JARQ 28, 177 - 184 (1994)

Ecology of and Their Importance to Virus Transmission

Shinkichi KOMAZAKI* Okitsu Branch, Fruit Tree Research Station (Okitsu, Shimizu, Shizuoka, 424-02 Japan)

Abstract World species attacking citrus are reviewed. The 4 aphids, citricidus, T. aurantii, Aphis gossypii and A. spiraecola are the major species whereas other 11 species are less important. Their occurrence varies with the countries or districts. Aphid life cycle in general and that of the major 4 species are described. Ecology of and factors affecting the occurrence of 3 important citrus aphids in Japan are described and relations between aphid populations and some factors controlling aphid populations are outlined. Transmission of (CTV) is reviewed and transmission rate of T. citricidus and A gossypii is compared in relation to different strains of CTV or of aphids. All of 4 world important species can transmit CTV. Especially, T. citrici­ dus andA. gossypii are efficient vectors of CTV in different areas of the world.

Discipline: pest Additional keywords: Aphis gossypii, Aphis spiraecola, CTV, Toxoptera citricidus, Toxopt,e ra aurantii

attack citrus but they occur occasionally and World aphid species attacking citrus their populations are small.

Several aphid species attack citrus in the General biology of aphids 2 4 13 2 world • • • 2.JS.37). All belong to the family . Four important species i.nclude Fig. I depicts the aphid life-cycle. Aphid Toxoptera citricidus, Toxoptera auranlii, Aphis propagates parthenogenetically and partheno­ gossypii and Aphis spiraecola (Table 1). The genesis is linked to viviparity. Sexual and par­ species composition and seasonal occurrence thenogenetic reproduction alternates in the li fe differ in each area or country. T. citricidus cycle, which is referred to as cyclical partheno­ is not distributed in the Mediterranean region genesis. Usually, sexual forms appear in fall and North America. Other major 3 species and oviposit overwintering eggs on the primary show a worldwide distribution. A. spiraecola host. This phenomenon is referred to as invaded the Mediterranean region in the 1960s holocyclic life-cycle. Eggs hatch in spring and and became a serious citrus pest there35>. In hatched larvae develop to parthenogenetic Japan, T. aurantii is not a major species but reproducing mothers (fundatrix). Several aphid is abundant on tea 20>. Other 11 species also species or some strains of a species reproduce

• Present address: Akitsu Branch, Fruit Tree Research Station (Akitsu, Hiroshima, 729-24 Japan) 178 JARQ 28(3) 1994

Table I. Aphid species :attacking citrus in the world

Species Distribution Major species Toxoptera citricidus Asia, South Africa, Central and South America, Australia, New Zealand Toxoptera a11ra11tii Worldwide Aphis gossypii Worldwide A phis spiraecofa ( = A. cifricola) Worldwide

Minor species Aphis craccivora Worldwide Aphis fabae Almost worldwide Aphis nerii The O ld and New World tropics A11lacorthum magnoliae Japan, Korea, India A11/acorthu111 solani Worldwide Brachyu11g11is lwrmalae Israel, Sudan Brachycaudus helichrysi Worldwide Myzus persicae Wo rldwide Macrosiphwn euphorbiae Worldlwide Toxoptera odinae South and East Asia, South Africa Ureleucon jaceae Europe, the Middle East and Central Asia

6- 9 ~ ~ -Egg Male Oviparn Fundatrix ~r,tcrous A latc G)•llOJ>ara ' ' v1v,p;ira vivi1>arn Primary host

