Fungal Diseases of Citrus Fruit and Foliage

Fungal Diseases of Fungal Diseases of Citrus Fruit and FoliageCitrus Fruit and Foliage

Megan Megan DewdneyDewdneyPLP 5115cPLP 5115c

Foliar Fungal Diseases to be Foliar Fungal Diseases to be CoveredCovered

Alternaria Brown Spot (and leaf Alternaria Brown Spot (and leaf spot of rough lemon)spot of rough lemon)

Greasy spotGreasy spot MelanoseMelanose Scab DiseasesScab Diseases Postbloom Fruit DropPostbloom Fruit Drop Black SpotBlack Spot Pseudocercospera Pseudocercospera Fruit and Leaf Fruit and Leaf

SpotSpot

Note on TerminologyNote on Terminology Many Ascomycete fungi have what is Many Ascomycete fungi have what is

know as an anamorph and teleomorphknow as an anamorph and teleomorphAnamorphAnamorph: asexual or imperfect stage: asexual or imperfect stageTeleomorphTeleomorph: sexual or perfect stage: sexual or perfect stageHave separate namesHave separate names

Fungi where no sexual stage has been Fungi where no sexual stage has been identified are grouped into the ‘identified are grouped into the ‘Fungi Fungi ImperfectiImperfecti’ ’ Synonym:Synonym: Deuteromycte Deuteromycte Some Basidiomycetes have also lost sexual Some Basidiomycetes have also lost sexual

stagestage Ex. Ex. RhizoctoniaRhizoctonia spp. spp.

Alternaria Brown SpotAlternaria Brown Spot

Causal agent: Causal agent: AlternariaAlternaria alternataalternataSynonyms Synonyms AlternariaAlternaria citricitri and and A. alternataA. alternata

pv. pv. citricitriNo known teleomorphNo known teleomorph

Important disease on tangerines and Important disease on tangerines and tangelostangelos

1903 First described in Australia on 1903 First described in Australia on Emperor mandarinEmperor mandarin

Alternaria Brown Spot cont.Alternaria Brown Spot cont.

1974 First identified in Florida1974 First identified in Florida Also found in South Africa, Turkey, Israel, Also found in South Africa, Turkey, Israel,

Spain, Colombia and other countriesSpain, Colombia and other countries Host specific toxinHost specific toxin

Isolates from tangerines and tangelos do not Isolates from tangerines and tangelos do not infect rough lemon except in rare infect rough lemon except in rare circumstancescircumstances

Disease on rough lemon same organism with Disease on rough lemon same organism with different toxindifferent toxin

Considered separate pathotypes of Considered separate pathotypes of A. A. alternataalternata

AlternariaAlternaria alternataalternata No sexual stage knownNo sexual stage known NecrotrophicNecrotrophic Conidia are small, thick walled, Conidia are small, thick walled,

pigmented and multicellularpigmented and multicellular The conidiophores are The conidiophores are

determinate and pigmenteddeterminate and pigmented Conidia are borne in chains Conidia are borne in chains Hyphae penetrate host tissue Hyphae penetrate host tissue

directly; No appresoriumdirectly; No appresorium

Tissue SusceptibilityTissue Susceptibility

Highly susceptible cultivarsHighly susceptible cultivarsDancy, Minneola, Orlando, Sunburst, Dancy, Minneola, Orlando, Sunburst,

Murcott, Nova and Lee Murcott, Nova and Lee Leaves susceptible from formation to Leaves susceptible from formation to

when fully expanded and hardenedwhen fully expanded and hardened Fruit are susceptible from petal fall Fruit are susceptible from petal fall

to 5 cm (2 inch) in diameterto 5 cm (2 inch) in diameter

SymptomsSymptoms

Alternaria Brown Spot Disease Alternaria Brown Spot Disease Cycle Caused by Cycle Caused by AlternariaAlternaria

alternataalternata

When are the Conidia When are the Conidia Released?Released? Conidia released Conidia released

by rain events or by rain events or sudden changes in sudden changes in relative humidityrelative humidity

In field trapping In field trapping number of conidia number of conidia in the air related in the air related to leaf wetness to leaf wetness durationduration

Number of Number of airborne conidia airborne conidia not related to not related to infection severityinfection severity

Timmer et al., Timmer et al., 19881988

Infection ConditionsInfection Conditions Optimum Optimum

temperatures 23-temperatures 23-27°C27°CCan get infection Can get infection

between 17-32°Cbetween 17-32°C

Infection can occur Infection can occur with as little as 4-6 with as little as 4-6 hours of leaf hours of leaf wetness but disease wetness but disease severity increases severity increases with leaf wetnesswith leaf wetness

Canihos et al., Canihos et al., 19991999

Alternaria Brown Spot Disease Alternaria Brown Spot Disease Cycle Caused by Cycle Caused by AlternariaAlternaria

alternataalternata

Cultural ControlsCultural Controls

Disease-free nursery treesDisease-free nursery trees Careful choice of planting siteCareful choice of planting site

