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Aonidiella aurantii (Maskell)--Diaspididae




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Events leading to the biological control of California red scale have been variously presented in previous sections, as it marks one of the most thorough and scientific approaches in biological control. It is also the longest campaign in the history of biological control.  Kennett et al. (1999) summarized the history of these studies, and Ebeling (1959) regarded red scale as the most important citrus pest worldwide.  Although it is not as widely distributed as purple scale, it causes greater damage and is more difficult to control.  California red scale is believed to be of oriental origin (Quayle 1938). 


During 1889-1947 a variety of exotic natural enemies were introduced into California for control, the earliest efforts emphasizing introductions of coccinellid predators, of which more than 40 species were imported during 1889-1892 (Compere 1961).  Most failed to established and attention was then given to parasitoids.  During 1900-1908 several species, including Aspidiotiphagus citrinus (Craw), Comperiella bifasciata Howard and Pteroptrix (= Casca) chinensis (Howard) were imported from southern China, but none established (Compere 1961).  One parasitoid that became associated with the scale in southern California during this time was Aphytis chrysomphali (Mercet), although its origin remained obscure.  This parasitoids was propagated during 1902-1904 and distributed to citrus orchards on request, but dramatic results were not obtained (Compere 1961).  Following this poor performance of A. chrysomphali, additional parasitoids in the genus Aphytis were discovered in foreign areas, but they were erroneously believed to be the same species. 


During 1916-1924 additional introductions of Comperiella bifasciata were made from Japan (Compere 1961).  It did not rear on red scale in the laboratory so a factitious host, Chrysomphalus bifasciculatus Ferris was used.  Releases in the field did not result in parasitism of red scale, but rather the yellow scale, Aonidiella citrina (Coquillett) (Smith 1942).  Later the original host scale in Japan was identified as Aonidiella taxus Leonardi Chrysomphalus bifasciculatus and not A. aurantii and C. aonidium (L.) as originally believed.


Several coccinellid predators were imported from South Africa, Australia, South America and China during 1918-1934 (Compere 1961).  An Aphytis sp. (probably A. lingnanensis DeBach) was imported from southern China in 1924 under the erroneous name of A. chrysomphali, but did not become established. The endoparasitoid Habrolepis rouxi Compere was imported from South Africa in 1937, and was widely colonized.  Establishment was obtained in a very small area, however (Flanders 1944a).  Comperiella bifasciata was tried once more in 1940, but this time the collections were made on A. auranti in southern China (Smith 1942), and  were then successfully propagated on that host in California (Flanders 1943a).  The parasitoid eventually spread throughout all of the southern California area except near the coast (DeBach et al. 1955).  Flanders (1944b) and Teran & DeBach (1963) distinguished two distinct biological races of this parasitoid, one from A. auranti in China and the other from A. taxus and C. bifasciculatus in Japan, which solved the earlier puzzle.


The period 1947-1949 marked many shipments of parasitized red scales being sent to California from southern China and Taiwan.  Propagation was successful with many species, but only Aphytis lingnanensis from southern China and Encarsia (= Prospaltella) perniciosi (Tower) from Taiwan became established (DeBach et al. 1950, DeBach 1953, Rosen & DeBach 1978).  Encarsia perniciosi readily established in the coastal areas of southern California.  However, A. lingnanensis became dominant by 1958, displacing the long established A. chrysomphali everywhere but in a few coastal areas (DeBach & Sundby 1963).  Although producing good biological control in coastal areas, A. lingnanensis was relatively ineffective in the warmer, drier interior areas of southern California. 


Explorations were expanded in Asia during 1956-57, resulting in the importation of some new parasitoids, including two Aphytis spp. (DeBach 1959).  Only Aphytis melinus DeBach <PHOTO> from northern India and Pakistan was established in California, however.  Aphytis fisheri DeBach, Aphytis proclia (Walker), Coccobius (= Physcus) debachi (Compere & Annecke) and Aspidiotiphagus citrinus were liberated but did not become established.  Importations during 1960-1964 of Aphytis coheni DeBach and Aphytis holoxanthus DeBach from Israel and Aphytis africanus Quednau from South Africa, all failed to establish (Rosen & DeBach 1978).


