Major diseases of citrus in Asia

9 Major Major diseases of citrus in Asia Citrus greening Citrus greening is one of the most devastating diseases of citrus in Asia. Citrus greening was first identified in South Africa fifty years ago. It is now found all over the tropical and subtropical countries of Asia. In the Philippines, citrus greening is the main reason why citrus production fell by 60% between 1961 and 1970. In Vietnam, up to 90% of the citrus trees in some areas are believed to be infected with citrus greening. by citrus psyllids Citrus greening is transmitted by the citrus psyllid, a small insect that sucks the sap from trees. Psyllids are not highly efficient vectors of greening. Epidemics of the disease occur only when pysyllid populations are high (i.e. when there is a lot of new shoot growth), and when a high proportion of the psyllids are carrying the greening organism. The greening agent is vectored primarily by adult insects, although late-stage nymphs were found to be infective under laboratory conditions. by vegetative propagation Citrus greening is also transmitted by the vegetative propagation of cuttings and suckers from infected trees. In their early stages, greening disease and virus diseases may have few or no visible symptoms. Many of the trees used as mother stock in Asia are infected, and as a result, many of the seedlings sold in plant nurseries are infected too. of greening via infected budwood plays an important role in disease spread. (the organism which causes the disease) is a bacterium, Liberobacter asiaticum. The bacteria cannot be cultured, and so are known as fastidious bacteria. They take the form of rigid rods, but are too small to be seen through an ordinary microscope. They can be seen only through an electron microscope. of citrus greening The Asian greening organism produces symptoms in either warm temperatures (27-32 o C) or a cool climate, and is classified as a heat-tolerant form. (In contrast, the South Africa greening organism belongs to a heat-sensitive form. are most severe when the temperature is only 22-24 o C). The greening agent can infect most citrus species, cultivars and hybrids. Most mandarins, sweet oranges and mandarin hybrids are severely affected. Pummelo was formerly thought to be resistant, but infected pummelo trees have been found in Taiwan since 1970. In recent years, pummelo trees grown in the Philippines, Malaysia, Vietnam and 56

Southern China have also been found to be infected. Most greening organisms isolated from mandarin trees produce severe greening symptoms in mandarin and sweet orange trees, but only mild symptoms in pummelo. However, a few isolates cause severe symptoms in both mandarin and pummelo. The pummelo isolate causes severe symptoms in pummelo, and also in mandarin and sweet orange. of the tree shaded side (hence the name "greening disease"). As well as citrus trees, citrus psyllids can live and feed on a few other plant species. These are Jasmine orange (Murraya paniculata), woody apple (Lemonia acidissima), Chinese box orange (Severinia buxifolia) and curly leaf (Murraya euchrestifolia). However of these alternate hosts for psyllids, only one species, box orange, can be infected with the greening pathogen. Diagnosis and detection Greening is tentatively identified in the field by symptoms in the foliage and fruit. Further diagnostic tests are carried out in the laboratory. Trees affected with greening become stunted and bear multiple off-season flowers and leaves, most of which fall off. Shoots are yellow (hence the Chinese name of "Huang-lungpin", or "yellow shoot"). moves slowly through citrus trees. In the early stage of infection, it tends to remain confined to the localized branches into which it has been introduced by the psyllid vector. Later, the symptoms spread slowly through the tree. There is dieback of twigs, the decay of feeder rootlets and lateral roots, a decline in vigor, and ultimately the death of the entire plant. Fig. 9-1. Leaf symptoms of pummelo with greening disease (left), showing yellowing and mottling of leaves and vein corking, compared to a healthy leaf (right) of the leaf Common symptoms are yellowing of the veins and adjacent tissues, followed by yellowing or mottling of the entire leaf, occasionally with corking of the veins. Diseased leaves become hardened and curl outward, while young leaves developed after premature defoliation are small and slender, with symptoms of zinc deficiency (Fig. 9-1). of the fruit The fruit of infected trees are small and irregularly shaped (Fig. 9-2). They taste bitter, with a higher acid and a lower sugar content. They do not color properly, remaining green on the Fig. 9-2. The twig and fruit on the left come from a tree with greening disease. The diseased leaves are yellow, and the diseased fruit is small and pale green in color. A healthy green leaf and normal large fruit are shown on the right. 57

