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Vectors of Beet Yellows Virus

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Vectors of Beet Yellows Virus Transmission Efficiencies of Field-Collected Aphid (Homoptera: Aphididae) Vectors of Beet Yellows Virus MARYELLYN KIRK,' STEVEN R. TEMPLE,* CHARLES G. SUMMERS,3 AND L. T. WILSON' University of California, Davis, California 95616 J. Econ. Entomol. 84(2). 638-643 (1991) ABSTRACT Alate aphids (Homoptera: Aphididae) were collected at weekly intervals in 1988 in six California sugarbeet fields-three on each side of a boundary line which separates overwintered spring harvest beet fields in Solano County from fall harvested fields in Yolo County. Alate aphids landing on a yellow board during a 45-min morning collection period were captured live and tested for ability to transmit beet yellows virus (BYV) by allowing individual aphids to feed on healthy sugarbeet seedlings immediately after capture. Test plants were evaluated for BYV infection by enzyme-linked immunosorbent assay (ELISA). and aphids were preserved and later identified. Myzus persicae (Sulzer), Aphis fabae Scopoli complex, and Rhopalostphum padi (L.) were the principal aphid species which transmitted BYV. Five additional captured aphid species were found to be carrying BYV, including Macrostphum rosae (L.) and Amphorophora spp., which are reported as BYV vectors for the first time. Geographically distinct isolates of A. fake complex were collected from fields in Fresno, Monterey, Santa Barbara, Tehama and Yolo counties; M. persicae was collected from Yolo County and R. padi was collected from Fresno and Yolo counties. A laboratory colony of R. padi was also obtained from New York. All aphid collections were tested for their relative efficiency in transmitting BYV. Differential transmission ability was found among geographically isolated aphid colonies of the same species and also among the different genera. A. fake complex aphids from Santa Barbara County were the most efficient BYV vectors, followed by M.persicae, A. fake complex from Fresno County, and R. padi from Fresno County. KEY WORDS Insecta, beet yellows virus, aphid vectors BEET YELLOWS VIRUS (BYV) is a closterovirus trans- current BYV management strategy is similar to that mitted in a semi-persistent manner by at least 22 recommended 20 years ago, with the addition of aphid vectors (Kennedy et al. 1962, Russell 1965) field leaf sampling for BYV infection to identify to nine plant families (Peters 1988). BYV is the fields or areas which represent BY V reservoirs and most important component of the yellows virus to schedule such fields for early harvest to reduce complex affecting sugarbeets (Beta uulgaris L.) in BY V reservoirs. However, the incidence of BY V in California (Tamaki et al. 1979). This complex in- California has increased in recent years due to cludes beet yellows virus, beet western yellows vi- changes in populations and species composition of rus, and beet mosaic virus. BYV infection reduces the aphid vectors, changes in the implementation yields by 20-35% (Bennett et al. 1957) and has an of beet-free programs (Temple et al. 1988), and additive effect on yield loss when plants are co- reduced control of ground keeper beets, weed beets, infected with beet western yellows virus (BWY V) and other weed hosts of the virus (Duffus 1977, and beet mosaic virus (BMV) (Bennett & Mc- Temple et al. 1988). Overwintered beets adjacent Farlane 1964). BYV also increases beet plant sus- to spring planted beets continue to serve as the ceptibility to infection by several pathogenic fungi principal inoculum source for beet yellows virus and beet curly top virus (Duffus 1973). (Shepherd & Hills 1970, Temple et al. 1988). BYV was largely controlled in California from Little is known about the aphid species respon- 1969 to 1975 by using tolerant cultivars, manipu- sible for spread of BYV in the field (Heathcote lating planting dates, controlling aphid vectors, and 1988), and much of the evidence is based on re- by not planting beets in designated districts at spec- peated tests of suspected vectors. It is recognized ified times of the year: in accordance with the that virus spread is more likely when vectors are statewide beet-free program (Duffus 1978). The less adapted to the virus host plant, because trang- mission of virus depends on vector movement (Kennedy 1950, Watson et al. 1951, Heathcote & I Department of Entomology, University of California. Davis, Calif. 95616. Cockbain 1964). The green peach aphid, Myzus * Department of Agronomy and Range Science, University of persicae (Sulzer), has been recognized as the most California, Davis, Calif. 95616. important aphid vector of BYV (Watson et al. 1951, Department of Entomology, University of California, Berke- ley, Calif. 