Invasive Species Compendium

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Datasheet

Guignardia citricarpa
(citrus black spot)

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Datasheet

Guignardia citricarpa (citrus black spot)

Summary

  • Last modified
  • 03 October 2018
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Preferred Scientific Name
  • Guignardia citricarpa
  • Preferred Common Name
  • citrus black spot
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Fungi
  •     Phylum: Ascomycota
  •       Subphylum: Pezizomycotina
  •         Class: Dothideomycetes

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Pictures

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PictureTitleCaptionCopyright
Guignardia citricarpa, black spot of green (unripe) lemons.
TitleSymptoms
CaptionGuignardia citricarpa, black spot of green (unripe) lemons.
Copyright©Anna L. Snowdon
Guignardia citricarpa, black spot of green (unripe) lemons.
SymptomsGuignardia citricarpa, black spot of green (unripe) lemons.©Anna L. Snowdon

Identity

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Preferred Scientific Name

  • Guignardia citricarpa Kiely

Preferred Common Name

  • citrus black spot

Other Scientific Names

  • Phoma citricarpa McAlpine
  • Phoma citricarpa var. mikan Hara
  • Phyllosticta citricarpa (McAlpine) Aa
  • Phyllostictina citricarpa (McAlpine) Petr.

International Common Names

  • Spanish: mancha negra de las frutas de cítricos; manchas negras de los agrios
  • French: maladie des taches noires des agrumes; taches noires des fruits des agrumes
  • Portuguese: pinta preta dos citros

Local Common Names

  • Germany: Fruchtfleckigkeit: Zitrus; Schwarzfleckigkeit: Zitrus

EPPO code

  • GUIGCI (Guignardia citricarpa)

Taxonomic Tree

Top of page
  • Domain: Eukaryota
  •     Kingdom: Fungi
  •         Phylum: Ascomycota
  •             Subphylum: Pezizomycotina
  •                 Class: Dothideomycetes
  •                     Order: Botryosphaeriales
  •                         Family: Botryosphaeriaceae
  •                             Genus: Guignardia
  •                                 Species: Guignardia citricarpa

Notes on Taxonomy and Nomenclature

Top of page The position of the black spot fungus within the Ascomycetes has been unclear. Barr (1972) proposed that the genus Guignardia Viola & Ravaz be considered synonymous with Botryosphaeria Ces. & De Not., but the genera currently remain separated. Guignardia differs from Botryosphaeria in having unilocular ascomata, smaller ascospores and different anamorphs. Punithalingam (1974) limited the genus Guignardia to species with Phyllosticta anamorphs and assigned species with other anamorphs to the genus Discosphaerina Höhn. Bissett (1986) proposed that the species of Guignardia with Phyllosticta anamorphs be placed in the genus Discochora Höhn. Currently the anamorph is Phyllosticta citricarpa with a Leptodothiorella spermatial state (van der Aa, 1973).

The anamorph of the black spot fungus was first described by McAlpine (1899) and designated Phoma citricarpa McAlpine. The telemorph was described in 1948 and designated Guignardia citricarpa Kiely (Kiely, 1948). Van der Aa (1973) reclassified the anamorph as Phyllosticta citricarpa (McAlpine) van der Aa.

Two strains of Guignardia citricarpa have long been recognized, one pathogenic to citrus and the other non-pathogenic to citrus and widespread on other hosts (Kiely, 1948; Chiu, 1955; Lee, 1969; Kotzé, 1981). The non-pathogen can be distinguished by its faster growth, colony type, and production of pycnidia in ascocarps in culture. Its geographic distribution is much wider than the type that is pathogenic to citrus. Meyer et al. (2001) considered that the two types represented different species. Baayen et al. (2002) used many of the above characteristics, as well as the presence or absence of a mucoid sheath on conidia, the sequences of the ITS region and amplified fragment length polymorphisms to distinguish the types as species. The widespread non-pathogenic strain is now designated Guignardia mangiferae and the citrus black spot pathogen as Guignardia citricarpa.

Description

Top of page Ascomata of G. citricarpa are formed on fallen, decomposing leaves. Perithecia are aggregated, globose, non-papillate, and about 100-175 µm in diameter (Kotzé, 2000). Asci are cylindrical, clavate, and each contain eight spores. Ascospores are 4.5 x 6.5 µm wide by 12.5-16 µm long, hyaline, nonseptate, multi-guttulate and swollen in the centre. A colourless appendage occurs at each end.

