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The Leafhopper Vectors of Phytopathogenic Viruses (Homoptera, Cicadellidae) Taxonomy, Biology, and Virus Transmission

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The Leafhopper Vectors of Phytopathogenic Viruses (Homoptera, Cicadellidae) Taxonomy, Biology, and Virus Transmission /«' THE LEAFHOPPER VECTORS OF PHYTOPATHOGENIC VIRUSES (HOMOPTERA, CICADELLIDAE) TAXONOMY, BIOLOGY, AND VIRUS TRANSMISSION Technical Bulletin No. 1382 Agricultural Research Service UMTED STATES DEPARTMENT OF AGRICULTURE ACKNOWLEDGMENTS Many individuals gave valuable assistance in the preparation of this work, for which I am deeply grateful. I am especially indebted to Miss Julianne Rolfe for dissecting and preparing numerous specimens for study and for recording data from the literature on the subject matter. Sincere appreciation is expressed to James P. Kramer, U.S. National Museum, Washington, D.C., for providing the bulk of material for study, for allowing access to type speci- mens, and for many helpful suggestions. I am also grateful to William J. Knight, British Museum (Natural History), London, for loan of valuable specimens, for comparing type material, and for giving much useful information regarding the taxonomy of many important species. I am also grateful to the following persons who allowed me to examine and study type specimens: René Beique, Laval Univer- sity, Ste. Foy, Quebec; George W. Byers, University of Kansas, Lawrence; Dwight M. DeLong and Paul H. Freytag, Ohio State University, Columbus; Jean L. LaiFoon, Iowa State University, Ames; and S. L. Tuxen, Universitetets Zoologiske Museum, Co- penhagen, Denmark. To the following individuals who provided additional valuable material for study, I give my sincere thanks: E. W. Anthon, Tree Fruit Experiment Station, Wenatchee, Wash.; L. M. Black, Uni- versity of Illinois, Urbana; W. E. China, British Museum (Natu- ral History), London; L. N. Chiykowski, Canada Department of Agriculture, Ottawa ; G. H. L. Dicker, East Mailing Research Sta- tion, Kent, England; J. W. Evans, Sidney, Australia; N. W. Fra- zier, University of California, Berkeley; T. Fukushi, University of Sapporo, Sapporo, Japan; M. S. K. Ghauri, British Museum (Natural History), London; R. M. Gilmer, Cornell University, Ithaca, N.Y.; N. E. Grylls, Canberra, Australia; Karl Maramo- rosch, Boyce Thompson Institute, Yonkers, N.Y.; H. N. Pollard, U.S. Department of Agriculture, Port Valley, Ga.; W. R. Rich- ards, Canada Department of Agriculture, Ottawa; C. T. Rivera, Los Banos, Philippines ; R. F. Ruppel, Michigan State University, East Lansing; Y. Tahama, Kumamoto Siriculture Experiment Station, Kumamoto, Japan; R. G. Timian, U.S. Department of Agriculture, Fargo, N. Dak.; and Carlo Vidano, University of Torino, Torino, Italy. I am also indebted to D, A. Young, North Carolina State Uni- versity, Raleigh, for information on the taxonomy of the subfamily Cicadellinae and to W. H. Anderson, U.S. Department of Agri- culture, Beltsville, Md., for permitting me access to the unpublished manuscript of the GÍeneral Catalogue of the Homop- tera, fascicle VI, Cicadelloidea, by Z. P. Metcalf. My sincere appreciation is expressed to P. W. Oman and F. F. Smith, U.S. Department of Agriculture, Beltsville, Md., for many helpful suggestions. THE LEAFHOPPER VECTORS OF PHYTOPATHOGENIC VIRUSES (HOMOPTERA, QCADELLIDAE) TAXONOMY, BIOLOGY, AND VIRUS TRANSMISSION By M. W. NIELSON Technical Bulletin No. 1382 Agricultural Research Service UNITED STATES DEPARTMENT OF AGRICULTURE Washington, D.C. Issued August 1968 For sale by the Superintendent of Documents, U.S. Government Printing Office Washington; D.C. 20402—Price $1.50 CONTENTS Page History of transmission of leafhopper-borne viruses 2 Taxonomic considerations 6 Leaf hopper vectors and phytopathogenic viruses — 9 Virus-vector relationships 11 Geographical distribution 15 Preservation and disposition of vector specimens — 15 Classification and treatment of vector species 16 Subfamily Agalliinae 17 Subfamily Macropsinae 50 Subfamily Coelidiinae 58 Subfamily Aphrodinae 60 Subfamily Gyponinae 67 Subfamily Cicadellinae 72 Subfamily Typhlocybinae 143 Subfamily Deltocephalinae 147 Addenda 318 Literature cited 318 Appendix - Table 1.—Summary of leaf hopper vectors and transmission of phytopathogenic viruses 370 Index to genera and subfamilies 378 Index to trivial names 380 Index to leafhopper-borne viruses and virus-like dis- orders 385 THE LEAFHOPPER VECTORS OF PHYTOPATHOGENIC VIRUSES (HOMOPTERA, CICADELLIDAE) TAXONOMY, BIOLOGY, AND VIRUS TRANSMISSION By M. W. NiELSON, Entomology Research Division^ Agricultural Research Service During a span of 70 years significant contributions were made in the field of plant pathogenic viruses and transmission of vi- ruses by cicadellid vectors. Unfortunately progress in taxonomic research did not keep pace with virus-vector research and as a consequence nearly two-thirds of the known vector species re- quired one or more taxonomic changes. Most of the changes were made not as a result of initial vector discoveries but from subse- quent research in leafhopper taxonomy. General acceptance and usage of the change in a new name for a vector species were slow. Often research workers were unaware of name changes, and sometimes the old