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CHAPTER 8 Prevention of Spread Plant-pathogenic nematodes move only relatively short distances under their own power; therefore, the most usual means of nematode spread is the trans- portation of infested soil and infected vegetative plant parts by man. Nema- todes may also be carried by wind, water, and domestic or wild animals and birds. Active stages of most nematodes are susceptible to desiccation; thus, the resistant or resting stages are the ones most important in long-distance spread. Establishment in a new area occurs only when sufficient numbers of viable nematodes are transported to a location where susceptible hosts are subsequently planted and where the environment is suitable for reproduction of the nematode species. MEANS OF DISSEMINATION SOIL AND PLANT TISSUE Soil and vegetative plant parts, because they often protect nematodes from desiccation and are frequently transported by man, are important carriers of nematodes over both short and long distances. Soil is also important because most plant-pathogenic nematodes spend at least part of their lives in soil, and soil thus infested is commonly transported along with plant materials. Nematodes are frequently present on the surface of true seed and in asso- ciated debris or soil. For example, cysts of the sugar-beet nematode (Heter- odera schachtii) have been found on sugar-beet seeds. Only a few nematode species, such as seedgall nematodes (Anguina spp.) and the stem nematode 85

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86 BASIC PRINCIPLES OF CONTROL (Ditylenchus dipsaci), infect true seed, but many kinds of plant-pathogenic nematodes infect vegetative plant materials used for propagation, such as transplants, ornamentals, nursery stock, bulbs, and corms. Since these high- acre-value plants are cultivated on the best soil available, one crop is grown frequently or continuously on the same land, often resulting in damaging nematode populations in plant materials and in the soil. Infected propagation materials are particularly important in nematode spread, because materials from a relatively small area are used to plant much larger and often widely separated areas. A pathogenic nematode introduced into a field in this manner is likely to spread throughout the field (Figure 39), to adjacent fields on the same farm, and to adjacent farms. Although experimental data indicate that plant-parasitic nematodes passing through the digestive tracts of animals are killed, infected plant parts and soil associated with manure are important in spreading nematodes. MACHINERY, REUSABLE CONTAINERS, AND FERTILIZER Nematode-infested soil and infected plant materials may be transported along with machinery and reusable containers, such as burlap bags and crates. Nema- todes moved by these means are often deposited in soil in which susceptible crops are grown later. Nematodes may also be carried from infested to clean FIGURE 39 Areas of poor growth shown in aerial view of sugar- beet field indicate pattern of spread of sugar-beet nematode (Heter- odera schachtii).

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PREVENTION OF SPREAD 87 fields on automobiles, especially in soil clinging to tires and fenders. The pea- nut lesion nematode (Pratylenchus brachyurus) is spread by the use of in- fected peanut hulls as a conditioner in fertilizers. The golden nematode (Heterodera rostochiensis), an introduced pest, was found in more than 30 fields of one grower on Long Island, New York. These fields were on various farms located among uninfested fields. It was con- cluded that nematode spread was associated with the movement of machinery and used burlap bags. ANIMALS Undoubtedly, nematodes are disseminated in mud or plant debris clinging to birds and other animals, but there is little published information on the extent of this means of spread. Potentially, stages of plant-pathogenic nematodes resistant to drying could be carried for long distances by migrating birds. Some animals, such as rodents and insects, live in the soil and thus are often con- taminated with infested soil. Horses and other animals used to pull farm im- plements may transport infested soil within and between fields. Many kinds of nematodes may be spread on clothing, shoes, hand tools, or hands. Rhadi- naphelenchus cocophilus, the causal agent of red ring of coconut, is dissemi- nated by the palm weevil and other insects. WATER Although nematodes may be carried for relatively long distances in irrigation water, only local spread generally occurs in surface water. Nematodes may be transported short distances by spattering raindrops. Living nematodes may be carried by the movement of underground water, but dead or inactive nema- todes are not carried through soil, even by water at high flow rates. In coarse-textured soils of Florida citrus orchards, spread of the burrowing nematodes (Radopholus similis) downhill in surface-drainage water was eight times the rate of uphill movement. Also, in Florida citrus orchards this nema- tode moved under a hard-surface road in underground water. In an experiment in which a column of coarse-textured Florida soil 42 inches high and 3 inches in diameter was watered intermittently from the top, the burrowing nematode was moved from top to bottom in 30 hours. Nematode spread by water, particularly long-distance spread, depends on resistance of the nematode to submersion in water, and resistance varies among species and among stages of a species.