VIRUS DISEASES About viruses Fig. 9-3. Tree with stem-pitting strain of tristeza virus, showing dieback and poor fruit-set Fig. 9-4. of stem pitting from citrus tristeza virus A citrus virus is a tiny organism that can multiply only when it is inside a living cell. Usually, this is the cell of a citrus plant, but it may be able to multiply inside the body of an aphid or some other vector. A virus which can multiply inside the body of a vector insect is called "persistent". Prevention is the only way of controlling plant viruses. Virus diseases of plants are incurable. Once a plant is infected, it remains infected until it dies. Any cuttings taken from an infected tree will also be infected. However, virus infection is not usually transmitted through the seed, so rootstock grown from seed should be free of virus. Some viruses infect only citrus trees. Others may infect a wide range of other plant species as well. Virus diseases may infect citrus trees for months or years before any visible symptoms appear. In other cases, the symptoms may appear soon and progress quickly. Different strains of virus differ in their symptoms, and their disease virulence. Sometimes, the only symptom is a reduction in yield. Fig. 9-5. Yellow spots, a symptom of stem pitting disease caused by citrus tristeza virus on Iyo orange (a Japanese cultivar) 58

Citrus tristeza virus Citrus tristeza virus (CTV) seems have originated in China many years ago. Tristeza (known as "quick decline" in the United States) is the most destructive disease of citrus in North and South America, although it has a world-wide distribution. Less than two decades after tristeza was introduced from Africa into South America in the 1920s, the disease wiped out the citrus industries of Argentina, Brazil, and Uruguay. The same virus also causes Hasaku Dwarf, a serious disease of citrus in Japan. CTV is transmitted by some species of aphids found on citrus plants. Of these, citrus brown aphid (Toxoptera citricida Kirkaldy) is the most effective vector. Trials found that if five infected aphids are feeding on a plant, there is a 50% chance that the tree will become infected. If 15 aphids are feeding on the plant, there is a 70% probability of infection. Melon aphid (Aphis gossypii Glover) is also an important vector, especially in Spain, Israel, California, and in Florida where T. citricida is not established. However, the level of transmission from the melon aphid is low in Japan, probably because of a difference in the virus strain. Two other aphid species, Aphis citricola Van der Goot and Toxoptera aurantii Boyer de Fonscolombe, have also been shown to be potential vectors of CTV in some countries, but their efficiency is very low. The virus can also be transmitted by means of infected budwood. The disease is caused by a type of virus which is known as a closterovirus. Fig. 9-6. Citrus tristeza virus (CTV) infects nearly all species, cultivars and hybrids of citrus. It is found all over the world, and there are many different strains of the virus. Some of these may be very mild, others may be severe and very destructive. Often several strains may exist together in the same plant. The symptoms and their severity vary greatly from one tree to another. They are affected by environmental conditions, the type of citrus tree, and the strain of the virus. Quick decline Sweet orange, mandarin (including Satsuma and Ponkan), Tankan, Iyo, Tangor, many varieties of tangelo, and grapefruit are all affected by CTV Grapefruit tree infected with severe strain of tristeza virus, showing stunting and yellowing if they are grown on sour orange, pummelo, or lemon rootstock. However, they are not affected if they are grown on rough lemon rootstock. When an adult tree of such a combination is affected, it turns yellow and wilts rapidly, and dies within a few years. If the tree is grafted onto resistant rootstock such as trifoliate orange or mandarin, it recovers immediately after grafting. Seedling yellows Self-rooted trees of sour orange, Natsudaidai, lemon and buntan are affected by this disease after being infected with the seedlings yellow strain of citrus tristeza (CTV-SY). These trees become yellow and die back. If the affected trees are grafted onto a resistant rootstock, they will generally soon recover. 59

Stem pitting disease Most varieties of citrus are affected by stem pitting disease, even if they are grafted onto a rootstock resistant to tristeza. Grapefruit, buntan and its relatives, tangelo, tangor, sweet orange, Iyo, Yuzu, and natsudaidai are all susceptible, although many varieties of mandarin are resistant, including Satsuma and Ponkan. Susceptible plants develop a large number of pits on both their trunks and their stems. Affected trees become dwarfed and show less vigor, and occasionally die back (Fig. 9-3, Fig. 9-4, Fig. 9-6, Fig. 9-7, Fig. 9-8). As a result, although there is profuse flowering, the trees bear only poor crops of small sized or irregularly shaped fruit. Some cultivars develop rind-oil spots, or brown spots with gumming on the fruit (Fig. 9-5). The causal virus is a severe strain of CTV-SP. CTV infects nearly all species, cultivars and hybrids of citrus. The only known host which is not a member of the citrus family is passionfruit (Passiflora spp.). Diagnosis and detection Failure of sweet orange or grapefruit budded onto sour orange stock is the distinctive symptom of CTV. The virus is often present in tolerant citrus cultivars in a latent form, without producing any symptoms. In many areas, including Taiwan, all citrus cultivars are cultivated on CTV-tolerant rootstock. However, some new, virulent strains of CTV are beginning to evolve in different parts of the world, and are a serious threat to the citrus industry. A new strain, CTV-D, appeared in Taiwan in 1981 and caused marked dwarfing of pummelo trees, which were formerly resistant to this virus. A severe new strain which causes severe damage to sweet orange appeared in Brazil in 1988. Some new stem pitting strains have been found which attack navel orange in Peru and Australia, grapefruit in South Africa and Australia, Valencia sweet orange in Indonesia and China, and mandarin and calamondin in Thailand, the Philippines and East Malaysia. Fig.9-7 and Fig. 9-8. Severe stem-pits on the trunk of a 20-year-old citrus tree. Note the normal growth of annual rings until the tree is 10 years old, and the very slow and irregular growth afterwards. 60