Air drainage importantAir drainage importantWider spacingWider spacing

No vigorous rootstocksNo vigorous rootstocks No over-fertilization or over-No over-fertilization or over-

wateringwatering Hedge in late MarchHedge in late March No overhead irrigationNo overhead irrigation

FungicidesFungicides Copper –Works well for fruit but not leavesCopper –Works well for fruit but not leaves Ferbam – Only moderately effectiveFerbam – Only moderately effective Strobulurins – Most effective but specific Strobulurins – Most effective but specific

MOAMOAAzoxystrobinAzoxystrobinTrifloxystrobinTrifloxystrobinPyraclostrobinPyraclostrobin

First spray when spring flush ¼-1/2 full First spray when spring flush ¼-1/2 full expansion; high inoculum another before expansion; high inoculum another before full expansion or at petal fallfull expansion or at petal fall

Rest of the year maintain protective Rest of the year maintain protective coatingcoating

ALTER-RATER: A Forecasting ALTER-RATER: A Forecasting SystemSystem

Weather-based point system to Weather-based point system to better time fungicide applicationsbetter time fungicide applications

Points assigned based on:Points assigned based on:Rainfall and leaf wetnessRainfall and leaf wetnessAverage daily temperatureAverage daily temperature

Thresholds vary by cultivar Thresholds vary by cultivar susceptibilitysusceptibility

More information found at: More information found at: http://edis.ifas.ufl.edu/ch183

http://edis.ifas.ufl.edu/ch183

The ALTER-RATERThe ALTER-RATERSuggested Threshold Suggested Threshold

ScoresScoresScoreScore SituationSituation

5050Heavily infested Minneola, Dancy, Heavily infested Minneola, Dancy, Orlando, Sunburst; Many flatwood Orlando, Sunburst; Many flatwood groves, east coast, and SW Florida.groves, east coast, and SW Florida.

100100Moderately infested Minneola or Moderately infested Minneola or Dancy, many Murcotts; Ridge and Dancy, many Murcotts; Ridge and north Florida groves.north Florida groves.

150150Light infestations, any variety, Light infestations, any variety, mostly Ridge and north Florida mostly Ridge and north Florida groves.groves.

ALTER- RATER Daily ALTER- RATER Daily PointsPoints

Rain > 0.1 Rain > 0.1 inchinch LW > 10 hrLW > 10 hr Avg daily Avg daily

TempTempAssigned Assigned

scorescore

++ ++ 68-8368-83 1111

++ ++ > 83> 83 88

++ ++ < 68< 68 66

++ __ 68-8368-83 66

++ __ > 83> 83 44

++ __ < 68< 68 33

__ ++ 68-8368-83 66

__ ++ > 83> 83 66

__ ++ < 68< 68 44

__ __ 68-8368-83 33

__ __ > 83> 83 00

__ __ < 68< 68 00

Greasy SpotGreasy Spot

Causal agent: Causal agent: MycosphaerellaMycosphaerella citricitri Anamorph: Anamorph: StenellaStenella citri-griseacitri-grisea Anamorph synonym Anamorph synonym CercosporaCercospora citri-griseacitri-grisea

Other similar diseases described around Other similar diseases described around world but caused by other world but caused by other Mycosphaerella Mycosphaerella sppspp..

Important disease on most types of citrusImportant disease on most types of citrus 1915 First described in Florida and Cuba1915 First described in Florida and Cuba

Greasy Spot cont.Greasy Spot cont.

Also occurs in Texas, the Caribbean, Also occurs in Texas, the Caribbean, Central and South America, and Central and South America, and parts of Asiaparts of Asia

Primary effect is to cause defoliation Primary effect is to cause defoliation which can lead to decreases of yield which can lead to decreases of yield and fruit sizeand fruit sizeUp to 25% on sweet orange in FloridaUp to 25% on sweet orange in Florida Up to 45% on grapefruitUp to 45% on grapefruit

MycosphaerellaMycosphaerella citricitri LoculoascomyceteLoculoascomycete

Pseudothecia up to 90 µmPseudothecia up to 90 µmFound in leaf litterFound in leaf litterAscospores fusiform and hyaline Ascospores fusiform and hyaline

with one septum (2-3 x 6-12 µm)with one septum (2-3 x 6-12 µm)

StenellaStenella citri-griseacitri-grisea Conidia are pale olive Conidia are pale olive

brown, cylindrical with brown, cylindrical with indistinct septae that indistinct septae that can be in chainscan be in chains

Two types of Two types of conidiophoresconidiophores

Most common simple, Most common simple, smooth, dark and erectsmooth, dark and erect

Rare, in clusters Rare, in clusters (fasciculate) found in (fasciculate) found in necrotic areas on leavesnecrotic areas on leaves

MyceliumMycelium Epiphytic hyphaeEpiphytic hyphae

Highly branchedHighly branchedRough walls Rough walls Olive brown color when Olive brown color when

young but darken with young but darken with age and the walls become age and the walls become smoothsmooth

