Insect-Pest Management and Control (1969)

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CHAPTER 6 Plant and Animal Resistance to Insects The principle of host resistance in control and management programs in- volving pests of plants or animals should be given consideration. It should be taken into account in breeding programs aimed at improving the quality or yield of agricultural crops or livestock and in introducing known crop varie- ties or animal breeds into new geographic areas. Exploitation of resistance to its full potential involves a broad interdisciplinary approach. With a few con- spicuous exceptions, consideration has not been given to host resistance in past entomological research. In recent years there has been some increase in studies of insect resistance in plants, both in respect to the number of plants and insects investigated and to the depth of the studies. There have also been improvements in knowledge of insect physiology and behavior, together with means of studying the mi- nute quantities of various substances that are probably the basis of resistance. For these reasons, some of today's concepts about resistance may soon re- quire modification or replacement. Breeds or lines of cattle, sheep, hogs, and horses possess different degrees of resistance to arthropod attack. This dif- ference in resistance among animals is present from birth to old age and does not depend on previous exposure to the pests. HISTORY AND EXAMPLES The ease of insect-pest control by the use of insecticides, at least since 1940, has often resulted in the neglect of a study of host resistance to the pests. This was true even before the widespread use of DDT and other organic in- 64

PLANT AND ANIMAL RESISTANCE TO INSECTS 65 secticides. For example, the satisfactory control of the Colorado potato beetle, Leptinotarsa decemlineata (Say), obtained with the early arsenicals, apparently made any real, detailed study of the biology of this insect in the United States less necessary, particularly the relation of the insect to its hosts. In no respect has the study or use of resistance to arthropod pests in do- mestic animals advanced as far as with domesticated plants. This is partly be- cause of the negligible cost of plants compared with animals, the far shorter time usually required for a generation in plants, and because of greater oppo- sition to hybridization between animal breeds compared with the crossing of plant varieties. In many instances, the findings in studies of resistance to in- sects, mites, and ticks in animals are similar to principles developed in studies of insect resistance in plants. Most differences are related to mobility of ani- mals, the presence of a blood system and immune reactions, and complexities introduced by the wider role of hormones in animals. The first instances of the use of plant resistance to insects are as old as the earliest work in applied entomology. The earliest record of a recognizable insect-resistant variety is the Winter Majetin variety of the apple, Malus pumila Miller, which was reported resistant to the woolly apple aphid, Eriosonw lanig- erum (Hausmann), in 1831 and is still resistant at the latest report. Within a few years after the introduction of the Hessian fly,Mayetio!a destructor (Say), into the United States, an unnamed resistant variety of wheat, Triticum aesti- vum Linnaeus, was mentioned in 1785 by an unknown writer in a farm paper. All trace of some of the first varieties reported as resistant to the Hessian fly has apparently been lost, but, in a few cases, selections of wheat bearing the same names were later found to be resistant. In 1878 it was reported that there was a great difference in susceptibility to grasshoppers, Melanoplus spp., in corn, Zea mays Linnaeus (Figure 2), as compared with that in sorghums, Sorghum vulgare (Persoon). The corn was much more susceptible than the sorghums. Since then, this difference has been seen repeatedly during each grasshopper outbreak in areas in North America where these crops are grown. This is true for all species of grasshoppers that have been observed in outbreak numbers in the area, despite the fact that, during the intervening years to the present, the resistant sorghums have increased from a few thou- sand acres to many millions, and grasshoppers have not yet "learned" to eat the sorghums. About the middle of the nineteenth century, it was found that some of the American species of grapes, Vitis spp., were highly resistant to the grape phylloxera, Phylloxera vitifoliae (Fitch), and the European species, Vitis vinifera Linnaeus, was very susceptible. This knowledge made possible the grafting of European grapevines onto phylloxera-resistant rootstocks from the United States and formed the basis for a method of control that is still most important. These examples, which are about a century old, and as old as or older than any other insect-control method, emphasize the relative permanence of resistance.

66 INSECT-PEST MANAGEMENT AND CONTROL r - •• i .m FIGURE 2 Differences in damage to adjacent corn hybrids by grasshoppers, Melanoplus spp. Left: Kansas hybrid 2234. Right: U.S. hybrid 35. Resistance to grass- hoppers occurs more commonly in corn inbreds derived from varieties formerly grown in the western United States, where grasshoppers have long been a feature of the en- vironment, than from those in more eastern parts of the country. (Courtesy of Kansas Agricultural Experiment Station) The first extensive search for sources of plant resistance to insects was made in California over a period of 10 years, beginning in 1881. Seeds of over a hundred varieties of small grains, especially wheat, were obtained, and plants grown from these seeds were exposed to infestation by the Hessian fly. The results were recorded, but nothing further was done for several decades, when

PLANT AND ANIMAL RESISTANCE TO INSECTS 67 development of knowledge of plant-breeding made possible the practical use of the information in incorporating genetic factors for resistance into a satis- factory wheat variety. Possibly the earliest studies of the inheritance of pest resistance were in 1916 and 1917 and involved the resistance of cotton, Gos- sypium spp., to the leaf blister mite,Eriophyesgossypii (Banks), and the black scale, Saissetia oleae (Bernard). Field and, later, greenhouse studies of Hessian fly resistance in wheat were begun by the Kansas Agricultural Experiment Sta- tion in 1914, and have since continued without interruption. These studies led to the distribution in Kansas of the Hessian fly-resistant wheat selection Kawvale in 1931 and in following years to the distribution of nine wheat varieties de- rived from hybrids and resistant to the insect. There are excellent examples of the successful use of resistant crop varieties for control of infestation and damage caused by various insects. Six varieties of wheat, resistant to the wheat stem sawfly, Cephus cinctus Norton, are being grown on several million acres in Canada and in Montana, North Dakota, and neighboring states, where wheat sometimes could not previously be produced because of this insect, for which no other economic control measure is avail- able. The availability of cotton varieties resistant to the leafhopper Empoasca fascialis (Jack) in South Africa has made the growing of cotton possible where it could not be grown economically before the advent of DDT, and without resistant varieties. Hessian fly-resistant varieties of winter wheat, satisfactory in milling and baking qualities, with high yield, and disease-resistant are avail- able in all the major wheat-growing areas of the United States. More than 20 such fly-resistant wheat varieties are presently recommended by the agricul- tural experiment stations of the states involved. For the first time a high level of Hessian fly control is available to all wheat-growing farmers at no cost except, perhaps, a small amount for superior seed (Figure 3). Breeds of animals with demonstrated resistance to arthropod attack have been recognized in recent times only, but reported differences date back much further. An Arabic report of the Crusades indicates that Arabian horses were less bothered by Hippobosca ssp. than were European horses. Native tribes of West Africa claim that West African small-humped cattle are more resistant to the attacks of tsetse flies (Glossina spp.) and the trypanosomes they transmit than the more recently introduced breeds. Definite attempts to develop arthropod resistance in domestic animals are difficult to trace. Early in the twentieth century, efforts were made in South Africa to combine the freedom from insects and ticks shown by the Afrikander cattle with the more desirable qualities of European breeds. Results were not gratifying.•Somewhat later, European and Asian cattle were crossed to com- bine the greater resistance to flies and ticks of the Asian cattle with the more desirable conformation of European breeds. These efforts led to the establish- ment of several breeds that are less adversely affected by biting flies than the

68 INSECT-PEST MANAGEMENT AND CONTROL FIGURE 3 Differential fall injury by Hessian fly, Mayetiola destructor (Say), to plants of wheat varieties at Hays Branch Kansas Agricultural Experiment Station, October 29,1962. (Wheat planted September 6, 1962). Left to right: Kaw, tolerant; Bison, susceptible; Ottawa, resistant (with stake); Tenmarq, susceptible (with stake); Ponca, resistant; Pawnee, resistant. Tolerant wheats have nearly as many insects at the base as susceptible ones but are less injured. On resistant wheat varieties, few or no flies develop, even though the plants receive just as many eggs as the susceptible or tolerant varieties. (Courtesy of Kansas Agricultural Experiment Station) common European breeds. Some of the best known lines of purebred Here- fords have been selected on a basis of light-colored hair coat, because these strains are less susceptible to the horn fly, Haematobia irritans (Linnaeus). Australian sheep ranchers have found that English breeds of sheep are far less susceptible to attack by wool maggots (larvae of several Calliphoridae) than are the Spanish-developed Merino breed. Crosses between the breeds show intermediate resistance. COMPONENTS OF RESISTANCE Plants or animals that are inherently less damaged or less infested by a pest than others under comparable environments in the field are called resistant. The term "resistance" is used for beginning studies in the field or in the green- house when one does not know what components are involved. Most such cases of resistance are made up of varying degrees of one or more components: nonpreference and preference, antibiosis, and tolerance. These components appear to be generally comparable in plants and animals. Nonpreference and

