Invasive Species Compendium

Detailed coverage of invasive species threatening livelihoods and the environment worldwide

Datasheet

Guignardia citricarpa
(citrus black spot)

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Datasheet

Guignardia citricarpa (citrus black spot)

Summary

  • Last modified
  • 10 March 2021
  • 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

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

Notes on Taxonomy and Nomenclature

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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

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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.

A record of G. citricarpa in Victoria, Australia (EPPO, 2020) published in previous versions of the Compendium is considered erroneous. The record was based on herbarium specimens (CMI, 1983; CMI, 1990) but no information on the State or locality of the specimens could be retrieved. According to Agriculture Victoria (Biosecurity & Agriculture Services (DJPR), Agriculture Victoria, communication to CABI, 2021), G. citricarpa has never been found in Victoria.

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.

Last updated: 20 Jul 2021
Continent/Country/Region Distribution Last Reported Origin First Reported Invasive Reference Notes

Africa

AlgeriaAbsent, Confirmed absent by survey
AngolaPresent
BeninAbsent, Unconfirmed presence record(s)
BotswanaAbsent, Confirmed absent by survey
Burkina FasoAbsent, Confirmed absent by survey
CameroonAbsent, Unconfirmed presence record(s)
Central African RepublicAbsent, Confirmed absent by survey
Congo, Democratic Republic of theAbsent, Confirmed absent by survey
Congo, Republic of theAbsent, Confirmed absent by survey
Côte d'IvoireAbsent, Confirmed absent by survey
EgyptAbsent, Confirmed absent by survey
EswatiniAbsent, Unconfirmed presence record(s)
EthiopiaAbsent, Confirmed absent by survey
GabonAbsent, Confirmed absent by survey
GhanaPresent
GuineaAbsent, Unconfirmed presence record(s)
Guinea-BissauAbsent, Confirmed absent by survey
KenyaPresent
LiberiaAbsent, Confirmed absent by survey
LibyaAbsent, Confirmed absent by survey
MadagascarAbsent, Confirmed absent by survey
MalawiAbsent, Confirmed absent by survey
MauritiusAbsent, Confirmed absent by survey
MoroccoAbsent, Confirmed absent by survey
MozambiquePresent, Localized
NamibiaPresent, Few occurrences
NigeriaAbsent, Unconfirmed presence record(s)
SenegalAbsent, Confirmed absent by survey
SeychellesAbsent, Confirmed absent by survey
Sierra LeoneAbsent, Confirmed absent by survey
SomaliaAbsent, Confirmed absent by survey
South AfricaPresent, Localized
SudanAbsent, Confirmed absent by survey
TanzaniaAbsent, Confirmed absent by survey
TogoAbsent, Unconfirmed presence record(s)
TunisiaPresent
UgandaPresent
ZambiaPresent
ZimbabwePresent

Asia

AfghanistanAbsent, Confirmed absent by survey
AzerbaijanAbsent, Confirmed absent by survey
BahrainAbsent, Confirmed absent by survey
BangladeshAbsent, Unconfirmed presence record(s)
BhutanPresent
BruneiAbsent, Confirmed absent by survey
CambodiaAbsent, Confirmed absent by survey
ChinaPresent, Localized
-ChongqingPresent
-FujianPresent
-GuangdongPresent
-GuangxiPresent
-JiangsuPresent
-JiangxiPresent
-SichuanPresent
-YunnanPresent
-ZhejiangPresent
GeorgiaAbsent, Confirmed absent by survey
Hong KongPresent
IndiaPresent, Localized
-AssamAbsent, Confirmed absent by survey
-MaharashtraPresent
-Tamil NaduPresent
IndonesiaPresent
-JavaPresent
IranAbsent, Confirmed absent by survey
IraqAbsent, Confirmed absent by survey
IsraelAbsent, Confirmed absent by survey
JapanAbsent, Unconfirmed presence record(s)
-HonshuAbsent, Confirmed absent by survey
-Ryukyu IslandsAbsent, Confirmed absent by survey
JordanAbsent, Confirmed absent by survey
KuwaitAbsent, Confirmed absent by survey
LebanonAbsent, Confirmed absent by survey
MalaysiaAbsent, Confirmed absent by survey
-Peninsular MalaysiaAbsent, Confirmed absent by survey
-SabahAbsent, Confirmed absent by survey
-SarawakAbsent, Confirmed absent by survey
MyanmarAbsent, Confirmed absent by survey
OmanAbsent, Confirmed absent by survey
PakistanAbsent, Confirmed absent by survey
PhilippinesPresent
QatarAbsent, Confirmed absent by survey
Saudi ArabiaAbsent, Confirmed absent by survey
South KoreaAbsent, Unconfirmed presence record(s)
Sri LankaAbsent, Confirmed absent by survey
TaiwanPresent
ThailandAbsent, Unconfirmed presence record(s)
TurkeyAbsent, Confirmed absent by survey
UzbekistanAbsent, Confirmed absent by survey
VietnamAbsent, Confirmed absent by survey
YemenAbsent, Confirmed absent by survey

