A review of the invasion of Drosophila suzukii in Europe and a draft research agenda for integrated pest management

Bulletin of Insectology

Volumn 65, Issue 1, 2012, Pages 149-160

  Cini, Alessandro ^a,b   Ioriatti, Claudio ^a   Anfora, Gianfranco ^a  

^a RESEARCH AND INNOVATION CENTRE   (Italy)

^b UPMC University Paris 06   (France)

Author keywords

Berry fruit; Cherry fruit fly; Insect control; Invasive species; Spotted wing drosophila

Indexed keywords

DIPTERA; DROSOPHILA SUZUKII; DROSOPHILIDAE; HEXAPODA; RHAGOLETIS CINGULATA;

EID: 84860797136     PISSN: 17218861     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (103)

1. Amin Ud Din M., Mazhar K., Haque S., Ahmed M., 2005. A preliminary report on Drosophila fauna of Islamabad (Capital, Pakistan). Drosophila Information Service, 88: 6-7.
2. Antony C., Jallon J. M., 1982. The chemical basis for sex recognition in Drosophila melanogaster. Journal of Insect Physiology, 28: 873-880.
3. Barmina O., Kopp A., 2007. title typecontributorSex-specific expression of a Hox gene associated with rapid morphological evolution/title. Developmental Biology, 311: 277-286.
4. Baroffio C., Fischer S., 2011. Neue Bedrohung für Obst-plantagen und Beerenpflanzen: die Kirschessigfliege. UFA-Revue, 11: 46-47.
5. Bartelt R. J., Schaner A. M., Jackson L. L., 1985. title typecontributorCis-vaccenyl acetate as an aggregation pheromone in Drosophila melanogaster/title. Journal of Chemical Ecology, 11: 1747-1756.
6. Beers E. H., Van Steenwyk R. A., Shearer P. W., Coats W. W., Grant J. A., 2011. Developing Drosophila suzukii management programs for sweet cherry in the Western US. Pest Management Science, 67: 1386-1395.
7. Bock I. R., Wheeler M. R., 1972. The Drosophila melanogaster species group. University of Texas Publications, 7213: 1-102.
8. Bolda M. P, Goodhue R. E., Zalom F. G., 2010. Spotted wing drosophila: potential economic impact of a newly established pest. Agricultural and Resource Economics Update, Giannini Foundation of Agricultural Economics, University of California, 13 (3): 5-8.
9. th Annual Meeting, November 13-16, Reno, NV, 0325.
10. Bruck D. J., Bolda M., Tanigoshi L., Klick J., Kleiber J., Defrancesco J., Gerdeman B., Spitler H., 2011. Laboratory and field comparisons of insecticides to reduce infestation of Drosophila suzukii in berry crops. Pest Management Science, 67: 1375-1385.
11. Calabria G., Maca J., Bachli G., Serra L., Pascual M., 2012. First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe. Journal of Applied Entomology, 136: 139-147.
12. Chung Y. J., 1955. Collection of wild Drosophila on Quelpart Island, Korea. Drosophila Information Service, 29: 111.
13. Coop L., 2010. Online phenology and degree-day model for agricultural and decision-making in the US. Integrated Plant Protection Center, Botany & Plant Pathology Dep. Oregon State University, Corvallis, Oregon, USA. [online] URL: http://uspest.org/risk/models?spp_swd
14. Da Mata R. A., Tidon R., Cortes L. G., De Marco P., Diniz-Filho J. A. F., 2010. Invasive and flexible: niche shift in the drosophilid Zaprionus indianus (Insecta, Diptera). Biological Invasions, 12: 1231-1241.
15. Damus M., 2009. Some preliminary results from Climex and Maxent distribution modeling of Drosophila suzukii. Version 2. CFIA Plant Health Risk Assessment, Ottawa, Canada. [online] URL: http://entomology.oregonstate.edu/sites/default/files/DrosophilaSuzukiiInfestationModel.pdf
16. Dedeine F., Vavre F., Fleury F., Loppin B., Hochberg M. E., Bouletreau M., 2001. Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proceedings of the National Academy of Science USA, 98: 6247-6252.
17. Dekker T., Ibba I., Siju K. P., Stensmyr M. C., Hansson B. S., 2006. Olfactory shifts parallel superspecialism for toxic fruit in Drosophila melanogaster sibling, D. sechellia. Current Biology, 16: 101-109.
