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Natural Enemies of the Woolly Apple Aphid, Eriosoma Lanigerum

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Natural Enemies of the Woolly Apple Aphid, Eriosoma Lanigerum 166 Plant Protection Quarterly Vol.12(4) 1997 Parasitoids The most important parasitoid of E. lani- Natural enemies of the woolly apple aphid, Eriosoma gerum is the Chalcid wasp, Aphelinus mali lanigerum (Hausmann) (Hemiptera: Aphididae): a (Haldeman) (Hymenoptera: Aphelinidae) (Tillyard 1921, Lundie 1924, Bodenheimer review of the world literature 1947, Evenhuis 1958, DeBach 1964). Very scanty information is available for other S.K. Asante, Department of Zoology, University of New England, Armidale, parasitoids of this aphid. DeSantis (1939) New South Wales 2351, Australia. reported the occurrence of Neoanisotylus Present address: International Institute of Tropical Agriculture, Oyo Road, sp. in E. lanigerum in Argentina. In the United Kingdom, Rosenberg (1934) and PMB 5320, Ibadan, Nigeria. Stary (1976) reported the occurrence of Proan simulans Prov. and Areoproan lepel- leyi Wat., respectively as parasitoids of E. Summary In view of its economic importance, a lanigerum. Childers and Rock (1981) re- Literature information was used to considerable amount of work has been corded Balaustium putmani Smiley (Aca- compile a summary of natural enemies conducted on its biology, ecology, popu- rina) whereas Marchal (1929) reported Al- (parasitoids, predators and a fungal lation dynamics and control by the use lothrombium fuliginosum Herm. as ectopar- disease) reported attacking the woolly of insecticides, resistant apple varieties asites of this aphid in the United States apple aphid, Eriosoma lanigerum and natural enemies in all the countries and France, respectively. Gurney (1926) (Hausmann) under field conditions. in which it occurs (Baker 1915, Staniland observed that Aphelinus niger Girult para- Five species of hymenopterous endo­ 1924, Hatton et al. 1937, Bodenheimer sitize E. lanigerum in New South Wales parasitoids and two species of Acarina 1947, Evenhuis 1958, Brown and Schmitt and Queensland before the introduction (ectoparasites) were reported to attack 1994, Asante 1995a). Despite the exten- of A. mali. E. lanigerum. Altogether, 73 species sive work on its natural enemies world of predatory insects belonging to five wide for over a century, there has been Origin and introduction of A. mali into orders and seven families (i.e. Coccinel­ no attempt to collate the literature. Hence, other apple-growing countries lidae, Chrysopidae, Hemero biidae, For­ the information on the natural enemies of The most significant advance in the biolog- ficulidae, Lygaeidae, Syrphidae, and Ce­ E. lanigerum remains scattered and ob- ical control of E. lanigerum was made in the cidomyiidae) have been reported to feed scured which precludes the selection and early 1920s when A. mali, an endoparasi- on this aphid species. Verticillum leca- use of suitable biological control agents toid, was introduced from its native home, nii (Zimm.) ViËgas was the only fungal in regions where Aphelinus mali (Halde- North America, into many countries in an pathogen reported to infect this aphid. man) (Hymenoptera: Aphelinidae), the attempt to control it (DeBach 1964). This Although Aphelinus mali (Haldeman) most important parasitoid of this aphid parasitoid was originally known to occur has been widely acclaimed as the most species (DeBach 1964) has proved to be in areas of the eastern United States and important natural enemy of this aphid ineffective. Canada (MacPhee et al. 1976). It was initial- species, a review of literature, however, This paper presents a worldwide ly introduced into Europe in the early part revealed a number of other natural en­ review of the natural enemies of E. lani- of 1920 and has since then been released in emies which should be considered in gerum. It provides information on natural 51 other countries; becoming established biological control or integrated pest man­ enemies which could be manipulated for in 42 (van Lenteren 1990). It was intro- agement programs of E. lanigerum. the biological control or integrated pest duced from North America into France management of this aphid species in dif- in 1920 and 1921 (Marchal 1929), South Introduction ferent geographic regions. Africa in 1920 (Georgala 1953) and Uru- The woolly apple aphid, Eriosoma lani- guay early in 1921 and 1922. From France, gerum (Hausmann) (Hemiptera: Aphidi- Materials and methods it reached Austria in 1926 (Werneck 1931) dae) is one of the economically important Information on the natural enemies of E. and batches were sent to Argentina, Eng- and most widely distributed pests of ap- lanigerum was obtained using abstracts in land, Italy, Chile and Spain from Uruguay ple, Malus domestica (Borkh.) and other the Review of Applied Entomology (from (Trujillo 1922, Nonell 1932). From Italy, it species of Malus, Cotoneaster, Crataegus, 1913 to 1994), Biological Abstracts and was imported into Malta and Gozo dur- Sorbus and Pyracantha (Eastop 1966, Hill original journal articles. The search was ing 1933ñ34 (Borg 1936). This parasitoid 1983). A native of North America (Baker made in the Dixonís Library, University