Invasive Species Compendium

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Datasheet

Pseudocercospora angolensis
(leaf spot of Citrus spp.)

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Datasheet

Pseudocercospora angolensis (leaf spot of Citrus spp.)

Summary

  • Last modified
  • 27 September 2018
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Preferred Scientific Name
  • Pseudocercospora angolensis
  • Preferred Common Name
  • leaf spot of Citrus spp.
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Fungi
  •     Phylum: Ascomycota
  •       Subphylum: Pezizomycotina
  •         Class: Dothideomycetes
  • Summary of Invasiveness
  • P. angolensis is a dematiaceous hyphomycete occurring in sub-Saharan Africa and Yemen. This fungus requires moisture for infection and the production of wind-borne conidia and causes a devastating fruit and leaf...

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Pictures

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PictureTitleCaptionCopyright
Sporulation in lesion on Citrus sinensis. Original X55.
TitleSporulation in lesion
CaptionSporulation in lesion on Citrus sinensis. Original X55.
CopyrightUSDA-ARS/Systematic Mycology & Microbiology Laboratory
Sporulation in lesion on Citrus sinensis. Original X55.
Sporulation in lesionSporulation in lesion on Citrus sinensis. Original X55.USDA-ARS/Systematic Mycology & Microbiology Laboratory
Pseudocercospora angolensis; conidia.  Original X1000.
TitleConidia
CaptionPseudocercospora angolensis; conidia. Original X1000.
CopyrightUSDA-ARS/Systematic Mycology & Microbiology Laboratory
Pseudocercospora angolensis; conidia.  Original X1000.
ConidiaPseudocercospora angolensis; conidia. Original X1000.USDA-ARS/Systematic Mycology & Microbiology Laboratory
P. angolensis leaf spots. CMI Descriptions of Pathogenic Fungi and Bacteria No. 843. CAB International, Wallingford, UK.
TitleP. angolensis leaf spots - line drawing
CaptionP. angolensis leaf spots. CMI Descriptions of Pathogenic Fungi and Bacteria No. 843. CAB International, Wallingford, UK.
CopyrightCAB International
P. angolensis leaf spots. CMI Descriptions of Pathogenic Fungi and Bacteria No. 843. CAB International, Wallingford, UK.
P. angolensis leaf spots - line drawingP. angolensis leaf spots. CMI Descriptions of Pathogenic Fungi and Bacteria No. 843. CAB International, Wallingford, UK.CAB International

Identity

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Preferred Scientific Name

  • Pseudocercospora angolensis (T. de Carvalho & O. Mendes) Crous & U. Braun 2003

Preferred Common Name

  • leaf spot of Citrus spp.

Other Scientific Names

  • Cercospora angolensis T. de Carvalho & O. Mendes 1953
  • Phaeoramularia angolensis (T. de Carvalho & O. Mendes) P.M. Kirk 1986
  • Pseudophaeoramularia angolensis (T. de Carvalho & O. Mendes) U. Braun 1999

International Common Names

  • English: Cercospora fruit and leaf spot; cercosporiose of citrus; fruit and leaf spot of citrus; Phaeoramularia fruit and leaf spot
  • French: Cercosporiose des agrumes

Local Common Names

  • Germany: Blattfleckenkrankheit: Zitrus
  • Portugal: Cercosporiose em Citrinos

EPPO code

  • CERCAN (Phaeoramularia angolensis)

Summary of Invasiveness

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P. angolensis is a dematiaceous hyphomycete occurring in sub-Saharan Africa and Yemen. This fungus requires moisture for infection and the production of wind-borne conidia and causes a devastating fruit and leaf spot disease of cultivated species of Citrus. Losses of 50-100% of yield can occur and growers may cease production where the disease is endemic. Although species and cultivars of Citrus vary in susceptibility, no source of resistance is known (Kuate, 1998). An A1 quarantine pest for Europe and the Mediterranean region (EPPO, 2009), this fungus is also of concern for other warm humid regions where citrus is grown, such as Florida, USA. Other than by wind, conidia can be transported on infected fruit or propagated material.