Appressoria formed in Appressoria formed in stomatal chambersstomatal chambers

Mycelia within leaf Mycelia within leaf grow intercellularly grow intercellularly and are not very and are not very branchedbranched


Highly susceptible cultivarsHighly susceptible cultivarsGrapefruit, Pineapple, Hamlin, and Grapefruit, Pineapple, Hamlin, and

TangelosTangelos Less susceptible cultivarsLess susceptible cultivars

Valencia, Temple, Murcott and most Valencia, Temple, Murcott and most tangerinestangerines

Young and mature leaves susceptible Young and mature leaves susceptible to infectionto infection

Immature fruit susceptibleImmature fruit susceptible

SymptomsSymptoms

Greasy Spot Disease Cycle Greasy Spot Disease Cycle Caused by Caused by MycosphaerellaMycosphaerella citricitri

Pseudothecia MaturationPseudothecia MaturationMoistureMoisture

Mondal and Timmer, Mondal and Timmer, 20022002

Pseudothecia MaturationPseudothecia MaturationTemperatureTemperature

Optimal Optimal Temperatures for Temperatures for

Ascospore Ascospore ProductionProduction

28 28 °C = 82.4 °F°C = 82.4 °F


Peak Ascospore EjectionPeak Ascospore Ejection

The peak The peak ascospore ejection ascospore ejection period has shifted period has shifted to earlier in seasonto earlier in seasonWhy?Why?Is this beneficial?Is this beneficial? 0

5

10

15

20

25

30

35

Months

Perc

ent o

f tot

al a

scos

pore

s

2000-01

2001-02

1969

Epiphytic GrowthEpiphytic Growth

Occurs during the wet Occurs during the wet summer monthssummer months

Ascospore dose does not Ascospore dose does not determine level of determine level of epiphytic growthepiphytic growth

Similar patterns on fruit Similar patterns on fruit and leavesand leaves


Epiphytic Growth and Epiphytic Growth and InfectionInfection

Tissue penetrated only Tissue penetrated only through stomatathrough stomata

High density of High density of penetration required penetration required for symptomsfor symptoms

Requires high Requires high humidityhumidity

Symptoms caused by Symptoms caused by swelling stimulated by swelling stimulated by hyphaehyphae

Greasy Spot Disease Cycle Greasy Spot Disease Cycle Caused by Caused by MycosphaerellaMycosphaerella citricitri


Reduce leaf litter in winter and early Reduce leaf litter in winter and early springspringDiskingDiskingFrequent irrigation to promote Frequent irrigation to promote

decompositiondecompositionMulch leaf litterMulch leaf litterPut urea or lime on the leaf litterPut urea or lime on the leaf litter

Problem with this approachProblem with this approachNot enough of the leaf litter is Not enough of the leaf litter is

decomposeddecomposed

FungicidesFungicides

Petroleum oil – gives adequate control on Petroleum oil – gives adequate control on less susceptible cultivarsless susceptible cultivars

Copper – more consistent control than oilCopper – more consistent control than oil Strobilurins – same concerns about MOAStrobilurins – same concerns about MOA

AzoxystrobinAzoxystrobinTrifloxystrobinTrifloxystrobinPyraclostrobinPyraclostrobin

Fenbuconazole – moderate risk for Fenbuconazole – moderate risk for resistanceresistanceDMI fungicide or sterol biosynthesis inhibitorsDMI fungicide or sterol biosynthesis inhibitors

Spray TimingSpray Timing Less susceptible cultivarsLess susceptible cultivars

One spray between May and June often One spray between May and June often sufficient especially in Northern sufficient especially in Northern production regionsproduction regions

In South Florida, more susceptible In South Florida, more susceptible cultivars and in groves with severe cultivars and in groves with severe defoliationdefoliationTwo sprays; one mid-May – June, the Two sprays; one mid-May – June, the

second once flush has expandedsecond once flush has expandedA third and final spray may be needed A third and final spray may be needed

for fresh grapefruit in a grove that was for fresh grapefruit in a grove that was heavily infested the previous yearheavily infested the previous year

Spray Timing EffectsSpray Timing Effects

0

1

2

3

4

5

May Jun Jul Aug Sep Oct Nov Dec Jan

Ep

iph

ytic

myc

elia

l gro

wth

Unsprayed controlMay sprayJuly sprayAugust sprayMay+June spray

MelanoseMelanose

Causal agent: Causal agent: DiaportheDiaporthe citricitriAnamorph:Anamorph: Phomopsis citri Phomopsis citri

Disease is present in most citrus Disease is present in most citrus producing countriesproducing countries

Important only where fresh fruit is Important only where fresh fruit is produced in humid areasproduced in humid areas

Causes lesions on fruit and leavesCauses lesions on fruit and leaves All citrus susceptible but grapefruit All citrus susceptible but grapefruit

and lemons are the most susceptibleand lemons are the most susceptible

DiaportheDiaporthe citricitri

Ascospores formed in peritheciaAscospores formed in peritheciaSpherical with flattened base (125-160 Spherical with flattened base (125-160

