Tristeza in the Hargeisa region
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CTV was detected in citrus material from the Hargeisa region both by ELISA on bark samples from young shoots of trees suspected of being infected with the virus, and by electron microscopy of ultra-thin sections through leaf midribs of trees suspected of having greening disease (Figs 32 and 33).
Two navel sweet orange trees (trees 3 and 4), one Jaffa sweet orange tree (tree 5) and one unidentified sweet orange tree (tree 6) that were all infected with the greening organism, were also infected with CTV. One mandarin tree (tree 1) and one additional sweet orange tree (tree 2) were also infected with CTV; they were not tested for greening, but it is likely that they carried the disease. The case of the Osman Ashour Hasan orchard (trees 6 and 7) is significant. This orchard contained many sweet orange trees with greening symptoms, and the greening organism was detected in one tested tree (tree 6). This tree was also infected with CTV and it is probable that all the trees infected with greening were also infected with CTV. In the same orchard, a small-fruited acid lime (C. aurantifolia) (tree 7) had severe greening-like leaf mottle symptoms and, in addition, mild stem pitting. ELISA showed this tree to be CTV positive. On the basis of leaf mottle and ELISA, this tree could be infected by both greening and CTV. Many other lime trees have been observed in various orchards in the Hargeisa region, but no symptoms of tristeza could be seen on these trees.
Tristeza has been reported in Ethiopia and more particularly in the Dire Dawa region, I 00 km west of Hargeisa (Schwarz, 1976; Dereje et al., 1977). The most efficient aphid vector of CTV, T. citricida, is reported as the most common aphid on citrus in Ethiopia (Crowe and Kamal, 1979). If so, the presence of T. citricida in the Hargeisa region is to be expected, even though no evidence of it was seen during the survey. It should not be confused with Toxoptera aurantii (see the drawings on p. 36). A. gossypii is another vector of CTV. Its presence in the Mogadishu area is well established but whether it occurs in the Hargeisa region is not known.
The rootstock used in the Hargeisa region would appear to be rough lemon, even though no records are kept by the farmers. Sweet orange trees on rough lemon are tolerant of CTV, and only indexing on acid lime seedlings and ELISA are able to detect the virus in these trees. It is likely that there are many more such infected, symptomless trees in the Hargeisa region.
Other virus and virus-like diseases
Scaly bark psorosis
Scaly bark psorosis, or psorosis A, is a graft-transmissible, virus-like disease. Symptoms of it (see Figs 98 to 100) were seen on Jaffa sweet orange trees in the Hadj Ali orchard (Horo-Hadley area). These trees are grafted on rough lemon rootstock and also show bud-union crease (see below).
Concave depressions typical of concave gum were seen on the trunks of navel sweet orange trees and mandarin trees on rough lemon rootstock.
Jaffa sweet orange trees grafted on rough lemon often show bud-union crease, a sign of incompatibility between the rootstock and the scion. In certain cases it has been shown that bud-union crease is a graft-transmissible disease. Symptoms of it have been seen in many orchards of the Hargeisa region (Fig. 134). Practically all Jaffa sweet orange trees on rough lemon that were seen showed bud-union crease.
Stubborn-like symptoms, including bushy growth, off-season flowering and navel closure, were seen on navel sweet orange in the Awbarkadle area.
TABLE 48 Diseases observed in Somalia on citrus in October-November 1986
|Virus and virus-like diseases|
|Scaly bark psorosis||+|
|Diseases due to phloem-restricted prokaryotes|
|Rio Grande gummosis||+ + +||+|
Several cases of footrot due to poor cultural practices were observed on mandarin and sweet orange trees on rough lemon (Awbarkadle area), on acid lime (Horo-Hadley area) and on Jaffa sweet orange on rough lemon (Malukta area).
Rio Grande gummosis
Severe Rio Grande gummosis with abundant gum exudations was seen on Jaffa sweet orange (Malukta and Horo-Hadley areas).
Figure 255 shows typical symptoms of salt toxicity or leaf burn on sweet orange leaves. This is not surprising as the irrigation water often has a high chloride content, sometimes reaching 700 mg/l.
