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9 Major diseasesMajor diseasesMajor diseasesMajor diseasesMajor diseasesof citrus in Asiaof citrus in Asiaof citrus in Asiaof citrus in Asiaof citrus in AsiaCitrus greeningCitrus greening is one of the mostdevastating diseases of citrus inAsia. Citrus greening was firstidentified in South Africa fifty yearsago. It is now found all over thetropical and subtropical countriesof Asia. In the Philippines, citrusgreening is the main reason whycitrus production fell by 60%between 1961 and 1970. InVietnam, up to 90% of the citrustrees in some areas are believedto be infected with citrus greening.

Transmission

Transmission by citrus psyllids

Citrus greening is transmitted bythe citrus psyllid, a small insectthat sucks the sap from trees.

Psyllids are not highlyefficient vectors of greening.Epidemics of the disease occuronly when pysyllid populations arehigh (i.e. when there is a lot of newshoot growth), and when a highproportion of the psyllids arecarrying the greening organism.The greening agent is vectoredprimarily by adult insects, althoughlate-stage nymphs were found tobe infective under laboratoryconditions.

Transmission by vegetativepropagation

Citrus greening is also transmittedby the vegetative propagation ofcuttings and suckers from infectedtrees. In their early stages,greening disease and virus

diseases may have few or novisible symptoms. Many of thetrees used as mother stock in Asiaare infected, and as a result, manyof the seedlings sold in plantnurseries are infected too.Transmission of greening viainfected budwood plays animportant role in disease spread.

The pathogen

The pathogen (the organism whichcauses the disease) is abacterium, Liberobacter asiaticum.The bacteria cannot be cultured,and so are known as fastidiousbacteria. They take the form of rigidrods, but are too small to be seenthrough an ordinary microscope.They can be seen only through anelectron microscope.

Symptoms of citrus greening

The Asian greening organismproduces symptoms in eitherwarm temperatures (27-32oC) or acool climate, and is classified as aheat-tolerant form. (In contrast, theSouth Africa greening organismbelongs to a heat-sensitive form.Symptoms are most severe whenthe temperature is only 22-24oC).

The greening agent caninfect most citrus species, cultivarsand hybrids. Most mandarins,sweet oranges and mandarinhybrids are severely affected.Pummelo was formerly thought tobe resistant, but infected pummelotrees have been found in Taiwansince 1970. In recent years,pummelo trees grown in thePhilippines, Malaysia, Vietnam and

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Southern China have also beenfound to be infected.

Most greening organismsisolated from mandarin treesproduce severe greeningsymptoms in mandarin andsweet orange trees, but onlymild symptoms in pummelo.However, a few isolates causesevere symptoms in bothmandarin and pummelo. Thepummelo isolate causes severesymptoms in pummelo, and alsoin mandarin and sweet orange.

Symptoms of the tree

Trees affected with greeningbecome stunted and bearmultiple off-season flowers andleaves, most of which fall off.Shoots are yellow (hence theChinese name of "Huang-lung-pin", or "yellow shoot").

The pathogen movesslowly through citrus trees. In theearly stage of infection, it tendsto remain confined to thelocalized branches into which ithas been introduced by thepsyllid vector. Later, thesymptoms spread slowly throughthe tree. There is dieback oftwigs, the decay of feeder rootletsand lateral roots, a decline invigor, and ultimately the death ofthe entire plant.

Symptoms of the leaf

Common symptoms areyellowing of the veins andadjacent tissues, followed byyellowing or mottling of the entireleaf, occasionally with corking ofthe veins. Diseased leavesbecome hardened and curloutward, while young leavesdeveloped after prematuredefoliation are small andslender, with symptoms of zincdeficiency (Fig. 9-1).

Symptoms of the fruit

The fruit of infected trees are

shaded side (hence the name"greening disease").

Host range

As well as citrus trees, citruspsyllids can live and feed on afew other plant species. Theseare Jasmine orange (Murrayapaniculata), woody apple(Lemonia acidissima), Chinesebox orange (Severinia buxifolia)and curly leaf (Murrayaeuchrestifolia).

Fig. 9-1. Leaf symptoms of pummelo with greening disease (left), showing yellowingand mottling of leaves and vein corking, compared to a healthy leaf (right)

However of these alternate hostsfor psyllids, only one species,box orange, can be infected withthe greening pathogen.

small and irregularly shaped(Fig. 9-2). They taste bitter, witha higher acid and a lower sugarcontent. They do not colorproperly, remaining green on the

Fig. 9-2. The twig and fruit on the left come from a tree with greeningdisease. The diseased leaves are yellow, and the diseased fruit is small andpale green in color. A healthy green leaf and normal large fruit are shownon the right.

Diagnosis and detection

Greening is tentatively identifiedin the field by symptoms in thefoliage and fruit. Furtherdiagnostic tests are carried outin the laboratory.

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VIRUS DISEASESAbout viruses

A citrus virus is a tiny organismthat can multiply only when it isinside a living cell. Usually, thisis the cell of a citrus plant, but itmay be able to multiply insidethe body of an aphid or someother vector. A virus which canmultiply inside the body of avector insect is called"persistent".