µm)µm)Long tapered beaks (200-800 µm)Long tapered beaks (200-800 µm)

Ascospores are hyalineAscospores are hyaline2 cells each with 2 oil droplets (guttulae)2 cells each with 2 oil droplets (guttulae)3.2-4.5 x 11.5-14.2 µm3.2-4.5 x 11.5-14.2 µm

PhomopsisPhomopsis citricitri

Pycnidia are dark, ovoid and Pycnidia are dark, ovoid and erumpent with thick wallserumpent with thick wallsFound scattered on dead twigs Found scattered on dead twigs 200-450 µm200-450 µmSpores are extruded in a tendril (cirrhus)Spores are extruded in a tendril (cirrhus)

PhomopsisPhomopsis citri citri contcont..

Two forms of hyaline conidiaTwo forms of hyaline conidia α-conidia are unicellular α-conidia are unicellular

2 oil droplets (biguttulate)2 oil droplets (biguttulate)2.5-4 x 5-9 µm2.5-4 x 5-9 µm

β-conidia β-conidia Filiform and hookedFiliform and hookedDon’t germinate and are predominant Don’t germinate and are predominant form in older pycnidiaform in older pycnidia

0.7-1.5 x 20-30 µm0.7-1.5 x 20-30 µm


Spring flush usually not severely Spring flush usually not severely infectedinfected

On summer flush infection can lead to On summer flush infection can lead to defoliation especially after diebackdefoliation especially after dieback

Leaves become resistant once fully Leaves become resistant once fully expandedexpanded

Fruit resistant 12 weeks after petal fall Fruit resistant 12 weeks after petal fall and when infection occurs later during and when infection occurs later during the 12 weeks, lesions are smallerthe 12 weeks, lesions are smallerGrapefruit are susceptible until 7-10 cm in Grapefruit are susceptible until 7-10 cm in

diameterdiameter

SymptomsSymptoms

Melanose Disease Cycle Caused Melanose Disease Cycle Caused by by DiaportheDiaporthe citricitri

Pycnidia ProductionPycnidia Production

Mondal Mondal et alet al., 2004., 2004

Wetting period, twig Wetting period, twig diameter, temperature diameter, temperature and disease severity on and disease severity on the twig all had the twig all had significant effects on significant effects on pycnidia formationpycnidia formation

Formation takes Formation takes between 3-5 months in between 3-5 months in field and can occur on field and can occur on dead twigsdead twigs

Pycnidia ProductionPycnidia Production

Mondal Mondal et alet al., 2004., 2004

Most of the Most of the inoculum is inoculum is produced on twigs produced on twigs that die between that die between January and AprilJanuary and April

Conidia produced Conidia produced at low %RH are at low %RH are viable for several viable for several weeks to monthsweeks to months

Mondal Mondal et alet al., ., 20072007

InfectionInfection

Conidia germinateConidia germinate6 hrs at 16 °C6 hrs at 16 °C4 hrs 20 to 28 °C4 hrs 20 to 28 °C

Literature has Literature has varying times and varying times and temperatures temperatures needed for needed for infectioninfection

Optimum temp Optimum temp determined to be determined to be 24-28 °C24-28 °C Agostini Agostini et alet al., 2003., 2003

Melanose Disease Cycle Caused Melanose Disease Cycle Caused by by DiaportheDiaporthe citricitri


Select younger groves for fresh fruitSelect younger groves for fresh fruitLess dead wood for inoculum Less dead wood for inoculum

productionproduction

Remove dead wood from canopyRemove dead wood from canopy

Clear out brush pilesClear out brush piles


Copper –Most economical but can Copper –Most economical but can cause blemishes in hot dry weathercause blemishes in hot dry weather

Strobilurins – Low residual activity Strobilurins – Low residual activity compared to copper but useful in hot compared to copper but useful in hot weatherweatherAzoxystrobinAzoxystrobinTrifloxystrobinTrifloxystrobinPyraclostrobinPyraclostrobin

Spray TimingSpray Timing Oranges and TangerinesOranges and Tangerines

First spray mid to late AprilFirst spray mid to late AprilOne to two applications sufficientOne to two applications sufficient

Grapefruit (fresh market)Grapefruit (fresh market)First application when fruit ¼ to ½ inchFirst application when fruit ¼ to ½ inchCopper to be applied every 3 weeks Copper to be applied every 3 weeks

until fruit resistant in late June to early until fruit resistant in late June to early JulyJuly

There is a model to determine whether There is a model to determine whether copper residues are sufficient to control copper residues are sufficient to control disease based on weathering of copper disease based on weathering of copper and the growth rate of fruitand the growth rate of fruit

Citrus ScabCitrus Scab Causal agent: Causal agent: ElsinoëElsinoë fawcettiifawcettii

Anamorph:Anamorph: Sphaceloma fawcettii Sphaceloma fawcettii Found in most humid citrus production Found in most humid citrus production

regionsregions Important for fresh fruit productionImportant for fresh fruit production Sweet orange scab: Sweet orange scab: E. australisE. australis; ; S. S.

australisaustralisFound in southern South America and S. Found in southern South America and S.

