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Entomologica, Bari, 33, (1999): 179-184 ABD-RABOU, S.; HANAFI, A.; HUSSEIN, N. Plant Protection Research Institute, Agricultural Research Center, Dokki-Giza, Egypt NOTES ON THE PARASITOIDS OF THE SOFT BROWN SCALE, COCCUS HESPERIDUM (HEMIPTERA: COCCIDAE) IN EGYPT. ABSTRACT NOTES ON THE PARASITOIDS OF THE SOFT BROWN SCALE, COCCUS HESPERIDUM (HEMIPTERA: COCCIDAE) IN EGYPT. Thirteen species of hymenopterous parasitoid were found in association with Coccus hesperidum at three locations in Egypt: 4 species of Aphelinidae (of which three were recorded for the first time); seven species of Encyrtidae (of which three were recorded for the first time), the first record of a species of Mymaridae, plus a species of Pteromalidae. The relative abundance of these parasitoids is discussed. Key words: survey, rearing methods, percentage parasitism, Coccophagus, Marietta, Diversinervis, Metaphycus, Microterys, Parachthrodryinus, Prochilonerus, Alaptus, Scutellista. INTRODUCTION The soft brown scale, Coccus hesperidum L. (Hemiptera: Coccidae) is one of the most cosmopolitan and polyphagous coccid species (Gill et al., 1977). It has been recorded off about 236 host plants in 93 plant families, distributed among 112 countries (Ben-Dov, 1993). In Egypt, it is considered to be a serious pest, attacking 18 plant species belonging to 15 families, including citrus, guava and some ornamental plants (Mohammad & Nada, 1991). Both in Egypt and elsewhere, there have been numerous studies on the role of parasitoids in the control of the soft brown scale. In Egypt, Priesner & Hosny (1940) recorded 5 aphelinid species and an encyrtid associated with C. hesperidum. In California, Bartlett (1978) emphasised the important role of Metaphycus luteolus Timberlake in the control of this species, while, in Israel, Rosen (1967) recorded 15 species of parasitoid belonging to the Aphelinidae, Encyrtidae, Euphilidae and Pteromalidae. The parasitoid species discussed below were those collected in Egypt in association with C. hesperidum. MATERIALS AND METHODS A survey of the species and abundance of the parasitoids associated with C. hesperidum in Egypt, was carried out between June 1996 and June 1997 on http://dx.doi.org/10.15162/0425-1016/830

180 Ficus nitida, Psidium guajava and Nerium sp. in three localities, namely El- Arish, Gharbiya and Giza. The eggs, larvae and non-ovipositing stages of C. hesperidum were sampled monthly on the leaves of each host (30 infested leaves per sample). These were transferred to the laboratory in wellventilated boxes and then all first-instar larvae and ovipositing adults were removed, as well as all other insects. The total number of each of the remaining C. hesperidum stages was recorded per leaf. Each leaf was stored in a well-ventilated glass tube and monitored daily for the emergence of parasitoids. In the calculations of percentage parasitism, it was assumed that only one parasitoid emerged from each scale individual. All emerging parasitoids were either card or slide mounted (depending on family) and identified to species. RESULTS AND DISCUSSION Thirteen species of hymenopterous parasitoid and hyperparasitoid were collected from samples of C. hesperidum on F. nitida, P. guajava and Nerium sp. in Giza, Gharbiya and El-Arish locations. These are listed in alphabetical order below: Aphelinidae Coccophagus bivittatus Compere: here recorded from Egypt for the first time parasitising C. hesperidum but restricted to Giza, where the percentage parasitism on F. nitida was 0.7%, with a peak of 4% in Feb. 1997. C. bivittatus has also been recorded as a parasitoid of C. hesperidum from South Africa (Compere, 1931a), Argentina (De Santis, 1948), Italy (Zinna, 1961), India (Sankaran, 1955) and Israel (Rosen, 1967). Coccophagus ishii Compere: here recorded from Egypt for the first time parasitising C. hesperidum but restricted to El-Arish, where the percentage parasitism on Nerium sp. was 0.4%, with a max. of 2% in June 1996. C. ishii has been recorded from Japan as a parasitoid of various soft scale species, especially of the genus Pulvinaria (Compere, 1931a; Ishihara, 1977). Coccophagus scutellaris (Dalman): first recorded in Egypt in Alexandria by Priesner & Hosny (1940) parasitising C. hesperidum and Pulvinaria floccifera (Westwood) on citrus and Ficus respectively; in this study, only found at Gharbiya, where the percentage parasitism on P. guajava was 1.1%, with a peak of 7% in Nov. 1996. C. scutellaris is a well-known, cosmopolitan

