Management of Aphid-Borne Legume Viruses
Station Bulletin 615 June 1974
Agricultural Experiment Station Oregon State University, Corvallis ABSTRACT
Most legume viruses are aphid-borne. The viruses involved in tem- perate North America and their host plant relationships are described, as are the host plant relationships of the principal North American aphid vector, the pea aphid Pest control measures for the pea aphid and legume viruses are reviewed Aphid-resistant perennial legumes are advocated as a means of simultaneously reducing the aphid and the virus problem in both annual and perennial legumes Some of the ramifications of such resistance are discussed
Authors:
K. G. Swenson, Professor of Entomology, Oregon State University, has worked on legume virus transmission in California, New York, Oregon, and Australia.
D. J. Hagedorn, Professor of Plant Pathology, University of Wisconsin, recently spent a sabbatical leave at Oregon State University.
Acknowledgement:
This bulletin isa contribution of the Oregon StateUniversity Plant Protection Comittee. This Committee is an interdisciplinary group dedi- cated to the formationof an interdepartmental pest management curriculum and to the furtheranceof research on pest management and control and on plant health. MANAGEMENT OF APHID-BORNE LEGUME VIRUSES
K. G. Swenson and D. J. Hagedorn
Legume viruses are significant pathogens of some of our most important crop plants and often incite diseases which resultineconomic loss to the farmer or rancher. They are a problem because they are able to survive from season to season in perennial legumes. There would be little problem with legume viruses if only annual legumes were grown because hosts of these viruses are primarily restricted to the Leguminosae, a notable exception being the alfalfa mosaic virus. Both annual and perennial legumes are made available to the viruses in temperateNorth
American agricultural situations by the activities of the pea aphid,
Acyrthosiphon pisum (Harris) (Figs. 3 and 4). Some perennial legumes harbor the wintering eggs of the pea aphid which spreads the viruses amongperennial legumes and also carries the viruses from perennial to annual legumes.
The principal viruses involved in temperate North America are alfalfamosaic, bean yellow mosaic, alsike clover mosaic, pea enation mosaic, peamosaic, pea streak, and red clover vein-mosaic viruses(Figs.1 and 2). Alsike clover mosaic, pea mosaic and bean yellow mosaic viruses are verysimilar and may be related strains.
An epidemiological approach to management of legume viruses, the development of aphid-resistant perennial legumes, is advocated here the objectives being to reduce the number of vectors and the virus reservoir which they perpetuate. Migrations to annual legumes would be later in the season and less intense, decreasing the probabilityof direct feeding injury and virus spread. This should decrease the need to apply insecticides or
release mass-produced parasites to protect the annual legumes. Anyway, much virus spread in the annual legumes already would have taken placeby 2
the time the aphids were sufficiently numerous to invoke such measures.
Epidemiological Relationships of Legume Viruses
Alfalfa (Medicago sativa L.) serves as a perennial host for alfalfa mosaic (Grill etal. 1970, Oswald 1950) and pea enation mosaic viruses
(McEwen and Schroeder 1956); red clover (Trifolium pratense L.) as a perennial host of alfalfa mosaic, alsike clover mosaic, bean yellow mosaic, pea mosaic, pea streak, and red clover vein-mosaic viruses (Hanson and
Hagedorn 1961, Diachun and Henson 1956); white clover (Trifolium repens L.) as a perennial host of alfalfa mosaic, bean yellow mosaic and pea enation mosaic viruses (Houston and Oswald 1953, Kreitlow and Price 1949, McEwen and Schroeder 1956); and sweetciover (Melilotus spp.) as a perennial host of bean yellow mosaic and pea enation mosaic viruses (Harter and Zaumeyer
1944, McEwen and Schroeder 1956, Zaumeyer and Thomas 1957). Alsike clover
(Trifolium hybridum L.) is susceptible to all of these viruses except pea enation mosaic virus but the continuing sharp decrease in the acreage of this plant in the United States indicates that it is likely to be of relatively little importance as an aphid or virus host.
Susceptible annual legumes include crimson clover (Trifolium incarnatum
L.), pea (Pisum sativum L.), vetches (Vicia spp.), and bean (Phaseolus vulgaris L.). Crimson clover and some pea varieties are susceptible to all of the viruses. Crimson clover, vetches and field peas (P. sativum arvense Poir.) are planted as winter crops in some areas such as western
Oregon. Under these conditions, they may germinate and grow in the fall before aphid activity ceases and serve as winter hosts for the aphids and viruses (Rôckwood and Reeher 1942).
