Incidence of virus and virus-like diseases in citrus orchards

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Field survey

A survey to determine the incidence of virus and virus-like diseases in citrus orchards was conducted during Salibe's short visit. Several farms in the districts of Paphos, Limassol, Nicosia and Famagusta were visited and their trees inspected for disease symptoms. They included various citrus species cultivated commercially, namely orange, grapefruit, lemon and mandarin. Various packing houses were also visited and the fruits inspected for symptoms of stubborn and impietratura diseases.

Reliable symptoms of psorosis scaly bark, infectious variegation, cachexia-xyloporosis, impietratura, stubborn and rumple diseases were observed. In a few trees in four orchards, symptoms resembling those induced by tristeza virus were observed, but all the symptoms of the disease were not present and the abnormalities were called "tristeza-like symptoms". Further indexing of these trees should be carried out to determine the possible presence of tristeza virus.

Virus and virus-like diseases

Psorosis A and concave gum. During the field survey, typical symptoms of psorosis A bark scaling were observed in trees of Valencia orange on sour orange rootstock in the districts of Limassol, Nicosia, Liopetri, Phrenaros (Fig. 98) and Famagusta. Diseased trees were more than ten years old and were scattered in large orchards. Only a few showed scaling symptoms, with diseased branches, and the entire tree was rarely affected. The existence of large orchards of Valencia orange apparently free from psorosis symptoms suggests that more than one introduction of this variety must have been made into the country and certainly some of them were from psorosis-affected trees.

TABLE 27 Cypriot production and exports of citrus fruit in 1981

Some trees of Valencia orange with trunk and branch malformations and concavities were encountered, suggesting concave gum or "finger marks".

Psorosis A was also observed on Clementine mandarin trees in an orchard in the Limassol district that were about 25 years old. Nearly a quarter of the trees were diseased with trunks and branches displaying bark scaling.

Surprisingly, no symptoms of psorosis A were found in grapefruit trees, although they are commonly infected by this virus in most citrus areas of the world. A more extensive survey may reveal the presence of psorosis-infected grapefruit trees, but this does not appear to be an economically significant problem for this citrus species in Cyprus.

No psorosis A symptoms were found in trees of other citrus species and varieties, including lemons, mandarins and oval sweet oranges (Shamouti orange). The navel orange trees inspected in a few orchards were also apparently healthy. The absence of the disease in the orchards of the Paphos district was probably due to the young age of the trees and the extensive use of nucellar budlings in the area.

There is no economical means of eliminating psorosis virus from trees. Removal of bark lesions and chemical treatment may delay tree deterioration, but cure is impossible. The virus builds up through the use of budwood taken for propagation from infected mother trees. Prevention, through the selection and propagation of psorosis-free mother trees, will result in virus-free progenies. No mechanical or insect transmission of psorosis A is known to occur in the Mediterranean area.

Infectious variegation-crinkly leaf This disease is not commonly seen in citrus and, because of its severe and conspicuous symptoms, it can be easily avoided in commercial plantings. According to Bové (1966), infectious variegation has been seen in Algeria, Corsica, Sardinia, Sicily and Morocco. Salibe, during a visit to Greece in 1975, observed a much higher incidence of infectious variegation than he had seen in other citrus areas of the world.

In Cyprus, Salibe found Valencia sweet orange trees infected with infectious variegation, crinkling and distortion in three Valencia orange orchards. Most trees in these orchards displayed symptoms, with the exception of nearby Washington navel orange and lemon trees.

On affected trees, the number of leaves showing the yellow mosaic pattern varied, but on some nearly all the leaves were affected. Fruit production on the very severely affected trees was low and many fruits showed yellow sectorial lines.

Bové observed symptoms of infectious variegation-crinkly leaf virus on 1 7-year-old Jaffa sweet orange trees in the Limassol area. Leaves were crinkled and warped (Fig. 107) and fruits were bumpy (Fig. 108). The virus strain involved is the more severe infectious variegation strain as only it, and not the crinkly leaf strain, induces fruit symptoms. Both strains produce similar symptoms on sweet orange leaves in the field. The leaf symptoms induced by infectious variegation-crinkly leaf virus should not be confused with those resulting from chimera or mutations (Fig. 314).

Cachexia-xyloporosis. Cachexia-xyloporosis is widespread and is probably present in all citrus-growing areas of the world. It has been particularly important in the Mediterranean countries and was reported to occur in Cyprus by Littlejohn (1939).

Trees of sweet orange and of grapefruit on sour orange rootstock, the combinations most widely used in Cyprus, are tolerant of cachexia-xyloporosis. Therefore, trees of these combinations may be infected by the cachexia viroid without exhibiting symptoms.

