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INTRODUCTION
The aphid-borne viruses which collectively produce the disease commonly called "yellows" have had serious effects on CalifomiXs sugarbeet industry. From about 1950 to 1970, beet root yield averaged around 20 tons per acre despite many improvements in the technology of sugarbeet production. The failure of yields to increase during this period has been largely attributed to the yellows viruses (Duffus, 1977). Since the widespread use of appropriate control measures, root yield has risen from 24 to 28 tons per acre for the 200,000 and more acres of sugarbeets grown annually in California.
Dr. Raymond Hull of the Rothamsted Experiment Station in England, a specialist on virus yellows, visited California in 1951 and was convinced that the symptoms of a malady we then called "Salinas yellows" or "June yellows" were comparable to those of a virus-induced yellows in Europe where the disease had been known for many years. Shortly after this, Dr. G. H. Coons and Dr. C. W. Bennett of the U.S. Department of Agriculture proved that an aphid-borne virus was indeed causing a yellowing of sugarbeets in California (Bennett, 1960). Since then a great deal of research has been done to define the problem and excellent progress has been made in the development of control measures.
THE DISEASES AND THEIR VECTOR
Two main viruses cause yellows symptoms. One, the beet yellows virus (BYV) is more severe in its effect on sugarbeet than is the other, the beet western yellows virus (BWYV). The latter, which was identified and described by J. E. Duffus (1960, 1961), causes less than one-half the loss caused by the BYV when plants are infected at a comparable stage of growth. BWYV, however, is more widespread in occurrence, and in most years is the predominant virus causing economic losses. A third virus, the beet mosaic virus (BMV), often occurs with BYV and also causes yield reductions of economic importance (Shepherd, et at, 1964). The effects of the viruses are additive: sugarbeets infected at thinning time with all three viruses have suffered losses in root yield of as high as 50 percent.
The yellowing viruses, especially the BYV, can also cause losses in root sucrose concentration. Experiments at UC Davis have shown a 0.1 percentage point loss in sugar concentration and a ton per acre loss in root yield per 10 percent increase in BYV infection for plants inoculated soon after thinning and evaluated for virus infection about July I (Loomis and Bennett, 1966; Hills et al., 1972) (Fig. 1).
The three viruses are transmitted primarily by the green peach aphid (Myzus persicae), and must be acquired by aphids from living plants before they can be transmitted to healthy sugarbeets. They all differ in the length of time they are retained by aphids. An aphid carrying BMV loses its ability to infect in from 2 to 4 hours. For BYV this period is from 12 to 72 hours, but aphids can retain BWYV for life (Table 2).
The viruses also differ in the plants they can infect, but one very important fact is that the sugarbeet crop itself is the most important source of inoculum for the beet mosaic and the beet yellows viruses. Although both viruses infect other plants, most disease epidemics are associated with transferral from sugarbeet-tosugarbeet. Sugarbeets are also an important source of BWYV, but this virus is also commonly found in several other host plants.
Symptoms
Beet Yellows Virus (BYV). An irregular yellowing of older leaves,
frequently more intense at the tips of leaves, appears as soon as 4 weeks
following infection. Yellowing may progress to where the entire leaf blade
is yellow, with only narrow bands of green along veins. Leaves become thick
and brittle when crumpled in the hand. Plants infected by the sugarbeet
mosaic virus are often also infected with BYV. Such plants are stunted,
light green and show severe symptoms of sugarbeet mosaic before typical
yellows symptoms develop or older leaves.
Beet Western Yellows Virus (BWYV). In sus. ceptible varieties, BWYV symptoms are im. possible to distinguish from those of mild strains of BYV. In varieties resistant to BWYV this virus seldom induces symptoms that car be clearly recognized. About all that can be seen is a slight lessening of the normal greener color and a vague interveinal yellowing, usually at the tips of older leaves. The virus reduce,, yield, however, even though symptoms do no, show.
Beet Mosaic Virus (BMV). Symptoms appeai on young leaves as soon as I week after inoc ulation. There is much variation in the typi of mosaic mottling-ranging from more or les circular light-green spots to very irregula: splotches of light and dark green. At time the first symptoms may be a yellowing o clearing of veins of young leaves. Symptom tend to disappear as temperatures warm, bu often reappear in autumn as the weather cool again.
The Green Peach Aphid (GPA)
Although other aphids can transmit the yellowing and mosaic viruses,
the GPA appears to be the most important. During the mild winters of California's
beet-growing areas, GPMs overwinter on a variety of weed and crop hosts.
Climatic conditions favorable for reproduction, development, and dispersal
flights seldom occur before March in central California and not before
April in some years.
As optimum temperatures and favorable host plant situations develop, aphid populations may increase dramatically and extensive dispersal flights occur. Figure 3 shows typical dispersal flight patterns in various California areas.
When daily maximum temperatures exceed 80OF and host conditions become less favorable, aphid populations decrease to very low levels and virus transmission essentially ceases. A recognition of aphid activity patterns are important in planning strategies for virus control. For example, beets planted in February-March in central California, where a large acreage of the previous year's planting has overwintered, will be exposed to extensive flights of the GPA for an extended period while they are young and very susceptible to damage by the viruses that many of these insects will be carrying. Planting about May I usually allows emerging plants to escape yellows and mosaic infection due to termination of aphid flights.
