Nematocides and Nematicides - History
by
 A. L. Taylor

This document was constructed and is maintained by KHUONG B. NGUYEN

        Introduction
        The history of nematicides* can be divided into three parts, ancient, medieval and modern.  Ancient history of nematicides is closely associated with the early history of soil insecticides, and probably had its beginning about 1854, when Garreau recognized the insecticidal value of carbon bisulphide (also spelled disulphide and bi- or disulfide).

        According to Fleming and Baker (1935) the use of carbon bisulphide for soil fumigation was first suggested by Thenard in 1869.** At that time, damage to French Vineyards by an aphid known as the grape phylloxera (Phylloxera vitifoliae) was reaching alarming proportions.  Indeed, the root-infesting form of this insect, introduced from America about 1860, destroyed about 1,000,000 hectares of French vineyards by 1885 (Metcalf and Flint, 1962, p. 779).  Research was started on the use of carbon bisulphide about 1870.  According to Newhall (1955), by 1877 Dr. Crola had formulated excellent rules for its use in soil fumigation, and application methods and apparatus were well developed.

        The most popular and successful application method was injection of carbon bisulphide into holes 50 centimeters apart.  From these application points, fumes diffused through the soil.  Later, application by spraying the undiluted liquid into the soil while plowing was tried but found to be often ineffective.  Carbon bisulphide is slightly soluble in water.  At 20C, one liter of water can absorb 1.79 grams of carbon bisulphide.  This makes application in irrigation water possible and this method seems to have been with some success (Newhall, 1955).

        With the introduction about 1900 of phylloxera-resistant rootstocks from grapes native to the eastern United States, the use of carbon bisulphide in vineyards was abandoned as no longer needed.  But in the meantime, the idea that soil pests could be controlled by injection of volatile chemicals in the soil had been well established, and as detailed by Fleming and Baker (1935), a great deal of research had been done on control of other soil insects.  This work has continued, and CS2 is still available for use in control of soil insects.

        Ancient history
        The sugarbeet nematode, Heteroderaschachtii, was first reported as the cause of a serious disease of sugarbeets by Schacht (1859).  Kuhn reported experiments with carbon bisulphide for its control in 1871.*** The experiments were evidently not very successful, but sufficiently encouraging to prompt further work by Bessey against root-knot nematodes in the United States during the first two decades of century.  These experiments were reported in various U.S. Department of Agriculture publications, but there are few reports of commercial use of carbon bisulphide for nematode control.

Medieval history
        World War I started in 1914 and ended in 1918.  We might date the end of the era of ancient history of nematicides as falling somewhere during this period.  One of the developments of the war was the use of poisonous gases as weapons to disable enemy soldiers without necessarily killing them.  The first to be used was chlorine.  Another was chloropicrin (CC13NO2).  Chloropicrin fumes in the air in low concentration cause irriation of the eyes, with profuse flow of tears, so it was called "tear gas"  Higher concentrations cause lung irritation, nausea and vomiting.  Exposure is seldom fatal because the victim leaves the contaminated area as rapidly as possible, or is forced to use a gas mask.  At the end of the war on November 11, 1918, large stocks of chloropicrin were on hand as military surplus.  Chloropicrin was tested among other chemicals in England by Mathews (1920) for control of fungi, nematodes and wireworms, and for its beneficial effect on soil bacteria.  Chloropicrin was outstanding in several respects.  Yield of tomatoes in pots was increased from 857 grams to 1,480 grams; it was classed among the "most effective" chemicals for control of nematodes and wireworms, and most "beneficial to bacterial activity"  It also "had a remarkable effect on root action, producing the great mass of fibrous roots which has hitherto only been obtainable in a steamed soil.  Many attempts have previously been made to reproduce this effect of steaming, but until this season without success".  The medieval era of nematicides starts with this paper.

        In 1927 and 1928, Johnson and Godfrey (1932) started field work with chloropicrin in pineapple fields in Hawaii.  The concluded that:

        1. Plots treated with chloropicrin consistently had the highest percentages of plants free of nematode root knot.

        2. There was good negative correlation between infection by root-knot nematodes and amounts of chloropicrin applied.

        3. Weight of pineapples produced on treated plots was as much as 57.0% more than weight from control plots.

        4. The value of the additional pineapples from treated plots was considerably more than the cost of the chloropicrin and its application.

