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. information about aerial populations of other spe- Absorbances were measured at 405 nm using a cies (Robert et al. 1988). Aphids were collected for Tit&& Multiskan photometer (Flow Laborato- a 45-min period between 0900 hours and 1200 ries, Inglewood, Calif ,), Transmission studies were hours PST, a time of peak aphid activity (C.G.S, conducted to verify infection in 27 Plants whose unpublished data). All aphids landing on the yellow ELISA values were ambiguous. In these transmis- board were captured. A mouth aspirator with screen sion studies, healthy M. persfcue were transferred similar to that described by Sylvester (1962) was to the test plant and allowed an AAP of 24 h and used to transfer aphids individually from the board then caged in clip-on cages on healthy New 640 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 84, no. 2

land spinach seedlings for an IAP of 24 h. M. per. sicae were then removed and plants were observed

-4 for visual symptoms after 3 wk and tested for BYv c by ELISA after 4 wk. Plants in all tests were recorded as being infected if the photometric absor- bance values were greater than the mean value of 3. 3. the healthy control plus four times its standard deviation (approximately 95% CI). dI Transmission Studies with Three Vector Spe- cies from Different Geographic Areas. A. fahe complex were collected from sugarbeet fields in Yolo, Fresno, Monterey, Santa Barbara, and Te- hama counties, and M.persicae was collected from Yolo County. R. padi colonies were obtained from Fresno and Yolo counties and from New York. Each colony was composed of at least 50 individuals from three or four fields, with the exception of R. padi from New York which was obtained as a laboratory colony. Upon arrival from the field, 100 aphids were membrane-fed a 50% sucrose solution on parafilm for 24 h. Approximately 50 first instar nymphs produced by these field-collected aphids were transferred from the membrane and caged on healthy 3-wk-old (6 leaf stage) sugarbeet plants or oats in the case of R. padi, for 3 wk in the growth chamber at 18.3”C, 32% relative hu- midity and a 12:12 (L:D) photoperiod. The assumptions made in the membrane feeding procedure were that transovarial passage of BYV will not occur and that the sucrose solution between the parafilm membranes would not become a source ’ of virus for the newborn nymphs (Sylvester 1980). Predators, parasites, and disease are also excluded by selecting only the first instar nymphs. Using a No. 1 camel’s-hair brush, approximately 200 non-viruliferous apterae were transferred to a Petri dish (12.7 cm) containing two BYV-infected beet leaves. Aphids were allowed an acquisition access period (AAP) of 24 h in the laboratory at 22°C. At the end of the AAP, 120 apterae were confined individually in small clip-on cages on 120 healthy sugarbeet seedlings, for an IAP of 24 h in the laboratory. Seedlings were then moved to a greenhouse maintained at 21 3- 2”C, treated with nicotine sulfate immediately and subsequently at 10 d intervals for 4 wk. Each test seedling was evaluated for BYV infection by ELISA 4 wk after inoculation. Statistical Analyses. On several sample dates, one or more fields had low numbers of aphids but a high percentage of them were carrying BYV. Averaging percent infected aphids in these instanc- es would have greatly overestimated true numbers of infective aphids. Therefore, number of infected aphids are reported as total infected aphids divided by total trapped aphids in all six fields on each sample date. Differences in transmission ability for

’ the season among M. persicae, A. fahe complex, st and R. padi were tested using chi-square. Chi- ca square tests were also used to evaluate differences d among geographic isolates of A. fabae complex and R. padi. Analysis of variance and Duncan’s mul- April 1991 KIRK ET AL.: BYV TRANSMISSION BY FIELD-COLLECTED APHID VECTORS 64 1

Table 2. Proportion of BYV-infective field-captured Table 3. BYV vector ability of selected end laboratory- vectors, summed over 6 fields and 9 sampling weeks, Yolo reared geographic isolates of A. fabae complex and Solano counties, 1988

