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Host Plant Resistance and the Spread of Plant Viruses1 GEORGE Department of Entomology, G. KENNEDY" North Carolina State University, Raleigh 27607 ABSTRACT Crop cuitivars resistant to insect vectors of plant viruses are likely to alter the population size, activity, and probing and feeding behavior of the vector, thereby influencing the pattern of virus spread. The effect of a vector resistant cuitivar on virus spread will depend upon the type of resistance (nonpreference, antibiosis, or tolerance), the level of resistance, the relative importance of primary and secondary virus spread, the length of the acquisition, inoculation, retention, and latent periods of the virus, and the efrect of virus infection on vector resistance in the plant. Each combination of these factors may result in a different effect on virus spread; the possibilities are discussed. Because of the complexities involved, a thorough understanding of the ecology of virus spread, the biology of vector resistance, and the ecology of the vector arc essential to predict the effect of vector resistance on virus spread. virus spread by Aphis craccivora Koch (Evans ]954). Although no more resistant to rosette virus than other cultivars, Mwitunde often escapes infection in the field at least in part because A. craccivora breeds more slowly on it than on other cultivars and is eliminated more rapidly by natural enemies. Other factors may also be involved since aphids reared on Mwitunde have a reduced ability to transmit the virus. Resistance in red clover to A cyrthosiphon pisli/ll (Harr.) has been associated with reduced infection by the clover virus complex present in Minnesota (Wilcoxon and Peterson 1960). ]n the field, the aphid resistant cultivar had less than 10% virus infection, while adjacent plots of a susceptible cultivar had greater than 90%. Both cultivars were equally susceptible to mechanical inoculation of the viruses. The authors concluded that breeding red clover for resistance to aphids may be a more successful approach than trying to breed for resistance to virus diseases. Thomas and Martin (] 97]) found that non preference by the beet leafhopper, Circuli/er f(!llellu'\" (Baker) was responsible for a portion of the resistance in certain tomato cultivars to infection by curly top virus. Vector non preference accounted for 2123 % of the resistance of certain tomato cultivars to infection. The major portion of resistance to curly top, however, could not be attributed to vector preference. A somewhat similar situation was observed by Linn (1940) who concluded that variation in the incidence of aster yellows in commercia] plantings of lettuce cultivars was probably due to differential feeding preferences of the leafhopper vector. Insect resistance in rice has been related to reduced spread of several virus diseases (Pathak 1970). For example, the rice cultivar IR-8 is susceptible to Tungro virus but highly resistant to its vector, the leafhopper Nepl10tettix impicficeps Ishihara. In the field, cultivars susceptible to the vector develop about 4 times as much Tungro virus infection as IR-8. Simi]arly, resistance in IR-8 to the delphacid, Sogatodes orizico/a (Muir) results in a reduction in the incidence of hoja blanca disease. Finally, 'Mudgo' rice is highly resistant to the plant hopper vector of Research on host plant resistance to insects has expanded tremendously in the last decade and numerous recent comprehensive reviews on resistance and its role in pest management arc available (e.g., Maxwell et al. ] 972, Pathak 1970, Stoner 1970, Luginbill 1969, Gallun et al. 1975, Kogan 1975). Very limited consideration has been given to the potential value to plant disease control of resistance to an insect vector of a plant pathogen. Painter (] 951 ) recognized the potential value of such resistance in disease control as did Holmes (1954), Swenson (1968), Pathak (1970), Roane (1973), and Adams ( 1975). There are, however, relatively few documented instances in which resistance to an insect vector has contributed to disease control. Resistance in red raspberry to the aphid AmphoropllOra agathonica Hottes approaches complete immunity (Daubeny ] 966, Kennedy et al. ] 973) and has been considered responsible for the field resistance of certain cuitivars to the common raspberry mosaic virus (RMV) complex. The cultivar 'Lloyd George' is immune to A. agatllonica and only rarely shows symptoms of RMV in the field (Harris ]935). When artificially infected with RMV by grafting, the leaves show symptoms (Schwartze and Huber 1937). In Europe, Lloyd