It is important to be able to identify the GPA. The most useful characters are the presence of converging frontal tubercles and the cornicles which are slightly inflated at the terminal portion. The potato aphid commonly occurs on sugarbeet but is of little importance in virus transmission. This aphid can be dis- tinguished by the lack of frontal tubercles and by the long tapering cornicles with scale-like reticulations covering the terminal portion.
The winter of 1950 in California was particularly wet and many fields in northern California could not be harvested in the fall as was the custom. Surprisingly, the roots left in the ground did not rot and were of good quality when harvested in the spring of 1951. Thus the practice of overwintering was born. The industry soon realized the benefits to be had from operating factories much longer annually than before, and farmers were able to plant more acres as the result of the increased factory capacity. As overwintering increased, however, the aphid-borne virus problem be- came more and more severe until research and careful observation determined that the overwintering beet crop was the principal source of virus inoculum for the crop following. Additional research and experience led to the development of several methods of control.
METHODS OF CONTROL
Some degree of control can be achieved by one or more of the following: eliminating virus sources, planting to escape infection, using a resistant variety, and preventing infection by aphid control. Which method or combination of methods to use depends upon the local situation.
The Beet-free period
The most effective method of control is to break the sugarbeet-to-sugarbeet
cycle of virus transmission by providing a degree of isolation between
older infected crops and newlyplanted beets. This isolation can be in
terms of time or space. In terms of time, the removal of old crops before
the emergence of new beets gives a beet-free period and no infected plants
from which to acquire virus.
Another important aspect of using a beet-free period for virus control is the matter of how far aphids can carry viruses from old beet fields to new crops. Studies in California (Shepherd and Hills, 1970) have shown that a distance of from 10 to 20 miles between overwintered sugarbeet fields and new spring plantings is sufficient to appreciably delay the introduction of these viruses into new plantings (Fig. 6). Experience has shown that a distance barrier of even 5 miles is likely to be an effective means for improving production (Table 3).
To achieve control by a beet-free period, growers must completely destroy all living virus sources from previous crops. Old beet crowns, beets missed by harvesters, and weed beets in waste areas must be destroyed. Growers should be careful not to allow beets to produce seeds which will become weed beets in other crops.
The California Beet Growers Association and the sugar processors have cooperatively agreed that overwintering should be limited to certain areas and that in other areas beet harvest will be completed in the fall, thus providing a beet-free period in these areas to enable growers to plant in early spring. Such arrangements have been quite successful, and have been administered by the formation of a grower-processor committee in each of the local districts of the California Beet Growers Association.
Late planting
In the mid 1950s, surveys by sugar companies established that late-planted
beets in California's central valleys frequently remained free of yellows,
and produced higher yields than did early-planted fields which became exten-
sively infected early in the season. Studies of aphid dispersal flight
patterns showed that escape from disease is due to the fact that the population
of flying aphids rapidly diminishes in most years, due to warm weather
and predaceous insects, and essentially disappears by early June (Fig.
3).
Delayed planting was &we overdone, however, with some growers planting as late as July or August. The resulting yields were usually disappointing and often not profitable. Studies at Davis have indicated that planting later than May almost invariably reduces production regardless of harvest date and despite escape from yellows (Tables 4 and 5). In areas where beets are not overwintered, planting is usually as early as possible to permit profitable yields for the harvest date assigned by the sugar company. Beet-free periods in these areas are essential for profitable crop production.
Resistant varieties
The USDA Sugarbeet Research Station at Salinas, California, has developed
varieties outstanding in their ability to produce despite yellows. In many
tests throughout California under conditions of moderate to severe yel-
lows, these varieties have produced an average of 25 percent more sugar
per acre than did a standard nonresistant hybrid. Resistant varieties
were released for commercial use in 1968 and have undoubtedly contributed
to the rise in sugar production throughout California since that time.
Despite this increased production, however, there are still improvements
to be made because the new varieties still lose a considerable amount of
their potential root yield when infected with yellows viruses at an early
stage of growth (Fig. 7).
Aphid control
Where sugarbeets are overwintered, production can be improved 15
to 20 percent over that achieved by a May planting by seeding in early
April and protecting the young plants from virus infections by limited
applications of an effective aphicide. Depending upon duration of aphid
flights in a given year, from one to three applications of an aphicide
are usually necessary. The best procedure seems to be placing an effective
systemic granular aphicide just below the seed at planting time. This application
usually controls aphids for about 4 weeks and can be followed with one
or two topical applications of an aphicide if the number of wingless aphids
reaches the economic injury level of 0.5 per plant. Such a procedure
delays virus infection and is usually effective in improving production
(Tables 6 and 7). Where there are overwintered beets, planting earlier
than April I runs a risk of too long an exposure of the new crop to viru-liferous
aphids, and the inability to prevent extensive early infection in spite
of repeated aphicide applications.
Table 7 illustrates the possibility for improving sugarbeet yields by a combination of control measures: a month advancement in planting date (April instead of May), a variety with some yellows resistance (USH9B instead of USH7A), and the suppression of yellows by timely use of aphicides (aphid control).
Monitoring Aphids
To determine whether or not an additional aphicide application may
be necessary, examine at least ten plants, in each quarter of a field.
Count apterae (wingless aphids) only as their presence indicates a loss
in the effectiveness of the insecticide. Counts can be by direct observation
on the plants or by collecting aphids in a collection device such as the
Gray & Schuh (1941) shaker. If there are 0.5 or more apterae per plant,
an additional control treatment is indicated.
