THE SPREAD OF BEET YELLOWS AND BEET MOSAIC VIRUSES IN THE SUGAR-BEET ROOT CROP I. FIELD OBSERVATIONS ON THE VIRUS DISEASES OF SUGAR BEET AND THEIR VECTORS MYZUS PERSICAE SULZ. AND APHIS FABAE KOCH

A survey of aphids and virus diseases of sugar-beet root crops in eastern England was made between 1940 and 1948. Prior to 1943 the observations were made on fertilizer experiments; from 1943 onwards they were made on commercial fields selected for position in relation to beet and mangold seed crops. The incidence of beet yellows increased with increasing numbers of Myzus persicae , but not of Aphis fabae. The relation with M. persicae was sufficiently close to suggest that it is the most important, possibly the only important, vector of beet yellows virus. Beet mosaic virus also increased with increasing numbers of M. persicae , but the relation was not close enough to exclude the possibility of other vectors.
Numbers of A. fabae on sugar beet were slightly, but consistently, depressed by the use of salt as a fertilizer. Other fertilizers had variable effects. Neither aphids nor virus are likely to be greatly affected by fertilizers.
Beet yellows is most prevalent in areas where seed crops are grown, but within these areas nearness to individual seed crops did not appear to increase its incidence. M. persicae were more numerous on sugar beet in seed-crop areas than elsewhere, and this alone might account for the prevalence of yellows. Beet mosaic virus is more closely associated with seed crops than is beet yellows. It is most prevalent near to seed crops within the seed-crop areas.     

Experiments on the time of application of insecticide to decrease the spread of yellowing viruses of sugar beet, 1954-66

Sprays of demeton-methyl insecticide decreased the spread of yellowing viruses by aphids in sugar-beet crops in England. Between 1957 and 1960, when yellows was prevalent, the incidence, assessed as ‘infected-plant-weeks’, was decreased by 36–41 % by one spray, depending on when it was applied, and by 55 % by two sprays, giving average yield increases of 1½ and 2 ton/acre of roots respectively. Between 1962 and 1966, when yellows spread less, a spray at the time when growers were advised to spray by the British Sugar Corporation decreased yellows incidence by 37 %, whereas sprays 2 weeks earlier or later decreased it by 24 % and 25 % respectively. Between 1958 and 1966 an annual average of 160000 of the country's 440000 acres of sugar beet has been sprayed, often to control Aphis fabae as well as to check the spread of yellows. A spray gives a profitable yield increase when yellows incidence in unsprayed plots is 20 % at the end of August.     

EXPERIMENTS ON THE CONTROL OF BEET YELLOWS VIRUS IN SUGAR-BEET SEED CROPS BY INSECTICIDAL SPRAYS

Field experiments made in eastern England between 1943 and 1951 showed that Myzus persicae lived on the stecklings throughout some winters, and that most plants with yellows in transplanted seed crops were from infections that occurred in the steckling bed. A larger proportion of stecklings sown at the end of July or in early August became infected than of those sown about a month later. The incidence of yellows was reduced by nicotine sprays which cleared the stecklings of aphids after autumn migrations had ceased, thus preventing spread of the disease during the winter. A greater reduction was obtained with persistent and systemic organo-phosphorous insecticides; in one experiment three applications of E 605 reduced incidence to one-ninth that in unsprayed plots. However, in years when stecklings were exposed to large migrations of aphids, even plots sprayed three times had 78% of the plants with yellows. Although spraying often greatly reduces the incidence of yellows, it is unlikely to give adequate control in years and districts in which many viruliferous aphids move in the autumn. Spraying in September and October was usually more effective than in August.     

STUDIES ON THE IMPORTANCE OF WILD BEET AS A SOURCE OF PATHOGENS FOR THE SUGAR-BEET CROP

Beet yellows virus, beet mosaic virus, rust ( Uromyces betae (Pers) Lév.), and downy mildew ( Peronospora schachtii Fuckel.) were found to be common in wild beet ( Beta vulgaris s.-sp. maritima L.) growing on the foreshores of south Wales and southern England. The virus diseases were more prevalent in southeast England than in the west, rust more in the west than in the east, and downy mildew is equally prevalent in all regions.
Beet yellows is the most commercially important disease and is more common in sugar-beet crops in East Anglia than elsewhere in Great Britain. There was no evidence that beet yellows spread in East Anglia from wild beet to nearby sugar-beet crops during the springs of 1958 or 1959, and Myzus persicae Sulz., the principal vector of yellows, was rarely found on wild beet growing on the foreshore.
In glasshouse experiments aphids colonized sugar-beet plants watered with tap water in preference to those watered with sea water. Daily watering with sea water made plants unpalatable to aphids within 14 days. Aphids also preferred leaves sprayed with distilled water to those that had been sprayed with sea water. Salt solutions gave results similar to those obtained with sea water.     