Salt burn was seen in many orchards in all the areas visited. In the Malukta area, rough lemon seedlings in the nursery showed severe salt toxicity symptoms.
Severe infestations of scales (Coccus spp.) on navel sweet orange fruit and twigs have been seen in the Awbarkadle area. This scale problem was even more important in 1983. Coccus hesperidum (soft brown scale) and Coccus viridis (soft green scale) have been reported in Somalia. Control may be obtained by spraying with oil emulsion or malathion. Note that parathion not only does not control soft scale but also destroys the parasites that exert some biological control over it. Chalcid wasps are known to control Coccus spp. in Somalia. Severe infestations of cottony cushion scales (Icerya aegyptiaca) (Homoptera, Margarodidae) have been seen in the Dararwegne area.
Fruit damage due to fruit-flies was mentioned in connection with several orchards, where crop losses as high as 50 percent have been observed. Ceratitis capitata, the Mediterranean fruit-fly, is believed to be involved.
Conclusions and recommendations
Diseases present in Somalia
Table 48 shows the diseases observed in Somalia on citrus during the survey (October-November 1986). As may be seen, the major diseases in the Mogadishu region are Rio Grande gummosis, phytophthora footrot and cachexia-xyloporosis. In the Hargeisa region, greening and tristeza are of paramount importance, but salt toxicity and phytophthora footrot are important too.
Need for certified budwood
In spite of several introductions of budwood in 1966, 1969 and 1978, some apparently free of virus and virus-like diseases, many symptoms of such diseases could still be seen in the Somali orchards, especially on sweet orange and mandarin.
The Genale nursery has begun to release grapefruit trees propagated from the seven grapefruit varieties (Marsh seedless, David seedless, Little River, Thompson, Redblush, Ruby, Shambar) certified free of virus and virus-like diseases, and introduced in 1981-82 from the French Citrus Experiment Station at San Ginliano, Corsica.
Cultivars of sweet orange and mandarin, certified free of virus and virus-like diseases, must also be reintroduced from reliable sources.
Introduction of plant material from countries that cannot guarantee the quality of their material should be prevented. In particular, no citrus plant material should be introduced from the countries in Table 49, because of the presence of the diseases and their vectors as indicated.
Recommendations concerning greening and tristeza in the Hargeisa region
Greening and tristeza are the two most important graft-transmissible diseases of citrus found in Somalia. They occur in the Hargeisa region but not in the Mogadishu region. They are transmitted by insect vectors, the psyllid T. erytreae for greening, and aphids T. citricida, A. gossypii, etc. for tristeza.
An extensive survey based on ELISA detection of the virus must be carried out for tristeza in order to determine the exact extent of the disease. Infected trees must be eradicated if at all possible. It must be remembered that trees on rough lemon rootstock show no symptoms of tristeza as they are tolerant of CTV.
TABLE 49 Presence of diseases and vectors by country
|Oman||Witches' broom disease of lime||Not identified|
|Saudi Arabia||Greening||D. citri|
|United Arab Emirates||Witches' broom disease of lime||Not identified|
A similar survey must be carried out for greening. It seems likely that trees infected with CTV are also infected with the greening organism. Thus, eradication of tristeza-infected trees would also remove many greening-affected trees.
Even though no evidence of T. erytreae, the psyllid vector of greening, was found, further surveys are necessary to evaluate the vector status. Also, the presence of T. citricida, the aphid vector of CTV, must be confirmed. This aphid should not be confused with T. aurantii (see the drawings on p. 36).
Finally, no plant material (except fruit) must be moved out of the Hargeisa area. This is to prevent spread of tristeza and greening to other parts of Somalia.
Chapot, H. 1970. The possibilities of improving and developing fruit crops, with particular reference to citrus. Addis Ababa, Inst. Agric. Research.
Childs, J.F.L. 1953. An actinomycete associated with gummosis disease of grapefruit trees. Phytopathol., 43: 101 - 103.
Crowe, T.J. & Kamal, A. 1979. A checklist of aphids recorded from Ethiopia (Homoptera: Aphididae). Inst. Agric. Res. [Addis Ababa] Entomol. Bull., 3.