Citrus tatter leaf virus Citrus Tatter Leaf Virus (CTLV) was first found in 1962 in Mayer lemon trees introduced to California from China. Later, the same virus was detected in Mayer lemon trees in Australia and South Africa. Several lines of Satsuma mandarin grown in Japan have been found to be infected by CTLV since 1975. Many citrus trees grown in China and Taiwan, including Ponkan mandarin and Liuchen sweet orange, have recently been found to have the virus. Most citrus species and cultivars grown on tolerant mandarin rootstock have a latent form of the virus and show no symptoms. Examples of tolerant rootstock are Sunki and Cleopatra mandarins. This disease is caused by a virus (a type known as a capillovirus). This virus does not seem to be spread by insects or other vectors. The main way in which the virus spreads is when growers propagate new trees using infected budwood. The virus can also be transmitted in sap. It is sometimes spread mechanically when pruning shears or other tools are used first on an infected tree, and then on a healthy one. Most citrus species and cultivars can have a latent form of the virus, and show no symptoms. However, infected trees of C. excelsa, citrange and citremon are stunted, and produce dwarfed, distorted and blotched leaves (Fig. 9-10, Fig. 9-11). A zig-zag pattern of twigs is sometimes induced in citrange. One very obvious effect of the virus in commercially planted citrus trees is a crease, groove or yellow ring at the bud-union (where the budwood is grafted onto the rootstock) (Fig. 9-9, Fig. 9-12). This is found in infected citrus trees grafted onto trifoliate orange and its hybrids, citrange and citrimelo. In recent years, many growers have been using trifoliate orange as a rootstock, and also hybrids such as Troyer and Carrizo citrange and Swingle citrimelo. As a result, tatter leaf virus has been becoming more common. Fig. 9-10. Blotchy mottle on rusk citrange leaves, caused by tatter leaf virus Fig. 9-9. Bud unions of Ponkan trees grown on trifoliate rootstock, which have been broken by the wind Fig. 9-11. (above) Tatter leaf symptoms on Citrus excelsa Fig. 9-12. (left) A bud union crease in Valencia orange grown on trifoliate rootstock, one year after inoculation (left), compared with uninoculated healthy bud union (right). 61

Citrus exocortis Citrus Exocortis Virus (CEV) was first identified in 1948 in Australia, where it was known as "scaly butt". It is now found in many countries. Citrus exocortis causes bark-shelling and stunting of trifoliate orange, trifoliate hybrids, and Rangpur lime rootstocks. Sour orange rootstock is tolerant. Some severe isolates cause extensive damage to trees grafted onto sensitive rootstock. Citrus exocortis is easily transmitted by grafting. It is often spread when infected budwood which has no symptoms is used for propagation. The viroid is also transmitted mechanically via cutting and pruning tools. of the disease is a virus-like organism which is called a viroid. The viroid kills the bark, which dries, cracks, and may lift in thin strips (Fig. 9-13). Droplets of gum often appear under the loose bark. Infected trees grafted onto susceptible rootstock produce scaly bark on the rootstock only. The quality of the fruit is generally not affected. CEV can infect most citrus species and cultivars, and several non-citrus hosts, but it is latent in most of them. Sensitive species include trifoliate orange, Rangpur lime and some citrons and lemons. These may develop blotching on the stem, or the bark may split. Fig. 9-13. Susceptible rootstock damaged by citrus exocortis virus 62