Biological control of the damson-hop aphid,Phorodon humuli (Hom.: Aphididae), using the ladybeetleHarmonia axyridis (Col.: Coccinellidae)

The possibility of usingHarmonia axyridis (Pallas) to control the damson-hop aphidPhorodon humuli (Schrank) in a dwarf-hop garden was studied in northern France in 1994 and 1995. Second and third instar larvae ofH. axyridis were released at different stages of the aphid population increase (early, at the time of insecticide treatment threshold was exceeded and late). In the control, the number of aphids reached 191.3±30.8 per leaf at the end of June. In the plots where 50 larvae per plant were released, the best control was obtained when larvae were released early and the aphid population was approximately 20 per leaf. In this case, the average number of aphid per leaf did not exceed 54.5±10.3 aphids at the end of June, which is lower than the insecticide treatment threshold of 80 aphids per leaf. Indigenous predators, especiallyAdalia bipunctata L., complemented the effect ofH. axyridis.     

Some effects of spraying with thiabendazole on the susceptibility of sugar beet to yellowing viruses and on their vector, Myzus persicae (Sulz.)

In a field experiment fewer sugar-beet plants became infected with aphid-transmitted yellowing viruses in plots that had been sprayed with solutions of thiabendazole lactate than in water-sprayed plots, after exposure to natural infestation with aphids. Subsequent glasshouse tests showed that foliar sprays of o·o1 % thiabendazole lactate in water significantly reduced the proportion of inoculated sugar-beet plants which became infected with beet yellows virus (BYV) or beet mild yellowing virus (BMYV) after inoculation with viruliferous Myzus persicae (Sulz.). This effect on virus transmission was not apparently due to a direct insecticidal action of thiabendazole, because adult aphids usually survived equally well on sprayed and unsprayed plants. Treatment of test plants with thiabendazole did not affect the transmission of beet mosaic virus to them by M. persicae. The fecundity of M. persicae was greatly reduced by transferring them to plants which had been sprayed with thiabendazole or by spraying them with thiabendazole before transfer to unsprayed plants. The fertility of adult Aphis fabae Scop, was also reduced by spraying with thiabendazole. The mechanisms whereby thiabendazole affected fecundity of aphids and transmission of viruses are not understood.     

The use of weather data and counts of aphids in the field to predict the incidence of yellowing viruses of sugar-beet crops in England in relation to the use of insecticides

Partial regression equations were calculated that relate the mean percentage of plants infected with yellowing viruses (beet yellows and beet mild yellowing viruses) in sugar-beet crops at the end of August to the number of days during January, February and March when temperatures fell below – 0.3 °C (31-5 °F) and the mean temperatures in April, for the 21 yr, 1951–71, using weather records from Rothamsted Experimental Station. Regression analyses were also made to find the effect of other factors including mean and minimum temperatures for the same months, and also mean counts of ‘green aphids’, mainly of the vector Myzus persicae, on sugar-beet plants during May and June. Significant relationships were established with all factors, but ‘frost-days’ and April mean temperatures accounted for the greatest percentage of the variance in yellows incidence. The calculations were made separately for the years from 1951 to 1958, when no routine advice was given to farmers about aphid control, and 1959–71 when a ‘spray-warning scheme’ was in operation, and many crops were sprayed at critical times to prevent aphid- and virus-spread. Weather factors had the same effects in both periods, but for any particular weather less virus was spread in the second period than in the first, although there were sufficient aphids, i.e. the numbers expected from the prevailing weather conditions. There was no evidence that insecticide treatment used in any one year affected aphid-incidence in subsequent years. Regression analyses on weather variables were also calculated separately for each of seventeen beet-sugar factory collection-areas, using weather records from local weather stations, and also the Rothamsted weather records. Unexpectedly, the fit of the regressions was always better with Rothamsted weather data than with local weather records. Mean yellows-incidence for the different factory areas declined from south to north, and there was a linear relationship with the square root of the latitude above 50 °C. At the same time the correlation coefficients relating yellows-incidence to ‘frost-days’ became smaller and less significant, and those showing dependence     