Dereje, A., Alemu, M., Niemann, E., Lemma, K., Van Bruggen, A.H.C. & Gebre, S.K. 1977. A report on a preliminary phytopathological survey of citrus and pepper plantations. Addis Ababa, State Farms Development Authority.
Rossetti, V. & Salibe, A.A. 1965. Incidence of different types of psorosis in citrus varieties in the State of Sao Paulo. In Proc. 3rd Conf: IOCV, p. 150-153. Gainesville, Univ. Fla. Press.
Schmutterer, H. 1971. Contribution to the knowledge of the crop pest fauna in Ethiopia. Z. Angew. Entomol., 67: 371 389.
Schwarz, R.E. 1976. Citrus greening in Ethiopia. Technical Report for UNDP/ FAO Project ETH/74/002. Addis Ababa, Inst. Agric. Research.
SOGREAH. (n.d.) Report on the North-West Region Agricultural Development Project. Grenoble, France, SOGREAH, Ing. Conseils.
Van Bruggen, A.H.C. & Almaz Yilma. 1985. Virus and virus-like diseases of citrus in Ethiopia. FAO Plant Prot. Bull., 33(1): 2-12.
Chapter 20: The Sudan
Major varieties and rootstocks
Conclusions and recommendations
The first report on citrus trees in the Sudan dates back to 1896 (see Map 18). Several sweet orange and grapefruit varieties as well as other citrus species (mandarin, lime, etc.) have been imported subsequently, as shown in Table 50.
These introductions, except those between 1967 and 1970 from California, were mostly old lines, whose virus status was unknown at the time of importation. It is, however, very likely that the plant material introduced from Egypt and the country then known as Palestine was infected with several pathogens, namely those known today to have been present in these countries in the 1930s and 1940s (cachexia, psorosis, exocortis, gummy bark, etc.). It should also be noted that sweet orange introductions were made from Kenya and Rhodesia (now Zimbabwe), where the citrus is known to be infected with CTV and the greening bacterium. Hence, infected trees of Kenyan or Rhodesian origin might have been propagated in the Sudan.
Thus the known history leads one to expect the presence of infectious diseases of citrus in the Sudan.
Major varieties and rootstocks
The Sudan grows mostly the following species and varieties: Balady (local) small-fruited acid lime (Citrus aurantifolia), mainly Foster pink but also Marsh seedless grapefruits, Valencia-like and Balady sweet oranges and Balady
(Willowleaf) mandarins. Sour orange is the major rootstock. However, in old plantings other rootstocks have been used: Balady lime, rough lemon, Adalia lemon, sweet lemon and citron. In general, citrus growers do not know on which rootstock their trees are growing. The use of acid lime (C. aurantifolia) as rootstock was imported from Egypt, and the use of sweet lime probably came from Palestine. For these reasons, "Old plantings of citrus orchards in Northern Province are therefore combinations of a range of citrus varietal groups introduced from several places and worked on a number of rootstock varieties" (Khairy, Mahgoub and El Hage, 1969), a statement equally applicable to the other major citrus areas of the Sudan.
Table 51 lists the infectious diseases of citrus that have been diagnosed in the various citrus-growing provinces of the Sudan, except the southern provinces. Table 52 indicates the citrus species and varieties found to be affected.
Virus and virus-like diseases
Cachexia. Figures 42, 43 and 46 to 49 illustrate typical and severe symptoms of cachexia on Balady (Willowleaf) mandarin trees on sour orange rootstock in the Sudan: stunting and yellowing of the leaves (Fig. 46) and gum impregnation of the bark (Figs 42, 43, 48 and 49). The disease affects a high percentage of the Balady mandarin trees- probably more than half. All citrus-growing areas are affected (see Table 51). Symptoms are often severe with stem pitting and bark pegging (Fig. 43) and abundant bark gumming extending high above bud-union (Figs 42 and 49). In very severe cases, bark cracking is observed (Fig. 47).
