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Outlook on plant nematodes and their control in Cyprus

J. Philis


Introduction
Important parasitic nematodes and their control
Nematode control and side-effects
Research and facilities
Advisory work on nematology and training
Conclusions and recommendations
Bibliography


Introduction

Agriculture in Cyprus is still considered to be one of the most important sectors of the economy, mainly because of its contribution to gross domestic product. The production and value of the main crops in 1990 are shown in Table 10. The island, with an area of 9 500 km2, is basically an agricultural country, its agricultural exports being the most important source of national income. The annual mean precipitation is around 470 mm while the yearly average air temperature is approximately 19°C.

Between 1960 and 1989 the Government of Cyprus initiated several projects for water storage in dam reservoirs and increased their capacity from 6 million m3 before 1960 to 300 million m3 at the outset of the republic in 1960 (Ministry of Finance, 1991). It is also worth noting that the population engaged in agriculture is 35 400, or approximately 15 percent of the total economically active population.

Threats to crop production

Agricultural production in Cyprus is very often affected by adverse conditions. Some of these are unavoidable and farmers can do very little to prevent their effects on crop yields. However, there are cases where the farmer, if advised properly, has the ability to use modem techniques and cultural practices to prevent crop failure.

Pests and diseases often threaten agricultural production. The severity of attack depends on the kind of crop grown, but mostly on the crop sequence that is followed by growers. Nematodes are among the parasites that attack numerous economically important plants reducing their yield potential substantially. Many people call this large group of tiny parasitic worms, which destroys the root system of plants by penetrating into the roots, the hidden enemy. In many cases the role of these tiny microorganisms can easily be overlooked unless someone is very familiar with them. It is well known that plant nematodes can thrive in warm climates of tropical and subtropical countries. This does not mean that temperate regions are excluded from nematode damage. A classical example of this is the potato-cyst nematode which seriously attacks potato crops in the northern hemisphere.

TABLE 10
Production and value of production of main crops (1990)

Crop

Production
(million tonnes)

Value of production at producers prices
(US$ million)

Potato

185000

59.6

Citrus

203 000

37.8

Grapes

160000

30.8

Cereals, olives

121 080

41.0

Vegetables

4930

63.4

Fresh fruits

28400

26.4

Other

-

22.4

Total


281.4

Severity of problem

In Cyprus, annual soil temperatures at the depth of the root zone (10 cm) range from 10°C in winter to around 30°C in summer (Fig. 10). This indicates that most nematode genera are active and can develop freely almost throughout the year. Most nematode damage, however, occurs from late spring to mid-autumn (April to November).

Yield losses caused by parasitic nematodes cannot easily be assessed unless a thorough and systematic study is carried out for each crop. However, an attempt was made to assess damage of sampled crops caused by several pathogenic nematodes, as determined by visual observations in the field (Table 11).

The figures in Table 11 are only estimates. It is logical, however, to assume that national crop damage caused by root-knot (Meloidogyne spp.) and citrus nematode (Tylenchulus semipenetrans) is considerable, compared with non-infested fields. These two nematodes are at present considered to be the most destructive. It is anticipated that for citrus and vegetables the national loss in yield caused by the citrus and root-knot nematodes reaches around US$8 million per year, while for potato and bananas, as a result of the effective control measures practised by farmers, the losses are much smaller (US$1 million). Information on yield losses concerning other crops, such as cereals, vetch, broad bean, deciduous trees and vines is not, as yet, available.

Important parasitic nematodes and their control

Citrus nematode (Tylenchulus semipenetrans Cobb)

This nematode, which is spread all over the country, infests all varieties of citrus. The infestation level varies greatly depending mostly on the age of trees. Young trees normally harbour smaller populations than old trees. The most widely used rootstock is bitter orange (Citrus aurantium).