         Further field experiments with chloropicrin reported by Godfrey in 1935 confirmed these results, with pineapple yield increases in plots treated with chloropicrin 31.4% and 51.2% more than the controls.  Carbon bisulphide was also included in this experiment, with yield increase of 31.3% for the best treatment.  The current market value of the increased yield of pineapples from plots treated with chloropicrin was $208.70 per acre ($515.49 per hectare).  Subtracting the cost of the chloropicrin treatment, $125.00 per acre or $308.75 per hectare, the profit was $83.70 per acre or $206.74 per hectare.  This was only actual weight increase of the plant crop (first crop after planting) without regard to the higher grade of the fruit because of increased average weight, or the prospects for and increased ratoon crop (second crop after planting) because of the superior condition of the plants.

        Shortly thereafter, applications of chloropicrin before planting pineapples became a widely used practice in Hawaii and continued as long as World War I surplus chloropicrin remained available (Thorne, 1961, pp. 28-29).

        In 1935, I was appointed Junior Nematologist by the Bureau of Plant Industry, U.S. Department of Agriculture and assigned to the Coastal Plain Experiment Station at Tifton, Georgia.  My principle assignment was investigation of the possibilities of soil nematicides.  Being entirely unaware of the details of the French work with carbon bisulphide in the late 1800's, I spent some time in reinventing the hand applicatior (Taylor, 1939), appartus for delivering a continuous stream of nematicide into a furrow, and a plow applicator.  I also confirmed the work of Dr. Godfrey and his colleagues, reporting good results with 200 and 400 pounds of chloropicrin per acre (224 to 448 kilograms per hectare).  Equally good results were obtained with 500 to 1000 lbs. of carbon bisulphide per acre (560 to 1120 kg/ha) applied by injection into the sandy loam soil at Tifton.  When carbon bisulphide was applied as a water emulsion in furrows, about five times as much was required (Taylor, 1943, 1949).

        Between 1937 and 1941, the Innis Speiden Company of Niagara Falls, New York, (later renamed Larvacide Products Co.) was actively promoting the use of chloropicrin as a soil nematicide and insecticide in addition to its use as a fumigant for grain in storage.  Their principal nematicide customers were owners of greenhouses, nurseries and seedbeds for large-scale vegetable production.  So far as I am aware, this was the first commercial promotion of nematicides.

         In 1940, Christie and Cobb reported an experiment with the insecticide methyl bromide for control of chrysanthemum foliar nematode on planting material.  Methyl bromide is a liquid if kept in closed containers, but becomes a gas at about 4C at atmospheric pressure.  They concluded that control was impractical because of phytotoxicity, and because only recently hatched larvae were killed.  Hawkins (1939) used methyl bromide for control of white-fringed beetle (Graphognathus leucoloma) in potting soil.  This suggested trails as a soil nematicide by Taylor and McBeth (1940).  After partially successful preliminary experiments, satisfactory results were obtained in field plots by releasing methyl bromide as a gas in tile lines buried under soil covered with a gas impervious glue-coated paper.  These authors (1941a) had better results by simply covering the soil with a gas imperious paper supported about 8 centimeters above the soil surface, and releasing the methyl bromide between the cover and the soil surface.  This method is still widely used, but plastic covers have long since replaced paper.  In the course of this work, apparent control of soil fungi and bacteria were noted.

Taylor and McBeth (1941b) reported an experiment with "spot" treatment of soil as a means of saving nematicide and the labor of applying it in fields where crops planted in widely spaced hills are to be grown.  They referred to previous experiments which indicated that root-knot nematode larvae move through the soil at an average rate of less than one centimeter per day in the sandy loam soil of southern Georgia.  If planted in a nematode-free area of soil, a plant would not be heavily attacked in its early stages of growth when comparatively few nematodes can damage it severely.  The method was successful for watermelon production.  Later, the logical extension of the method to "row" treatment was made (Taylor, 1949).  Row treatments can be made with power applicators and have probably been used more than any other method.

Modern history
        The end of the medieval era of nematicide history and the beginning of the modern era was marked by the publication in 1943 of a paper by Dr. Walter Carter, of the Pineapple Research Institute, Honolulu, Hawaii.  This was a report of field experiments with a mixture of 1,3-dichloropropene and 1,2-dichloropropane.  The material, called "D-D mixture" by Carter, was reported to be less expensive and easier to handle than chloropicrin, while producing comparable results so far as control of nematodes and insects, and favorable growth response were concerned.  A second more detailed paper by Carter (1945) supported these conclusions with excellent data.

