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Citrus in southern Yemen
Citrus has been introduced into southern Yemen from various countries, such as Egypt, Iraq and Italy. None of the introduced plant material was certified free of virus and virus-like diseases, and can thus be expected to be contaminated with a whole range of diseases known to be present in the countries of origin.
The major citrus area is the Lawdar-Mudia region, with approximately 22 000 sweet orange trees covering a total of 100 ha. Sweet orange makes up about 60 percent of all citrus, the other cultivars including Willowleaf mandarin and Clementine, grapefruit, lemon and Balady lime (Citrus aurantifolia). Water for irrigation is from wells. The decrease in rainfall over the last ten years is probably the reason why the Lawdar-Mudia area is running short of water for irrigation, and explains why the acreage of citrus has declined over the last decade. Now, rainfall ranges from 200 to 400 mm per year and occurs in the cool winter season. The summers are hot and dry.
The Say'un-Tarim area in Wadi Hadramawt (see Map 19) grows mostly Balady lime seedling trees (12 000) and some sweet orange trees (2 000). The soils are saline and of high pH, about 8.0. The Bayhan area, close to Harib in northern Yemen, has mainly sweet orange trees (4 000). The author surveyed the Harib area in 1983 but not the Bayhan. Finally, there are about 6 000 Balady lime trees in the coastal Zinjibar-Gaar area.
Two rootstocks seem to have been used in southern Yemen: sour orange and rough lemon. Unfortunately the rootstocks are almost never recorded. Lack of rootstock identification has made it difficult to interpret certain symptoms seen on rootstocks.
Greening in southern Yemen and the Arabian Peninsula
The situation in southern Yemen. Since greening disease and its insect vector, the African psyllid T erytreae, are both present in northern Yemen and in particular at Al Baida, an area very close to Mukayras in the south, the probability was high that the disease and the vector also existed in the Mukayras area. The 1987 survey has indeed shown that T. erytreae is present and reproduces on citrus in the Mukayras region. Developing nymphs and young adults (Fig.189) of the psyllid have been found in the A. Hydan orchard on sour orange (Figs 189 and 190) and Balady lime. Evidence for the occurrence of T erytreae is based on the presence of nymphs and adults, but conveniently also on the development of bumps on the upper leaf surface (Fig. 190). Each "bump" is a concave depression seen on the lower surface of the leaf, and represents a nest in which a nymph has grown. (It should be pointed out that D. citri does not produce concave depressions or bumps.)
In spite of the presence of T erytreae, symptoms of greening disease were not seen in the Mukayras region, while across the border at Al Baida the disease was widespread. The reason is that there is very little citrus in the Mukayras region. In fact, citrus could only be seen in one farm, and even there the number of citrus plants was very small. Yet, on these few isolated citrus trees, there was abundant multiplication of T erytreae Greening being present at Al Baida, it is clear that if citrus orchards were to be developed in the Mukayras region, greening disease would soon appear.
Greening disease and T erytreae are not present in the Lawdar-Mudia area, in spite of its close proximity to the Mukayras area. The reason is that Mukayras is at an altitude of 2 100 m, which offers favourable climatic conditions for the development of T erytreae and the African heat-sensitive form of greening. In contrast, the Lawdar region is at a much lower altitude, 800 m, and the climate is probably too hot and dry for T erytreae and greening to occur.
There was no evidence of greening or T. erytreae in Jawl-Madrum, near Musaymir, on the road to Ta'izz and close to the former border with northern Yemen. There are, however, other areas in southern Yemen adjacent to the northern part of the country where greening and its vector could occur. Dhala in the south is near Qataban in the north. If Qataban turns out to be affected by the disease and its vector, Dhala might also be, unless its location is similar to that of Lawdar, i.e. at too low an altitude for the disease and its vector to survive.
Bayhan on the southern side of the former border is close to Harib on the northern side. The 1983 survey showed that there was no greening or T erytreae in Harib (or in nearby Marib). For that reason, it is likely that the Bayhan area is also unaffected.
Recommendations concerning greening in southern Yemen. Greening disease is absent from the citrus-growing regions of southern Yemen, but the African psyllid vector, T. erytreae, is present in Mukayras and perhaps in other areas close to northern Yemen where the disease and its vector occur.
