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CHAPTER 1 The Science of Nematology Although worldwide recognition of nematodes as important causal agents of plant diseases did not occur until the middle of this century, nematodes were studied in both the British Isles and Europe more than 100 years earlier. Four milestones mark these studies: in 1743, the first observation of a plant- parasitic nematode-the wheat gall nematode (Anguina tritici); in the 1850's, the discovery that a root-knot nematode (Meloidogyne sp.) caused galls on cucumber roots; recognition that the sugar-beet nematode (Heterodera schachtii) damaged sugar beets; and, shortly thereafter, the publication of the first comprehensive paper on free-living nematodes. A great deal of credit for the early progress of general nematology belongs to workers in Europe and the British Isles. In the United States, limited attention was given to the study of nematodes during the early 1900's. Several significant discoveries during 1945-1955 ac- celerated the development of plant nematology as a separate discipline. These were the introduction of practical nematocides; the discovery of the golden nematode (Heterodera rostochiensis) in a major potato-producing region of the United States; the demonstration that the burrowing nematode (Radoph- olus similis) was the cause of spreading-decline disease of citrus in Florida; recognition of the serious damage caused by nematodes feeding at root sur- faces; recognition of the many interactions between nematodes and other soil-inhabiting organisms in plant-disease complexes, including breakdown of disease resistance; and the discovery of the transmission of viruses by certain nematodes. Because of these and other developments, research in nematology received increased attention and financial support.
4 INTRODUCTION In the United States, early research in nematology was conducted by a few scientists, some trained in Europe, working in the U.S. Department of Agri- culture and various experiment stations of the agricultural colleges. Many of the important contributions in nematology prior to 1950 were made by U.S.D.A. nematologists. Some experiment-station plant pathologists and entomologists trained themselves, almost unaided, to identify plant-pathogenic nematodes and to conduct research on the biology and control of important species. When the importance of nematodes to crop production was recognized and funds for both research and personnel were available, the research was handicapped by the scarcity of trained nematologists. To meet this need, teaching programs in nematology were developed or expanded, primarily within departments of plant pathology or entomology. Universities then em- ployed nematologists to teach and to work cooperatively with plant patholo- gists and other biologists in solving many nematological problems. In 1940, the number of scientists engaged in plant nematology in the United States was less than 25; today it is more than 300. Because of the introduction of undergraduate and graduate courses for the training of nematologists at several universities, the availability of textbooks emphasizing plant and soil nematodes, new research equipment and techniques, and regional cooperative research throughout the United States, progress in nematology should continue. The establishment of regional centers where nematologists could study all aspects of a particular phase of nematology would further accelerate progress. The training of nematologists varies widely. In England and Europe, most undergraduate and graduate students receive instruction in broad fields such as mathematics, physics, chemistry, and biology rather than in nematology. At the postgraduate level, only a few formal courses in nematology are offered; most postgraduate students receive training on an informal basis, working with a nematologist at a laboratory. Professional societies serve to bring scientists together for discussion and exchange of ideas. The founding of the Society of European Nematologists in 1953 and its subsequent growth resulted from the nematologist's need for contact and collaboration with others in the same field. To satisfy this need, the Society conducts a symposium every two years and issues a newsletter twice a year. Nematologica, an international journal of nematological research, includes research papers on nematodes of agricultural importance, articles on free- living nematodes, and general papers on morphology, taxonomy, ecology, and physiology. In all countries, and particularly in the United States, the role of the societies is important to nematologists, because of the fragmentation of the subject matter among other disciplines. In 1910, five scientists founded the
THE SCIENCE OF NEMATOLOGY 5 Helminthological Society of Washington. The Society publishes its Proceed- ings, in which many important research papers in all areas of nematology ap- pear. By tradition, the study of nematodes parasitic to man and animals is called "helminthology," and the study of plant-parasitic and free-living nema- todes is called "nematology." Papers, symposia, and informal discussions on nematode diseases of plants have been presented for many years at annual meetings of the American Phytopathological Society. Numerous papers on this subject are published in Phytopathology, the official journal of this society, first issued in 1910. In 1962, the Society of Nematologists was formed as an outgrowth of the American Phytopathological Society. Membership is open to anyone inter- ested in any phase of nematology. The Society publishes a newsletter, will publish the first volume of the Journal of Nematology in 1969, and holds annual meetings at which papers representing many aspects of nematology are presented. Although important contributions in nematology are coming from labora- tories in numerous countries, greatly expanded research programs on all kinds of nematodes are urgently needed. Rapid development of this science, based on worldwide cooperation, would bring immeasurable benefits to all peoples of the world.