PLANT AND ANIMAL RESISTANCE TO INSECTS 69 preference refers to a group of host characters and insect responses that lead away from or to the selection and use of a particular host, variety, or breed for oviposition, for food, for shelter, or for combinations of the three. Anti- biosis refers to the adverse effects on the insect mortality, size, and life history that result from pests feeding on a resistant host. Tolerance refers to a basis of resistance in which the host shows an ability to grow or reproduce or repair injury while supporting a population approximately equal to that damaging a susceptible host. Each of these components is controlled by one or more genetic factors. Therefore, higher or more stable levels of resistance may often be ob- tained by combining components of resistance from several sources or by com- bining genetic factors for each of the three components. Analyses of the com- ponent or components of resistance present are needed early in the research, first as a prelude to a separate study of the basis of resistance of each compo- nent, and, second, before a separate study of the genetics of each component of resistance is initiated. Only one case is known where two components of resistance are governed by a single genetic factor, the H3 gene for Hessian fly resistance in wheat. The chemical resistance factor, 6-methoxybenzoxazolinone (RFA), the genetics of which is unknown, is found in corn leaves of inbreds re- sistant to the European corn borer, Ostrinia nubilalis (Hiibner). It acts as a feeding deterrent as well as a growth inhibitor; hence, it could be classified both as a nonpreference and an antibiotic component. Some research workers on insect resistance would confine the term resis- tance to what is here designated as the component antibiosis. There are at least four reasons for using the term resistance for any combinations of one or more of the components just named. (1) A number of examples of resistance of economic importance include antibiosis as only a minor element, if at all. One example is the resistance to greenbugs, Schizaphis graminum (Rondani), in wheat and barley, Hordewn vulgare Linnaeus (Figure 4). (2) In studies before the components concerned are analyzed there is no general term except resis- tance available. (3) The recognition of the three components of resistance emphasizes the importance of finding and, where necessary and possible, gene- tically combining the components into a single variety to provide the most stable type of resistance. (4) The component of resistance being studied should be defined before studies are attempted on the basis of resistance (Figures 4 and 5). It cannot be emphasized too often that the resistance as first seen in the field generally results from one or more components of resistance, each of which is a complex of interacting factors. NONPREFERENCE AND PREFERENCE The nonpreference and preference component of resistance has been discounted perhaps incorrectly in many studies of insect resistance. Increasingly, research

70 INSECT-PEST MANAGEMENT AND CONTROL FIGURE 4 Differential damage by greenbug, Schizaphis graminum (Rondani), in greenhouse to plants of barley varieties, Dicktoo, resistant (plants healthy), and Reno, susceptible (plants flattened). Reproduction of the aphid is twice as great on the suscep- tible as on the resistant variety, but the resistant variety carries a high level of tolerance. Compare with Figure 5. (Courtesy Kansas Agricultural Experiment Station) has demonstrated that inherent responses of insects to inherited constitutents or characteristics of plants are far more stable than previously supposed. Thus, the value of the nonpreferred characteristics can rarely be estimated on the basis of present information. Insects May Starve Rather Than Feed on Resistant Plants There are at least two types of nonpreference: first, that which is manifest only in the presence of a preferred host; second, one that can be demonstrated as present in the resistant plant even in the absence of the preferred host. In the latter type, the nonpreference may be so strong that the insect would starve to death, even though no untoward results would follow if it fed on the nonpre- ferred plant. This was clearly demonstrated by Waldenbauer's studies of the tobacco hornworm, Manduca sexta (Johannson), where large intact larvae re- fused to feed on nonpreferred plants, but larvae with maxillae removed some- times ate the plants without ill effects. In nature, the original choice or original response to the host after oviposition is made by first-instar larvae or nymphs, which may be more sensitive to the constituents of the host than larger larvae or nymphs. Therefore, it is very difficult to separate extreme nonpreference

PLANT AND ANIMAL RESISTANCE TO INSECTS 71 from antibiosis, or to determine whether the insects starve to death in the presence of adequate food or are poisoned by minute amounts of that food. Studies on feeding pea aphi<ls,Acyrthosiphon pisum (Harris), with a chemi- cally defined diet under various colored lights are examples of extreme non- preference and apparently are not complicated by other possibilities. In this research, the aphids were given a choice of samples of the same chemically defined diet illuminated by different colors. The insects usually picked the food illuminated with yellow or orange light, and they reproduced abundantly. How- ever, when confined with the same food illuminated only with blue light, they did not feed sufficiently to live or reproduce. On food illuminated with red light, they gained very little and reproduction was poor. When similar artificial food was illuminated with green light, survival was about 50 percent, but weight gained by survivors was normal. The females of some insects refuse to oviposit on nonpreferred hosts. Others will oviposit on a nonpreferred host near the preferred one but not on a non- preferred host some distance away. The work on the pink bollworm, Pectino- phora gossypiella (Saunders), of cotton showed wide differences between ovi- FIGURE 5 Differential damage by spotted alfalfa aphid, Therioaphis maculate (Buckton), in greenhouse to alfalfa varieties, Cody, resistant (plants healthy), and Buffalo, susceptible (plants killed). Cody was derived from 22 spotted alfalfa aphid- resistant plants found in Buffalo alfalfa. The resistance of Cody is partially dependent on the tolerance component but is principally due to the fact that the aphid is unable to maintain a population on the variety long enough to kill many plants. Compare with Figure 4. (Courtesy Kansas Agricultural Experiment Station)

72 INSECT-PEST MANAGEMENT AND CONTROL position on two species of Gossypium both when the two plant species were caged together and when they were caged separately. The feeding and oviposition patterns in most insects are a complex series of responses to features of the environment and to characteristics of the host. Presumably, the earliest insects found their hosts through random searching, and some still do. Many insects respond to such features of the environment as gravity, light, light-dark margins, and wind movement of a given level. These responses bring them within a range from which they can respond to a specific attribute of the host. Such responses may then take the form of either kineses or taxes. The former provide response to arrestants, the latter to attractants. At first the taxes appear to come from a stimulus for biting or piercing but, later, from a stimulus to continue feeding. As applied to resistance, nonprefer- ence may take the form of one or more breaks in the chain of responses leading to feeding or oviposition. These breaks are the absence of an arrestant or attrac- tant, the presence of a repellent, or an unfavorable balance between arrestant or attractant or both on the one hand, and a repellent on the other. Most of what is known of the bases of differences in relationships of insects to susceptible and resistant hosts comes from studies of insects on different host species. Less information is available on the bases of interactions between any insect and susceptible or resistant host varieties. Presumably, the same information acquired by the study of differences between host species would apply to differences between resistant and susceptible varieties, but the latter area greatly needs detailed study. The preference phenomena responded to by insects are extensive, including such physical characters as color, plant surface, internal structure of the plant, and reflection of infrared and other rays. It is generally believed that chemical characteristics are the most important. An insect usually responds to only a few chemicals, and with unbelievable sensitivity when it does. For example, the diamondback moth, Plutella maculipennis (Curtis), can taste one 1/1,000 part of the amount of sinigrin that man can taste. A single sensory hair of the black blow fly, Phormia regina (Meigen), when touched by a sucrose concentra- tion of 3 one-millionths of a gram per cc of water will cause the blow fly to respond. There appear to be little data on the long-time persistence of various repellents. Materials extracted from resistant trees or parts of resistant trees have protected susceptible wood from the powder-post termite, Cryptotermes brevis Walker, for periods of 4 to 11 years. The value of preference as a resistance mechanism has been questioned by various workers. In a few cases preference appears to be the only component of resistance. It is characteristic of a number of insects with chewing mouthparts where the first-instar larvae on resistant plants take only small nibbles. This is true of the Colorado potato beetle on wild potato, Solanum demissum Lindley