MAP 18 The Sudan
TABLE 50 Citrus introductions in the Sudan
|Citrus||Location||Year of introduction||Imported from:|
|Sweet orange and limes||Dongola||1896||INA1|
|Balady white grapefruit||Merowe||1904||USA|
|Khalily (red and white)||1930s||Egypt|
|Lue Gim Gong||"||"|
|More recent introductions|
|Many species and varieties||Shendi||1967-1970||California³|
1 Information not available.
2 Grafted on acid lime rootstock.
3 From Willits and Newcomb nurseries
TABLE 51 Geographical distribution of infectious diseases of citrus in the Sudan
|Disease||Khartoum Province||Kassala Province||Northern Province||Gezira Province||Darfur Province|
|Gummy bark||(l) (3)||(3)||(3)|
|Bark gumming (Kassala disease)||(3)||(3)||(3)||(3)|
|Psorosis young leaf symptoms||(1)||(1)|
|Concave gum-blind pocket||(1)||(1)||(1)||(1)(3)|
|Scaly bark psorosis||(1)||(1)||(1)|
|Rio Grande gummosis||(1)||(1)||(1)(2)(3)||(1)||(1)(3)|
(1) The disease was seen by Childs, 1964.
(2) The disease was seen by Krezdorn, 1983.
(3) The disease was seen by Bové. 1986.
Sweet orange and grapefruit are important symptomless carriers of cachexia. Infection of these varieties is revealed when they are grafted on susceptible rootstocks such as Citrus macrophylla, Rangpur lime or sweet lime. Such a situation has been observed by Childs (1964) in Shendi (north of Khartoum) in the case of a Valencia sweet orange tree grafted on sweet lime (see Table 52) and by Krezdorn (1983) at the Horticultural Research Station in Hudeiba in the case of Foster grapefruit trees on C. macrophylla and Rangpur lime (see Table 52). These observations show that not only the symptomatic Balady mandarin, but also the tolerant, symptom-less Valencia sweet orange and Foster grapefruit lines carry the cachexia agent. Probably many other sweet orange and grapefruit lines carry the cachexia viroid, but demonstration of this would require indexing.
The same is also true for exocortis, as noted below.
Gummy bark. Figures 60 to 79 illustrate the symptoms of gummy bark on sweet orange rootstock. These symptoms are similar to those of cachexia on mandarin. The disease was first described by Nour-Eldin in 1956 in Egypt (see Chapter 10), on sweet orange trees grafted on sour orange rootstock. While the disease has drawn little attention in America, it is widespread and serious not only in Egypt, but in many other citrus-growing countries in the Near East. Bové has seen severe cases of gummy bark in the Islamic Republic of Iran, Iraq, Oman, Saudi Arabia, the Syrian Arab Republic, Turkey and southern Yemen. Surveys in these countries show the disease to be much more widespread than initially thought. It was probably distributed throughout 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 to the Sudan, it is not surprising that gummy bark is probably present in all the citrus-growing areas of the country. Bové saw severe cases of it in the three areas visited: Kassala, Atbara (Northern Province) and Nyala-Zalingei (Darfur Province) (see Table 51) and more particularly on Balady navel and Nouri sweet oranges (see Table 52). Childs (1964) has mentioned the disease on Balady and Gebeit sweet orange trees (see Table 52).
TABLE 52 Citrus species and varieties affected by infectious diseases in the Sudan
The expression of gummy bark symptoms on sweet orange like that of cachexia on mandarin is probably independent of the rootstock used to grow the sweet orange scion. Sour orange is the major rootstock used in the countries where gummy bark occurs and, therefore, the disease is most often seen on sweet orange trees grafted on sour orange. In mild cases, the gum streaks are not very numerous and affect the bark only in the vicinity of the bud-union. In severe cases, gumming is abundant and extends high above bud-union (see Fig. 66), and may be responsible for bark scaling (see Figs 68 and 71).
Kassala disease, or bark gumming of grapefruit. This new disease was discovered by the author on Foster grapefruit trees in Kassala. While tristeza and cristacortis are able to induce stem pitting in grapefruit, they never result in the production of streaks of gum in the grapefruit bark. He was, therefore, quite surprised to find a grapefruit tree with gum impregnations in the bark - the tree also showed relatively mild stem pitting. The first-such case was observed in Kassala, but later numerous cases were also seen in Khartoum, Atbara, Nyala and Zalingei, not only on Foster, but also Marsh seedless grapefruit trees.