No, of aphids ProprtionOf Proportion County, aphid species aphids trans- Aphid species No. of aphids ot aphids mitting BYV tested" transmitting BYV Santa Barbara, A. fahe complex 90 0.63 Fresno, A. fabae complex 85 0.45 Amphorophola spp. 2 1.00 Yolo, M.perstcae 61 0.44 Acyrthosiphon kondoi 53 0.58 Monterey, A. fabae complex 100 0.18 Acgrthosfph pisum 26 0.69 Yolo, A. fahe complex 85 0.16 Macrosiphum rosae 20 0.65 Tehama, A. fabae complex 85 0.14 Breoicoryne brasstcae 5 1.OO a 1 aphid/plant. Seasonal value based on total no. of plants infected by each vector species throughout the season over total no. of plants tested with that vector. 1 vector/plant. (L.), were found to be carrying BYV. Numbers were too few to permit statistical comparison with M. persicae, A. fabae complex, and R. padi, but tiple range (1955) tests were performed to quantify the proportion of infective individuals was sur- differences in proportion of BY V-infective vectors prisingly high (Table 2). among sample dates, using aphid x data interac- BYV Transmission by Geographic Isolates. Due tion as the error term. to differences in aphid mortality after the acquisition access period, the actual number of plants tested for transmission efficiency by feeding on Results healthy sugarbeet seedlings varied from 61 to 100. Our initial objective was to capture and deter- Transmission efficiency ranged from a high of 63% mine the relative infectivity of M.persicae, the for A. fahe complex from Santa Barbara County principal BYV vector, throughout the spring aphid to a low of 14% for the A. fahe complex from flight. However, because several species were col- Tehama County. Significant differences for ability lected, we report here on all aphids captured which to transmit BYV were found among the five A. transmitted BYV and which may therefore have a fabae complex collections (x* = 80.84, n = 506, P role in virus epidemiology. 6 0.001). A. fabae complex from Santa Barbara BYV Transmission by Field-Collected Aphids. county had significantly higher BY V transmission Fields were monitored for aphids beginning 24 ability than A. fabae complex from Fresno county February 1988, but significant numbers of aphids (xz = 7.89, n = 175, P < 0.01). A. fabae complex were not observed on the yellow board nor in water from Monterey, Tehama, and Yolo counties did pan traps in nearby sugarbeet fields until 16 March not differ in BYV transmission ability (Table 3).R. 1988 (V. E. Burton, unpublished data 1988). The padi from Fresno had a significantly higher BYV weather in the weeks preceding the first significant transmission ability than the New York (x2= 13.30, aphid count was very windy, reaching 25 km/h n = 210, P < 0.01) or Yolo County R. padi (xz= and averaging 11.3km/h between 1 and 16 March 4.84, n = 205, P < 0.05); the latter two were not (University of California IPM Davis Weather Da- significantly different from each other (Table 4). tabase Information 1988). Field Infection with BYV. Overwintered fields Myzus persicae, A. fabae complex, and R. padi (south) contained various levels of BYV infection comprised 75% of the total alate aphids captured when sampling began in February, probably a re- during the study (n = 688). R. padi was the most sult of fall vector flights (Table 5). Plants in fields abundant, comprising 33%of the total aphid catch. north of the boundary line were just emerging at Vector numbers within individual fields were too this time. By 22 March, plants in the north fields low to provide meaningful information and were were large enough to sample and process by ELISA, summed over all six fields for statistical analysis but no infected plants were detected. By mid-April, and reporting. The total proportion of infective vectors increased significantly (F = 3.02, df = 10, Table 4. BYV vector ability of laboratory-reared R. P < 0.05) throughout the sampling period reaching padi collected from two California counties and New York, a maximum of 0.78 on 11 May, a two-fold increase 1988 from the beginning of the sampling period (Table 1). Vector infectivity among the three species var- Prowrtion ied considerably with sampling date but was not No. of aphids of hphids County /state tested" transmitting- significantly different (P > 0.05) on any sample BYV date or for the season (x2= 2.15,n = 514, P > 0.05) Fresno, Calif. 90 0.33 (Table 1). In addition to the aforementioned vec- New York 120 0'12 tors, five additional captured aphid species, Acyr- Yolo, Calif. 85 0.18 thosiphon pisum, A. kondot Shinjii, Amphoro- phora spp., B. brassicae, and Macrosiphum rosae a 1 aphidlplant. ~