Prevention is the only wayof controlling plant viruses.Virus diseases of plants areincurable. Once a plant isinfected, it remains infecteduntil it dies. Any cuttings takenfrom an infected tree will alsobe infected. However, virusinfection is not usuallytransmitted through the seed,so rootstock grown from seedshould be free of virus.

Some viruses infect onlycitrus trees. Others may infecta wide range of other plantspecies as well.

Virus diseases may infectcitrus trees for months or yearsbefore any visible symptomsappear. In other cases, thesymptoms may appear soonand progress quickly. Differentstrains of virus differ in theirsymptoms, and their diseasevirulence. Sometimes, the onlysymptom is a reduction in yield.

Fig. 9-3. Tree with stem-pitting strain of tristeza virus, showingdieback and poor fruit-set

Fig. 9-5. Yellow spots, a symptom of stem pitting diseasecaused by citrus tristeza virus on Iyo orange(a Japanese cultivar)

Fig. 9-4. Symptoms of stem pitting from citrus tristeza virus

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Fig. 9 -6. Grapefruit tree infected with severe strain oftristeza virus, showing stunting and yellowing

Citrus tristeza virusCitrus tristeza virus (CTV) seemshave originated in China manyyears ago. Tristeza (known as"quick decline" in the UnitedStates) is the most destructivedisease of citrus in North andSouth America, although it has aworld-wide distribution. Lessthan two decades after tristezawas introduced from Africa intoSouth America in the 1920s, thedisease wiped out the citrusindustries of Argentina, Brazil,and Uruguay. The same virusalso causes Hasaku Dwarf, aserious disease of citrus inJapan.

Transmission

CTV is transmitted by somespecies of aphids found on citrusplants. Of these, citrus brownaphid (Toxoptera citricidaKirkaldy) is the most effectivevector. Trials found that if fiveinfected aphids are feeding on aplant, there is a 50% chance thatthe tree will become infected. If15 aphids are feeding on theplant, there is a 70% probabilityof infection.

Melon aphid (Aphisgossypii Glover) is also animportant vector, especially inSpain, Israel, California, and inFlorida where T. citricida is notestablished. However, the levelof transmission from the melonaphid is low in Japan, probablybecause of a difference in thevirus strain.

Two other aphid species,Aphis citricola Van der Goot andToxoptera aurantii Boyer deFonscolombe, have also beenshown to be potential vectors ofCTV in some countries, but theirefficiency is very low.

The virus can also betransmitted by means of infectedbudwood.

Symptoms

Citrus tristeza virus (CTV) infectsnearly all species, cultivars andhybrids of citrus. It is found allover the world, and there aremany different strains of thevirus. Some of these may be verymild, others may be severe andvery destructive. Often severalstrains may exist together in thesame plant.

The symptoms and theirseverity vary greatly from one treeto another. They are affected byenvironmental conditions, thetype of citrus tree, and the strainof the virus.

if they are grown on sour orange,pummelo, or lemon rootstock.However, they are not affected ifthey are grown on rough lemonrootstock.

When an adult tree of sucha combination is affected, it turnsyellow and wilts rapidly, and dieswithin a few years. If the tree isgrafted onto resistant rootstocksuch as trifoliate orange ormandarin, it recoversimmediately after grafting.

Seedling yellows

Self-rooted trees of sour orange,Natsudaidai, lemon and buntanare affected by this disease afterbeing infected with the seedlingsyellow strain of citrus tristeza(CTV-SY). These trees becomeyellow and die back. If theaffected trees are grafted onto aresistant rootstock, they willgenerally soon recover.

Quick decline

Sweet orange, mandarin(including Satsuma andPonkan), Tankan, Iyo, Tangor,many varieties of tangelo, andgrapefruit are all affected by CTV

The pathogen

The disease is caused by a typeof virus which is known as aclosterovirus.

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Stem pitting diseaseStem pitting diseaseStem pitting diseaseStem pitting diseaseStem pitting disease rind-oil spots, or brown spotswith gumming on the fruit(Fig. 9-5). The causal virus is asevere strain of CTV-SP.

all citrus cultivars are cultivatedon CTV-tolerant rootstock.

However, some new,virulent strains of CTV arebeginning to evolve in differentparts of the world, and are aserious threat to the citrusindustry. A new strain, CTV-D,appeared in Taiwan in 1981and caused marked dwarfing ofpummelo trees, which wereformerly resistant to this virus. Asevere new strain whichcauses severe damage tosweet orange appeared inBrazil in 1988. Some new stempitting strains have been foundwhich attack navel orange inPeru and Australia, grapefruit inSouth Africa and Australia,Valencia sweet orange inIndonesia and China, andmandarin and calamondin inThailand, the Philippines andEast Malaysia.

Fig.9-7 and Fig. 9-8. Severe stem-pits on thetrunk of a 20-year-old citrus tree. Notethe normal growth of annual rings untilthe tree is 10 years old, and the veryslow and irregular growth afterwards.

Host range

CTV infects nearly all species,cultivars and hybrids of citrus.The only known host which is nota member of the citrus family ispassionfruit (Passiflora spp.).