The symptoms resemble those of cachexia on mandarin or of gummy bark on sweet orange. However, the amount of gum in the bark or the number of gum streaks seems to be smaller, even though bark gumming can extend high above bud-union (Figs 80 to 82). In some cases, the pegs on the cambial side of the bark have rounded tips; in more severe cases they are more pronounced and sharper.
When sour orange is the rootstock of an affected Foster grapefruit tree, there seems to be no bark gumming or stem pitting in the sour orange. In the case of a Marsh seedless grapefruit tree on a rootstock, according to the farmer, either of sour orange or of Balady lime, bark gumming affected only the grapefruit scion bark, but stem pitting was present on both the scion and the rootstock (Fig. 82). This indicates that, perhaps, Balady lime was the rootstock and that it is susceptible to Kassala disease of grapefruit.
Bark gumming of grapefruit is probably not due to the agent of cachexia or that of gummy bark, since the agents of these two diseases do not induce symptoms on grapefruit. Tristeza does not seem to be involved, since CTV could not be detected by ELISA in two of the Foster grapefruit trees showing bark gumming in Kassala. Also, in the case of grapefruit trees with Kassala disease grafted on sour orange rootstock, the trees did not show the type of decline associated with CTV.
The two symptoms of Kassala disease, i.e. bark gumming and stem pitting, were always observed on grapefruit trees that were 20 years old. In Kassala, 13-year-old Foster grapefruit trees showed only stem pitting. They were propagated from Foster grapefruit trees now 20 years old, which showed both bark gumming and stem pitting. This observation indicates that stem pitting may be an earlier symptom than bark gumming. In this respect, Childs (1964) noticed, in the Rest House Garden in Kassala, two grapefruit trees with fairly strong wood pitting. He suggested that this symptom could result from CTV infection. As Bové found no evidence of tristeza in the Kassala area, the symptom observed by Childs might have been due to Kassala disease.
Cachexia of mandarin and gummy bark of sweet orange are graft-transmissible diseases. In view of the similarities between the symptoms of these two diseases and those of bark gumming of grapefruit, the latter is probably also due to a graft-transmissible agent, but proof of this must await completion of graft-transmission experiments. The possibility that gummy bark of sweet orange and bark gumming (Kassala disease) of grapefruit could be of a viroid nature is under investigation.
Scaly bark psorosis (psorosis A). This is a classical disease (see Figs 98 to 100) in California, Florida, Morocco, etc. but it seems to be less of a problem in the Sudan. Childs (1964) saw a few cases of it, and some of these trees also showed psorosis young leaf symptoms, thus confirming the psorosis nature of the bark scaling syndrome. Accurate diagnosis of scaly bark psorosis is not always easy, as Rio Grande gummosis and, to a lesser degree, phytophthora gummosis also result in bark scaling, as noted below.
Popcorn. The name refers to numerous small pustules which erupt on the bark of the trunk of sweet orange trees (see Fig. 101). Small scales of the outer bark loosen, break away and finally drop (Rossetti and Salibe, 1965). This disorder has been observed in several citrus areas of the world, including the Sudan (Childs, 1964). It is sometimes associated with scaly bark psorosis, even though nothing is known about the aetiology and pathology of the disorder. As shown by Tables 51 and 52, Balady and Gebeit sweet orange trees in three of the citrus-growing provinces showed symptoms of the affliction.
Exocortis. Commercial citrus species and varieties do not show symptoms of exocortis, as they are symptomless carriers of the exocortis agent, a complex of various viroids. Hence, when grafted on susceptible rootstocks such as Poncirus trifoliata, citranges, Rangpur lime, sweet lime and citron, they infect these rootstocks which, after a period of time, will show symptoms of exocortis: bark scaling (see Figs 83, 85 to 87), stunting or both. Sour orange is a symptomless carrier of the exocortis viroids and so 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. Indexing (see Fig. 90) is required to diagnose exocortis in these symptomless trees.
