

One method of preventing the development of reservoir populations of E. lanigerum underground is to use rootstocks of resistant cultivars. Apple cultivars with some degree of reported resistance include Northern Spry (Cummins et al., 1981) and Golden Delicious (Sachan and Gangwar, 1987). However, most interest has centred on the Malling Merton (MM) series of rootstocks, which are derived from Northern Spry. These rootstocks are not totally resistant to E. lanigerum, but infestation levels are significantly and consistently lower than on other rootstocks, and they have been widely used in pest control programmes.

Thirty cultivars and breeding lines of eight Malus species were tested for resistance to E. lanigerum in a Chinese study (Deng et al., 1993), in which a line of Malus baccata (Jin 67) was selected as stock for future breeding. It exhibited less root damage due to E. lanigerum, was winter hardy and induced dwarfism in apple crosses.

Chemical Control

Recommended chemical treatments against E. lanigerum on the aerial parts of trees usually consist of yellow mineral oil, applied in the winter against hibernating immature forms of the aphid and other apple pests. This is followed by sprays of systemic products such as chlorpyrifos or demeton-methyl during the growing period of the tree, but especially after flowering, when predators are less abundant (Molinari, 1986).

Chlorpyrifos also gives good control, but is highly toxic to Aphelinus mali, the most important parasitoid of E. lanigerum. Pirimicarb gives reasonable aphid control without adversely affecting A. mali, although it lacks persistence and is not efficient in killing colonies hidden in cankers or pruning wounds (Staubli and Chapuis, 1989).

In nurseries, root dips of fenitrothion can provide effective control. Subterranean populations in orchards can be treated with granules of dimethoate. Banding of trunks with granules of these insecticides has also been useful in decreasing infestations, by checking the movement of first-instar nymphs that migrate between aerial and subterranean habitats on apple (Thakur and Dogra, 1980).

IPM

The reduced use of broad-spectrum pesticides, enhanced diversity of arboreal predators and parasitoids, and high populations of key natural enemies, particularly the parasitoid A. mali, are key features of IPM in apple against E. lanigerum. IPM programmes have been described in Australia (Thwaite, 1997), New Zealand (Shaw et al., 1996), Romania (Baicu et al., 1997) and South Africa (Nel and Addison, 1993).

Air-blast sprayer applications of mineral oil, or oil plus buprofezin are applied in apple orchards under IPM programmes in New Zealand. The natural enemy A. mali can then control E. lanigerum populations under these spray regimes (Shaw et al., 1996).

References

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