PLANT AND ANIMAL RESISTANCE TO INSECTS 73 where the feeding of the insect is limited to small nibbles. The repellent ma- terial is apparently demissine, which may also be toxic. Colonies of the insect cannot be maintained on this resistant species. The same small feeding lesions are characteristic of other examples of resistance, including the resistance of some strains of corn to the European corn borer. It is not always clear whether these reduced feedings are the result of extreme nonpreference, or some form of antibiosis, or both. In Some Animals Pest Feeding Is Not Always Related to Skin Thickness The component nonpreference and preference is recognized in several species of domestic animals. Horn flies are normally more prevalent on dark-colored areas of an animal than on lighter areas. Significant differences in the preference for dark over light hair coat by horn flies and stable flies have been demon- strated in Holstein, Ayreshire, and Hereford breeds of cattle when the animals are pastured together. However, if light-colored animals are separated from darker animals, they may have large numbers of flies. Lines of Herefords less attractive to horn flies have been developed, but the ease with which these flies can now be controlled by other means has resulted in less emphasis on selecting for nonpreference by horn flies and more emphasis on conformation and effi- cient food utilization. Skin thickness has long been suggested as a factor in preference or non- preference of stable flies, Stomoxys calcitrans (Linnaeus), and horn flies occur- ring on Holstein, Ayreshire, Jersey, or Guernsey cattle. Significant correlations have been demonstrated with the first three breeds but not with the last. No significant differences in the numbers of house flies, Musca domestica Linnaeus, feeding on animals of different skin thickness were noted except when biting flies were numerous. Then the house flies fed on drops of blood resulting from the feeding punctures of the biting flies, and the numbers of house flies were correlated with the activity of biting flies and hence indirectly with the skin thickness. The site of skin measurement was important, and measurements on the side of the bovine provided the best estimate of fly numbers, followed by the neck and escutcheon. Irritability or nervousness of the host has been suggested as a factor in non- preference of stable flies and horn flies for individuals, and a high degree of cor- relation has been obtained between the number of flies feeding and the tendency of the animal to frighten the flies away. The heritability of this factor is high but of questionable value in a breeding program. Nonpreference in ticks for breeds of cattle has been ascribed to several fac- tors, including shorter or thinner hair coat; thicker skin; wrinkled, loose-fitting skin; and differences in the secretions of the sebaceous glands. Some of the tick

74 INSECT-PEST MANAGEMENT AND CONTROL nonpreference of zebu cattle has been transferred to hybrids with European breeds of cattle. However, the nonpreference of mosquitoes and horse flies for zebu cattle has not been transferred successfully. ANTIBIOSIS Abnormal Effects When Insect Feeds on Resistant Plant The resistance component is called antibiosis when an insect feeds on a resistant plant, and one or more abnormal effects occur: (1) Death of first-instar nymphs or larvae has often resulted, so that the differences between resistant and sus- ceptible plants vary from zero infestation on resistant plants to high infestation on susceptible plants. (2) A lowered reproduction by females reared or feeding on resistant plants is probably the second most common observed effect. (3) Smaller size and lower weight often occur when the effect is not sufficient to result in death of the insect (Figure 6). Sometimes this effect is easily evi- dent; at other times significant differences can only be shown by numbers of measurements. (4) Abnormal length of life frequently occurs either as longer FIGURE 6 Size of 12-day-old larvae of corn earworm, Heliothis zea Boddie, after feeding on corn silks of two different corn hybrids. The larger larva had fed on silk of the cornhybridMp317 x 319; the smaller larva had fed on silk of the hybrid F44 x F6. (USDA photograph)

PLANT AND ANIMAL RESISTANCE TO INSECTS 75 nymphal or larval period, or as shorter adult life compared with insects reared on susceptible hosts. A longer nymphal or larval period exposes the young insect to its enemies for a longer period of time and may lead to fewer genera- tions per year; shorter adult life limits the time available for the female to mate and lay eggs. (5) Smaller food reserves often are accumulated. This affects the ability of the insect to survive if it hibernates and possibly when it aestivates. (6) In a few cases, death has been observed just before the adult stage, thus reducing the population. Hence, death occurs at a time of physiological stress, particularly in an insect with complete metamorphosis. (7) Various behavioral and physiological abnormalities sometimes appear. In the Colorado potato beetle, for example, extra secretions of certain dermal glands, irregular heartbeat, and increased sensitivity to stimulus have been observed. In several insects, regurgitation occurs after feeding on resistant plants. Experimenters have frequently observed a marked general restlessness when either young or adult insects were caged on resistant plants. This often occurs in species where resistance is considered to be antibiotic but may actually be the result of extreme nonpreference. This restlessness has been commonly ob- served with aphids caged on resistant plants and with the Colorado potato beetle on resistant potato plants, and it probably occurs with the Hessian fly on resistant wheat plants. In the last case, first-instar larvae normally settle down behind the leaf sheath just above the node, but on resistant plants dead first- instar larvae or small flaxseed (puparia) may be found higher up between the nodes. Effect of Resistant Plant Variety on Insect Population In areas where resistant varieties of plants predominate, their effect on the population of the insect resisted is specific, persistent, and cumulative. Since the adverse effects reoccur in each insect generation, most of them tend to reduce the population of the affected pest species. The result may be an elimi- nation of the species in areas where the resistant variety is used. Even a differ- ence of 50% between resistant and susceptible varieties, which is cumulative each generation, would be of high value as a control measure. This actually occurred in Kansas, where the Hessian fly was virtually eliminated for 15 years following the extensive planting of the Hessian fly-resistant Pawnee variety of wheat and other resistant wheats. The Pawnee variety normally carries a level of only about 50% of the infestation compared with susceptible varieties and never occupied 100% of the acreage in any county (Figure 7). The original distribution of Pawnee occurred at the time of high fly population and during favorable weather conditions. Despite this favorable situation, the reduction of fly population occurred. In California the distribution of Hessian fly-resistant Poso 42 and Big Club 43 released in 1942 and 1944, respectively, was followed

76 INSECT-PEST MANAGEMENT AND CONTROL 70 % RESISTANT VARIETIES 60 S0 20 HESSIAN FLY INFESTATI0N N0 PUPAE PER I00 STEMS. __.»-- I949 50 5I 52 53 54 55 56 57 58 59 60 6I 62 63 64 65 FIGURE 7 Relationship of average percentage of Hessian fly, Mayetiola destructor (Say), resistant wheat varieties planted in counties of the eastern half of north central Kansas to Hessian fly infestation, 1949-1965. When the acreage of resistant wheat de- creased in 1960, the Hessian fly infestation increased. by a practical disappearance of the insect from the infested area, and this scarcity persisted from 1942 to near the present time. The range of differences found in examples of plant resistance believed to be the result of antibiosis is illustrated in Table 1, showing a range from the high-level resistance to the corn leaf aphid and the pea aphid to the 50% or less resistance to the greenbug. The antibiotic resistance shown for the greenbug is accompanied by a considerable level of tolerance and is of high economic value. Possible Physiological and Biochemical Bases of Antibiosis in Plants There has been no evidence of a general or single explanation of antibiosis any more than for all three components of resistance as a group (Figures 4 and 5). A first possible basis of antibiosis is the presence of a toxin in the resistant plant. The term as used here covers a number of possible physiological reac- tions, which certainly need to be analyzed further as information accumulates. Entomologists and often other people are generally conversant with the fact that insecticides such as nicotine, pyre thrum, and rotenone may be secured from plants. Lists are available of several hundred species of plants containing biochemicals capable of killing insects. Furthermore, varietal differences influ- ence the insecticidal properties of the three insecticides mentioned above. A

PLANT AND ANIMAL RESISTANCE TO INSECTS 77 lethal factor has been reported in silks of corn resistant to larvae of the corn earworm, Heliothis zea (Boddie). This has been questioned, but difference in opinion may be related to the presence of the lethal factor in the silks for only a short period of time. A second possible basis of antibiosis is the presence of a growth or reproduc- tion deterrent or both. For example, gossypol in cotton retards the growth of the bollworm, Heliothis zea (Boddie). Resistance Factor A (RFA), identified as 6-methoxybenzoxazolinone, acts as a growth deterrent of the European corn borer; it is possibly the most important factor in leaf resistance to this insect. Resistance Factor A is confined to certain tissues in certain hybrids and also to definite growth periods in the plant. A third possible basis of antibiosis is the absence of some nutritional mate- rials, such as vitamins, vitaminlike substances, or essential amino acids, in the particular part of the resistant plant eaten by the insect. No evidence for this sort of basis is available except the known sensitivity of insects to deficiency or near-deficiency in some of these substances. In the house fly, for example, absence of certain vitamins in synthetic foods results in death in the first instar, while absence of other vitamins results in death at about the time of pupation. A fourth possible basis of antibiosis is the deficiency in certain nutritional materials, especially animo acids or specific sterols. In pea aphid resistance in peas, Pisum sativum Linnaeus, lower concentrations of amino acids occur in resistant than in susceptible lines. The silks of certain corn lines resistant to the TABLE 1 Range of Differences in Antibiosis Average Progeny per Insect and Crop3 Female Aphid per Day* Corn leaf aphid, Rhopalosiphum maidis (Fitch) Sudan 428-1 (R) 0.09 White Martin sorghum (S) 9.85 Pea aphid, Acyrthosiphon pisum (Harris) Alfalfa plant No. 5 (R) 0.07 Alfalfa plant No. 2 (S) 2.29 Greenbug, Schizaphis graminum (Rondani) Dicktoo winter barley (R) 1.02 Dickinson spring wheat (R) 1.27 Ponca winter wheat (S) 1.46 Kiowa winter wheat (S) 2.13 Reno winter barley (S) 2.46 a(R), resistant; (S) susceptible Results from various sources and generally at most favorable temperature for reproduction of the insect concerned.