642 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 84, no. 2

Table 5. Percent plants infected in a random 35-leaf first weeks of the spring aphid flight. Past studies sample from each of six sugar beet fields located on both have suspected and then dismissed R. padi as a sides of a boundary line which separates Overwintered beet fields from spring planted fields in Yolo and Solano coun- significant vector influencing the epidemiology of ties, spring 1988 BYV (Watson et al. 1951, Russell 1965, Jadot 1975). It is unclear from this study what actual role R. Date padi plays in field spread of BYV, because its be- Field no. Location" 22 Feb. 22 Mar. 21 Apr. 21 May havior with respect to feeding on beet plants has 1 South 5 26 71 -b not been studied. The absence of known weed or 2 South 41 41 50 59 crop hosts for BY V other than sugarbeets strongly 3 South 0 25 82 -b suggests that viruliferous R. padi were captured 4 North 0 0 36 100 after feeding on infected beets. At the time of this 5 North 0 0 14 100 study, winter cereals, overwintered sugarbeets, and 6 North 0 0 73 100 orchards were the dominant vegetation in the area

0 Fields were located north or south of the boundary line which surveyed. In the present tests, R. padi did not re- separated overwintered beet fields (south) from early spring plant- produce well on sugarbeets and were raised on oat ed fields (north). seedlings to generate sufficient numbers for labo- b Fields were harvested during the week beginning 22 Apr. ratory studies. When R. padi were transferred from oat seedlings to beet test plants during the transmission study, a high level of mortality was ob- the percentage of infected plants on both sides of served. This high mortality could explain the low the boundary line had increased substantially and transmission efficiency experienced in the green- by May the north fields were 100% infected. house-reared aphids compared with R. padi collected from the field, where the previous host plant Discussion may have been less desirable to R. padi than oats. After confinement for 6 wk in pots containing both While yellow traps are generally not considered a sugarbeet seedling and an oat plant under growth attractive to cereal aphids, Robert (1987) reported chamber conditions, R. padi reproduced on sugar- that they are in fact attractive to such species, and beet plants, indicating that R. padi may become obtained good correlation between yellow traps and adapted to beets. Russell (1965) dismissed R. padi's suction traps (Robert et al. 1988). Kieckhefer et al. role in BYV spread in part due to its infrequent (1976) found R. padi to be more attracted to green association with sugarbeets. Our findings show that than to yellow light. However, they did show that field-captured alate R. padi are efficient BYV vec- approximately 35% of the R. padi were attracted tors and suggest that this species may play a sig- to yellow. Pike et al. (1989) reported that R. padi nificant role in BYV epidemiology, especially if comprised 43% of the total aphids collected in a present in high numbers. suction trap located ~8 km from our sample fields. Neither M. rosae nor any Amphorophora spp. Our finding that 33%of the aphids removed from has previously been reported as a vector of BYV. the yellow board were R. padi compares favorably Their role in virus epidemiology remains to be with their findings and supports previous studies determined. Summers et al. (1990) reported A. (Robert 1987) showing that cereal aphids can be kondoi as a vector under laboratory conditions. Our captured in or on yellow traps. Our field study present work confirms that it was a vector under showed no apparent season-long difference among field conditions but its role in epidemiology re- captured M. persfcae, A. fabae complex, and R. mains unclear. padi with respect to ability to inoculate sugarbeet No infected plants were found on 22 March, a seedlings. week after aphid flights began, but by 21 May, Greenhouses transmission studies conducted to infections in the north fields were well established. test individual aphids from geographically isolated Higher seasonal BYV infection rates in the north colonies for BYV transmission ability showed. dif- fields were probably due to the increased suscep- ferences between species and among geographic tibility of younger plants to BYV infection (Lange collections of the same species. A. fahe complex et al. 1971), combined with the effects of a large from Santa Barbara County was the most efficient spring aphid flight (Pike et al. 1989). vector of the aphids studied, followed by A. fabae complex from Fresno County, and M.persicae from Yo10 County. Variations in vectoring ability among Acknowtedgment 10 clones of A. craccivora have been found in other studies in the transmission of groundnut rosette We thank Vern Burton (University of California Ex- virus (Sylvester 1980) and of spinach yellows virus, tension Entomologist) and Susan Halbert (University of Idaho) for identifying aphids. F. Jackson Hills helped potato leafroll virus, barley yellow dwarf virus, with experimental design and statistical analysis. We bean yellow mosaic virus, pea enation mosaic virus, thank Bryce Falk (Department of Plant Pathology, Uni- and cucumber mosaic virus (Swenson 1968). versity of California at Davis) for his advice on serolog- R. padi was the dominant alate aphid captured ical techniques and for donating BYV antisera. W. F. on the yellow board in sugarbeet fields during the Rochow provided the New York isolate of R. pa&. We April 1991 KIRK ET AL.: BYV TRANSMISSION BY FIELD-COLLECTED APHID VECTORS 643