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Fungi
  •         Phylum: Ascomycota
  •             Subphylum: Pezizomycotina
  •                 Class: Dothideomycetes
  •                     Subclass: Dothideomycetidae
  •                         Order: Capnodiales
  •                             Family: Mycosphaerellaceae
  •                                 Genus: Pseudocercospora
  •                                     Species: Pseudocercospora angolensis

Notes on Taxonomy and Nomenclature

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This species was first described as Cercospora angolensis by de Carvalho and Mendes (1953), causing a leaf spot on Citrus sinensis in Angola. It was subsequently reported by Emechebe (1981) as Phaeoisariopsis sp. from Citrus in Nigeria and from other citrus-growing areas in Africa (see Seif and Hillocks, 1993). Kirk (1986) transferred it to the genus Phaeoramularia because the pale-brown conidia are produced in chains and the scars at the conidiogenous loci are conspicuous and slightly pigmented (Pretorius et al., 2003). Braun (1999) assigned it to a new genus, Pseudophaeoramularia, because the scars on the conidiogenous cells are unthickened, i.e. the conidiogenous loci do not fit with those of the former genus Phaeoramularia (now Passalora emend., see Crous and Braun, 2003). Crous and Braun (in Pretorius et al., 2003) carried out molecular analyses and reassessments of conidiogenesis and the structure of the conidiogenous loci. They determined that the conidiophore morphology is not distinct from that of the genus Pseudocercospora. Other species of Pseudocercospora also produce short conidial chains. Furthermore, P. angolensis clustered in molecular sequence analyses with other species of Pseudocercospora. Consequently, Cercospora angolensis is placed in Pseudocercospora (Pretorius et al., 2003).

Description

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Conidiophores solitary, fasciculate, or forming loose synnemata 12-45 µm wide, unbranched, septate, smooth, pale-brown to brown, (60-)120-240 x 4.5-7 µm, usually arising from a dark stroma, 30-60 µm diameter.

Conidiogenous cells terminal, slightly geniculate, scars conspicuous, but unthickened and only slightly pigmented.

Conidia solitary or in simple or branched chains of 2-4, cylindrical to narrowly obclavate, straight or slightly flexuous to more or less curved, smooth, hyaline to very pale-brown, (1-)3-4(-6)-septate, 24-79 x 4-5 (-6.5) µm, apex rounded, base truncate. Basal and apical scars slightly thickened and pigmented, 2-3 µm.

For additional details, see Kirk (1986).

Distribution

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P. angolensis appears to be restricted primarily to the humid tropics in Africa between altitudes of 80 and 1500 m (Brun, 1972; Seif et al., 1989). It has also been reported from Yemen (Kirk, 1986). Derso (1999) and Mohammed Yesuf (2007) describe the spread and impact of the fungus in Ethiopia. As of 2008, it was no closer to the citrus-producing regions of South Africa than the moister northern part of Zimbabwe (Pretorius and Holtz, 2008).

P. angolensis was reported in Sierra Leone in 2010 (Harling et al., 2010) and has been recorded in Ghana (Cornelius and Entsie, 2010Alidu et al., 2013; Brentu et al., 2013). A review of the disease by Mohammed Yesuf (2013) includes a history of the occurrence of P. angolensis in Africa.

See also CABI/EPPO (1998, No. 223).