Cachexia-xyloporosis in field trees having intolerant tissues requires an incubation period of five or more years before symptoms appear, and only rarely can they be seen without removing a piece of bark at the union. Typical symptoms of this disease were encountered in three trees of Clementine mandarin budded on sour orange root-stock. The trees were more than 20 years old and were growing in an orchard in the Astromerites area. Extensive gumming, pegs and pits occurred in the scion portion of the trees, beginning at the bud-union and extending about 50 cm above it on the larger limbs. Bové observed similar cachexia symptoms on Clementine trees on sour orange rootstock in the Liopetri area. The use of budwood from healthy mother trees is apparently responsible for the low incidence of cachexia-xyloporosis in Cyprus. However, further indexing of orange and grapefruit trees may disclose a high percentage of infection in a latent form. Indexing is thus extremely important in the event that virus-intolerant rootstocks come into use in the country. It has not been determined how much reduction in tree size results from infection by cachexia-xyloporosis virus in the so-called tolerant combinations.

Cachexia-xyloporosis virus can be excluded from new orchards by using only budwood certified free of virus and virus-like pathogens in the new propagations. No insect vector of the cachexia viroid has been reported. Mechanical transmission has been obtained experimentally.

Impietratura. Impietratura is a disorder affecting citrus fruits and is considered to be of viral aetiology (Ruggieri, 1955). It occurs in most citrus-growing areas of the Mediterranean (Algeria, Corsica, Cyprus, Greece, Israel, Italy, Lebanon, Morocco, Sardinia, Spain, the Syrian Arab Republic and Turkey) and only a few locations elsewhere. Trees affected by impietratura show symptoms only in the fruits, many of which are small and hard. Deposits of brownish gum are present in the albedo and sometimes in the stem end of the fruit. Not all fruits from infected trees show these symptoms. On the surface of severely affected fruits, one can easily note brownish spots or bumps due to gum pockets in the albedo. Similar symptoms have been observed in Florida and Brazil, but have been found to be due to boron deficiency.

Impietratura causes heavy losses to citrus growers and packers because affected fruit is not suitable for the commercial export market. In some instances, as much as 80 percent of the mature fruit on impietratura-infected trees is unmarketable as fresh fruit and can only be used for juice.

Impietratura is widespread in Cyprus, and was first described there by Papasolomontos (1965), who pointed out that the problem had been increasing in recent years. Papasolomontos and Economides (1967) reported that impietratura-diseased fruits occurred in grapefruit trees budded on several different rootstocks, but that infected trees tended to produce a smaller percentage of abnormal fruits as they grew older.

Impietratura can be considered one of the main causes of loss to the Cypriot citrus industry. Its symptoms were found in fruits of Marsh seedless grapefruit in orchards of all four districts visited. They were also observed in one lemon orchard (probably Lisbon lemon) that was top-worked into old grapefruit trees in the Nicosia district.

Severe symptoms of impietratura were encountered on fruits of Valencia orange trees on sour orange rootstock, aged about 22 years, in Phrenaros (Famagusta district). Bové observed impietratura symptoms on fruit from Marsh grapefruit trees in Liopetri (Famagusta district). No impietratura symptoms were found on Washington navel and Shamouti oranges or on mandarins.

Impietratura is graft-transmitted (Ruggieri, 1955; Papasolomontos, 1965). There is no evidence of spread of the causal agent of impietratura other than by bud perpetuation or by grafting.

Tristeza and stem pitting Apparently, all cases of tristeza disease found in the citrus-growing areas of the Mediterranean basin can be traced back to introductions of infected budwood from abroad. All countries that have introduced Meyer lemon trees have also introduced tristeza (Bové, 1966). These include Algeria, Cyprus, Israel, Italy, Morocco and Tunisia. Other varieties imported from Australia, Japan, South Africa and the United States of America have also been reported to have introduced tristeza into the Mediterranean countries.

Tristeza was first suspected in Cyprus in 1956 in a few Meyer lemon and Cecily grapefruit trees (Mender, 1956). All the trees involved were uprooted. Papasalomontos and Economides (1968) reported the results of extensive indexing for tristeza, which showed a wide distribution of infected trees in the various citrus-producing areas of the country. Four varieties were found to carry tristeza: Washington navel orange and Naartjie mandarin, born on rough lemon rootstocks, an unidentified everbearing lemon and another citrus type locally referred to as "Koumandandas". The total number of infected trees was 24. There appeared to be very little natural spread of the disease agent, the local strains of aurantii being rather inefficient vectors of tristeza virus. The Aphis gossypii and Toxoptera presence of various aphid species that may eventually become vectors of CTV in citrus trees in Cyprus was reported by Eastop and Christophi (1981). These species included T. Aphis citricola and A. gossypii.aurantii.