also thank the sugarbeet growers who cooperated on this Homopteran. Proc. 2nd Conf. Pot. Virus Diseases. project (J. H. Meek & Sons, Hiro Nishikawa, Jim Camp- 104: 55-69. bell, and Tony Borchard), and the California Beet Crow- Peters, D. 1988. A conspectus of plant species as hosts ers Association. This article is a portion of a thesis sub- for viruses causing beet yellows diseases, pp, 87-117. mitted to satisfy requirements for the Master of Science In Virus yellows monograph: a synopsis of research of the senior author in Plant Protection and Pest Man- carried out on beet yellowing viruses and their vectors agement. University of California Integrated Pest Man- in Europe. International Institute for Sugar Beet Re- agement Project Internship Grant and the California search. Pests and Diseases Study Group. November. sugarbeet industry provided funding. Pike, K. S., D. Allison, L. Boydston, C. 0. Qualset, H. E. Vogt & C. G. Summers. 1989. Suction trap reveals 60 aphid species, including Russian wheat References Cited aphid. Calif. Agric. 43(6): 22-24. Reed, R. & B. W. Falk. 1989. Purification and partial Bennett, C. W. 1960. Sugarbeet yellows disease in the characterization of beet yellow stunt virus. Plant Dis. United States. USDA Technical Bulletin 1218. 73: 358-362. Bennett, C. W. & J. S. McFarlane. 1964. A progress Robert, Y. 1987. Aphid vector monitoring in Europe, report on yellows research, pp. 43, 46-47. In Sugar pp. 81-129. In K. F. Harris [ed.], Current topics in beet, 1964. vector research, vol. 3. Springer, New York. Bennett, C. W., C. Price & J. S. McFarlane. 1957. Robert, Y., C. A. Dedryver & J. S. Peirre. 1988. Sam- Effects of virus yellows on sugarbeet with a consid- pling techniques, pp. 1-20. In A. K. Minks & P. Har- eration of some of the factors involved in changes rewijn [eds.], World crop pests. Aphids: their biology, produced by the disease. J. Am. SOC.Sugar Beet Tech- natural enemies and control, vol. 28. Elsevier, Am- , nologists. 6: 479-494. sterdam. Cockbain, A. J., A. J. Gibbs & G. D. Heathcote. 1963. Russell, G. E. 1965. Observations on the epidemiol- Some factors affecting the transmission of sugar beet ogy of sugar beet virus yellows in eastern England in mosaic and pea mosaic viruses by Aphids fabae and 1963 and 1964. Plant Pathol. 14: 95-101. Myzus persicae. Ann. Appl. Biol. 52: 133. Shepherd, R. J. & F. J. Hills. 1970. Dispersal of beet Duffus, J. E. 1973. The yellowing virus diseases of yellows and beet mosaic viruses in the inland valleys beet. Adv. Virus Research. 18: 347-386. of California. Phytopathology. 60: 798-804. 1977. Beet free periods-the key to higher sugar beet Sumbers, C. G., A. S. Newton Jr., M. Kirk & S. R. yields. Calif. Agric. 31(10): 18-19. Temple. 1990. Transmission of beet yellows and 1978. The impact of yellows control on California beet mosaic viruses by non-colonizing aphid vectors. sugar beets. J. Am. SOC.Sugar Beet Technologists. 20: J. Econ. Entomol. 83: 2448-2451. 