was introduced into Holland in 1925 (van 1915), it now occurs throughout the apple- of New England, Armidale, New South Poeteren 1925) and Mexico in 1953 (Coro- growing countries of the world (Eastop Wales, Australia. Original articles which nado 1955). From Ontario, Canada, A. mali 1966). Both the nymphs and adults cause were not available in this library were ob- was introduced into the Okanagan valley, damage to apple by feeding on the roots tained from other libraries in either Aus- British Columbia, in 1929 (Venables 1931). and stems, particularly the tender places tralia or overseas through inter-library It reached Transcancasia from the Crimea on the trunk and branches, new lateral loans. Furthermore, on-line and CD-ROM in 1932 (Stephanov 1935) and Korea from growth and areas with damage caused services were used to search for other in- Japan in 1934 (Nakayama 1936). Cisílik by mechanical injury (Asante 1995a). Its formation which could not be obtained and Kawecki (1935) reported that A. mali damage to apple is much more serious in from the journal abstracts. appeared in Poland without having been the United States where root infestation is artificially introduced. prevalent (Marcovitch 1934, Brown 1986). Results Similarly, Kovacevic (1937) reported Infestation of the aphid on apple roots and The literature reports that E. lanigerum is its discovery in Yugoslavia in 1930. The shoots has been shown to reduce survival attacked by five species of hymenopterous parasitoid was introduced into New Zea- of nursery trees and to weaken mature ap- endoparasitoids, two species of Acarina land in 1921 (Tillyard 1921) and from there ple trees, leading to the loss of vitality and (ectoparasites), 73 species of predatory it was brought to Tasmania, Australia, in poor quantitative and qualitative yields insects and a fungal pathogen. Other spe- 1922 (Nicholls 1932, Wilson 1960). In Aus- (Sherbakoff and McClintock 1935, Klim- cies found to be associated with this aphid tralia, A. mali reached the Stanthorpe dis- stra and Rock 1985). pest are hyperparasitoids. trict of Queensland in 1923 (Jarvis 1926), Plant Protection Quarterly Vol.12(4) 1997 167 New South Wales and Victoria in 1924ñ25 moth, Cydia pomonella (L.) (Georgala 1953, orchards. The functional response data ob- (Gurney 1926, Pescott 1935). Bengston 1960, Adlakha and Hameed tained in the laboratory for F. auricularia, 1972, Yothers 1974, Hely et al. 1982). On P. australasiae and H. conformis all fitted The effectiveness of A. mali as a the other hand, Holdsworth (1970) stated well to the type II model of the Holling biological control agent that in addition to killing A. mali, some disc equation (Asante 1995b). These The effectiveness of A. mali as a biologi- spray programs used generally in apple predators were found to consume larger cal control agent for E. lanigerum has been pest control, also control E. lanigerum so numbers of early than later instars of reported worldwide such as New Zea- that the natural control disturbance may E. lanigerum within the same time pe- land (Tillyard 1924), Australia (Nicholls not become an economic factor. riod. Many studies have confirmed that 1932, Evans 1938, Sproul 1981), South F. auricularia is an effective predator of Africa (Lundie 1939), India (Rahman and Hyperparasitoids of A. mali E. lanigerum (McLeod and Chant 1952, Khan 1941), The Netherlands (Evenhuis Evenhuis (1958) recorded three species Mueller et al. 1988, Asante 1995b). Asante 1958), Japan (Hukusima 1960), Russia of hyperparasitoids, Pachyneuron aphidis (1995b) reported that an adult F. auricu- (Boldyreva 1970) and Iraq (El-Haidari and (Bouche), Asaphes vulgaris Walk and Cera- laria could consume up to 107 individual Aziz 1978). phron sp. from E. lanigerum in The Nether- nymphs of E. lanigerum per day. However, The introduction of this parasitoid has lands. Also, P. aphidis has been reported to F. auricularia has only been recorded in been cited in the literature as the first ac- attack A. mali occasionally in Yugoslavia Australia and The Netherlands as a preda- knowledged case of successful biological (Kovacevic 1937) and Australia (Asante tor of E. lanigerum. Also, the seven spe- control program of an aphid species (van 1995a). Moreover, the two Pteromalids, P. cies of predatory Hemiptera found in the Lenteren 1990) and of a tree fruit pest aphidis and A. vulgaris have been reported literature have all been recorded in The (MacPhee et al. 1976). In western Aus- to attack A. mali in Crimea (Meier and Netherlands (Table 2). tralia, its introduction has resulted in one Telenga 1933) and in Germany (Sprengel of the Stateís most outstanding successes 1931). Conclusion in biological control (Sproul 1981). It has, The following species have been record- It has been found from this study that however, been found to be ineffective un- ed from E. lanigerum in New South Wales, apart from the exotic endoparasitoid, der cool climatic conditions (Massee 1943, Australia; Ophelosia bifasciata Girault, Mo- A. mali, which has been introduced into Miller 1947, Rawat et al. 1989, van Len- ranila comperei (Ashmead), a Chartocerum all apple-growing regions of the world teren 1990, Asante and Danthan arayana sp.
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