KoreaKoreaNewly discovered in Texas and LouisianaNewly discovered in Texas and Louisiana

Elsinoë fawcettii Elsinoë fawcettii and and E. E. australisaustralis

Only been found in BrazilOnly been found in Brazil Distinguished by ascospore sizeDistinguished by ascospore size

E. fawcettiiE. fawcettii 5-6 x 10-12 µm 5-6 x 10-12 µmE. australisE. australis 12-20 x 15-30 µm 12-20 x 15-30 µm

Function in the disease cycle is Function in the disease cycle is unknown but clearly not essentialunknown but clearly not essential

Sphaceloma spp.Sphaceloma spp. Conidia are hyaline, Conidia are hyaline,

single celled and ellipticalsingle celled and ellipticalIndistinguishable between Indistinguishable between

speciesspeciesCan reproduce by buddingCan reproduce by budding

Also fusiform conidia (Also fusiform conidia (E. E. fawcettiifawcettii))PigmentedPigmentedGerminate to form hyaline Germinate to form hyaline

conidiaconidia Conidia borne in acervuliConidia borne in acervuli

Host Range and Tissue Host Range and Tissue SusceptibilitySusceptibility

Young leaves and fruit are susceptibleYoung leaves and fruit are susceptibleLeaves immune to infection in a few days Leaves immune to infection in a few days Fruit remain susceptible up to two monthsFruit remain susceptible up to two months

Summer flush can be especially badly Summer flush can be especially badly affectedaffected

The host range of The host range of E. fawcettiiE. fawcettii is is complicated complicated

Matter of considerable ongoing Matter of considerable ongoing phylogenic researchphylogenic research

Host RangeHost RangeDisease Pathogen Pathotyp

eHosts

Citrus scab

Elsinoë fawcettii

FBHR Lemon, grapefruit, Temples, sour orange, sweet orange, many tangerines

FNHR Lemon, grapefruit

Tyron’s Lemon, Cleopatra

Lemon Lemon

Sweet orange scab

E. australis

Sweetorange

Sweet oranges, tangerines

Natsu-daidai

Natsudaidai

SymptomsSymptoms

Citrus Scab/Sweet Orange Scab Citrus Scab/Sweet Orange Scab Disease Cycles Caused by Disease Cycles Caused by ElsinoëElsinoë

fawcettifawcetti and and E.E. australisaustralis

InfectionInfection

Contradictory Contradictory information in the information in the literature about leaf literature about leaf wetness and wetness and temperature temperature

Optimal temperature Optimal temperature range range 23.5 to 27 °C23.5 to 27 °C

Optimal leaf wetnessOptimal leaf wetnessBetween 12 and 24 hrsBetween 12 and 24 hrs Agostini Agostini et alet al., 2003., 2003

Conidia ProductionConidia Production

Conidia can be produced in 1-2 Conidia can be produced in 1-2 hours with sufficient wetnesshours with sufficient wetness

Optimum temperature 24-28°COptimum temperature 24-28°C Spores are splash dispersedSpores are splash dispersed The greater the number of spores, The greater the number of spores,

the greater the number of lesionsthe greater the number of lesions Tend to see more disease with low Tend to see more disease with low

lying areas where there more dew lying areas where there more dew and longer dew periodsand longer dew periods

Citrus Scab/Sweet Orange Scab Citrus Scab/Sweet Orange Scab Disease Cycles Caused by Disease Cycles Caused by ElsinoëElsinoë

fawcettifawcetti and and E.E. australisaustralis


Disease-free nursery treesDisease-free nursery treesStart clean and problems are unlikelyStart clean and problems are unlikely

Hedge and top badly-affected Hedge and top badly-affected plantingsplantingsDoes not move far even within treesDoes not move far even within trees

No vigorous rootstocksNo vigorous rootstocks No overhead irrigationNo overhead irrigation


CopperCopper FerbamFerbam Strobulurins – Most effective but specific Strobulurins – Most effective but specific

MOAMOAAzoxystrobinAzoxystrobinTrifloxystrobinTrifloxystrobinPyraclostrobinPyraclostrobin

FenbuconazoleFenbuconazole

Spray TimingSpray Timing

Sprays are mainly for groves with a Sprays are mainly for groves with a recent history of Scabrecent history of Scab

First spray – spring flush 2-3 inchesFirst spray – spring flush 2-3 inches can be omitted if severity was lightcan be omitted if severity was light