George is an excellent host for the RMV vector, A. rubi (Kltb.), and RMV symptoms arc commonly observed in the field (Harris 1935). Wilcox and Beckwith (1933) observed a negative correlation between the spread of false-blossom virus and the relative suitability of cranberry cultivars as hosts for the leafhopper vector, Scleroracus vaccinii (Van. D.). They suggested that field resistance to false-blossom virus actually consisted of resistance to the vector. This was further supported, although not proven, by the agreement between laboratory host preference tests with S. vaccinii and field resistance to false-blossom (Wilcox] 95] ). A somewhat more complex relationship exists in the field resistance of 'Mwitunde' peanut to rosette 1 Paper no. 4962 of the Journal Series of the North Carolina State Vniv. Agric. Exp. Stn., Raleigh, NC. Received for publication April 2, 1976. o Asst. Prof. of Entomology. 827 828 Vol. 5, no. 5 ENVIRON M ENTAL ENTOMOLOGY grassy stunt virus, Nilaparvata lungens (Stat). Mudgo is susceptible to grassy stunt, but generally escapes infection in the field because of its resistance to the vector. Resistance to an insect vector need not result in a reduction of disease spread. During a year of high aphid infestation, Russell (1965) observed no difference between virus incidence in inbred sugar beet lines resistant and susceptible to the aphid vector. Baerecke (1958) found spread of leaf roll virus was greater in aphid resistant potato cultivars than in susceptible cultivars. This was attributed to the greater activity of aphids between plants of less than optimum host status. Kennedy (1950) recognized this possibility when he emphasized that both abundance and activity of winged aphids as well as their ability to transmit the virus are more important influences on virus spread than their ability to thrive on the crop. This is apparent from the fact that aphids will spread some viruses to plants they do not colonize. For example, the most important vector of watermelon mosaic virus (= cantaloupe mosaic) in cantaloupe in the southwestern U.S., Myzus persicae (Sulz.), does not colonize cantaloupe (Dickson 1949, Dickson et a!. 1949), and cucumber mosaic virus spread in gladiolus is the result of transient rather than colonizing aphids (Swenson and Nelson 1959). Kennedy et at. (1959) discussed the general relationship between host plant suitability and spread of a nonpersistent virus by an aphid vector; they concluded that the behavior of winged aphids will favor the spread of nonpersistent viruses among moderate or borderline hosts more than among better hosts. This conclusion, however, does not necessarily apply to persistent (cf. Orlob 1961) or semipersistent viruses which differ from nonpersistent viruses in their transmission characteristics (d. Sylvester 1969). Thus, while the possibility of a vector resistant cultivar increasing the severity of a disease problem is serious and must be recognized, there are a sufficient number of examples in which vector resistance has reduced virus spread to indicate its potential value. An understanding of the ways in which vector resistance can impact upon disease spread may help to minimize the use of vector resistance in those instances where it will increase disease spread. This paper represents an attempt to analyze the relationship between vector resistance and disease spread. The complexities of this relationship have made desirable the abundant use of references and illustrative examples; however, no attempt is made to provide a comprehensive review of the available literature on virus spread. General Considerations Some aspects of the biology and ecology of the most important insect vectors of plant pathogens, aphids and leafhoppers, have been reviewed elsewhere (van Emden et a!. 1969, Swenson 1968, Kring 1972, Kennedy and Fosbrooke 1973, DeLong 1971) as has the general subject of insect transmission of plant pathogens (Carter 1973, Maramorosch 1969). The present discussion will be restricted to the spread of plant viruses, although the interactions discussed may apply to other pathogens as well. The effect of a vector resistant cultivar on the spread of a plant virus will depend upon the type of resistance (nonpreference, antibiosis or tolerance) (d. Painter 1951), the level of resistance, the relative importance of primary and secondary virus spread, the precise virus-vector relationship (i.e., length of acquisition, inoculation, retention and latent periods), and the effect of virus infection on vector resistance in the plant. Each combination of these factors may result in a different