Insecticidal control of aphids and the spread of potato leafroll virus in potato crops in eastern Scotland

Field experiments were carried out in eastern Scotland in 1976-78 to test the ability of granular insecticides, applied to soil at planting, and of insecticide sprays applied to the foliage, to control aphids and spread of potato leafroll virus (PLRV) in potatoes. The three years provided contrasting opportunities for virus spread. In 1976, the main vector of PLRV, Myzus persicae, arrived in early June and multiplied rapidly in untreated plots, and PLRV spread extensively. In 1977, M. persicae arrived 4–6 wk later than in 1976 and most spread of PLRV, which was less than in 1976, occurred after the end of July. In 1978, few M. persicae were recorded but the potato aphid, Macrosiphum euphorbiae, arrived early and very large populations developed in untreated plots. However, little spread of PLRV occurred in 1978, supporting other evidence that M. euphorbiae is an inefficient vector of PLRV in field conditions. In each year, granular insecticides decreased PLRV spread to a quarter or less of that in control plots. Thiofanox gave somewhat better and longer-lasting control of aphid populations than disulfoton, especially of M. persicae, but did not give greater control of PLRV spread. Application of three (1976) or five (1977) sprays of demeton-S-methyl to plots treated with granular insecticides further improved the control of M. euphorbiae but had less or no effect on M. persicae, especially where organophosphorus resistant aphids (R1 strain) were found. These supplementary sprays of insecticide did not further improve the control of PLRV but, in 1978, four sprays of demephion or pirimicarb to plots not treated with granular insecticide decreased PLRV spread. These data, together with previous findings, indicate that the amount of virus spread depends on the date of arrival and rate of multiplication of M. persicae in relation to the timing and effectiveness of removal of PLRV sources in crops. It is concluded that in Scotland insecticide granules should be used routinely only in crops of the highest grade of seed potato. Their use for other grades need be considered only in years following mild winters, when aphids can be expected to enter crops earlier and in larger numbers.     

Manganous oxide as a seed-pellet additive for controlling manganese deficiency in sugar-beet seedlings

Summary Experiments in the laboratory, glasshouse and field during 1975–78 tested manganous oxide as a seed-pellet additive for controlling deficiency in sugar-beet seedlings. There was no experimental evidence that manganous oxide in the seed pellet was ever harmful to seedling establishment. On the contrary, germination tests in the laboratory and experiments in the glasshouse indicated that, in certain conditions, manganous oxide may improve plant establishment even when plants are not likely to be deficient, probably by accelerating germination of seed and emergence of seedlings. In field experiments where sugar beet were severely deficient, the plants were heavier and contained more manganese on plots sown with seed pelleted with material containing 50% manganous oxide than on plots sown with ordinary pelleted seed. Applying a foliar spray of manganese sulphate during the third week of June in addition to pelleting the seed with material containing manganous oxide gave bigger yields than either the seed-pellet treatment or foliar spraying alone.     

Detection of the luteoviruses, beet mild yellowing virus and beet western yellows virus, in aphids caught in sugar-beet and oilseed rape crops, 1990–1993