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88 BASIC PRINCIPLES OF CONTROL Irrigation, which is used more in crop production every year, effectively transports nematodes. More information of the importance of this means of spread is urgently needed. WIND Although wind is often mentioned as an important factor in nematode dis- semination, there is little evidence of long-distance spread by wind or of ex- tensive local spread in the direction of prevailing winds. Large quantities of soil and small pieces of plant debris are blown from field to field, farm to farm, and for even greater distances, but only nematodes resistant to drying survive such dissemination, and most stages of the majority of nematodes are killed easily by desiccation. Large numbers of cysts of the golden nematode, which are highly resistant to drying, were found in snow along roads adjacent to Long Island, New York, potato fields infested with this nematode. It ap- pears doubtful that these relatively heavy cysts would be carried by wind for long distances. NATURAL BARRIERS Natural barriers such as mountains and oceans reduce nematode spread by water, wind, animals, and by soil adhering to farm machinery. However, the use of refrigerated ships and trucks and of airplanes makes possible the trans- portation of infected plant materials over or around practically all natural barriers. Infested soil may be carried along with both host and nonhost plants. If the climate is unsuitable, an introduced nematode species either will not survive or its population increase will be so slow that it will not become an economically important pest. Climatic factors not only influence nematode survival directly but also influence it indirectly by their effect on kinds of crop plants that can be grown. Although a nematode is transported to a new area with favorable environ- ment, it will not become established unless one or more cultivated or wild hosts is present. If a cultivated host is grown infrequently in a crop rotation and wild hosts are absent, the introduced nematode may die from starvation. However, any species of plant-parasitic nematode should be considered a potential threat to agriculture in areas free of that species, and all means should be taken to prevent its entry.

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PREVENTION OF SPREAD 89 PRACTICES TO RESTRICT SPREAD SANITATION It is particularly important to control nematodes in nurseries, because plant materials from them are widely distributed. All soils in nurseries should be treated with steam or nematocides. Floors, benches, containers, tools, and storage areas of buildings in which plant materials are handled or stored should be thoroughly cleaned or fumigated. Splashing of water should be avoided, and hose nozzles should be kept off the floor. Clothing and shoes worn by workers in nematode-infested areas should not be worn in nematode- free areas. The identity of new plant material should be maintained and the material isolated until it is known to be free of plant-parasitic nematodes. Nematode- contaminated plant material should be isolated and either discarded or treated, if satisfactory treatments are available. NEMATOCIDAL TREATMENTS The control of plant-pathogenic nematodes in nurseries by the use of heat and nematocidal chemicals results in the production of high-quality nursery stock and reduction of nematode spread. Moist heat, when properly used, will eliminate nematodes from soil, but it is expensive and thus practical only for relatively small areas or quantities of soil. Nematocidal chemicals, when used commercially as preplan! treatments, will not eradicate nematodes from soil but will kill a high percentage of them. Because of application problems and phytotoxicity of most nematocidal chemicals, the treatment of soil around living plants is generally less effective than preplant treatments. Control, which approaches eradication of nematodes inside roots of some plant species, has been achieved by dipping bare roots in aqueous solutions of nematocidal chemicals. Although extensive plant damage often results, some hot-water treatments kill nematodes in plant tissues. For example, hot water is used to treat garlic bulbs infected with stem nematodes, grape rootstocks infected with root-knot and lesion nematodes, and citrus rootstocks infected with burrowing nematode and citrus nematode (Tylenchulus semipenetrans) (Figure 40). To increase the effectiveness of nematocidal treatments, research should be directed toward developing inexpensive, effective, nonphytotoxic chemical-dip treatments for bare-rooted stock; safe and effective drenches or fumigants for established plants and container-grown or balled stock; and effective systemic nematocides.

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90 BASIC PRINCIPLES OF CONTROL FIGURE 40 Hot-water treatment of grapevine rootings for eradica- tion of root-knot (Meloidogyne spp.) and lesion (Pratylenchus spp.) nematodes: right tank for presoaking; center tank for treatment, 51.5°C for 5 minutes; left tank for cooling. (Courtesy of the Depart- ment of Nematology, University of California.) CERTIFIED PLANT MATERIALS The production of vegetative plant-propagation material that is certified to be nematode free or to have a specified level of infection is accomplished by growing clean plants in clean soil or other media. Strict sanitation must be practiced, and both the material and the rooting medium must be periodically checked for the presence of pathogenic nematodes. Vegetative seed of banana free of the burrowing nematode, potato seed pieces free of the golden nema- tode, garlic cloves free of the stem nematode, and strawberry plants free of root-knot and lesion nematodes are produced commercially. The use of resistant or immune plant varieties also reduces nematode spread. Of course, resistant varieties, which are symptomless hosts of a patho- genic nematode, reduce chances of nematode detection and thus increase spread. QUARANTINES AND REGULATIONS Practically all countries and subdivisions of countries have some type of plant disease and pest act under which exclusionary measures are promulgated.