In the Sudan, sour orange is the major rootstock and no symptoms of exocortis have been seen in commercial orchards except, perhaps, in one case, a white Marsh grapefruit tree on citron, severely stunted and showing exocortis type bark scaling on the rootstock (see Table 52) (Childs, 1964). In citrus experiment stations where rootstocks other than sour orange are tested, exocortis disease is frequently observed in rootstock experiments in which scion varieties of unknown health status have been used. This is, for instance, the case in the rootstock trial at the Hudeiba Horticultural Research Station, where a Foster grapefruit line was grafted on various rootstocks, including Rangpur lime and Citrus macrophylla. The trees on Rangpur lime were stunted and the rootstock showed exocortis-type bark scaling (Krezdorn, 1983). This Foster grapefruit line also carried cachexia, as witnessed by cachexia symptoms not only on Rangpur lime but also C. macrophylla rootstocks (see Table 52). Another example is the government orchard of the Agricultural Research Corporation at Nyertete (Darfur Province), where Foster grapefruit trees on Carrizo and Savage citranges were severely stunted (see Table 52).
These examples show that selection based only on visual examination is totally inadequate as a means of establishing the health status of citrus trees: good-looking, symptomless trees may be symptom-less carriers of several pathogens such as exocortis and cachexia. Only indexing can reveal the true health status in such cases.
The importance of these considerations is related to the problem of tristeza. Control of tristeza implies the replacement of the sour orange rootstock by tristeza-tolerant rootstocks, such as P. trifoliata, citranges, Rangpur lime or sweet orange. As indicated above, some of these are susceptible to exocortis, cachexia or both. Citrus lines to be budded on these rootstocks must be free of exocortis, cachexia and other pathogens, and must therefore be indexed to determine their true health status.
Stubborn. Childs (1964) mentions stubborn disease in all the citrus areas of the Sudan that he surveyed (see Table 51). He also refers to "greening" symptoms. In those days, the respective agents of stubborn and greening were not yet known, and the two conditions were often thought to be closely related. Today it is well known that the agent of stubborn is the helical mollicute, Spiroplasma citri (Saglio et al., 1973), for which Koch's postulates have been fulfilled. In the case of greening, a bacterium of the Gram-negative type, not a mollicute [mycoplasma], has been found to be associated with the disease (Garnier, Danel and Bové, 1984); Koch's postulates have not yet (1990) been fulfilled.
Bové observed typical symptoms of stubborn on Foster grapefruit trees in the Kassala area, bearing not only small, cupped leaves with mottle and zinc-deficiency symptoms, but also small, lopsided fruits with blue albedo (see Fig. 169) and aborted seeds. Blue albedo is a characteristic internal fruit symptom of stubborn, particularly in abnormally small fruits, as is the case here.
In a private orchard in Nyertete, stubborn-like symptoms were seen on a navel tree. The tree was, however, affected by phytophthora gummosis and this is probably the reason for the stubborn-like symptoms.
S. citri is transmitted in nature by leafhopper vectors. The major vector in the Mediterranean area and the Near East, an area extending from the Atlantic coast of Morocco to Afghanistan, is Neoaliturus haematoceps, a leafhopper not present in the Americas. Neoaliturus tenellus, a related species, is the major vector in North America. Nothing is known about these species in the Sudan. They are, however, present in Egypt and could very well occur in the Sudan. Interestingly, at Kassala airfield, Bové found that most of the ornamental periwinkle (Catharanthus roseus) plants showed severe phyllody symptoms. Electron microscopy confirmed the presence of MLOs in these plants. As infection of periwinkle plants by MLO is through leafhopper vectors, the Kassala periwinkles demonstrate that leafhopper species able to transmit MLOs are present in the area. Whether they include N. haematoceps and N. tenellus remains to be determined.
Impietratura. Impietratura disease affects grapefruit trees and results in the presence of gum pockets in the albedo (see Figs 116 and 117). Impietratura-like symptoms have been seen in the albedo of a Foster grapefruit but they were not conspicuous enough to allow unambiguous diagnosis. Indexing is required for accurate determination of the disorder.
