BIOLOGY AND VIRUS TRANSMISSION OF

Shinkichi Komazaki Akitsu Branch, Fruit Tree Research Station, Ministry of Agriculture, Forestry and Fisheries, Akitsu, Hiroshima 729-24, Japan

ABSTRACT

Aphid species of the world which attack citrus and transmit (CTV) are reviewed. Four aphids, 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 life cycle in general, and that of the four species listed above in particular, are de- scribed, together with the seasonal occurrence of major citrus aphids in Japan and the virus dis- eases they transmit. The control of aphids in order to prevent virus disease is also discussed.

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

Key words: Toxoptera citricidus, Toxoptera aurantii, Aphis gossypii, Aphis spiraecola, life-cycle, citrus tristeza virus, seasonal occurrence, resistance.

1 Table 1. Aphid species attacking citrus

is estimated to be 0.04, and of A. gossypii 0.03 live on a single species of plant or a group of closely according to data in Roistacher et al. 1984 and related species. The aphid life cycle is generally within the range 0.01 - 0.11 according to other defined by two criteria, the appearance of sexual estimates (Yokomi et al. 1989). forms and host alternation. Some aphid species, including A. gossypii, A. spiraecola and T. citricidus, BIOLOGY OF APHIDS have both holocyclic and anholocyclic strains. Aphids have many morphs (Hille Ris Aphids can propagate parthenogenetically, Lambers 1966), including winged and wingless forms. their parthenogenesis being linked with viviparity. Winged parthenogenetic females (alate vivipara or Sexual and parthenogenetic reproduction alternate virginopara) disperse and search for new host plants, in the life cycle (cyclical parthenogenesis). Sexual while the wingless parthenogenetic females (apter- forms usually appear in fall and oviposit overwinter- ous vivipara) can quickly reproduce on host plants. ing eggs on the primary host (holocycle) (Fig. 2). In host alternating species, the winged female mi- Eggs hatch in spring, and each hatched larva devel- grates between primary and secondary hosts: the ops into a mother which reproduces parthenogeneti- fundatrix or her daughter on the primary host pro- cally (fundatrix). Several aphid species and strains duce winged females which fly to the secondary host. of species reproduce parthenogenetically all year Some morphs appear in a particular season. The round (anholocycle). Host alternation is another gynopara appear in fall, producing sexually repro- characteristic of aphids. Most alternate between ducing females (ovipara) which lay overwintering host plants belonging to different families. Overwin- eggs. The males also appears in fall, and mate with tering eggs are deposited on one host (the primary the ovipara. The fundatrix appears in spring. In host), while nymphs of the parthenogenetically re- some species, the parthenogenetic female produces producing generation are on another host (the sec- both ovipara and male (sexupara). Aphid life cycles ondary host, usually the summer one). However, are complex because of their range of hosts and their some aphid species do not change their hosts, and polymorphism.

2 Fig. 1. CTV transmission by T. citricidus. Circles show observed data and the line is Y = 1­exp (­np) when n = number of aphids, p = transmissibility by one aphid (= 0.04).

Fig. 2. The life cycle of aphids

3 Life Cycles of Major Citrus Aphids A. spiraecola

T. citricidus This aphid may be holocyclic (North America and Japan) or anholocyclic. In Japan, citrus This aphid has holocyclic and anholocyclic is one of the primary hosts (Komazaki et al. 1979) for life-cycles. In Japan, the aphid overwinters one type, and can be distinguished from another type holocyclically on citrus (Komazaki et al. 1979), but which overwinters on spirea (Komazaki 1983). The overwintering eggs have not been found in other former attacks mainly citrus, and the latter attacks countries (Blackman and Eastop 1984). Host plants other fruit trees belonging the family are almost completely restricted to species belong- (Komazaki 1990). The two types can also be distin- ing to the family Rhutacea. guished by the esterase banding patterns when elec- trophoresis is carried out (Komazaki 1991). This T. aurantii aphid is polyphagous.

This species is almost completely Seasonal Occurrence of Major Citrus anholocyclic. This aphid has a wide host range, and Aphids in Japan in Japan, overwintering eggs have been reported on tea. The three most important citrus aphid spe- cies in Japan are T. citricidus, A. spiraecola and A. A. gossypii gossypii. T. aurantii also attacks citrus, but does not do serious damage (Table 2). These three major The taxonomic status of this species is aphid species occur continuously on citrus from complicated. In Europe, it is distinguished from the spring to fall (Fig. 3) and overwinter on citrus as Aphis frangulae group by the absence of sexual eggs. A. gossypii appears on citrus first in the spring, reproduction (Thomas 1968). In East Asia, Japan followed by A. spiraecola, and finally T. citricidus. and China, however, it has a holocyclic life-cycle in The early appearance of A. gossypii is explained by addition to an anholocyclic one (Komazaki 1979), the fact that the aphid has a wide range of overwin- Inaizumi 1980; Zhang and Zhong 1990). Primary tering hosts other than citrus, such as vegetables and hosts belong to four families, and parthenogenetic weeds, on which it overwinters parthenogenetically. overwintering populations are reported from Japan The role of the citrus overwintering population in (Inaizumi 1980). It is a highly polyphagous species. spring infestation may be comparatively slight, be-