Diagnosis and detection

Failure of sweet orange orgrapefruit budded onto sourorange stock is the distinctivesymptom of CTV. The virus isoften present in tolerant citruscultivars in a latent form, withoutproducing any symptoms. Inmany areas, including Taiwan,

Most varieties of citrus areaffected by stem pitting disease,even if they are grafted onto arootstock resistant to tristeza.Grapefruit, buntan and itsrelatives, tangelo, tangor, sweetorange, Iyo, Yuzu, andnatsudaidai are all susceptible,although many varieties ofmandarin are resistant, includingSatsuma and Ponkan.

Susceptible plants developa large number of pits on boththeir trunks and their stems.Affected trees become dwarfedand show less vigor, andoccasionally die back (Fig. 9-3,Fig. 9-4, Fig. 9-6, Fig. 9-7, Fig. 9-8). As a result, although there isprofuse flowering, the trees bearonly poor crops of small sized orirregularly shaped fruit.

Some cultivars develop

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Fig. 9-9. Bud unions of Ponkan trees grown ontrifoliate rootstock, which have been broken bythe wind

Fig. 9-11. (above) Tatter leaf symptomson Citrus excelsa

Fig. 9-10. Blotchy mottle on rusk citrangeleaves, caused by tatter leaf virus

Fig. 9-12. (left) A bud union crease in Valencia orangegrown on trifoliate rootstock, one year afterinoculation (left), compared with uninoculatedhealthy bud union (right).

Citrus tatter leaf virus The pathogen

This disease is caused by avirus (a type known as acapillovirus).

Transmission

However, infected trees of C.excelsa, citrange and citremonare stunted, and producedwarfed, distorted and blotchedleaves (Fig. 9-10, Fig. 9-11). Azig-zag pattern of twigs issometimes induced in citrange.

One very obvious effect ofthe virus in commercially plantedcitrus trees is a crease, groove oryellow ring at the bud-union(where the budwood is graftedonto the rootstock) (Fig. 9-9,Fig. 9-12). This is found ininfected citrus trees grafted ontotrifoliate orange and its hybrids,citrange and citrimelo.

In recent years, manygrowers have been usingtrifoliate orange as a rootstock,and also hybrids such as Troyerand Carrizo citrange and Swinglecitrimelo. As a result, tatter leafvirus has been becomingmore common.

This virus does not seem to bespread by insects or othervectors. The main way in whichthe virus spreads is whengrowers propagate new treesusing infected budwood.

The virus can also betransmitted in sap. It issometimes spread mechanicallywhen pruning shears or othertools are used first on an infectedtree, and then on a healthy one.

SymptomsMost citrus species and cultivarscan have a latent form of thevirus, and show no symptoms.

Citrus Tatter Leaf Virus (CTLV)was first found in 1962 in Mayerlemon trees introduced toCalifornia from China. Later, thesame virus was detected inMayer lemon trees in Australiaand South Africa. Several lines ofSatsuma mandarin grown inJapan have been found to beinfected by CTLV since 1975.Many citrus trees grown in Chinaand Taiwan, including Ponkanmandarin and Liuchen sweetorange, have recently beenfound to have the virus.

Most citrus species andcultivars grown on tolerantmandarin rootstock have a latentform of the virus and show nosymptoms. Examples of tolerantrootstock are Sunki andCleopatra mandarins.

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Citrus exocortisCitrus Exocortis Virus (CEV) wasfirst identified in 1948 inAustralia, where it was known as"scaly butt". It is now found inmany countries.

Citrus exocortis causesbark-shelling and stunting oftrifoliate orange, trifoliate hybrids,and Rangpur lime rootstocks.Sour orange rootstock is tolerant.Some severe isolates cause

extensive damage to treesgrafted onto sensitive rootstock.

Symptoms

The viroid kills the bark, whichdries, cracks, and may lift in thinstrips (Fig. 9-13). Droplets ofgum often appear under theloose bark.

Infected trees grafted ontosusceptible rootstock producescaly bark on the rootstock only.The quality of the fruit isgenerally not affected.

CEV can infect most citrusspecies and cultivars, andseveral non-citrus hosts, but it islatent in most of them. Sensitivespecies include trifoliate orange,Rangpur lime and some citronsand lemons. These may developblotching on the stem, or the barkmay split.

Fig. 9 -13 . Susceptible rootstock damaged by citrus exocortis virus

The pathogen

The pathogen of the disease is avirus-like organism which iscalled a viroid.Transmission

Citrus exocortis is easilytransmitted by grafting. It is oftenspread when infected budwoodwhich has no symptoms is usedfor propagation. The viroid is alsotransmitted mechanically viacutting and pruning tools.

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seedlings, using certified healthybudwoord. Seedlings andmother stock must be checkedrepeatedly by indexing.

Procedures for growers

Sanitation

Growers must promptly cut downand burn any citrus trees withgreening disease or virusdisease. They must even dig outthe roots and burn them. Theymust do the same for alternatehosts (i.e. other plant specieswhich suffer from the samediseases).

Box orange (Serveriniabuxifolia) should not be grownnear citrus orchards, as it is analternative host for citrusgreening. It can serve as asource of infection, and spreadgreening disease to healthycitrus seedlings growing nearby.