Pycnidia are found in abundance on dead fallen leaves, and are also produced on fruit and peduncles. They are dark brown to black and 115-190 µm in diameter. Conidia are obovate to elliptical, hyaline, nonseptate, multiguttulate with a colourless appendage and are 5.5-7.0 µm wide by 8.0-10.5 µm long.

In culture, colonies of G. citricarpa are dark brown to black and the mycelium is thick and prostrate. On cherry decoction agar, colonies are dark with a wide translucent zone and lobate margins (Baayen et al., 2002). Pycnidia are produced in culture, but if perithecia form they are usually infertile. However, in vitro production of ascospores by G. citricarpa has been reported (Moran Lemir et al., 2000).

Distribution

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Previous records of Guignardia on citrus in some countries may involve the non-pathogenic species Guignardia mangiferae. The countries, states and provinces listed are locations where G. citricarpa is known to be present or where substantial evidence exists that black spot occurs.

G. citricarpa has additionally been reported from Mexico and Japan (Stringari et al., 2009) and but an established presence is not confirmed by other publications.

A record for New Zealand in CMI (1990) refers to G. mangiferae (Everett and Rees-George, 2006).

Records in CMI (1990) for Burma, India, Iran, Israel, Korea Republic, Lebanon, Malaysia, Pakistan, Singapore, Sri Lanka, Thailand, Vietnam, Egypt, Tanzania, Cook Islands, Niue, Tonga, W. Samoa, Fiji, Hawaii (USA), Papua New Guinea, Georgia, Belize, Honduras, Jamaica, Trinidad, Peru, Vanuatu and Venezuela may also be misidentifications.

The situation in Hong Kong, Swaziland and Nigeria is still unclear.

See also CABI/EPPO (1998, No. 204).

 

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Continent/Country/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Asia

AfghanistanAbsent, confirmed by surveyEPPO, 2014
AzerbaijanAbsent, confirmed by surveyEPPO, 2014
BahrainAbsent, confirmed by surveyEPPO, 2014
BangladeshAbsent, unreliable recordEPPO, 2014
BhutanPresentEPPO, 2014
Brunei DarussalamAbsent, confirmed by surveyEPPO, 2014
CambodiaAbsent, confirmed by surveyEPPO, 2014
ChinaRestricted distributionZheng, 1983; CABI/EPPO, 2012; EPPO, 2014
-FujianPresentCABI/EPPO, 2012; EPPO, 2014
-GuangdongPresentCABI/EPPO, 2012; EPPO, 2014
-GuangxiPresentCABI/EPPO, 2012
-Hong KongPresentGrasso, 1970a; Grasso, 1970b; CABI/EPPO, 2012; EPPO, 2014
-JiangsuPresentCABI/EPPO, 2012
-SichuanPresentCABI/EPPO, 2012; EPPO, 2014
-YunnanPresentCABI/EPPO, 2012; EPPO, 2014
-ZhejiangPresentCABI/EPPO, 2012; EPPO, 2014
Georgia (Republic of)Absent, confirmed by surveyEPPO, 2014
IndiaRestricted distributionEPPO, 2014; Das et al., 2018
-AssamAbsent, confirmed by surveyEPPO, 2014
-MaharashtraPresentDas et al., 2018
IndonesiaPresentCABI/EPPO, 2012; EPPO, 2014
-JavaPresentCABI/EPPO, 2012; EPPO, 2014
IranAbsent, confirmed by surveyEPPO, 2014
IraqAbsent, confirmed by surveyEPPO, 2014
IsraelAbsent, confirmed by surveyEPPO, 2014
JapanAbsent, reported but not confirmedCABI/EPPO, 2012; EPPO, 2014
-HonshuAbsent, confirmed by surveyEPPO, 2014
-Ryukyu ArchipelagoAbsent, confirmed by surveyEPPO, 2014
JordanAbsent, confirmed by surveyEPPO, 2014
Korea, Republic ofAbsent, unreliable recordCABI/EPPO, 2012; EPPO, 2014
KuwaitAbsent, confirmed by surveyEPPO, 2014
LebanonAbsent, confirmed by surveyEPPO, 2014
MalaysiaAbsent, confirmed by surveyEPPO, 2014
-Peninsular MalaysiaAbsent, confirmed by surveyEPPO, 2014
-SabahAbsent, confirmed by surveyEPPO, 2014
-SarawakAbsent, confirmed by surveyEPPO, 2014
MyanmarAbsent, confirmed by surveyEPPO, 2014
OmanAbsent, confirmed by surveyEPPO, 2014
PakistanAbsent, confirmed by surveyEPPO, 2014
PhilippinesPresentGrasso, 1970a; Grasso, 1970b; CABI/EPPO, 2012; EPPO, 2014
QatarAbsent, confirmed by surveyEPPO, 2014
Saudi ArabiaAbsent, confirmed by surveyEPPO, 2014
Sri LankaAbsent, confirmed by surveyEPPO, 2014
TaiwanPresentGrasso, 1970a; Grasso, 1970b; Chiu, 1955; Huang and Chang, 1972; CABI/EPPO, 2012; EPPO, 2014
ThailandAbsent, reported but not confirmedCABI/EPPO, 2012; EPPO, 2014
TurkeyAbsent, confirmed by surveyEPPO, 2014
UzbekistanAbsent, confirmed by surveyEPPO, 2014
VietnamAbsent, confirmed by surveyEPPO, 2014
YemenAbsent, confirmed by surveyEPPO, 2014

