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Plant nematology in developing countries: Problems and progress

F. Lamberti

Methods of control


This short contribution introduces the major nematode pests in developing agricultural systems and discusses possible measures for their control.

Root-knot nematodes (Meloidogyne spp.)

Meloidogyne species constitute the major nematode problem in developing countries. The most common species is M. incognita, which causes considerable losses in many crops. Many vegetable crops, in several botanical families, such as Solanaceae, Cucurbitaceae, Leguminosae, Liliaceae, Chenopodiaceae, Compositae, Umbelliferae, Cruciferae and Malvaceae, suffer the greatest damage. But M. incognita is also highly pathogenic to some staple crops such as cereals, including rice, maize, potato, soybean, banana, plantain, sweet potato and yam; or industrial crops such as tobacco, coffee, sugar cane, sugar beet, cotton and black pepper. Often this species also causes economic damage to fruit crops such as guava, pineapple, papaya and grapes.

Meloidogyne javanica is also widespread and prevalent in warmer climates. It attacks almost all the plants affected by M. incognita except cotton and pepper, although in the case of pepper there are a few reports. Many vegetable crops are severely affected by M. arenaria which, however, causes the most significant losses on groundnuts, especially in West Africa. Meloidogyne hapla has a more restricted distribution, being more common in cool climates or on winter crops in the Mediterranean area. Major economic damage has been reported on carrots, potatoes, alfalfa, clover and strawberries.

A few other species of root-knot nematodes have restricted areas of distribution and affect locally various crops to different extents. Among them is M. artiellia, pathogenic to legumes and cereals in southern Europe and in the Near East. Meloidogyne naasi, which is widespread in northern Europe, has been reported affecting cereals in South America. Meloidogyne exigua and M. decalineata attack coffee in South America and Africa, respectively. Meloidogyne brevicauda is pathogenic to tea planted at high elevations in Sri Lanka. Meloidogyne graminicola affects cereals in India.

Cyst nematodes (Globodera spp., Heterodera spp. and Punctodera spp.)

Less cosmopolitan, but as pathogenic as root-knot nematodes, are species of cyst-forming nematodes. Among them the most widespread are certainly Globodera rostochiensis and G. pallida. They are very common in Central and South America where they are thought to be indigenous, but their occurrence has now been reported also in hilly African and Asian countries. They cause considerable damage in the western countries of North Africa.

Heterodera avenae is a common species in temperate areas of India where it is the causal agent of a disease of wheat called molya. It also attacks barley. Heterodera schachtii attacks sugar beet in North Africa, the Near East and Mexico. Heterodera sacchari is reported to damage sugar cane in Africa and India and rice in Africa. Heterodera oryzae parasitizes rice and banana in Africa. Heterodera cajani is perhaps the most pathogenic species in India on various leguminous crops such as pigeon pea, cowpea and chickpea. Heterodera zeae is very widespread and affects maize, sugar cane and sorghum from North Africa to India.

Of local importance, although destructive, are H. daverti and/or H. trifolii in North Africa. H. ciceri and H. latipons are other important nematode pests in the Near East, and Punctodera chalcoensis in Mexico.

Other important nematode pests

Anguina tritici is a common parasite of wheat on the plateaus of Africa and Asia. In Asia and, to a lesser extent, in Africa, Aphelenchoides besseyi, the causal agent of the white tip disease of rice, is responsible for major losses of this cereal. Aphelenchoides ritzemabosi is widespread in hilly areas of northern India on zinnia and A. agarici seems to be a destructive pest of cultivated mushrooms in India.

The stem nematode, Ditylenchus dipsaci, attacks several crops in the Mediterranean region and causes major losses of onion, garlic, broad bean and strawberry crops. D. dipsaci is also a major pest of garlic in many countries in South America. The phytopathological importance of D. angustus to rice in the Far East is also well known.

Within the genus Helicotylenchus, H. dihystera has worldwide distribution, being a pest of many crops. Its damaging effect, however, has been demonstrated only on olive in Egypt and on rice in Mauritius. Helicotylenchus indicus causes some damage to vegetable crops in India, but only when at high population densities and H. multicinctus occurs wherever bananas are cultivated. Fortunately, this species is a weak parasite affecting only the cortical tissues and causing economic damage only at high population densities. Mesocriconema onoense, M. curvatum and Hemicycliophora typica are parasites of rice in Africa.