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PREVENTION OF SPREAD 91 Quarantine measures are fundamentally regulatory and prohibitory. They prohibit the introduction into a specified area of a particular plant or possible carrier of a pest, whether or not it is known to be carrying the pest, but nearly every quarantine includes provisions that allow for the introduction of plants or possible carriers that in some manner have been protected against or freed from contamination by the pest against which the quarantine is estab- lished. These exceptions to total exclusion regulate rather than prohibit the movement of the pest and of plant parts with which it is associated. For example, the United States federal soybean cyst-nematode (Heterodera glycines) quarantine prohibits the movement of root crops from the regulated areas where they are grown, but it also provides that root crops (except sugar beets) may be exempted "if cleaned free of soil." The prohibition of move- ment is a quarantine measure, while the provision for cleaning the root crops is a regulation allowing free movement of plant materials freed of the pest. The New York State golden-nematode quarantine prohibits the movement of plants of tomato or eggplant grown on infested or dangerously exposed fields. Quarantine acts may be either local or general. A local or district quaran- tine, of which the soybean cyst-nematode quarantine is an example, prohibits introduction of plants or other potential carriers from specified districts in which the nematode pest is known to occur. A general quarantine forbids the importation of plants or carriers from any area, regardless of whether or not the pest is known to occur there. The California quarantine against the burrowing nematode is not a general quarantine, as it prohibits introduction of soil and rooted plants from Florida, Hawaii, and Puerto Rico, with various specified exceptions and regulatory provisions. However, administrative instructions added as an appendix to the quarantine require that host plants in nine specified genera must be intercepted and inspected for burrowing nematodes by laboratory methods, regardless of their origin. These latter provisions, in effect, extend the quarantine into a general one in regard to certain plants. Provisions included in quarantines, and other regulatory measures, may in- volve a wide variety of measures aimed at giving assurance that the pest is not being introduced with the exempted plants or articles. Certification of origin is one of the most common provisions. The California burrowing-nematode quarantine provides, for example, that plants may be exempted if they bear an official certificate stating that they were grown where surveys failed to detect the pest. The same quarantine includes another type of provision that deals with the conditions under which the plants were produced, viz., "above ground in sterilized soil or other suitable material prepared or treated to assure freedom from burrowing nematode." Another common regulatory measure requires that plants or carriers be subjected to a specified treatment for destruction of the pest. Several counties

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92 BASIC PRINCIPLES OF CONTROL in California's central valley restrict the entrance of sugar-beet harvesting machinery unless it has been thoroughly steam-cleaned, and similar require- ments are in effect in soybean cyst-nematode and golden-nematode quaran- tines. United States federal plant-quarantine officials at ports of entry require methyl bromide fumigation of used bags that may be contaminated with golden-nematode cysts. Regulations may place stringent controls over every aspect of the growing of crops to prevent the possibility of spread of nematode pests. The New York State Golden Nematode Act of 1947 placed the planting, growing, and harvest- ing of potatoes under the direction of the project administrator and included regulations relating to crop rotation, topsoil movement, and soil treatment. In addition to compulsory regulations issued in direct connection with quarantines, other types of regulatory measures may be used on a voluntary basis to exclude nematode pests or restrict their spread. These include various programs mentioned earlier for certification, registration, or inspection of nursery stock, bulb crops, seed potatoes, seed garlic, or other types of agri- cultural seed. While these programs may contribute to the purposes of quar- antine and are often enforced by quarantine officials, their principal object is improvement of quality of the planting stock, and they are usually instigated by the growers themselves. Accurate knowledge of the distribution of a nematode is essential before the promulgation of a quarantine or regulation involving that nematode. Be- fore the distribution can be determined, the nematode species must be cor- rectly identified by a taxonomic specialist. In general, a nematode is quarantined or regulated only when it is of known economic importance in one area and unknown, or occurs as a localized or incipient infestation, in the area to be protected. Occasionally, as a safeguard, a quarantine or regulation is established against a nematode believed to be new to an area and suspected of being economically important. When the barley root-knot nematode (Meloidogyne naasi) was identified in a small area in the Tulelake Basin of northern California, regulations on the movement of root crops and machinery were established. The economic im- portance of the nematode was not well known, but it was the only known infestation of this nematode in North America, and safeguards against spread appeared to be warranted. Inspections for the presence of nematode pests, for enforcement of quaran- tines and regulations, may be made at either the point of origin or destination. Inspection at origin offers several advantages over destination inspection: nematodes are more readily detected in fresh soil or plant samples collected from the growing crop; infested areas may be effectively delimited; duplica- tion of sampling of material shipped to many destinations is avoided; and shipping costs of contaminated materials are avoided. Bulb crops and other