Africa

AlgeriaAbsent, confirmed by surveyEPPO, 2014
AngolaPresentEPPO, 2014; Bassimba et al., 2018
BeninAbsent, unreliable recordEPPO, 2014
BotswanaAbsent, confirmed by surveyEPPO, 2014
Burkina FasoAbsent, confirmed by surveyEPPO, 2014
CameroonAbsent, confirmed by surveyEPPO, 2014
Central African RepublicAbsent, confirmed by surveyEPPO, 2014
CongoAbsent, confirmed by surveyEPPO, 2014
Congo Democratic RepublicAbsent, confirmed by surveyEPPO, 2014
Côte d'IvoireAbsent, confirmed by surveyEPPO, 2014
EgyptAbsent, confirmed by surveyEPPO, 2014
EthiopiaAbsent, confirmed by surveyEPPO, 2014
GabonAbsent, confirmed by surveyEPPO, 2014
GhanaPresentBrentu et al., 2012; CABI/EPPO, 2012; EPPO, 2014
GuineaAbsent, unreliable recordEPPO, 2014
Guinea-BissauAbsent, confirmed by surveyEPPO, 2014
KenyaPresentCABI/EPPO, 2012; EPPO, 2014
LiberiaAbsent, confirmed by surveyEPPO, 2014
LibyaAbsent, confirmed by surveyEPPO, 2014
MadagascarAbsent, confirmed by surveyEPPO, 2014
MalawiAbsent, confirmed by surveyEPPO, 2014
MauritiusAbsent, confirmed by surveyEPPO, 2014
MoroccoAbsent, confirmed by surveyEPPO, 2014
MozambiqueRestricted distributionCarvalho, 1974; CABI/EPPO, 2012; EPPO, 2014
NamibiaPresent, few occurrencesCABI/EPPO, 2012
NigeriaPresentCABI/EPPO, 2012; EPPO, 2014
SenegalAbsent, confirmed by surveyEPPO, 2014
SeychellesAbsent, confirmed by surveyEPPO, 2014
Sierra LeoneAbsent, confirmed by surveyEPPO, 2014
SomaliaAbsent, confirmed by surveyEPPO, 2014
South AfricaRestricted distributionMcOnie, 1964; Whiteside, 1965; CABI/EPPO, 2012; EPPO, 2014
SudanAbsent, confirmed by surveyEPPO, 2014
SwazilandRestricted distributionCABI/EPPO, 2012; EPPO, 2014
TanzaniaAbsent, confirmed by surveyEPPO, 2014
TogoAbsent, confirmed by surveyEPPO, 2014
TunisiaAbsent, confirmed by surveyEPPO, 2014
UgandaPresentReeder et al., 2009; CABI/EPPO, 2012; EPPO, 2014
ZambiaPresentCABI/EPPO, 2012; EPPO, 2014
ZimbabwePresentWhiteside, 1965; CABI/EPPO, 2012; EPPO, 2014

North America

MexicoAbsent, reported but not confirmedCABI/EPPO, 2012; EPPO, 2014
USARestricted distributionNAPPO, 2010; CABI/EPPO, 2012; EPPO, 2014
-FloridaPresent, few occurrencesNAPPO, 2010; CABI/EPPO, 2012; Schubert et al., 2012; EPPO, 2014
-HawaiiAbsent, confirmed by surveyEPPO, 2014