CHAPTER 2 Nematodes and Their Importance to Man Nematodes are probably the most numerous multicellular animals in the world. They escape notice because most kinds are so minute that they cannot be seen without the aid of a microscope. However, not all nematode species are small. One, parasitic in whales, is comparable in length to a 25-foot section of garden hose. Nematodes abound everywhere and are found in nearly every biological niche that will support life-including deserts, the ocean bottom, Antarctic ice, and hot springs. Some of the soil-inhabiting nematode species feed on microorganisms such as bacteria, fungi, algae, and other nematodes. Many soil-dwelling species feed only on higher plants. Both insects and higher animals have nematode parasites. Many of the animal parasites are several centimeters long and are easily detected. Some of them cause man great phys- ical discomfort and debilitation. For these reasons, the animal parasites were the first nematodes to be recorded and studied. Domesticated animals suffer similar parasitism and debilitation, with resultant indirect losses to man. PLANT-PARASITIC NEMATODES IMPORTANT TO MAN In addition to the nematode parasites of man and higher animals, there are many species that parasitize our food and fiber crops, thus reducing supplies of both throughout the world. The earliest records of plant-parasitic nema- todes were published in the mid-1700's. At that time, nematodes were scien- tific curiosities that were used to explore the capabilities of the microscope, which Leeuwenhoek had recently developed. During the next century, a great deal of effort was directed toward the application of science to agriculture,
NEMATODES AND THEIR IMPORTANCE TO MAN 7 especially in Europe. One of the results of this effort was the discovery that certain plant-parasitic nematodes, such as the wheat nematode (Anguina tritici) and the sugar-beet nematode (Heterodera schachtii), often were the principal limiting factors of the growth of crop plants. Until the 1940's, knowledge of other nematode species important to agri- culture accumulated slowly. The chemical industry then introduced the soil fumigants 1,3-D (principal active ingredient 1,3-dichloropropene) and EDB (ethylene dibromide), which reduced nematode populations in soils at much less expense than was previously required. Improvement of plant growth and yield following the use of nematocidal soil fumigants led to rapid grower ac- ceptance of the importance of nematodes to agriculture. Only a decade after the introduction of these soil fumigants, 5 percent of all pesticide expendi- tures were for such materials. Improved plant growth following soil fumigation does not prove nematode pathogenicity, but these chemicals are far more ef- fective as nematocides than as bactericides or fungicides. Plant-growth re- sponses following the use of nematocides indict nematodes by associating them with poor growth. Further means for testing nematode pathogenicity are discussed in Chapter 5. Virtually every crop has its complement of nematode parasites. More than 150 nematode species are being studied to determine their role in plant dis- ease, and many new nematode parasites are discovered every year. In experi- mental studies, it has been found that plant weight is usually inversely pro- portional to the number of pathogenic nematodes added to the soil around the roots of plants. This relationship varies with the particular crop and nematode and is influenced by environmental factors such as fertility, moisture, temper- ature and soil type. Given an adequate food supply and proper environment, nematodes, like other organisms, increase logarithmically. Perennial crops provide a constant food supply and hence are especially vulnerable to nema- tode damage. Similarly, annual crops grown as a monoculture intensify nema- tode problems. As pathogens, nematodes affect crop yield and quality or both. They limit the utilization of nutrients by plants, thus causing waste of fertilizers. They predispose perennial plants to winter injury. Nematode- infected plants wilt more readily than noninfected ones, which necessitates more frequent irrigation. Certain nematode species act as vectors for patho- genic viruses. Others alter the physiology of their host so that it becomes more susceptible to fungal diseases, or they provide avenues of entry for pathogenic bacteria. Unrecognized nematode infestations confound and often totally negate experiments designed to study other factors that limit plant growth. Quarantine actions by federal, state, and local agencies against such well- known nematode pathogens as the golden nematode of potato (Heterodera rostochiensis) in New York, the burrowing nematode of citrus (Radopholus