Heteroecious Autoecious Ho/ocyclic type Anholocyc/ic type

Fig. I. Outline of aphid life-cycle parthenogenetically all the year round (an­ overwintering host and the secondary host is holocyclic life-cycle). Host alternation is the summer host. The term heteroccious is used another characteristic of aphids. Aphids mi­ for the host alternating life-cycle. Some aphid grate among host plants of di ffcrent families. species do not change hosts and live on a plant Overwintering eggs are deposited on one host or a group of kin plants. This life-cycle is (primary host), and parthenogenetic reproduc­ designated as autoecious or monoecious. The ing generation occurs on another host (secon­ aphid li fe cycle is generally defined by two dary host). Usually, the primary host is the criteria, the appearance of sexual forms and Komazaki: Ecology of Citrus Aphids a11rl Their /111porta11ce to Virus Transmission 179 host alternation. Some aphid species, incl ud­ holocyclic JiJe-cycle in addition to an anholocy­ 12 19 38 ing A. gossypii, A. spiraeco/a and T. citrici­ clic one • • >. Primary hosts in 4 families dus, have both holocyclic and anholocyclic and parthcnogenetic overwintering populations strains. have been reported in Japan. This is a highly Aphids exhibit many morphs differing in polyphagous species and many biotypes or morphological and physiological character­ strains differing in host preference, Life-cycle istics 10>. Winged and wingless forms appear. pattern and level of resistance arc Winged parthenogenetic females (vivipara or segregated 9 .11 , 12 .Jo ,J2 ,J3,J8>. virginopara), disperse and look for new host (4) A. spiraecola plants while wingless parthenogenetic females The name of A. citricola has been used for (apterous vivipara) can quickly reproduce on more than 10 years after it was proposed by host plants. In the host alternating species, the East op and Hille Ris Lambers ( I 976) 7>. But, winged female migrates between primary and Eastop and Blackman reported in 1988 that A. secondary hosts. The fundatrix or its daugh­ citricola van der Ooot is a synonym of A. ter produces winged females that fly to tlhe fabae8>. Then the 11amc of A . spiraecola has secondary host. Some morphs appear in a par­ been used for the citrus-auacking green aphid. ticular season. The gynopara appears in fall This aphid is holocyclic in North America and and produces sexually reproducing female Japan or anholocyclic in other countries. In (ovipara), that produces overwintering eggs. Japan, citrus is one of the primary hosts 19> for The male also appears in fall and mates with one type and can be distinguished from another 151 the ovipara. The fundatrix appears in spring. type which overwinters on Spirea • The form­ In some species, the parthenogenetic Female er auacks mainly citrus and the latter attacks produces both ovipara and male. Aphid Life other fruit trees in 17>. The two types cycles are complicated due to the pattern and can also be distinguished by the esterase band­ polymorphism. ing pattern when electrophoresis is carried out 18>. This aphid is polyphagous. Life-cycles of major citrus aphids Seasonal occurrence of major citrus aphids (I) T. citricidus in Japan This apbjd shows holocyclic and anholocy­ clic life-cycles. In Japan, the aphid overw inters The 3 major citrus aphids in Japan are T. holocyclically on citrus 191 but overwintering 41 eggs have not been found in other couritries • Table 2. Citrus aphid species and their Host plants arc almost completely restricted rn occurrence in J apan the species in the family Rutacea. (2) T. aurantii Species Occurrence This species is almost completely anholocy­ Toxoptera citricidus All seasons clic. This aphid has a wide host range, and Aphis spiraecola All seasons overwintering eggs have been reported in Japan. Aphis gossypi i All seasons Toxoptera a1mmtii Spring to early summer•> (3) A. gossypii A 11/acor1h11111 111ag110/iae Spring to early summer•> T he taxonomic status of this species is com­ Aphis craccivora Spring to early summer•> plicated. In Europe, thi s aphid has been di.s­ Myzus persicae Spring to early surnmer•l tinguished from the A phis frangulae group by Aulaconhum solani Spring to early summer"' the absence of sexual reproduction34>. In East Si110111ego11ra citricola Occasional Asia, Japan and China, howeve r, it has a a): Occasional in other seasons. 180 JARQ 28(3) 1994 citricidus, A. spiraecola and A . gossypii. T. A. gossypii appears on citrus first, followed aurantii also attacks citrus but does not cause by A . spiraecola, and T. citricidus. The early serious damage (Table 2). These 3 aphid spe­ appearance of A. gossypii is attributed to the cies continuously occur on citrus from spring fact that the aphid has a wide range of hosts to fall (Fig. 2) and overwimer on citrus as eggs. other than citrus, such as vegetables and weeds, The other species occur only from spring to on which it overwinters parthenogenetically. early summer or occasionally. The role of the citrus overwimering population

100

0 10 0 .c.,, -"' "'·;:; N"\t', 0. ! •,' \.\f \\.. "' 0 z J ···.J··. A . gossypii

\,) 7 ,:;:;:;d,,, 0.1 r:1 May June July Aug. Sept. Oct.