Integrated control of virus and greening Virus diseases and greening diseases of citrus are transmitted in two main ways. One way is during propagation, when new seedlings are produced using infected budwood and/or rootstock. The second way is by insects, which suck the sap of infected trees and move onto healthy ones, taking the disease with them. These diseases are easily spread if mother stock and seedlings are infected, particularly if this is a latent infection without any visible symptoms. The main way of controlling them is to establish a pathogen-free nursery system. The only way to overcome these diseases is to ensure that all the new seedlings which are planted by growers are free of citrus greening and virus. Virus-free trees Growers cannot eliminate virus or greening disease from seedlings by themselves. This must be done by skilled technicians in a laboratory. The method they use is micrografting of shoot tips combined with heat treatment. Rapid and precise indexing techniques, to test whether virus is present, are another indispensable part of any pathogen-free nursery program. This type of testing too must be done in a laboratory. In order to combat these systemic diseases, the following integrated control measures have been adopted in Taiwan. Procedures for the laboratory and plant nursery Pathogen-free foundation stock are produced through modified methods of shoot-tip grafting, heat-therapy or nucellar line selection (except in the case of pummelo), followed by the rapid propagation of seedlings. This is followed by the cultivation of healthy citrus seedlings, using certified healthy budwoord. Seedlings and mother stock must be checked repeatedly by indexing. Procedures for growers Sanitation Growers must promptly cut down and burn any citrus trees with greening disease or virus disease. They must even dig out the roots and burn them. They must do the same for alternate hosts (i.e. other plant species which suffer from the same diseases). Box orange (Serverinia buxifolia) should not be grown near citrus orchards, as it is an alternative host for citrus greening. It can serve as a source of infection, and spread greening disease to healthy citrus seedlings growing nearby. Protecting healthy trees Growers must protect healthy citrus seedlings planted out the field from reinfestation. There are three ways to do this, and growers should use all of them if they can, combined into an integrated control program. Vector control Firstly, growers should spray their trees with insecticide (Dimethoate 44% EC or Malathion 50% EC 1,000X). Alternatively, they can apply Fig. 9-14. Eulophid wasp Tamarixia radiata on mummified body of citrus psyllid insecticide (Confidor) to the trunk of the tree. This should be done at 10-20 day intervals, during critical infection periods, particularly at times of rapid sprouting and new growth. The aim is to control the vector psyllids and aphids, in order to prevent reinfection with citris greening and citrus tristeza virus. Psyllids can also be controlled by mass release of the eulophid wasp, Tumarixia radiata, if this is available (Fig. 9-14 and Fig. 9-15). Cross protection Healthy trees used as foundation stock or mother trees should be inoculated with mild strains of citrus tristeza virus (CTV), if this is available, as cross protection against severe strains of CTV. Inoculation is carried out by scratching the leaves and applying the inoculum with a small brush or piece of cloth. Keeping tools clean of infection Pruning tools and cutting tools which may be contaminated with citrus tatter leaf virus or exocortis viroid must be disinfected. This is done by dipping the tools in 1% NaOCl (sodium chloride) (10X bleach), and rinsing them with 2% summer oil + 5% acetic acid (vinegar). Growers must be careful to repeat this procedure every time the tools are used on a different tree. Fig. 9-15. Field release of wasps to control citrus psyllids 63

BACTERIAL DISEASES About bacteria Bacteria are one-celled organisms which can be seen only with a microscope. They can generally be grown, or "cultured" in a growing medium in a laboratory. They enter the plant through a wound or some natural opening and multiply quickly, using the plant as food. Citrus canker This disease seems to have originated in Southeast Asia, but has now spread to many other areas, including South America. It can be a serious disease, especially in areas with high rainfall during growth flushes and early fruit development. The bacteria survive in lesions in the leaves, stems and fruit. If Fig. 9-16. Citrus canker: of the leaf water falls on the lesions, the bacteria can ooze out to infect new plants. The bacteria may be spread by wind and wind-driven rain. They may also be spread in other ways, such as people carrying the infection on their hands or clothing, or by sprayers and other machines as they move through the orchard. The bacteria may also be transmitted on pruning tools, or by animals and birds. Finally, they can be spread if infected planting materials or cuttings are taken from one area to another. Citrus canker is a bacterial disease. The causal pathogen is a rod-shaped gram-negative bacterium, Xanthomonas campestris pv. citri. The optimum temperature for growth of the bacteria is 28-30 o C, although they can grow in temperatures as high as 35-39 o C. The most characteristic symptom is brown, raised lesions on the leaves and fruit. All the lesions on a leaf tend to be about the same size. They are found mainly on the edges and tips of the leaves. On fruit, the lesions may be of a different size, because the rind is susceptible for a longer time than the leaves. Lesions on the leaves first become visible on the underside, and soon afterwards also appear on the upper surface (Fig. 9-16). They begin as small dots, and grow to a maximum size of about 1 cm across. At first the lesions are raised and circular. Later, they may become irregular in shape, and develop a raised margin and a sunken center. Sometimes the center of an old lesion drops out, creating a hole in the leaf. A characteristic symptom of citrus canker is that the lesions are surrounded by a yellow ring or halo (Fig. 9-17). However, spots caused by other fungus diseases may also be surrounded by yellow tissue. A more reliable symptom of citrus canker is the water-soaked margin that develops around the edge of each lesion. Sometimes the disease may cause premature leaf and fruit drop. Canker lesions on the fruit do not affect the flavor of the fruit. However, fruit infected with canker have such an poor appearance that they are difficult to market. Fig. 9-17. Citrus canker: of the fruit Citrus canker affects only citrus trees. In general, grapefruit and trifoliate orange are highly susceptible. Lemon and sweet orange are moderately susceptible, and mandarins are moderately resistant. The disease infects only young leaves and fruit. Mature leaves, stems and fruit are resistant to canker. 64