From surveys made around the island, populations can reach up to a maximum of 200 000 larvae/kg soil, while experimental work with Valencia trees has shown that control measures should be taken by growers when populations reach around 20 000 larvae/kg soil (Philis, 1989a). Highly infested trees exhibit symptoms of poor growth, small leaves and reduced fruit size; the most pronounced effect following successful nematode control is the increase in fruit weight rather than the number of fruits. The control of this nematode in an established young orchard of grapefruits almost doubled yields compared with the untreated crop, because the fruit were larger and of better grade during the very early harvest Total yields, at the end of the trial, however, had no significant difference between treatments (J. Philis, unpublished). Increased weight of fruit earns a better price and the number of exportable cases is considerably increased. No chemical residues were found in the fruit at harvest. This has been confirmed in trials on oranges, grapefruits and lemons due to the prolonged time from application (spring) to harvest (winter).

TABLE 11
Estimated yield loss1 caused by nematodes in Cyprus

Crop

Percentage yield loss (sampled fields)

Main pathogenic nematodes involved

Estimated national loss (%)

Artichoke (Cynara scolymus)

30

Meloidogyne spp.

15


Pratylenchus penetrans


Almond (Amygdalus communis)

-

Meloidogyne spp.

-

Apple (Malus communis)

-

Pratylenchus spp.

-

Banana (Musa cavendishii)

30

Meloidogyne spp.



Helicotylenchus multicinctus

151


Pratylenchus spp.


Barley (Hordeum vulgare)

40

Heterodera latipons

-


Pratylenchus thornei


Broad bean (Vicia faba)

25

Ditylenchus dipsaci

20

Citrus (Citrus aurantium)

25

Tylenchulus semipenetrans

151

Carrot (Daucus carota)

35

Heterodera carotae



Paratylenchus neoamblycephalus



Meloidogyne spp.

20

Cowpea (Vigna sinensis)

20

Meloidogyne spp.

20

Carnation (Dianthus cariophyllus)

25

Meloidogyne spp.

15


Pratylenchus spp.


Celery (Apium graveolens)

30

Meloidogyne spp.

20

Cucumber (Cucumis sativus)

30

Meloidogyne spp.

20

Eggplant (Solanum melongena)

35

Meloidogyne spp.

25

Fig (Ficus carica)

-

Meloidogyne spp.

-

Vine (Vitis vinifera)

-

Xiphinema index

-

 

Xiphinema pachtaicum


Meloidogyne spp.


Criconemoides spp.


Haricot bean (Phaseolus vulgaris)

40

Meloidogyne spp.

20


Pratylenchus penetrans


Lettuce (Lactuca sativa)

30

Meloidogyne spp.

20

Okra (Hibiscus esculentum)

35

Meloidogyne spp.

20

Olive (Olea europea)

-

Helicotylenchus spp.

-

Pepper (Capsicum annuum)

20

Meloidogyne incognita

15

Plum (Prunus domestica)

-

Meloidogyne spp.

-


Criconemoides spp.



Pratylenchus spp.


Potato (Solanum tuberosum)

40

Globodera rostochiensis



Globodera pallida



Pratylenchus penetrans



Meloidogyne spp.

10

Peach (Prunus persica)

30

Meloidogyne spp.

-


Mesocriconema xenoplax



Pratylenchus spp.


Sweet melon (Cucumis melo)

25

Meloidogyne spp.

20

Watermelon (Citruus vulgaris)

25

Meloidogyne spp.

15

Squash (Cucurbita pepo)

20

Meloidogyne spp.

10

Strawberry (Fragaria vesca)

20

Meloidogyne spp.

15

Tomato (Lycopersicum esculentum)

40

Meloidogyne spp

20

Tobacco (Nicotiana tabaccum)

30

Meloidogyne spp.

20


Pratylenchus spp.


Vetch (Vicia sativa)

40

Paratylenchus microdorus

-

1 Refers to present losses regardless of control measures taken by the farmers.

Recommended nematicides for controlling the nematode

Granular nematicides. Aldicarb (Temik 15 percent) @ 3 g or oxamyl (Vydate 10 percent) @ 2 g a.i./m2 is applied in soil at both sides of the trees during spring (flush growth) and plants irrigated. Treatments are applied annually or every other year (after harvest).

Liquid nematicides. Oxamyl L.24 (Vydate), fenamiphos 40 (Nemacur), prophos (Mocap 70) and isazofos (Miral 50), respectively, @ 1.2, 4, 2.8 and 3 g a.i./m2 may be applied through the irrigation system (mini-sprinklers) during flush growth and after harvest. It is important to avoid leaching nematicides beyond the root zone.

