Dialeurodes citri
(citrus whitefly)

D. citri is believed to be of oriental origin and is probably native to India. It has been widely spread across the world by the activities of man. It has a cosmopolitan distribution in southeastern Asia, the Middle East, the Mediterranean Region, USA, Central and South America. In northern and southern hemispheres, the distribution of D. citri does not cross the line of the 45th parallel. Outside of this zone, infestations by D. citri have been detected only under glass and on imported Citrus material (Bowman and Bartlett, 1978). Moreover, in these situations D. citri can be easily and promptly eradicated.

D. citri should be regarded as a quarantine pest in all citrus-growing areas where its occurrence has not yet been detected. Transport of living host-plants or fresh foliage of host-plants presents the main quarantine risk.

D. citri is one of the more polyphagous whiteflies, having been reported on ca 80 plant species, belonging to more than 50 genera and 30 families (Mound and Halsey, 1978). It is an important pest of Citrus, coffee, Diospyros kaki and a number of ornamentals.

D. citri is one of the best-investigated species of whitefly. It is polyvoltine, having several generations per year; in suitable areas, where optimum environmental conditions occur, up to five or six generations are reported yearly. A long winter diapause (spent in the nymphal stage), and a consequently lower number of generations may be observed in nearly all non-native areas, such as the Mediterranean Region. Two generations per year occur in Corsica and Spain (Onillon et al., 1975; Llorens and Capilla, 1994), two to four in Turkey (Soylu, 1980; Ulu, 1985; Uygun et al., 1990), and three in Italy (Priore, 1969; Barbagallo and Patti, 1978). Moreover, the life cycle of D. citri seems to vary according to the host plant. Gargani (1990) noted three yearly generations on privet but only one on persimmon.

Adults of D. citri normally live for ca 10 days, but they can live for as long as 27 days. The female lays her pale yellow eggs scattered singly on the underside of leaves, particularly young ones. The eggs usually hatch in 8-24 days, depending on the season. The young nymphs move around for several hours, then they settle on the leaf underside. Nymphs become sedentary, and their legs become vestigial.

A large number of natural enemies are known to develop on D. citri, but only a few of them are of relevance to biological control.

The fungal pathogen, Aschersonia is of major importance, especially in areas where the humidity is high. A. aleyrodis is the best known species among this group. In studies carried out in China (Shu-Zheng, 1996), this pathogen was shown to survive, grow and produce spores at 10-32°C (optimum 20-25°C); the temperature for the germination of conidia ranged from 5 to 30°C (optimum 20-30°C). The fungus grew at pH 3-10, although values ranging from 6 to 7 appeared to be optimal for mycelial growth and sporulation. In the field, A. aleyrodis survived 15 months (compared to 17 months at room temperature and 28 months at 0°C under laboratory conditions). Gao et al. (1985) state that this pathogen is highly effective in controlling D. citri in China. When branches infected with spores of the fungus were hung over trees infested by D. citri, the infection rate was 74% 8 months after treatment. A. placenta (which may be conspecific with A. aleyrodis) has been shown to attack nymphs (especially the second and third instars) of D. citri at a rate of 33-78% (Zou, 1988), and has been introduced in the former USSR, where in Adzharia it achieved up to 90% parasitism under favourable conditions (Ponomarenko et al., 1975).

Insect predators of D. citri belong to the Thysanoptera, Heteroptera, Neuroptera and the Coleoptera (including coccinellid beetles of the genera Clitosthethus, Delphastus and Serangium). Clitostethus arcuatus is a predator of D. citri and other similar species (Bemisia tabaci, Siphoninus phillyreae and Trialeurodes vaporariorum). In Italy, C. arcuatus has four generations per year (Loi, 1978; Liotta, 1981). In Sicily, the first generation occurs from mid-April to mid-May, the second in June, the third in July and the fourth from mid- or late-August to the end of September; adults overwinter in cracks in tree bark or in walls, but move into citrus orchards during mild sunny days. Studies carried out in the Republic of Georgia, record C. arcuatus as having only one generation per year (Agekyan, 1977; Loi, 1978). Each C. arcuatus female lays 11-41 eggs on the lower surface of Citrus leaves. Larvae hatch after 3-8 days and pupate after a further 8-24 days, dependent on the temperature. They mainly feed on eggs but also on nymphs of D. citri. Adults emerge 3-8 days after pupation. Another coccinellid species, Serangium parcesetosum, is probably native to India; but it has been introduced in several Citrus-growing areas for the biological control of D. citri, for example in southern France and Corsica (Malausa et al., 1988), during 1986-87, and the former Soviet Union (Timofeeva and Hoang, 1978). On the Black Sea coasts of the Caucasus, S. parcesetosum has four generations per year and destroys up to 90% of whitefly colonies. It passes the winter as adults, which congregate in masses in old leaves and beneath the bark of trees, and resume activity in early April (Timofeeva and Hoang, 1978).