Europe

AlbaniaAbsent, Confirmed absent by survey
BelgiumAbsent, Intercepted only
Bosnia and HerzegovinaAbsent, Confirmed absent by survey
CroatiaAbsent, Confirmed absent by survey
CyprusAbsent, Confirmed absent by survey
FranceAbsent, Confirmed absent by survey
GreeceAbsent, Confirmed absent by survey
ItalyAbsent, Intercepted only
-SicilyAbsent, Confirmed absent by survey
MaltaAbsent, Confirmed absent by survey
MontenegroAbsent, Confirmed absent by survey
NetherlandsAbsent, Intercepted only
PortugalAbsent, Confirmed absent by survey
RussiaPresentPresent based on regional distribution.
-Russian Far EastPresent
SloveniaAbsent, Intercepted only
SpainAbsent, Intercepted only

North America

Antigua and BarbudaAbsent, Confirmed absent by survey
BahamasAbsent, Confirmed absent by survey
BelizeAbsent, Confirmed absent by survey
Cayman IslandsAbsent, Confirmed absent by survey
Costa RicaAbsent, Confirmed absent by survey
CubaPresent
DominicaAbsent, Confirmed absent by survey
Dominican RepublicAbsent, Confirmed absent by survey
El SalvadorAbsent, Confirmed absent by survey
GrenadaAbsent, Confirmed absent by survey
GuatemalaAbsent, Confirmed absent by survey
HaitiAbsent, Confirmed absent by survey
HondurasAbsent, Confirmed absent by survey
JamaicaAbsent, Confirmed absent by survey
MexicoAbsent, Unconfirmed presence record(s)
MontserratAbsent, Confirmed absent by survey
NicaraguaAbsent, Confirmed absent by survey
PanamaAbsent, Confirmed absent by survey
Puerto RicoAbsent, Confirmed absent by survey
Saint LuciaAbsent, Confirmed absent by survey
Saint Vincent and the GrenadinesAbsent, Confirmed absent by survey
Trinidad and TobagoAbsent, Confirmed absent by survey
United StatesPresent, Localized
-FloridaPresent, Localized
-HawaiiAbsent, Confirmed absent by survey

Oceania

American SamoaAbsent, Confirmed absent by survey
AustraliaPresent, Localized
-New South WalesPresent
-QueenslandPresent
-VictoriaAbsent, Invalid presence record(s)
Cook IslandsAbsent, Invalid presence record(s)
FijiAbsent, Invalid presence record(s)
French PolynesiaAbsent, Confirmed absent by survey
GuamAbsent, Confirmed absent by survey
New ZealandAbsent, Invalid presence record(s)
NiueAbsent, Invalid presence record(s)
Papua New GuineaAbsent, Unconfirmed presence record(s)
SamoaAbsent, Invalid presence record(s)
TongaAbsent, Invalid presence record(s)
VanuatuAbsent, Unconfirmed presence record(s)
Wallis and FutunaAbsent, Confirmed absent by survey