Petal fallPetal fall Three week after petal fallThree week after petal fall

Postbloom Fruit DropPostbloom Fruit Drop

Causal agent: Causal agent: ColletotrichumColletotrichum acutatumacutatumTeleomorph: Teleomorph: GlomerellaGlomerella acutataacutataFormerly thought to be Formerly thought to be Colletotrichum Colletotrichum

gloeosporioidesgloeosporioides Widespread throughout humid Widespread throughout humid

subtropics and tropics of the Americassubtropics and tropics of the Americas Problematic in years with high rainfall Problematic in years with high rainfall

around bloomaround bloom First reported in Belize in 1979First reported in Belize in 1979

ColletotrichumColletotrichum acutatumacutatum

Conidia are fusiform Conidia are fusiform rather than roundrather than round

Pigmented to give spore Pigmented to give spore mass a salmon colormass a salmon color

Slower growing than Slower growing than C. C. gloeosporioidesgloeosporioides

Borne in an acervulusBorne in an acervulusFew setae on host tissue Few setae on host tissue

or in cultureor in culture Appressoria are the Appressoria are the

survival structuressurvival structures

Host RangeHost Range

Affects most citrus cultivarsAffects most citrus cultivars Most severe on sweet oranges, Most severe on sweet oranges,

lemons, and limeslemons, and limes Less severe on grapefruit and Less severe on grapefruit and

tangerinestangerines Is a limiting factor for citrus Is a limiting factor for citrus

production in high rainfall areas of production in high rainfall areas of Belize, Mexico, Costa Rica, and the Belize, Mexico, Costa Rica, and the Caribbean islandsCaribbean islands

Susceptible TissueSusceptible Tissue

Open flowers are the most Open flowers are the most susceptiblesusceptible

Unopened or pin-head bloom much Unopened or pin-head bloom much less severe infectionless severe infection

Does not appear to affect the foliage Does not appear to affect the foliage except that around the calyxes which except that around the calyxes which is distorted with large veinsis distorted with large veins

Fruitlets abscise at base of ovary to Fruitlets abscise at base of ovary to form persistent calyxes or ‘buttons’form persistent calyxes or ‘buttons’

SymptomsSymptoms

Post Bloom Fruit Drop Disease Post Bloom Fruit Drop Disease Cycle Caused by Cycle Caused by ColletotrichumColletotrichum

acutatumacutatum

Timmer and Zitko, 1993

Inoculum levels most importantInoculum levels most important Rainfall is importantRainfall is important Need infection of early bloom to get Need infection of early bloom to get

inoculum build upinoculum build up Optimum temperature for conidia Optimum temperature for conidia

germination is 23°C but over 50% of germination is 23°C but over 50% of conidia can germinate between 10-conidia can germinate between 10-30°C30°C

Disease ProgressDisease Progress

Post Bloom Fruit Drop Disease Post Bloom Fruit Drop Disease Cycle Caused by Cycle Caused by ColletotrichumColletotrichum

acutatumacutatum


No overhead irrigationNo overhead irrigationIf necessary only at nightIf necessary only at night

If there are trees in decline from If there are trees in decline from other diseases such as tristeza, other diseases such as tristeza, blight or HLB that promote off blight or HLB that promote off season bloom, remove them from season bloom, remove them from your PFD prone blockyour PFD prone block

FungicidesFungicides FerbamFerbam Strobulurins – Most effective but Strobulurins – Most effective but

specific MOAspecific MOAAzoxystrobinAzoxystrobinTrifloxystrobinTrifloxystrobinPyraclostrobinPyraclostrobin

FenbuconazoleFenbuconazole Thiophanate methyl – No longer Thiophanate methyl – No longer

registered due to toxicology resultsregistered due to toxicology results

Fungicide TimingFungicide Timing

577.1250048.016.163.13 LWRTDy

yy = Percentage of flowers infected 4 = Percentage of flowers infected 4 days in the futuredays in the future

TDTD = total number of infected flowers = total number of infected flowers on 20 trees; however if on 20 trees; however if TDTD < 75 then < 75 then TDTD =0 =0

R R = rainfall total for the last 5 days in = rainfall total for the last 5 days in inchesinches

LWLW = Average number of hours of leave = Average number of hours of leave wetness daily for the last 5 days - 10 wetness daily for the last 5 days - 10 hourshours

When to Follow the ModelWhen to Follow the Model A fungicide application is indicated if A fungicide application is indicated if

these three criteria are met:these three criteria are met: 1) the model predicts a disease 1) the model predicts a disease

incidence of greater than 20%incidence of greater than 20%

2) sufficient bloom is present or 2) sufficient bloom is present or developing to represent a significant developing to represent a significant portion of the total cropportion of the total crop

3) no fungicide application has been 3) no fungicide application has been made in the last 10-14 daysmade in the last 10-14 days

Model found at: Model found at: http://pfd.ifas.ufl.edu/

http://pfd.ifas.ufl.edu/

Black SpotBlack Spot

Causal agent : Causal agent : Guignardia Guignardia citricarpa citricarpa Anamorph: Anamorph: Phyllosticta citricarpaPhyllosticta citricarpaSyn.: Syn.: Phoma citricarpaPhoma citricarpa

Hosts : Citrus species and hybrids Hosts : Citrus species and hybrids Sweet oranges, mandarins and Sweet oranges, mandarins and

tangerines, lemonstangerines, lemons ‘‘Tahiti’ lime - non-symptomatic Tahiti’ lime - non-symptomatic

infectioninfection

Black Spot cont.Black Spot cont.