Protecting healthy trees

Growers must protect healthycitrus seedlings planted out thefield from reinfestation. There arethree ways to do this, andgrowers should use all of them ifthey can, combined into anintegrated control program.

Vector control

Firstly, growers should spraytheir trees with insecticide(Dimethoate 44% EC orMalathion 50% EC 1,000X).Alternatively, they can apply

Integrated control ofvirus and greeningVirus diseases and greeningdiseases of citrus aretransmitted in two main ways.One way is during propagation,when new seedlings areproduced using infectedbudwood and/or rootstock. Thesecond way is by insects, whichsuck the sap of infected treesand move onto healthy ones,taking the disease with them.

These diseases are easilyspread if mother stock andseedlings are infected,particularly if this is a latentinfection without any visiblesymptoms. The main way ofcontrolling them is to establish apathogen-free nursery system.The only way to overcome thesediseases is to ensure that all thenew seedlings which are plantedby growers are free of citrusgreening and virus.

Virus-free trees

Growers cannot eliminate virusor greening disease fromseedlings by themselves. Thismust be done by skilledtechnicians in a laboratory. Themethod they use is micrograftingof shoot tips combined with heattreatment. Rapid and preciseindexing techniques, to testwhether virus is present, areanother indispensable part ofany pathogen-free nurseryprogram. This type of testing toomust be done in a laboratory. Inorder to combat these systemicdiseases, the followingintegrated control measureshave been adopted in Taiwan.

Procedures for the laboratoryand plant nursery

Pathogen-free foundation stockare produced through modifiedmethods of shoot-tip grafting,heat-therapy or nucellar lineselection (except in the case ofpummelo), followed by the rapidpropagation of seedlings.

This is followed by thecultivation of healthy citrus

insecticide (Confidor) to the trunkof the tree . This should be doneat 10-20 day intervals, duringcritical infection periods,particularly at times of rapidsprouting and new growth.

The aim is to control thevector psyllids and aphids, inorder to prevent reinfection withcitris greening and citrus tristezavirus. Psyllids can also becontrolled by mass release ofthe eulophid wasp, Tumarixiaradiata, if this is available (Fig. 9-14 and Fig. 9-15).

Cross protection

Healthy trees used as foundationstock or mother trees should beinoculated with mild strains ofcitrus tristeza virus (CTV), if this isavailable, as cross protectionagainst severe strains of CTV.Inoculation is carried out byscratching the leaves andapplying the inoculum with asmall brush or piece of cloth.

Keeping tools clean of infection

Pruning tools and cutting toolswhich may be contaminated withcitrus tatter leaf virus or exocortisviroid must be disinfected.

This is done by dipping thetools in 1% NaOCl (sodiumchloride) (10X bleach), andrinsing them with 2% summer oil+ 5% acetic acid (vinegar).

Growers must be careful torepeat this procedure everytime the tools are used on adifferent tree.

Fig. 9- 14. Eulophid wasp Tamarixiaradiata on mummified body ofcitrus psyllid

Fig. 9-15. Field release of wasps tocontrol citrus psyllids

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BACTERIAL DISEASES

quickly, using the plant as food.

Citrus canker

as high as 35-39oC.

Symptoms

The most characteristic symptomis brown, raised lesions on theleaves and fruit. All the lesionson a leaf tend to be about thesame size. They are foundmainly on the edges and tips ofthe leaves. On fruit, the lesionsmay be of a different size,because the rind is susceptiblefor a longer time than the leaves.

Lesions on the leaves firstbecome visible on the underside,and soon afterwards also appearon the upper surface (Fig. 9-16).They begin as small dots, andgrow to a maximum size of about1 cm across. At first the lesionsare raised and circular. Later,they may become irregular inshape, and develop a raisedmargin and a sunken center.Sometimes the center of an oldlesion drops out, creating a holein the leaf.

A characteristic symptomof citrus canker is that thelesions are surrounded by ayellow ring or halo (Fig. 9-17).However, spots caused by otherfungus diseases may also besurrounded by yellow tissue. Amore reliable symptom of citruscanker is the water-soakedmargin that develops around theedge of each lesion.

Sometimes the diseasemay cause premature leaf andfruit drop. Canker lesions on thefruit do not affect the flavor of thefruit. However, fruit infected withcanker have such an poorappearance that they are difficultto market.

water falls on the lesions, thebacteria can ooze out to infectnew plants.

The bacteria may bespread by wind and wind-drivenrain. They may also be spread inother ways, such as peoplecarrying the infection on theirhands or clothing, or by sprayersand other machines as theymove through the orchard. Thebacteria may also be transmittedon pruning tools, or by animalsand birds. Finally, they can bespread if infected plantingmaterials or cuttings are takenfrom one area to another.

The pathogen

Citrus canker is a bacterialdisease. The causal pathogen isa rod-shaped gram-negativebacterium, Xanthomonascampestris pv. citri. The optimumtemperature for growth of thebacteria is 28-30oC, althoughthey can grow in temperatures

Fig. 9-16. Citrus canker: Symptoms of the leaf

Fig. 9-17. Citrus canker: Symptoms of the fruit

About bacteria

Host range

Citrus canker affects only citrustrees. In general, grapefruit andtrifoliate orange are highlysusceptible. Lemon and sweetorange are moderatelysusceptible, and mandarins aremoderately resistant.