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, confirmed by surveyEPPO, 2014
BhutanAbsent, confirmed by surveyEPPO, 2014
Brunei DarussalamAbsent, confirmed by surveyEPPO, 2014
CambodiaAbsent, confirmed by surveyEPPO, 2014
ChinaAbsent, confirmed by surveyEPPO, 2014
Georgia (Republic of)Absent, confirmed by surveyEPPO, 2014
IndiaAbsent, confirmed by surveyEPPO, 2014
IndonesiaAbsent, confirmed by surveyEPPO, 2014
IranAbsent, confirmed by surveyEPPO, 2014
IraqAbsent, confirmed by surveyEPPO, 2014
IsraelAbsent, confirmed by surveyEPPO, 2014
JapanAbsent, confirmed by surveyEPPO, 2014
JordanAbsent, confirmed by surveyEPPO, 2014
Korea, Republic ofAbsent, confirmed by surveyEPPO, 2014
KuwaitAbsent, confirmed by surveyEPPO, 2014
LebanonAbsent, confirmed by surveyEPPO, 2014
MalaysiaAbsent, confirmed by surveyEPPO, 2014
MyanmarAbsent, confirmed by surveyEPPO, 2014
OmanAbsent, confirmed by surveyEPPO, 2014
PakistanAbsent, confirmed by surveyEPPO, 2014
PhilippinesAbsent, confirmed by surveyEPPO, 2014
QatarAbsent, confirmed by surveyEPPO, 2014
Saudi ArabiaAbsent, confirmed by surveyEPPO, 2014
Sri LankaAbsent, confirmed by surveyEPPO, 2014
TaiwanAbsent, confirmed by surveyEPPO, 2014
ThailandAbsent, confirmed by surveyEPPO, 2014
TurkeyAbsent, confirmed by surveyEPPO, 2014
UzbekistanAbsent, confirmed by surveyEPPO, 2014
VietnamAbsent, confirmed by surveyEPPO, 2014
YemenPresentKirk, 1986; Seif and Hillocks, 1993; UK CAB International, 1996; EPPO, 2014

Africa

AlgeriaAbsent, confirmed by surveyEPPO, 2014
AngolaWidespreadDe and Carvalho Mendes, 1952; Seif and Hillocks, 1993; UK CAB International, 1996; Ragazzi, 1997; EPPO, 2014
BeninAbsent, confirmed by surveyEPPO, 2014
BotswanaAbsent, confirmed by surveyEPPO, 2014
Burkina FasoAbsent, confirmed by surveyEPPO, 2014
BurundiPresentSeif and Hillocks, 1993; Kuate, 1998; EPPO, 2014
CameroonRestricted distributionMenyonga, 1971; Seif and Hillocks, 1993; UK CAB International, 1996; EPPO, 2014
Central African RepublicPresentBrun, 1972; Seif and Hillocks, 1993; EPPO, 2014
ComorosPresentAubert, 1984; Seif and Hillocks, 1993; EPPO, 2014
CongoPresentBrun, 1972; Seif and Hillocks, 1993; EPPO, 2014
Congo Democratic RepublicPresentBrun, 1972; Seif and Hillocks, 1993; UK CAB International, 1996; EPPO, 2014
Côte d'IvoirePresentBrun, 1972; Seif and Hillocks, 1993; EPPO, 2014
EgyptAbsent, confirmed by surveyEPPO, 2014
EthiopiaLocalisedIntroduced Invasive UK CAB International, 1996; Derso, 1999; EPPO, 2014
GabonPresentSeif and Hillocks, 1993; UK CAB International, 1996; EPPO, 2014
GambiaPresentUK CAB International, 1996; Crous Braun, 2003; EPPO, 2014
GhanaPresentBrentu et al., 2013; EPPO, 2014
GuineaLocalisedIntroduced Invasive Diallo, 2001; EPPO, 2014
Guinea-BissauAbsent, confirmed by surveyEPPO, 2014
KenyaPresentIntroduced1972 Invasive Seif and Whittle, 1984b; Seif and Hillocks, 1993; IPPC-Secretariat, 2005; 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
MozambiquePresentDe and Carvalho Mendes, 1952; Seif and Hillocks, 1993; UK CAB International, 1996; EPPO, 2014
NigeriaPresentEmechebe, 1981; Seif and Hillocks, 1993; EPPO, 2014
RwandaPresentKuate, 1998
SenegalAbsent, confirmed by surveyEPPO, 2014
SeychellesAbsent, confirmed by surveyEPPO, 2014
Sierra LeonePresentHarling et al., 2010; EPPO, 2012; EPPO, 2014EPPO Reporting Service, No. 2012/061.
SomaliaAbsent, confirmed by surveyEPPO, 2014
South AfricaAbsent, confirmed by surveyEPPO, 2014
SudanAbsent, confirmed by surveyEPPO, 2014
SwazilandAbsent, confirmed by surveyEPPO, 2014
TanzaniaPresentSeif and Hillocks, 1993; EPPO, 2014
TogoPresentBrun, 1972; Seif and Hillocks, 1993; EPPO, 2014
TunisiaAbsent, confirmed by surveyEPPO, 2014
UgandaPresentSeif and Hillocks, 1993; UK CAB International, 1996; EPPO, 2014
ZambiaPresentSeif and Hillocks, 1993; UK CAB International, 1996; EPPO, 2014
ZimbabweLocalisedSeif and Hillocks, 1993; UK CAB International, 1996; Pretorius and Holtz, 2008; EPPO, 2014