Therefore the recommendations below are directed at preventing the disease and its vector reaching the Lawdar-Mudia area, the major citrus-growing region in southern
Yemen. Even though the relatively low altitude of the Lawdar-Mudia area (800 m) seems to protect it from becoming easily affected, the following recommendations are made for further security.
Stubborn-like symptoms were shown by several sweet orange trees in the Lawdar-Mudia and Say'un-Tarim areas. The symptoms were seen on Washington navel (Mudia and Lawdar nurseries), Valencia late (Al Radod orchard, Say'un) and unrecorded sweet orange trees (El Hayied orchard, Lawdar-Mudia area; Jaima orchard, Say'un area).
The presence of stubborn in southern Yemen is not surprising as countries such as Egypt and Iraq, from whence the initial citrus budwood was introduced, are known to harbour stubborn disease (Bové et al., 1984).
Infection in the south could spread through natural transmission of S. citri by leafhoppers, though nothing is known about the presence there of S. citri-vector leafhoppers such as N. haematoceps and N. tenellus. It is, however, established that leafhoppers able to transmit MLOs are present in southern Yemen, since typical symptoms of MLO-infection such as phyllody were seen on periwinkle (Catharanthus roseus) plants at the El Kod experiment centre. These plants contained MLOs as determined by electron microscopy. Whether the leafhoppers able to transmit MLOs in the south are also able to transmit S. citri remains to be seen.
At the present time, stubborn does not seem to be a major problem in southern Yemen. Caution is necessary, however, as the hot climate of the citrus-growing areas favours symptom expression of the disease. The following recommendations should be followed.
Gummy bark of sweet orange
Of all virus and virus-like diseases of citrus, gummy bark of sweet orange is probably the most conspicuous disease of citrus in southern Yemen.
The symptoms of gummy bark on sweet orange are similar to those of cachexia on mandarin. The disease was first described by Nour Eldin (1956) in Egypt on sweet orange trees grafted on sour orange rootstock. While the disease has attracted little attention in America, it is a widespread and serious disease not only in Egypt, but in many other citrus-growing countries in the Near East. The author has seen severe cases of gummy bark in the Islamic Republic of Iran, Iraq, Oman, Saudi Arabia, the Syrian Arab Republic, the Sudan and Turkey. Surveys in these countries show the disease to be much more widespread than initially thought. It was probably distributed in many countries by the introduction of citrus material from Egypt. Indeed, the sweet orange varieties on which the disease is seen are most often of Egyptian origin. In view of the many citrus introductions from Egypt into southern Yemen, it is not surprising that gummy bark is present in all the citrus-growing areas.
All the major sweet orange varieties grown in the southern region (Washington navel, Valencia late and Hamlin) are affected. In the Lawdar-Mudia area, the Lawdar and the Mudia government nurseries have distributed many trees to commercial orchards. Since sweet orange trees in these nurseries are affected by gummy bark, it is not surprising that the disease has been distributed by these nurseries all over the area. The same situation occurs in the Say'un-Tarim area: severe gummy bark affects Aboussoura navel sweet orange trees of Egyptian origin in the Jaima farm. This farm acts as a local nursery and is probably responsible for the dissemination of the disease.
Several cases or different types of gummy bark have been seen in southern Yemen (see Table 57). When the sweet orange bark is heavily impregnated with gum and the outer bark is rough or scaly (Fig. 68), scaling probably starting at the bud-union. Some trees show gummy bark symptoms only on the sweet orange scion (Figs 61, 68 and 69), others on both the scion and the rootstock (Figs 74, 75 and 77).
Only two citrus rootstocks have been used in southern Yemen: sour orange and rough lemon. Sour orange is tolerant, but rough lemon is susceptible to the gummy bark agent (Nour-Eldin, 1956, 1968, 1980). Therefore, it is very likely that the gummy bark-affected sweet orange trees without symptoms on the rootstock are grafted on sour orange, while those with symptoms are on rough lemon roots. In addition, it is known that when sweet orange trees on rough lemon are infected with the gummy bark agent, a bud-union crease is obtained. This is exactly what is observed with the gummy bark-affected sweet orange trees on symptomatic rootstocks (Figs 74, 76 and 77), suggesting that these rootstocks are indeed rough lemon.