8 INTRODUCTION similis) in Florida, and root-knot nematodes (Meloidogyne spp.) and lesion nematodes (Pratylenchus spp.) in California have acquainted many growers, and segments of the general public, with plant-parasitic nematodes and the damage that they cause. PRINCIPAL CHARACTERISTICS OF NEMATODES Nematodes are roundworms that are bilaterally symmetrical, mostly micro- scopic in size, but complex in organization, possessing all the major physio- logical systems of higher animals except respiratory and circulatory systems. Species parasitizing man and higher animals vary in length from 2 to 300 cm. Plant-parasitic species are comparatively small, ranging from 0.5 to 3 mm and 0.01 to 0.5 mm in width. Most nematodes are cylindrical and slender, taper- ing toward the head and the tail (Figure 1), but females of some of the plant- parasitic species assume varying forms, such as pear, lemon, or kidney shapes. Most soil-inhabiting nematodes are semitransparent. With a compound light microscope and an oil-immersion objective, sufficient anatomical detail can be seen to identify nematode specimens to species. Increasing use of electron microscopy promises to add greatly to information about nematodes. The nematode body lacks internal segmentation and is covered with a multilayered cuticle which has various surface markings. Underlying and in- side the cuticle is the hypodermis, which is a thin unicellular layer. The hypo- dermis protrudes into the body cavity ventrally, dorsally, and laterally, pro- ducing longitudinal ridges called chords. Nematodes possess two types of musclesâthe somatic muscles (Figure 1) and specialized muscles. The somatic muscles occur as a layer of longitudinal cells underlying the hypodermis between the chords. Specialized muscles are connected with the stylet, esophagus, intestine, and reproductive organs. The major center of the nervous system, called the nerve ring, surrounds the esophagus in the region of the isthmus, where associated ganglia also are concentrated. Somatic nerves are contained in the hypodermis, and they con- nect with sensory organs in the head region and with the esophagus, intestine, and reproductive systems. The excretory system usually opens to the exterior by a pore that is located ventrally at about the level of the nerve ring. Leading to the pore is a duct that is often lined with cuticle. This duct connects with tubules that extend most of the length of the body and may be free in the body cavity or contained in the lateral chords. The digestive system of nematodes is tubular and is divided into three main regions: esophagus, intestine, and rectum. The anterior oral opening is terminal and is usually surrounded by various types of lip structures and sensory organs (papillae).
NEMATODES AND THEIR IMPORTANCE TO MAN FIGURE 1 A typical plant-parasitic nematode, Rotylenchus breviglans Sher, 1965. (Courtesy of the Department of Nematology, University of California, Riverside.)
10 INTRODUCTION Plant-parasitic forms possess a stylet, which is usually hollow and is used for piercing and feeding on plant cells. Most plant-parasitic nematodes are members of the taxonomic order Tylenchida, a group characterized by a three-part esophagus. In most species of the Tylenchida, the esophageal region behind the stylet (the procorpus) is slender, and the midregion (meta- corpus or median bulbar region) is swollen and equipped with a cuticularized valvular apparatus, which appears to function as a pump. Behind the meta- corpus, the esophagus narrows to a slender isthmus and ends in a glandular region. There are usually three esophageal glands, one dorsal and two sub- ventral, although there may be as many as six in some nematodes, such as the genus Hoplolaimus. In two groups of the order Tylenchida (superfamilies Tylenchoidea and Criconematoidea), the two subventral glands open into the lumen of the esophagus near the valve in the median bulb, and the dorsal gland opens into the lumen farther forward, just posterior to the stylet. In the third superfamily (Aphelenchoidea), all three esophageal glands open into the lumen near the esophageal valve. Some plant-parasitic nematodes, and all that are known to transmit viruses, belong in another order, the Dorylaimida. Nematodes in this order have a two- part esophagus consisting of a slender anterior region that leads to a shorter, swollen glandular region. Some of the nematodes in this group, such as dagger nematodes (Xiphinema spp.) and needle nematodes (Longidorus spp.), have hollow stylets, but others (stubby-root nematodes, Trichodorus spp.) have a toothlike stylet (onchiostyle). The intestinal wall is composed of a single layer of cells, which are de- terminate in number. The intestine ends in a constricted region that leads to the prerectum, then the rectum, and finally opens to the outside by a ventral, subterminal, or terminal anus in the female or by a cloacal opening in the male. Male and female nematodes are usually similar in appearance except for the reproductive systems. However, pronounced dimorphism occurs in some species: females become swollen, and males remain slender and cylindrical. Reproduction without males is common, and in some species females pro- duce both spermatozoa and eggs. Usually, the females have one or two tubu- lar ovaries, a spermatheca, oviduct, and uterus. Eggs are deposited through a slitlike opening called the vulva. The vulva is usually ventral and subterminal to midway in the body, but it may be terminal. Males usually have one testis, rarely two; two cuticularized spicules; and a gubernaculum or guiding apparatus. They may have caudal alae, which are lateral extensions of the cuticle in the region of the spicules and are thought to be clasping organs used in copulation. The male intestine joins the reproductive system pos- teriad, forming a true cloaca.