18. Dreves A. J., 2011. IPM program development for an invasive pest: coordination, outreach and evaluation. Pest Management Science, 67: 1403-1410.
19. Dreves A. J., Walton V., Fisher G., 2009. A new pest attacking healthy ripening fruit in Oregon. Spotted wing dro-sophila: Drosophila suzukii (Matsumura). Oregon State University Extension Publication EM 8991.
20. Dyck V. A., Hendrichs J., Vreysen M. J. B., Enkerlin W. R., Cayol J. P., 2005. Strategic options in using sterile insects for area-wide integrated pest management, pp. 563-600. In: Sterile insect technique principles and practice in area-wide integrated pest management (Dyck V. A., Hendrichs J., Robinson A. S., Eds). Springer, Dordrecht, The Netherlands.
21. st Annual Pacific Northwest Insect Management Conference, 9-10 January 2012, Portland (OR), USA.
22. Eriksson A., Anfora G., Lucchi A., Lanzo F., Virant-Doberlet M., Mazzoni V., 2012. Exploitation of insect vibrational signals reveals a new method of pest management. PLoSONE, 7 (3): e32954.
23. Ewing A. W., 1978. The antenna of Drosophila as a "love song" receptor. Physiological Entomology, 3: 33-36.
24. Fast E. M., Toomey M. E., Panaram K., Desjardins D., Ko-laczyk E. D., Frydman H. M., 2011. Wolbachia enhance Drosophila stem cell proliferation and target the germline stem cell niche. Science, 334 (6058): 990-992.
25. Ferndandez Iriarte P. J., Balanya J., Pascual M., Mestres F., Hasson E. R., Fontdevila A., Serra L., 2009. Tracking the origin of an invasive species: Droso-phila subobscura in Argentina. Journal of Evolutionary Biology, 22: 650-658.
26. Ffrench-Constant R. H., Roush R. T., 1991. Gene mapping and cross-resistance in cyclodiene insecticide-resistant Drosophila melanogaster (Mg.). Genetical Research, 57: 17-21.
27. Franchi A., Barani A., 2011. Un nuovo agente di danno per frutta e vite in Emilia. Notiziario Fitopatologico, 2: 14.
28. Fry A. J., Palmer M. R., Rand D. M., 2004. Variable fitness effects of Wolbachia infection in Drosophila melanogaster. Heredity, 93: 379-89.
29. Fuyama Y., 1979. A visual stimulus in the courtship of Dro-sophila suzukii. Cellular and Molecular Life Sciences, 35: 1327-1328.
30. Goodhue R. E., Bolda M., Farnsworth D., Williams J. C., Zalom F. G., 2011. Spotted wing drosophila infestation of California strawberries and raspberries: economic analysis of potential revenue losses and control costs. Pest Management Science, 67: 1396-1402.
31. Grassi A., Palmieri L., Giongo L., 2009. Nuovo fitofago per i piccoli frutti in Trentino. Terra Trentina, 55 (10): 19-23.
32. Grassi A., Palmieri L., Giongo L., 2012. Drosophila (Sophophora) suzukii (Matsumura), new pest of soft fruits in Trentino (North-Italy) and in Europe. IOBC/wprs Bulletin, 70: 121-128.
33. Griffo R., Frontuto A., Cesaroni C., Desantis M., 2012.L'insetto Drosophila suzukii sempre più presente in Italia. L'Informatore Agrario, 68 (9): 56-60.
34. th Annual Meeting, November 13-16, Reno, NV, 0555.
35. Hauser M., 2011. A historic account of the invasion of Dro-sophila suzukii (Matsumura) (Diptera: Drosophilidae) in the continental United states, with remarks on their identification. Pest Management Science, 67: 1352-1357.
36. Hsu T. C., 1949. The external genital apparatus of male Dro-sophilidae in relation to systematics. University of Texas Publications, 4920: 80-142.
37. Ideo S., Watada M., Mitsui H., Kimura M. T., 2008. Host range of Asobara japonica (Hymenoptera: Braconidae), a larval parasitoid of drosophilid flies. Entomological Science, 11: 1-6.
38. Ioriatti C., Frontuto A., Grassi A., Anfora G., Simoni S., 2011. Drosophila suzukii, una nuova specie invasiva dan-nosa alle colture di piccoli frutti. Accademia dei Georgofili, Giornata di studio "Criticità e prospettive delle emergenze fitosanitarie, 1 December 2011, Firenze, Italy.