The importance of legume viruses in peas varies considerably from year to year and among different geographical areas. Economically important virus disease outbreaks are probablyassociated with unusuall' uccsfu 3
wintering and subsequent development of aphids. Bean yellow mosaic virus, which, is sometimes very common in peas (1-lagedorn and Walker 1950, McWhorter
1954), has gained new importance in that it may also be involved in a viral complex causing streak diseases of peas (Kim and Hagedorn 1959;
Schroeder, Provvidenti and McEwen 1959). Bean yellow mosaic and bean comon mosaic viruses are two of the three major viruses of beans (Phaseolus vulgaris L.) in North America (Zaumeyer and Thomas 1957) and are spread in bean fields by migrating aphids of many species which do not breed on legumes (Hampton 1967, Swenson 1957, Zaumeyer and Kearns 1936).
Traditional Management (Control) Practices
The management or control of legume viruses for many years has been primarily through discovering or incorporating resistance in new varieties.
Key research efforts with varying degrees of success have been undertaken in the following virus-host combinations: Alfalfa mosaic virus in alfalfa
(Crill etal. 1971); bean common mosaic virus in bean (Pierce l935a)
(Parker 1936); bean yellow mosaic virus in bean (Baggett and Frazier 1958,
Hagedorn 1953); pea (Johnson and Hagedorn 1958), red clover (Diachun and
Henson 1960) and subetrranean clover (Hutton and Peak 1954); pea enation mosaic vi rus in pea (Schroeder and Barton 1958); pea mosaci vi rus in pea
(Pierce 1935b); pea seed-borne mosaic virus in pea (Hagedorn and Gritton 1973,
Hampton and Baggett 1972); subterranean clover stunt virus in subterranean clover (Grylls and Peak 1960).Among these, bean varieties resistant to bean conimon mosaic virus, and pea varieties resistant to bean yellow mosaic virus, pea enation mosaic and pea mosaic viruses are in 3resent agriciiltura use.
In addition to the researches mentioned above, there is the possibility that virus-resistant red clover could be developed (Stuteville and Hanson
1964). Existing red clover varieties and breedini lines contain plants 4
which are resistant to one or more of the following viruses: bean yellow mosaic virus, pea mosaic virus, red clover vein-mosaic virus.
Pea aphid has been controlled in peas and forage legumes with insec- ticides and pea aphid resistance has been sought in alfalfa, primarily for arid areas. Resistant varieties may produce a 3-fold increase in yield
(Harvey et al 1971).
Biological Control
There is a tendency to discount the possibility of reducing virus spread by biological control of aphids. This may result from considering control of virus spread in individual fields rather than on an area basis.
The papers reviewed by Swenson (1968) showeda relationship between virus spread and aphid numbers in different areas and in different seasons. Any factor which consistently depresses aphid populations can be expected to have a similar or greater effect on virus spread. Thus, the destruction of Myzus persicae oviparae by predators on peach trees in the fafl had a direct effect on virus spread in sugar beet and potato in the following year in eastern Washington (Tamaki et al. 1967. Numerous parasites and predators of the pea aphid are known (Cook 1967, Mackauer 1971), but they have only been partially effective, at best, in the control of this insect, except in the case of Aphidius smithi Sharma and Subba Rao in some parts of
California (Hagen and Schlinger 1968) and Oregon. A. smithi is widely dis- tributed in Oregon, either as the result of spread from introductions or from adjoining states, but only in the Blue Mountains of northeastern Oregon does it give appreciable control of the pea aphid (Halfhill et al 1972).
In this area, A. smithi has largely replaced the native A. ervi pulcher
Baker which parasitizes both the pea aphid and the alfalfa aphid,
Macrosiphum creeli Davis. A. smithi parasitizes only the pea aphid and
may have caused the selective development of . creeli, which was previously relatively rare in this area as a pest (Halfhill , cited in Johansen and
Eves 1973).
A New Approach to Management of Legume Viruses
Another approach to the control of aphid-borne legume viruses would be the development of aphid-resistant varieties of perennial legumes.
Alfalfa and red clover appear to be the principal source of wintering pea aphids. This approach is suggested as an addition to, rather than a substitute for, developing resistance to specific viruses in crop plants where genes for resistance can be found. It would, however, provide a less fragmented approach to the problem of managing legume viruses than developing varieties resistant to specific viruses, and be likely to have a greater overall effect on the virus problem because aphid resistance would affect the prevalence of the entire complex of aphid-borne viruses.
There are several advantages in aphid-resistant perennial legumes as compared to incorporating resistance to viruses into each crop where they
are a problem. First of all , the pea aphid is one of the most serious pests of alfalfa and must be controlled anyway. In fact, several research programs for developing pea aphid resistant alfalfa varieties are in progress (Hunt et al. 1971, Harvey et al. 1972), but they are primarily in relatively arid regions where virus transport to annual legumes is not a problem and from which resistant varieties would not be suitable for other regions from the standpoint of desirable agronomic characteristics. Red clover varieties also differ greatly in their resistance to pea aphid and resistant varieties would contribute to aphid control in this crop (Wilcoxon and Peterson 1960).