effect on virus spread. Present discussions concentrate on the potential responses of individual insects to resistant plants and their effects on virus sprcad. It is, however, recognized that virus spread in the field results from activity of a large number of individuals, and that all individuals need not respond in the manner specifically described below for the net effect of the resistance on virus spread to approach that described. Throughout this discussion, it is assumed that vector resistant and susceptible plants are equally susceptible to the virus. In actuality, this need not be true and differential virus susceptibility may profoundly influence patterns of virus spread in vector resistant and susceptible plants. Nevertheless, the general virus-vector-plant interactions outlined below will remain influential in determining the ultimate degree of virus spread. NOllpreference Resistance The effect of a feeding non preference on primary virus spread (i.e., introduction of a virus into a field from a source outside the field) will depend upon the rapidity with which the vector recognizes the resistant plant as a nonhost relative in the inoculation and retention times of the virus. Several possibilities exist. If the nonpreference is extreme and the vector does not probe the plant for the inoculation threshold period, then the virus will not be transmitted; primary virus spread will be eliminated. This is most likely to occur with persistent viruses for which there is typically a positive correlation between the inoculation access period and the probability of transmission (Sylvester 1969) and which usually are not transmitted during brief probes. Most persistent viruses must be inoculated into the phloem and typically require probes of 15 min or longer for inoculation (Watson and Plumb 1972). In addition, this may occur with some of the semipersistent viruses for which there is also a positive correlation between the duration of the inoculation feeding period and the probability of transmission (Sylvester 1969). It is unlikely in the case of nonpersistent viruses which can be transmitted by probes of only a few seconds duration, unless the resistant plant is recognized as unsuitable before the vector probes the plant. This can occur; Mueller (1956 cited by Broadbent 1964) reported that brown lettuce varieties had only % as many aphids alight on them and were less frequently infected with lettuce mosaic virus than green varieties. With a more moderate non preference in which the October 1976 KENNEDY: RESISTANCE AND VIRUS SPREAD vector must probe the plant for a considerable period before recognizing it as unsuitable (e.g., Pathak 1971, Kennedy and Schaefers 1974, 1975), primary spread wilIlikely not be eliminated. Should tlie duration of the vector's test probe exceed both the inoculation and retention times of the virus, the plant wilI become infected with the virus, but the vector will lose its infectivity. The resulting pattern of primary spread would be the same as observed in a planting of a susceptible cultivar. This is most likely to prevail among the nonpersistent viruses which have brief retention times (Sylvester 1969) and is less likely with semipersistent viruses which are retained for varying periods ranging from hours to days (Sylvester 1969, Swenson 1968). This situation typicalIy wilI not prevail for persistent viruses which are retained by the vector for many days (Sylvester 1969). Alternatively, the level of nonpreference may be such that the vector probes sufficiently long to inoculate the plant with the virus, but recognizes the plant as an unsuitable host before it has lost its infectivity. If the vector then moved to another nearby plant in search of a suitable host and repeated the procedure one or more times, the resulting primary spread could exceed that typically observed in susceptible cultivars. Those persistent and semipersistent viruses having relatively short inoculation periods, are most likely to fall in this category. Despite their very brief retention times, nonpersistent viruses may also faIl into this category if the vector probes the plant only briefly before recognizing it as a nonhost (d. Kennedy et al. 1959). The overall magnitude of the resistance operating as a nonpreference will influence the degree of primary spread. If the resistance borders on total immunity as in the case of resistance in red raspberry to the aphid vector of raspberry mosaic (Kennedy and Schaefers 1974), then all of the above situations are possible. The one that prevails will depend on the probing behavior of the aphid on the immune