Central America and Caribbean

Antigua and BarbudaAbsent, confirmed by surveyEPPO, 2014
BahamasAbsent, confirmed by surveyEPPO, 2014
BelizeAbsent, confirmed by surveyEPPO, 2014
Cayman IslandsAbsent, confirmed by surveyEPPO, 2014
Costa RicaAbsent, confirmed by surveyEPPO, 2014
CubaPresentCABI/EPPO, 2012; EPPO, 2014
DominicaAbsent, confirmed by surveyEPPO, 2014
Dominican RepublicAbsent, confirmed by surveyEPPO, 2014
El SalvadorAbsent, confirmed by surveyEPPO, 2014
GrenadaAbsent, confirmed by surveyEPPO, 2014
GuatemalaAbsent, confirmed by surveyEPPO, 2014
HaitiAbsent, confirmed by surveyEPPO, 2014
HondurasAbsent, confirmed by surveyEPPO, 2014
JamaicaAbsent, confirmed by surveyEPPO, 2014
MontserratAbsent, confirmed by surveyEPPO, 2014
NicaraguaAbsent, confirmed by surveyEPPO, 2014
PanamaAbsent, confirmed by surveyEPPO, 2014
Puerto RicoAbsent, confirmed by surveyEPPO, 2014
Saint LuciaAbsent, confirmed by surveyEPPO, 2014
Saint Vincent and the GrenadinesAbsent, confirmed by surveyEPPO, 2014
Trinidad and TobagoAbsent, confirmed by surveyEPPO, 2014

South America

ArgentinaRestricted distributionRodriguez and Mazza Gaiad, 1996; Foguet et al., 1985; Garran, 1996; CABI/EPPO, 2012; EPPO, 2014
BoliviaAbsent, confirmed by surveyEPPO, 2014
BrazilRestricted distributionCABI/EPPO, 2012; EPPO, 2014
-AmazonasPresentCABI/EPPO, 2012
-Espirito SantoPresentCABI/EPPO, 2012
-Minas GeraisPresentCABI/EPPO, 2012
-ParanaPresentCABI/EPPO, 2012
-Rio de JaneiroPresentRobbs et al., 1980; CABI/EPPO, 2012; EPPO, 2014
-Rio Grande do SulPresentRobbs et al., 1980; Robbs and Bittencourt, 1995; CABI/EPPO, 2012; EPPO, 2014
-Santa CatarinaPresentCABI/EPPO, 2012
-Sao PauloPresentGoes and Feichtenberger, 1993; Goes at al., 2000; CABI/EPPO, 2012; EPPO, 2014
ChileAbsent, confirmed by surveyEPPO, 2014
ColombiaAbsent, confirmed by surveyEPPO, 2014
GuyanaAbsent, confirmed by surveyEPPO, 2014
ParaguayAbsent, confirmed by surveyEPPO, 2014
PeruAbsent, confirmed by surveyEPPO, 2014
SurinameAbsent, confirmed by surveyEPPO, 2014
UruguayAbsent, unreliable recordEPPO, 2014
VenezuelaAbsent, confirmed by surveyEPPO, 2014

Europe

AlbaniaAbsent, confirmed by surveyEPPO, 2014
Bosnia-HercegovinaAbsent, confirmed by surveyEPPO, 2014
CroatiaAbsent, confirmed by surveyEPPO, 2014
CyprusAbsent, confirmed by surveyEPPO, 2014
FranceAbsent, confirmed by surveyEPPO, 2014
GreeceAbsent, confirmed by surveyEPPO, 2014
ItalyAbsent, intercepted onlyCABI/EPPO, 2012; EPPO, 2014
-SicilyAbsent, confirmed by surveyEPPO, 2014
MaltaAbsent, confirmed by surveyEPPO, 2014
MontenegroAbsent, confirmed by surveyEPPO, 2014
NetherlandsAbsent, intercepted onlyNPPO of the Netherlands, 2013; EPPO, 2014
PortugalAbsent, confirmed by surveyEPPO, 2014
Russian FederationPresentPresent based on regional distribution.
-Russian Far EastPresentCMI, 1990
SpainAbsent, intercepted onlyCABI/EPPO, 2012; EPPO, 2014
-Spain (mainland)Absent, intercepted onlyCABI/EPPO, 2012