The disease infects onlyyoung leaves and fruit. Matureleaves, stems and fruit areresistant to canker.

Bacteria are one-celledorganisms which can be seenonly with a microscope. Theycan generally be grown, or"cultured" in a growing mediumin a laboratory. They enter theplant through a wound or somenatural opening and multiply

This disease seems to haveoriginated in Southeast Asia, buthas now spread to many otherareas, including South America.It can be a serious disease,especially in areas with highrainfall during growth flushesand early fruit development.

TransmissionThe bacteria survive in lesions inthe leaves, stems and fruit. If

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FUNGAL DISEASESAbout fungi

The fungi which cause manycitrus diseases belong to alarge group which also includesmushrooms and molds. Fungireproduce by forming millions oftiny spores. These are spreadby wind, rain, insects etc .

When the sporesgerminate, they produce tinythreads called hyphae. Thehyphae spread internally bydigesting their way through theplant's cell walls. Eventually theygrow into a tangled mass called amycelium, which is the actualbody of the fungus.

Depending on the speciesof fungus, the mycelium mayappear as a coating of mildew onleaves, as patches of black mold,or as the familiar mushroom. Themycelium eventually developsnew spores. This completes thelife cycle of the fungus.

Black spotDistribution

Black spot is one of the mostserious citrus diseases in Asia. Itis also found in Australia, SouthAfrica and South America.

Transmission

Under moist conditions, fungalspores are produced underfallen citrus leaves. The sporesare airborne. They infect moistfruit and leaves.

The pathogen

The causal pathogen is afungus, Guignardia citricarpa.The dark brown and blackpycnidia are abundant on deadleaves. They may also occur onfruit. (Pycnidia are the spore-bearing structures of Black spotand several other species offungi which infect woody plants).

Symptoms

Black spot appears as sunkenlesions. These lesions vary intheir size, shape and color,depending on stage of fruit orleaf development.

It is the fruit that suffer thegreatest damage from Blackspot. The skin shows sunkenlesions. These vary in size,shape and color, depending onthe stage of fruit development.Symptoms may appear on younggreen fruit or on mature ones. Onmature fruit, lesions are usuallydark brown in color (Fig. 9-18).

Black spot also causespostharvest losses. Fruit maysometimes show no visiblesymptoms when they are picked.Later, they may develop thecharacteristic lesions of thedisease in storage or in retailoutlets, if the temperature andhumidity are suitable.

Black spot is particularlyvirulent late in the season, whenfruit is mature and temperaturesare relatively high. Losses can beheavy in late-maturing varietiessuch as late Valencia orange.

Host range

Black spot affects all commercialcitrus cultivars. Lemons areparticularly susceptible to thisfungus disease (Fig. 9-19).

Fig. 9-18. Black spot on mandarin.

Fig. 9-19. Black spot on lemon.

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MelanoseDistribution

Melanose is found all over theworld, but is a major problem onlyin areas favorable for itsdevelopment. These are placeswhere there are warmtemperatures and plenty ofrainfall at the stage of early fruitdevelopment.

Transmission

The fungus reproduces in deadtwigs, particularly those whichhave died recently. For thisreason, pruning away deadwoodis an essential part of controllingmelanose.

The fungus produces twokinds of spores. One kind arenumerous but do not travel far.They are mainly carried insplashes of water such asraindrops. Infected dead twigs inthe upper part of the tree maycause heavy infestations in lowerbranches.

The other kind of spore isfairly scarce. These spores areairborne and can be carried onthe wind. They are likely to causeoutbreaks if heaps of dead citruswood are left lying on the groundin or around the citrus orchard.

The pathogen

The causal pathogen is thefungus Diaporthe citri. Trees aresusceptible only for a few monthsafter petal-fall. The severity of thedisease is determined mainly bythe amount of dead wood in thecanopy, and by the length of timethe fruit remains wet after rainfallor sprinkler irrigation.

Temperature also plays arole. After a spore lands on wetleaves or fruit tissue, it mustremain moist for some hours totransmit the disease. At 15°C, 18-24 hours of wetness are neededfor infection, but at 25°C, only 10-12 hours are needed. Youngtrees suffer less from melanosethan older ones, because theyhave less dead wood.

Symptoms Postharvest damage

Fig. 9-20. Melanose on the fruit. Fig. 9-21. Melanose on the leaf

Melanose can also causepostharvest losses. It takes theform of a postharvest diseaseknown as” stem-end rot”. Hyphaeof the fungus may be present infruit when they are harvested,and develop in storage.

Symptoms usuallyappear ten days after harvest. Apatch of brownish rot appearsaround the stem end of the fruit,and the inside of the fruitbecomes infected and turnsdark. Fruit harvested late in theseason are more likely todevelop stem-end rot .

Symptoms of melanose appearone week after infection, assmall brown sunken spots onthe leaves and fruit (Fig. 9-20 andFig. 9-21). They are surroundedby a yellow ring or halo. Later, thedamaged tissues exude agummy substance which turnsbrown and becomes hard. Thehalo disappears.