Salibe visited orchards in Limassol, Nicosia and Famagusta where a few trees of Marsh seedless grapefruit and Valencia orange were found with symptoms resembling those of tristeza. Sudden death of grapefruit, mandarin and Mineola tangelo trees on sour orange rootstock was reported by the growers in several plantations. Trees found with tristeza-like symptoms were all stunted, with some overgrowth about the bud-union and discoloration in the cambium of the sour orange rootstock. Recommendations were made for immediate elimination of these declining trees, as they may be a source of inoculum for the spread of CTV.

Kyriakou and Polycarpou (Agricultural Research Institute, Nicosia) conducted an extensive programme of indexing for CTV in Cyprus. During 1987-88, 435 trees of 28 citrus varieties grown in 92 blocks of the main citrus-producing areas of Cyprus were tested. Typical CTV symptoms developed only on two small-fruited acid lime seedlings inoculated with buds of five trees from a single block of ten-year-old Clementine trees on sour orange rootstock. Symptoms on the lime seedlings consisted of leaf vein clearing, reduction and cupping of lower leaves and stem pitting. The two lime seedlings with symptoms were tested by ELISA against CTV from Ingenasa, Spain, against polyclonal antibodies from California and against MAs purchased from Bioreba, Switzerland. Results were positive with all types of antisera, but the strongest and clearest reaction was obtained with the MAs from Spain.

In the spring of 1989, all trees of the Clementine block in which infection was detected in 1987-88 were tested by ELISA using a mixture of antisera from Ingenasa and Bioreba. Out of 332 Clementine trees tested 190 (57 percent) were found to be infected. Ninety-two trees of four other citrus varieties scattered among the Clementine trees were also tested, but only one tree of an unknown mandarin variety was found to be infected. About 40 percent of the Clementine trees positive for tristeza exhibited evident decline symptoms: tree stunting, general chlorosis, off-season flowering, vein chlorosis and vein corking of mature leaves.

The high incidence of CTV in the single Clementine block in which infection was located indicates that the disease arrived with infected budwood. However, the presence of the virus in one out of 92 trees of other citrus varieties indicates that limited natural spread has probably occurred. Future studies will focus on the transmissibility of CTV by aphid species infesting citrus in Cyprus, and efforts will be made to trace the source and spread of infected Clementine budwood. In the meantime, two control measures are strongly recommended. All trees of the infected Clementine block should be eliminated, and a routine indexing and eradication programme for tristeza should be undertaken in order to prevent severe damage to the island's citrus industry in the future.

Rumple. The name "rumple" has been given to a disorder affecting lemon fruits of certain clones of Lisbon and some other varieties. According to Klotz (1973), rumple disorder occurs in Cyprus, Ethiopia, Lebanon, Turkey and the United States of America. It appears in late summer, first as faint chlorotic specks on the rind surface, which subsequently turn brownish-black and finally collapse. Large fruits develop a higher incidence of rumple than smaller ones. The number of affected fruits varies from year to year and from orchard to orchard. There are no apparent tree symptoms. Rumple is suspected to be of a viral nature, but no definite proof of this has been obtained. Careful selection of budwood for propagation from disease-free trees is recommended to avoid the problem in new plantings.

Rumple-like symptoms were observed during a field survey of fruits in two lemon orchards, one in the Paphos district and the other in the Limassol district. The lemon variety grown in both orchards was unknown, but resembled Lisbon. The growers and owners complained that they were losing part of the crop because of the fruit abnormalities. They had not been advised that such problems could occur when they bought the trees. Some other lemon peel problems found in other orchards visited were attributed to hail damage.

Exocortis. Exocortis has been found in many Mediterranean citrus areas including Algeria, Corsica, Israel, Morocco, Spain and Tunisia (Bové, 1966). In Cyprus, Economides (1976) reported exocortis in Marsh seedless grapefruit trees. He pointed out that all trees planted in the country trace their origin back to a single Marsh seedless tree imported from South Africa. Thus, exocortis must be widespread, but no visual symptoms are usually present.

No tree showing typical exocortis symptoms (stunting and rootstock bark scaling) was found during the field survey. This was to be expected, since sour orange, the only rootstock used in the country, is tolerant of the pathogen. Only systematic indexing can reveal the true incidence of exocortis in Cyprus.

For this reason, a survey for citrus exocortis was conducted by Kyriakou in commercial groves of the main citrus-producing areas of Cyprus from 1987 to 1990. Out of 573 trees of 25 species and varieties sampled, 506 (88.3 percent) were found infected, when indexed on seedlings of Etrog citron (Citrus medica L.) selection Arizona 861. Isolates of exocortis from old-line citrus (introduced in the island before the 1940s) produced more severe symptoms on the citron indicators than isolates from new introductions. In greenhouse tests a severe isolate was readily transmitted from citron to healthy citron and gunura (Gynura aurantiaca DC.) by the method of knife-blade inoculation.