North America

MexicoAbsent, confirmed by surveyEPPO, 2014
USAAbsent, 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
CubaAbsent, confirmed by surveyEPPO, 2014
DominicaAbsent, confirmed by surveyEPPO, 2014
Dominican RepublicAbsent, confirmed by surveyEPPO, 2014
El SalvadorAbsent, 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

ArgentinaAbsent, confirmed by surveyEPPO, 2014
BoliviaAbsent, confirmed by surveyEPPO, 2014
BrazilAbsent, confirmed by surveyEPPO, 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, confirmed by surveyEPPO, 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, confirmed by surveyEPPO, 2014
MaltaAbsent, confirmed by surveyEPPO, 2014
MontenegroAbsent, confirmed by surveyEPPO, 2014
NetherlandsAbsent, confirmed by surveyNPPO of the Netherlands, 2013; EPPO, 2014Based on ongoing long-term monitoring for plant passport system.
PortugalAbsent, confirmed by surveyEPPO, 2014
SpainAbsent, confirmed by surveyEPPO, 2014

Oceania

American SamoaAbsent, confirmed by surveyEPPO, 2014
AustraliaAbsent, confirmed by surveyEPPO, 2014
Cook IslandsAbsent, confirmed by surveyEPPO, 2014
FijiAbsent, confirmed by surveyEPPO, 2014
French PolynesiaAbsent, confirmed by surveyEPPO, 2014
GuamAbsent, confirmed by surveyEPPO, 2014
New ZealandAbsent, confirmed by surveyEPPO, 2014
NiueAbsent, confirmed by surveyEPPO, 2014
Papua New GuineaAbsent, confirmed by surveyEPPO, 2014
SamoaAbsent, confirmed by surveyEPPO, 2014
TongaAbsent, confirmed by surveyEPPO, 2014
VanuatuAbsent, confirmed by surveyEPPO, 2014
Wallis and Futuna IslandsAbsent, confirmed by surveyEPPO, 2014

History of Introduction and Spread

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Since its identification in Angola and Mozambique in 1952 (de Carvalho and Mendes, 1952), P. angolensis has appeared to spread north to other parts of Africa (Seif and Hillocks, 1993). It was found in central African countries in the late 1960s, in West Africa in the next decade, and then in eastern Africa in the 1980s (Seif and Hillocks, 1993). Derso (1999) described the appearance of the disease in southern Ethiopia in 1990 and later in the highlands of Guinea in 1993 (Diallo, 2001). Because wild hosts may harbour this pathogen, it is not clear to what extent increased development of the cultivation of citrus has resulted in the fungus spreading from local sources, compared to the role of increased commercial and private transport of infected plant materials in carrying the pathogen across distances.

Risk of Introduction

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The fungus can be transported in or on infected fruit or propagative material. If conidia are not present, substantial moisture appears to be required for their production and for new infections (Emechebe, 1981). Wind is the known means of local dissemination of conidia. Spread of the fungus is probable in warm regions where there is enough moisture, but it is not clear if the Mediterranean climate is suitable (Vicent and García-Jiménez, 2008). The warm and humid conditions of the important citrus-growing regions of Florida, USA are likely to be favourable for this pathogen (Chung and Timmer, 2009).

 

Habitat

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Within the humid African range of the distribution of the fungus, elevation appears to play a role in the epidemiology of the disease. Kuate (1998) described the fungus as most common above 200 m, and Diallo (2001) reported that disease was serious on trees of the highlands of Guinea, whereas the lowland areas appeared to be disease-free. In Kenya, the disease is serious at altitudes above 600 m (Sief and Hillocks, 1993). To the south, in Angola, trees at lower altitudes were more at risk (Ragazzi, 1997).