FUNGAL DISEASES About fungi The fungi which cause many citrus diseases belong to a large group which also includes mushrooms and molds. Fungi reproduce by forming millions of tiny spores. These are spread by wind, rain, insects etc. When the spores germinate, they produce tiny threads called hyphae. The hyphae spread internally by digesting their way through the plant's cell walls. Eventually they grow into a tangled mass called a mycelium, which is the actual body of the fungus. Depending on the species of fungus, the mycelium may appear as a coating of mildew on leaves, as patches of black mold, or as the familiar mushroom. The mycelium eventually develops new spores. This completes the life cycle of the fungus. Black spot Black spot is one of the most serious citrus diseases in Asia. It is also found in Australia, South Africa and South America. Under moist conditions, fungal spores are produced under fallen citrus leaves. The spores are airborne. They infect moist fruit and leaves. The causal pathogen is a fungus, Guignardia citricarpa. The dark brown and black pycnidia are abundant on dead leaves. They may also occur on fruit. (Pycnidia are the sporebearing structures of Black spot and several other species of fungi which infect woody plants). Black spot appears as sunken lesions. These lesions vary in their size, shape and color, depending on stage of fruit or leaf development. It is the fruit that suffer the greatest damage from Black spot. The skin shows sunken lesions. These vary in size, shape and color, depending on the stage of fruit development. may appear on young green fruit or on mature ones. On mature fruit, lesions are usually dark brown in color (Fig. 9-18). Black spot also causes postharvest losses. Fruit may sometimes show no visible symptoms when they are picked. Later, they may develop the characteristic lesions of the disease in storage or in retail outlets, if the temperature and humidity are suitable. Black spot is particularly virulent late in the season, when fruit is mature and temperatures are relatively high. Losses can be heavy in late-maturing varieties such as late Valencia orange. Black spot affects all commercial citrus cultivars. Lemons are particularly susceptible to this fungus disease (Fig. 9-19). Fig. 9-18. Black spot on mandarin. Fig. 9-19. Black spot on lemon. 65

Melanose Melanose is found all over the world, but is a major problem only in areas favorable for its development. These are places where there are warm temperatures and plenty of rainfall at the stage of early fruit development. The fungus reproduces in dead twigs, particularly those which have died recently. For this reason, pruning away deadwood is an essential part of controlling melanose. The fungus produces two kinds of spores. One kind are numerous but do not travel far. They are mainly carried in splashes of water such as raindrops. Infected dead twigs in the upper part of the tree may cause heavy infestations in lower branches. The other kind of spore is fairly scarce. These spores are airborne and can be carried on the wind. They are likely to cause outbreaks if heaps of dead citrus wood are left lying on the ground in or around the citrus orchard. The causal pathogen is the fungus Diaporthe citri. Trees are susceptible only for a few months after petal-fall. The severity of the disease is determined mainly by the amount of dead wood in the canopy, and by the length of time the fruit remains wet after rainfall or sprinkler irrigation. Temperature also plays a role. After a spore lands on wet leaves or fruit tissue, it must remain moist for some hours to transmit the disease. At 15 C, 18-24 hours of wetness are needed for infection, but at 25 C, only 10-12 hours are needed. Young trees suffer less from melanose than older ones, because they have less dead wood. of melanose appear one week after infection, as small brown sunken spots on the leaves and fruit (Fig. 9-20 and Fig. 9-21). They are surrounded by a yellow ring or halo. Later, the damaged tissues exude a gummy substance which turns brown and becomes hard. The halo disappears. Melanose symptoms on citrus tend to follow a streaked pattern from the top to the bottom of the fruit, following the pattern of water flow over the skin. Fruit which are infected when they are young may remain small and fall prematurely. Fruit which are infected when they are almost mature are more resistant to infection. The main symptom is small brown lesions on the skin. Infection when the fruit are small produces larger lesions. Sometimes these run together into a solid dark-brown patch, known as "mudcake". Black or dark brown patches on fruit caused by melanose can be distinguished from the similar lesions caused by citrus rust mites because melanose damage has a rough surface. Fruit with melanose lesions on the rind have a normal taste, but their poor appearance makes them difficult to market. Fig. 9-20. Melanose on the fruit. Postharvest damage Melanose can also cause postharvest losses. It takes the form of a postharvest disease known as stem-end rot. Hyphae of the fungus may be present in fruit when they are harvested, and develop in storage. usually appear ten days after harvest. A patch of brownish rot appears around the stem end of the fruit, and the inside of the fruit becomes infected and turns dark. Fruit harvested late in the season are more likely to develop stem-end rot. Melanose infects only citrus trees. Grapefruit and lemons tend to be more susceptible than other kinds of citrus. Fig. 9-21. Melanose on the leaf 66