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PREVENTION OF SPREAD 93 ornamentals grown in the Netherlands are inspected annually for presence of the golden nematode before they are shipped to the United States. In the enforcement of the U.S. Plant Quarantine Act and subsequent regu- lations and quarantines, federal port and border inspections annually intercept numerous important plant-pathogenic nematodes. During the fiscal year 1964- 1965, the golden nematode was intercepted 101 times; the oat cyst nematode (Heterodera avenae), 42 times; and root-knot nematodes, 66 times. State regulatory agencies also make quarantine or regulatory inspections of plant materials in interstate shipments. In 1965, the nematology laboratory of the California Department of Agriculture examined about 1,250 soil and plant samples taken from shipments originating outside the state: 31 of the samples contained nematodes not known to be established in California, and nematode pests of significant economic importance to agriculture were found in 275 of the samples. Although careful inspections and surveys are of great value, all nematodes are not detected by present methods. Thus, populations below the detectable level must be considered in an over-all control program. The detection of nematodes by quarantine and regulatory workers is diffi- cult, because plant symptoms are not diagnostic for most of the important root-feeding nematodes. Although visual inspection for nematodes is widely used, it is recognized that usually only heavy infections of root-knot and lesion nematodes can be detected in this manner. Despite the limitations of quarantines and regulatory measures and the difficulties in measuring their effectiveness, they have played an important role in limiting the spread of plant-pathogenic nematodes. Furthermore, they encourage growers to produce clean plant materials and discourage the ship- ment of nematode-infected materials. Basic information from future research in such areas as nematode taxon- omy, host-range studies, pathogenicity, and soil- and plant-sampling is urgently needed for improving methods used to prevent nematode spread. BIBLIOGRAPHY McCubbin, W. A. 1950. Plant pathology in relation to federal domestic plant quaran- tines. Plant Dis. Rep. SuppL 191:67-91. McCubbin, W. A. 1954. The plant quarantine problem. Chronica Botanica Co., Waltham, Mass. 255 pp.

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CHAPTER 9 Reduction of Nematode Populations through Land-Management and Cultural Practices Most plant-parasitic nematodes can be controlled to varying degrees by land- management and cultural practices. These include fallow, the practice of keep- ing the land free of all plant growth; flooding; growing cover crops; crop rota- tion; time of planting; organic manuring; removal or destruction of infected plants; trap and antagonistic crops; nutrition and general care of host; and sanitation and the use of nematode-free planting stock. The specific principles involved in control of nematodes by land- management and cultural practices differ; however, all are based on the inability of nematodes to survive, multiply, and cause disease under the con- ditions imposed on them by the use of these practices. Most of these practices reduce nematoui, populations gradually over a period of weeks, months, or even years, as opposed to rapid kill such as that obtained with heat or toxic chemicals. Furthermore, as control is relative, satisfactory economic control may not be achieved by any single practice but by a combination of several practices. The fact that a practice that reduces the nematode population con- siderably may not be economically effective at present does not preclude the possibility that it may be economically feasible in the future. With the advance of knowledge of the effect of specific practices on nematode populations and with more efficient implementation of practices, for example, through im- proved machinery, a high degree of control may be possible. Because of this possibility, those practices that are known to reduce nematode populations to a measurable extent are discussed even though they may not be economically feasible or widely used at this time. 94