Oceania

American SamoaAbsent, confirmed by surveyEPPO, 2014
AustraliaRestricted distributionCABI/EPPO, 2012; EPPO, 2014
-New South WalesPresentCABI/EPPO, 2012; EPPO, 2014
-QueenslandPresentCABI/EPPO, 2012; EPPO, 2014
-VictoriaPresentEPPO, 2014
Cook IslandsAbsent, invalid recordCABI/EPPO, 2012; EPPO, 2014
FijiAbsent, invalid recordCABI/EPPO, 2012; EPPO, 2014
French PolynesiaAbsent, confirmed by surveyEPPO, 2014
GuamAbsent, confirmed by surveyEPPO, 2014
New ZealandAbsent, invalid recordCABI/EPPO, 2012; EPPO, 2014
NiueAbsent, invalid recordCABI/EPPO, 2012; EPPO, 2014
Papua New GuineaAbsent, unreliable recordEPPO, 2014
SamoaAbsent, invalid recordCABI/EPPO, 2012; EPPO, 2014
TongaAbsent, invalid recordCABI/EPPO, 2012; EPPO, 2014
VanuatuAbsent, reported but not confirmedCABI/EPPO, 2012; EPPO, 2014
Wallis and Futuna IslandsAbsent, confirmed by surveyEPPO, 2014

Growth Stages

Top of page Fruiting stage, Post-harvest, Vegetative growing stage

Symptoms

Top of page Several different types of symptoms occur on citrus, generally referred to as hard or shot hole spot, false melanose, freckle spot and virulent spot. The lesions of hard spot generally occur on mature fruit and are several millimeters in diameter. These spots are crater-like with a light centre, a dark-brown to black rim, and often have a green halo on mature orange fruit. Pycnidia are often apparent in these lesions. False melanose usually appears on green fruit and consists of raised dark-brown to black specks that may coalesce. No pycnidia form on these lesions and the pathogen is difficult to isolate. Freckle spots are orange to red, slightly depressed, 1-3 mm in diameter and occur late in the season. The spots turn brown with age. Virulent spots are large, slightly sunken and spread irregularly over large areas of the mature fruit. The pathogen is most readily isolated from these types of lesions and pycnidia may eventually form.

Leaf lesions are uncommon on most citrus but may be more frequent on lemons. Lesions are small, sunken necrotic spots with light centre and a dark rim and may have a chlorotic halo.

List of Symptoms/Signs

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SignLife StagesType
Fruit / extensive mould
Fruit / lesions: black or brown
Fruit / lesions: scab or pitting
Leaves / abnormal colours
Leaves / abnormal leaf fall
Stems / discoloration of bark

Biology and Ecology

Top of page Biotypes

Initially two strains were recognized, the pathogenic and the non-pathogenic. These have now been separated in to two species, Guignardia citricarpa and G. mangiferae. However, both species occur on citrus fruit (Sutton and Waterston, 1966). G. citricarpa causes black spot and can be readily isolated from certain lesion types. G. mangiferae is most commonly recovered from wounds on fruit produced by mechanical injury, spray burns or other damage.

The cultural characteristics and morphology of Phoma citricarpa and P. citricarpa var. mikan and their teleomorphs were compared (Wang and Tsai, 1974). No differences were found between the two taxa in morphology, sporulation or other characteristics when grown on several types of media at varying temperatures. Studies of the formation of conidiomata, conidia and spore ooze showed that the size of conidia varied with media type, temperature and light conditions. The teleomorph of the two taxa produce ascospores of the same size and shape when grown on potato dextrose agar with plant tissue. The authors concluded that there was insufficient information to separate the two taxa on the basis of morphological criteria (Wang and Tsai, 1974).

Epidemiology

Ascospores from infected, fallen leaves are the major source of inoculum (McOnie, 1967; Timmer, 1999; Kotze, 2000). Pseudothecial development in decomposing leaves occurs from 40 to 180 days after leaf fall, depending on the frequency of wetting and drying. The optimum temperature for ascomata formation is 21-28°C and no pseudothecia are formed below 7°C or above 35°C (Lee and Huang, 1973). Prolonged periods of wetness prevent pseudothecia formation since the leaves are rapidly colonized by competing saprobes. Once ascospores are mature, rainfall or irrigation may trigger their release. Ascospores are carried by wind throughout the canopy and long distances beyond (Huang and Chang, 1972).