Various species of Pratylenchus parasitize crops in developing countries. Pratylenchus brachyurus attacks many plants in Africa and in the Mediterranean region. Under tropical climatic conditions P. coffeae is an important pest of coffee, banana, cowpea and citrus. Pratylenchus penetrans is frequently associated with declining date-palms in Saharan oases. Pratylenchus thornei and P. mediterraneus are parasites of legumes and cereals in North Africa and the Near East and. P. loosi is a major pest of tea in Sri Lanka and India. Finally, P. zeae attacks maize and sugar cane in Africa and Asia.

Radopholus similis is a destructive parasite of banana throughout the tropics. It also causes great damage to black pepper in Java, to coconut palms in India and to tea in Sri Lanka.

Species of Hirschmanniella such as H. oryzae, H. gracilis, H. spinicauda and H. mexicana cause varying extents of damage to rice in Africa, Asia and Mexico.

Hoplolaimus seinhorsti has been shown to be pathogenic to black pepper and various vegetable crops in Sri Lanka, and H. indicus and H. pararobustus are often found associated with a decline of sugar cane and other plants in Africa and Asia. Yams in Africa are severely affected by Scutellonema bradys, and it is also an important postharvest pest attacking yams in storehouses.

Hemicriconemoides mangiferae may be the most widely associated nematode species with mango. It occurs mainly in Asia and Africa where it is found also in the rhizosphere of other fruit-trees. Among Tylenchorhynchus species, T. brassicae is the most frequently occurring in the rhizosphere of crops. It is associated with different plants in Africa and Asia. Other common species are T. claytoni and T. indicus.

Rotylenchulus reniformis is widespread in all the regions with tropical and subtropical agriculture. It causes economic damage to many plants, including vegetable crops, fruit-trees and staple and fibre crops. The citrus nematode, Tylenchulus semipenetrans is invariably associated with citrus groves, which are affected to different extents depending on the paedoclimatic and edaphic situations. Rhadinaphelenchus cocophilus, the causal agent of red ring disease, is very destructive on coconut and oil-palms in Central and South America.

There are species of Longidorus, Paralongidorus and Xiphinema that may cause serious problems, although restricted to local situations. Longidorus africanus is a parasite of cotton in Mexico and the Sudan, but it also occurs in the Near East and East Africa. Longidorus laevicapitatus attacks sugar cane in many African countries, Longidorus cohni is a pest to cereals and alfalfa in the Near East, Paralongidorus buchae attacks many crops in Mauritius, P. oryzae is a parasite of rice in India and P. citri has been consistently found associated with declining groundnut crops in India.

Among the Xiphinema species, the most common in the tropics, from West Africa to India and Sri Lanka, are X. ifacolum, which is highly pathogenic to rice and many vegetable crops, and X. elongatum which is a parasite of olive in Egypt and sugar cane in West Africa and India.

Methods of control

Possible control measures vary with the paedoclimatic conditions, the socio-economic situation, the economics of the crop, the availability of chemicals and/or resistant cultivars, and the feasibility of some agricultural practices.

Crop rotations can always be adopted against species with narrow host ranges. However, plant sequence and time intervals between susceptible crops depend on the nematode species. For ectoparasites, with long life cycles and with a few generations each growing season, one- or two-year intervals might be appropriate. In the case of root-knot nematodes, or at least with species that lay eggs in a gelatinous matrix, at least three years between susceptible crops must elapse. But when cyst nematodes occur, even five years may not be sufficient to obtain economic results. High-value cash crops are often grown intensively by specialist growers and so it may be difficult to find a suitable plant sequence that will not alter the economic and cultural balance of a farm.

Resistant cultivars are without doubt the easiest and most convenient choice for the farmer. However, they are not always available, they may bring on to the market innovations not easily and quickly accepted by consumers, and they can develop resistant pathotypes or races of the parasite if used in monoculture for many years. Nematicidal treatments have been successfully used, but nematicides are usually expensive and may raise problems of environmental pollution and/or of accumulation of toxic residues in edible plant products. Methyl bromide is one of the most effective fumigants to control a broad range of problems (nematodes, fungi, insects, weeds). Being highly toxic to humans and highly volatile, it must be applied by skilled personnel and under a plastic tarp. Removal of tarping should be done two days after treatment and planting not earlier than one week after application. The high cost of the operation, lack of licensed operators and unavailability of the product, which requires proper storage facilities, are limiting factors for the use of this chemical.

A cheaper fumigant with predominant nematicidal effect is 1,3 dichloropropene (1,3-D). Its volatility is much lower compared with methyl bromide, therefore it does not require tarping. However, to be effective it needs to be injected into the soil by efficient machines which are not always available in developing countries and require accurate maintenance practices. The easiest and most effective way of applying 1,3-D is by injector gun, but this requires much labour. An interval of at least three weeks is necessary between application of this chemical and planting to avoid phytotoxicity.