Fig. 2. Seasonal occurrence of 3 major c.itrus aphids in Japan 20>

A. spiraecola 1977 ---- -A------~ ------­ '78 ---"1------4----~------'79 - --lCJ------1------'80 ---f:!1------,t.---1----

A. gossypii 1977'78 -_ -A---______--<1----_ -1------__....,..,______--_

'79 --H------1------'80 ------

T.citricidus 1977 ----A------1----- '78 ----- 4------1---­ '79 ------1--­ '80 -~-~-~ -~-~-~ -~-~-~--~ Mar. Apr. May June O : Time of egg hatch • : Time of the appearance of 2nd generation • ; Appearance of al ates o n trees with overwintering eggs • : Appearance of ala tes on trees without overwintering eggs

Fig. 3. Development processes of 3 major citrus aphids 13> Komazoki: Ecology of Citrus Aphids and Their lmport1111ce to Virus Tro11smissio11 181 in spring infestation may be comparatively alates among populations overwintering on negligible, because the invasion from other citrus (Fig. 3). In the case of A. spiraecola, hosts begins earlier than the appearance of the appearance of alates in populations over­ wintering on citrus is earlier than, or occurs o.s at the same time as the invasion. This 0.4 phenomenon suggests that the population over­ wintering on citrus is an important source of ~ 0.3 infestation in spring, which is supported by the :!2. ::. 0.2 fact that migrants from Spirea plants cannot ~ reproduce well on citrus 18>. ln the case of T. 0.1 citricidus, a late egg hatch, and the fact that 0 only a few overwintering eggs are found on 10 Temperature ( •c) citrus, result in a delay in spring infestation. o. T. citricidus, e : II . spiraeco/11 The population of A. spiraecola increases 6 : 11. g<>SSyf)ii from March to August and decreases after Au­ gust (Fig. 2). The population of A. gossypii fig. 4. Change of r with temperature 14> gives a peak in late May and decreases, and again, gives a peak in September. The popu­ lation of T. citricidus gives peaks in July and August or September. Their increasing capac­ ity may affect their pattern of occurrence. The maximum increase of the population of T. citricidus and A. spiraecola occurs at 27°C while that of A. gossypii at 22 or 23°C (Fig. 4). The population of the aphids can increase on young shoots and their numbers depend on the 13 Year amount of new shoots available >. The range • : II. spimec<>i<1. o: 7: citricidus of annual fluctuations is large in A. spiraecola <>: ii. f?OSS)'/lii but relatively small in T, citricidus and A. gos­ sypii (Fig. 5). These fluctuations are associat­ Fig. 5. Annual nuctuations of aphid populations20> ed with the amount of new shoots, climatic conditions and activity of natural enemies. 200 Many natural enemies attack citrus aphids. 100 Some natural enemies are occasionally abun­ 50 -+ dant. The , japonicus, ~,, e 20 allacks the 3 major aphid species, especially Eg 10 T. citricidus. The coccinellid, Scymnus hilalis, also attacks these aphids, especially A. spirae­ 0 5 z cola, while many other species, Syrphids, Crys­ 2 opids, mites are known to attack citrus aphids. I 3 10 30 100 300 1,000 3.000 10.000 Although it is assumed that natural enemies No. :iphids + I play an important role in the control of aphid Fig. 6. Relation between aphid (A. spiraecola) populations, since these natural enemies appear population and no. of parasitiz.ed mummies after the increase of the aphid population Arrows indicate time sequence. (Fig. 6), the effect of their control occurs after 182 JARQ 28(3) 1994