plant and the inoculation and retention times of the viruses involved. If the resistance is less than total immunity then primary spread wiII probably not be eliminated, although it may be increased, decreased or unaffected. The effect of a nonpreference on secondary virus spread will be influenced by many factors including the magnitude of the resistance, the relative importance of transient and resident vector populations in secondary spread, the acquisition, inoculation and retention times of the virus and the effect of the virus on the resistance. In the case of aphids, the relative roles of alatae and apterae in secondary virus spread have not been completely resolved (d. Swenson 1968). Most evidence suggests that alate aphids occupy a significant role in the secondary spread of both nonpersistent and persistent viruses (Broadbent and Martini 1959). The simplest situation involves a nonpreference type of immunity in which no vector population develops on the plants and alI secondary spread attributable to the resident vector population is eliminated. 829 Immunity in 'Canby' red raspberry to A. agathonica, the vector of raspberry mosaic, represents this situation (Kennedy and Schaefers 1974). Secondary spread by a transient vector population will be related to the vector's probing behavior relative to the acquisition, inoculation and retention times of the virus. It will also be influenced by the occurrence and duration of a latent period for the virus in the vector. If the transient vector recognizes the virus infected plant as a nonhost and departs before it has probed or fed for the acquisition period of the virus, than secondary spread will not occur. Alternatively, if the vector probes sufficiently long to acquire the virus before it recognizes the plant as an unsuitable host then secondary spread may occur. For nonpersistent and semipersistent viruses which have no latent period in the vector, the amount of secondary spread will depend upon the proportion of viruliferous vectors moving to other plants in the field as opposed to leaving the field, and the probing behavior of the vector relative to the inoculation and retention times of the virus. The effect of these latter will be the same as described under primary spread. For persistent viruses, the duration of the latent period in the vector relative to the length of time the vector continues to search the field for a suitable host will influence secondary spread. Vectors leaving the field before the latent period has elapsed will not contribute to secondary spread. When, as is usualIy the case, the resistance is less than total immunity a resident vector population will develop and will likely contribute to secondary virus spread. Since the non preference may result in an increase in the amount of interplant movement by members of the resident population, their contribution to secondary spread may be greater than in plantings of a susceptible cultivar (e.g., Baerecke 1958). Secondary spread may be profoundly affected if virus infection results in the loss of resistance to the vector. Numerous instances are known in which virus infected plants are more suitable hosts for the vector than healthy plants (Kennedy 1951). For example, Baker (1960) noted that aphid resistance in inbred sugar beet lines was lost when the plants were infected with yellows virus; 3 aphid species were more fecund and lived longer on virus infected than on healthy leaves. Arenz (cited in Swenson 1968)" found reproduction of M. persicae to be greater on \ leaf roll infected plants of a normally aphid-resistant cultivar than on a healthy susceptible cultivar. This need not occur, however. Lowe and Strong (1963) reported that infection by cucumber mosaic virus reduced the suitability of 3 plant species as hosts for M. persicae. Where virus infection resu']ts in a loss of resistance, the magnitude of that loss and the number of plants involved (i.e., primary infections) will determine the size of the resident vector population which develops and very likely the degree to which it contributes to secondary spread. The importance of transient vectors in secondary spread will be in part determined 830 ENVIRONMENTAL by their ability to acquire the virus from an infected resistant plant. A ntibiosis Resistance An antibiosis type of resistance to a vector will influence virus spread in a manner similar to insecticidal control. The detailed discussions of insecticidal control of plant virus spread by Broadbent (1957, .1969) are highly pertinent. In general, an antibiosis type of immunity, like an effective insecticidal control