The pea aphid is also an important pest of peas and has been controlled 6
primarily by insecticides in this crop. Aphids on peas are another problem
that would be greatlydiminished by aphid-resistant perennial legumes.
Secondly, the number of parasite-host relationships is much smaller
than would be required if control were based on virus resistance ineach
crop. E.g., if bean yellow mosaic virus were dealt with on the basisof
plant resistance to the virus, virus-resistant clovers, peas, and beans
would all have to be developed separately and for all the other viruses
involved. Wilcoxon and Peterson (1960) found that virus spread was cor-
related with susceptibility to pea aphid in red clover varietiesand con-
cluded that breeding aphid-resistant varieties was a more practical approach
to reducing virus spread than developing varieties resistant tothe several
viruses present in red clover. Eichmann and Webster (1940) also recognized
aphid-resistant alfalfa varieties as a possible solution to the peaaphid
problem in peas in the Blue Mountain region of Oregon and Washington.The
proportion of acreage devoted to alfalfa seed production hasincreased
greatly in this area in recent years, however, due to the use ofalkali
bees and leafcutter bees.
Stanford (1960) has described the maintenance of resistance in a crop
as a contest between plant breeders and pathogens becauseof the appearance
of new races or variants of the parasite, although disease resistancehas
been quite stable in some varieties. Use of resistance to aphidswould
entail fewer "contests" than developing and maintaining resistancein all
the important virus-host combinations. There is less experience with the
stability of aphid resistance in plants. Within a few years after discovery
of the spotted alfalfa aphid, Theriophis maculata(Buckton), in the United
States, a biotype of the aphid was found which couldsurvive and reproduce 7
on clones of alfalfa resistant to the general population of this aphid
species (Pesho etal. 1960). On the other hand, the Lloyd George red
raspberry has remained resistant to Amphorophorarubi in the Pacific
Northwest for 30 years (Stace-Smith 1960). Genetic variation in the pea
aphid is well known, various biotypes havingbeen discussed (Eastop 1971).
A further advantage of aphid resistanceis that control will be
obtained of some viruses incrops where the particular virus is not con-
sidered a sufficiently urgent problem toresult in development of a specific
control measure. The combined effect of several such minor viruses might
add up to a significant total. Decreasing the vector population is the only
approach which would simultaneously decreasethe problem with all these
viruses. Finally, aphid-resistant perennial legumes might prolongthe
"resistance life" of virus-resistantlegume varieties. Diminished spread
of the viruses would decrease theopportunity for viarl mutations.
A problem in the use of aphid-resistantvarieties is that there would
still exist an uncultivated populationof perennial legumes along roadsides,
in waste lands, etc. Those that appear to be most importantas aphid reser-
voirs are, however, not nativespecies and are varieties which have been
cultivated. Cultivation of aphid-resistant varieties fora period of time
would probably result in the gradualreplacement of the present uncultivated
legumes by aphid-resistant plants. Even if this did not happen, cultivated
perennial legumes would still have beenremoved as a source of virus-
transmi tti ng aphids.
Aphid resistance would not haveto be complete to be useful. The
physiological condition or suitabilityof a plant as an aphid host is a primary regulator of aphid populations. A physiologically optimal host plant would have to bea completely susceptible genotype. Generally, an 8
aphid population can increase in spite of parasites and predators as long as the host plant is physiologically suitable. The antibiotic effect of a partially resistant host plant would decrease the developmental rate of the aphid but not that of the natural enemies, permitting the natural enemies to overtake the aphid population sooner on resistant than on susceptible varieties (Starke etal. 1973).
This report has been concerned primarily with the pea aphid as a vector of legume viruses in temperate North America. Similar problems exist in other areas. A notable example is the interrelationships among sub- terranean clover, Aphis craccivora Koch (Fig. 5), annual legumes, and sub- terranean clover stunt and bean yellow mosaic viruses in southeastern
Australia (Grylls 1972). Subterranean clover has been planted on 20-30 million acres with a potential of possibly 100 million acres more (Morely
1961). In Iran, alfalfa is the principal reservoir of pea leafroll virus, the most serious legume virus of that region (Kaiser 1972).
Perennial legumes are a focal point in the ecology of many viruses and their vectors. The use of aphid-resistant perennial legumes would probably be the most effective single measure that could be taken to manage these important plant diseases. 9
Figure 1. Symptoms of the Wisconsin pea stunt virus in the field. The dis- eased plant (left) shows severe stunt, shortened internodes, and severely rosetted apical foliage compared to healthy plant (right). 10
Figure 2. Perfection-type pea in- Figure 3. Pea aphid on alfalfa. fected with pea enation mosaic virus. (Photo by Ken Gray)
Figure 4. Pea aphid on pea. Figure 5. Cowpea aphid, Aphis crac- (Photo by Ken Gray) civora. (Photo from N. E. Grylls) References
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