Melanose symptoms oncitrus tend to follow a streakedpattern from the top to the bottomof the fruit, following the patternof water flow over the skin.

Fruit which are infectedwhen they are young may remainsmall and fall prematurely. Fruitwhich are infected when they arealmost mature are moreresistant to infection. The mainsymptom is small brown lesionson the skin.

Infection when the fruit aresmall produces larger lesions.Sometimes these run togetherinto a solid dark-brown patch,known as "mudcake".

Black or dark brownpatches on fruit caused bymelanose can be distinguishedfrom the similar lesions causedby citrus rust mites becausemelanose damage has a roughsurface.

Fruit with melanoselesions on the rind have anormal taste, but their poorappearance makes them difficultto market.

Host rangeMelanose infects only citrustrees. Grapefruit and lemonstend to be more susceptible thanother kinds of citrus.

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Citrus scabDistribution

Citrus scab is a commonproblem all over the world,wherever conditions are suitable.The optimum temperature forgermination is in the range 21-27oC. However, this fungus canthrive in a much widertemperature range of 18-30oC.

Transmission

Spores of this fungus areproduced by scab pustules onthe leaves and fruit of citrustrees. They are dispersed ontohealthy tissue by wind and rain.Overhead sprinkler irrigation atflushing, or when the fruit are veryyoung, increases the risk of scab

infection. Generally, citrusleaves or fruit must remain wetfor at least three hours after aspore has been deposited forthe spore to be able togerminate and develop.

The pathogen

This disease is caused by thefungus Elsinoë fawcettii.

The main symptom issmall, greyish-brown corkyscabs which develop on thewigs, young leaves and fruit (Fig.9-22 and Fig. 9-23). If fruit areinfected when they are veryyoung, the scabs are larger andwarty. These growths areparticularly large on lemons.

The scabs on fruit whichare infected later are only slightlyraised above the surface of therind. If the scabs are numerous,they may join together to formlarge scabby areas. These maydevelop cracks as the fruit grows.

Fig. 9-23. Citrus scab on the fruit oftankan orange.

Fig. 9-22. Citrus scab on the leafof tankan orange

Symptoms

Only young tissues are affectedby citrus scab. Leaves are mostsusceptible to infection just asthey emerge from the bud. By thetime they have reached their fullsize, they are immune. Fruitremain susceptible for aboutthree months after petal fall.

Host range

Scab affects all varieties of citrus.Lemon and some kinds ofmandarin are particularlysusceptible to scab.

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Greasy spotDistribution

This fungus disease has a widedistribution, from the Americancontinent to the Caribbean,Australia and many Asiancountries. It generally causesonly minor damage, except inareas which are very favorable forinfection. These are areas wherehigh temperatures and nearly100% relative humidity occurtogether for a prolonged period oftime. It is thus mainly the humidtropics and subtropics wheregreasy spot is a serious diseaseof citrus orchards.

are released when the leavesbecome wet. Germination of thespores requires hightemperatures and high humidity.

The pathogen

The pathogen which causesgreasy spot is the fungusMycosphaerella citri.

take several months to appearafter infection. They take the formof brown specks in the skin,where cells have died.

On most cultivars, thespecks are too small to cause asignificant blemish, but coloringmay be delayed in areas aroundthem. This results in unsightlypatches of green on the ripe fruit.

In grapefruit, the lesionsare larger and often form largespeckled patches. The lesionsare pink at first, and later turnbrown.

Fig. 9-24. Citrus leaves with symptoms of greasy spot

Transmission

Spores are produced indecomposing fallen leaves, and

Symptoms

The first symptom to appear is asmall yellowish blister on theunderside of the leaf. This ismatched by a yellow mottle on theupper surface of the leaf. Later,infected areas of the leaf turn darkbrown and become greasy inappearance (Fig. 9-24). Leaf-dropof infected leaves is common.

On the fruit, symptoms may

Host range

The fungus infects citrus only.Greasy spot occurs on all kindsof citrus, but is more severe ongrapefruit, lemons and early-maturing orange cultivars.

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Green mold Transmission

The fungus survives in theorchard from season to seasonmainly in the form of conidia.Infection is from airborne spores,which enter the peel of the fruit inplaces where there are smallinjuries or blemishes.

It can also invade fruitwhich have been damaged onthe tree by chilling injury.Infected fruit in storage do notinfect the fruit packed aroundthem. However, infected fruit maygive off abundant green fungusspores which soil the skin ofadjacent fruit.

Since it attacks only injuredfruit, the best way to preventgreen mold is to handle the fruitcarefully during and after harvest.

Fig. 9-25. Green mold in fruit still on the tree

Fig. 9.-26. Green mold in stored fruit

The pathogen

The causal fungus is Penicilliumdigitatum.

Symptoms

The first symptom is a tiny soft,watery spot 5-10 mm indiameter. In one day, the spotenlarges until it measures 2-4cm across. After it reaches a sizeof 2.5 cm, the fungus begins toproduce green spores. Thesedisperse easily if the fruit ishandled, or exposed to the wind.