Cristacortis. Deep stem pitting, with pronounced pegs on the cambial face of the bark, is typical of cristacortis (see Figs 109 to 1 15). A few such pegs have been seen on a Marsh seedless grapefruit scion in the Kassala area. However, there was, in addition, a milder stem pitting, suggesting early expression of Kassala disease, especially since a line of gum was present at the bud-union. Indexing is required for precise diagnosis.
Woody gall-vein enation. This disease (see Figs 130 and 131) is characterized by the development of galls on rough lemon, Balady lime and Citrus volkameriana rootstocks. On certain species such as Balady lime, sour orange and rough lemon, the virus induces leaf vein enations. Three aphid species transmit the virus: Toxoptera citricida, Myzus persicae and Aphis gossypii.
Childs (1964) saw galls resembling those of woody gall in Balady sweet orange trees (at Merowe, Gureir and Nyala). He did not specify the rootstocks on which these trees were growing. However, since Balady lime is used as a rootstock in the Sudan, the possibility exists that the galls observed by Childs were on Balady lime rootstocks and, if so, they might be due to the woody gall virus.
Phytophthora gummosis or footrot. This disease is caused by a soil fungus (Phytophthora citrophthora, Phytophthora parasitica or related species) that kills the bark. This very serious disease is controlled by using 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 this species has been used so widely as a root stock for more than a century in many parts of the world. The benefit of using a phytophthora-resistant rootstock is however lost when the tree is budded too low bringing the phytophthora-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. Finally, severe forms of gummy bark are associated with bark cracking and scaling. These outer bark lesions may become points of entry for the fungus, especially when, in addition, the bud-union line is close to the soil.
Cases of phytophthora gummosis are numerous in the Sudan and are invariably due to the inadequate horticultural practices mentioned above. 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 the Sudan, phytophthora gummosis affects sweet orange, 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 footrot lesions on the susceptible lime bark and can result in the death of the tree.
Rio Grande gummosis. Figures 236 to 247 show typical symptoms of Rio Grande gummosis. The disease exists in all citrus areas of the Sudan (see Table 51) and affects grapefruit, including Foster, the major variety, and sweet orange (see Table 52). Childs (1964) also reports cases on Balady mandarin, pomelo and Balady lime. Krezdorn (1983) was impressed by the prevalence of the disease in the Sudan. Bové saw typical and severe cases of it during his survey in the Sudan in November 1986, immediately after his visit to Somalia. In the Mogadishu area of Somalia, Rio Grande gummosis is the most important of all diseases of citrus (see Chapter 19). In the Sudan, the situation seems less severe.
On grapefruit and orange trees, the symptoms appear high up the trunk and out on the larger branches. They are expressed as profuse gum production (see Figs 236 to 240). The gum oozes out of vertical cracks in the bark (Fig. 244) and runs down along the trunk or hangs down from the branches, in stalactite manner. At the time of initial gumming there is no scaling of the bark at the sites where the bark is split. However, the first stage in the healing-over process is the sloughing of thin scales of dead outer bark. Then follows the development of scar tissue generated by the bark. Repair is only temporary and healed-over lesions may again start gumming and enlarging. In this way, lesions may pass through repeated cycles of recovery and relapse, in the course of which they progressively enlarge and expose more and more wood. In old, inactive lesions the wood is exposed (see Fig. 240). The gum pockets may be located deep in the wood (Fig. 245), and the gum travels considerable distances in and along the wood, so that gum pockets may exist far removed from the nearest active, gum-producing lesion.
The bark scaling associated with the healing-over process and the sloughing of scales of dead outer bark can be pronounced but should not be confused with scaly bark psorosis or popcorn symptoms. Rio Grande gummosis should not be confused either with phytophthora gummosis or footrot. Table 14 on p. 83 helps to distinguish between Rio Grande gummosis, scaly bark psorosis and phytophthora gummosis:
Greasy spot. Childs (1964) observed greasy spot sometimes causing considerable defoliation of sweet orange (Darfur Province), grapefruit (Darfur and Blue Nile Provinces) and Balady lime (Blue Nile Province). Early symptoms appear as a slight blistering on the underside of the leaves. The blistered area becomes first pale yellow, then pale orange and later turns brown or black, suggesting a spot of grease. The causal agent of greasy spot is the fungus Mycosphaerella citri Whiteside.