MAP 5 Map of Cyprus showing the distribution of: 1) Salsola kali,the favoured host plant of Neoaliturus haematoceps; 2) Neoaliturus haematoceps, the leafhopper vector of Spiroplasma citri; 3) Spiroplasma citri, the causal agent of stubborn - in citrus, periwinkles and N haematoceps

Multiple sprouting. Symptoms resembling multiple-sprouting virus disease were observed in a few old trees of Lapithos lemon and on three trees of Marsh seedless grapefruit in the Limassol area. In recent years, 35 trees of the same lemon type with similar symptoms had been eradicated. Affected trees showed a bushy aspect and willowy branches, with brittle branches growing to the ground and multiple branching throughout the tree. Leaves and fruits were small, with many fruits showing sectorial chimeras and a large number of aborted seeds. Symptoms in the grapefruit trees were less conspicuous, but leaves were generally distorted. Some conditions, such as copper deficiency, infestations of the bud mite, Aceria sheldoni Ewing, or genetic factors may be involved in the problem, but the highly abnormal conditions displayed by the severely affected trees resembled multiple-sprouting disease.

Bud-union crease. Typical symptoms of bud-union crease were found in four trees of Marsh seedless grapefruit on sour orange rootstock. The affected trees were about 12 years old, stunted and showed foliocelosis. Mild stem pitting was observed in young branches of two of them. They were surrounded by healthy trees. The line at the bud-union was typical of bud-union crease disorder, but only one out of the four diseased trees showed gum pockets in the bark. This disorder may result from genetic incompatibility. It may also be caused by tristeza or by a suspected "bud-union crease" virus.

Stubborn

For many years stubborn was suspected to be a limiting factor in citrus production in Cyprus. The situation was examined in a joint project between the Agricultural Research Institute, Nicosia, and the INRA laboratory in Bordeaux, France.

Surveys in January and November 1987 showed symptoms of stubborn disease to be present in many of the sweet orange orchards surveyed (see Table 28). The proportion of symptomatic trees was generally below 5 percent in the orchards, but in young plantations the proportion of affected trees was higher. For instance, in the six-year-old Valencia late and navel sweet orange blocks of the Experiment Station in Akhelia (Paphos area, see Map 5), there were 11 percent and 8 percent affected trees respectively (see Table 29). In the Marsh grapefruit block only 6 percent of trees were affected.

The navel oranges from stubborn-affected trees were often acorn-shaped (Fig. 165). The fruit from Valencia late orange trees was reduced in size and had a high percentage (85 percent) of aborted seeds (see Table 29). S. citri could be cultured from many symptomatic trees (see Tables 28 and 29).

The mother block of the Akhelia Experiment Station was also found to be infected with the stubborn agent, even though the budwood (of nucellar origin) was certified free of virus and virus-like agents and came, in 1970, from the University of California at Riverside. Trees of both Washington navel and Valencia late sweet oranges were found to be affected and S. citri was cultured from the trees (see Table 28). These observations suggested natural transmission of S. citri. This hypothesis was examined by exposing periwinkle (Catharanthus roseus) seedlings to natural contamination at the Akhelia Experiment Station in May 1987. The plants were examined in October. Six periwinkle plants showed typical symptoms of S. citri infection and the spiroplasma was cultured from them (see Table 28). These results prove that natural transmission of S. citri occurs in the Akhelia area.

TABLE 28 Detection of Spiroplasma citriin Cyprus in sweet orange trees, periwinkle (Catharanthus roseus) seedlings and Neoaliturus haematoceps leafhoppers

TABLE 29 Stubborn in sweet orange and grapefruit trees at Akhelia, Cyprus

Note:
¹ S. citri infection was detected by culture of the spiroplasma.

Work in Morocco and the Syrian Arab Republic has shown that the major vector of S. citri in the Mediterranean and the Near East is the leafhopper Neoaliturus haematoceps and that the preferred host plant of this leafhopper is Salsola kali. Therefore a survey for the leafhopper and its host plant was carried out in October 1987 in the southern part of Cyprus.

Map 5 shows the island and gives the results of the survey. S. kali was present in many locations and often in great abundance all along the southern coast (Figs 171 to 173), from the Paralimni area in the east to Argaka in the west. Occurrence of S. kali in northern

Cyprus as obtained from literature is also indicated on the map. Leafhoppers were collected wherever S. kali occurred. N. haematoceps was always present in great numbers within the leafhopper catches. Several of the N. haematoceps batches were found to be positive for S. citri either by culture or ELISA.