Potato-cyst nematode (Globodera rostochiensis Woll.)

The potato-cyst nematode, Globodera rostochiensis, first observed on the island in 1975, is present in the Kokkinochoria area (red soils), in the southeastern part of the island. An area of approximately 500 ha is infested with the nematode. Nematode-infested plants are stunted, chlorotic and wilt easily soon after irrigation. Yields are greatly reduced depending on the initial infestation. It is believed that the nematode was introduced into the country with potato seed imported from Europe. Estimates of yield losses have shown that, if no measures against the nematode are taken, the value of crop loss would reach over US$1 million per year. The critical population level of the nematode is around 20 eggs/g soil at planting (Philis, 1991).

The problem of potato-cyst nematodes has become very serious in the last decade because farmers grow potatoes almost continuously throughout the year. In more than 50 percent of nematode-infested fields potatoes are grown twice per year in the same field because of the mild climatic conditions in that particular area; the spring crop is planted in early January and harvested in May and the autumn crop planted in mid-August and harvested in early December. Recently, 10 percent of the infested area has been planted in late October and harvested in February. This growing season enables the crop to escape serious nematode attack mainly because of the low temperature in the soil near the roots that to a great extent inhibits nematode development.

Control of potato-cyst nematode may be achieved with the following treatments:

Use of nematicides. Aldicarb or oxamyl granules @ 3 to 4 kg a.i. per hectare in soil at planting time.

Phenological (control). In infested fields in frost-sensitive areas, plant potatoes during late October and harvest in late January. This enables plants to escape mass larval invasion because of low soil temperatures near the roots. Generally, nematodes fail to multiply.

In frost-free areas, plant during early December and harvest in early March. Nematode control is achieved as above. Both planting seasons secure very good prices.

Use of resistant cultivars. Plant occasionally (one in three years) the nematode resistant (Ro1) cultivars Nicola or Cara. Avoid planting continuously in the same field due to the danger of selecting G. pallida which may become dominant.

Fallow. Although this method, if practised properly, can be effective, it cannot be applied under Cyprus conditions because of the shortage of land.

Guarantee measures. Stop the movement of seed, soil and machinery from infested to clean areas.

Banana nematodes (Helicotylenchus multicinctus and Meloidogyne spp.)

Banana (Musa cavendishii) has an area of approximately 420 ha with an annual value of approximately US$3 million. The crop is grown in the western coastal part of the island where climatic conditions are mild, thus avoiding the danger of frost damage. Both nematodes are serious pests of bananas, infecting the root system.

Symptoms of attack on roots caused by Meloidogyne are the formation of numerous knots, whereas damage caused by the spiral nematode (Helicotylenchus multicinctus) appears first as brown lesions becoming, at a later stage, black in appearance. As a final result of attack by both nematodes, roots rot and the whole root system is unable to absorb sufficient nutrients. Yields are greatly reduced depending on the severity of nematode attack. Control measures against both nematodes are as follows:

Planting of healthy stock (suckers). Nematode-infested suckers should be peeled until all lesions and knots are completely removed from the suckers. Preferably stock from fields where these two nematodes are not present should be used.

Application of nematicides. Apply either fenamiphos or oxamyl @ 4 and 1.5 g a.i./m2 with irrigation water in spring. A further application of oxamyl may be applied during early September, if necessary.

Root-knot nematodes (Meloidogyne javanica and M. incognita)

This group of nematodes is the most destructive on the island. It attacks numerous economically important crops (Table 11) and can also be found on many weeds. Owing to its polyphagous nature and endoparasitic feeding habit, it is very difficult to control especially on established crops.

The warm climate of Cyprus favours the development of root-knot nematodes. Soil temperatures for most of the year are very suitable for nematode activity. In the coastal areas, where vegetables are grown intensively, soil temperatures during winter (December to February) drop to an average minimum of about 12°C (Fig. 10). It may, therefore, be assumed that root-knot nematode activity during this season is extremely poor. However, nematode activity will continue throughout the year in vegetable crops grown under cover.