        In 1944, ethylene dibeonide (EDB) was being tested as a soil nematicide by the Dow Chemical Company at Seal Beach, California (according to Thorne and Jensen, 1947), and apparently at about the same time by Christie (1945) at the USDA Plant Industry Station at Beltsville, Maryland.  Dr. Christie's small-scale test indicated that EDB was as effective as D-D mixture for control of root-knot nematodes.  So far as I am aware, the results of the tests at Seal Beach were never published.  In 1947, Thorne and Jensen published the first paper on field experiments with EDB for control of the sugarbeet nematode, Heteroderaschachtii.

        Starting in 1946, experimental and commercial use of nematicides increased rapidly.  Both the Shell Chemical Corporation and the Dow Chemical Company decided to market nematicides.  A vigorous campaign of advertising, demonstration, and development of methods and application equipment was started.  Screening programs to find other and perhaps better nematicides were started.  DD and EDB were inexpensive enough so that their use was potentially profitable for the farmer on crops of moderate to high value per acre.  Both were already in extensive use by the Hawaiian pineapple industry.

         I, as an employee of the Shell Chemical Corporation from 1946 to 1949, was assigned to market development in the southeastern United States, concentrating on tobacco in the Carolinas, Georgia and Florida.  My experience there was similar to that of numerous colleagues in other parts of the United States and in foreign countries.

        The market for nematicides developed slowly because an enormous amount of education work has necessary.  Many farmers had never heard of nematodes and had certainly never seen any.  Some were familiar with root-knot nematode galls, but did not know what caused them and did not associate their presence with reduced growth and yield.  There was little data to show that nematodes could cause significant reductions of crop yields.  To sell nematicides, farmers must be persuaded to believe that:

        1. There are little worms called nematodes which attack crop plants.  Nematodes, which are too small to recognize without a microscope, exist in enormous numbers in farm fields.

        2. Nematodes damage roots and are a primary cause of reduced plant growth and crop yields.

        3. Nematodes can be controlled by application of nematicides.

        4. Control results in increased crop yields.

        5. With crops of moderate to high value per acre, the selling price of the yield increase is 4 to 5 times the cost of the nematicide and its application.

    6. Nematicides are therefore a good investment.

An educational program was needed because the farmers had been cultivating the same land for many years and were satisfied that they were getting as good yields as possible, certainly average for the neighborhood.  The old way of farming was working very well; why should they change?  We were asking them to invest money in chemicals and equipment to control pests they had never seen in all the years they had been working the soil.  The application methods were unlikely any they had ever used before, and the results were unknown.

         Eventually a marketing technique based on field demonstrations was developed.  With the generous help of Extension Service personnel, arrangements would be made to cooperate with leading farmers in a community.  Equipment and chemical was furnished to fumigate areas in fields where tobacco was to be planted.  The rest was done by the farmers, who planted, fertilized and cultivated the whole field as usual.  Early in the growing season, results began to be visible.  Tobacco plants in the treated area were larger and more uniform than those in the adjacent untreated part of the field.  The improvement continued all through the season.  At any time, it was possible to dig roots for comparison of stunted, knotted or rotted roots from untreated soil with extensive, healthy roots from treated soil.  The growth difference was plainly visible in the field and far more convincing than any amount of talking and advertising.  The next step was to convince the farmer that use of nematicides was profitable, that the selling price of the increased yield was at least 4 or 5 times as much as the expenditure for nematicide and its application.

        Field demonstrations were slow to produce results because only one could be conducted each season.  A series was needed to provide convincing evidence that nematicides would produce dependable results if properly used.  The usual sequence of events in a neighborhood was at least two years of demonstrations followed by two or more years of independent trails by the farmers.  Then the more prosperous and progressive farmers were ready to adoopt nematicides as a regular practice.  In the meantime, neighboring farmers were watching developments over the fence, and were being shown results by the County Agent or other Extension Service personnel.  The time from the first demonstrations in most communities to widespread use of nematicides was about eight years.  Looking back, it is easy to see why so much time was needed.  Everytime was new and unfamiliar, and learning required time and experience.