78 INSECT-PEST MANAGEMENT AND CONTROL corn earworm also have lower concentrations of amino acids than those of susceptible lines (Figure 6). It has not been shown that this is the principal factor in resistance in either case. Carnitine, lysine, linoleic acid, lecithin, and inositol are other examples of substances reported affecting the biology of particular insects, when deficient in amount. Differences in utilization or digestibility between plant species or even between parts of the same plant are known. A fifth and related basis could be the imbalance in available nutrients, especially the sugar-protein or sugar-fat ratios. The effect on the growth of larvae of the Angoumois grain moth, Sitotroga cerealella (Olivier), resulting from different amylose content of corn grains, may belong in this category, since both high and low amylose-bearing corn lines appear more favorable than certain medium-high lines. Some evidence for bases 3, 4, or 5 comes from studies of food plants of certain grasshoppers, where two plants, which by themselves constitute poor foods, when fed together produce as good growth and survival as a single good food plant. A sixth basis for antibiosis may involve proliferating tissue or increased secre- tions of resistant plants, such as that causing the death of eggs or young larvae of the boll weevil, Anthonomus grandis Boheman, the melon leaf miner, Liriomyza pictella (Thompson), pine resin midges, Retinidiplosis spp., and possibly bark beetles, Dendroctonus spp. Several problems are associated with the location of the basis of antibiosis, possibly the most difficult of which is the necessity that work be done with minute first-instar larvae or nymphs. Because the nutritional needs of different insect instars are often materially different, the results with large larvae cannot be substituted for those obtained with first-instar ones. A second difficulty is that the first instars of many insects begin feeding on specific kinds of plant tissue, often meristematic. Therefore, this particular tissue must be analyzed, because general analysis of the entire plant or a large plant part is of little value. A third difficulty lies in the fact that biochemicals concerned are often present in minute quantities and may occur only at certain times in the growth of the plant, times that coincide with periods of attack by the insect, a relationship that probably has arisen through natural selection. Where a completely artificial food is available for an insect, the study of antibiosis can be advanced by its use. Very few leaf-feeding insects have been reared on a completely refined synthetic food. The addition of yeast, ground leaf tissue, or other substances of unknown composition has usually been neces- sary for natural maturation and reproduction. The addition to a synthetic food of various biochemicals isolated from resistant or susceptible plant tissues may help solve some of the problems associated with the bases of resistance. No general bases of insect resistance have been found, but extensive investigations may show that certain groups of related biochemicals are involved.

PLANT AND ANIMAL RESISTANCE TO INSECTS 79 Physical and Antibiosis Differences in Plants Are Rarely Important Physical and mechanical differences have sometimes been cited as one of the bases of insect resistance in plants. The rice weevil, Sitophilus oryzae (Linnaeus), can certainly be excluded by the long husk carried by some corn ears. Common bread wheats with solid straw are resistant to the wheat stem sawfly, although the way in which the solidness affects the insect is not precisely known. How- ever, the relationship between resistance and solid straw has been useful in breeding for sawfly resistance. Hairy cottons in South Africa have been resistant to some species of Empoasca spp. leafhoppers, but the same hairy varieties have not been resistant under other conditions to other species of Empoasca. A high correlation coefficient alone is not sufficient proof of the basis of resistance, but a visible character segregating in parallel with resistance is of great usefulness to breeders. Very long tight corn husks may reduce suscepti- bility to the corn earworm, but to breed for long husks may also mean to breed for short ears, which are sometimes difficult to harvest. Long husks are effective by confining the cannibalistic earworm larvae together so that most are killed, providing more food for the larvae before they reach the ear proper, possibly confining larvae for a longer time on silks deleterious to the larvae, or all three reasons. No full evaluation of these possibilities has been made. Effect of Antibiosis on Numbers of Pests of Animals Antibiosis is important in reducing the numbers of parasites on or in domestic animals. Some animals collect many ticks, yet relatively few of the parasites are able to complete feeding on the host. This is particularly apparent in one- host ticks such as the cattle tick, Boophilus annulatus (Say), or the winter tick, Dermacentor albipictus (Packard). There is little evidence to indicate why these differences occur or the heritability to be expected. Common cattle grubs, Hypoderma lineatum (de Villers), are unable to com- plete development in one line of Hereford cattle because of the intense irrita- tion that arises in the host when the grub larvae encyst in the back. The fluids that develop in the cyst and the swelling and secondary infection that usually occur cause the death of the grub larva within a week after the cyst is formed. Heritability of this factor is said to be high but of doubtful value in a breeding program because of the severe effect on the host. Antibiosis is also evident at an earlier age during the migration of the larvae through the body to the back. Extensive variations are noted between animals in the number of larvae that appear in their backs when equal numbers of eggs have been deposited on each animal. The factors involved are not yet understood. Morphological Differences as Basis of Resistance in Animals During extended periods of warm wet weather, fleeceworm (Calliphoridae larvae) attack of sheep may be extensive. Portions of the body contaminated

80 INSECT-PEST MANAGEMENT AND CONTROL with urine, particularly the breech of females and the prepuce of males, are most frequent sites of larval attack. Infestation is correlated with heavy fine fleece in these areas, combined with extensive wrinkling of the skin. Merino sheep are usually most severely attacked. They have deep heavy wrinkles around the tail, on the escutcheon, and on the backs of the hind legs. The major pre- disposing morphological characters are the heavy wrinkling and narrowness of the breech, which permits more soiling of that area with urine and feces. Breeding to remove the undesirable characters has been successful in several cases. Strains of Merino sheep are under development by breeding for less wrinkled sheep, but progeny-testing of the rams is necessary, because the con- formation of the lambs cannot be adequately predicted from that of the parents. The Rambouillet breed of sheep has retained the fine wool of the Merino, but the wrinkles and narrow breech of the Merino have been greatly altered to pro- vide a less attractive morphology to the blow flies of this critical area. Sheep raisers still using Merino sheep may obtain the same results at greater cost by a fold-removal operation (Mules operation), which removes a crescent-shaped strip of skin from above both sides of the tail, down around the vulva for about 2-inches in toward the inside of the leg, to remove excess folds of skin and leave the area relatively free of wool, as it is in the English breeds. TOLERANCE The tolerance component of resistance is present when the plant shows an ability to grow and reproduce itself or to repair injury to a marked degree de- spite supporting a population approximately equal to that damaging or destroy- ing a susceptible host. This component of resistance differs from the other two components in that it concerns a response of the plant, whereas nonpreference and preference, and antibiosis, require characteristics of the plant and an insect response. An understanding of tolerance requires a knowledge of how insects injure plants and how plants repair this injury, and tolerance is more likely to be influenced by adaptation of a variety to climatic conditions. Commonly grown varieties may carry tolerance rather than other components of resistance to an insect that has been present in an area for a long period. Tolerant plants may have more adventitious buds and greater ability to seal off injured parts when attacked by insects with chewing mouthparts (Figure 8). The replacement, regrowth, and repair of tissues are usually dependent on the stage of maturity of the plant at the time of insect attack. Plant tolerance is possibly present most often in connection with the feeding of insects with sucking mouthparts, such as aphids, leafhoppers, and true bugs. Damage by these insects may result in loss of fluid; loss of food, auxins, and other substances; clogging of conducting tissues by

PLANT AND ANIMAL RESISTANCE TO INSECTS 81 FIGURE 8 Comparative injury by corn rootworms, Diabrotica spp., to roots of a sus- ceptible U.S. hybrid 187-2 x L317 (right) and to roots on 4 stalks of a resistant 3-way hybrid involving the susceptible hybrid and a Guatemalan inbred (left). At least part of the resistance is due to the ability of the plant to replace roots faster than they are destroyed. Other components of resistance may also be present. (Courtesy Guatemala- Iowa State Tropical Research Center) stylet sheath material; and introduction of toxic fluids and enzymes. Together or individually these kinds of damage result in stunting or ab- normal growth of the plant. There has been less research on tolerance than on either of the other two components of resistance. Auxins may play a considerable part in the tolerance component. Studies of the relationship between the two aphids—greenbug and spotted alfalfa aphid, Therioaphis maculata(Buckton)- and their resistant and susceptible hosts have indicated that susceptible varieties generally had more free auxins in both quantity and kind than did resistant varieties. This suggests either that the auxins in resistant plants were bound and not available for extraction from the phloem fluid or that the aphids did not reach the phloem or other tissue containing the auxins of the resistant plants. Tolerance, especially to sucking insects, is greatly influenced by water. The water in the soil of plants being tested with populations of insects