The nematode occurs throughout the island where intensive agriculture is practised. However, at altitudes higher than 680 m its activity is drastically reduced. On the island there are two species of root-knot nematodes, Meloidogyne javanica and M. incognita race 2. Meloidogyne incognita race 1 is also present but to a much lesser extent (Philis, 1983b). Estimates concerning the damage caused by this group of nematodes on vegetables indicate that the annual loss can reach around US$3 million.

Control measures are as follows:

Chemical control. On tomato, eggplant and cucumber crops use undercover pre-plant treatment with methyl bromide @ 50 to 75 g/m2. Also, Basamid Gr., @ 40 to 50 g/m2, incorporated in the soil prior to planting, may be used. Considerable care should be taken to avoid phytotoxicity caused by fumes remaining in the soil. Aerate the soil completely at intervals of three to five weeks. In open fields, use of Vydate Gr. or Mocap Gr. @ 3 and 6 kg a.i. per hectare, respectively, at planting time for tomato and other non-leafy vegetables.

FIGURE 10: Mean monthly soil temperature at 10 cm depth (Cyprus, 1966-1974)

Resistant cultivars. The tomato varieties Barelli, Carmello (Philis, 1990) and others (Philis, 1977) are highly resistant to Meloidogyne spp. Also, Nemared, a nematode-resistant peach rootstock, is available for use under local conditions for controlling losses caused by root-knot nematodes (Philis, 1989b).

Fallow-rotation. Because of scarcity of suitable (irrigated) land and the prolonged time required for effective nematode control (three to five years) this method is not easily adopted by farmers.

Dagger nematode, Xiphinema Index, on vines

From a systematic survey on the island, in which more than 1 100 soil samples were examined, it was found that the nematode X. index, vector of grapevine fanleaf virus (GFV) is present. Other nematodes found associated with vines but of unknown pathogenic nature were X. pachtaicum and X. turcicum. Xiphinema italiae was found in a very few cases.

The presence of X. index is very important in the grape-producing areas of the island mainly because of the ongoing implementation of the Vine Replanting Scheme. This project, which was initiated a few years ago, aims at partial replacement of the old traditional wine-making varieties (local black and local white), which face serious problems in the export market, with new improved varieties suitable for making good-quality wine.

Work on dagger nematodes on vines in Cyprus can be summarized as follows:

Survey. The survey covered 60 vine-growing villages in which 20 percent of the total number of samples examined contained the nematode X. index. Xiphinema pachtaicum, another species very often associated with vines, was found in more than 90 percent of the samples examined.

From the data obtained it appears that several edapho-environmental parameters have not much influence on the distribution of the nematode (X. index).

Control (fallow). Two field experiments aimed at the control of the nematode by natural means have been established. The results indicate that fallow is the only suitable method for controlling the nematode under local conditions and can significantly reduce nematode populations in the soil after uprooting the old vineyard. Almost zero nematode populations in the soil have been reached after three years (mountainous areas) and four years (coastal areas) from the time of uprooting. Introducing barley in the fallow system had no significant effect on the nematode.

Other important nematodes

Ditylenchus dipsaci attacks broad bean (Vicia faba). Infestation is more severe in the western part of the island where favourable climatic conditions (especially moisture) favour rapid nematode development and reproduction. No systematic work has been done on either the biology or control of this nematode.

Heterodera latipons. The so-called Mediterranean cereal-cyst nematode, Heterodera latipons is probably being overlooked. Serious infestation exists in areas where barley (Hordeum vulgare) is grown almost every year as a monoculture. No work has been done to estimate damage caused by this nematode. However, examination of several nematode-infested fields suggests that losses can easily reach 50 percent.

Paratylenchus microdorus. This nematode has been found in very large populations near the roots of vetch (Vicia sativa). Plants showed reduced growth and symptoms of leaf burning. No work has been done with this nematode.

Pratylenchus penetrans. From a survey done recently on potato (Solarium tuberosum) and haricot bean (Phaseolus vulgaris) it was evident that this nematode is a serious pest of these two important crops. Almost all the samples examined, both soil and roots, contained large populations of this nematode. With potato, nematode-infested plants had poor growth and matured earlier than normal. Yields were also reduced. Characteristic symptoms of attack (early dying of mature leaves) matched the so-called potato early dying (PED) effect described in the United States.