Citrus scab Citrus scab is a common problem all over the world, wherever conditions are suitable. The optimum temperature for germination is in the range 21-27 o C. However, this fungus can thrive in a much wider temperature range of 18-30 o C. Spores of this fungus are produced by scab pustules on the leaves and fruit of citrus trees. They are dispersed onto healthy tissue by wind and rain. Overhead sprinkler irrigation at flushing, or when the fruit are very young, increases the risk of scab infection. Generally, citrus leaves or fruit must remain wet for at least three hours after a spore has been deposited for the spore to be able to germinate and develop. This disease is caused by the fungus Elsinoë fawcettii. Only young tissues are affected by citrus scab. Leaves are most susceptible to infection just as they emerge from the bud. By the time they have reached their full size, they are immune. Fruit remain susceptible for about three months after petal fall. The main symptom is small, greyish-brown corky scabs which develop on the wigs, young leaves and fruit (Fig. 9-22 and Fig. 9-23). If fruit are infected when they are very young, the scabs are larger and warty. These growths are particularly large on lemons. The scabs on fruit which are infected later are only slightly raised above the surface of the rind. If the scabs are numerous, they may join together to form large scabby areas. These may develop cracks as the fruit grows. Scab affects all varieties of citrus. Lemon and some kinds of mandarin are particularly susceptible to scab. Fig. 9-22. Citrus scab on the leaf of tankan orange Fig. 9-23. Citrus scab on the fruit of tankan orange. 67

Greasy spot This fungus disease has a wide distribution, from the American continent to the Caribbean, Australia and many Asian countries. It generally causes only minor damage, except in areas which are very favorable for infection. These are areas where high temperatures and nearly 100% relative humidity occur together for a prolonged period of time. It is thus mainly the humid tropics and subtropics where greasy spot is a serious disease of citrus orchards. Spores are produced in decomposing fallen leaves, and are released when the leaves become wet. Germination of the spores requires high temperatures and high humidity. which causes greasy spot is the fungus Mycosphaerella citri. The first symptom to appear is a small yellowish blister on the underside of the leaf. This is matched by a yellow mottle on the upper surface of the leaf. Later, infected areas of the leaf turn dark brown and become greasy in appearance (Fig. 9-24). Leaf-drop of infected leaves is common. On the fruit, symptoms may take several months to appear after infection. They take the form of brown specks in the skin, where cells have died. On most cultivars, the specks are too small to cause a significant blemish, but coloring may be delayed in areas around them. This results in unsightly patches of green on the ripe fruit. In grapefruit, the lesions are larger and often form large speckled patches. The lesions are pink at first, and later turn brown. The fungus infects citrus only. Greasy spot occurs on all kinds of citrus, but is more severe on grapefruit, lemons and earlymaturing orange cultivars. Fig. 9-24. Citrus leaves with symptoms of greasy spot 68

Green mold Green mold is a common postharvest disease of citrus in many Asian countries, particularly those with a cooler climate or those which use cold storage for citrus fruit. Nearly all fungi prefer a humid environment, but whereas some fungal diseases are more common in high temperatures, green mold tends to develop most rapidly at temperatures near 24 o C. Growth is much slower if the temperature is above 30 o C. It is particularly common on fruit harvested in the middle of the season. The fungus survives in the orchard from season to season mainly in the form of conidia. Infection is from airborne spores, which enter the peel of the fruit in places where there are small injuries or blemishes. It can also invade fruit which have been damaged on the tree by chilling injury. Infected fruit in storage do not infect the fruit packed around them. However, infected fruit may give off abundant green fungus spores which soil the skin of adjacent fruit. Since it attacks only injured fruit, the best way to prevent green mold is to handle the fruit carefully during and after harvest. The causal fungus is Penicillium digitatum. The first symptom is a tiny soft, watery spot 5-10 mm in diameter. In one day, the spot enlarges until it measures 2-4 cm across. After it reaches a size of 2.5 cm, the fungus begins to produce green spores. These disperse easily if the fruit is handled, or exposed to the wind. The decayed fruit becomes soft and shrinks in size. If the atmosphere is humid, the infected fruit also becomes attacked by other molds and bacteria, and soon collapses into a rotted mass (Fig. 9-25 and Fig. 9-26).. This kind of fungus infects citrus only. Fig. 9-25. Green mold in fruit still on the tree Fig. 9.-26. Green mold in stored fruit 69