The cases of gummy bark with heavy gum impregnation of the sweet orange bark are probably due to severe strains of the pathogen. Some strains might, however, be more severe on rough lemon than on sweet orange, as illustrated by the tree in Figures 74 and 76, where gum impregnation and pegging are more severe on the rootstock (rough lemon) bark than the sweet orange bark (Figs 75 and 77).
Finally, in southern Yemen the most conspicuous symptom of gummy bark on sweet orange is gum impregnation of the bark. Stem pitting (bark pegging) is mild to moderate on sweet orange and sometimes more severe on the rootstock (rough lemon) (Fig. 77). In several cases, the cambial face of the sweet orange bark shows moderate to severe (Fig. 71) pinholing.
As shown in Figures 67 and 72, gummy bark can be detrimental to trees, not only when they are grafted on the sensitive rough lemon and show bud-union constriction, but also when grafted on the tolerant sour orange. As discussed above, there are different strains of the gummy bark agent and, obviously, severe strains that induce heavy gum impregnation of the bark accompanied by sweet orange bark scaling can seriously affect the tree.
When gummy bark is accompanied by bark scaling, the thin bark underlying the scales can become points of entry for Phytophthora spp. (Fig. 68) which, once established, can severely affect the sensitive sweet orange bark above the bud-union as well as sensitive rootstocks, such as rough lemon, below the bud-union.
The only recommendations concerning gummy bark are:
TABLE 57 Various cases of gummy bark in sweet orange in southern Yemen
In southern Yemen, a high percentage of mandarin in all areas visited showed typical symptoms of cachexia. In the Lawdar area, affected trees were seen in the Lawdar and Mudia government nurseries, and the El Hayed orchard (where Clementine trees were affected); the Quasr Al Qubba orchard in the Say'un-Tarim area had cachexia symptoms on all Willowleaf mandarin trees; the case illustrated by Figures 52 and 53 was seen in the Ali Mohson Al Fakir orchard in the Zinjibar-Gaar area.
Since mandarin trees in the Lawdar and Mudia government nurseries are affected, the disease has probably been spread to commercial orchards by budlings propagated with budwood from the affected trees. It is well known that many old lines of sweet orange, grapefruit and lemon often carry the cachexia viroid. As these species are tolerant of the cachexia agent, they show no symptoms of the disease. Therefore, the number of citrus cultivars carrying the cachexia agent is probably much larger than the number given by the affected mandarins only.
Recommendations concerning cachexia are:
Kassala disease or bark gumming of grapefruit
A survey for citrus diseases in the Sudan revealed a new disorder of grapefruit: Kassala disease - named after the area where it was first seen - or bark gumming if one refers to the major symptom, namely gum impregnation of the grapefruit bark. Affected trees show grapefruit stem pitting in addition to bark gumming. Kassala disease is probably not due to the agents of cachexia and gummy bark, since these pathogens do not induce symptoms in grapefruit. The disease is cited here, because of the similarities in symptomatology with gummy bark and cachexia. Its viroid nature is being investigated. Only a few cases were found at the Lawdar nursery.
Scaly bark psorosis (psorosis A), concave gum and psorosis young feat symptoms
During the December 1983 and April 1987 surveys, typical psorosis young leaf symptoms were seen on many sweet orange and mandarin trees, both on budling trees in the nursery and on mature trees in the orchard.
Historically, these young leaf symptoms were first thought to be associated only with scaly bark psorosis (psorosis A) and concave gum-blind pocket. Today, it is well established that they also accompany impietratura and cristacortis. Therefore, psorosis young leaf symptoms alone, when observed on young trees, are not sufficient for identification of the disease involved.
Two forms of such symptoms are distinguishable - vein flecking, in which small, cleared spots or bands of lighter colour than the rest of the leaf are present on, and adjacent to, veins and veinlets (see Fig. 91), and a zonate or oak-leaf pattern, in which part of the leaf on each side of the midvein vaguely resembles an oak leaf. The portion of the leaf outside this pattern displays vein flecking (see Figs 92 to 97).