NEMATODES AND THEIR IMPORTANCE TO MAN 11 LIFE CYCLE There is no true metamorphosis in nematodes. The young are smaller, but in other respects they generally resemble adults, and they could correctly be called juveniles. However, the term "larva" is firmly entrenched by usage in nematological literature. There are five stages in the life cycle. Inside the egg the developing embryo grows, elongates, and differentiates to become the first-stage larva. In most nematode species, the first-stage larva continues to develop and molts to the second stage while still within the eggshell. The second-stage larva usually emerges from the egg. The nematode then feeds, develops, and molts twice more while passing through the third and fourth larval stages to become a fully developed adult. There are exceptions to this cycle. The larvae of certain animal parasites develop to the third stage before emerging from the egg. Larvae of Xiphinema index and certain Rhabditis spp. are reported to emerge from the egg before the first molt. At the end of each larval stage, the cuticle is shed, including its extensions into the oral opening, excretory pore, vulva, and the rectum or the cloaca. Based on their life habits, the plant-parasitic species can be classified in two groups. The soil inhabitants normally complete the entire life cycle in the soil, in or about the roots of plants. The aboveground parasites may begin their cycle on the soil or in the shallow surface layers, often in host-plant residues; but when suitable host plants develop and favorable conditions pre- vail, the aboveground parasites ascend the plant or attack the growing seed- lings and mature aboveground. Trunks, stems, petioles, leaves, flowers, and seeds are known to be attacked. SOIL INHABITANTS Ectoparasitic Species Some nematode species spend their entire life cycle free in the soil, feeding externally on the roots of host plants. They usually stop feeding and detach themselves when the roots are disturbed. Eggs are deposited in the soil. Ex- amples of this kind of parasite are species of ring nematodes (Criconemoides spp.), pin nematodes (Paratylenchus spp.), and stubby-root nematodes. Other species, such as a sheath nematode (Hemicycliophora arenaria) and the walnut nematode (Cacopaurus pestis), are similar to the above nematodes but differ in that attachment of the adult female to the host root is more permanent. These have long stylets that penetrate deep into the root. In most cases, these nematodes are essentially sedentary after attachment to the root.
12 INTRODUCTION Endoparasitic Species Some endoparasites, such as the lesion nematodes, are migratory in the corti- cal parenchyma of host roots. They move through the root tissues, feeding on cells, multiplying, and often causing necrosis of root tissues. Overwintering occurs in the roots, or in soil about the roots, without any known special mechanism for protection from adverse conditions. Other endoparasitic types penetrate rootlets as second-stage larvae, become sedentary before molting, and remain through the remainder of the life cycle. Eggs are deposited in a matrix, as in the case of root-knot nematodes, or may be retained inside the body of the female, as in the cyst nematodes (Heterod- era spp.). The cuticle of the cyst nematodes undergoes chemical changes and becomes a durable, brown, so-called cyst that protects the eggs from adverse conditions. Most larvae remain inside eggshells within the cyst until favorable conditions occur, finally emerging to wander free in the soil and to find new infection sites. Intermediate forms are found in Tylenchulus andRotylenchulus, in which younger stages feed ectoparasitically and later stages penetrate host tissues. The posterior end of the body remains outside the root and becomes swollen and reniform in shape. Eggs are deposited in a gelatinous matrix. Second-stage larvae hatch from the eggs, and the cycles are continuous. ABOVEGROUND PARASITES Bud and Leaf Nematodes (Aphelenchoides spp.) The bud and leaf nematode (Aphelenchoides ritzemabosi), parasitizing chrysanthemum, is an example of a nematode that is endoparasitic in leaves. Individuals enter leaves through stomata and live in intercellular spaces. De- velopment is continuous, and all stages occur together. Nematodes also live in dormant buds or in growing points in crowns of plants, and they may be found in all stages of development in dead leaves on or in the ground. They may survive, quiescent, in dried leaves for at least two years and then revive when the leaves are moistened. The spring crimp nematode of strawberry (A. fragariae) typifies ectopara- sitism in buds. The nematodes survive adverse conditions in the soil or deep within developing buds. When a film of moisture is present on the plant, de- velopment is continuous, and the nematodes remain outside the plant tissues feeding ectoparasitically on epidermal tissues near the growing points of buds.