Rind spots cause the most economic Rind spots cause the most economic damage damage internal quality unaffectedinternal quality unaffected

Reduces fruit value for the fresh marketReduces fruit value for the fresh market

Restricts export of fresh fruitsRestricts export of fresh fruits mostly to European countries and formerly the mostly to European countries and formerly the

U.SU.S

Causes premature fruit drop reducing yieldCauses premature fruit drop reducing yield

World DistributionWorld DistributionOccurs mostly in summer rainfall areas or areas Occurs mostly in summer rainfall areas or areas with prolonged dew or fog in warm weatherwith prolonged dew or fog in warm weather

Legend - Crop losses

Major Epidemics

Guignardia citricarpaGuignardia citricarpa

Never found in fruit – in leaf litterNever found in fruit – in leaf litter Form aggregated ascomata - Form aggregated ascomata -

peritheciod pseudotheciumperitheciod pseudothecium100-175 µm diameter100-175 µm diameter

Ascopores are aseptate, hyaline, Ascopores are aseptate, hyaline, multiguttulate and cylindricalmultiguttulate and cylindrical

with swollen middleswith swollen middles 4.5-605 x 12.5-16 µm4.5-605 x 12.5-16 µm

PhyllostictaPhyllosticta citricarpacitricarpa

Forms pycnidiaForms pycnidiaDark brown or blackDark brown or blackForm on fruit and leaves and pedicles of Form on fruit and leaves and pedicles of

lemonslemons115-190 µm115-190 µm

Conidia are obovate, hyaline, aseptate Conidia are obovate, hyaline, aseptate and multiguttalateand multiguttalate5.5-7 x 8-10.5 µm5.5-7 x 8-10.5 µm


Hosts include Citrus species and Hosts include Citrus species and hybrids hybrids

Symptomatic hosts: Sweet oranges, Symptomatic hosts: Sweet oranges, mandarins and tangerines, lemonsmandarins and tangerines, lemons

Non-symptomatic host: ‘Tahiti’ limeNon-symptomatic host: ‘Tahiti’ limeProduces ascospores from leavesProduces ascospores from leaves

Fruit are susceptible for 5-6 months Fruit are susceptible for 5-6 months post-petal fallpost-petal fallLeaf susceptibility period still uncertainLeaf susceptibility period still uncertain

SymptomsSymptoms

Black Spot Disease Cycle Caused Black Spot Disease Cycle Caused by by GuignardiaGuignardia citricarpacitricarpa

EpidemiologyEpidemiology

Major source of inoculum: Major source of inoculum: decomposing infected leaves on decomposing infected leaves on orchard floor (ascospores)orchard floor (ascospores)

Additional source of inoculum: Additional source of inoculum: lesions on infected fruits, leaves and lesions on infected fruits, leaves and branches (conidia)branches (conidia)

Means of spread: Wind Means of spread: Wind (ascospores); Water splash (ascospores); Water splash (ascospores and conidia)(ascospores and conidia)

Epidemiology cont.Epidemiology cont.

Optimal conditions for infection: Optimal conditions for infection: Temp 21 – 32ºCTemp 21 – 32ºCWetting period 24 - 48hWetting period 24 - 48h

Symptom expression: 1 – 12 monthsSymptom expression: 1 – 12 months

Survival of the fungus: leaves, Survival of the fungus: leaves, branches, fruits and pedunclesbranches, fruits and peduncles

Black Spot Disease Cycle Caused Black Spot Disease Cycle Caused by by GuignardiaGuignardia citricarpacitricarpa

Cultural ControlsCultural Controls Increase air flow in trees to reduce leaf Increase air flow in trees to reduce leaf

wetness where possiblewetness where possible

Avoid cultivars with significant off-Avoid cultivars with significant off-season bloomseason bloom

Reduce leaf litter to reduce ascospore Reduce leaf litter to reduce ascospore loadload

Minimize trash when picking to avoid Minimize trash when picking to avoid inadvertent movement of the fungus inadvertent movement of the fungus from one location to anotherfrom one location to another

FungicidesFungicides Registered fungicides with reported Registered fungicides with reported

efficacy against black spotefficacy against black spotCopper - all formulations; use maximum Copper - all formulations; use maximum

label ratelabel rateStrobilurins (Abound, Gem, Headline) - Strobilurins (Abound, Gem, Headline) -

maximum label rate recommendedmaximum label rate recommendedRecommended at temperatures > 94Recommended at temperatures > 94ººF when F when

phytoxicity is a concernphytoxicity is a concernNo more than 4 strobilurins applications can be No more than 4 strobilurins applications can be

made in a year for all diseases made in a year for all diseases Consecutive applications not recommended due Consecutive applications not recommended due

to potential resistance developmentto potential resistance development

Black Spot Application TimingBlack Spot Application Timing

Late Spring Late Spring (April/May)(April/May)

