Toxoptera citricidus (Kirkaldy, 1907) (Homoptera, Aphidoidea), the tropical citrus aphid in continental Portugal

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1 Toxopter citricidus (Kirkldy, 1907) (Homopter, Aphidoide), the tropicl citrus phid in continentl Portugl Ilhrco F.A., Sous-Silv C.R. in D'Onghi A.M. (ed.), Djelouh K. (ed.), Roistcher C.N. (ed.). Citrus tristez virus nd Toxopter citricidus: serious thret to the Mediterrnen citrus industry Bri : CIHEAM Options Méditerrnéennes : Série B. Etudes et Recherches; n pges Article ville on line / Article disponile en ligne à l dresse : To cite this rticle / Pour citer cet rticle Ilhrco F.A., Sous-Silv C.R. Toxopter citricidus ( Kirkldy, 1907) ( Homopter, Aphidoide), the tropicl citrus phid in continentl Portugl. In : D'Onghi A.M. (ed.), Djelouh K. (ed.), Roistcher C.N. (ed.). Citrus tristez virus nd Toxopter citricidus: serious thret to the Mediterrnen citrus industry. Bri : CIHEAM, p (Options Méditerrnéennes : Série B. Etudes et Recherches; n. 65)

2 Toxopter citricidus (Kirkldy, 1907) (Homopter, Aphidoide), the tropicl citrus phid in continentl Portugl Ilhrco F. A. 1, Sous-Silv C. R. 2 1 Deprtmento de Protecção de Plnts, Entomologi Estção Agronómic Ncionl, Portugl 2 Universidde Federl de São Crlos, Deprtmento de Ecologi e Biologi Evolutiv São Crlos, Brsil Astrct. Surveys iming to detect the presence of T. citricidus in Portugl minlnd hve een crried out since The phid ws detected for the irst time in Mdeir Islnd in 1994 nd in the minlnd in 2003, in the north western region. In the yers tht followed the phid could e lwys detected, nd in some plces even in the winter months. The infested re is slowly enlrging. The preferred host is C. lemon. Predtors nd prsitoids re present in the period of popultion growth. A mcroscopic key is presented for the identiiction of the economiclly importnt Citrus phids in Portugl. Keywords. Aphids Citrus Portugl Toxopter citricidus Tristez Toxopter citrcidus (Kirkldy, 1907) (Homopter, Aphidoide), Le puceron tropicl des grumes dns le Portugl continentl Résumé. A prtir de 1963, des enquêtes ont été rélisées in de déceler le T. citricidus dns le Portugl continentl. Ce puceron été signlé pour l première fois sur l île de Mdère en 1994 et, en 2003, sur le territoire continentl dns le nord-ouest. Ensuite, le puceron continué d être signlé et dns certins endroits, il été mis en évidence ussi pendnt l hiver. L zone d infesttion s étend progressivement et le C. lemon reste l hôte préféré. Les prédteurs et prsitoïdes sont présents pendnt toute l période de croissnce de l popultion du puceron. Une clé mcroscopique est proposée pour fciliter l identiiction des pucerons des grumes économiquement importnts u Portugl. Mots-clés. Pucerons Agrumes Portugl Toxopter citricidus Tristez. I Historicl review The irst survey on T. citricidus in Portugl ws crried out in 1963, in the griculturl res of Coimr, Sntrém, Setúl, nd Algrve (Neves, 1965) nd, fterwrds y Ilhrco (1978), lso in the Algrve province. On those occsions, the phid ws not found T. citricidus ws reported in Mdeir Islnd (Aguir et l., 1994). The efforts to erdicte it were unsuccessful due to its fst dissemintion in the Citrus growing res of the islnd nd it ws considered to constitute potentil thret to Citrus orchrds in Continentl Portugl. New serch for the phid in the minlnd ws crried out. Cruz de Boelpepe nd Ferreir (1998) conducted surveys in the Citrus growing res from the Agriculturl Regions of Entre Douro e Minho, Beir Litorl nd Ritejo nd Oeste, in the Northern, centrl nd centrlsouthern re of Portugl, respectively. From 1997 to 1999 surveys of T. citricidus were done lso in Algrve (Rmos et l., 2000), without cptures. The phid ws detected on neither occsions T. citricidus ws reported in North Western Portugl in the Entre Douro e Minho region nd, in Spin, in Astúris nd Vigo (Ilhrco et l., 2005) Vrious surveys were done to evlute the dispersion of T. citricidus in continentl Portugl in citrus nd in other plnt species nd to check the ction of their nturl enemies. Options Méditerrnéennes, B n 65, Citrus Tristez Virus nd Toxopter citricidus: serious thret to the Mediterrnen citrus industry