82 INSECT-PEST MANAGEMENT AND CONTROL can be manipulated to increase or decrease the survival pressures on plants by the insects. Other variables in such research may be the number of insects per plant or the size or maturity of the plants used in the studies. RESISTANCE FACTORS MOST DESIRABLE TYPE OF RESISTANCE The most desirable and most studied type of resistance is one that is valid wherever the insect resisted is a pest; that is, resistance resulting from inherited characters rather than from ecological conditions. However, inherited characters, especially those involving physiological character- istics, are often influenced to a greater or lesser degree by environmental factors. The extent of such modifying factors in insect resistance can best be studied by the establishment of uniform nurseries, where seeds of varieties considered resistant may be assembled, packaged, and sent to various geographic areas to be grown and rated for insect infestation or damage in a uniform manner. Not all the modifying factors mentioned here will be found in any one insect-plant relationship, but the worker should be aware of their possible existence in each case studied. Climate is an important modifying factor. High humidity increases the ease of detection of odors and thus may influence in a positive or negative manner the re- sponse of insects to plant odors, thus affecting the nonpreference and preference component of resistance. SOIL MOISTURE AND NUTRITION Soil moisture conditions greatly affect tolerance levels in comparisons of susceptible and resistant plants fed on by insects with sucking mouthparts. Under drought conditions, differences between such plants are often more evident. Edaphic conditions, particularly those concerned with plant nutrition, have often been studied in connection with resistance. The suggestion is sometimes made that the use of fertilizer increases the resistance of plants to insects. The reverse, however, is true in the case of the European corn borer, where frequently the most highly fertilized, most vigorously growing corn carries the heaviest attack. Parallel tests of resistant and susceptible plant varieties under different fertility conditions show that resistance and suscep- tibility tend to be affected in the same way. Under no conditions of soil fertility has a resistant plant become susceptible or a susceptible one become

PLANT AND ANIMAL RESISTANCE TO INSECTS 83 highly resistant. The review of a number of studies of the effect of soil fer- tility on the host plant-insect relationship indicates that each species of insect, each host-plant species, and often each type of soil, constitutes a separate problem. Consequently, no general conclusion regarding the effect of a particular nutrient element can be advanced. Soil nutrition may take one of two relationships to resistance: differences in soil nutrients in small sections of plot tests may be a source of variability in resistance studies, or the soil-plant relationship may provide a mechanism of resistance. Certain plant species and varieties have the ability to extract and utilize various chemicals from the soil with greater efficiency than other species and varieties. If the increased absorption and use of the element con- tributes to resistance, the ability indicated may be a basis for resistance. TEMPERATURE Some genes for resistance to aphids in plants appear to be highly sensitive to temperature. The single genetic factor known in the resistance of wheat to the greenbug is expressed better at temperatures below 24°C than at tempera- tures of 27°C or above. At higher temperatures it is often difficult to tell resistant from susceptible plants. This temperature-resistance relationship is of minor importance in greenbug control, since resistance is required princi- pally at lower temperatures and indigenous parasites and predators usually control the greenbug at higher temperatures. The reverse temperature relationship has been true of the resistance of alfalfa, Medicago sativa Linnaeus, to the pea aphid and the spotted alfalfa aphid. In both cases a number of clones carrying genetic factors for resistance are more resistant at high than at low temperatures. In the case of resistance to each of these insect species, however, other clones carry a high level of re- sistance at all temperatures favorable to growth of plants and aphids. In clones that are variable in resistance as related to temperature, the shift from resis- tance to susceptibility can occur in a relatively few hours. The reverse shift back to resistance takes about the same length of time. Alfalfa clones with genes that are not appreciably affected by temperature, where such can be found, are preferred in practical plant-breeding. BIOLOGICAL FACTORS INFLUENCING RESISTANCE Biotypes In plant-disease resistance studies the development of races of pathogens capable of growing on disease-resistant varieties has been a feature of studies

84 INSECT-PEST MANAGEMENT AND CONTROL in some diseases. This development of races has not occurred in all plant diseases; however, it is conspicuous in the case of rust resistance in cereals. The growing of an insect-resistant variety may lead to the natural selection of insect biotypes capable of surviving on the resistant varieties. For early recog- nition of biological strains, the finding of insects of normal size developing on resistant plants, rather than the usual absence of any development or the presence of small individuals, suggests the beginning of the selection of bio- types that will feed on the resistant plants. The term biotype is used here for groups of insects primarily distinguisha- ble on the basis of interaction with relatively genetically stable varieties or clones of host plants. Such biotypes may or may not be similar to the geo- graphic races of the taxonomist or populations of insects that are distin- guishable on other biological grounds. The few cases in which biotypes have developed on resistant varieties are listed in Table 2. The European corn borer is an additional insect for which biotypes related to host plants exist, but no detailed comparative studies of the biotypes on resistant and suscepti- ble corn strains have been made. A possible reason for the relative rarity of biotypes in insect resistance as compared with plant-disease resistance is related to two features of insect resistance. First, there is often the greater complexity in the bases of insect resistance with the presence of two or more components. The second feature is the presence of the host-finding behavior of the insect, which is absent in plant-disease examples. There apparently are two kinds of insect biotypes in their relation to re- sistance. In one, exemplified by the pea aphid on peas, the biotype able to feed on resistant plants appears to be simply larger and more vigorous. In the other, such as biotypes of the Hessian fly on wheat and of the aphid Amphoro- phora rubi (Kaltenbach) on raspberry, there appears to be a "lock and key" relationship between a particular insect biotype and a genetic factor for re- sistance in the plant. Biotype B of the Hessian fly, for example, is able to feed TABLE 2 Insect Biotypes Involved in Plant Resistance (to 1966)." Insect Host Plants Number of Biotypes Known Hessian fly, Mayetiola destructor (Say) Aphid, Amphorophora rubi (Kaltenbach) Spotted alfalfa aphid, Therioaphis maculata (Buckton) Greenbug, Schizaphis graminum (Rondani) Corn leaf aphid, Rhopalosiphum maidis (Fitch) Pea aphid, Acyrthosiphon pisum (Harris) Wheat Raspberry Alfalfa Wheat Sorghum, corn Peas, alfalfa 4 4 2 2 4 3-9 "In these examples, geographic populations may be mixtures of biotypes.

PLANT AND ANIMAL RESISTANCE TO INSECTS 85 on resistant wheat plants carrying the H3 gene but not on resistant plants carrying the HS gene, or genes for resistance from the species hybrid-wheat variety, Marquillo. The lock and key kind of biotype appears to be the most common, and its presence emphasizes the importance of assembling as many genetic factors for resistance as possible in one variety or at least in each insect resistance breeding program. Plant and Insect Diseases Another biological factor influencing resistance is the presence or absence of plant diseases on the resistant and susceptible plants. The presence of a disease in a plant naturally changes its metabolism and thus may affect a basis for insect resistance. Insects are frequently vectors of plant-disease organisms and, in at least one example, that of raspberries and the aphid Amphorophora rubi (Kaltenbach), varieties resistant to the aphid also are resistant in the field to a mosaic virus carried by the insects; but in the greenhouse the aphid may carry the virus to the aphid-resistant variety. A peculiar biological feature has been found in one case of an insect disease. When European corn borer larvae feed on certain resistant corns, a protozoan disease organism, which the larvae sometimes carry, may be elim- inated, possibly by the action of RFA, so that the few larvae surviving on the resistant plants are healthier and hibernate more successfully than the greater number of larvae surviving on the susceptible plants. Other Factors There are many other factors in the environment that may affect the expres- sion of resistance and may be responsible for discrepancies in results secured by investigators under different environmental conditions. That they do occur does not change the fact of the inheritance of resistance that must form the basis of any plant-breeding. Fewer factors affect the permanence of resistance. These mostly concern changes in the genes of either plant or animal, or a small degree of learning on the part of the insect. Such possibilities exist, but ex- perimental evidence or examples of such loss of resistance are rare or nonexistent. RESISTANCE PROGRAM RESEARCH PERSONNEL In the beginning of a new resistance program, the personnel should include at least a competent plant or animal breeder and a well-trained entomologist.