Aphytis melinus spread rapidly following liberation in 1958, and soon displaced A. lingnanensis throughout the area.  By 1964 A. melinus was the dominant parasitoid on A. aurantii in southern California except along coastal areas, where A. lingnanensis remained common or dominant (DeBach 1966, 1969).  There was a gradual decline in red scale abundance in southern California after 1962 which was attributed to these two parasitoids.  Presently A. melinus is complemented by C. bifasciata in the interior and intermediate areas  while A. lingnanensis is complemented by E. perniciosi in coastal areas (DeBach 1965a, 1969).  Control varies from partial to complete depending on the climatic zone in which red scale occurs.  Extreme temperatures cause abnormal sex ratios and progeny production in A. melinus and A. lingnanensis which helps to explain some of the poor performance witnessed with these parasitoids in certain climatic zones (Kfir & Luck 1979).  The discovery of Aphytis melinus was the result of increased taxonomic knowledge and of previous ecological field studies with A. chrysomphali beginning in 1946 and with A. lingnanensis starting in 1948 (DeBach 1974).  Studies with these parasitoids showed the importance of the genus Aphytis, and led to the search for additional species from climatic zones similar to the interior areas of southern California. 


Biological control of red scale was investigated in Australia on the same pattern as that for California.  Around 1902 several species of natural enemies were imported from different countries, but only one species, Aphytis chrysomphali established in Western Australia (Wilson 1960).  Comperiella bifasciata became established in the 1940's, and the subsequent importations of Aphytis melinus in 1961 and Encarsia perniciosi in 1970 established these parasitoids.  Attempts to establish in Australia Aphytis lingnanensis, A. coheni, A. riyahdi DeBach and Habrolepis sp. after 1977 were not successful (Furness et al. 1983).  Aphytis chrysomphali was displaced by A. melinus after 1972 in the Lower Murray Valley in the states of Victoria and South Australia (Furness et al. 1983).  A decline in A. aurantii abundance following colonization of Aphytis melinus was documented (Campbell 1976).  In Queensland effective biological control was caused by Aphytis lingnanensis and Comperiella bifasciata (Smith 1978a). 


Importations of Aonidiella aurantii parasitoids were also made in South Africa, France, Sicily, Cyprus, Greece, Morocco and Israel, with the same pattern of displacement by A. melinus of A. chrysomphali witnessed (DeBach & Argyriou 1967, Rosen 1967, Orphanides 1984).  On the other hand, in Israel A. melinus displaced A. chrysomphali, but it did not displace A choeni (Rosen 1967); and in South Africa A. africanus is still dominant despite the establishment of A. melinus, A. lingnanensis and A. coheni (Annecke & Moran 1982).  Partial to complete biological control was reported in other countries, such as Greece (DeBach & Argyriou 1967), France (Benassy & Bianchi 1974), Argentina (Crouzel et al. 1974), Cyprus (Orphanides 1984), and Chile (Gonzalez 1969).  For some unknown reason, Comperiella bifasciata alone was responsible for the successful biological control witnessed in France (Kennett et al. 1999) (also see Coquillett 1893, Coquillett & Koebele 1893, Jones 1936, Sokoloff & Klotz 1942, Campbell 1943, Jenkins 1945, Gressitt & Flanders 1949, Bodenheimer 1951, Flanders 1953, Flanders & Gressitt 1958, Landi & DeBach 1960, Harpaz 1961, Quednau 1964, 1965; Quednau & Hübsch 1964, Rosen 1965, Gonzalez & Rojas 1966, Benassy & Euverte 1967).


The strategy of managing red scale in California by 2004 had developed into a periodic parasitoid release program in those orchards where climate posed restrictions on the natural annual increase of the parasitoids or where insecticidal drift from neighboring areas  upset  natural  balances..  The boost of adding additional parasitoid individuals in such areas provides satisfactory red scale control in many orchards.



REFERENCES:          [Additional references may be found at:   MELVYL Library ]


Annecke, D. P. & V. C. Moran.  1982.  Insects and Mites of cultivated plants in South Africa.  Butterworth & Co., South Africa.  383 p.


Benassy, C. & H. Bianchi.  1974.  Observations sur Aonidiella aurantii Mask. et son parasite indigene Comperiella bifasciata How. (Hymenoptera, Encyrtidae).  Bull. SROP 3:  39-50.


Benassy, C. & G. Euverte.  1967.  Perspectives nouvelles dans la lutte contre Aonidiella auranti au Maroc (Hom. Diaspididae).  Entomophaga 12:  449-59.


Bodenheimer, F. S.  1951.  Citrus Entomology in the Middle East.  Junk Publ., The Hague.  663 p.


Campbell, M. M.  1976.  Colonization of Aphytis melinus DeBach [Hymenoptera: Aphelinidae] in Aonidiella aurantii (Mask.) [Hemiptera: Coccidae] on citrus in South Australia.  Bull. Ent. Res. 65:  659-68.


Campbell, T. F.  1943.  Introduction of scale parasites from California.  Austral. Council Sci. & Indus. Res. J. 16:  41-2.