181 parasitoid of various soft scale species (Rosen, 1967). Nikol skaya (1952) recorded it associated with Saissetia oleae (Olivier) and Ceroplastes floridensis (Comstock). Marietta picta (André): here recorded for the first time as a hyperparasitoid from C. hesperidum in Egypt but only recorded from El-Arish, where the percentage parasitism on Nerium sp. was 2.5%, with a peak of 8% in Feb. 1997. M. picta is a well-known and widely distributed species in the Palaearctic region and has also been recorded from Canada, India and Mexico (Hayat, 1986). Encyrtidae Diversinervus elegans Silvestri: first recorded in Egypt by Priesner & Hosny (1940) parasitising S. oleae, P. floccifera and C. hesperidum; in the present study only recorded from Giza and Gharbiya. Percentage parasitism in Giza on F. nitida was 5.3% and in Gharbiya on P. guajava 10.9%, with a max. in Giza of 15% in Oct. 1996 and in Gharbiya of 23% in June 1996. First recorded from Eritrea (Silvestri, 1915) but now also known from Australia (Compere, 1931b; Wilson, 1960) and Southern Africa (Annecke, 1964). It has been found to be a common parasitoid of S. oleae on olives but rare in Saissetia coffeae (Walker) (Rosen et al., 1971). Metaphycus flavus (Howard): first recorded from Delta and Upper Egypt by Priesner & Hosny (1940) parasitising C. hesperidum on citrus, P. floccifera on P. guajava and S. oleae on Cycas revoluta; in the present study, only recorded from Giza and Gharbiya. Percentage parasitism in Giza on F. nitida was 1.4% and in Gharbiya on P. guajava was 3.9%, with a maximum parasitism of 12% in Giza in June and 7% at Gharbiya in July. Metaphycus helvolus (Compere): recorded here for the first time in Egypt parasitising C. hesperidum, but only recorded from El-Arish and Gharbiya. Percentage parasitism in Gharbiya on P. guajava 0.9% and in El-Arish on Nerium sp. 4.0%, with a max. parasitism of 4% in Gharbiya during March, 1997 and of 14% in El-Arish in June, 1997. M. helvolus was originally described from South Africa (Compere, 1926), where it is an abundant primary parasitoid of various soft scales, including Saissetia sp., Marsipococcus proteae (Brain) and C. hesperidum (Annecke, 1964).

182 Microterys flavus (Howard): here recorded from Egypt for the first time parasitising C. hesperidum, but only recorded from Giza and Gharbiya. Percentage parasitism in Giza on F. nitida 11.2%, with a max. of 24%. M. flavus is a widely distributed parasitoid of various soft scale insects and has been recorded from North America, North and South Africa, the Far East, Australia, New Zealand, Europe and around the Mediterranean Basin (Thompson, 1954; Annecke, 1964; Rosen, 1967; Saakyan-Baranova, 1968). Microterys sp.: here recorded from Egypt for the first time parasitising C. hesperidum, but only found at El-Arish, where the percentage parasitism was 1.9% on Nerium sp., with a peak of 6% in June, 1996. Parechthrodryinus coccidiphagus (Mercet): first recorded from Lower and Upper Egypt by Priesner & Hosny (1940) parasitising C. hesperidum on citrus and Parasaissetia nigra (Nietner) on Ficus carica respectively; in the present study, only found at Gharbiya, where the percentage parasitism was 0.2% on P. guajava, with a peak of 1% in July 1996. Prochilonerus aegyptiacus (Mercet): first recorded in Egypt by Priesner & Hosny (1940) parasitising various coccid species on Zilla sp.; in the present study, only recorded from El-Arish, where the percentage parasitism was 2% on Nerium sp., with a peak of 1% in June and Aug., 1996. Mymaridae Alaptus pallidicornis Forester: here recorded from Egypt for the first time parasitising C. hesperidum, but only from El-Arish, where percentage parasitism was 1% on Nerium sp., with a peak of 5% in June, 1996. Pteromalidae Scutellista caerulea (Fonscolombe): first recorded from Lower and Upper Egypt by Priesner & Hosny (1940) from a range of soft scale species: namely Ceroplastes africanus Green on Acacia nilotica, Albizzia lebbek, F. carica and Tamarix sp.; Ceroplastes rusci (L.) on F. carica; P. nigra on Ficus sycomorus; S. oleae on Compositae, and S. coffeae on olive. In the present study it was only found at Giza and Gharbiya. Percentage parasitism in the present study was 5.5% in Giza on F. nitida and 6.1% in Gharbiya on P. guajava, with peaks in Sept. 1996 of 13% in Giza and 25% in Gharbiya. This species is a cosmopolitan egg predator and a facultative ectoparasitoid of various soft scale insects, probably of African or Far Eastern origin (Smith &