In California, oak-leaf pattern is thought to be specific to concave gum, but this view is not shared by other experts. Nevertheless, the presence of psorosis young leaf symptoms is indicative of either psorosis A, concave gum-blind pocket, cristacortis or impietratura. The first three diseases are characterized by trunk symptoms on mature trees: bark scaling, concave depressions and stem pitting, respectively. Impietratura causes typical fruit symptoms (gum pockets in the albedo). When such trunk or fruit symptoms are seen, it is wise to look for psorosis young leaf symptoms: their presence confirms the diagnosis. For instance, in southern Yemen, young leaf symptoms were seen in particular on adult trees with concave depressions and trees with bark scaling, thus confirming that these trunk symptoms were due to concave gum-blind pocket and scaly bark psorosis, respectively.
Psorosis young leaf symptoms can be seen only on young leaves, particularly during the spring and autumn growth flushes. They do not develop when the temperatures are too high. Also, they can be observed only for a relatively short time, since they disappear as leaves mature. These are the reasons why adult trees affected by concave gum-blind pocket or scaly bark psorosis do not always, or constantly, show psorosis young leaf symptoms. In southern Yemen, such trees, with and without these symptoms, were encountered.
Concave gum-blind pocket-affected sweet orange and mandarin trees were more numerous than trees with scaly bark psorosis. In concave gum, the concave depressions are wider than in blind pocket where the longitudinal lips or rims of the vertical depressions are closer together. The two types of concavity can often be seen on the same tree. Whether concave gum and blind pocket are different strains or different manifestations of the same virus is not yet clear. In southern Yemen, concave gum was the major form of the disease and could be seen in the following orchards of the Lawbar-Mudia area: Mudia nursery, El Hayed, M. Ali Rabbash, M.S. Al Daker and Abdullah Hosein orchards and Lawdar nursery. In the Hadramawt valley, strong psorosis young leaf symptoms were seen on young budlings in the nursery of the Jaima farm. In the M. Ali Rabbash orchard, severe concave gum symptoms were seen only on five-year-old Hamlin sweet orange trees; these trees came from the Mudia government nursery. These examples show that young nursery trees showing psorosis young leaf symptoms, and thus infected with either psorosis A, concave gum-blind pocket, cristacortis and/or impietratura, are the major means by which these diseases are spread.
Control is only possible by the use of budwood certified free of virus and virus-like diseases.
The disease is caused by any of a number of related soil-borne fungi of the genus Phytophthora, usually P. citrophthora or P. parasitica, which kill the bark. Control of this serious disease resides in the use of resistant rootstocks to prevent the fungus from attacking the susceptible mandarin, sweet orange or grapefruit scion varieties.
Sour orange is a phytophthora-resistant rootstock, and this is the major reason why the species has been used so widely as a rootstock for more than 100 years. However, the benefit of using a phytophthora-resistant rootstock is lost when the tree is budded too low, bringing the susceptible scion too close to the soil or, even worse, when the tree is planted too deep and the bud-union becomes buried in the soil. Phytophthora gummosis is also favoured when farmers put soil around the trunks and cover up the bud-union lines (Figs 224 to 226).
Cases of phytophthora gummosis are numerous in southern Yemen (see Table 58) and are often due to the bad horticultural practices mentioned above. Infection is favoured by gummy bark-induced bark cracking or scaling. Phytophthora gummosis, like all other fungal diseases, is not graft-transmissible, but it is a very serious disease, as the tree will die as soon as the bark lesions caused by the fungus have girdled the trunk.
In southern Yemen, phytophthora gummosis affects primarily sweet orange, but also grapefruit and Balady lime. Lime trees represent a special case as they are grown as seedling trees on their own roots. Allowing irrigation water to come into contact with the trunk favours development of phytophthora lesions on the susceptible lime bark and can result in the death of the tree. Infection can be prevented by planting the tree on a heap of soil.
Rio Grande gummosis
The disease was seen in the Lawdar nursery on grapefruit trees (Table 58) but seems less widespread in southern Yemen than in the Sudan or Somalia. Rio Grande gummosis is sometimes confused with phytophthora gummosis as well as scaly bark psorosis. To avoid confusion, Table 14 on p. 83 distinguishes between the symptoms of these three diseases.