86 INSECT-PEST MANAGEMENT AND CONTROL After resistance genes are located and some information is accumulated re- garding the genetics of resistance and the biological bases of insect-plant or insect-animal relationships, a biochemist can profitably be added to the team. The cooperative program by members of the team involves not only written agreements but friendly understanding and cooperation in all phases of the work. The breeder should be cognizant of the difficulties and problems in handling the insect concerned; the entomologist should have or develop a genetic point of view in looking at procedures and explanations of develop- ments. Most entomologists are trained to understand the ecological aspects but rarely the genetic possibilities of a problem. As quickly as possible, the entomologist working on insect resistance in plants, for example, should also make himself familiar with breeding procedures and materials in the crop under study, the more important varieties, and particular problems that the plant breeder faces. Moreover, he should understand that unless a new variety, carrying insect resistance, is equal to or better than currently grown varieties in other respects it will not be approved for release; more importantly, it will not be grown by farmers. It is essential that the entomologist become thoroughly familiar with the insect pest under investigation and also, as far as practicable, its near relatives. The correct identification of all instars of the insect and their type of damage as distinguished from that of other insects is of primary importance. A thorough knowledge of the biology and behavior of the insect is necessary, especially details of the relationship to known varieties of the host plant. This may be secured during or before the initiation of the resistance research. At this stage in these studies a most valuable approach is the field-planting, at different dates, of a series of varieties chosen to represent the maximum range in maturity. Such a plot series will help to separate ecological from genetic effects on insect biology. INSECT POPULATIONS An initial problem of the entomologist is maintaining and controlling the insect population so that consecutive tests of a series of crop varieties may be conducted under quite similar levels of infestation as well as other environ- mental conditions. This continuity can rarely be maintained in the field; it can be maintained more easily in greenhouse or laboratory. ANIMAL MATERIAL The development of breeds of animals that show resistance to arthropod attack is not as advanced as the work with plants. Factors involved in this lack

PLANT AND ANIMAL RESISTANCE TO INSECTS 87 of progress include the much greater cost of experimental work, particularly the purchase and maintenance of animals; the longer time required to com- plete a generation; the usually fewer offspring per generation; and the smaller number of breeds or lines available to the animal breeder. Thousands of varieties of wheat, for example, have been evaluated for insect resistance, but very few animal breeders have access to more than a small fraction of that number of breeds or lines of domestic animals. In spite of the problems involved, research is progressing. PLANT MATERIAL Where strains or individual plants (Figure 9) are less injured, sometimes have greater yield, or carry smaller numbers of a pest than nearby strains or indi- viduals of the same species, the presence of resistance may be suspected. The first plant material to be examined is the locally grown, adapted, or near-adapted varieties, together with those strains being used as sources of disease resistance and other qualities to be incorporated into an improved variety. It is difficult to find an adapted variety already resistant to the insect pest unless it is a newly introduced variety. This did occur in the case of the FIGURE 9 Alfalfa plant resistant to pea aphid, Acyrthosiphon pisum (Harris), among plants badly injured by the insect in farmer's field, Stafford County, Kansas, May 1959. (Courtesy Kansas Agricultural Experiment Station)

88 INSECT-PEST MANAGEMENT AND CONTROL spotted alfalfa aphid. When this insect in its early spread reached breeding nurseries, Lahontan, an improved variety resistant to the stem nematode, Ditylenchus dipsaci Filipjev, was quickly found also to be resistant to the aphid. There was, however, no relationship between resistance to the nema- tode and resistance to the aphid, because some of the basic clones used in the makeup of the variety were resistant to the nematode but susceptible to the aphid. The resistance of the other clones to the two organisms was simply fortuitous. SEARCH FOR GENETIC RESISTANCE The goals being sought for resistance are genetic characters and not ready- made resistant varieties. If such genetic characters cannot be found in varieties adapted to the region of study, they must be sought in plant varieties of the same crop species or, later, in related species. After studies of local varieties, the first place to look for such genetic factors is in varieties from the original home of the insect or species of the same insect genus. The second area from which to secure plant varieties is the region of maximum variability of the crop under study. The first area depends on the possibility of natural selection for resistance; the second depends on the fact that in areas where visible characters show great diversity, there also may be wide differences in physio- logical characters that could be the basis of resistance. An important principle is that the chance of finding genes for resistance is generally in proportion to the number and diversity of plants or animals that can be studied. Plant material to be studied may be secured from other re- search men working on the same crop; from the United States Department of Agriculture, which maintains germ-plasm nurseries or storage of available varieties of many crop plants; and through the help of the Food and Agricul- ture Organization of the United Nations. In all cases where sufficient germ plasm has been studied, levels of resistance of economic importance have been discovered. Also, in studies of large numbers of exotic varieties, the varieties more susceptible than those currently grown were more plentiful than resis- tant varieties. Thus, the introduction of new varieties without known insect resistance may introduce genes for greater susceptibility. As a matter of policy, all new and improved crop varieties, or animal breeds and hybrids, should be routinely tested for reaction to important pests of the crop or animal before being approved or released to farmers by the agricultural experiment station. Evidence that resistance is genetic comes primarily from a study of progeny of the supposedly resistant host, which are compared, where possible, with standard or susceptible varieties or with the original resistant plant or animal.

PLANT AND ANIMAL RESISTANCE TO INSECTS 89 To secure such progeny in plant-breeding requires self-pollination of the plant being tested or crosses with a known susceptible parent. The inherited charac- teristic is the reaction of the plant under comparable environments. If the environment is changed, the reaction may or may not be changed, but if a plant retains its resistance under different environments there is considerable proba- bility that the resistance reaction is inherited. A comparison of the detailed biology or behavior of an insect on possible resistant and susceptible hosts in various places or various environments may suggest inherent stability of the resistance. In cross-pollinated crops where one or more individual plants resistant to the insect can be found in one or more adapted varieties, such plants can be increased vegetatively or by seed for extensive testing and possible release. This was the procedure by which varieties of alfalfa resistant to the spotted alfalfa aphid were produced. Synthetic varieties produced by interpollination of individual resistant plants may also constitute important sources of selec- tion for resistant factors under various environments. If the source of resistance is found in a nonadapted variety in a self- pollinated crop, it becomes necessary to cross the resistant plant with another that is adapted to the conditions under study. This may involve choices of sources of resistance and choices of possible susceptible parents. The best parental sources of resistance are those carrying evidence of more than a single component of resistance and, if possible, more than a single gene for resis- tance. If more than a single source of resistance is available, it may be worth- while to begin a breeding program in which several sources are used simul- taneously, with the possibility of later combining the different genetic factors. The susceptible parent should not only be satisfactory for other agricultural characteristics, but, if possible, it should complement those carried by the resistant line. A single genetic factor, for instance, is easier to manipulate in plant-breeding, but its use may encourage natural selection of insect biotypes that may be able to overcome the resistance of the single gene. PLANNING EXPERIMENTS In this early search, the characteristic to look for is the relative absence of insects or insect damage on the individual variety or plant compared with a commonly grown variety. One should not attempt to look for some physical character that the entomologist thinks might be disliked by or be deleterious to the insect. To find and use insect resistance, it is not necessary that the researcher know the basis of resistance any more than it is essential that the plant breeder know the basis of high yield in order to breed for this desirable character. Where funds, personnel, and space are limited, the first tests can

90 INSECT-PEST MANAGEMENT AND CONTROL be nonreplicated trials. A single test of many new possible sources of resis- tance is sometimes better than a replicated test of a few possible sources. Varieties or individual plants appearing to be resistant may then be retested on a replicated basis, preferably under various environmental conditions. An important principle is that resistance and not immunity is being sought. Thus, the best infestation level to use is not the highest one that can be secured, but rather the level providing the maximum differences between varieties or plants in the test, or between resistant or susceptible selections, if such are available. If infestations in the tests are too low, varieties of plants or animals escaping infestation may be too plentiful. However, if infestations are too high, valuable sources of resistance may be missed. It is important to plan experiments so that individual plants or animals as well as single plant varie- ties or animal strains may be studied in a way that will ensure finding resis- tance due to all the different components. When a large group of varieties has been assembled, it is worthwhile to consider the possibility of looking for resistance to more than one insect pest, even though primary consideration may have been given to the most important one. After a possible source of resistance has been found, the next need is to determine, by cage tests if necessary, what component or components of resistance are involved and to be sure that the reaction obtained is genetic and not the result of chance, special ecological circumstances, or the genetic earliness or lateness of the variety under study. Some information on com- ponents of resistance may already be available from observation or may be secured from cage tests that compared results where insects were compelled to feed or oviposit on a single variety, plant, or animal with those in which free choice was available. TESTING PROCEDURES FOR SEGREGATING GENERATIONS Testing procedures for segregating generations of crosses between resistant and susceptible plants are generally similar to those used in the search for resistance. It is important, wherever possible, to make selection during F2 and following generations in nurseries where satisfactory insect infestations can be maintained. As in the search for resistance, tests should be designed to reveal the presence of as many components of resistance as possible in a single test or in a series of tests. Test after test and year after year, insect popula- tions should be controlled so that as nearly as possible the same level of in- festation is obtained. Here, as in the search for sources of resistance, the tests should be made in the seedling stage of the plant, provided resistance at this stage is correlated with resistance in older plants. The use of seedlings will greatly speed up testing procedures and permit the study of many more plants