program, will have little or no effect on primary virus spread, but will eliminate that portion of secondary spread attributable to resident vector populations. Primary spread and secondary spread by transient vectors would be reduced or eliminated only if the antibiosis were so effective that it killed the vector or otherwise prevented it from probing for the requisite virus inoculation and/or acquisition period. The presence of a dense pubescence of glandular hairs such as that found in some species of Solanum (e.g., Gentile and Stoner 1968) might entrap the vector before it could inoculate the plant with the virus. In most cases, it is unlikely that the vector will be killed quickly enough to prevent primary spread. Secondary spread by transient vectors would be prevented if they were killed or incapacitated before they had the opportunity to acquire the virus, move to another plant, and infect it with the virus. The probability of this occurring might be greatest for persistent viruses which have a latent period. An antibiosis might influence virus spread in other ways as well. Where resistance results in an alteration of the vectors normal feeding site, the probability of virus transmission could be altered. This is most likely for persistent viruses which typically are acquired and inoculated when the vector feeds in the phloem (Watson and Plumb 1972). McMurtry and Stanford (1960) and later Nielson and Don (1974) demonstrated that resistance in alfalfa to Therioaphis maculata (Buckton) interferes with that aphid's ability to locate the phloem. What effect, if any, this has on virus transmission is not known. With sugar beets, the results of Hills et a1. (1969) suggested that Ivarietal resistance to the semipersistent beet yellows virus was due to resistance to virus transmission by M. persicae rather than resistance to virus infection per se. Haniotakis and Lange (1974) confirmed this and demonstrated the resistance to transmission was associated with differences in the aphids probing behavior on resistant plants. If resistance alters the pattern of alate production in an aphid population, the degree of virus spread might be similarly altered as indicated by the corrclation between the abundance of alate aphids and virus spread (cf. Swenson 1968). Alate production in aphids is often closely related to the condition of the host plant (cf. Schaefers 1972); thus it follows that aphid resistance might alter the normal pattern of alate production. This occurs on cantaloupe lines resistant to A phis gossypii Glover (Kennedy and Kishaba 1976). A, gossypii populations on resistant plants are not only smaller, but produce a signifi- Vol. 5, no. 5 ENTOMOLOGY cantly smaller percentage of alate progeny than populations on susceptible plants. In those cases where virus infection does not alter this effect of resistance, virus infected resistant plants are likely to assume a reduced importance as sources for virus spread. The effect of reduced alate production on virus spread would be greatest when most of the crop acreage consisted of resistant cultivars and the vector had few important alternate hosts. As with insecticides, an antibiosis type of immunity can be expected to provide little reduction in the spread of nonpersistent viruses (ct. Broadbent 1957). Greatest reductions can be expected for persistent viruses. In the more common situation involving a moderate level of vector resistance, the reduction in virus spread may be negligible, especially in individual fields. Virus spread will be reduced to the extent that it is positively correlated with vector abundance. Widespread cultivation of a moderately resistant cultivar in a crop that is the principal host of a virus vector, could significantly reduce the vector population over a large area. Any factor consistently reducing a vector population may be expected to have a similar or greater impact on virus spread (Swenso.n 1968) . Tolerance Tolerance to feeding injury by an inscct pest is a valuable character (Painter 1951), but if that pest is also the vector of a plant virus, the use of a tolerant cultivar could prove disastrous. If larger vector populations are allowed to develop on tolerant than on susceptible cultivars, there might be a corresponding increase in virus spread. This would be especially true if the tolerant cultivar were widely cultivated over large areas. The danger of increased virus spread might extend to other crops susceptible to the same viruses or affected by viruses transmitted by the vector. The potential problem is illustrated by the important role of sugar beets in the spread