39. Jaenike J., Unckless R., Cockburn S. N., Boelio L. M., Perlman S. J., 2010. Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science, 329: 212-215.
40. Kacsoh B. Z., Schlenke T.A., 2012. High hemocyte load is associated with increased resistance against parasitoids in Drosophila suzukii, a relative of D. melanogaster. PLoS-ONE, 7 (4): e34721.
41. Kaneshiro K. Y., 1983. Drosophila (Sophophora) suzukii (Matsumura). Proceedings Hawaiian Entomological Society, 24: 179.
42. Kang Y. S., Moon K. W., 1968. Drosophilid fauna of six regions near the demilitarized zone in Korea. Korean Journal of Zoology, 11: 65-68.
43. Kanzawa T., 1934. Research into the fruit fly Drosophila suzukii Matsumura. Yamanashi Prefecture Agricultural Experiment Station Report, October 1934: 48.
44. Kanzawa T., 1935. Research into the Fruit-fly Drosophila suzukii Matsumura (Preliminary Report). Yamanashi Prefecture Agricultural Experiment Station Report.
45. Kanzawa T., 1936. Studies on Drosophila suzukii Mats.Journal of Plant Protection (Tokyo) 23: 66-70, 127-132, 183-191. In: Review of Applied Entomology, 24: 315.
46. Kanzawa T., 1939. Studies on Drosophila suzukii Mats. Kofu, Yamanashi Agricultural Experiment Station 49 pp. In: Review of Applied Entomology, 29: 622.
47. Kawase S., Uchino K., Takahashi K., 2007. Control of cherry Drosophila, Drosophila suzukii, injurious to blueberry. Plant Protection, 61: 205-209.
48. Kikkawa H., Peng F. T., 1938. Drosophila species of Japan and adjacent localities. Japanese Journal of Zoology, 7: 507-552.
49. Kimura M. T., 1988. Adaptation to temperate climates and evolution of over-wintering strategies in the Drosophila melanogaster species group. Evolution, 42: 1288-1297.
50. Kimura M. T., 2004. Cold and heat tolerance of drosophilid flies with reference to their latitudinal distributions.Oecologia, 140: 442-449.
51. st Annual Pacific Northwest Insect Management Conference, 9-10 January 2012, Portland (OR), USA.
52. Kopp A., True J. R., 2002. Phylogeny of the oriental Droso-phila melanogaster species group: a multilocus reconstruction. Systematic Biology, 51: 786-805.
53. Landolt P. J., Adams T., Rogg H., 2012. Trapping spotted wing drosophila, Drosophila suzukii (Matsumura) (Diptera: Drosophilidae), with combinations of vinegar and wine, and acetic acid and ethanol. Journal of Applied Entomology, 136: 148-154.
54. Lee J. C., Bruck D. J., Curry H., Edwards D., Haviland D. R., Van Steenwyk R. A., Yorgey B. M., 2011a. The susceptibility of small fruits and cherries to the spotted-wing drosophila, Drosophila suzukii. Pest Management Science, 67: 1358-1367.
55. Lee J. C., Bruck D. J., Dreves A. J., Ioriatti C., Vogt H., Baufeld P., 2011b. In focus: spotted wing drosophila, Drosophila suzukii, across perspectives. Pest Management Science, 67: 1349-1351.
56. Lethmayer C., 2011. Gefhrliche Fliegen für Äpfel & Co.Bessers Obst, 12: 4-5.
57. Lin F. J., Tseng H. C., Lee W. Y., 1977. A catalogue of the family Drosophilidae in Taiwan (Diptera). Quarterly Journal of Taiwan Museum, 30: 345-372.
58. Louis C., Girard M., Kuhl G., Lopez-Ferber M., 1996.Persistence of Botrytis cinerea in its vector Drosophila melanogaster. Phytopathology, 86: 934-939.
59. Mandrin J. F., Weydert C., Trottin-Caudal Y., 2010. Un nouveau ravageur des fruits: Drosophila suzukii. Premiers dégâts observés sur cerises. Infos CTIFL, 266: 26-33.
60. Martelli G., 1910. Notizie sulla Drosophila ampelophila.Bollettino del Laboratorio di Zoologia Generale e Agraria del-la R. Scuola Superiore d'Agricoltura in Portici, 4: 163-174.
61. Masten Milek T., Seljak G., Šimala M., Bjeliš M., 2011. Prvi nalaz Drosophila suzukii (Matsumara, 1931) (Diptera Droso-philidae) u Hrvatskoj. Glasilo Biljne Zaštite, 11: 377-382.
62. Mitsui H., Kimura M. T., 2010. Distribution, abundance and host association of two parasitoid species attacking frugivo-rous drosophilid larvae in central Japan. European Journal of Entomology, 107: 535-540.