36 citrus has been damaged. strains3· '. Transmissibility of CTV by single aphid is listed in Table 4. T. citricidus is the 1 5 31 Virus transmission by citrus aphids most effective vector of CTV • • >. A. gos­ sypii which was not an effective vector pre­ The aphid species transmit.ting citrus tristeza viously6·23>, has now become a serious one in 26 virus (CTV) are listed in Table 3. CTV can the USA and Israel ·28l. A. spiraecola and only be transmitted by the aphids among the T. aurantii are much less effective vectors29> citrus viruses. The 4 important aphids previ­ except for T. aurantii in lndia21 >. In T. citric­ ously described can transmit CTV 1.s,i3 •31i. idus, there is no difference in the virus trans­ Other species can transmit CTV in South Asia. missibility between alate and apterous aphids, 5 Aphids transmit CTV in a semi-persistent man­ or between adults and nymphs ·31l. Similarly ner except in several cases in India and the adults and nymphs of A. gossypii can both 24 28 Philippines. Aphids can acquire CTV for 30 transmit the virus equally • >. min by feeding on a virus-infected plant and Transmission curve by T. citricidus is illus­ transmit it for 30 min by feeding on a healthy trated in Fig. 7, based on experimental data plant. Transmissibility increases when the feed­ using Mexican lime, and a 2-day feeding peri­ ing period lasts for 24 hr and aphids lose their od for acquisition and inoculation. Data are transmitting ability after 2-day feeding on a fitted to the formula Y = I-exp (-np), where healthy plant31> or a synthetic diet 16>. In South n is the number of aphids inoculated, and p Asia, aphids transmit the virus non-persistcnily is the average transmission rate of single aphid. in India, Thailand and the Philippines. In this In this formula, the transmissibility by single case, aphids acquire and transmit the virus by T. dtricidus is estimated at 0.04 (Fig. 7). feeding for a few seconds21 •27>. Another estimate 0.02 was calculated from the Transmissibility of the virus by aphids data reported by Costa and Grant (1951 ). For 25 29 11 varies with the aphid species • •• > and virus A. gossypii, the value was 0.03 according to the data reported by Roistacher et al. (1984) Table 3. Aphid species transmitting CTV (Table 4) and within the range 0.0! -0.1 1 ac­ 36 cording to other estimates '. The differences Worldwide South Asia in the virus strains and presumably the aphid Toxoptera citricidus Aphis craccivora Aphis gossypii Aphis /oboe 0.6 Aphis spiraecolo Aphis 11erii Toxoptera aurantii Acythosiphon piswn 0.5 Myzus persicae >. :: 0.4 Uro/eucon (Dacty1101us) 3 jaceoe :~ 0.3