The incidence of beet mild yellowing luteovirus (BMYV) and non-beet-infecting strains of beet western yellows luteovirus (BWYV) in individual winged aphids, caught in yellow water-traps, in sugar beet during the spring and early summer, and in oilseed rape plots in the autumn, was monitored using monoclonal antibodies in ELISA tests from 1990 to 1993. Between 0% and 8% of the Myzus persicae trapped in sugar beet each year carried BMYV, whereas 0% to 4% caught in oilseed rape in the autumn contained this virus. In 1990, 6.5% of Macrosiphum euphorbiae trapped in sugar beet contained BMYV, but in subsequent years less than 1% were carrying virus. Much higher proportions (26–67%) of the M. persicae tested from sugar beet contained BWYV, and similar proportions tested from oilseed rape (24–45%) also carried this virus in the autumn. In contrast only 3–19% of the M. euphorbiae caught in sugar beet contained BWYV, and none in oilseed rape. In 1991 and 1992 large numbers of Breuicoryne brassicae were caught in the plot of oilseed rape, of which over 50% contained BWYV; none were carrying BMYV. In transmission studies between 1990 and 1992, 1% and 27% of M. persicae transmitted BMYV and BWYV respectively to indicator plants; subsequent ELISA tests on the same aphids showed that 3% and 33% respectively contained the two viruses. One percent of M. euphorbiae transmitted BMYV, but none were found to contain BMYV using ELISA; 15% transmitted BWYV whilst only 5% were found to carry the virus. In 1992 and 1993 the incidence of BMYV-infection in the sugar-beet fields in which aphids had been trapped ranged from 1.2%, in a field which had received granular pesticide (aldicarb) at drilling plus three foliar aphicidal sprays, to 39.5% in a field which had received only one foliar spray. In 1992 in a sugar-beet crop which had received no aphicidal treatments, and where 2.8% of immigrant M. persicae and 2.5% of M. euphorbiae contained BMYV, 11.6% of plants developed BMYV infection. Lowest levels of infection were associated with the use of granular pesticides at drilling. In 1990, 80% of oilseed rape plants in a field plot were infested with a mean of seven wingless M. persicae per plant by mid-December; 37% of these plants were infected with BWYV. The studies show that M. persicae is the principal vector of BWYV, and large proportions of winged M. persicae carry the virus, in contrast to BMYV, which is consistent with the common occurrence of BWYV in brassica crops such as oilseed rape.     

Breeding for resistance to infection with yellowing viruses in sugar beet

Differences in resistance to infection with beet yellows virus (BYV) and beet mild yellowing virus (BMYV) have been observed in virus-tolerant sugar-beet breeding material. The results of glasshouse virus-susceptibility tests usually agreed well with those of field experiments in which plants were exposed to artificial, or natural, infestation with viruliferous aphids. Breeding lines and varieties, which showed resistance to BYV when Myzus persicae Sulz, was used as vector, generally showed a similar resistance to this virus when Aphis fabae Scop. was used. Varieties which were resistant to infection with one virus were not necessarily resistant to the other, although some showed resistance to both BYV and BMYV. Preliminary results suggest that resistance to infection may be controlled by recessive genes which occur widely in sugar-beet cultivars. The mechanism of this form of resistance is not understood, but it does not appear to be closely associated with resistance to the aphid vectors of the viruses. The observed differences in resistance to infection demonstrate the possibility of breeding a sugar-beet variety in which two forms of resistance to virus yellows, tolerance and resistance to infection, are combined.     

Leaf surface wax and plant morphology of peas influence insect density

Insect predators and parasitoids adhere better, forage more effectively, and take more aphid prey on pea plants (Pisum sativum L.) (Leguminosae) with mutations that reduce the crystalline wax bloom on the plant surface. To assess the agronomic potential of this trait for pest management, abundance of pea aphids (Acyrthosiphon pisum L.) (Homoptera: Aphididae) and coccinellid predators, and percent parasitism of the aphids were evaluated on pea lines differing in wax bloom and plant architecture over two field seasons. Three pairs of pea lines were evaluated, each pair with a different architecture and differing within the pair in the amount of surface wax bloom (reduced or normal). The trials included plots treated with a narrow spectrum insecticide (pymetrozine) to reduce aphid populations and untreated controls. Reduced wax peas had significantly fewer aphids per plant in 2002 but not in 2003. Total natural enemy abundance was greater on reduced wax than on normal wax pea lines in both years of the study. Pymetrozine reduced aphid densities significantly in both years. Among the four pea lines evaluated for yield, seed yield per plant was affected by plant morphology and insecticide treatment. Yield was greatest on semileafless plants and on pymetrozine sprayed plots in both years. Yield of the reduced wax line in the semileafless background was similar to or exceeded yield in its normal wax sister line, suggesting that this morphological type was best for an agronomically viable reduced wax phenotype. Pea weevil (Bruchus pisorum L.) (Coleoptera: Bruchidae) damage to seed was overall more frequent on seeds from reduced wax varieties than from normal wax varieties. The results illustrate the trade‐offs associated with a reduced wax trait in peas but also show that certain combinations of reduced wax and gross morphology lead to reduced pea aphid populations and yields similar to those of normal wax peas.     