Compere, H.  1961.  The red scale and its natural enemies.  Hilgardia 31:  173-278.


Coquillet, D. W.  1893a.  Report on the Australian insects sent by Albert Koebele to Ellwood Cooper and B. M. LeLong.  Insect Life 5:  251-54.


Coquillet, D. W. & A. Koebele.  1893.  The present status of the recent Australian importations.  Insect Life 6:  24-9.


Crouzel, I. S., H. G. Bimboni, M. Zanelli & E. N. Botto.  1973.  Lucha biológica contra la "cochinilla roja australiana" Aonidiella aurantii (Maskell) (Hom.: Diaspididae) en cítricos.  Patología Vegetal Ser. 5(10): 251-318.


DeBach, P.  1953.  The establishment in California of an oriental strain of Prospaltella perniciosi Tower on the California red scale.  J. Econ. Ent. 46:  1103.


DeBach, P.  1959.  New species and strains of Aphytis (Hymenoptera, Eulophidae) parasitic on the California red scale, Aonidiella aurantii (Mask.) in the Orient.  Ann. Ent. Soc. Amer. 52:  354-62.


DeBach, P.  1962.  Ecological adaptation of parasites and competition between parasite species in relation to establishment and success.  11th Intern. Cong. Ent. 2:  687-90.


DeBach, P.  1965a.  Some biological and ecological phenomena associated with colonizing entomophagous insects, p. 287-306.  In:  H. G. Baker & G. L. Stebbins (eds.), The Genetics of Colonizing Species.  Academic Press, Inc., New York.


DeBach, P.  1965b.  Weather and the success of parasites in population regulation.  Canad. Ent. 97:  848-63.


DeBach, P.  1966.  The competitive displacement and coexistence principles.  Ann. Rev. Ent. 11:  183-212.


DeBach, P.  1969.  Biological control of diaspine scale insects on citrus in California.  Proc. 1st Intern. Citrus Symp., Riverside, Calif. 2:  801-15.


DeBach, P. & L. C. Argyriou.  1967.  The colonization and success in Greece of some imported Aphytis spp. (Hym.: Aphelinidae) parasitic on citrus scale insects (Hom.: Diaspididae).  Entomophaga 12:  325-42.


DeBach, P. & R. A. Sundby.  1963.  Competitive displacement between ecological homologues.  Hilgardia 34:  105-66.


DeBach, P., E. J. Dietrick, C. A. Fleschner & T. W. Fisher.  1950.  Periodic colonization of Aphytis for control of the California red scale.  Preliminary tests, 1949.  J. Econ. Ent. 43:  783-802.


DeBach, P. J. H. Landi & E. B. White.  1955.  Biological control of red scale.  Citrograph 40:  254, 271-72.


Ebeling, W.  1959.  Subtropical Fruit Pests.  Univ. Calif. Div. Agric. Sci.  436 p.


Flanders, S. E.  1943a.  Mass production of the California red scale and its parasite Comperiella bifasciata.  J. Econ. Ent. 36:  233-35.


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Flanders, S. E.  1944b.  Observations on Comperiella bifasciata, an endoparasite of diaspine coccids.  Ann. Ent. Soc. Amer. 37:  365-71.


Flanders, S. E.  1953.  Variations in susceptibility of citrus-infesting coccids to parasitization.  J. Econ. Ent. 46:  266-69.


Flanders, S. E. & J. L. Gressitt.  1958.  The natural control of California red scale in China.  Calif. State Dept. Agric. Bull. 47:  23-33.


Furness, G. O., G. A. Buchanan, R. S. George & N. L. Richardson.  1983.  A history of the biological and integrated control of red scale, Aonidiella aurantii on citrus in the lower Murray Valley of Australia.  Entomophaga 28:  199-212.


Gonzalez, R.  1969.  Biological control of citrus pests in Chile.  Proc. 1st Intern. Citrus Symp., Riverside, Calif. 2:  839-47.


Gonzalez, R. H. & S. P. Rojas.  1966.  Estudio analítico del control biológico de plagas agrícolas en Chile.  Agric. Tech. 26:  133-47.


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Kfir, R. & R. F. Luck.  1979.  Effects of constant and variable temperature extremes on sex ratio and progeny production by Aphytis melinus and A. lingnanensis (Hymenoptera: Aphelinidae).  Ecol. Ent. 4:  335-44.


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Quednau, F. W. & H. M. Hübsch.  1964.  Factors influencing the host-finding and host-acceptance pattern in some Aphytis species (Hymenoptera: Aphelinidae).  South Africa J. Agric. Sci. 7:  543-53.


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