3 Toxopter citricidus ws collected directly from the Citrus plnts or y yellow wter trps; smll citrus orchrds were inspected, long with single ckyrd plnts or ornmentl citrus in towns, other neighouring plnt species were lso inspected. The phid identiiction ws mde in the ield, ided y mgnifying lenses, or in the lortory, if it ws necessry. Smples cught y trps were identiied under stereoscopic microscope nd nominted vgrnts. In 2004, Toxopter citricidus ws cught in Vlenç, Monção, Vil Verde, Amres, Brcelos, Brg, Vil Nov de Fmlicão, Guimrães, Ffe, Snto Tirso, Felgueirs, Celorico de Bsto, Amrnte, Peniel, Mrco de Cnveses nd Snt Mrt de Penguião. In 2005, in Vil do Conde, Pços de Ferreir, Lousd, Vil Nov de Gi, Espinho, Ovr nd Ílhvo nd in 2006, in Arcos de Vldevez, Vin do Cstelo, Ponte de Lim, Ponte d Brc, Terrs de Bouro, Esposende, Vieir do Minho, Póvo de Lnhoso, Gondomr, Aveiro nd Estrrej (Fig. 1). Figure1. Dispersion of Toxopter citricidus (Kirkldy), in Continentl Portugl. The coloured res on the mp re relted to the res where the phid ws irstly designted. In this period, the limits of T. citricidus dispersion in Continentl Portugl re Vlenç nd Monção in the north, Ílhvo in south, nd Snt Mrt de Penguião in the est, nd its presence ws checked ll over the yer (T. 1). This shows the cpcity to resist the therml vritions from winter to summer in the studied re. Blckmn nd Estop (2000) hve mentioned tht lthough T. citricidus develops etter in hot wether, it cn, pprently, tolerte low tempertures etter thn T. urntii (Boyer de Fonscolome, 1841), which is well-dpted species in Portugl. Tle 1. Toxopter citricidus survey in the continentl Portugl in the period Yer/ Month J F M A M J J A S O N D x x x x x x x x 2005 x - x x x x x x 2006 x x 0 x x x x x: presence of T. citricidus -: month without survey 0: sence of T. citricidus J-D: Jnury Decemer My nd June/2004: Smples cught y trps (vgrnt phids) In 2005, from Ferury to April only one pterous T. citricidus ws cught on Citrus urntium L., nd one lte phid on Citrus sinensis (L.) lthough it ws oserved tht lemon trees hd suitle folige for the phids ll the yer round in opposition to ornge trees. 54 Options Méditerrnéennes B 65

4 In 2006, during Mrch nd erly April, no T. citricidus specimen ws found. However, in the surveyed loctions the plnts hd received phytosnitry tretments ginst phids. In lter April, 2006, in Guimrães region lrge popultion ws oserved on single lemon tree tht hd not received ny phytosnitry tretment. This suggests tht the isolted hosts cn ecome focus of phid dispersion when wether nd citrus folige conditions meliorte. This could explin the gret mount of T. citricidus cught lter in My, 2006, in the sme res where in the previous month the phids were lmost sent. Proly during Ferury-April, the dverse conditions, plus the snitry tretments, cn e responsile for the decrese in the phid popultions in the studied res. Prticulrly in the ornge tree, the lck of suitle folige is n dditionl fctor ffecting dversely the development of T. citricidus popultion. During the period of popultion growth some nturl enemies, predtors nd prsitoids were oserved (Fig. 2, 3). Michud (1998) reports n extensive literture out this. T. citricidus hs een collected on Citrus only, prticulrly in C. limon (over 60% of the smples). When lrge popultions develop the phids my e oserved lso on the top twigs nd lowers (Fig. 4). c d e f Figure 2. T. citricidus predtors: ) Syrphids; ) Cecidomiids; c, d, e,) Coccinellids; f) Chrysopids (Photogrphs y C. R. Sous-Silv). Figure 3. Mummiied T. citrici dus. (Photogrphs y C. R. Sous-Silv). Figure 4. T. citricidus (Kirkldy) on Citrus limon: ) long the veins; ) on the lowers. (Photogrphs y C. R. Sous-Silv). Citrus Tristez Virus nd Toxopter citricidus: serious thret to the Mediterrnen citrus industry 55