The decayed fruit becomessoft and shrinks in size. If theatmosphere is humid, theinfected fruit also becomesattacked by other molds andbacteria, and soon collapsesinto a rotted mass (Fig. 9-25 andFig. 9-26).

.Host range

This kind of fungus infectscitrus only.

Distribution

Green mold is a commonpostharvest disease of citrus inmany Asian countries, particularlythose with a cooler climate orthose which use cold storage forcitrus fruit.

Nearly all fungi prefer ahumid environment, but whereassome fungal diseases are morecommon in high temperatures,green mold tends to developmost rapidly at temperaturesnear 24oC. Growth is muchslower if the temperature isabove 30oC.

It is particularly common onfruit harvested in the middle ofthe season.

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Powdery mildewDistribution

Powdery mildew is a commondisease of citrus in many Asiancountries. Different cultivarsshow different levels ofsusceptibility to the disease.

In India, the citrus varietieswhich are most susceptible topowdery mildew are mandarins,sweet oranges and tangerines.In Java (Indonesia) and in thePhilippines, powdery mildewaffects mainly mandarins.

Transmission

The powdery mildew fungus livesin both buds and on fallenleaves. It produces spores whichare airborne.

Warm days and coolnights, together with longperiods of dry weather, favor theappearance of powdery mildew.

The pathogen

Symptoms

Symptoms on citrus trees areseen mainly on the young leaves,which turn a pale whitish green.The ends of badly mildewedleaves curl upward or twist (Fig.9-27 and Fig. 9-28).

Malformation and whitepowdery spores are found,mostly on the upper surface ofthe leaves. Leafdrop may occurwith severe infection . Youngshoots heavily colonized by thepowdery mildew fungus may die.

Host range

This species of fungus is foundonly on citrus. Powdery mildewon other crops shows similarsymptoms, but is caused bydifferent (though related)species of fungus.

Fig. 9-28. Powdery mildew on the stemFig. 9-27. Powdery mildew on the leaves

Powdery mildew of citrus iscaused by the fungusOidium tingitaninum.

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Pink diseaseDistribution

The disease is widespread inboth Asia and the Americancontinent. All species of citrusare susceptible to pink disease.Damage can be severe intropical areas with high rainfall.

Transmission

The fungus invades the bark ofcitrus and other trees. Themechanism of disease spread isnot well understood. However, itis widely agreed that infectedbark and wood serves as asource of infection for healthytrees. It is important for growers

to cut off infected branches andburn them, to prevent thedisease from spreading (seesection on “Orchard sanitationand pruning, page 77)).

weather conditions, the fungalgrowth spreads rapidly along thebark. Later, it may change colorto grey or white.

Eventually, the bark diesand splits off from the tree. Majorbranches or entire trees may bekilled by the disease.

Symptoms

The fungus invades the bark ofbranches and mature trees,causing branches to split andexude gum (Fig. 9-29). A pinkfungal growth is visible on thebark, particularly in wet weather.

Under wet or humid

Fig. 9-29. Citrus tree with pink disease

The pathogen

Pink Disease is caused by thefungus Erythricium salmonicolor.

Host range

The same species of fungusalso infects a range of othertrees, including apple andrubber. It produces similarsymptoms in all these trees.Because of the wide host range,infection rates are often highwhen citrus orchards are locatedclose to tropical forest.

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irrigation water. They can evenbe spread on shoes or onvehicle tires.

Spread of the disease ispromoted by high humidity andrainfall. Hot, dry weather slowsdown the spread of the disease,and helps the lesions to dry upand heal.

The pathogen

Phytophthera disease of citrustrees is caused by the soil-dwelling fungus Phytophthoracitrophthora. Related species ofPhytophthora infect a widerange of other woody plants.

areas develop on the trunk of thetree, close to the ground. The barkstays dry, and eventually dies andbreaks off.

The lesion may growaround the lower trunk of the tree.If it has grown to the point where itencircles more than 50% of thetrunk, the tree is probably beyondsalvage. It should be cut downand replaced. Dead wood shouldbe burned, to prevent it frombecoming a source of infection forhealthy trees. If the lesion isallowed to progress until itencircles the whole trunk, the treewill die.

Trees growing on resistantrootstock show trunk rot only inthe area above the bud union.Branches of the tree can alsodevelop Phytophthora rot if theyare frequently wet and splashedwith soil.

Control of this diseasedepends on correcting theconditions which cause it, suchas poor drainage. If citrusorchards are being planted inpoorly drained areas, the soilshould be mounded to a height ofat least 20 cm, to protect the rootsfrom this disease.

Growers should also selectresistant rootstock such as sourorange or trifoliate orange.

Symptoms

An early symptom ofPhytophthora infection is sap orgum oozing from cracks in thebark near the base of the tree.Because of this symptom, thedisease is sometimes referredto as "gummosis" (Fig. 9-30).Another name for the samecondition is "Phytophthoraroot rot".

Trees suffering from thiscondition show poor growth, witha sparse canopy. The leaves turnyellow, and there is dieback ofmany twigs. Dark water-soaked

Fig. 9-30. Gum oozing from tree with Phytophthora root rot, acondition known as “gummosis”.