When ascospores are deposited on fruit or vegetative tissues under moist conditions, they germinate to form an appressorium (Timmer, 1999; Kotzé, 2000). An infection peg penetrates the cuticle and epidermis to form quiescent infections on leaves or fruit. Quiescent infections on fruit develop to produce the typical black spot symptom after the fruit attains full size or becomes mature. Such infection on leaves seldom develops. However, the fungus colonizes the leaf as a saprophyte after the leaf dies and eventually forms pycnidia or pseudothecia.

The anamorph probably plays only a minor role in the disease cycle (Timmer, 1999; Kotze, 2000). Conidia produced on the leaves and fruit in the canopy are capable of infecting the leaves and fruit. However, conidia produced on dead leaves can only reach susceptible fruit and leaves by splash dispersal into the canopy. Conidia produced on fruit can be washed down through the canopy and infect leaves and younger fruit that are still at the susceptible stage.

In most subtropical citrus areas, leaf fall occurs just before or about the time of bloom. Fruit are susceptible for at least 4-5 months after petal fall. Ascospores are released whenever conditions are favorable during that time and produce the quiescent infections. Thus infections probably occur throughout spring until at least mid-summer whenever conditions are favorable. Fruit must be protected during that entire time to achieve a high degree of control.

Plant Trade

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Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
Flowers/Inflorescences/Cones/Calyx hyphae; spores Yes Yes Pest or symptoms usually visible to the naked eye
Fruits (inc. pods) hyphae; spores Yes Yes Pest or symptoms usually visible to the naked eye
Leaves hyphae; spores Yes Yes Pest or symptoms usually visible to the naked eye
Stems (above ground)/Shoots/Trunks/Branches hyphae; spores Yes Yes Pest or symptoms usually visible to the naked eye
Plant parts not known to carry the pest in trade/transport
Bulbs/Tubers/Corms/Rhizomes
Growing medium accompanying plants
Roots
Seedlings/Micropropagated plants
Wood

Impact

Top of page Black spot has been present in Australia, South Africa and parts of Asia for many years (Kotze, 2000). Most of the losses in Australia and South Africa have been due to the external blemishes which make fruit unsuitable for the fresh market. Some losses to fruit drop occurred in years favourable for disease development and when fruit was held on the trees past peak maturity. However, now that black spot is well established in areas of southern South America, fruit losses may periodically be severe. Internal quality of fruit may also be affected. Total soluble solids were unaffected in black spot affected fruit, but acid was lower (Anon., 1988).

Latent infections are common on leaves and occasionally symptoms appear. No harmful effects from leaf infection have been reported.

Diagnosis

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A method for detection of G. citricarpa using loop-mediated isothermal amplification (LAMP) has been developed which can be used to confirm the presence of G. citricarpa in black spot lesions, including those lacking pycnidia (Tomlinson et al., 2013). The LAMP assay can be used to test crude extracts prepared directly from lesions on fruit, and the entire test is faster than previously described PCR-based methods for detection of G. citricarpa. The method is sufficiently simple to allow deployment of the test in the field, for example, in the course of import inspections.

Detection and Inspection

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Often black spot can be identified with considerable certainty if hard spot lesions with pycnidia are present. However, freckle spot, false melanose and virulent spot can be confused with many other diseases and injuries (Kotze, 2000). G. citricarpa is isolated relatively easily from virulent spot or hard spot lesions, but may be difficult or impossible to isolate from the other symptom types.

Once a species of Guignardia has been isolated from symptomatic tissue, the species involved must be determined. G. citricarpa grows more slowly on cherry decoction agar than G. mangiferae, produces lighter colonies which are more lobate, with a wider translucent zone than G. mangiferae (Baayen et al., 2001). G. citricarpa produces a yellow pigment on oatmeal agar not produced by G. mangiferae. G. mangiferae usually produces fertile perithecia in culture whereas G. citricarpa does not. Conidia of G. citricarpa lack the visible mucoid sheath present on those of G. mangiferae.

The two species can also be distinguished by Amplified Fragment Length Polymorphism (AFLP) analysis or sequencing of the ITS spacer region (Baayen et al., 2000).