PLANT AND ANIMAL RESISTANCE TO INSECTS 91 in the same space. Where insectary and greenhouse tests are made in which pest colonies bred for that purpose (and perhaps consisting of single strains) are used, frequent comparable tests must be made in the field with unse- lected populations. In some insectary colonies of insects, selections have been made, either consciously or unconsciously, with the result that such popula- tions may not behave the same as the unselected wild populations in respect to hosts. While the entomological tests in segregating populations are proceeding, parallel tests should be conducted to determine the agronomic or horti- cultural possibilities of the plant hybrid. When one or more strains approach a variety with the desired qualifications, more detailed replicated tests will be required throughout the area the new variety is expected to occupy. Such tests should be made both with and without the presence of the insect against which resistance is sought and should be designed to give comparisons with currently grown varieties and with improved varieties carrying little or no insect resistance. Information of this kind is needed for submission to committees or others in authority who approve the release of new cultivars. Advantage should be taken of all available agricultural experiment stations in the known range of the insect pest and in the area of probable adaptation of the new plant variety. RESISTANCE STUDIES BEST MATERIAL FOR STUDY Partly in parallel or following the preceding research, a study of the basis of resistance should be made, even though in either plant- or animal-breeding or insect control, information on the basis of resistance is not essential. In plants, such a study should be preceded by thorough biological and behavioral analy- ses and preferably also by genetic analysis of the insect-plant interaction. Possibly the best material for use in basis-of-resistance studies would be sus- ceptible-and-resistant isogenic lines concerned with a single genetic character for resistance. This would entail the comparison of two selections differing primarily only in the single gene for resistance with its biochemical or bio- physical basis. VALUE OF KNOWLEDGE OF BASES OF RESISTANCE It has sometimes been suggested that research on resistance should begin with a study of the bases of resistance. Available information on causes in all cases

92 INSECT-PEST MANAGEMENT AND CONTROL of resistance is not yet adequate for such research at the beginning of a new study; it must wait until sources of resistance are found. Furthermore, knowledge of one basis of resistance may be of little practical use when seedlings can be screened for resistance by exposure to insects, and many thousands of the plants can be examined in a short time. New and additional sources of resistance with different bases also may be detected when insects rather than physical or chemical tests are used. A knowledge of the basis of resistance, however, can be of value in a re- sistance program in two ways: first, to permit screening for resistant plants or animals in the absence of insects; second, with such knowledge it should be possible to combine two noncumulative kinds of resistance in the same variety or breed and be sure both are there. The only other way to do this is through genetic analysis, which might be more time-consuming. Information on the basis of resistance would be of special use in working with resistance in woody plants and in animals, where each generation takes several to many years. In both cases, sources of resistance must be known, or the indirect approach to the study must be used. The study of the mechanisms of resistance may be useful in other areas of research (see Chapters 12, 13, and 14). In addition to providing basic knowledge of insect behavior and physiology in relation to hosts, it might lead to the discovery of attractants that could be combined with insecticides away from the hosts and used in a search for or destruction of both male and female insects, or at least the females. Repellents, feeding deterrents, or toxins, if found, should be specific and useful, especially if they or related biologically active chemicals can be synthesized. Such supplementary uses may be more valuable than results in connection with resistance. KINDS OF STUDIES Studies of the bases of resistance may be either direct or indirect. A direct study involves the comparison of chemical analyses of resistant and suscep- tible plant or animal strains for differences that can be related to the insect- host reactions of the contrasting resistant and susceptible organisms. An indirect study involves a search for characteristics responsible for attraction of the insect and for characteristic responses normally shown by the insect in the finding of food materials present in susceptible hosts. A comparison with similar attempted isolations from a large number of hosts or from resistant plants or animals may lead to the location of biochemicals concerned with resistance. The indirect approach may provide a knowledge of what com- pounds to look for in resistant plants.

PLANT AND ANIMAL RESISTANCE TO INSECTS 93 LIMITATIONS TIME REQUIRED The time usually required for the development of a new variety resistant to an insect may be considerable; for a wheat variety it may be 15 to 20 years or more. This objection is, however, more apparent than real. With sufficient funds and personnel there are means of speeding up this time requirement. The comparison ordinarily thought of is with the broad-spectrum synthetic insecticides that have been rather quickly adapted to control of a new insect pest. In resistance, a comparable case is the finding of the alfalfa variety Lahon- tan, resistant to the spotted alfalfa aphid, which was evident as soon as the insect reached alfalfa-breeding nurseries where this variety was being grown. The resistant variety Lahontan was usable immediately. When resistance can be found in an adapted variety, its use for insect control can be as fast as working out a dosage for an existing insecticide. Examples of the time required for development of some insect-resistant varieties from the beginning of a search for resistance or location of a specific source of resistance to the release to farmers are: in Hessian fly resistance in wheat—Kawvale, 18 years; Pawnee, 29 years; Ponca, 19 years; in spotted aphid resistance in alfalfa-Cody, 5 years (Figure 10), Moapa, 3 years. FIGURE 10 Spotted alfalfa aphid, Therioaphis maculata (Buckton), injury preceding fall to plants of alfalfa varieties resulted in very low survival of plants of susceptible varieties at the Mound Valley Kansas Agricultural Experiment Station, April 22, 1959. Left to right: Cody, resistant; Lahontan, resistant; Buffalo, susceptible; Zia, partially resistant; Cody, resistant. Compare with Cody and Buffalo in Figure 5.

94 INSECT-PEST MANAGEMENT AND CONTROL In contrast, development and subsequent use of broad-spectrum synthetic insecticides has been considered relatively brief. Often the time required for synthesis, formulation, and small-scale testing by the patent holder or basic manufacturer, or both, is overlooked by most people. There also are ever- increasing demands for more data on toxicity before an insecticide can get label approval. It would certainly take much longer to obtain label approval now for DDT, heptachlor, dieldrin, and many other insecticides than it did during and immediately after World War II. Techniques for speeding up plant selection and plant-breeding are being constantly improved. BIOTYPES AS LIMITATIONS The presence or selection of insect biotypes able to infest resistant varieties can limit the effectiveness of such varieties. The list of known examples is given in Table 2. Such biotypes have not been as much of a problem as the development of races of pathogens in the case of plant resistance to diseases or of insect resistance to insecticides. This may be because of the complex bases of many examples of plant resistance to insects. In contrast, in the natural selection of biotypes resistant to insecticides, the organism is con- cerned with a single chemical compound, and the basis of plant-disease resis- tance may also be less complex than that of insect resistance. Although the problem of plant pathogens able to utilize a disease-resistant host is trouble- some to plant breeders and pathologists, it is usually not insurmountable. Breeders and entomologists should also be able to solve the problem of biotypes of insects. INCOMPATIBILITY OF RESISTANCE CHARACTERS WITH OTHER NEEDED CHARACTERS Another possible limitation of resistant varieties is the incompatibility of factors for resistance with other desirable agricultural or economic character- istics. For instance, it has been suggested that if chinch bugs, Blissus leucop- terus (Say), fail to grow and reproduce on a resistant sorghum the same might be true of man's domestic animals; yet Atlas sorgo, which is highly resistant to chinch bugs, became the leading forage sorghum in the United States, in part because of its high palatability to livestock. The fact is that insects rarely eat the whole plant and frequently feed in restricted areas not used as food by man or domestic animals, or they feed for only a short time during plant growth. Actually, incompatability has rarely been a problem in insect resis- tance studies. One example, however, is that of hairiness of leaves of a cotton

PLANT AND ANIMAL RESISTANCE TO INSECTS 95 resistant to leafhoppers, which may present difficulties in ginning because of leaf fragments mixed with the cotton fibers. Hairy cottons have also been reported as more favorable for the development of the cotton aphid, Aphis gossypii Glover. It is not certain, however, that the hairiness of leaves of cotton is the only factor in either leafhopper resistance or aphid susceptibility. REPLACEMENT OF VARIETIES Another possible limitation is concerned with the replacement of the old sus- ceptible varieties by new resistant varieties; or the replacement of the old re- sistant varieties, after the insect and its damage are not obvious, by new susceptible varieties, soon accompanied by a return of the pest. If the new resistant variety is also highly superior in agronomic quality, there is usually no problem in its displacing older susceptible varieties, even though farmers may normally be conservative in changes of this kind. After the new resistant variety has decreased the pest population, farmers and agricultural specialists often forget the importance of the insects until the use of a highly susceptible variety again permits an increase of the insect population. The use of secret pedigrees of plant hybrids or varieties by commercial companies aggravates situations of this kind. OTHER LIMITATIONS There may be other limitations to the use of insect-resistant varieties. There is little information, for example, regarding the effect of resistant varieties on insect parasites or diseases, especially those that have an obligate relationship to the pest. It is quite possible that with some insect-plant relationships the effect could be adverse instead of favorable. Other problems may occur as resistant varieties come into more general use. ADVANTAGES AND POTENTIALITIES EFFECT OF RESISTANCE IS CUMULATIVE AND PERSISTENT Possibly the most important advantage of the use of insect-resistant plants in insect-pest control has been that the effect of the resistant variety on the pest population is specific, cumulative, and persistent. Near-immunity to the insect is not required. A resistant plant variety that reduces the insect population 50% each generation is sufficient to eliminate in a few generations an insect of