NEMATODES AND THEIR IMPORTANCE TO MAN 13 Seedgall Nematodes (Anguina spp.) The wheat nematode (A. tritict) will serve as an example. Quiescent second- stage larvae survive within seedgalls that drop to the ground at harvest or that are harvested with the healthy grain. Up to 70,000 larvae per gall have been reported. When galls are moistened, the larvae emerge and migrate to the growing points of developing grain seedlings. Here they feed ectoparasitically, protected within the leaf sheaths. When seed primordia begin to form, the larvae enter the embryo and become endoparasitic. Within the primordial tissues, the larvae grow rapidly and molt several times to become adults. After mating, the females deposit eggs inside the transformed seed tissues. These eggs develop and hatch so that second-stage larvae remain free inside the gall. There is only one cycle per year. Stem Nematode (Ditylenchus dipsaci) This species has a life cycle similar to that of the chrysanthemum foliar nema- tode, except that it invades stems as well as leaves. Development is continuous, and several life cycles are completed in one season, but the principal stage that overwinters or survives unfavorable environmental conditions is the fourth-stage or preadult larva. This stage is exceptionally resistant to drying and to chemical toxicants. SIGNIFICANCE OF LIFE HABITS Life histories of nematodes should be understood when control measures are considered. The wheat nematode may be effectively controlled by crop rota- tion with nonhost plants, because the emergence of larvae from the galls is virtually complete when soil moisture and temperature become favorable. Larvae die when they are outside the gall in the absence of the host. Control of certain cyst nematodes by crop rotation, however, is much more difficult. These nematodes remain encysted in the absence of a host. They can survive for long periods in this state. The protection afforded endoparasitic nema- todes by roots often makes them more difficult to control than ectoparasites. GEOGRAPHIC DISTRIBUTION Plant diseases caused by nematodes have been found in every country and region where nematological investigations have been conducted. It is difficult
14 INTRODUCTION to find data from which the origin of the various economic nematode pests can be deduced. Many species occur wherever their host crops are grown and appear to have been spread as the culture of the crop spread. The sugar-beet nematode is one of many species that appears to have been spread in this manner. A few nematodes appear to be native parasites of wild plants but have become adapted to cultivated crops when these were grown in the area; the false root-knot nematode (Nacobbus batatiformis) in Nebraska and ad- joining states is probably such a nematode. Water and, in some cases, wind are responsible for local spread of nematodes, but long-range distribution is largely by man's movement of plants and soil. Are nematode diseases increasing, decreasing, or being contained? Current discoveries often reflect the initiation or extension of surveys and investiga- tions rather than new introductions. There is usually a lag of several years be- tween the time of infestation and the time when the nematode population reaches a detectable level. For these reasons, the question is difficult to an- swer with precise data. We believe nematode diseases are increasing because of spread by man as well as man's tendency to monoculture plants. In recent years, the spread of nematode diseases has been accompanied by development of a variety of methods of prevention of nematode disease. In general, these methods are being used only in countries with an advanced agricultural tech- nology. Countries with greatest food needs are doing the least and are the most poorly equipped to control nematodes. In the future, the extension of nematode-control methods to new areas and the development of improved methods will be important means for increasing the world food supply. BIBLIOGRAPHY Chitwood, B. G., and M. W. Allen. 1959. Ward and Whipple's freshwater biology, pp. 368-401. 2nd ed. John Wiley & Sons, Inc., New York. 1248 pp. Cobb, N. A. 1914. Nematodes and their relationships. U.S. Department of Agriculture Yearbook, 1914. pp. 457-490. U.S. Government Printing Office, Washington, D. C. Fischer, C. D. 1956. Pesticides past, present, and prospects. Chemical Week 79(17): 59-90; (18):53-58. Thome, G. 1961. Principles of nematology, McGraw-Hill Book Co., Inc., New York. 553pp.
PART FACTORS INFLUENCING NEMATODE CONTROL