of watermelon mosaic virus (= cantaloupe mosaic) in cantaloupe in the Imperial Valley of California (Dickson 1949, Dickson et al. 1949). There, large M. persicae populations leaving sugar beet acquire the virus from various cucurbits and transmit it to cantaloupe, which the aphid does not colonize. Concluding Remarks Resistance to a virus vector is likely to exert a complex influence on virus spread. Since nonpreference, antibiosis, and tolerance are often combined into a single resistant cultivar, their relative contribution to the resistance as well as the overall magnitude of the resistance will influence the effect of resistance on virus spread. In addition, since observed virus spread is the result of both primary and secondary spread, the relative importance of these and the effect of the resistance on them is important. The complexities involved are such that without a thorough understanding of the ecology of both the virus and vector and the biology of vector resistance it would be impossible to predict, a priori, the effect of vector October 1976 KENNEDY: RESISTANCE resistance on virus spread. Each combination of virus, vector, and resistance must be considered separately. Because resistance to a vector may result in an increased level of virus spread, it is incumbent upon those breeding for resistance to consider the probable effects of vector-resistance on virus spread. In addition, since resistance to one arthropod species may be associated with altered levels of susceptibility to other species, the potential impact on virus spread of cross resistance to a vector species should not be ignored. Despite these dangers, the potential for controlling certain types of virus diseases through vector resistance is considerable. There exist a sufficient number of examples wherein vector resistance has contributed to disease reduction to justify continued efforts in this area. REFERENCES CITED • Adams, J. B. 1975. Comments on aphid resistance in potatoes. Am. Pot. J. 52: 313-5. Baerecke, M. L. 1958. Bllatrollresistenzzuchtung. Pages 97-106 ill H. Kappert and W. Rudorf (eds.). Handbuch der Planzenzuchtung. 3: 97-106. Paul Parey. Berlin. Baker, P. F. 1960. Aphid behavior on healthy and on yellows-virus infected sugar beet. Ann. Appl. BioI. 48: 384-91. Broadbent, L. 1957. Insecticidal control of the spread of plant viruses. Ann. Rev. Entomol. 2: 339-54. 1964. Control of plant viruses. Pages 330-64 ill M. K. Corbett and H. D. Sisler (eds.). Plant virology. Univ. Florida Press. Gainesville, 527 p. 1969. Disease control through vector control. Pages 593-630 ill K. Maramorosch. (ed.). Viruses, vectors, and vegetation. Interscience. New York. Broadbent, L., and C. Martini. 1959. The spread of plant viruses. Adv. Virus Res. 6: 94-130. Carter, W. 1973. Insects in relation to plant disease. 2nd Edition Wiley-Tnterscience. New York. Daubeny, H. A. 1966. Inheritance of immunity in the red raspberry to the North American strain of the aphid Amp/wrap/lOra rubi (Kalt.). Proc. Amer. Soc. Hort. Sci. 88: 346-51. DeLong, D. M. 1971. The bionomics of leafhoppers. Ann. Rev. Entomol. 16: 179-210. Dickson, R. C. 1949. Aphid flights in relation to cantaloupe mosaic. Plant Dis. Rept. Suppl. 180: 7-8. Dickson, R. C., J. F. Swift, L. D. Anderson, and J. T. Middleton. 1949. Insect vectors of cantaloupe mosaic in California's desert valleys. 1. Econ. Entomol. 42: 770-4. Evans, A. C. 1954. Rosette disease of ground nuts. Nature (London) 173: 1242. Gallun, R. L., K. J. Starks, and W. D. Guthrie. 1975. Plant resistance to insects attacking cerals. Ann. Rev. Entomol. 20: 337-57. Gentile, A. G., and A. K. Stoner. 1968. Resistance in Lycnpersicoll and Solanum species to the potato aphid. J. Econ. Entomol. 61: 1152-4. Haniotakis, G. E., and W. H. Lange. 1974. Beet yellows virus resistance in sugar beets: mechanism of resistance. Ibid. 67: 25-8. Harris, R. V. 1935. Some observations on the raspberry disease situation in North America. East Mailing Res. Sta. Rept. for 1934. Pages 156-64. AND VIRUS SPREAD 831 Hills, F. J., W. H. Lange, and J. Kishiyama. 1969. Varietal resistance to yellows, vector control, and planting date as factors in the suppression yellows and mosaic of sugar beet. Phytopathology 59: 1728-31. Holmes, F. O. 1954. Inheritance of resistance to viral diseases in plants. Adv. Vir. Res. 2: 1-30. Kennedy, G. G., and G. A. Schaefers. 1974. Evidence for nonpreference and antibiosis in aphid-resistant red raspberry cultivars. Environ. Entomol. 3: 7737. 1975. Role of nutrition in the immunity of red raspberry to A mpllOrop/lOra agathollica Hottes. Environ. Entomol.4: 115-9. Kennedy, G. G., and A. N. Kishaba. 