183 Compere, 1928; Rubtsov, 1954). Bodenheimer (1951) listed it as an important natural enemy of several soft scale insects, while Rosen (1967) found it to be often the dominant parasitoid of C. floridensis and abundant in S. oleae but rare in C. rusci on citrus. REFERENCES ANNECKE, D.P., 1964 - The encyrtid and aphelinid parasites (Hymenoptera: Chalcidoidea) of soft brown scale, Coccus hesperidum Linnaeus (Hemiptera: Coccidae) in South Africa. South African Department of Agricultural Technical Services, Entomological Memoirs, 7: v+74pp. BARTLETT, B.R., 1978 - Coccidae. Pp 57-74 in C.P. Clausen (Ed.), Introduced Parasites and Predators of Arthropod Pests and Weeds: a World Review. Agricultural Handbook. 480 United States Department of Agriculture, Washington, D.C. BEN-DOV, Y., 1993 - A Systematic Catalogue of the Soft Scale Insects of the World (Homoptera: Coccoidea: Coccidae), with Data on Geographical Distribution, Host Plants, Biology and Economic Importance. Sandhill Crane Press, INC. 497pp. BODENHEIMER, F.S., 1951 - Citrus Entomology in the Middle East. W. Junk, The Hague. 663pp. COMPERE, H., 1926 - Description of new coccid-inhabiting chalcidoid parasites. University of California Publications in Entomology, 4: 1-31. COMPERE, H., 1931a - A revision of the species of Coccophagus, a genus of hymenopterous coccid-inhabiting parasites. Proceedings of the United States National Museum, 78: 1-132. COMPERE, H., 1931b - A revision of the genus Diversinervus Silvestri, encyrtid parasites of coccids (Hymenoptera). University of California Publications in Entomology, 5: 233-245. DE SANTIS, L., 1948 - Estudio monografico de los afelinidos de la republica Argentina. Revista del Museo de La Plata (Zool.), 5: 23-280. GILL, R.J., NAKAHARA, S., WILLIAMS, M.L., 1977 - A review of the genus Coccus Linnaeus in America north of Panama (Homoptera: Coccoidea: Coccidae). Occasional Papers in Entomology, State of California Department of Food and Agriculture, 24: 44. HAYAT, M., 1986 - Notes on some species of Marietta (Hymenoptera: Aphelinidae), with a key to world species. Colemania, 2: 1-18. ISHIHARA, T.K., 1977 - Japanese species of Coccophagus and the related genera (Hymenoptera: Aphelinidae). Transactions of the Shikoku Entomological Society, 13: 89-103. MOHAMMAD, Z.K., NADA, S., 1991 - Observations on the Coccidae of Egypt (Homoptera: Coccoidea: Coccidae). Fourth Arab Congress of Plant Protection, 105-110. NIKOL SKAJA, M.N., 1952 - The chalcid fauna of the USSR. Opredeliteli po Fauna SSSR, Izdavaemye Zoologicheskim Muzeem, 44, 574 pp, Moscow-Leningrad (in Russian: English Translation, Israel Programme of Scientific Translations, Jerusalem, 1963, 593pp). PRIESNER, H., HOSNY, M., 1940 - Notes on parasites and predators of Coccidae and Aleyrodidae in Egypt. Bulletin de la Société Entomologique d Egypte, 24: 58-70.

184 ROSEN, D., 1967 - The hymenopterous parasites of soft scales on citrus in Israel. Beiträage zur Entomologie, 17: 251-279. ROSEN, D., HARPAZ, I., SAMISH, M., 1971 - Two species of Saissetia (Homoptera: Coccidae) injurious to olive in Israel and their natural enemies. Israel Journal of Entomology, 4: 35-53. RUBTSOV, I.A., 1954 - Citrus pests and their natural enemies. Akademiya Nauk SSSR, Leningrad. 260pp (in Russian). SAAKYAN-BARANOVA, A.A., 1968 - Microterys flavus How. (Hymenoptera: Encyrtidae), an effective parasite of soft brown scale (Coccus hesperidum L.) on the Black Sea Coast of the Caucasus. Trudy Vsesoyuznogo Entomologicheskogo Obshchestva, Akademiya Nauk SSSR, 52: 126-153 (in Russian). SANKARAN, T., 1955 - The natural enemies of Ceroplastes pseudoceriferus Green (Hemiptera: Coccidae). Journal of Scientific Research, Banaras Hindu University, 5: 100-119. SILVESTRI, F., 1915 - Contributo alla conoscenza degli insetti dell olivo dell Eritrea e dell Africa meridionale. Bolletino del Laboratorio di Zoologia Generale Agraria della R. Scuola Superiore d Agricoltura in Portici., 9: 240-334. SMITH, H.S., COMPERE, H., 1928 - A preliminary report on the insect parasites of the black scale Saissetia oleae (Bern.). University of California Publications in Entomology, 4: 231-334. THOMPSON, W.R., 1954 - A catalogue of the parasites and predators of insect pests. Section 2: Host parasite catalogue. Part 3: Hosts of Hymenoptera (calliceratid to evaniid). CIBC, Ottawa, pp 191-232. WILSON, F., 1960 - A review of the biological control of insects and weeds in Australia and Australian New Guinea. CIBC Technical Communication, 1, 102pp. ZINNA, G., 1961 - Richerche sugli insetti entomofagi II. Specializzazione entomoparassitica negli Aphelinidae: Studio morfologico, etologico e fisiologico del Coccophagus bivittatus Compere, nuovo parassita del Coccus hesperidum L. per l Italia. Bollettino del Laboratorio di Entomologia Agraria Filippo Silvestri, Portici, 19: 301-358.