        About 95% of tobacco growers in North Carolina now start the season by planting seedbeds on soil treated with methyl bromide, then about 85% transplant into fields treated with nematicide, usually by row treatments.  Anslysis of field demonstration experiments (Todd, 1976, 1977) of the North Carolina Extension Service indicates that the best treatments increase yields of a root-knot-susceptible tobacco variety by an average of about 35%, as compared with the untreated control plots.  This is only one example of the way nematicides have increased farming efficiency, not only in the United States, but in much of the rest of the world.  It is also an example of the results of intensive Extension Service effort backed by research.

        All the activity and publicity associated with the development of nematicides had a highly important effect on nematology and on the number of nematologists.  In 1945, there were a few nematologists employed by the U.S. Department of Agriculture at Beltsville and four field stations.  There was one professional nematologist in California, a few at Rothamsted, and a few more elsewhere in the world, probably less than 20 devoting even part time in research in any phase of nematology.

        The next historic event was the discovery of the nematicidal value of DBCP (1,2-dibromo-3-chloropropane).  The first publication in which the chemical formula was given by McBeth and Bergson (1955).  McBeth was in charge of the Shell Chemical Corporation nematicide screening program.  In a previous paper (McBeth, 1954) DBCP was discussed under its experimental number, OS 1897.  DBCP is another fumigant, but unlike DD and EDB, is not highly toxic to many crop plants and can be applied at planting or after planting.  It has been extensively used for control of citrus-root nematodes (Tylenchulussemipenetrans), and for control of other nematodes on living trees and grapevines.

         As experience with nematicides accumulated, it became evident that there were other effects in addition to killing nematodes.  Insects in the soil at the time of application were killed.  There were occasional reports of weed control with DD, but it evidently was not a dependable weed killer.  Methyl bromide applied under a plastic cover killed weed seeds in soil, eliminating expensive hand weeding of vegetable seedbeds.  Control of bacteria and fungi in soil was good with methyl bromide, and occasionally good with DD or EDB.

Vapam*** (sodium N-methyl dithiocarbamate dihydrate), introduced by the Stauffer Chemical Company in 1956, was effective for control of nematodes, weed seeds and soil fungi.  Vapam was not a volatile liquid but decomposed in the soil to form a penetrating gas, and thus acted as a fumigant.

The next nematicide to be placed on the market was a "nonfumigant" called "V-C 13 Nemacide"**** by the Virginia-Carolina Corporation of Richmond, Virginia, in 1957.  Its active ingredient was 0-2, 4-dichlorophenyl 0,0-diethyl phoshorothioate, the first of a series of organophosphate nematicides.  These are commonly called "nonfumigant" nematicides, and sometimes "contact" nematicides.

Since 1960, numerous new nematicides have been tested, and some placed on the market.  The principal difficulty has not been in finding chemicals which control nematodes with ideal conditions, but in finding chemicals which will control nematodes dependably when used by farmers under a wide variety of farm conditions.

The nematicides listed in Table 1 are now available on world markets, and application methods for use in a wide variety of crops, both annual and perennial, have been developed by cooperation between Experiment Stations, Extension Service personnel and industry.  The list is short, but use of one or more of the chemicals named will solve most nematode problems.  The expense of nematicide application has also decreased.  Nematicides are now regularly used by growers of many crops once considered to be outside the profitable range.

The important advances have been in simplification of application methods, and in reduction of application rates.  Granular formulation of non-fumigant nematicides may be distributed over the soil surface, or liquid formulations sprayed on the soil surface.  Both methods are more effective if followed by mixing with the upper layer of the soil, but this is not considered essential by many manufacturers and users.  Several of the non-fumigant nematicides have systematic action.  They are taken up by the plant and nematodes feeding on the plant are controlled.

Oxamyl, introduced by E. I. DuPont de Nemours and Company in 1969, is translocated downward to plant roots after being sprayed on foliage.  In early experiments in California, Radewald et al. (1970) reported that foliar sprays of oxamyl (D-1410) applied at the same time as Meloidogyneincognita or Pratylenchus scribneri inoculum was added to soil "provided a high degree of protection from nematode attack for periods ranging from 21 to 28 days.  Sprays applied one week or more after inoculation retarded nematode development or interfered with reproduction".

        Development of the nematicide market and farmer profit

 As the use of nematicides developed in the modern era, commercial production and sales increased to about $70,000,000 per year in the United States in 1978.  Estimated by the Committee on Crop Losses of the Society of Nematologists to be $60,000,000 in 1970 (Feldmesser et al., 1970).  Nematicide markets in foreign countries have been developed concurrently with the U.S. market.  There has been a corresponding increase in number of nematologists, and a parallel process of farmer education in many other countries.