ii:: 0.2 !- Table 4. Transmissibility of CTV by single aphid 0. 1

Species Transmissibility Reference 5 10 15 20 No. ~r> hitls per 1>lant T. citricidus 0.04 This paper 0.02 Costa & Grant, 195 1 Fig. 7. CTV transmission by T. cilricidus Raccah et 1980 A. gossypii 0.009 al., Circles show observed data and the O.o3 Roistachcr ct al. , 1984 regression line is Y = I-exp( - np), where Yokomi ct al., 1989 0.004 n = number of aphids inoculated, Manjunath, 1985 T. a11ra111ii 0.33 p = lransmissibility by one aphid. Kom"wkl: Ecology of Citrus Aphids and Their !111vorta11ce to Vin,s Tra11s111issio11 183 slrains may account for the inconsistency of tibility. Jpn. J. Appl. E111omol. Zoo/., 37, the transmissibili ty. 83-90 (In Japanese with English summary). T. citricidus is the most dangerous aphid in 12) lnaizumi, M. (1980): Studies on the li fe-cycle & polymorphism of Aphis gossypii Glover Japan as a vector of CTV due Lo its high trans­ (Homoptera, Aphididae). Special Bull. Coll. missibility and relalively narrow host range thal Agric. Uts1111omiya Univ., 37, I32pp. [In is exclusively restricted to citrus. In conLrast Japanese wi th English summary]. to T. citricidus, A. gossypii transmits CTV at 13) Komazaki, S. (1981): Life cycles and popula­ a low percentage and has many host plants so tion fluctuations of aphids on citrus. Pro. Int. that the importance of A. gossypii as a CTV Soc. Citricul. 1981, Tokyo, 2, 692-695. 14) Komazaki, S. (1982): Effects of constant tem­ vector is negligible. A. spiraecola does not peratures on population growth of three aphid transmit CTV. species, Toxoplera citricidus (Kirkaldy), Aphis citricola van der Goot and Aphis gossypii Glover (Homoptera: Aphididae) on citrus. Appl. £11- References tomol. Zoo/., 17, 75 - 81. 15) Komazaki, S. (1983): Overwintering of the l) Ahlawat, R. S. & Raychaudhuri, S. P. (1988) : spirea aphid, Aphis citricola van dcr Goot Status of citrus triste1.a and dieback diseases in (Homoptera: Aphididae) on citrus and spirea India and their detection. /11 Proceedings of the plants. Appl. Entomot. Zool., 18, 301-307. 6th International Citrus Congress, Tel Aviv, 16) Komazaki, S. (1984): Rearing of the brown 871 -879. citrus aphid, Toxoptera citricidus (Kirkaldy), 2) Barbagallo, S. (1966) : L'afido fauna degli agru­ (Homoptera : Aphididac), on a synthetic diet mi in Sicilia. Entomologica, 2, 201-260 with special reference to pH and sucrose con­ 3) Bar-Joseph, M. & Loebenstein, G. (1973): Ef­ centration of diet and rearing density. Appl. rects of strain, source plant, and temperature E11101110/. Zoo/., 19, 114- I 17. on the Lransmissibility of citrus tristeza virus by 17) Komazaki, S. (1990): Variation in the hatch the melon aphid. Phytopathology, 63, 716- 720. timing of the overwintering egg among popula­ 4) Blackman, R. L. & Eastop, V. F. (1984): Aphids tions of Aphis spiraecola Patch (Homop­ on the world's crops. John Wiley & Sons, tera: Aphididae) collected from different host Chichester, UK. 466pp. plants and localities in Japan. Appl. E111omol. 5) Costa, A. S. & Grant, T. J. (1951): Studies Zoo/., 25, 27-34. on transmission of the tristeza virus by the vec­ 18) Komazaki, S. (1991): Studies on the biology tor, A phis citricidus. Phytopathology, 4 1, of the spirea aphid, Aphis spiraecola Patch, with 105 - 113. special reference of biotypic differences. /11 Dull. 6) Dickson, R. C. M. ei al. ( 1956): Flying aphid Fruit Tree Res. Stn. (extra No.2), 60pp. (In populations in southern California citrus groves Japanese with English summary). and their relation to the transmission of the 19) Komazaki, S. et al. (J 979): Overwintering of tristeza virus. Phytopathology, 46, 204-210. aphids on citrus trees. Jpn. J. Appl. Entomol. 7) East op, V. F. & Hille Ris Lambers, D. (1976): Zoo!. , 23, 246-250 (In Japanese with English Survey of the world's aphids. W. Junk, Pub­ summary]. lishers, Hague, 573pp. 20) Komazaki, S. et al. (1985): Population dynam­ 8) Eastop, V. F. & Blackman, R. L. ( 1988): The ics of citrus aphids. I. Attacking species and identity of Aphis citricola van der Goot. Syst. seasonal and annual population trends. Bull. Entomol., 13, 157-160. Fruil Tree Res. Stn., 812 , 87-94 (In Japanese 9) furk, C. et al. (1980): Pirimicarb resistance in with English summary]. the melon and cotton aphid, Aphis gossypii 21) Manjunath, K. L. (1985): Studies on the dis­ Glover. Pla111 Pai/10/., 29, 191- 196. tribution, transmission, strains and strain inter­ 10) Hille Ris Lambers, D. (1966): Polymorphism action of citrus tristeza virus. z. Pfla11ze11kr. in Aphididae. Ann. Rev. Enlomol., 11 , 47-78. Pflanzensch., 92, 502-508. 11) Hosoda, A. et al. (1993) : Insecticide resistance 22) Niet Nafria, J.M. et al. (1984): Catalogo de of the cotton aphid, Aphis gossypii Glover. 111. los pulgoncs (Homoptera Aphidoidea) de Espana Host preference and organophosphorus suscep- y de sus plantas hospedadoras. Universidad de 184 JARQ 28(3) 1994