94720. (Person to whom reprint requests should be Bennett 1960), and does not prefer sugarbeet as a sent.) host plant (Gladders & Peters 1986). Jadot (1975) 0022-0493/91/0638-0643$02.00/00 1991 Entomological Society of America April 1991 KIRK ET AL.: BYV TRANSMISSION BY FIELDCOLLECTEDAPHID VECTORS 639 related the importance of M. persicae to field spread to small clip-on cages, which in turn were clipped of BYV to this vector’s mobility and restlessness. to a piece of stiff paper and immediately trans- The bean aphid, Aphis fabae Scopoli, transmits ported to the greenhouse. Clip-on cages were con- BYV with less efficiency than does M. persicae in structed of pieces of Tygon tubing (Norton Co., greenhouse tests, and is considered the second most Akron, Ohio), 1.2 cm long and 1.2 cm in diameter, important BYV vector (Watson & Healy 1953, glued tot aluminum hair clips. Cockbain et al. 1963). Other aphids found in beet In transmission studies described in this paper, fields and known to transmit BYV in laboratory a 24-h inoculation access period (IAP) and a 24-h tests include Metopolophium dirhodum (Walker) acquisition access period (AAP) were used to allow (Russell 1965), Brevicoryne brassicue (L.), Acyr- maximum time for probing and adapting to cage thosiphon pisum (Harris) (Kennedy et al. 1962), and greenhouse conditions, because evidence for Macrosiphum euphorbiae (Thomas) (Watson et al. optimal IAP and AAP is conflicting for M.persicae 1951), Rhopalosiphum padi (L.) (Russell 1965, Ja- (Bennett 1960, Sylvester 1956, Gladders & Peters dot 1975), and Sitobion avenue (F.) (Jadot 1975, 1986) and undocumented for A. fabae. Upon ar- Heathcote 1988). rival from the field, individual caged aphids were The purpose of this study was to assess BYV placed on virus-free sugarbeet seedlings (6-8 leaf transmission by alate aphids captured in sugarbeet stage) and allowed a 24-h IAP in a greenhouse fields and to compare the efficiency of geographic maintained at 21 4 2°C. After the IAP, aphids were isolates of selected vector species. individually preserved in 70% ethanol for later identification. Test plants were maintained in a Materials and Methods greenhouse at 21 _+ 2°C and evaluated for BYV infection by ELISA 4 and 8 wk after inoculation. Aphid Identification. The ability to distinguish Greenhouses were treated regularly with nicotine between Aphis craccivora Koch and A. fabae was sulfate (Fulex nicotine fogger, 14%AI, A. H. Hum- under taxonomic scrutiny for the duration of this mert Seed Company, St. Louis, Mo.) and monitored study. Therefore, we recorded these specimens as daily for contamination by stray aphids. Eight su- A. fabae complex. Random aphid samples were garbeet and eight New Zealand spinach (Tetra- sent to the Department of Entomology, University gonia expansa Murr.) plants of the same age as the of Idaho, lab to verify our identifications. Mounted test plants were maintained in the same greenhouse voucher specimens are in the University of Cali- as healthy controls. fornia, Davis Museum Collection. Field and Test Plant Evaluation of BYV Infec- Field Collection of Aphids and Determination tion by ELISA. Initial BYV infection in each su- of BYV Infection. A California beet-free boundary garbeet field was assessed before aphid sampling line separates September harvest sugarbeet fields began by walking a large arc through the field and (Yo10 County, 15 miles west of Sacramento) from selecting the youngest leaf large enough (26 mm) overwintered May harvest fields (Solano County). to sample by ELISA from 35 randomly selected Three sugarbeet fields located in the February beet plants. Leaf samples were taken every 4 wk plant/September harvest area, on the north side of until the infection level, determined with ELISA, the beet-free boundary (Yolo), and three located reached a maximum. opposite these in the May plant/May harvest area Indirect ELISA was used to assay leaves for BYV on the south side (Solano), were sampled for aphids antigens (Voller et al. 1976) using BYV antisera from 20 February to 11 May 1988. South side fields described by Reed & Falk (1989). Leaf tissue was were separated by 1.6 to 4.8 km from north side macerated using the Dayton leaf roller (Piedmont fields. Tool and Die, Six Mile, S.C.) from a 26-mm disk, Alate aphids were collected at weekly intervals or equivalent area if leaf diameter was smaller, cut from a collapsible, easel-type 1-m2board painted through the midrib and leaf center. Sap pressed John Deere yellow (Deere & Company, Moline, from the tissue was diluted 1:10 (vol : vol) with SO- Ill.), erected in the field, 0.5 m above the ground. dium carbonate buffer, pH 9.6, and transferred The sampling boards were painted yellow to attract into Immulon-2 flat-bottom-well Immulon micro- M. persicae, thought to be the dominant BYV vec- titer ELISA plates. Duplicate wells were used for tor, and known to be attracted to yellow (Moericke each sample. Samples from three non-infected and 1951, 1955). Such traps have been shown to give three known BYV-infected sugarbeet plants of the fairly reliable epidemiological information about Same age as the test plants were included on each species such as M. persicae and provide adequate microtiter plate as healthy and infected contro1s.
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