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LAND-MANAGEMENT AND CULTURAL PRACTICES 95 FALLOW Fallow is the practice of keeping land free of all vegetation for varying periods by frequent tilling of the soil by disking, plowing, harrowing, or by applying herbicides to prevent plant growth. At least two principles of nematode con- trol are represented by this practice. The first principle, and perhaps the most important, is starvation of the nematode. Plant-parasitic nematodes are obligate parasites, depending on living hosts for the food necessary to develop to maturity and to reproduce. There- fore, in the absence of a host plant, the nematode will die after the stored food in the body has been depleted. Some of the cyst nematodes (Heterodera spp.) can survive as unhatched eggs or dormant larvae in cysts in the soil in the absence of a host for at least 14 years, but these are exceptions. In upper soil layers, most plant-parasitic nematodes probably do not survive for more than 12 to 18 months, and many do not survive the first 6 months. Compared with upper soil layers, soil at lower depths is more constantly cool and moist, increasing the length of nematode survival. Survival is also influenced by the amount of infected root debris remaining in the soil from the previous crop. The second principle involved in fallow is death through desiccation and heat. With some exceptions, nematodes of most species, depending on stage of development, will die if exposed to the drying action of the sun and wind. When fallow land is tilled frequently to destroy vegetation, the surface strata of soil are exposed to the drying and heating effects of wind and sun. Fallow is especially effective in areas of low rainfall and high soil temperatures or in areas where rainfall is seasonal, thus resulting in long periods, perhaps 6 months or more, of dry conditions. There are several objections to the practice of fallow: the operations nec- essary to maintain lands completely free of vegetation are difficult and ex- pensive; fallow in areas of high rainfall is a poor soil conservation practice and is likely to impair the physical structure of the soil; and fallow land does not contribute to farm income. FLOODING Flooding of fields to control nematodes is not widely accepted. Results of early investigations indicated that flooding for 12 to 22 months is required to rid soil of root-knot nematodes (Meloidogyne spp.). Where water is plentiful and level land can be taken out of production for long periods, flooding may be a useful control practice. Certain crops, such as rice, can grow under flooded conditions. Experiments showed that rice seeded in water and kept flooded for 4 to 6 weeks had only a trace of the white tip disease caused by

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156 BASIC PRINCIPLES OF CONTROL BIBLIOGRAPHY Allen, M. W., and D. J. Raski. 1950. The effect of soil type on the dispersion of soil fumigants. Phytopathology 40:1043-1053. Carter, W. 1943. A promising new soil amendment and disinfectant. Science 97(2521): 383-384. Castro, C. E. 1964. The rapid oxidation of iron (II) porphyrins by alkyl halides. A pos- sible mode of intoxication of organisms by alkyl halides. J. Amer. Chem. Soc. 86:2310-2311. Chitwood, B. G. 1952. Nematocidal action of halogenated hydrocarbons. Advan. Chem. Ser. 7:91-99. Christie, J. R. 1945. Some preliminary tests to determine the efficacy of certain sub- stances when used as soil fumigants to control the root-knot nematode, Heterodera marioni (Cornu) Goodey. Proc. Helminthol. Soc. Wash. 12(1):14-19. Good, J. M., and A. L. Taylor. 1965. Chemical control of plant-parasitic nematodes. U.S. Department of Agriculture Handbook No. 286. Goring, C. A. I. 1957. Factors influencing diffusion and nematode control by soil fumi- gants. The Dow Chemical Company ACD. Information Bulletin No. 110. Goring, C. A. I., and C. R. Youngson. 1957. Factors influencing nematode control by ethylene dibromide in soil. Soil Sci. 83(5):377-389. Ichikawa, S. T. 1956. Nematode control versus application depths of Nemagon. Phyto- pathology 46:637. (Abstract) Lear, B., and D. J. Raski. 1962. Survival of root-knot nematodes in excised grape roots in moist soil fumigated with ethylene dibromide. Phytopathology 52:1309-1310. Moje, W. 1960. The chemistry and nematocidal activity of organic halides. Advan. Pest Contr. Res. 3:181-217. Rohde, R. A. 1960. Acetylcholinesterase in plant-parasitic nematodes and an anticholin- esterase from asparagus. Proc. Helminthol. Soc. Wash. 27:121-123. Stromberg, L., L. W. Carter, J. R. Stockton, and G. A. Paxman. 1965. Placement of fumigant affects root knot control. California Farmer, February 6, 1965, p. 20.

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CHAPTER 14 Evaluation and Selection of Control Measures A nematode disease problem can usually be solved in a number of different ways. The research nematologist, agricultural specialist, and farmer are faced with the evaluation of the disease problem. From the various control methods available, they must select the method that is the most effective, most economi- cal, or both. The method selected will depend on the nematode species, the host plant, the environmental situation, the cash value of the crop, and the relative cost of available control methods. INTEGRATION OF CONTROL MEASURES In most cases, practical control of a nematode disease involves integration of several diverse control measures. Some nematode diseases can be prevented merely by using nematode-free seed or vegetative propagating materials. For example, the disease caused by the wheat nematode (Anguina tritici) is pre- vented by planting clean seed in land that has not been planted to wheat for at least one year. The garlic disease caused by the stem nematode (Ditylen- chus dipsacf) can be prevented by planting nematode-free garlic cloves in clean soil. The disease of banana caused by the burrowing nematode (Ra- dopholus similis) can be controlled in banana plantations by eradicating the nematode from the rhizomes used to propagate bananas and planting this seed in soil that is free of the nematode. New citrus orchards can be kept free of either the citrus nematode (Tylenchulus semipenetrans) or the burrowing nematode by using trees produced in clean nursery soils and planting in orchard sites free of these nematodes. 157