Leon serv1c10 de publicaciones, Leon, l 74pp. summary). 23) Norman, P. A. & Grant, T. J. (1956): Trans­ 32) Sun, Y. Q. et al. (1987): Biochemica.l mechan­ mission of tristeza virus by aphids in Florida. ism of resistance of cotton aphids to or­ Proc. Florida State Hort. Soc., 69, 39-42. ganophosphorus . Acta Entomol. 24) Norman, P.A. & Sutton, R. A. (1969): Effi­ Sinica, 30, 13-20. ciency or mature and immature melon 33) Takada, H. & Murakami, Y. (1988): Esterase aphids in transmitting tristeza virus. J. Econ. variation and insecticide resistance in Japanese Entomol., 62, 1237-1238. A phis gossypii. Entomol. Exp. Appl., 48, 25) Raccah, B. et al. (1977): Transmission of triste­ 37-41. za by aphids prevalent on citrus, and operation 34) Thomas, K. H. ( 1968): Die Blattlliusc aus dcr of the tristeza suppression program in Israel. engcren Verwandtschart von Aphis gossypii b1 Proceeding of 7th IOCV Conference, Athens, Glover und A. frangulae Kaltenbach unter be­ 47-49. sondcrcr Beriicksichtigung ihres Vorkomrnens an 26) Raccah, B. et al. (1980): Aphid-t.ransmissibility Kartoffel. Entomol. Abh. Staatl. Mus. Tierkd. variants of citrus tristeza virus in infected citrus in Dresden, 35, 337-389. trees. Pltytopatho/ogy, 70, 89-93. 35) Viggiani, G. (1988): Citrus pests in the Mediter­ 27) Retuerma, M. L. & Price, W. C. (1972): Evi­ ranean Basin. In Proceedings of the 6th Inter­ dence that tristeza virus is stylet-borne. FAO national Citrus Congress, 1067- 1073. Plant Prot. Bull., 20, 111- 114. 36) Yokomi, R. K. et al. (1989): Transmission of 28) Roistacher, C. N. et al. (1984): Transmission exotic citrus tristeza virus isolates by a Florida of tristcza and seedling yellows tristeza virus by colony of A phis gossypii. Plant Dis., 73, small populations of Aphis gossypii. Plant Dis., 552-556. 68, 494 - 496. 37) Yokomi, R. K. et al. (1992): Establishment of 29) Roistacher, C. N. & Bar-Joseph, M. (1989): Toxoptera citricidus (Homoptera: Aphididae) in Aphid transmission of CT virus. Citrograph, Central America. In Proceedings 14th Interna­ 74, 117-125. tional Congress of Entomology, 392. 30) Saito, T. (1993): Insecticide resistance of the 38) Zhang, G. X. & Zhong, T. S. {1990): Ex­ cotton aphid, Aphis gossypii Glover (Homop­ perimental studies on some aphid lifo-cyclc tera: Aphididae). VI. Qualitative variations or patterns and the hybridization of two sibling aliesLerase activity. Appl. Entomol. Zoo/., 28, species. /11 Aphid-plant genotype interactions. 263-264. eds. Campbell, R. K. & Eikenbary, R. D., 31) Sasaki, A. (1974): Studies on Hassaku dwarf. Elsevier, Amsterdam, 37-50. Special Bull. Fruit Tree Exp. Sm. Hiroshim<1 Pref., No. 2, 106pp. [ In Japanese with English (Received for publication, March 17, 1994)