Biology and virus transmission of citrus aphids.

Aphid species of the world which attack citrus and transmit citrus tristeza virus (CTV) are reviewed. Four aphids, Toxoptera citricidus, T. aurantii, Aphis gossypii and A. spiraecola, are all common species, and all of them transmit CTV. Their occurrence varies in different countries and localities. T. citricidus and A. gossypii are particularly dangerous vectors of CTV. The aphid life cycle in general, and that of the four species listed above in particular, are described, together with the seasonal occurrence of major citrus aphids in Japan and the virus diseases they transmit. The control of aphids in order to prevent virus disease is also discussed. APHID SPECIES AND VIRUS TRANSMISSION Several aphid species attack citrus in different parts of the world (Barbagallo 1966, Komazaki 1981, Niet Nafria et al. 1984, Blackman and Eastop 1984, Viggiani 1988, Yokomi et al. 1992). All of these belong to the families Aphidinae and Aphididae. Four important species are Toxoptera citricidus, Toxoptera aurantii, Aphis gossypii and Aphis spiraecola (= citricola) (Table 1). Species composition and seasonal occurrence vary in different countries and regions. T. citricidus is not found in the Mediterranean area or North America, while A. spiraecola invaded the Mediterranean region in the 1960s and has become a serious citrus pest there (Viggiani 1988). T. aurantii is not a major species, although it is abundant on tea in Japan (Komazaki et al. 1985). Citrus tristeza virus (CTV) can only be transmitted by aphids, including the four important aphid species listed above (Costa and Grant 1951, Norman and Grant 1956, Sasaki 1974, Ahlawat and Raychaudhuri 1988). CTV is transmitted by the aphids in a semi-persistent manner. It can be acquired by the aphid as it feeds for 30 minutes on a plant infected with virus, and is transmitted as the aphid feeds for 30 minutes on a healthy plant. Transmissibility rises as the feeding period is prolonged up to 24 hr, but the aphid loses its ability to transmit CTV after it has fed for two days on healthy plants (Sasaki 1974) or a synthetic diet (Komazaki 1984). In some cases, the virus is transmitted non-persistently (Retuerma and Price 1972, Manjunath 1985). Aphid transmissibility of the virus varies with different aphid species (Sasaki 1974, Raccah et al. 1977, Roistacher and Bar-Joseph 1989) and virus strains (Bar-Joseph and Loebenstein 1973, Yokomi et al. 1989). T. citricidus is the most potent vector of CTV (Costa and Grant 1951, Sasaki 1974, Ahlawat and Raychaudhuri 1988). A. gossypii was not formerly a potent vector (Dickson et al. 1956, Norman and Grant 1956), but has now become a dangerous one in USA and Israel (Raccah et al. 1980, Roistacher et al. 1984). A. spiraecola and T. aurantii are much less effective vectors (Roistacher and Bar-Joseph 1989), with the exception of T. aurantii in India (Manjunath 1985). With regard to T. citricidus, there is no difference in virus transmissibility between alate and apterous aphids, or between adults and nymphs (Costa and Grant 1951, Sasaki 1974). Similarly, the adults and nymphs of A. gossypii can both transmit the virus equally (Norman and Sutton 1969, Roistacher et al. 1984). Transmission curves of T. citricidus are shown in Fig. 1. This is based on experimental data using Mexican lime, and a twoday feeding period for acquisition and inoculation. Data are fitted to the formula Y=1-exp (-np), where n is the number of aphids inoculated, and p is the average transmission rate of a single aphid. In this formula, the transmissibility of a single T. citricidus