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158 BASIC PRINCIPLES OF CONTROL The application of a preplan! nematocide is often all that is required to control a nematode disease effectively. For example, diseases of a number of annual crops caused by the root-knot nematodes (Meloidogyne spp.) can be controlled by preplant soil fumigation. Several procedures, however, are necessary to control nematode diseases on a number of perennial and annual crops propagated from vegetative materials such as roots, bulbs, corms, rhizomes, slips, and transplants. The propagating stock and soil must be rela- tively free of nematodes. For perennials, such as tree and vine crops, the com- bination of nursery propagation of nematode-free plants and preplant soil fumigation is required when the soil is infested. In The Netherlands, the pro- duction of bulbs requires the use of treated bulbs in fields that have had care- fully controlled rotations. In addition, the field must be surveyed prior to planting and must be free of the golden nematode (Heterodera rostochiensis) to prevent contamination of the bulbs by infested soil at harvest. Control of root-knot damage to sweet potatoes involves at least three phases of the pro- duction: first, the selection of seed roots that are either free of nematodes or freed of nematodes by hot-water or dry-heat treatments; next, the placing of the seed roots into beds of sand or coarse-textured soil that either is nematode- free or, if infested, is preplant fumigated, preferably under tarps, or steamed to eliminate the nematodes; and, finally, the transplanting of the clean "slips" into nematode-free soil or preplant-fumigated soil. With many nematode problems, there is a tendency to rely too heavily on only one method of control. More research is needed on utilization and inte- gration of nematode control measures. EFFECTIVENESS AND ECONOMICS The ideal way to control a nematode disease is to eradicate the nematode, or nematodes, involved. This has been accomplished only in very limited areas such as greenhouses or propagating beds. With the soil fumigants in use today, it is not feasible to eradicate nematodes that are distributed throughout the soil mass to a depth of 12 to 15 feet, such as root-knot nematodes on grape or burrowing nematode on citrus. In such cases, preplanting fumigation is di- rected at reducing the nematode population density to well below the tolerance level of young transplanted trees and vines. However, eradication of nema- todes with present-day preplant soil fumigants is more likely for those nema- todes distributed in the surface soil, such as the potato rot nematode (Dity- lenchus destructor). Large sums of money are spent for nematocides to limit spread and pos- sibly achieve eradication of incipient infestations of introduced nematode pests that cause severe crop damage and are difficult to control by other means.

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EVALUATION AND SELECTION OF CONTROL MEASURES 159 Such control involves high nematocide dosage rates, gas-proof tarps, and re- peated treatment. Funds expended for this purpose are justified because of the potential crop loss if noninfested acreage becomes infested. The actual cost of restoring the infested acreage to a productive level is not involved. On a more restricted basis, the same cost-effectiveness criteria can be ap- plied to nurseries. With the recent advent of quarantine laws requiring close inspection of nursery plants moving in inter- and intrastate commerce, nema- tode problems have become much more acute for nurserymen. In some cases, nematocide at a cost in excess of $200 per acre is applied to nursery soils; the expenditure is justified, since noninfected nursery plants can generally move freely in the trade. The use of nematocides for possible eradication of nematodes in nurseries has received considerable attention. New chemicals or combinations of chemi- cals for testing are continually available. New application equipment, such as mechanized tarp layers, has been developed. Research to determine which pre- plant nematocide to use and how to use it most effectively should be inte- grated with studies on the use of postplant nematocides designed to keep nematode populations below economic levels on living plants. Further studies on the detection of nematodes at very low population densities also are needed. This would assist in quarantine work and in the evaluation of the ef- fectiveness of control practices. In some cases, treating soil with high dosages of nematocides before plant- ing perennial crops is justified purely on the basis of increased plant growth and production. An initial cost of $250 per acre for preplant treatment of citrus soil with 1,3-D (1,3-dichloropropene) can be less than the increased value of fruit in the first three years of production. The investment of $250 per acre for soil fumigation is not unreasonable for a crop such as citrus, for which the investment in land and trees may exceed $4,000 per acre. The effectiveness of preplant soil fumigation of soils planted to perennial crops has been judged on the basis of how closely nematode control approxi- mates eradication. This reflected the long-term nature of the crop, the inability to rotate, and the lack of an effective nematocide that could be used for postplant treatment. The development of DBCP (l,2-dibromo-3-chloropropane), which is effective in controlling a limited number of nematode species around the roots of living plants, changes this situation somewhat and points the way for additional research. A critical need remains for nematocides to use in postplant treatments to kill endoparasitic nematodes in the roots of perennial crops. Such chemicals would further reduce the necessity of striving for eradi- cation, with its high cost in preplant treatments for perennial crops. After soil application, such a chemical would enter roots from the soil, or, after foliar application, it would move from the foliage to the roots. Various com- binations of nematocide treatments could then be utilized to control all kinds of nematodes that parasitize plants.

