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Home , Euscelis, Muracciole, Spiroplasma citri

Epidemiology of citri in

P. Brun, S. Riolacci, R. Vogel, A. Fos, J. C. Vignault, J. Lallemand and J. M. BovC

ABSTRACT. The Neoaliturus (Circu1i;fer) haematoceps has been shown recently to be vector of . N haematoceps is present in Corsica and its distribution on the island has been surveyed. While the leafhopper extends from the coastal dune vegetation up to the "maquis" covered hills and mountains of the interior, it has never been found in citrus orchards. Several host plants of this leafhopper have been identified. S. citri-infected N. haematoceps have been found at certain times in various areas of the east coast of Corsica. N. haematoceps individuals naturally infected with S. citri are able to transmit the causal agent of stubborn to periwinkle plants, but transmission to citrus seedlings has not yet been attained. Wild host plants harboring S. citri are being sought.

The leafhopper, Neoaliturus Detection of S. citri in field-col- haematoceps Mulsant & Rey, is pres- lected or plants was conducted ent in Corsica (I), as well as other by enzyme-linked immunosorbent countries of the Mediterranean area assay (ELISA) and by culturing the (4), and has been collected recently mycoplasma on artificial media (2,7). from different sites on the island. In some wild vegetation areas, as Since this leafhopper is a vector of well as in the citrus mother blocks of Spiroplasrnu citri (3,5), and stubborn the San Giuliano Research Station, is an important disease for commer- periwinkles were used as indicator cial varieties of citrus in orchards or plant for natural transmission of S. in nurseries, it was necessary to in- citri. vestigate the status of the leafhopper and natural transmission of the dis- RESULTS AND DISCUSSION ease. Surveys were conducted in vari- In an attempt to find the leafhop- ous regions of the island in order to per N. haematoceps in Corsica, sur- collect and determine the veys were conducted in various re- occurrence of S. citri in both the in- gions of the island, along the coast or sect vector and its host plant. in the inland foothills. The main sur- vey took place in the oriental coastal MATERIAL AND METHODS area corresponding to the major localisation of commercial citrus or- Research on the presence of N. chards. Samples were obtained from haematoceps in various areas of Cor- citrus orchards (on trees or on ground sica has been done using a portable weeds), and in other crops, along D-Vac suction sampler (D-Vac Corp., roads, or from natural vegetation. Riverside, Calif., U.S.A.) with a 33- The different localities, where N. cm-diameter intake. Samples with the haematoceps was collected are indi- D-Vac were made by placing the col- cated in table 1. In the north zone, as lecting cone as close as possible to the well as in the inland valleys, the pop- ground vegetation or pressed to the ulations were very low and each lo- ground over the vegetation for a few cation gave only few individuals (1 seconds. For sampling bushes, the to 5 adults). In the other areas, collecting cone was placed near the the leafhopper population of N. canopy and then swept up and down. haematoceps was frequently low and Leafhopper samples were sorted only in some locations did the number according to species (6) using a of individuals rise to 10 or 50, or stereomicroscope after anesthesia sometimes up to 100 adults. The with COz. "high-level" populations were located Diseases Induced by Proearyotic Pathogens 301