Pratylenchus thornei. This nematode has frequently been recovered in large numbers from barley (root and soil). Infested fields had many patches of stunted plant growth with symptoms of wilting and plants were chlorotic. Nematode-infested feeder roots were short, abnormally developed and free from root hairs.

Pratylenchus spp. This group of nematodes, the lesion nematodes, was found to be associated with many deciduous fruit-trees affecting yields adversely. Also, results from the survey work showed that Mesocriconema xenoplax (ring nematode) was widely spread and closely associated with "peach tree short life".

Nematode control and side-effects

Increased costs of production and scarcity of irrigated land very often oblige farmers to use chemicals (nematicides) in case of serious nematode attack. As mentioned earlier, significant nematode damage occurs on citrus, potatoes, vegetables, bananas and vines, while other crops need to be thoroughly studied to determine their susceptibility to nematode attack.

Several nematicides, either in the group of carbamates (aldicarb, oxamyl) or organophosphates (fenamiphos, prophos, isazofos) are used for nematode control in established crops. These are easily applied by either granular applicators (incorporated in the soil) or by mini-sprinklers through the irrigation system (pestigation).

Research by the Agricultural Research Institute (ARI) in Cyprus has shown that all the above nematicides can effectively control nematodes when applied at recommended rates and with the correct method of application. Their cost of application, including the product, varies accordingly, ranging between US$150 and $200 per hectare for each application. Studies are in progress to lower the cost of nematicidal application further by spraying liquid nematicides after plant emergence. An example of this is the control of the lesion nematode (P. penetrans) attacking potato and haricot bean, using Oxamyl L.

Recently, several biological products have appeared on the market claiming to be nematicidal. Unfortunately, there is very little information about their nematicidal efficiency. Also, other important details (optimum rate and frequency of application as well as their method of application) are very difficult to obtain. Nevertheless the great and urgent need for testing such compounds cannot, for obvious reasons, be questioned.

There is no problem of toxic residues remaining in the crops at harvest after applying nematicides on citrus, potatoes and bananas. However, for non-leafy vegetables (tomato, eggplant, carrot, strawberry) care must be taken to ensure that the correct chemical at the proper rate is used. For leafy vegetables, the advice to farmers is to avoid using systemic nematicides. Instead, the use of solar sterilization or Basamid (a fumi-gant) prior to planting, is recommended.

A serious problem that we may soon face, mostly in established plantations, is the pollution of groundwater. Degradation of nematicides (either carbamates or organophosphates) is not well understood in the various types of soils in different regions where they are used. Parameters, such as water-table depth, soil temperature and available soil moisture after application, are important factors in determining the danger of polluting groundwater. There is little experience with these problems in Cyprus, but it is very important and necessary to take into consideration the dangers encountered from applying nematicides to the soil.

Research and facilities

In Cyprus, most of the research work in plant nematology concentrates mainly on the chemical control of important parasitic nematodes in economically important crops. However, during the last few years there has been an increasing interest in testing other means for controlling losses resulting from nematode attack. Examples of these are the following: screening of nematode-resistant cultivars of tomato and peach against root-knot nematode attack; control of the potato-cyst nematode by choosing the right time of planting, i.e. phenological control; and control of Xiphinema index, vector of GFV disease of vines by fallow treatment.

The experimental work is done almost exclusively in the field while sample processing and monitoring of nematode populations are done in the Nema Laboratory. Basic facilities for extracting nematodes from either soil or roots exist. An Olympus compound microscope and a Bausch-Lomb stereoscope are also available. Extra space (constant temperature room) for maintaining live nematode cultures is also provided. Very recently a gyratory shaker has been introduced for extracting nematodes from roots.

Assistance in field and laboratory work is provided by a single assistant (secondary school graduate) with 24 years' experience. Research in nematology is the responsibility of ARI where there is only one professional nematologist. Another agriculturist in the Department of Agriculture is partially involved in plant nematology.

Advisory work on nematology and training

Results of completed nematological work by the institute are passed on to the appropriate body of the Department of Agriculture (Plant Protection) for evaluation and advisory work. However, it is believed that most agricultural field advisers are not fully aware of the existing nematological problems. There is a need, therefore, for more careful and regular briefing on the subject.