TABLE 58 Virus and virus-like diseases and fungal diseases in southern Yemen
Sphaeropsis knot and witches' broom
A typical case of this fungal disorder was seen on lime trees in the Jawl Madrum area. The causal fungus, Sphaeropsis tumefaciens, can infect most citrus species but is found naturally only on lime and sweet orange trees. The fungus will live for several years in citrus tissue and is probably disseminated by pycnidiospores developed in dead tissues. The disease can damage and even kill trees of all ages.
An effective means of control is to remove the affected parts several inches beyond the innermost gall, thus removing all invaded tissue.
Boron toxicity and salt injury
Boron toxicity has been commonly observed in arid areas dependent on irrigation, such as Wadi Hadramawt. Even a very low boron content in irrigation water is sufficient to produce boron toxicity symptoms in citrus (see Figs 255 to 257). Irrigation water containing over I ppm of boron is generally considered unsuitable for use on citrus. The fact that boron is highly toxic to citrus in relatively low concentrations explains why, in the case of saline water or soils, boron toxicity symptoms are often the first manifestation of salt excess. As shown by Figure 255, in the case of boron toxicity, leaves show tip yellowing, followed by interveinal yellowing, which is more prominent at the apex. Burning (necrosis) of tips and margins occurs as injury progresses. Brownish, resinous gum spots or pustules are characteristic on the underside of leaves (not shown in Figure 255). It is generally observed that lemon, including rough lemon (see Figs 256 and 257), is more susceptible than sweet orange.
In Australia, the order of decreasing susceptibility is lemon, sour orange, mandarin, kumquat, grapefruit and sweet orange; trees of sweet orange are more affected by boron toxicity when grown on rough lemon than on sour orange. In the Islamic Republic of Iran and the Sudan, Bové observed that Balady lime (C. aurantifolia) seedling trees were much more tolerant of salt injury than sour orange seedling trees; also, trees on Balady lime showed less salt burn than trees on sour orange.
The same could be seen in Wadi Hadramawt, where rough lemon trees showed severe boron toxicity, while adjacent Balady lime seedling trees showed much less toxicity. These lime trees were, however, severely affected by mite damage and this resulted in defoliation of the upper shoots. Balady lime is also fairly drought-resistant. Salt tolerance and drought resistance explain why Balady lime has been used as a rootstock in Egypt, Iran, Iraq, Saudi Arabia and the Sudan. However, as Balady lime is very susceptible to phytophthora gummosis and tristeza virus, it is not recommended as a modern rootstock.
The commercial citrus species (sweet orange, mandarin, grapefruit and lemon) do not show symptoms of exocortis. They are symptomless carriers of the exocortis agent, a complex of various viroids. Hence, when grafted on exocortis-susceptible rootstocks such as Poncirus trifoliata, citranges, Rangpur lime, sweet lime or citron, they infect these rootstocks which, after a period of time, will show symptoms of exocortis, namely bark scaling and/or stunting. Sour orange and rough lemon are symptomless carriers of exocortis viroids and, in contrast to the above susceptible rootstocks, will not show symptoms of the disease. Therefore, exocortis infection cannot be detected by visual examination of scion-rootstock combinations such as sweet orange, mandarin or grapefruit on sour orange or rough lemon. Indexing is required to diagnose exocortis in these symptomless trees.
In southern Yemen, sour orange and rough lemon are the major rootstocks, and no symptoms of exocortis have been seen in commercial orchards. It is, however, highly probable that many sweet orange, mandarin, grapefruit and lemon cultivars carry the exocortis agent. Indeed, in citrus experiment stations where exocortis-susceptible rootstocks have been tried, exocortis disease is frequently observed in rootstock experiments in which scion varieties of unknown health status have been used.
Balady lime is very susceptible to CTV and shows specific symptoms of the disease namely, leaf vein clearing and stem pitting. Limes in southern Yemen are grown as seedling trees and, since CTV is not transmitted through the seed, seedling trees are free of the virus (as well as of most other virus and virus-like agents of citrus). When seedling lime trees show symptoms of tristeza, it means that aphid vectors of the virus have inoculated it into the trees. Several aphid species are vectors of CTV, the most efficient being Toxoptera citricida, the black tropical citrus aphid. This aphid is not present in southern Yemen, and northern Yemen, Saudi Arabia and Oman are also free of it. However, other aphid vectors of tristeza such as Aphis gossypii, the cotton aphid, occur in southern Yemen and could transmit CTV.