63. Mitsui H., Takahashi H. K., Kimura M. T., 2006. Spatial distributions and clutch sizes of Drosophila species ovipositing on cherry fruits of different stages. Population Ecology, 48: 233-237.
64. Mitsui H., Van Achterberg K., Nordlander G., Kimura M. T., 2007. Geographical distributions and host associations of larval parasitoids of frugivorous Drosophilidae in Japan. Journal of Natural History, 41: 1731-1738.
65. Mitsui H., Beppu K., Kimura M. T., 2010. Seasonal life cycles and resource uses of flower- and fruit-feeding droso-philid flies (Diptera: Drosophilidae) in central Japan. Entomological Science, 13: 60-67.
66. Ohashi Y. Y., Haino-Fukushima K., Fuyama Y., 1991. Purification and characterization of an ovulation stimulating substance from the male accessory glands of Drosophila su-zukii. Insect Biochemistry, 21: 413-419.
67. st Annual Pacific Northwest Insect Management Conference, 9-10 January 2012, Portland (OR), USA.
68. Okada T., 1954. Comparative morphology of drosophilid flies. I. Phallic organs of the melanogaster group. Kontyu, 22: 36-46.
69. Okada T., 1968. Systematic study of the early stages of Dro-sophilidae. Bunka Zugeisha Co., Tokio, Japan.
70. Okada T., 1976. New distribution records of the Droso-philids in the oriental region. Makunagi, 8: 1-8 (in Japanese).
71. Pansa M. G., Frati S., Baudino M., Tavella L., Alma A., 2011. Prima segnalazione di Drosophila suzukii in Piemon-te. Protezione delle Colture, 2: 108.
72. Panteleev D. Y., Goryacheva I. I., Andrianov B. V., Reznik N. L., Lazebny O. E., Kilikov A. M., 2007. The endosymbiotic bacterium Wolbachia enhances the nonspecific resistance to insect pathogens and alters behaviour of Drosophila melanogaster. Russian Journal of Genetics, 43: 1066-1069.
73. Parshad R., Duggal K. K., 1965. Drosophilidae of Kashmir, India. Drosophila Information Service, 40: 44.
74. Parshad R., Paika I. J., 1965. Drosophilid survey of India II. Taxonomy and cytology of the subgenus Sophophora (Dro-sophila). Research Bulletin of the Panjab University, 15: 225-252.
75. Peng F. T., 1937. On some species of Drosophila from China. Annotationes Zoologicae Japonenses, 16: 20-27.
76. Powell J. R., 1997. Progress and prospects in evolutionary biology: The Drosophila model. Oxford University Press, Inc. New York, USA.
77. Profaizer D., Angeli G., Trainotti D., Marchel L., Zadra E., Sofia M., Ioriatti C., 2012. Drosophila suzukii: valuta-zione di agrofarmaci ed analisi sul corretto posizionamento in campo. ATTI Giornate Fitopatologiche 2012, 1: 229-235.
78. Prud'homme B., Gompel N., Rokas A., Kassner V. A., Williams T. M., Yeh S. D., True J. R., Carroll S. B., 2006.Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene. Nature, 440: 1050-1053.
79. Raspi A., Canale A., Canovai R., Conti B., Loni A., Stru-mia F., 2011. Insetti delle aree protette del comune di San Giuliano Terme. Felici Editore, San Giuliano Terme, Pisa, Italy.
80. nd edition.Rural Culture Association Japan, Tokyo, Japan.
81. Sasaki M., Sato R., 1995. Bionomics of the cherry droso-phila, Drosophila suzukii Matsumura (Diptera: Drosophili-dae) in Fukushima prefecture (Japan). Annual Report of the Society of Plant Protection of North Japan, 46: 164-172.
82. Schawaroch V., 2002. Phylogeny of a paradigm lineage: the Drosophila melanogaster species group (Diptera: Droso-philidae). Biological Journal of the Linnean Society, 76: 21-37.
83. Schmidt T., Choffat Y., Schneider M., Hunziger P., Fuy-ama Y., Kubli E., 1993. Drosophila suzukii contains a pep-tide homologous to the Drosophila melanogaster sex-peptide and functional in both species. Insect Biochemistry and Molecular Biology, 23: 571-579.
84. Seljak G., 2011. Spotted wing Drosophila, Drosophila su-zukii (Matsumura), a new pest of berry-fruit in Slovenia.Sadjarstvo, 22 (3): 3-5.