Identification of species of Guignardia from citrus requires isolation of the slow-growing fungus and comparison of several of the above-listed traits to verify the identity. Proof of pathogenicity requires inoculation of fruit or leaves and an incubation period of weeks or months before symptoms appear (Kotze, 2000). Thus, detection and identification is currently difficult and time-consuming. However, species-specific primers from the ITS region and other regions of the genome have been developed (Sanders et al., 2003). These primers are quite reliable for differentiation of the two species when used with pure cultures of the fungus. If they prove successful for detection and identification of species using colonized plant material they should greatly speed diagnosis of black spot.

Polymerase chain reaction (PCR) can be used to diagnose G. citricarpa. Bonants et al. (2003) recorded the efficiency of PCR-based detection methods as 60-70% for lesions without pycnidia and 90% for lesions with pycnidia, and a reliability of 99% by analysing multiple lesions per sample. Gent-Pelzer et al. (2007) developed a TaqMan PCR method for the diagnosis of G. citricarpa on citrus fruit which was more sensitive than conventional PCR. Their specific primer/TaqMan probe was able to discriminate between G. citricarpa and G. mangiferae. Stringari et al. (2009) used random amplified polymorphic DNA (RAPD) markers to develop specific primers for the identification of G. citricarpa with PCR.

Detection based on host plant symptoms and identification by morphological and molecular methods are detailed in OEPP/EPPO (2003; 2009).

Prevention and Control

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Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Exclusion

Efforts have been made to exclude black spot from areas where it is not currently present. Clearly, living or dead vegetative tissues represent a high risk for introduction since airborne ascospores can be produced on these tissues under favourable conditions. Living trees or even budwood could carry quiescent infections. The importance of dispersal by fruit has been questioned since the fungus produces only water-dispersed conidia on symptomatic fruit (Kotze, 2000).

Sanitation

The removal of infected, off-season fruit may be useful to reduce conidial inoculum in some situations (Kotze, 1981). Mechanical removal of leaf litter from the orchard floor reduces disease pressure and facilitates control, but is costly.


Host-Plant Resistance

Sour orange (Citrus aurantium) is one of the few species of citrus that is resistant to black spot. Grapefruit (C. paradisi) and lemons (C. limon) are the most susceptible, whereas some mandarins (C. reticulata) are more tolerant (Kotze, 2000). Some attempts have been made to produce tolerant hybrids using sour orange as a source of resistance (Anon., 1974). It is unlikely that conventional breeding will produce commercially useful, tolerant cultivars in the foreseeable future. Genetic modification holds more promise for developing resistant cultivars, but progress is likely to be slow using these methods.

Chemical Control

A number of fungicides such as copper products, dithiocarbamates, benzimidazoles and strobilurins are effective against black spot. However, resistance has developed to benzimidazoles in many areas (Kotze, 2000; Goes et al., 2000; Goes, 2002) and there is a potential problem with strobilurins. Fungicides must be chosen carefully to minimize the possible development of resistance.

For many years, protective products such as the coppers and dithiocarbamates were the basis for the control program ( Bertus, 1981; Kiely, 1950,1976; Kotzé, 1981; Tsai, 1981). Subsequently mid-summer postinfectional applications of benzimidazoles were sufficient for control in many areas (Kellerman and Kotzé, 1973, 1979). However, with the development of resistance (Herbert and Grech, 1985) many growers have returned to the use of protectant sprays or combinations of systemic and protectant products (Goes et al., 2000; Goes, 2002).

Spore trapping and rainfall and dew measurements have been helpful in determining the timing of ascospore release and the need for fungicide applications in South Africa (Kotze, 2000). In Brazil, infections seem to occur to varying degrees throughout the susceptible period and fruit must be protected from petal fall to mid-summer (Reis, 2002).


Postharvest

Fruit from black spot-infested groves often bear quiescent infections that may later develop into black spot lesions in transport or at the final destination (Hall, 1973). Fruit produced for the fresh market should be refrigerated and kept as cold as possible to slow development of the lesions. On the other hand, if it is desirable that black spot symptoms are expressed as soon as possible for detection of the disease, then fruit should be held at 27°C under continuous light.

Preharvest sprays of benzimidazole fungicides are effective in preventing or delaying symptom expression during transport or storage (Nam et al., 1993). Postharvest applications of fungicides are generally less effective in preventing symptom development (Andrade et al., 2001a, b). However, treatment with guazatine or imazalil, hot water or waxing decreased the viability of the pathogen in black spot lesions (Korf et al., 2001). Postharvest waxing also decreased the manifestation of symptoms following postharvest storage (Wild, 1981).

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