CopperCopper

Continue applications at 1 month intervalsContinue applications at 1 month intervals

Fruit is susceptible for 5-6 months Fruit is susceptible for 5-6 months post-petal fallpost-petal fall

Copper and/or strobilurinsCopper and/or strobilurinsCopperCopper

Copper and/or strobilurinsCopper and/or strobilurinsCopperCopper

Use strobilurins when concerned Use strobilurins when concerned about copper phytotoxicityabout copper phytotoxicity

PseudocercosporaPseudocercospora Fruit and Fruit and Leaf SpotLeaf Spot

PseudocercosporaPseudocercospora angolensis angolensis Syn.: Syn.: PhaeoramulariaPhaeoramularia angolensisangolensis

No know teleomorphNo know teleomorph Serious disease of fruit and foliage in Serious disease of fruit and foliage in

much of Sub-Saharan Africa except much of Sub-Saharan Africa except South AfricaSouth Africa

First described in Angola and First described in Angola and Mozambique in 1952Mozambique in 1952

Quarantine diseaseQuarantine disease

Host RangeHost Range

All citrus speciesAll citrus species Most susceptibleMost susceptible

Grapefruit, oranges, pummelo and mandarinGrapefruit, oranges, pummelo and mandarin Less susceptibleLess susceptible

LemonLemon Least susceptibleLeast susceptible

LimeLime Yield losses between 50-100% not Yield losses between 50-100% not

uncommonuncommon

PseudocercosporaPseudocercospora angolensisangolensis

Forms dense tufts (synnemata) of Forms dense tufts (synnemata) of light chestnut multi-septate light chestnut multi-septate conidiophoresconidiophores

Emerge from the stromata through Emerge from the stromata through stomata on lower leaf surfacesstomata on lower leaf surfaces

Conidia are single or catenulate (2-4)Conidia are single or catenulate (2-4)Hyaline, cylindrical and slightly flexuousHyaline, cylindrical and slightly flexuousOne to six septate (mostly 3-4)One to six septate (mostly 3-4)3-7 X 240 µm3-7 X 240 µm

PseudocercosporaPseudocercospora angolensisangolensis

Susceptible TissueSusceptible Tissue

Young leaves are highly susceptible Young leaves are highly susceptible to infection from lesions older to infection from lesions older tissuestissues

Young fruit up to golf ball size are Young fruit up to golf ball size are highly susceptiblehighly susceptible

Not certain whether the fruit have a Not certain whether the fruit have a reduced susceptibility or become reduced susceptibility or become immuneimmune

SymptomsSymptoms

Disease SpreadDisease Spread So far restricted to humid tropics of Africa So far restricted to humid tropics of Africa

between 80-1500 mbetween 80-1500 m Favoured by prolonged wet weather Favoured by prolonged wet weather

followed by dry periods with temps between followed by dry periods with temps between 22-2622-26°C°C

Long distance spread by windborne conidiaLong distance spread by windborne conidiaInfected planting material may also contribute to Infected planting material may also contribute to

long distance spreadlong distance spread

Within orchard spread by splash dispersed Within orchard spread by splash dispersed conidiaconidia

Environmental ConditionsEnvironmental Conditions

Pretorius, 2005

ControlsControls Inoculum control via collecting and destroying Inoculum control via collecting and destroying

all fallen fruit and leaves in affected orchardsall fallen fruit and leaves in affected orchards Burying or burning Burying or burning

Plant windbreaks around the citrus orchards Plant windbreaks around the citrus orchards Wind is the primary dispersal agent sporesWind is the primary dispersal agent spores

Discouraging inter-planting in affected Discouraging inter-planting in affected orchards with mature producing treesorchards with mature producing trees Prevents creation of a microclimate of relatively Prevents creation of a microclimate of relatively

cool temperatures and high RHcool temperatures and high RH Potential inoculum source for young treesPotential inoculum source for young trees

Judicious pruning of shoots to allow light Judicious pruning of shoots to allow light penetration into aeration within the tree penetration into aeration within the tree canopycanopy shorten leaf wetness period, lower RH and shorten leaf wetness period, lower RH and

moderate temperaturesmoderate temperaturesSeif and Hillocks, 1993

FungicidesFungicides FungicidesFungicides

Alternate benylate and copper sprays Alternate benylate and copper sprays every 2 weeks from a week following every 2 weeks from a week following the onset of rainsthe onset of rains

When fruit are golf ball sized an When fruit are golf ball sized an addition 3 copper sprays should be addition 3 copper sprays should be applied followed by another benylateapplied followed by another benylate

Seif and Hillocks, 1993 and 1997

Fungal Diseases of Citrus Fruit and Foliage

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