1976. Bionomics of Aphis gossypii on resistant and susceptible cantaloupe. Environ. Entomol. 5: 357-61. Kennedy, G. G., G. A. Schaefers, and D. K. Ourecky. 1973. Resistance in red raspberry to A mphorapllOra agatllOllica Hottes and A phis rubico/a Oestlund. HortScience 8: 311-3. Kennedy, J. S. 1950. Aphid migration and the spread of plant viruses. Nature (London). 165: 1024-5. 1951. A biological approach to plant viruses. Nature (London). 168: 890-4. Kennedy, J. S., and I. H. M. Fosbrooke. 1973. The plant in the life of an aphid. Pages 129-40 in H. F. Van Emden. Insect/Plant Relationships. Symposia of Royal Entomol. Soc. London: No.6. Blackwell Scientific Publ. Oxford. Kennedy, J. S., C. O. Booth, and W. J. S. Kershaw. 1959. Host finding by aphids in the field. II. Aphis fabae (gynoparae) and Bre\'icorYlle brassicae L. with a reappraisal of the role of host finding behavior in virus spread. Ann. Appl. BioI. 47: 424-44. Kogan, M. 1975. Plant resistancc in pest management. Pages 103-46 ill R. L. Metcalf and W. H. Luckman (ed.) Introduction to insect pest management. John Wiley & Sons. New York. Kring, J. B. 1972. Flight behavior of aphids. Ann. Rev. Entomol. 17: 461-92. Linn, M. B. 1940. The yellows disease of lettuce and endive. N. Y. S. Agric. Exp. Stn., Ithaca. Bull. 742. Lowe, S., and F. E. Strong. 1963. The unsuitability of some viruliferous plants as hosts for the green peach aphid, Myzus persicae. J. Econ. Entomol. 56: 307-9. Luginbill, P., Jr. 1969. Developing resistant plantsthe ideal method of controlling insects. USDAProd. Res. Rept. No. III. Maramorosch, K. (ed.). 1969. Viruses, vectors. and vegetation. Interscience. New York. Maxwell, F. G., J. N. Jenkins, and W. L. Parrott. 1972. Resistance of plants to insects. Adv. Agron. 24: 187-265. McMurtry, J. A., and E. H. Stanford. 1960. Observations on feeding habits of the spotted alfalfa aphid on resistant and susceptible alfalfa plants. J. Econ. Entomol. 53: 714-7. Nielson, M. W., and H. Don. 1974. Probing behavior of biotypes of the spotted alfalafa aphid on resistant and susceptible alfalfa clones. Entomo\. Exp. & App\. 17: 477-86. Orlob, G. B. 1961. Host plant preference of cereal aphids in the field in relation to the ecology of barley yellow dwarf virus. Ibid. 4: 62-72. Painter, R. H. 1951. Insect resistance in crop plants. Macmillian Co. New York. 832 ENVIRONMENTAL ENTOMOLOGY Pathak, M. D. 1970. Genetics of plants in pest management. Pages 138-57 in R. L. Rabb and F. E. Guthrie (eds.). 1970. Concepts of Pest Management, North Carolina State University. Raleigh. Pathak, M. D. 1971. Resistance to leafhoppers and planthoppe'rs in rice varieties. Pages 179-93 in Symposium on rice insects. Proc. of a Symposium on Tropical Agr. Res. 19-24 July, 1971. Trop. Agr. Res. Ser. No.5. Roane, C. W. 1973. Trends in breeding for disease resistance in crops. Ann. Rev. Phytopath. II: 46386. Russell, G. E. 1965. Preliminary studies in breeding for aphid resistance in beet. J. Inst. Intern. Rech. Better. I: 117-25. Schaefers, G. A. 1972. The role of nutrition in alary polymorphism among the Aphididae-an overview, Search, Agriculture 2 (4). Schwartze, C. D., and G. A. Huber. 1937. Aphis resistance in breeding mosaic escaping red raspberries. Science (Wash., DC) 86: 158-9. Stoner, A. K. 1970. Breeding for insect resistance in vegetables. HortScience. 5: 76-9. Swenson, K. G. 1968. Role of aphids in the ecology of plant viruses. Ann. Rev. Phytopath. 6: 351-74. Vol. 5, no. 5 Swenson, K. G., and R. L. Nelson. 1959. Relation of aphids to the spread of cucumber mosaic virus in gladiolus. J. Econ. Entomol. 52: 421-5. Sylvester, E. S. 1969. Virus transmission by aphidsa viewpoint. Pages 159-73 in K. Maramorosch (ed.) Viruses, vectors and vegetation. Interscience. New York. Thomas, P. E., and M. W. Martin. 1971. Vector Preference, a factor of resistance to curly top virus in certain tomato cultivars. Phytopathology 61: 1257-60. Van Emden, H. F., V. F. Eastop, R. D. Hughes, and M. J. Way. 1969. The ecology of Myzus persicae. Ann. Rev. Entomol. 14: 197-270. Watson, M. A., and R. T. Plumb. 1972. Transmission of plant-pathogenic viruses by aphids. Ibid. 17: 425-44. Wilcox, R. B. 1951. Tests of cranberry varieties and seedlings for resistance to the leafhopper vector of false-blossom disease. Phytopathology 41: 722. Wilcox, R. B., and C. S. Beckwith. 1933. A factor in the varietal resistance of cranberries to the falseblossom disease. J. Agric. Res. 47: 583-90. Wilcoxon, R. D., and A. G. Peterson. 1960. Resistance in Dollard red clover to the pea aphid Macrosiphurn pisi. J. Econ. Entomol. 53: 863-5.