Worldwide achievements in both the scientific and technological sectors have greatly improved recently. Therefore, the need for strengthening and upgrading nematological research with suitably qualified (additional) personnel should be seriously considered. Prolonged stagnation in personnel and technology restrains progress and should, by all means, be avoided.

Conclusions and recommendations

· Upgrade (qualitatively and quantitatively) nematological work by recruiting additional (suitably qualified) personnel. Also, train existing staff in modem techniques, preferably on the extraction and identification of important pathogenic groups.

· Emphasize to official authorities and administrators the effect of nematode damage on crop losses.

· Refer not only to high-value crops (irrigated) but also to field crops (rain-fed).

· Exchange regularly information and visits with research stations in neighbouring countries on nematological problems of mutual interest. This will enable a better understanding of the problems and increase the chances of their successful handling.

· Organize a suitable body that will be responsible for collecting, updating and evaluating all necessary information concerning the safe use of nematicides on a regional basis. Pass, without delay, all relevant information to interested regional nematological research stations.

Bibliography

Ministry of Finance. 1991. Agricultural statistics 1990-91. Department of Statistics and Research. Nicosia.

Philis, J. 1971a. Control of root-knot nematode Meloidogyne javanica Treub. on eggplant by pre-planting treatments. Phytopath. Medit., 10: 117-119.

Philis, J. 1971b. Control of root-knot and spiral nematodes on bananas in Cyprus. PI. Dis. Reptr., 55: 707-710.

Philis, J. 1974. Chemical control of the root-knot nematode Meloidogyne javanica Treub. on tomato. ARI Technical Paper No. 4. Nicosia, ARI.

Philis, J. 1975. Control of the citrus nematode, Tylenchulus semipenetrans Cobb, in a grape fruit orchard in Cyprus. ARI Technical Paper No. 10. Nicosia, ARI.

Philis, J. 1977. Resistance of tomato varieties to the root-knot nematode Meloidogyne javanica in Cyprus. Nematol. Medit., 5: 39-44.

Philis, J. 1978. Effect of D-D, EDB and dazomet on potato-cyst nematode control in clay soils of Cyprus. Nematol. Medit., 6: 77-81.

Philis, J. 1980. Life history of the potato-cyst nematode, Globodera rostochiensis, in Cyprus. Nematologica, 26: 295-301.

Philis, J. 1981a. Chemical control of the potato-cyst nematode, Globodera rostochiensis (Wall.) in Cyprus. ARI Technical Paper No. 21. Nicosia, ARI.

Philis, J. 1981b. Species of potato-cyst nematode from the Xylophagou area in Cyprus. Nematol. Medit., 9: 57-61.

Philis, J. 1983a. Occurrence of Meloidogyne javanica on tomato in Cyprus. Nematologica, 30: 470-474.

Philis, J. 1983b. Occurrence of Meloidogyne spp. and races on the island of Cyprus. Nematol. Medit., 11: 13-19.

Philis, J. 1986. Phenological control of the potato-cyst nematode. ARI Technical Bulletin No. 81. Nicosia, ARI.

Philis, J. 1988. Control of the citrus nematode Tylenchulus semipenetrans Cobb in Valencia orange groves in Cyprus. Nematol. Medit., 16: 159-161.

Philis, J. 1989a.Yield loss assessment caused by the citrus nematode Tylenchulus semipenetrans on Valencia oranges in Cyprus. Nematol. Medit., 17: 5-6.

Philis, J. 1989b. Resistance of peach seedlings to root-knot nematode attack. Int. Nematol. Network Newsl., 6(3): 3-5.

Philis, J. 1990. The efficacy of nematode resistant tomato cultivars to Meloidogyne javanica under greenhouse conditions. Nematol. Medit., 18: 209-211.

Philis, J. 1991. Assessment of potato yield loss caused by the potato-cyst nematode, Globodera rostochiensis Woll. Nematol. Medit., 19: 191-194.

Philis, J. & Siddiqi, M.R. 1976. A list of plant-parasitic nematodes in Cyprus. Nematol. Medit., 4: 171-174.


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