South America

ArgentinaPresent, Localized
BoliviaAbsent, Confirmed absent by survey
BrazilPresent, Localized
-AmazonasPresent
-Espirito SantoPresent
-Minas GeraisPresent
-ParanaPresent
-Rio de JaneiroPresent
-Rio Grande do SulPresent
-Santa CatarinaPresent
-Sao PauloPresent
ChileAbsent, Unconfirmed presence record(s)
ColombiaAbsent, Confirmed absent by survey
GuyanaAbsent, Confirmed absent by survey
ParaguayAbsent, Confirmed absent by survey
PeruAbsent, Confirmed absent by survey
SurinameAbsent, Confirmed absent by survey
UruguayPresent
VenezuelaAbsent, Confirmed absent by survey

Growth Stages

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Fruiting stage, Post-harvest, Vegetative growing stage

Symptoms

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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

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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

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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).

References

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Alves, A., Phillips, A. J. L., Henriques, I., Correia, A., 2007. Rapid differentiation of species of Botryosphaeriaceae by PCR fingerprinting. Research in Microbiology, 158(2), 112-121. doi: 10.1016/j.resmic.2006.10.003

AVA, 2001. Diagnostic records of the Plant Health Diagnostic Services, Plant Health Centre, Agri-food & Veterinary Authority, Singapore

Baayen RP, Bonants PJM, Verkley G, Carroll GC, Aa HAvan der, Weerdt Mde, Brouwershaven IRvan, Schutte GC, Maccheroni WJr, Blanco CGde, Azevedo JL, 2002. Nonpathogenic isolates of the citrus black spot fungus, Guignardia citricarpa, identified as a cosmopolitan endophyte of woody plants, G. mangiferae (Phyllosticta capitalensis). Phytopathology, 92(5):464-477; 43 ref

Barr ME, 1972. Preliminary studies on the Dothideales in temperate North America. Contrib. Univ. Mich. Herb., 9:523-638

Bassimba, D. D. M., Nzambi, N., Paixão, M. I. S., Katula, I. G., Vicent, A., 2018. First report of citrus black spot caused by Phyllosticta citricarpa in Angola. Plant Disease, 102(3), 683. http://apsjournals.apsnet.org/loi/pdis doi: 10.1094/pdis-09-17-1374-pdn

Bertus AL, 1981. Fungicidal control of black spot and melanose on coastal Valencia oranges in New South Wales. Australasian Plant Pathology, 10(3):53-55

Biosecurity & Agriculture Services (DJPR), Agriculture Victoria, 2021. communication to CABI. Australia: Agriculture Victoria.

Bissett J, 1986. A note on the typification of Guignardia. Mycotaxon, 25:519-522

Bonants PJM, Carroll GC, Weerdt Mde, Brouwershaven IRvan, Baayen RP, 2003. Development and validation of a fast PCR-based detection method for pathogenic isolates of the citrus black spot fungus, Guignardia citricarpa. European Journal of Plant Pathology, 109(5):503-513

Brentu FC, Oduro KA, Offei SK, Odamtten GT, Vicent A, Peres NA, Timmer LW, 2012. Crop loss, aetiology, and epidemiology of citrus black spot in Ghana. European Journal of Plant Pathology, 133(3):657-670. http://springerlink.metapress.com/link.asp?id=100265

CABI/EPPO, 1998. Distribution maps of quarantine pests for Europe (edited by Smith IM, Charles LMF). Wallingford, UK: CAB International, xviii + 768 pp

CABI/EPPO, 2012. Phyllosticta citricarpa. [Distribution map]. Distribution Maps of Plant Diseases, No.October. Wallingford, UK: CABI, Map 53 (Edition 7)

Carvalho MC de, 1974. Pests and diseases of citrus fruits and treatments recommended in Sofala and Tete. Gazeta do Agricultor, 26(298):162-191

Chiu RJ, 1955. Studies on black spot of citrus. J. Agric. For., 9:1-8

CMI, 1990. Distribution Maps of Plant Diseases. Map No. 53. Edition 5. Wallingford, UK: CAB International

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