85. Sidorenko V. S., 1992. New and unrecorded species of Dro-sophilidae from Soviet Far East (Diptera, Brachycera).Spixiana, 15: 93-95.
86. Sinkins S. P., Gould F., 2006. Gene drive systems for insect disease vectors. Nature Reviews Genetics, 7: 427-435.
87. Süss L., Costanzi M., 2011. Presence of Drosophila suzukii (Matsumura, 1931) (Diptera Drosophilidae) in Liguria (Italy). Journal of Entomological and Acarological Research, 42: 185-188.
88. Takamori H., Watabe H., Fuyama Y., Zhang Y., Aotsuka T., 2006. Drosophila subpulchrella, a new species of the Drosophila suzukii species subgroup from Japan and China (Diptera: Drosophilidae). Entomological Science, 9: 121-128.
89. Toda M. J., 1991. Drosophilidae (Diptera) in Myanmar (Burma) VII. The Drosophila melanogaster species-group, excepting the D. montium species-subgroup. Oriental Insects, 25: 69-94.
90. Unckless R. L., 2011. A DNA virus of Drosophila. PLoS-ONE, 6 (10): e26564.
91. van der Linde K., Houle D., 2008. A supertree analysis and literature review of the genus Drosophila and closely related genera. Insect Systematics and Evolution, 39: 241-267.
92. van der Linde K., Houle D., Spicer G. S., Steppan S. J., 2010. A supermatrix based molecular phylogeny of the family Drosophilidae. Genetics Research, 92: 25-38.
93. Vet L. E. M., Janse C., Van Achterberg C., Van Alphen J. J. M., 1984. Microhabitat location and niche segregation in two sibling species of drosophilid parasitoid: Asobara tabida (Nees) and A. rufescens (Foerster) (Braconidae: Alysiinae). Oecologia, 61: 182-188.
94. Vogt H., Baufeld P., Gross J., Kopler K., Hoffmann C., 2012. Drosophila suzukii: eine neue bedrohung für den Eu-ropäischen obst- und weinbau - bericht über eine internationale tagung in trient, 2, Dezember 2011. Journal für Kul-turpflanzen, 64: 68-72.
95. Vreysen M. J., Hendrichs J., Enkerlin W. R., 2006. The sterile insect technique as a component of sustainable area-wide integrated pest management of selected horticultural insect pests. Journal of Fruit Ornamental Plant Research, 14: 107-131.
96. Walsh D. B., Bolda M. P., Goodhue R. E., Dreves A. J., Lee J. C., Bruck D. J., Walton V. M., O'Neal S. D., Zalom F. G., 2011. Drosophila suzukii (Diptera: Drosophilidae): Invasive pest of ripening soft fruit expanding its geographic range and damage potential. Journal of Integrated Pest Management, 1: 1-7.
97. Werren J. H., Baldo L., Clark M. E., 2008. Wolbachia: master manipulators of invertebrate biology. Nature Reviews Microbiology, 6 (10): 741-51.
98. Westphal M. I., Browne M., Mackinnon K., Noble I., 2008. The link between international trade and the global distribution of invasive alien species. Biological Invasions, 10: 391-398.
99. Weydert C., Bourgouin B., 2011. Drosophila suzukii menace l'arboriculture fruitière et les petits fruits. Point de situation sur cette mouche, ravageur nouveau et déjà très nuisible, et ce qu'on peut faire contre elle. Phytoma, 650: 16-20.
100. Wu S. R., Tai H. K., Li Z. Y., Wang X., Yang S. S., Sun W., Xiao C., 2007. Field evaluation of different trapping methods of cherry fruit fly, Drosophila suzukii. Journal of Yunnan Agricultural University, 22: 776-778.
101. Yang Y., Hou Z. C., Qian H. Y., Kang H., Zeng Q. T., 2011. Increasing the data size to accurately reconstruct the phylogenetic relationships between nine subgroups of the Drosophila melanogaster species group (Drosophilidae, Diptera). Molecular Phylogenetics and Evolution, 62: 214-223.
102. Zabalou S., Riegler M., Theodorakopoulou M, Stauffer C., Savakis C., Bourtzis K., 2004. Wolbachia-induced cy-toplasmic incompatibility as a means for insect pest population control. Proceedings of the National Academy of Science USA, 101: 15042-15045.
103. Zindel R., Gottlieb Y., Aebi A., 2011. Arthropod symbio-ses: a neglected parameter in pest- and disease-control programmes. Journal of Applied Ecology, 48: 864-872.