These results show that N. haematoceps, the major leafhopper vector of the stubborn spiroplasma, is abundant in Cyprus in the coastal areas. In particular, the leafhopper was found on the coast in the Paphos area near the Akhelia Experiment Station where natural transmission of S. citri was demonstrated, as noted earlier. The presence of up to 10 percent stubborn-affected trees in the sweet orange blocks at Akhelia is very probably due to natural spread of S. citri. Table 29 shows that 44 of the 420 Valencia late sweet orange trees were already infected in 1986, when the trees had been in the field for five years. Only three more infected trees were found in 1989. This indicates that in Cyprus, as elsewhere, infection by S. citri primarily affects young trees. The young orchards that are now being planted in Cyprus, and especially those close to the coast where N. haematoceps occurs, must be carefully inspected once a year for the first four or five years. Suspect trees should be removed and replaced with healthy ones. This procedure will keep the percentage of stubborn-affected trees well below 10 percent.

Fungal diseases

Mal secco. Salibe noted that mal secco was severe on Eureka lemon trees, but that some local lemon trees, such as capithos, had resistance. Severe symptoms of mal secco were also observed by Bové on Ortanique tangor on sour orange rootstock in the Lanitis orchard at Limassol. The trees die suddenly (Fig. 315). Ioannou (personal communication) has shown that infection by the causal fungus Deuterophoma tracheiphila (Petri) is not through the canopy, but through the roots. The fungus moves up through the rootstock, invades the scion (Fig. 234) and kills the tree.

Rio Grande gummosis. Abundant gumming typical of Rio Grande gummosis was observed by Bové on many (70 percent) Jaffa sweet orange trees at the K. Hadji Georgiou orchard at Alaminos-Latouros (Figs 246 and 247). The severity of the Rio Grande gummosis problem in this orchard is probably due to the high salt content of the water (4 mmoles) which also results in severe leaf drop (Fig. 246).

In the same orchard, grapefruit trees were less affected by gumming and leaf drop, probably because they are more tolerant to salt. Marsh grapefruit trees were also affected in the Sotiris Yiorgallas orchard (15-year-old trees) at Latouros and the in Lanitis orchards (26-year-old trees) at Limassol.

A visit to northern Cyprus

A half-day trip was made to northern Cyprus to observe some aspects of the citrus industry in that part of the island, namely the Morphou (Guzulyurt) area. Citrus orchards here were very similar to others on the island. Some symptoms of malnutrition and iron deficiency were seen. No time was available for a virus survey, but fruits with impietratura were observed in the Cypfruvex packing house.

Since propagative materials used in the establishment of orchards in this and other areas of the island are probably of the same origin, findings on the incidence of virus and virus-like diseases in the Nicosia, Limassol and Famagusta areas may be considered valid for the Morphou area. Salibe was informed by local authorities that about 9 000 ha of citrus are grown in the northern area, with an estimated yearly production of 140 000 tonnes. About 70 percent of the fruit is exported by the government-managed Cypfruvex.

Because of the proximity of orchards to each other in the various areas of the island, the introduction and spread of virus problems in one place immediately endangers all other plantations. Phytosanitary measures should be extended to all citrus-growing areas of Cyprus for the protection of all existing plantations.

Bibliography

Bové, J.M. 1966. Citrus virus diseases in the Mediterranean area. Report presented at the meeting on Phytiatry and Phytopharmacy, Marseilles (France), 1965, updated for the 4th Conf. IOCV. 44 pp. (mimeo)

Eastop, V.F. & Christophi, S. 1981. Check list of Cyprus aphids. Prepared in the Research Department of Agriculture. 8 pp. (mimeo)

Economides, C.V. 1976. Exocortis in Marsh seedless grapefruit in Cyprus. Plant Dis. Rep., 60: 532-534.

Klotz, L.J. 1973. Color handbook of citrus diseases. Citrus Res. & Agric. Exp. Sta., Riverside, Univ. Calif. 122 pp.

Littlejohn, L. 1939. Annual report of the botanist and plant pathologist for the year 1938. In Rep. Dir. Agric., Cyprus, 1938.

Louca, A. 1981. Annual Report of Department of Agriculture. Cyprus, Ministry of Agriculture and Natural Resources.

Mendel, K. 1956. The threat of tristeza disease in the Mediterranean basin. FAO Plant Prot. Bull., 4: 106- 108.

Papasolomontos, A. 1965. The present status of impietratura, a citrus disease in Cyprus. Plant Dis. Rep., 49: 111 - 113.

Papasolomontos, A. & Economides, C.V. 1967. Effect of rootstock on the incidence of impietratura-diseased grapefruit fruits. Plant Dis. Rep., 51: 684-686.

Papasolomontos, A. & Economides, C.V. 1968. The presence of tristeza virus in certain species of citrus in Cyprus. FAO Plant Prot. Bull., 16: 8-9.

Ruggieri, G. 1955. Le arance impietrate. Rivista Agrumicoltura, I (2): 65-69.