Powdery mildew Powdery mildew is a common disease of citrus in many Asian countries. Different cultivars show different levels of susceptibility to the disease. In India, the citrus varieties which are most susceptible to powdery mildew are mandarins, sweet oranges and tangerines. In Java (Indonesia) and in the Philippines, powdery mildew affects mainly mandarins. The powdery mildew fungus lives in both buds and on fallen leaves. It produces spores which are airborne. Warm days and cool nights, together with long periods of dry weather, favor the appearance of powdery mildew. Powdery mildew of citrus is caused by the fungus Oidium tingitaninum. on citrus trees are seen mainly on the young leaves, which turn a pale whitish green. The ends of badly mildewed leaves curl upward or twist (Fig. 9-27 and Fig. 9-28). Malformation and white powdery spores are found, mostly on the upper surface of the leaves. Leafdrop may occur with severe infection. Young shoots heavily colonized by the powdery mildew fungus may die. This species of fungus is found only on citrus. Powdery mildew on other crops shows similar symptoms, but is caused by different (though related) species of fungus. Fig. 9-27. Powdery mildew on the leaves Fig. 9-28. Powdery mildew on the stem 70

Pink disease The disease is widespread in both Asia and the American continent. All species of citrus are susceptible to pink disease. Damage can be severe in tropical areas with high rainfall. The fungus invades the bark of citrus and other trees. The mechanism of disease spread is not well understood. However, it is widely agreed that infected bark and wood serves as a source of infection for healthy trees. It is important for growers to cut off infected branches and burn them, to prevent the disease from spreading (see section on Orchard sanitation and pruning, page 77)). Pink Disease is caused by the fungus Erythricium salmonicolor. The fungus invades the bark of branches and mature trees, causing branches to split and exude gum (Fig. 9-29). A pink fungal growth is visible on the bark, particularly in wet weather. Under wet or humid weather conditions, the fungal growth spreads rapidly along the bark. Later, it may change color to grey or white. Eventually, the bark dies and splits off from the tree. Major branches or entire trees may be killed by the disease. The same species of fungus also infects a range of other trees, including apple and rubber. It produces similar symptoms in all these trees. Because of the wide host range, infection rates are often high when citrus orchards are located close to tropical forest. Fig. 9-29. Citrus tree with pink disease 71

Phytophthora root rot, Gummosis Phytophthora fungus species have a world-wide distribution. They are the cause of the most serious soilborne diseases of citrus. Phytophthora disease spreads rapidly in wet soil. It is particularly destructive in citrus orchards growing in lowlying areas with a high water table, as in parts of Vietnam and Thailand. Phytophthora root rot is a fungus disease. The fungus lives in the soil, and under moist, cool conditions may produce large numbers of spores. The spores are carried in flowing water, including groundwater. Once the spores come into contact with suitable plant roots, they germinate and begin to invade the root tissues. As well as being transmitted in soil water, the fungal pathogens may also be spread in soil (e.g. the soil around infected container-grown plants), or in drainage or irrigation water. They can even be spread on shoes or on vehicle tires. Spread of the disease is promoted by high humidity and rainfall. Hot, dry weather slows down the spread of the disease, and helps the lesions to dry up and heal. Phytophthera disease of citrus trees is caused by the soildwelling fungus Phytophthora citrophthora. Related species of Phytophthora infect a wide range of other woody plants. An early symptom of Phytophthora infection is sap or gum oozing from cracks in the bark near the base of the tree. Because of this symptom, the disease is sometimes referred to as "gummosis" (Fig. 9-30). Another name for the same condition is "Phytophthora root rot". Trees suffering from this condition show poor growth, with a sparse canopy. The leaves turn yellow, and there is dieback of many twigs. Dark water-soaked areas develop on the trunk of the tree, close to the ground. The bark stays dry, and eventually dies and breaks off. The lesion may grow around the lower trunk of the tree. If it has grown to the point where it encircles more than 50% of the trunk, the tree is probably beyond salvage. It should be cut down and replaced. Dead wood should be burned, to prevent it from becoming a source of infection for healthy trees. If the lesion is allowed to progress until it encircles the whole trunk, the tree will die. Trees growing on resistant rootstock show trunk rot only in the area above the bud union. Branches of the tree can also develop Phytophthora rot if they are frequently wet and splashed with soil. Control of this disease depends on correcting the conditions which cause it, such as poor drainage. If citrus orchards are being planted in poorly drained areas, the soil should be mounded to a height of at least 20 cm, to protect the roots from this disease. Growers should also select resistant rootstock such as sour orange or trifoliate orange. Fig. 9-30. Gum oozing from tree with Phytophthora root rot, a condition known as gummosis. 72