TABLE 1 SITES SAMPLED FOR THE OCCURRENCE OF NEOALZTURUS HAEMATOCEPS IN CORSICA

No. sites Area Location sampled - -- North zone Arena - -Marana - San Stefano () Occidental coast Ile Rousse - Stareso - Galeria 9 Interior valleys Corte - - -Ponte Leccia 6 East coast and Bravone - Linguizetta -Aleria - - Oriental plain Diane -Alzitone - Rottani 58 South zone Balistra -Ventilegne -Monaccia - Ortolo (Bonifacio) on the East coast (Bravone-Lin- round from these coastal dunes. Occa- guizetta-Diane) or in the South zone sional fluctuations of populations may (Balistra-Monaccia). at times lead to a complete disappear- Adults were the main stages col- ance of the leafhopper as in 1985 at lected during our survey; larvae were the Diane and Bravone sites. very scarce and some were collected Behind these coastal dunes exists only in places where relatively high another type of vegetation covering population levels were found. We the hills and very well represented in noticed that adults of N. haematoceps Corsica. The composition of this typi- were present all year round. Over- cal vegetation called "maquis" is indi- wintering stages were predominantly cated in table 3. Within the maquis, females. N. haematoceps, is found only in In Corsica, N. haematoceps can be sunny places where the soil is very collected in two typical places-near poor, sandy, and dry in summer with the seaside on sandy coastal dunes sparse vegetation. It is possible to and inland in typical vegetation called collect adults from the sunny side of "maquis". Within established citrus pathways in the "maquis", but not orchards in the oriental plain, it has from the shaded side. As a whole, N. never been possible to recover N. haematoceps populations are low in haematoceps. On sandy dunes, N. the "maquis" and most frequently few haematoceps is collected in places co- vered with different weeds as shown TABLE 2 in table 2. Among these weeds, MAIN WEED SPECIES FOUND IN THE Matthiola sinmta R. Br., is well rep- EASTERN COASTAL DUNES OF resented on the dunes and is found all CORSICA year round. This plant is the prefer- SPECIES FAMILY red host for N. haematoceps in this situation; it breeds actively on M. Pycnocmn rutaefolium L. Dipsacaceae Anthemis maritima L. Compositeae sinuata. Adult females lay eggs in the Silene nieaeensis All. Caryophyllaceae midrib of leaves or near the margin of Cyrwdon dactylon Pers. Gramineae the blades. Young larvae and adults Agropymm junceum P. B. Gramineae are able to feed on leaves and stems Avena barbata L. Gramineae in spite of the dense trichomes cover- Lagurus ovatus L. Gramineae Crucianella maritima L. Rubiaceae ing these organs. Cakile maritima Scop. Crucifereae Salsola kali L. is also found Matthiola sinuata R. Br. Crucifereae in coastal dunes on bare sandy Asphodelus aestivus L. Liliaceae places near the sea, and also sup- Plantago coronopus L. Plantagineae Eryngium maritimum L. Umbellifereae ports leafhopper populations. N. Salsola kali L. Chenopodiaceae haematoceps can be collected year 302 Tenth ZOCV Conference

TABLE 3 Comparison between species col- MAIN PLANT SPECIES IN THE lected in association with N. "MAQUIS" REGION OF CORSICA haematoceps in other countries of SPECIES FAMILY the Mediterranean area (Morocco, Syria, Turkey) indicates that 44 Cistus monspelliensis L. Cistaceae species are similar in Corsica with Cistus salwiifolius L. Cistaceae some differences in frequency and Lavandula stoechas L. Labiateae Erica arborea L. Ericaceae abundance within species. Only one Erica scoparia L. Ericaceae species, is well represented with high Arbutus unedo L. Erieaceae population levels in Corsica: Phil- Genista Corsica D.C. Leguminoseae aenus spumrius L., which is not Znula viscosa Ait. Compositeae Logfia gallica L. Compositeae found in the other countries except Odontites lutea Rchb. Scrophulariaceae for small numbers in Morocco. In Cor- Myrtus communis L. Myrtaceae sica, two other Neoaliturus spe- Phyllerea angustqolia L. Oleaceae cies are also represented besides N. Brachypodium memosum Gramineae R. haematoceops. Very few adults of Briza maxima L. Gramineae Neoaliturus fenestratus Herris Rosmarinus officinalis L. Labiateae Schaeffer, have been collected inland. Neoaliturus tenellus Baker was col- lected in October 1986 for the first adults are collected from colonized time in Corsica, near the sea at Diane spots (10 to 50 individuals). on the east coast. A few adults were Leafhoppers, froghoppers, and collected mixed with N. hematoceps planthoppers associated with N. adults. hematoceps represent 58 genera and The search for S. citri in field-col- 93 different species. Table 4 indicates lected leafhoppers or plant hosts was the species most frequently collected carried out in the places where N. during the survey. hematoceps had been collected.

TABLE 4 PLANTHOPPERS, FROGHOPPERS AND LEAFHOPPERS COLLECTED IN ASSOCIATION WITH NEOALZTURUS HAEMATOCEPS IN CORSICA - - Fulgoroidea-Planthoppers Delphacidae Laodelphm striatellus Fallen. Toya propinqua Fieber. Ribautodelphax pungem Ribaut. Cicadoidea-Froghoppers Cercopidae Philaenus sp~mariusL. Neophilaenus campestris Fallen. Cicadellidae-Leafhoppers Agallinae Agallia ribauti Oss. Agallia venosa Foure. Austroagallia sinuuta M. R. Typhlocybinae Empoasca vitis Goethe. Ribautiana debilis D. Eupteryx (5 species). Eupelicinae Eupelix cuspidata F. Aphrodinae Exitianus capicola Stal. Aphrodes bicinctus Schrank. Selenocephaline Phlepsius spinulosus Wgn. Psammotettix (4 species). (4 species). Balclutha rosea Scott. Macrosteles quadripunctulatus Kbm. Macrosteles sexnotatus Fallen. Neoalitum fenestratus Herris Schaeffer. Neoaliturus tenellus Baker. Neoaliturus haematoceps Mulsant & Rey. Diseases Induced by Proearyotic Pathogens 303

