Biological control of Diaphorina citri in Guadeloupe Original article Biological control of Diaphorina citri (Hemiptera: Psyllidae) in Guadeloupe by imported Tamarixia radiata (Hymenoptera: Eulophidae) Jean Étiennea*, Serge Quilicib, Daniel Marivala, Antoine Franckb a Inra-URPV, Biological control of Diaphorina citri (Hemiptera: Psyllidae) Domaine Duclos, in Guadeloupe by imported Tamarixia radiata (Hymenoptera: Eulophidae). 97170 Petit-Bourg, Abstract — Introduction. The Asian citrus psyllid, Diaphorina citri Kuwayama, is particu- Guadeloupe, France larly harmful to citrus plantations as it is one of the two psyllid vectors of the citrus greening b disease or Huanglongbing. This disease, which limits the longevity of trees, is due to an intra- Cirad Réunion, cellular bacterium which mainly affects the phloem. Past experience of biological control Pôle de Protection des Plantes, of D. citri in Reunion Island. In Reunion Island, this disease, detected in 1967, was the main 7 Chemin de L’Irat, obstacle to the development of the cultivation of citrus fruit. Control of the vector D. citri, by 97410 Saint-Pierre, introducing from India and multiplying on site the specific parasitoid Tamarixia radiata La Réunion, France (Waterston), was carried out during 1978 when nearly 4600 adult parasitoids were released. The success of T. radiata combined with the distribution of healthy plant material was at the [email protected] origin of the revival of the cultivation of citrus fruit in Reunion Island. Programme for a [email protected] biological control of D. citri in Guadeloupe. In Guadeloupe, D. citri was reported in Jan- uary 1998. No trace of insect parasitism was found and only one fungus, Hirsutella citriformis Speare, proved, under certain conditions, capable of regulating the populations of this psyl- lid. Taking into account the experience in Reunion Island and that the greening disease has not shown up in Guadeloupe, the introduction of T. radiata from Reunion Island was made in January 1999. About 1000 T. radiata were released all over the Guadeloupe islands. At pres- ent, just a little more than 1 year after the last releases, the parasitoid is established and pres- ent in almost all the citrus orchards where psyllid populations have decreased considerably. Quite favorable biological characteristics play a great part in explaining the excellent effec- tiveness of T. radiata in biological control programmes against D. citri. France (Reunion) / France (Guadeloupe) / Citrus / Diaphorina citri / Tamarixia radiata / insect control / biological control organisms Contrôle biologique de Diaphorina citri (Hemiptera : Psyllidae) en Guadeloupe par importation de Tamarixia radiata (Hymenoptera : Eulophidae). Résumé — Introduction. Le psylle asiatique des agrumes Diaphorina citri Kuwayama est particulièrement dangereux pour les plantations d’agrumes car c'est l’un des deux psylles vec- teurs de la maladie du greening des agrumes ou Huanglongbing. Cette maladie, qui limite la longévité des arbres, est due à une bactérie intracellulaire qui affecte principalement le phloème. Expérience passée sur le contrôle biologique de D. citri à l’île de la Réunion. À l’île de la Réunion, le greening détecté en 1967 était l’obstacle principal du développement de la culture des agrumes. Le contrôle de son vecteur D. citri, par introduction à partir d’Inde et multiplication sur place de son parasitoïde spécifique Tamarixia radiata (Waterston), a été effectué en 1978 ; près de 4600 adultes du parasitoïde ont alors été dispersés. Le succès de T. radiata combiné avec la distribution de plants sains a été à l’origine de la renaissance de la culture des agrumes à l’île de la Réunion. Programme pour un contrôle biologique de D. citri à la Guadeloupe. La présence de D. citri en Guadeloupe a été rapportée pour la * Correspondence and reprints première fois en janvier 1998. Une enquête menée alors n’a révélé aucune trace de parasitisme d’insecte et seul un champignon, Hirsutella citriformis Speare, a prouvé, dans certaines condi- tions, être capable de contrôler les populations de ce psylle. À partir de l’expérience de l’île Received 6 June 2001 de la Réunion et en considérant le fait que la maladie du greening n’avait pas encore été détec- Accepted 26 July 2001 tée en Guadeloupe, une introduction de T. radiata à partir de l’île de la Réunion a été faite en janvier 1999. Environ 1000 adultes de T. radiata ont été libérés sur l’ensemble de la Gua- deloupe. Actuellement, à peine plus de 1 an après le dernier lâcher, le parasitoïde est bien établi et présent dans presque tous les vergers d’agrumes où les populations de psylles ont considérablement diminué. Les caractéristiques biologiques tout à fait favorables de l’insecte Fruits, 2001, vol. 56, p. 307–315 jouent un grand rôle pour expliquer l’excellente efficacité de T. radiata dans des programmes © 2001 Cirad/EDP Sciences de lutte biologique contre D. citri. All rights reserved France (Réunion) / France (Guadeloupe) / Citrus / Diaphorina citri / Tamarixia RESUMEN ESPAÑOL, p. 315 radiata / lutte anti-insecte / auxiliaire de lutte biologique Fruits, vol. 56 (5) 307 J. Étienne et al. 1. Introduction 2. Review of past experience of biological control of D. citri Citrus greening disease, or Huanglongbing, in Reunion island represents one of the major obstacles in cultivating citrus fruit in the numerous Asian In Reunion Island, citrus greening disease and African countries where it is present was first reported on the island by Moreira [1–4]. Indeed, plantations affected by this [22]. The following year, its presence was disease decline rapidly; their longevity is confirmed by experimentations of labora- reduced and thus incompatible with an eco- tory transmission and by observation in the nomic, profitable activity. Between 1960 field of the two species of psyllid vectors: and 1980, decisive studies were carried out T. erytreae and D. citri [23]. At that time, the aiming at a better understanding of this dis- populations of the African psyllid T. ery- ease and its vectors [5–7]. The disease was treae were particularly abundant on citrus shown to be an intracellular bacterium fruit in zones of high altitude while D. citri affecting principally the phloem [8–10] and was mainly localized in the dry and hot significant differences were found between regions of the leeward coast, at altitudes bacterial strains from Africa and Asia [11, generally below 500 m. While the control 12], the latter having been characterized of the psyllid vectors was mainly achieved and named recently as Liberobacter asi- by intensive chemical spraying, Catling [24] aticum [13, 14]. suggested the introduction of parasitoids The specific vectors of this disease are originating from the same country as these two psyllid species found initially in two psyllids. This was the option chosen in distinct regions [15]. One species, Diapho- Reunion Island from 1975 to 1980 [25]. rina citri Kuwayama (figure 1) originating T. erytreae was controlled in a spectacular from the eastern region, is present in South way by the introduction of the parasitoid East and Southern Asia; the other species, Tamarixia dryi (Waterston) (Hymenoptera: Trioza erytreae (Del Guercio) originating Eulophidae) from South Africa [26] and was from the Ethiopian region, is confined to totally eliminated in a few years from its zones of high altitude in tropical Africa [3]. habitat. The parasitoid’s survival depended The presence, at the same time, of the on a related species of host-psyllid [27]. For greening disease and its two vectors in the the purpose of this paper, we will review Indian Ocean islands of Reunion and Mau- mostly some aspects of the Asian psyllid ritius as well as in Saudi Arabia is most bioecology and its control by means of probably due to the transport of contami- Tamarixia radiata (Waterston). nated plants. The presence of the Asian Since the early work of Husain and Nath psyllid, D. citri, in the neotropical region [28], the biology of D. citri has been studied has likely the same origin. This psyllid is by Pande [7] and, more recently, by Tsai and now reported in Brazil [16, 17], Honduras Liu [29]. D. citri develops uniquely on plants [18], Uruguay [19] and just recently in of the Rutaceae family, mainly on Citrus spp. Guadeloupe [20], Florida [21] and Cuba in and Murraya spp. The adult is small in size 1999 (Fernandez1, pers. com.). Even though (2.8–3.2 mm), with a spotted grey body and the greening disease has not yet been forewings forming a roof over the abdomen. detected in the neotropical region, the pres- These semi-transparent wings are greyish in ence of the vector D. citri is a serious threat appearance with a brownish stripe starting to citrus plantations which cover wide areas at the top half and ending at the apex. The in this region. adults are quite mobile, they jump when The bacterium responsible for the green- they are disturbed and fly off readily. The ing disease may also be spread easily by the feeding posture is characteristic, the body grafting of budwoods collected on contam- forms an angle of 30° with the surface of the 1 C. Gonzalez Fernandez, Instituto de Investigaciones inated plants. The use of healthy plant mate- vegetation. Mating occurs generally 1 to 3 d de Cítricos y Frutales, rial makes it possible to avoid this type of after the emergence of the adults when con- Ministerio de Agricultura, Cuba) dissemination. ditions are favorable (presence of young 308 Fruits, vol. 56 (5) Biological control of Diaphorina citri in Guadeloupe Figure 1. Adult of the Asian citrus psyllid, Diaphorina citri (D. Vincenot, Suad / Cirad). Figure 2. Nymphs of Diaphorina citri on a citrus shoot, with characteristic honeydew excretion (D. Vincenot, Suad / Cirad). Figure 3. Figure 4. Adult of Tamarixia radiata, with mummies of Diaphorina citri nymphs, Nymph of Diaphorina citri infected by the entomopatho- on leaves of Murraya paniculata (A.