Chapter 10: Egypt

Virus and virus-like diseases
Other observations
Integrated protection programme for citrus improvement
Recommendations
Bibliography

Egypt stands at present among the largest citrus-producing countries in the world. Although some citrus types were grown here about the time of Alexander the Great's conquest (332 BC), it was only at the beginning of this century that extensive commercial orchards were planted in the country, and expansion is still continuing. This development is reflected in strong annual increases in fruit production, which are likely to continue in the near future.

The area under citrus is estimated to be nearly 100 000 ha, with a production target of about two million tonnes, the overwhelming part of it being oranges. In the last decades, Egypt has certainly made the largest increases in citrus production of all Mediterranean countries, with an annual growth rate ranging from 11.4 percent in 1960-1970 to 8.7 percent in 1970-1980. Output of oranges and tangerines was estimated at 266 000 tonnes in 1960/ 61, 710000 tonnes in 1970/71, 971 000 tonnes in 1975/76 and 1 570000 tonnes in the 1980/81 season (Wolff, 1977). Most of the production is early season orange, a type well-suited for Egyptian growing conditions. Exports are increasing and were said to have reached nearly 180 000 tonnes in the 1982/83 season. Improved export performance was favoured by the construction of packing and storage plants, transportation facilities and modern laboratories for quality-control work.

The major citrus-producing countries of the world have highly developed systems of production, harvesting and marketing. Therefore countries trying to break into the world citrus market face major competition from the well-established producing and exporting areas. It is, however, feasible, provided that high-quality fruits are produced and that other factors are sufficiently favourable - for instance, high orchard productivity is necessary, as are low costs of labour, transportation and other needed items. The development effort must also be properly organized and adequately financed. Low productivity of orchards is a serious constraint to development of the citrus industry of most countries.

Fruit production per unit area is fairly low in the Egyptian citrus orchards, the average yield being, according to various estimates, around 15 to 20 tonnes per hectare. A good yield is considered to be around 50 tonnes per hectare.

In Florida, Sao Paulo (Brazil) and a number of other advanced citrus areas, the average yield of adult orchards ranges from 30 to 35 tonnes per hectare, although some orchards are known to produce larger crops, of up to 80 or 90 tonnes per hectare. Individual trees (40 to 70 years old) in exceptionally good health are known to produce up to 1 200 kg of fruit (about 30 boxes of 40 kg) per year. The cost of production obviously decreases with rising productivity.

Virus and virus-like diseases

Virus diseases are known to have been affecting citrus trees in Egypt for more than 50 years. In 1931, Fawcett found unhealthy trees (later proved to be affected by a virus) during a visit to the country's citrus orchards. Various surveys subsequently disclosed the presence of several virus and virus-like diseases causing disorders in commercial plantings and experimental orchards (Childs et al., 1955, 1956; Nour-Eldin and Bishay, 1958; Nour-Eldin, 1959; Knorr, 1961). Only recently, however, have virus diseases started to be recognized as a serious problem in the citrus industry. In spite of a number of attempts to eliminate viruses from new orchards, they continue to be a major constraint to high yields.

Scaly bark psorosis (psorosis A)

Scaly bark psorosis affects citrus trees worldwide and is found in most Mediterranean orchards. It is a slow-acting disease that may take several years to produce visual symptoms. Bark scaling rarely occurs before the tree is six years old and symptoms may be delayed for many years, sometimes 30 or 40. According to Nour-Eldin (1959), more than 90 percent of all grafted trees in Egypt carry psorosis A or concave gum. Knorr (1961) mentioned that some blocks of mature trees had up to 25 percent of trees suffering from typical bark-scaling psorosis. Salibe observed symptoms of psorosis bark scaling and/or concave gum-blind pocket on many Washington navel and Valencia late orange trees, but not on trees of other local varieties. Apparently, these two imported varieties were brought into the country carrying virus and all further propagations were also infected.

Possibly a few trees that escaped infection are free from disease. Inspection of large plantings of nucellar Washington navel orange trees revealed no psorosis symptoms, which practically eliminates the possibility of insect transmission of the virus.

Elimination of psorosis virus from new plantings can only be achieved by the use of budwood from healthy mother trees. Selection of psorosis-free trees to be used started in Egypt in the 1950s (Nour-Eldin, 1959).

Cachexia-xyloporosis

This is a bud-transmissible disease inducing wood pitting and gumming of sweet limes, mandarin-limes, certain varieties of mandarins, tangelos, Citrus macrophylla, and some other citrus types. Symptoms range from the severe in Orlando, Wekiwa and Seminole tangelos, Clementine, Mandalina and Parson's Special mandarins, Murcott and Ellendale tangors, to the undetectable in sweet orange, sour orange, grapefruit and trifoliate orange. The symptoms occur on the trunk of infected trees, above or below bud-union according to the position of the susceptible variety.