DISEASES CAUSED BY NEMATODES About nematodes Nematodes are tiny creatures which live in soil, or in the tissues of living plants and animals. The juveniles (larvae) are tube-shaped, and look like tiny worms. Adults may be round or lemon-shaped. Adult females of some species, including the citrus nematode, are sedentary (Fig. 9-31). They live all the time within a collection of plant cells which have been modified into a feeding and breeding site (Fig. 9-32). Most nematodes are so small (less than 2 mm) that they cannot be seen except with a powerful microscope. Nematodes may be very numerous. A single handful of ordinary soil may contain thousands of them. Since they are in effect invisible, they are usually treated as a plant disease rather than as a plant pest. Most nematodes which infest plants live in the soil and attack the roots. They pierce the walls of the root cells with a hollow tube (stylet) and withdraw the contents of the cell. They may move into the cell, or move between cells. Slow decline Caused by the citrus nematode Tylenchulus semipenetrans The citrus nematode is a worldwide pest of citrus trees. Description Growers cannot identify this nematode by its appearance, because it is too small. Juvenile nematodes (larvae) present in infected soil penetrate the root cells of citrus trees (Fig. 9-33). The females develop into adults which are partially embedded in the root. These each lay around 100 eggs in a sticky egg mass, part of which is embedded in the root and part of which extends into the soil. The eggs hatch into larvae, which travel up to three meters through the soil to find a new root. Nearly all larvae develop into egg-laying females. Male nematodes develop only occasionally, at times of stress such as drought. Female citrus nematodes may persist in the soil for years. Living female citrus nematodes have been recovered from soil which was stored for more than two years. They have also been found in the soil of former orchards four years after all the citrus trees were removed. Damage A tree infected with citrus nematodes may survive for many years after it has been infected. The main effect of nematode infestation is "slow decline". include the dieback of small branches, while leaves may turn yellow and fruit are small in size. There are reduced numbers of feeder roots. While citrus nematodes are too small to see, the roots they attack may have a gritty, knobbly appearance because of the egg masses which cling to them. A definite diagnosis must be made in a laboratory with a good microscope. Growers can expect some citrus nematodes to be present in most orchard soils. They do not become a problem unless populations are very high (i.e. more than 10,000 larvae per 500g of soil). Growers who are planting new orchards must be very careful not to introduce nematodes accidentally, in the soil around the roots of seedlings. If a large number of nematodes are already present in the soil, the best protection is to use resistant rootstock such as trifoliate orange or Troyer citrange. Life cycle The typical life cycle for this nematode is: Egg --> larva--> Adult female Fig. 9-31 Fig. 9-32 Fig. 9-33. Tree root infected with the citrus nematode Tylenchulus semipenetrans (magnified) Left (Figs. 9-31 and 9-32) Adult female citrus nematodes (magnified) 73

Root lesions Caused by the nematodes Pratylenchus sp. (including Pratylenchus coffeae and Pratylenchus citri). Root-lesion nematodes are a world-wide citrus pest. However, different species are found in different parts of the world. Which species is attacking a particular orchard can only be identified by a scientific expert, with the help of a powerful microscope. Description These nematode species attack the roots, causing them to turn black. Eventually the outer skin of the root rots away, and the root then dies. It may be difficult for even experienced growers to distinguish the symptoms of root lesion nematodes from those of Phytophthora root rot. Growers may need to take a sample of the infected roots to send to a laboratory for examination. The roots to be tested for nematodes should be taken from the top 30 cm of soil, from between the trunk of the tree and the drip-line of the outer canopy. Root lesion nematodes are migratory endoparastites (i.e. they are parasites which live inside their host). Unlike the citrus nematode, they do not establish a feeding spot. Instead, they travel through the root, feeding as they go, and damaging the root in the process (Fig. 9-34 and Fig. 9-35). Damage Heavily infested trees are stunted, and have few leaves and small fruit. There is no known citrus rootstock which is resistant to lesion nematodes. Life cycle The larvae of root lesion nematodes pass through four stages before becoming adult. Fig. 9-34. Nematodes (Pratylenchus sp.) in an infected root of citrus tree Fig. 9-35. Lesions on citrus roots caused by nematodes (Pratylenchus sp.) 74