When fumigants are applied, the soil must be carefully prepared by breaking plough pans and large soil aggregates and removing residues of the previous crop. Soil humidity and temperature must also be optimal to achieve satisfactory results.

Granular nematicides are more easily applied and safer for farmers compared with fumigants. However, they need high soil humidity to be effective. Those with systemic action are usually very effective and persistent.

Aldicarb, a carbamate, exerts its nematicidal activity for over six months, but it may cause problems of residues in edible plants. Therefore its use is allowed mainly on ornamental and industrial crops. Fenamiphos persists in the soil for about two months and if applied at rates of 15 to 20 kg a.i./ha gives good control even of root-knot and cyst nematodes without inducing accumulation of toxic residues in plants. It should be applied preferably two to three weeks before planting. Oxamyl is also a systemic nematicide but has shorter persistence (two weeks) and is less effective in tropical climates than carbofuran. Prophos performs its activity only by contact. Therefore it is effective against ectoparasitic nematodes and can control endoparasites only before they penetrate the roots. The limiting factor of all these chemicals is their high cost which makes them affordable only for cash crops. Even then, they are often not available on the market because hard currency is needed to import them, which is usually scarce in developing countries.

Two other pesticides that have mainly fungicidal activity have been used to control nematodes. To be effective dazomet needs moist soil and an interval of about six weeks between treatment and planting because of its high phytotoxicity. Metam-sodium has the same mode of action as dazomet, but has the advantage of being applicable through the irrigation system a few weeks before planting, and the disadvantage of having only modest nematicidal activity. Therefore, it needs very high rates of application to control root-knot or cyst nematodes, which are in most circumstances the only plant nematodes whose control gives economic benefit.

The hypothesis has been advanced that continuous application of nematicides might develop resistance to them in some nematodes. Up to now there is no evidence of resistance of nematodes to chemicals, and the cases in which low mortality of nematodes has been observed following nematicidal treatments have been interpreted as an enhanced degradation of the chemical itself resulting from the increased activity of micro-organisms.

Attempts have been made to control plant-parasitic nematodes by soil amendments of by-products of some agricultural industries, such as neem, mustard, castor bean, groundnut or coconut oilcakes. In fact they reduce numbers of nematodes and female fecundity, but they are effective only when modest populations occur.

Plant extracts such as those from Tagetes, Ruta, Cineraria or Pelargonium have also been effective in killing plant-parasitic nematodes, but results refer mainly to in vitro or pot experiments and practical application of these extracts has yet to be profitable.

Soil steaming is often suggested as an environmentally clean measure to control plant pathogens. However, this time-consuming method can be applied only on small areas and, for the amount of energy (oil or electric power) required and the sophisticated equipment needed, is one of the most expensive nematode control practices. It is worth while only in greenhouses for production of out-of-season luxury foods. Besides, it does not always give uniform results and, if excessive temperatures are produced, reduces soil fertility and deteriorates soil structure.

Soil solarization is a recently developed technique in warm areas. It is a hydrothermal process that occurs in moist soil covered with transparent plastic film in summer months. During solarization, soil temperatures reach values (42° to 50°C) that are lethal to plant-parasitic nematodes, or increase to 36° to 40°C which, if prolonged, may be lethal or may affect life cycles and host-parasite relationships of many plant-parasitic nematodes by depleting their energy reserves. This makes them more vulnerable to biotic (antagonistic organisms) and abiotic stresses. However, temperatures of solarized soil are seldom lethal or sublethal at levels deeper than 30 cm. Therefore it is most practical with annual crops with shallow root systems. Its effect can be further improved if used in combination with reduced rates of fumigants or non-volatile nematicides.

Biological control may be feasible if antagonistic organisms are cheap to mass produce and apply. Easy colonization of soil, high virulence, long persistence, good shelf-life, low sensitivity towards agrochemicals, safety for operators and the environment and effective nematode control at acceptable costs for farmers are important factors. Unfortunately the fact that none of the organisms so far used for biological control of nematodes possesses all these characteristics and the lack of technology for producing commercial preparations of such biocontrol agents are the main limitations to this practice.

In conclusion, different methods of nematode control could be combined in an integrated system, shifting from the concept of control to the concept of management which is a procedure directed at reducing and maintaining the numbers of plant-parasitic nematodes at non-injurious levels. This is particularly important in developing countries, where the lack of a commercial system and of a market for wealthy customers often means that high production costs are not justified. However, demographic increases require improvements in production from sustainable agriculture.

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