Since the cachexia-xyloporosis viroid is perpetuated by the use of infected budwood and no insect vector is known, it can be excluded from new plantings by using only healthy propagative material.

Cachexia-xyloporosis seems to be widespread in Egypt. According to various authors (Nour-Eldin, 1959; Knorr, 1961) it has been found that more than 60 percent of the Balady mandarin trees budded on sour orange rootstock are affected by the disease. Systematic indexing is necessary to reveal the extent of the problem on symptomless scion-rootstock combinations. Salibe observed cachexia-xyloporosis in the trunk above the bud-union (up to 1 m) on trees of Balady (Willowleaf) mandarin in commercial orchards. Some trees of satsuma and Clementine mandarins examined at the Barrage Horticultural Experiment Station also showed severe cachexia-xyloporosis symptoms. These two varieties, however, are not grown in large orchards in the country.

The presence of wood pitting on sour orange rootstock of some Balady mandarin trees affected by cachexia-xyloporosis raises the possibility of the presence of cristacortis virus in combination with the cachexia-xyloporosis pathogen, but further studies are necessary to clarify this point.

Stubborn

Stubborn is a very serious disease found in most countries growing citrus under desert or semi-desert conditions. It has been reported from the Arabian Peninsula, Arizona and California, Egypt, the Islamic Republic of Iran, Iraq, Israel, Lebanon, Morocco, Peru, the Syrian Arab Republic, Turkey and several other countries. Symptoms of stubborn include: tree stunting, an abnormally bushy aspect with small leaves and short internodes, fruits that are small, lopsided and acorn-shaped, with curved columella, inverse or pale coloration and sometimes blue albedo. In seedy varieties, excessive seed abortion occurs frequently. Pinholing of sour orange bark below the bud-union is found in severe cases (Calavan and Carpenter, 1965).

It is believed that many citrus varieties and combinations are susceptible to the stubborn pathogen, the helical mycoplasma Spiroplasma citri. These include, primarily, sweet orange, grapefruit, mandarin and tangelo. Several non-rutaceous hosts are known, including Vinca rosea, Trifolium repens, Trifolium pratense, Vicia faba, Pisum sativum and possibly others. The stubborn organism is transmitted through tissue grafts and through buds, and is also spread by leafhopper vectors. The two main leafhopper vectors Neoaliturus haematoceps and Neoaliturus tenellus - are present in Egypt. In many Mediterranean countries N. haematoceps is more abundant than N. tenellus. In Egypt, however, the reverse is true (Frazier, 1953).

Stubborn disease was discovered in Egypt by Nour-Eldin (1959) in trees of Safargali orange and was initially named Safargali decline. The same author (1967) described plasmodium-like structures and spherical inclusion bodies in hypertrophied cells of tumorous growths of flowers from stubborn (Safargali) trees cultured on potato dextrose agar.

Salibe observed severe symptoms of stubborn on trees of old-line and nucellar Washington navel orange in commercial and experimental plantings. No stubborn was found on trees of Valencia and Shamouti oranges or on other local varieties.

Gummy bark of sweet orange

A disease of sweet orange trees on sour orange rootstock was found by Nour-Eldin (1956, 1959) in Egypt and described as "phloem discoloration of sweet orange". In a further publication, the same author (Childs et al., 1968) showed that the gummy deposits are mainly in the outer layers of bark tissue, and changed the name of the disorder to "gummy bark of sweet orange". Affected orange trees are usually stunted and gum deposits become visible when bark of the trunk above the bud union is scraped off. The symptoms of the disease in the main resemble those of cachexia-xyloporosis on mandarin.

Salibe had previously observed symptoms of gummy bark on trees of sweet orange varieties in Italy and the Philippines. However, no diseased tree was shown to him during his visit to Egypt. Because it is a virus disease for which no vector is known, propagations from healthy trees may completely exclude the problem from new plantings in Egypt.

Tristeza complex

Tristeza is a very destructive disease caused by a virus which affects trees of sweet orange, mandarin and grapefruit on sour orange and certain other intolerant rootstocks. It occurs in most citrus areas of the world - Argentina, Brazil, California, Paraguay, Peru, Uruguay, Venezuela, in practically all countries of Southeast Asia, Australia, Spain and most African countries south of the Sahara. Tristeza has killed about 25 million trees in South America and about three million trees in California so far (Bové and Vogel, 1975). The disease represents a tremendous threat to the citrus industry of the Mediterranean basin, one of the last areas free from the virus, and in which intolerant scion-rootstock combinations are widely used. Spain is one of the few Mediterranean countries where extensive spread of tristeza has occurred. In the region of Alcira-Carcagente-Corbera, in the Valencia district, the spread started in 1957. More recently, spread of tristeza was suddenly observed in Israel, and an identification and suppression programme was immediately launched (Raccah et al., 1976; Bar-Joseph et al. 1980) but has apparently failed.