As a general rule, farmers investing in nematicides confidently expect and usually realize a minimum profit of four times their investment.  For the estimated total value of the nematicide market ($70,000,000 in 1978), the increase in crop values for the United States would be $280,000,000.

For tobacco in North Carolina in 1977, growers spend an estimated $14,737,000 for chemical soil treatment and $3,438,000 for application, a total of $16,175,000.  In that state alone in this one year, nematicides added at least $72,000,000 to the farm value of tobacco (Todd, 1977).

The cost of the research which developed the basic information for the industry and farmers is impossible to calculate accurately, but I doubt that as much as $1,000,000 was expended by federal or state research organizations in the United States during any one of the 35 years of the modern era of nematicide history.  Profits of American farmers every year are at least eight times the total cost of research.

        Indirect results of nematicide research and development

    Some indirect results of nematicide research and development are also significant.

1.  The importance of plant-parasitic nematodes as a major class of agricultural pests has been conclusively proven.

    Before widespread demonstrations of increased yields following applications of nematicides, nematodes had been mostly ignored.  Being practically invisible, their existence in enormous numbers in most all agricultural soils of the world was suspected only by a few pioneer scientists.

     Expect in the sugar beet industry, first in Germany during the ancient era, and in the United States during the medieval era, no organized effort was made to control any plant-parasitic nematode.  Sugar beets were a special case.  Sugar beet processors must have a steady and reliable supply of sugar beets within economic transportation distance of their expensive sugar factories.  Farmers near the factories planted beets year after year on the same land.  The sugarbeet nematode, Heterodera schachtii, multiplied in the fields until yields were reduced below the cost of production for the farmers, and the sugar factory no longer had enough beets for profitable operation.  The remedy was crop rotation systems developed by cooperative efforts of the farmers and the processors, and strictly followed by both to their mutual advantage (Thorne, 1961, pp. 284-286).

    Similar situations have been resolved more quickly and easily by use of nematicides during the modern era.  Numerous others remain and more will develop as farming continues its move toward specialization and industrialization in the more developed countries.  In less developed countries, the first step in reduction of crop losses caused by nematodes is training of native nematologists who can conduct a campaign to educate farmers.  An important part of the campaign is demonstrations of better growth and yield following application of nematicides.  Eventually, this campaign will have a highly significant effect on agricultural production in the countries where it is most needed.

2. Widespread use of nematicides has stimulated research on non-chemical methods of nematode control.

Because it is simple and easy for the farmer, reduction of crop loss due to nematodes by use of nematode-resistant cultivars of crop plants usually attacked is often the best method of control.  If the cultivar is nearly immune, the nematode population of the soil is also reduced (Oostenbrink, 1972).

In the ancient and medieval eras of nematicide history, few resistant cultivars were reported and there was little attempts to develop them by plant breeders.  In the modern era, many have been reported, and there is growing interest by plant breeders in adding nematode resistance to the other desirable qualities of crop plants.  Fassuliotis (1976) lists about 125 vegetable cultivars with resistance to various species of root-knot nematodes.  Numerous cultivars with resistance to various chapters of "Economic Nematology" (J. M. Webster, 1972, editor).  A few rootstocks for fruit and nut crops are also available.  Those resistant to Meloidogyne species are listed by Taylor and Sasser (1978).

Use of resistant cultivars has expanded greatly in the past 20 years.  According to Todd (1977) more than half of the tobacco grown in North Carolina in 1977 was cultivars resistant to Meloidogyne incognita, the most common root-knot nematode in that state.

        The future of nematicides
During the course of an investigation started in 1977, the Environmental Protection Agency of the United States Government cited health hazards and made stringent regulations of procedure used in manufacture, handling and application of DBCP (1,2-dicbromo-3-chloroporpane).  This nematicide which had been on the market for over 20 years is no longer manufactured in the United States.  This event will certainly have a considerable influence on the future history of nematicidies.  Perhaps it is the beginning of a new era.
__________
__________
*    Formerly spelled nematicide and sometimes nemacide.
**  Their reference was not direct, but to Bourcart, 1913 and 1925.
*** This statement is according to Thorne (1961, p. 28), but no reference was
       given unless Kuhn (1881) was intended.  This paper does report experiments
       with carbon bisulphide.
****Registered trade names.

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