APHID BEHAVIOUR ON HEALTHY AND ON YELLOWS-VIRUS-INFECTED SUGAR BEET

Myzus persicae Sulz., M. ascalonicus Doncaster, Aphis fabae Scop, and Aulacorthum solani Kalt., when caged on sugar-beet leaves in the glasshouse preferred yellows-virus-infected leaves to healthy ones; they chose those with the most severe symptoms on which they bred more rapidly and lived longer than on green leaves. M. persicae behaved similarly on whole plants in the glasshouse. The previous host influenced the aphid's preference. Differences between the multiplication rates of aphids on healthy plants of inbred sugar-beet varieties were eliminated or reversed by infection with yellows virus.
Spraying healthy plants with either sugar solutions or hydrolysate of casein increased the multiplication rate of M. persicae , but much less than did virus infection.     

New approaches for restricting spread of potato leafroll virus by different methods of eradicating infected plants from potato crops

Experiments were made at Invergowrie in 1984 and 1985 to compare the spread of potato leafroll virus (PLRV) after removing infected plants by three different methods; conventional roguing, desiccation with diquat, or incineration for 45–60s using a propane gas flame. Potato leaf roll 'infector' plants, grown in plots of virus-free Maris Piper seed potatoes, were artificially infested in June with aphids (Myzus persicae) from a laboratory culture, and removed from the plots after 2 or 3 wk. In both years, natural infestations of potato aphids were scarce during this period. There was no significant difference in the proportion of tubers infected with PLRV in adjacent plants after the neighbouring infector plants had been rogued by hand or desiccated with diquat, but the proportion was considerably reduced following incineration of the infector plants. In 1984, the spread of PLRV in conventionally rogued plots was also significantly reduced by a mixture of deltamethrin plus heptenophos, applied four times from 80% crop emergence, and was almost eliminated by a treatment with aldicarb granules, either at planting, or as a side-dressing 5 wk later. In 1985, delaying infector removal by 8 days in early July significantly increased the spread of PLRV to neighbouring plants from 2.3% (1 July) to 8.3% (9 July). A single application of deltamethrin plus heptenophos to infectors 1 wk before removal did not significantly decrease spread. Although incineration was quick and effective, the value of this method of eradicating infector plants in seed potato crops is limited because it failed to destroy infected tubers.     

THE INFLUENCE OF DENSITY OF PLANT POPULATION ON THE INCIDENCE OF YELLOWS IN SUGAR-BEET CROPS

The incidence of yellows virus in sugar-beet crops was reduced by increasing the density of plant population. The variations in plant population were obtained by differences in row width and singling distance. The differences in susceptibility between large- and small-topped varieties, and between early and late sown crops, could not be attributed solely to differences in plant size. It is suggested that close planting would increase the yields of sugar beet and reduce the losses caused by yellows virus. Roguing infected plants during the early part of the growing season did not reduce the incidence of disease.     

Early-season predation impacts the establishment of aphids and spread of beet yellows virus in sugar beet