1-5. Swenson, R. G. 1968. Role of aphids in the ecology Duncan, D. B. 1955. Multiple range and multiple F of plant viruses, Annu. Rev. Plant Pathol. 6: 351-377. tests. Biometrics 11: 1-42. Sylvester, E. S. 1956. Beet yellows virus transmission Gladders, D. W. & D. Peters. 1986. The effect of by the green peach aphid. J. Econ. Entomol. 49(6): previous host plant on the fecundity of Myzus per- 789-800. sicae and its ability to transmit beet yellows virus. 1962. Mechanisms of plant virus transmission by Ann, Appl. Biol. 109: 499-507. aphids, pp. 11-31, In Biological transmission of dis- Heathcote, C. D. 1988. Vectors and virus transmis- ease agents. Academic, New York. sion, pp, 37-41. In Virus yellows monograph: a syn- 1980. Circulative and propagative virus transmission opsis of the research carried out on beet yellowing by aphids. Annu. Rev. Entomol. 25: 257-286. viruses and their vectors in Europe. International In- Tamaki, G., L. Fox & B. A. Butt. 1979. Ecology of stitute for Sugar Beet Research. Pests and Diseases the green peach aphid as a vector of beet western Study Croup. November. yellows virus of sugar beets. USDA Technical Bulletin Heathcote, C. D. & A. J. Cockbain. 1964. Transmis- 1599. sion of beet yellows virus by alatae and apterous aphids. Temple, S. R., V. E. Burton & C. Summers. 1988. Ann. Appl. Biol. 53: 259-266. Managing aphids and viruses to reduce losses to beet Jadot, R. 1975. Transmission des virus de la juanisse yellows. The California Sugar Beet 1987 Annual Re- de la betterave par queques especes d’aphides. Parasi- port. January. tica 31(2): 62-66. Voller, A., D. E. Cidwell & A. Bartlett. 1976. Enzyme Kennedy, J. S. 1950. Aphid migration and the spread immuno-assays in diagnostic medicine: theory and of plant viruses. Nature, Lond. 165: 1024. practice, Bulletin of World Health Organization. 53: Kennedy, J. S., M. F. Day & V. F. Eastop. 1962. A 55-65. conspectus of aphids as vectors of plant viruses. Ex- Watson, M. A. & M.J.R. Healy. 1953. The spread of ecutive Council, Commonwealth Agricultural Bu- beet yellows and beet mosaic viruses in sugar beet reaux, Farnham Royal, Bucks, England. June. root crop. 11. The effects of aphid numbers on disease Kieckhefer, R. W., D. A. Dickmann & E. L. Miller. incidence. Ann. Appl. Biol. 40: 38-59. 1976. Color responses of cereal aphids. Ann. En- Watson, M. A., R. Hull, J. W. Blencowe & B.M.G. tomol. SOC.Am. 69(4): 721-724. Hamlyn. 1951. The spread of beet yellows and Lange, W. H., F. J. Hills & R. 3. Shepherd. 1971. beet mosaic viruses in the sugar beet root crop. 1. Yellows control, pp. 26-28, 30. In The California Field observations on the virus diseases of sugar beet Sugar Beet, 1971. and their vectors, Myzus persicae Sulz. and Aphb Moericke, V. 1951. Eine farbfalle zur kontrolle des fabae Koch. Ann. Appl. Biol. 38(4), 743-764. fluges von blattausen. Insebesondere der pfirsichblatt- laus, Myzode persicae (Sulz). Nachrichtenbl, Deut. Pflanzenschutzdienstes. 3: 23-24. Received for publication 4 May 1990; accepted 10 1955. Neue untersuchungen uber das farbsehen der October 1990.