name was perpetuated from author to author and year to year. Names of a few species that were passé 20 years ago were still in use at the time of this investigation. Among 8 subfamilies, 52 genera, and 114 species treated, 1 genus and 3 species were suppressed, 1 subgenus was given a new generic status, 1 genus and 1 species were reinstated, 2 new com- binations were proposed, 2 lectotype designations were made, and 5 vector species previously misdetermined were corrected. The vectorial and taxonomic status of four species remained uncer- tain. Research workers have recognized the need to clarify the tax- onomic and vectorial status of all leafhopper species incriminated in the transmission of plant viruses. In fulfillment of this need, I have restudied all knov^nn authentic vector species from the tax- onomic vievrpoint and reviewed the literature treating all cases of virus transmission by cicadellid vectors to ascertain the authentic- ity of the species reported as vectors. In scope, this bulletin presents the latest taxonomic status of all authentic vector species in light of the most recent acceptable tax- onomic concepts. Keys to the vector subfamilies, vector genera, and vector species are proposed. Each species has been rede- scribed and illustrated on the basis of the genitalia and general habitus of the adults. A complete resume of distribution, biology, and virus transmission for each species is also presented. Common names have been suggested for all species except those for which common names have already been officially accepted. 2 TECHNICAL BULLETIN 1382, U.S. DEPT. OF AGRICULTURE HISTORY OF TRANSMISSION OF LEAFHOPPER-BORNE VIRUSES Except for a few early accounts, a complete history of leafhop- per vectors of plant viruses up to the present has not been re- ported. The remarkable progress made in this field from 1895 to 1965 is graphically illustrated in figure 1, which shows the number of leafhopper vectors discovered per year and the accumulative total for this period. In all, 114 vectors transmitting 65 viruses and virus strains were implicated during this period. The earliest record of authentic transmission of plant patho- genic viruses by leafhoppers has been accredited to Takata / n NUMBER PER YEAR 1 ACCUMULATIVE NUMBER PER YEAR f «7 u 50 S 3-1 ... .Mr Ill 1930 YEAR FIGURE 1.—Number of leafhopper vectors discovered per year and accumu- lative total per year from 1895 to 1965. THE LEAFHOPPER VECTORS OF PHYTOPATHOGENIC VIRUSES ó (781)'^ in 1895, when he demonstrated transmission of rice dwarf virus in Japan by Recilia dorsalis (Motschulsky). Shortly after his discovery the Shiga Agricultural Experiment Station (718) in Japan provided evidence that the real vector was Nephotettix cincticeps (Uhler). From 1899 to 1916 a controversy developed to the extent that Takata's work was suppressed and cincticeps be- came generally accepted among Japanese workers as the only vec- tor of the virus. These developments were unknown to the west- ern world until 1936, when Katsura U09) reviewed the early history of transmission of plant viruses in Japan. A year later Fukushi (295) published his account of transmission of rice dwarf virus by dorsalis, and thus reestablished this species as the first authentic vector of a plant virus. During the first 25 years after Takata's discovery very little progress was made on leafhopper-bome viruses. Prior to 1920 only three leafhopper vector species and two viruses were known. The earliest work done in the United States was in 1909, when Ball (27) showed a relationship between the beet leafhopper (Cir- culifer tenellus (Baker)) and curly top disease of sugarbeets. However, it was not until 1910 that Shaw (716) offered substan- tial proof of the viral nature of the disease and transmission of the virus by tenellus. For many years this record was considered as the first published evidence of a leafhopper-borne virus until Takata's work was revealed by Katsura (i09). During the period 1920-30 four additional leafhopper vector species were discovered. In 1924 Kunkel (i22) presented his clas- sical experiments on transmission of the eastern strain of North American aster yellows virus by Macrosteles fascifrons (Stâl). In the same year in Africa Storey (766) transmitted maize streak virus by means of Cicadulina mbila (Naude), and the following year he (767) demonstrated transmission of Uba cane virus by the same leafhopper species. Fawcett (25Í) was credited for his work in 1927 on transmission of Argentine curly top virus of sugar- beets by Agalliana ensigera Oman. Transmission of the western strain of North American aster yellows virus by fascifrons was attributed to Severin (687) in 1929. In the same year Dobroscky (213) incriminated Scleroracus vaccinii (Van Duzee) as the vec- tor of cranberry false blossom virus. The number of new vectors discovered between 1930 and 1940 increased 125 percent over the previous decade. Ten vectors transmitting eight viruses were found. Perhaps the most significant work was done by Storey (770, 773, 77k) in 1931, 1936, and 1937 on transmission of maize streak and maize mottle viruses by two additional species of Cicadulina and by Kunkel (U28) in 1933 on transmission of peach yellows virus by Macrop- sis trimaculata (Fitch).
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