Apparently, the early cases of tristeza disease found in the citrus areas of the Mediterranean basin can be traced back to introductions of infected budwood from abroad. All countries that have introduced Meyer lemon trees have also introduced tristeza (Bové, 1966), and these include Algeria, Israel, Italy, Morocco and Tunisia. Other varieties imported from Australia, Japan South Africa and the United States of America have also been reported to have introduced tristeza into the Mediterranean countries.

The first report that tristeza virus was present in Egypt was made by Nour-Eldin in 1959. Two bergamot oranges on sour lime rootstock, one Tanarif sweet orange also on sour lime rootstock and one Valencia orange believed to be budded on sour orange were infected. The virus was not found in any commercial orchards, and indications are that, so far, it has not been spread by aphid vectors.

Trees with typical symptoms of tristeza were shown to Salibe by local scientists. Ten trees were involved at the Barrage Horticultural Experiment Station - mainly navel orange on sour orange rootstock and about 20 years old - and one tree at the Horticultural Research Institute in Giza of Balady mandarin on sour orange rootstock.

These trees were indexed for tristeza using the Mexican lime indicator and found positive for the virus, according to information given by local virologists. It is believed that tristeza-infected trees probably do not occur in commercial orchards. However, it is to be feared that spread of tristeza may suddenly occur, as happened in Spain and Israel, and government officers must be aware that a programme for tristeza indexing is needed in Egypt.

Exocortis

Symptoms of exocortis include stunting of trees and bark splitting and scaling of the rootstock portion of the tree. On trees budded on trifoliate or Rangpur lime rootstocks, bark scaling usually appears after four to eight years. Symptoms of exocortis also show up when intolerant varieties used as scions are infected. They include yellowing of the bark of young branches, splitting and limited shelling. Certain selections of Etrog citron develop leaf epinasty and are used as indicators for exocortis.

Symptoms of exocortis disease are uncommon in Egypt. On the basis of evidence obtained in most citrus-growing areas of the world, however, it must be assumed that the viroid responsible for exocortis disease is widely distributed in the country's citrus orchards. It is certainly causing tree debilitation in the so-called symptomless carriers, but the real destructive capacity of the disease will appear only if intolerant rootstocks are used. Salibe observed exocortis-like symptoms in a few trees of Valencia orange budded on sweet lime rootstock in a commercial orchard in the Kalioubiy area. Two trees of old-line Tahiti lime examined at the Horticultural Research Institute showed conspicuous bark symptoms of exocortis disease.

Other virus and virus-like problems

A number of surveys have shown the occurrence of several abnormalities in citrus orchards and experimental plots in Egypt, other than those mentioned above. Nour-Eldin (1959) indicated the presence of the following disorders in the citrus orchards: rusty bark sloughing, bud-union crease, bud-union overgrowth and stem pitting of grapefruit rootstock. Knorr (1961) added a number of other problems to this list, such as autumn leaf drop, bark splitting of Balady lime decline, Balady lime stunt, big-butt, citron stunt, dot-chlorosis, mandarin chlorosis, rugose sour orange, scion trunk swelling, shell bark, sweet orange bud-union swelling and sweet orange gumless pitting. Except for autumn leaf drop, which is widespread and causes losses in fruit production, especially in upper Egypt, all the other disorders are at present of minor importance.

It should be pointed out here that a number of trees exhibit gumless pitting in the sweet orange scion and in the sour orange rootstock. Some of this pitting may result from insect damage, particularly from scale infestation, but indications are that cristacortis virus may be the cause of the problem in many trees. Indexing for cristacortis is recommended. On account of the limited number of orchards inspected during Salibe's visit, it was impossible to obtain a full picture of the extent of the problem. It should be emphasized that nutritional disorders, herbicide toxicity, faulty irrigation, deep planting, insect pests and other horticultural problems are depressing crop yield in the citrus orchards.

A number of virus and virus-like disorders known to be affecting citrus trees in other areas of the world have not been reported in Egypt and were not seen during Salibe's visit. Among diseases apparently not occurring in the citrus orchards of Egypt are: impietratura, rumple, vein enation-woody gall, leaf curl, citrus tatterleaf, leprosis, yellow vein, greening, infectious variegation, citrus blight and citrus decline. Fortunately, citrus canker, a damaging bacterial disease caused by Xanthomonas campestris pv. citri, also apparently does not occur in Egypt. Local plant pathologists should be aware of the symptoms of these and other undesirable diseases so as to be able to recognize them and promptly eradicate any tree suspected of harbouring their agents. Good descriptions of disease problems have been made by Childs et al. (1968), Bové and Vogel (1975) and Wallace (1978) among others.

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