5 Bsed on Ilhrco nd Fonsec (1985) mcroscopic key is presented for the identiiction of the economiclly importnt Citrus phids in Portugl: Apterous forms: 1 Body green, yellow- green or rowned 2 - Body drk reddish-rown or shining lck 3 2 Body green to yellow-green. Cud s drk s the siphunculi Aphis spirecol Ptch (Fig. 5) - Body green, yellow-green or rowned. Cud lighter thn Aphis gossypii Glover (Fig. 6, ) siphunculi - Body light-yellow with some dorsl drk mrkings. Generlly smll insects Myzus orntus Ling (Fig. 7) 3 Body drk-rown. Apex of ntennl segments III, IV nd V, the picl hlf of se of VI nd some times lso the pex of Toxopter urntii (Boyer de Fonscolome) (Fig. 8) processus terminlis drk - Body reddish-rown or shining lck. Antennl segment III nd the sl prt of IV ple, V nd VI drk Toxopter citricidus (Kirkldy) (Fig. 9) Alte forms: 1 Adomen green, yellow-green or rowned, with or without 2 compct dorsl plte rowned to lck - Adomen drk-rowned, reddish-rown to drk or shining lck 4 2 Adomen light-green to ple-yellow with compct dorsl plte. Myzus orntus Ling (Fig. 7) Hed nd thorx rowned - Adomen without dorsl plte 3 3 Adomen green to yellow-green. Hed nd thorx lck, cud Aphis spirecol Ptch (Fig. 5) s drk s the siphunculi - Adomen yellow-lighted to drk or rowned green with lck stripe etween the siphunculi. Cud ple or lighted drk, lighter thn the siphunculi Aphis gossypii Glover (Fig.6c) 4 Adomen drk-rowned, fore wings with medin vein lmost lwys once rnched, pterostigm lck. Antennl segment III Toxopter urntii (Boyer de Fonscolome) (Fig. 8) ple with lck pex - Adomen drk reddish-rown or shining lck with smooth, Toxopter citricidus (Kirkldy) (Fig. 9) polished, shining cuticulr surfce, fore wings with medin vein usully twice rnched, pterostigm ple, ntennl segment III lck, in contrst with sl hlf of segments IV nd V, whicht re ple 56 Options Méditerrnéennes B 65

6 Figure 5. Aphis spirecol: ) pterous; ) lte. (Ilhrco nd Fonsec, 1985). c Figure 6. A. gossypii: ) pterous, summer form; ) pterous, winter form; c) lte. (fter Ilhrco nd Fonsec, 1985). Figure 7. Myzus orntus: ) pterous; ) lte. (Ilhrco nd Fonsec, 1985). Figure 8. T. urntii: ) pterous; ) lte (Ilhrco nd Fonsec, 1985). Figure 9. T. citricidus: ) pterous; ) lte. (Ilhrco nd Fonsec, 1985). Citrus Tristez Virus nd Toxopter citricidus: serious thret to the Mediterrnen citrus industry 57

7 II Conclusions i. T. citricidus is lredy well estlished in the north of Continentl Portugl, nd hs een collected ll the yer round. ii. Citrus limon is there the preferentil host of T. citricidus. iii. T. citricidus ws collected only on Citrus hosts. iv. Single lemon trees tht do not receive ny snitry tretment hve n importnt role in mintining T. citricidus popultions during the winter period. References Aguir A.M.F., Fernndes A., Ilhrco F.A., On the sudden ppernce nd spred of the lck citrus phid Toxopter citricidus (Kirkldy), (Homopter: Aphidoide) on the Islnd of Mdeir. Bocgin 168: 1-7. Blckmn R.L. nd Estop V.F., Aphids on the World s Crops. An identiiction nd informtion guide. 2nd ed. John Wiley nd Sons, Chichester, 466 pp. Cruz de Boelpepe M. O., Ferreir M.O., Survey of the rown citrus phid, Toxopter citricidus, nd other phid vectors of citrus tristez virus in Continentl Portugl. Aphids in nturl nd mnged ecosystems (Nieto Nfri, J.M. nd Dixon, A.F.G. eds.), Universidde de Léon (Spin). 1998: Ilhrco F.A., Prospecção de fídeos em citrinos no sul de Portugl (Homopter: Aphidoide). Agronomi Lusitn 38 (4): Ilhrco F.A. nd Fonsec P.A., Identiicção de fídeos por vi mcroscópic. I. Afídeos dos citrinos. Instituto Ncionl de Investigção Agrári e de Extensão Rurl, Liso. Ilhrco F.A., Sous-Silv C.R., Álvrez A.A., First report on Toxopter citricidus (Kirkldy) in Spin nd Continentl Portugl (Homopter, Aphidoide). Agronomi Lusitn 51 (1): Michud J.P., A review of the literture on Toxopter citricidus (Kirkldy) (Homopter: Aphidide). Florid Entomologist 81 (1): Neves M., Inquérito sore Toxopter citricidus (Kirkldy) vector d grve doenç dos citrinos denomind <tristez>. Agricultur 25: Rmos N., Fernndes J.E., Reis J., Nolsco G., Afídeos vectores do vírus-d-tristez-dos-citrinos (CTV) no Algrve. Livro de Acts do Congresso Ncionl de Citricultur, Fro, Nov. 2000: Options Méditerrnéennes B 65

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