Samples of weeds and bushes repre- fected with S. citri, have been tested senting the main botanical species many times at various seasons with- found in the "maquis" or in littoral out positive results. dunes were collected for S. citri de- Positive results with plants were tection. obtained only by artificial rearing on Of 566 samples (468 plants, and 98 host plants. Adults of N. haematoceps insects) analyzed with the ELISA naturally contaminated with S. citri procedure, or sampled for culturing and collected in autumn at three sites S. citri, only 19 insects and 15 plants on the oriental plain (Ventulella, Rot- gave positive results. Positive results tani, Alzitone), could transmit S. citri indicated that in Corsica N. to healthy plants of periwinkle grown haematoceps is the only species in- in the screenhouse. Until now, no fected with S. citri. The two other positive results have been obtained in species of Neoaliturus (N. fenes- transmission attempts to citrus seed- tratus and N. tenellus) gave negative lings. Since periwinkle is a very sensi- results. tive plant for detecting natural spread Males and adult females of N. of S. citri, periwinkles were estab- haematoceps are found to be naturally lished in "maquis (Rottani) for 2 infected with S. citri. Isolation of months in summer and for 8 months S. citri from field-collected adults of in a young grapefruit plantation sur- N. haematoceps was possible at any rounded by wild vegetation and lo- season of the year: from October, cated at 2 km from Ventulella. All of November, December, March to June these plants were negative for S. and August. Naturally infected citri. leafhoppers have been collected only Further research work is neces- in the "maquis" along the oriental sary for assessing the rate of trans- plain (Rottani, Ventulella, Bravone, mission of S. citri by vectors to Alzitone, , Abazzia) at spots citrus or wild plants. 2 to 12 km from the sea. The distance between the northern site (Ven- ACKNOWLEDGMENTS tulella) to the southern site is about We thank Mrs. M. Nicoli and Mr. 30 km. J. G. Borelli at the Station de Re- Plants representing the main cherche~ Agronomiques de San species growing in the "maquis" (20 Giuliano-Corsica, for their technical families, 34 genera and 36 species), assistance and M. M. Muracciole at and especially within delimited sites the Parc Natural Regional de la Corse where N. haematoceps is naturally in- for help in plant . LITERATURE CITED 1. Bonfils, J. and W. Della Giustinia 1978. Contribution a l'etude des Homopteres Auchenorhynques (Homoptera, Auchenor- rhyncha) de la Corse. Bull. Soc. Sci. Hist. Nat. de la Corse. 2"-?trim. 1978: 93-112. Bastia. 2. Bove, J. M., R. F. Whitcomb, and R. E. McCoy 1983. Culture technique for from plants, p. 225-234. In S. Razin and J. G. Tully (eds.). Methods in Mycoplasmology, Vol. 11. Academic Press, London, New York. 3. Fos, A., J. M. Bove, J. Lallemand, C. Saillard, J. C. Vignault, Y. Ali, P. Bmn, and R. Vogel 1986. La cicadelle Neoaliturus haematoceps (Mulsant & Rey) est vecteur de Spiroplasma citri en Mediterranee. Ann. Inst. Pasteur/Microbiol. 137A: 97-107. 4. Frazier, N. W. 1953. A survey of the Mediterranean region for the . J. Econ. Entomol. 46: 551-554. 5. Oldfield, G. N., G. H. Kaloostian, H. D. Pierce, A. L. Granett, and R. L. Blue 1976. Beet leafhopper transmits citrus stubborn disease. Calif. Agr. 30: 15. 6. Ribaut, M. 1952. Homopteres Auchenorhynques. 11. (Jassidae). Faune de . 57: 1-474. Lechevalier (ed.). 7. Saillard, C. and J. M. Bove 1983. Application of ELISA to spiroplasma detection and classification, p. 471-476. In S. Razin and J. G. Tully, (eds.). Methods in mycoplasmology, Vol. I. Academic Press, London, New York.