In mesophyll collapse the cells of the soft interior tissues of the leaves collapse. Affected areas are irregular in size and shape, but are frequently bounded by the midrib and main lateral veins. When held up to the light the affected areas appear translucent. Frequently part of the affected area will die and become tan-coloured.
Mesophyll collapse may result when the leaves lose water faster than the tree can supply it. Injury by citrus red mites, rust mites, dry winds, drought, heat damage and impairment of the root system, are among the contributory factors (Pratt, 1958). However, the disease probably starts as a physiological or nutritional imbalance.
Childs (1964) observed considerable mesophyll collapse on sweet orange trees in the Khartoum and Darfur provinces.
Salt injury (see Figs 255 to 257), or salt burn, has been observed in many orchards of grapefruit or sweet orange trees in the various citrus-growing areas of the Sudan, but especially in the Northern Province. Trees on sour orange show much more salt injury than those on Balady lime (C. aurantifolia) rootstock and the symptoms increase in severity with the age of the trees. That sour orange is more susceptible to salt injury than Balady lime is not only true when these species are used as rootstocks, but also in the case of seedling trees: seedling trees of sour orange are much more severely affected than seedling trees of lime. Balady lime is also more drought-resistant. Hence, salt tolerance and drought resistance explain why Balady lime has been used as a rootstock in Egypt, the Islamic Republic of Iran, Iraq, Saudi Arabia and the Sudan. Balady lime being, however, very susceptible to phytophthora gummosis, this species has been used as a rootstock primarily in light soils. It is also very susceptible to tristeza, and is not to be recommended as a modern rootstock.
Figure 259 shows bark cracking on the main branches of a Bearss lime tree; Foster grapefruit trees are also affected. Such longitudinal growth cracks are normal in a vigorously growing tree. However, in the case of Persian (Tahiti, Bearss) lime, certain trees show longitudinal cracks with sunken areas in the bark of trunk and branches and, in addition, their leaves show blotching and their fruits have chimera-like longitudinal sectors. This syndrome is called wood pocket or leaf blotch of Tahiti lime in Florida. In California, lemons also show wood pocket. Wood pocket of lemon in California and wood pocket leaf blotch of Persian lime in Florida are probably not infectious - they are of genetic origin. However, a disease of some Tahiti lime selections in Brazil has bark symptoms similar to wood pocket and has been shown to be caused by the agent of exocortis (Salibe and Moreira, 1965). Hence, these observations indicate that perhaps two different diseases are involved; one of genetic origin and another caused by the exocortis viroid(s).
From the above discussion, it follows that the cause of the bark cracking of the Bearss lime trees illustrated in Figure 259 can only be determined by experimentation, including indexing for exocortis.
Bové saw no evidence for the presence of greening disease and its African insect vector, the psyllid Trioza erytreae, in the Kassala, Atbara and Nyala-Zalingei regions. The disease is, however, present in neighbouring Ethiopia and Kenya.
Table 53 indicates the average maximum and minimum daily temperatures for each month in various locations in Ethiopia, Kenya and the Sudan. It is evident that the temperatures for various regions of the Sudan (Atbara, Dongola, El Fasher, Juba, Kassala, Khartoum) are far higher than those of regions in Ethiopia (Addis Ababa, Asmara) or Kenya (Nairobi) where greening disease and T. erytreae exist. The cooler climate in these regions of Ethiopia and Kenya is due to their relatively high elevation. The cool climate of the highlands of Ethiopia and Kenya is favourable to the multiplication of the psyllid and to the symptom expression of the disease. The climate of the Sudan is unfavourable.
TABLE 53 Average maximum and minimum daily temperature (°C)
Map 17 on p. 296 shows the greening-affected regions of Ethiopia and Somalia. Comparison of the region of Elaboret in Ethiopia (area 11 on Map 17) with that of Kassala (area 17 on Map 17) in the Sudan is instructive. Elaboret, at an altitude of 1600 m, is affected by the presence of greening and its vector, while Kassala, less than 150 km away, but at an altitude of only 529 m, is unaffected.
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