No evidence for insect (aphid) transmission of CTV has been seen in southern Yemen. Many Balady lime seedling trees have been observed in practically all of the citrus orchards visited. No symptoms of tristeza have been seen on these trees.
The two rootstocks used in southern Yemen are sour orange and rough lemon. Trees of sweet orange, mandarin and grapefruit on sour orange roots are susceptible to tristeza, and show decline with most strains of the virus (some very mild, rare strains do not produce decline). No declining trees on sour orange rootstock have been seen, except in 1983 in the Ahmed Ruwais orchard (Lawdar-Mudia area) where a row of seven Hamlin sweet orange trees on sour orange showed typical symptoms of quick decline of the tristeza type. These trees, however, indexed negative for CTV by ELISA when analysed in Bordeaux. The adjacent trees showed no decline and were still in a good condition in 1987. Both the declining and non-declining trees were on sour orange and showed symptoms of gummy bark.
Trees on rough lemon are tolerant of tristeza: when infected by the virus, they show no symptoms. Therefore, theoretically, the possibility remains that some trees on rough lemon could be infected. However, as there is no spread of CTV in southern Yemen, these trees have not served as sources of inoculum for aphids to become viruliferous and spread the virus, as of April 1987.
Conclusions and further recommendations
The African psyllid vector of citrus greening disease, T. erytreae, has entered the Mukayras area in the south from Al Baida in northern Yemen. Even though no symptoms of greening disease were seen in the Mukayras area, mainly because very little citrus is grown there, the disease could easily become established on the Mukayras plateau if citrus were to be developed, and from there the disease could eventually reach the Lawdar-Mudia area. The recommendations that have been made above are intended to keep the disease and its vector out of the citrus-growing areas of southern Yemen.
The major virus and virus-like diseases of citrus, the symptoms of which can be seen throughout southern Yemen (see Table 58), are gummy bark of sweet orange, cachexia of mandarin and psorosis young leaf symptoms, mainly associated with concave gum disease. Exocortis cannot be observed on the commercial trees in southern Yemen as the scions and rootstocks (sour orange or rough lemon) of these trees are symptomless carriers of the exocortis viroid(s). It is, however, probable that a high percentage of these grapefruit, sweet orange and mandarin trees carry the exocortis agent. Similarly, sweet orange and rough lemon are symptomless carriers of the cachexia viroid. It is highly likely that many of the sweet orange and grapefruit cultivars in southern Yemen are infected with the cachexia agent. The presence of exocortis or cachexia, or both, in symptomless carriers can only be determined by indexing. The indicator plant for exocortis indexing is Etrog citron 861S1 and Parson's Special mandarin for cachexia.
Many of the tristeza-tolerant rootstocks are susceptible to exocortis, cachexia or both. Such rootstocks (P. trifoliata, citranges, Rangpur lime or C. macrophylla) can only be used with cultivars free of cachexia and exocortis.
Bové, J.M. 1986. Greening in the Arabian Peninsula: toward new techniques for its detection and control. FAO Plant Prot. Bull., 34(1): 7-14.
Bové, J.M. & Garnier, M. 1984. Citrus greening and psylla vectors of the disease in the Arabian Peninsula. In Proc. 9th Conf. IOCV, p. 109-114. Riverside, Univ. Calif.
Bové, J.M., Saillard, C., Vignault, J.C. & Fos, A. 1984. Citrus stubborn disease in Iraq and Syria: correlation between symptom expression and detection of Spiroplasma citri by culture and ELISA. In Proc. 9th Conf IOCV, p. 145-152. Riverside, Univ. Calif.
Nour-Eldin, F. 1956. Phloem discoloration of sweet orange. Phytopathol., 46: 238239.
Nour-Eldin, F. 1968. Gummy bark of sweet orange. In J.F.L. Childs et al., eds. Indexing procedures for 15 virus diseases of citrus trees, p. 50-53. USDA/ARS Agriculture Handbook 333.
Nour-Eldin, F. 1980. In J.M. Bové & R. Vogel, eds. Description and illustration of virus and virus-like diseases of citrus. A collection of colour slides. Paris, IFRA SETCO-FRUITS.
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