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160 BASIC PRINCIPLES OF CONTROL The economic return from soil fumigation is an important consideration. A compilation of reports from the United States compares crop yields on plots treated with nematocides with yields on untreated plots. In 853 comparisons involving seven crops, an average increase in yield of 87 percent resulted from nematocide application. Yield increases for crops for which more than 25 comparisons were available are shown in Table 1. Although the evidence does not support the conclusion that differences were solely the result of nematode control, it is evident that nematocides have a favorable influence on the yield of several crops in many parts of the United States. While these data provide strong circumstantial evidence that nematodes severely reduce crop yields, they indicate little about the economic returns from fumigation. An increase of 100 percent in the yield of sugar beets may not result in a net profit to the grower, whereas an increase of 13 percent in tobacco may be profitable. In California, yields of sugar beets are increased consistently when soil infested with the sugar-beet nematode (Heterodera schachtii) is fumigated with nematocides containing 1,3-D; but if yields are increased from 9 to 18 tons per acre, no profit is returned to the grower, be- cause 18 tons per acre are required to pay production costs. Thus, although fumigation is successful from the standpoint of nematode control and in- creased sugar-beet yields, it is generally not considered economically successful and is not recommended. In other states, such as Colorado and Utah, soil fumigation consistently results in profits to sugar-beet growers and is recom- mended. In California, soil fumigation for root-knot nematode control on sugar beets in the San Joaquin Valley is recommended, because the nematode drastically reduces the tonnage of roots produced and also affects the quality of the root and, consequently, the ease with which sugar is extracted. As another example, the average yield of cotton in the United States is about one bale per acre. Yet, in Arizona and California, soils producing two to three bales per acre respond to soil fumigation. When the soil is sandy loam and root-knot nematodes are prevalent, soil fumigation consistently improves yields. Nematodes are the primary limiting factor to plant growth in these TABLE 1 Yield Increase Following Soil Application of a Nematocide Crop Plant Increase (%) Lima bean 35 Cotton 91 Soybean 126 Sugar beet 175 Tobacco 13 Tomato 73

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EVALUATION AND SELECTION OF CONTROL MEASURES 161 fields, since other crop inputs, including soil moisture, are rigidly controlled. On farms with large acreages, an increased return of $50 per acre is important. Shortly after the introduction of such successful nematocides as 1,3-D and EDB (ethylene dibromide), it was suggested that the increase in crop value compared with the cost of fumigation should be a ratio of 4 to 1. Actually, no generalized practical formula is applicable: every nematode-crop inter- action must be analyzed with respect to its individual geographic and economic circumstances. Data accumulated over a 20-year period on nematode prob- lems and soil-fumigation results on a certain crop in a specific geographic location provide much better criteria for making fumigation recommendations than do arbitrary figures on returns per dollar invested in nematocides. Root crops such as carrots, sweet potatoes, table beets, and white potatoes are markedly reduced in quality and in market acceptance by diseases caused by root-knot nematodes, even though the crop yield may not be materially affected. Cash returns on a crop of sweet potatoes are increased as much as $300 per acre from an expenditure of only $30 per acre for soil fumigation. This results from an increase in the pack-out of higher grades without any significant increase in total production. In Georgia, control of the lesion nematode (Pratylenchus brachyurus) on peanuts by soil fumigation increases the yield of high-grade peanuts. Postplant treatment of Valencia and navel oranges with DBCP significantly increases the percent of larger fruit, thereby increasing profits. At present, quality of crop produce as related to nematode control is usually considered only in terms of economics. However, with increased knowl- edge concerning the influence of nematodes on the nutrient status and physi- ology of host plants, it will be important to explore the effects of nematodes on factors such as fiber length and strength in cotton, flavor and vitamin con- tent in edible annual and perennial crops, and nutrient content of forage crops for livestock. Soil fumigation may adversely affect the growth and quality of some plants. Bromine-sensitive crops, such as onion, carnation, and citrus, are sometimes stunted by preplant soil fumigation with nematocides containing bromine. In some cases, this may be sensitivity to the nematocide itself rather than to bromine. These points need additional research for clarification. LEVEL OF AGRICULTURAL DEVELOPMENT RECOGNITION OF A PROBLEM In some areas of the United States, and in many of the underdeveloped coun- tries of the world, there are two primary obstacles to effective nematode