The potential of predators to impact the establishment of aphid vectors and the spread of beet yellows virus in sugar beet was examined. Myzus persicae carrying beet yellows virus (BYV) were released on six interior sites and six edge sites in each of four fields at the end of May. Aphids established at low densities and BYV was spread in circular patches around the infested plants at all sites. The number of diseased plants per patch at the end of September ranged from a field-average of 130 to 210 in the four fields. There was a weak tendency towards better aphid establishment and greater virus spread in fields in less complex landscapes. Edge sites had less virus spread than interior sites in one field, more virus spread in two other fields, and there was no statistically significant difference in the fourth field. In the field where virus spread was lowest at edge sites, we used predator exclosure and direct observation to manipulate and quantify the effects of early season predation. On a warm day in early June, 81% ofAphis fabae exposed to predators on young beet plants disappeared during a 24 h period, compared to 10% of aphids protected by clipcages. Intermediate levels of predator exclusion, allowing aphids to walk away but restricting predator access, showed that predation was responsible for aphid disappearance.Cantharis lateralis L. (Coleoptera: Cantharidae) was the most frequently observed foliar predator (>90%). It was found eating aphids on several occasions. The incidence of predators was 1.8 per plant per h in the field interior and 3.8 per plant per h. near the edge. In the same field, aphids and virus were released in six edge and six interior sites, that were surrounded by 0.5 m high plastic open-top barriers (‘exclosures’). Pitfall trapping inside the barriers reduced potential soil predator densities to ca. one-tenth of the open field level and arrivals of flying predators were reduced. Inside the exclosures, aphid establishment was enhanced, and virus spread at exclosure sites was increased by about 50% compared to open sites. Foliar and pitfall sampling yielded the following predators:Cantharis lateralis, C. rufa L. (Coleoptera: Cantharidae),Coccinella septempunctata L.,C. undecimpunctata L. (Coleoptera: Coccinellidae),Pterostichus cupreus (L.),Harpalus rufipes (de Geer),Patrobus atrorufus (Strom),Trechus quadristriatus (Schrk.),Bembidion lampros (Herbst) (Coleoptera: Carabidae). In a laboratory no-choice trial (with 10M. persicae /day offered), each of these species ate aphids with consumption rates varying from 1.7 to 9.2 aphids/day. The results show that early predation substantially impacted aphid establishment in one field, and resulted in reduced virus spread. Results in the other fields show that these results cannot be easily generalized.     

The effects of yellowing viruses on yield of sugar beet in field trials, 1985 and 1987

The separate effects of beet yellows virus (BYV) and beet mild yellowing virus (BMYV) on yield of sugar-beet cultivars inoculated at different growth stages were assessed in field trials in 1985 and 1987. Early or mid-season inoculation decreased sugar yield by up to 47% for BYV, and up to 29% for BMYV. Infections after the end of July had no significant effect on yield. Both viruses caused significant increases in the juice impurities sodium, potassium and amino-nitrogen after infecting plants early in the season. Yield losses associated with infection were determined by the causative virus, the time of infection, and susceptibility of the sugar-beet cultivars.     

A controlled environment study of the effect of leaf physiological age on the movement of apterous Myzus persicae on sugar-beet plants

Apterous Myzus persicae were found to move frequently from leaf to leaf on sugar-beet plants in controlled environment conditions. It is suggested that aphid movement can be related to changes in the rate and content of translocate flow during leaf development. These changes make newly-emerged leaves nutritionally favourable to colonising aphids and make expanding leaves slowly wane in favourability during the process of ‘sink to source’ conversion leading to aphid dispersal from the leaf. Variation in temperature was not found to alter the rate of aphid movement or the period (measured in thermal time) that aphids spent on particular leaves. However, the lower temperature was found to increase the rate of aphid development, aphid size and fecundity; these effects could also be due to nutritional factors. This dispersal behaviour may be a tactic to maximise food intake by a polyphagous aphid and increase the probability that nymphs are deposited on nutritionally-favourable leaves. The implications of the interleaf dispersal of apterous M. persicae for within- and between-plant spread of beet yellows virus (BYV) and beet mild yellowing virus (BMYV) are discussed.     

SEED AND SOIL TREATMENT WITH SYSTEMIC INSECTICIDES TO PREVENT APHID COLONIZATION OF EMERGING BEET SEEDLINGS

Dimefox at 2 lb. or diethyl ethylthiomethyl dithiophosphate (Thimet) at 1 lb. applied at drilling in 100 gal. water along the drills, or seed treated at rates giving 6–8 oz. Thimet or 8–24 oz. diethyl ethylthioethyl dithiophosphate (Disyston) per acre†, made sugar beet seedlings toxic to aphids up to 30 days after sowing four root crops in April-May, and up to 30–40 days after sowing five steckling crops in autumn. Malathion, demeton, demeton methyl, bis (dimethylamino) azido phosphine oxide (N.C.7) and schradan were less effective. The infestation of green aphids was decreased by the treatments during what is often a critical period for virus infection in summer-sown stecklings and occasionally in spring-sown root crops. Germination was 73–100% of the control after soil treatments, 91–98% after Disyston seed treatments and 62–84% after Thimet seed treatments. The treatments slightly decreased Aphis fabae injury to steckling seedlings in 1955 and the number of plants with yellows in a steckling experiment in 1956.