Encarsia lahorensis is regarded as the most efficient parasitoid of D. citri. Its introduction into various citrus-growing areas of the world has resulted in parasitization levels of up to 70-80%. E. lahorensis has been successfully introduced in Greece, Israel, Italy, Republic of Georgia, Turkey and Uzbekistan (Viggiani and Mazzone, 1978; Pappas and Viggiani, 1979; Argov, 1988, Basova, 1991; Yoldas and Oncuer, 1992). In Florida, USA, E. lahorensis has become well-established in 59 of 67 counties (Sailer et al., 1984). In Alabama, USA, populations of D. citri were drastically reduced one year after the introduction of E. lahorensis, and 3 years after its release, D. citri was no longer a pest in areas where E. lahorensis was present (Hudson and Williams, 1986). Females of E. lahorensis develop as primary endoparasites of D. citri, but the males (which hatch from unfertilized eggs) develop ectoparasitically on female parasite larvae or conspecific pupae within the host; occasionally they may develop on the larvae or pupae of other males, when superparasitism occurs (Viggiani and Mazzone, 1978). Larvae that had almost completed their development and young pupae of both sexes of D. citri appear to be the stages preferred by ovipositing E. lahorensis. E. lahorensis has 4-6 generations per year in southern Italy (Viggianni and Mazzone, 1978), taking 17-25 days to develop from egg to adult.

A slide-mounted preparation of the pupal case (made according to the procedures of Martin, 1987) should be examined microscopically at a high magnification to confirm diagnosis. Martin (1987) provides a key.

The leaves of potential host plants (especially their underside) should be inspected for D. citri. Colonies are likely to contain small white winged adults, as well as eggs and nymphs.

D. citri resembles D. kirkaldyi, with which it has several host plants in common (including Citrus and Jasminum spp.). D. citri differs from D. kirkaldyi by the absence, in the pupa, of the first abdominal setae and in the position of the eighth abdominal setae. A median brown patch usually occurs in D. kirkaldyi (Bink-Moenen and Gerling, 1990). D. citrifolii also occurs on Citrus in the Neotropical region, southern USA, Western Samoa, India and the Far-East of Asia. D. citrifolii clearly differs from D. citri by not having stippled tracheal folds, and by possessing thoracic tracheal pores each with 3-5 internal teeth (Martin, 1987).

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

IPM Programmes

Control of D. citri infestations should always be arranged according to the general criteria of integrated control; thus chemical and biological methods should be opportunely balanced to obtain a synergistic effect. Thresholds for the application of an artificial control are generally considered within the European Union as the occurrence of 20-30 whitefly nymphs per leaf on orange and lemon, and of 5-10 whitefly nymphs per leaf on mandarin or mandarin-like citrus species.

Biological Control

In areas where D. citri is a recent introduction, releases of the parasitoid Encarsia lahorensis are often beneficial. Introductions may be achieved using either the 'bouquets' or the 'small plants' methods: the former appears to be more practical for small-scale releases in private orchards, whilst the second is more useful in large-scale releases in large citrus growing areas (see Natural Enemies). Spring and autumn appear to be the best seasons for introducing E. lahorensis.

Chemical Control

Chemical applications usually provide only a temporary suppression of D. citri, which is often followed by resurgence. Thus, chemical control should be considered only for heavy infestations, when it is necessary to quickly reduce the whitefly population before trying to rebuild the balance with the re-introduction of natural enemies. Simple sprayed oils or oil emulsions are generally employed which contain 1% oil in the spray mixture (Priore and Pandolfo, 1972; Barbagallo and Patti, 1978; Ulu, 1987; Uygun et al., 1990). Particular attention should be given to carefully treating the underside of leaves, since the greatest number of nymphs is found there. Trials have been conducted in Israel for the use of the insect growth regulators, buprofezin and pyriproxyfen. The former proved to be more effective on first- and second- instar nymphs, whilst the latter exhibited more ovicidal properties. They were both reported not to adversely affect E. lahorensis (Peleg, 1990).