Table 2. Citrus aphid species and their occurrence in Japan

4 cause the invasion from other hosts begins earlier affect its distribution. T. citricidus and A. spiraecola than the appearance of alates among populations realize their maximum increase at 27°C, while opti- overwintering on citrus (Fig. 3). In the case of A. mum temperatures for A. gossypii are 22 or 23°C spiraecola, the appearance of alates in populations (Komazaki 1982). The aphids increase on young overwintering on citrus is earlier than, or occurs at shoots, so their numbers also depend on the number the same time as, the occurrence of invasion. This of new shoots (Komazaki 1981). The range in means that the population overwintering on citrus is annual fluctuations is large in the case of A. spiraecola, an important source of infestation in spring. This is but relatively small for T. citricidus and A. gossypii supported by the fact that migrants from spirea (Komazaki et al. 1985). These fluctuations are plants cannot reproduce well on citrus (Komazaki brought about by the availability of new shoots, 1991). In the case of T. citricidus, a late egg hatch, climatic conditions and the activity of natural en- and the fact that only a few overwintering eggs are emies. found on citrus, result in a delay in spring infestation. Many natural enemies attack citrus aphids, The population of A. spiraecola increases and may sometimes be abundant. The from March to August, and then begins to decrease Lysiphlebus japonicus attacks the three main aphid (Fig. 4). A. gossypii peaks in late May, then popu- species, especially T. citricidus. The coccinellid lations fall, to rise again to a second peak in Septem- Scymnus hilalis also attacks these aphids, especially ber. T. citricidus peaks between July and Septem- A. spiraecola. Many other species, including Syr- ber. The capacity of this species to increase may phids, Crysopids and mites, are also known to attack

Fig. 3. Developmental processes of three major citrus aphids, beginning with overwintering eggs (or time of first infestation on trees for populations that do not overwinter).

Source: Komazaki 1983

5 Fig. 4. Seasonal occurrence of major citrus aphids Source: Komazaki et al. 1985

citrus aphids. It is true that natural enemies have an the virus. In the same way, many alates appear in important role in controlling aphid populations. summer and disperse the virus. It has been noted that However, they generally appear after aphid popula- T. citricidus is restricted to citrus hosts and migrates tions have already become high, so that by the time only between citrus trees, which increases the possi- they act as control agents the citrus trees have bility of virus spread. In contrast, A. gossypii has already been damaged. Because virus transmission many host plants, and only a small percentage of the occurs a short time after infestation by aphids, natu- aphids transmit CTV (Ieki 1986) A. gossypii is not ral enemies cannot prevent the spread of virus dis- very important as a CTV vector, and A. spiraecola ease. does not transmit CTV at all (Ieki 1986).

SPREAD OF VIRUS IN JAPAN CONTROL

The aphid T. citricidus is a highly efficient Natural enemies cannot prevent virus trans- vector of CTV in Japan, transmitting it in a semi- mission, for the reasons explained above. Nor can persistent manner. The aphid overwinters on citrus repeated spraying suppress aphid populations at a trees in the form of eggs. Parthenogenetic females low level, because winged aphids continuously re- cannot survive during the winter, because of the lack colonize citrus trees, and insecticide sprays do not of new shoots on citrus trees. In spring, the eggs remain active for long on growing shoots. If insec- hatch and aphids reproduce parthenogenetically. ticide were to take effect quickly and remain for a The aphid population does not increase very much in long time, aphids and CTV disease could be con- the first and second generations, during which time trolled, because CTV is transmitted in a semi-persis- a small number of alates appear and the aphids tent manner. However in practice, there are several scarcely move from the tree on which they have difficulties: overwintered. In the third generation, many alate • Determining the timing of spray applica- aphids appear and disperse to other citrus trees. tions is very difficult, because insecticide Alate aphids spend the teneral period (one or two should be applied at an early stage of days after the final molt), on the host plant where the spring flush, and flushing of shoots they have developed. If the overwintering host is of different trees within a orchard is not infected with virus, they acquire virus during this synchronized. period and fly to other hosts to which they transmit • Aphid occurrence cannot be precisely 6 predicted. Hosoda, A., H. Hama, K. Suzuki and Y. • Citrus trees are a perennial crop, and Ando. 1992. Insecticide resistance in are attacked by aphids repeatedly. cotton aphid, Aphis gossypii Glover • Insecticide resistance has developed in A. (Homoptera: Aphididae) I. Aliesterase ac- gossypii (Furk et al. 1980, Sun et al tivity and organophosphorus-susceptibility 1987, Takada and Murakami 1988, Saito of populations on and cucum- 1991, Hosoda et al. 1992) and probably bers. Japanese Journal of Applied Ento- also in A. spiraecola. Resistance to or- mology and Zoology 36: 101-111. (In ganophosphates, carbamates and pyre- Japanese with English summary). throids has developed in A. gossypii, and Ieki, H. 1986. Transmission of citrus insecticide application is not a recom- tristeza virus by the melon aphid, Aphis mended way of controlling this aphid gossypii. Annals of the Phytopathological and the virus disease it transmits. Society of Japan 52: 511. (In Japanese). Cross-protection with mild strains of Ieki, H. 1989. The use of cross-protection CTV may be a practical and effective with mild strains of citrus cristeza virus method (Ieki 1989). (CTV) to control stem pitting disease of citrus in Japan. In: Virus Diseases of Citrus. 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8 mental studies on some aphid life-cycle Interactions, R.K. Campbell and R.D. patterns and the hybridization of two sib- Eikenbary (eds.). Elsevier, Amsterdam, ling species. In: Aphid-Plant Genotype Netherlands, pp. 37-50.

DISCUSSION

Dr. Choi asked for more information on the natural enemies of the citrus aphids. Dr. Komazaki explained that there are some species of parasitoid which have a wide host range but which mainly attack citrus aphids. The rate of predation had not yet been studied very much, but Coccinella spp. (ladybugs) and other predator species are abundant in Japan in summer, while Circad spp. () may also be abundant under favorable conditions.

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