Phytophthora root rot,GummosisDistribution

Phytophthora fungus specieshave a world-wide distribution.They are the cause of the mostserious soilborne diseases ofcitrus. Phytophthora diseasespreads rapidly in wet soil.

It is particularly destructivein citrus orchards growing in low-lying areas with a high watertable, as in parts of Vietnamand Thailand.

Transmission

Phytophthora root rot is a fungusdisease. The fungus lives in thesoil, and under moist, coolconditions may produce largenumbers of spores. The sporesare carried in flowing water,including groundwater. Once thespores come into contact withsuitable plant roots, theygerminate and begin to invadethe root tissues.

As well as beingtransmitted in soil water, thefungal pathogens may also bespread in soil (e.g. the soilaround infected container-grownplants), or in drainage or

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DISEASES CAUSEDBY NEMATODESAbout nematodes

DamageSlow declineCaused by the citrus nematodeTylenchulus semipenetrans

Distribution

The citrus nematode is a world-wide pest of citrus trees.

Description

Fig. 9-33. Tree root infected with the citrus nematodeTylenchulus semipenetrans (magnified)

Fig. 9-32

Fig. 9-31

Left (Figs. 9-31 and 9-32) Adult female citrus nematodes (magnified)

Growers cannot identify thisnematode by its appearance,because it is too small. Juvenilenematodes (larvae) present ininfected soil penetrate the rootcells of citrus trees (Fig. 9-33).The females develop into adultswhich are partially embedded inthe root. These each lay around100 eggs in a sticky egg mass,part of which is embedded in theroot and part of which extendsinto the soil. The eggs hatchinto larvae, which travel up tothree meters through the soil tofind a new root. Nearly all larvaedevelop into egg-laying females.Male nematodes develop onlyoccasionally, at times of stresssuch as drought.

Female citrus nematodesmay persist in the soil for years.Living female citrus nematodeshave been recovered from soilwhich was stored for more thantwo years. They have also beenfound in the soil of formerorchards four years after all thecitrus trees were removed.

Nematodes are tiny creatureswhich live in soil, or in thetissues of living plants andanimals. The juveniles (larvae)are tube-shaped, and look liketiny worms. Adults may beround or lemon-shaped.

Adult females of somespecies, including the citrusnematode, are sedentary (Fig. 9-31). They live all the time withina collection of plant cells whichhave been modified into afeeding and breeding site(Fig. 9-32).

Most nematodes are sosmall (less than 2 mm) that theycannot be seen except with apowerful microscope.Nematodes may be verynumerous. A single handful ofordinary soil may containthousands of them. Since theyare in effect invisible, they areusually treated as a plantdisease rather than as aplant pest.

Most nematodes whichinfest plants live in the soil andattack the roots. They piercethe walls of the root cells with ahollow tube (stylet) andwithdraw the contents of thecell. They may move into thecell, or move between cells.

A tree infected with citrusnematodes may survive for manyyears after it has been infected.The main effect of nematodeinfestation is "slow decline".Symptoms include the dieback ofsmall branches, while leavesmay turn yellow and fruit aresmall in size. There are reducednumbers of feeder roots.

While citrus nematodesare too small to see, the rootsthey attack may have a gritty,knobbly appearance because ofthe egg masses which cling tothem. A definite diagnosis mustbe made in a laboratory with agood microscope.

Growers can expect somecitrus nematodes to be presentin most orchard soils. They donot become a problem unlesspopulations are very high(i.e. more than 10,000 larvaeper 500g of soil).

Growers who are plantingnew orchards must be very carefulnot to introduce nematodesaccidentally, in the soil around theroots of seedlings. If a largenumber of nematodes are alreadypresent in the soil, the bestprotection is to use resistantrootstock such as trifoliate orangeor Troyer citrange.

Life cycle

The typical life cycle for thisnematode is: Egg --> larva--> Adult female

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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.)

Root lesions Description

These nematode species attackthe roots, causing them to turnblack. Eventually the outer skin ofthe root rots away, and the rootthen dies.

It may be difficult for evenexperienced growers todistinguish the symptoms of rootlesion nematodes from those ofPhytophthora root rot. Growersmay need to take a sample ofthe infected roots to send to alaboratory for examination. Theroots to be tested for nematodesshould be taken from the top 30cm of soil, from between thetrunk of the tree and the drip-lineof the outer canopy.

Root lesion nematodes aremigratory endoparastites

(i.e. they are parasites which liveinside their host). Unlike thecitrus nematode, they do notestablish a feeding spot. Instead,they travel through the root,feeding as they go, anddamaging the root in the process(Fig. 9-34 and Fig. 9-35).

Damage

Heavily infested trees arestunted, and have few leaves andsmall fruit. There is no knowncitrus rootstock which is resistantto lesion nematodes.

Life cycle

The larvae of root lesionnematodes pass through fourstages before becoming adult.

Distribution

Root-lesion nematodes are aworld-wide citrus pest. However,different species are found indifferent parts of the world. Whichspecies is attacking a particularorchard can only be identified bya scientific expert, with the help ofa powerful microscope.

Caused by the nematodesPratylenchus sp. (includingPratylenchus coffeae andPratylenchus citri).