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162 BASIC PRINCIPLES OF CONTROL control. The first, and perhaps the most important, is lack of recognition that plant-parasitic nematodes are seriously limiting the potential yield of crops. The main reason for this is the shortage of agriculturists at all levels who recognize and understand nematode diseases. This situation is changing as nematologists increase in numbers and more agriculturists receive training in nematode control. The second obstacle is primarily economic and represents a lack of capital to invest in equipment and nematocides. Cultural control methods and resistant varieties should be used where feasible, since, for many nematode diseases, nematocides are too expensive. In some countries, import duties and marketing costs raise the price of fumigants to levels that are pro- hibitive for most uses. Under such circumstances, it is not surprising that soil fumigation is not a widespread practice in all agricultural areas of the world. GROWTH OF SOIL FUMIGATION IN THE UNITED STATES The increase of soil fumigation in the United States is impressive. Since its infancy in 1943, it has developed into an established agricultural practice. According to the U.S. Bureau of Census, 1963 Census of Manufacturers, pro- duction of soil fumigants in 1958 amounted to 25,446,000 pounds, as com- pared with 61,356,000 pounds in 1963. Under intensive cultural conditions, large quantities of methyl bromide are used for the control of weeds, nema- todes, and soil insects. Large quantities are applied to tobacco seedbeds in southeastern states. In California, one of the oldest soil treatments is a mixture of methyl bromide and chloropicrin, which is applied, before planting, on a large proportion of the strawberry acreage at the rate of 300 pounds per acre, costing approximately $270. An estimated 10 million pounds of EDB are used annually in the United States for soil fumigation. EDB and 1,3-D are used extensively in tobacco fields of the southeast. In the pineapple fields of Hawaii, 1,3-D is the principal preplant fumigant that is used. In the cotton fields of Arizona and California, 1,3-D is also widely used as a preplant fumigant. Use of DBCP as a soil fumi- gant has increased rapidly; in 1962,1,545,000 pounds; in 1964, 5,314,000 pounds; and in 1966, 8,722,000 pounds were produced. Although the use of nematocides is expanding, only a fraction of the world's soils that could benefit from nematocide applications are presently treated. SPECIFIC METHODS OF EVALUATING CONTROL MEASURES NEMATODE CONTROL In previous sections, control measures were considered primarily from the standpoints of effectiveness in killing nematodes and of cost. The technical

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EVALUATION AND SELECTION OF CONTROL MEASURES 163 problems involved in actually evaluating the relative effectiveness of the control measures were not emphasized. With regard to nematode control, questions arise as to when, how, and where to sample fields for detection of crop-damaging nematodes. Detailed studies on sampling methods were made in England and The Netherlands on the cyst nematodes, Heterodera schachtii and Heterodera rostochiensis. Tech- niques that give consistent and statistically sound results were developed. With these nematodes, the level of infestation in the top 1 or 2 feet of soil is the primary concern. Reliable estimates of soil populations to depths of 8 to 10 feet or more are needed for many nematode species, particularly for those that are parasitic on deep-rooted perennials. Several reliable techniques are available for extracting nematodes from soil and plant samples. New procedures for collecting samples and obtaining information on the number of samples required for reliable data are needed. The most urgently needed information includes dependable procedures for making predictions on potential crop losses, based on the kinds and numbers of plant-pathogenic nematodes recovered from soil and root samples. On the basis of this information, recommendations can be made concerning whether or not soil fumigation of a particular area of land would be profitable. Such predictions cannot be made now even for fields infested with the most eco- nomically important species in the United States, namely the root-knot nema- todes. The cropping history of the land is presently the important source of information concerning possible infestation with the root-knot nematodes and with certain other species. ECONOMIC EVALUATION Efficient techniques are available for determining the value of nematode con- trol. These evaluations require detailed data on yield, quality, date of maturity, and other factors that might influence the value of the crop. The cost and effectiveness of alternate control methods also must be considered. The im- pact of nematode control measures on other cultural operations, such as rota- tion, must be taken into account. A nematode control measure, at first judged too expensive, may in practice prove economical if multiple benefits result, such as control of weeds and fungi, thereby eliminating weeding costs and in- suring a uniform stand and maturity. Nematode control may also aid in more efficient use of fertilizer and water. Although an important factor in the over- all economics of crop production, the economics of nematode control has yet to receive attention from the agricultural economists.

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PART IV RESEARCH NEEDS

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