96 INSECT-PEST MANAGEMENT AND CONTROL economic importance. This quickly cumulative and persistent effect of a re- sistant variety is in contrast to the sudden and decreasing effect of most insec- ticides and is possibly unique among insect control measures. LACK OF DANGERS TO MAN AND ENVIRONMENT Another important advantage of the use of resistant varieties is that there no problems of toxic residues; of harm to personnel, livestock, and wildlife; of toxicity to honey bees and other useful insects; or of contamination of the environment. These dangers may be present with the use of insecticides. LOW COST, ADVANTAGEOUS USE, AND POTENTIALITIES Other advantages include low cost to the farmer, utility in integrated control or pest-management programs, and the fact that a knowledge of attractants or repellents present in natural food plants may lead to the development of syn- thetic chemicals having these properties (see Chapters 13 and 14). The potentialities in the use of resistant varieties in the past have been limited primarily by funds and personnel available for research in this impor- tant area of insect-pest control. If a fraction of the amount spent on the de- velopment and testing of insecticides had been used in the development of insect-resistant varieties, many but not all of our major insect pests of crops might have been controlled or partially controlled by this means. Support for host-plant resistance development has gradually but substantially increased in recent years, as state and federal administrators have reduced emphasis on chemical-control investigations and have stressed noninsecti- cidal means, including host-plant resistance. VALUE OF LOW LEVELS OF INSECT RESISTANCE IN PLANTS The value of low levels of insect resistance in plants (Figure 11) has not received the attention it deserves. A low-level resistant variety with consid- erable tolerance, combined with the use of parasites or predators, may provide a satisfactory type of integrated control without insecticides. The host insect may furnish a steady supply of food for a parasite or predator, thus preventing its extinction, while at the same time the pest inflicts little or no damage to the host plant. There are instances where an insect cannot be controlled ade- quately on susceptible varieties even with repeated treatments by insecticides, whereas control can be achieved on resistant varieties with few treatments, if

PLANT AND ANIMAL RESISTANCE TO INSECTS 97 FIGURE 11 Varietal difference in alfalfa seedlings infested for 3 weeks with one potato leafhopper, Empoasca fabae (Harris), per two plants at 21°C. MSB-11 is resistant and Lahontan is susceptible to leafhoppers in the field. Here, the leaves of Lahontan seedlings are yellowish to reddish in color, and growth has been suppressed. The leaves of MSB-11 are deep green, and growth has been normal. (From Kansas Agricultural Experiment Station) any are needed. The corn earworm on sweet corn in the southern United States is an example of the former situation; the spotted alfalfa aphid on alfalfa illustrates the latter. SITUATIONS WHERE INSECT-RESISTANT PLANT VARIETIES ARE MOST USEFUL The use of resistant varieties is most valuable in crops of low value per acre, especially where yields fluctuate greatly because of weather and other inter- mittent hazards, or under situations where insecticidal control is unknown, unavailable, or too costly. Resistant crop varieties should be of special use in the developing countries where acreages worked by individuals are small and farmers are unfamiliar with the use of insecticides. A form of insurance can be provided by resistant varieties where the insect resisted shows wide fluctua- tions in populations, with outbreaks several years apart. The greenbug in the

98 INSECT-PEST MANAGEMENT AND CONTROL central United States is such an insect. Several greenbug-resistant varieties of barley are available, and greenbug-resistant wheats would be most useful. The insect can reproduce and destroy susceptible barley and wheat plants at low temperatures when the ordinarily useful parasites and predators are inactive and at temperatures too low for effective use of any available insecticide. Yet greenbug resistance is relatively higher at low than at high temperatures. The use of an insect-resistant variety of one crop may reduce the popula- tion of the same insect on another crop as well. In areas where corn earworm- resistant corn varieties are used in the southern United States, the damage by the same insect on cotton, where it is known as the boll worm, is reported to be reduced also, since there is a smaller total population. Where both alfalfa and peas are grown and subject to infestation by the pea aphid, a pea aphid- resistant alfalfa should reduce the problem with this insect on garden peas. In these respects the usefulness of host-plant resistance to insects is often unique among control measures. BIBLIOGRAPHY Auclair, J. L. 1957. Developments in resistance of plants to insects. Ann. Rep. Entomol. Soc. Ont. 88:7-17. Beck, S. D. 1965. Resistance of plants to insects. Annu. Rev. Entomol. 10:207-232. Bonsma, J. C. 1949. Breeding cattle for increased adaptabi1ity to tropical and sub- tropical environments. J. Agr. Sci. 39:204. Brazzel, J. R., and D. F. Martin. 1965. Resistance of cotton to pink bollworm damage. Tex. Agr. Exp. Sta. Bull. 843. 20 pp. Chesnokov, P. G. 1953. Methods of investigating plant resistance to pests. All-Union Society for the Dissemination of Political and Scientific Knowledge, Leningrad Branch. (Published from the translation of the Russian book, 1962.) Office of Technical Services, Department of Commerce, Washington, D.C. 107 pp. Chesnokov, P. G. 1955. Resistance of agricultural plants to pests. All-Union Society for the Dissemination of Political and Scientific Knowledge, Leningrad Branch. (Pub- lished from the translation of the Russian book, 1962.) Office of Technical Services, Department of Commerce, Washington, D.C. 17 pp. Chesnokov, P. G. 1956. Resistance of grain crops to insects. (In Russian) (Moskva, Gos. izd-vo "Sovetskaia nauka"). 306 pp. Harrington, J. B. 1952. Cereal breeding procedures. FAO Development Paper 28, Rome. 122 pp. Harvey, T. L., H. L. Hackerott, E. L. Sorensen, R. H. Painter, E. E. Ortman, and D. C. Peters. 1960. The development and performance of Cody alfalfa, a spotted alfalfa aphid resistant variety. Kans. Agr. Exp. Sta. Bull. 114. 27 pp. Hodgson, Ralph E., Editor. 1961. Germ plasm resources. Amer. Ass. Advan. Sci. Publ. 66. 381 pp. Horber, E. 1954. Breeding crop plants resistant to insects in the U.S.A. and Canada. (In German) Landw. Jb. Schweiz. 68 (new series 3):369-393.

PLANT AND ANIMAL RESISTANCE TO INSECTS 99 Kozyelka, A. W. 1929. The inheritance of natural immunity to disease. J. Hered. 20:519-530. McDonald, R. E., and J. W. Smith. 1966. The future of animal breeding for resistance to disease and pests, pp. 148-155. In Pest control by chemical, biological, genetic, and physical means. A symposium. U.S. Dep. Agr., ARS, 33-110. Mount, G. A., D. E. Howell, E. R. Berousek, and R. D. Morrison. 1962. Estimates of heritability of fly susceptibility in dairy cattle. J. Diary Sci. 45:543-544. Packard, C. M., and J. H. Martin. 1952. Resistant crops, the ideal way, pp. 429-436. In U.S. Dep. Agr. Yearb. 1952. Painter, R. H. 1951. Insect resistance in crop plants. Macmillan Co., New York. 520 pp. Painter, R. H. 1958a. Resistance of plants to insects. Annu. Rev. Entomol. 3:267-290. Painter, R. H. 19586. The study of resistance to aphids in crop plants. Proc. 10th Int. Congr. Entomol. Proc. Montreal 1956. 3:451-458. Painter, R. H. 1960a. Breeding plants for resistance to insect pests, pp. 245-266. In Biological and chemical control of plants and animal pests. Amer. Ass. Advan. Sci., Washington, D.C. Painter, R. H. 19606. Possibilities and methods of breeding for resistance to insects in forage crops, pp. 81-83. In Proc. 8th Int. Grassland Congr., The Grassland Res. Inst., Hurley, Berks., England. Painter, R. H. 1965a. Insect resistance in plants, pp. 648-656. In Advances in agricul- tural sciences and their applications. Madras Agr. J., Coimbatore, India. Painter, R. H. 19656. Resistencia de plantas cultivadas a los insectos. 6th Reunion Latinoamericana de Fitotecnia, 1-7 de noviembre, 1964, Lima, Peru. Actas Tomo 1:110-118. Painter, R. H. 1966. Lessons to be learned from past experience in breeding plants for insect resistance, pp. 349-362. In Breeding pest-resistant trees. Proc. NATO and NSF Symposium, Pergamon Press, London. Snelling, R. O. 1941. Resistance of plants to insect attack. Bot. Rev. 7:543-586. Trouvelot, B. 1961. Colloque sur la resistance des mais et cereales aux insectes. Ann. Epiphytiesl2(4):393-468.