Habitat List

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CategorySub-CategoryHabitatPresenceStatus
Terrestrial
Terrestrial – ManagedManaged forests, plantations and orchards Present, no further details Harmful (pest or invasive)

Hosts/Species Affected

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All species of cultivated Citrus appear to be susceptible, although the lime (Citrus latifolia) and smooth lemon (Citrus limon) are often reported to be relatively resistant. Of the other members of the Rutaceae in Africa, Citropsis tanakae is known to be infected (Kuate, 1998). The susceptibilities of the many wild Citrus species in Asia (USDA-ARS, 2009) remain unknown.

Growth Stages

Top of page Fruiting stage, Vegetative growing stage

Symptoms

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On leaves, the fungus produces circular, mostly solitary spots, which often coalesce, up to 10 mm in diameter, with a light-brown or greyish centre when dormant and non-sporulating during the dry season, but becoming black with sporulation after the onset of the rainy season (Sief and Hillocks, 1993). The lesions are usually surrounded by a dark-brown margin and a prominent yellow halo; occasionally the centre of the lesion falls out, creating a shot-hole effect. At first glance, the young lesions appear similar to those of canker (caused by Xanthomonas campestris pv. citri), but differ in being flat or shrunken. Leaf spots, especially on younger leaves, often coalesce and together cause generalized chlorosis, followed by premature abscission and defoliation of the affected tree. Young leaves and fruit appear to be more susceptible than older mature leaves (Sief and Hillocks, 1999), but whether the leaves or fruit are more affected varies with the host species and variety (Bella-Manga et al., 1999) and location (Derso, 1999).

On fruit, the spots are circular to irregular, discrete or coalescent, and mostly up to 10 mm in diameter. On young fruits, infection often results in hyperplasia, producing raised tumour-like growths surrounded by a yellow halo; these develop central necrosis and collapse (Kuate, 1998). Lesions on mature fruit are normally flat, but sometimes have a slightly sunken brown centre. Diseased fruits ripen prematurely and drop or dry up and remain on the tree (Kuate, 1998). Infection by the fungus seems to predispose the fruit to secondary infection by Colletotrichum gloeosporioides (De Carvalho and Mendes, 1952; Seif and Kungu, 1990); it is common to find a dark-brown to black sunken margin of anthracnose around the fruit spots.

Stem lesions are not frequent and mostly occur as an extension of lesions on the petiole. Occurrence of several such lesions at the stem tip results in dieback; those on other parts of the stem coalesce, become corky, and crack. At the base of the dead stem there is usually a profuse growth of secondary shoots (Menyonga, 1971).

List of Symptoms/Signs

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SignLife StagesType
Fruit / abnormal shape
Fruit / lesions: black or brown
Fruit / mummification
Fruit / premature drop
Inflorescence / lesions; flecking; streaks (not Poaceae)
Leaves / abnormal colours
Leaves / abnormal leaf fall
Leaves / fungal growth
Leaves / necrotic areas
Leaves / yellowed or dead
Stems / dieback
Stems / discoloration of bark
Stems / witches broom

Biology and Ecology

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Limited studies on field epidemiology have been carried out in western Africa (Emechebe, 1981; Kuante and Foure, 1988). The disease is favoured by prolonged wet weather conditions followed by dry spells (Emechebe, 1981; Kungu et al., 1989), coupled with moderately cool temperatures of 22-26°C (Kungu et al., 1989). Disease incidence varies with the amount of rainfall (Kuate et al., 1994).

At the onset of a rainy season, non-sporulating lesions may be present on older leaves when the new disease-free leaves are formed. Sporulation begins in the old lesions after a further 3-5 weeks and new symptoms appear on young leaves 2-3 weeks later (Emechebe, 1981). The old lesions appear to be the source of inoculum when conditions favour infection.

Long-distance dispersal of the fungus is by windborne conidia (De Carvalho and Mendes, 1952); local dispersal is primarily by rain splash or raindrops (Seif et al., 1989). Undoubtedly humans mediate in the dissemination of the fungus through the transport of infected plant material and/or fruits from infected areas. Because leaf lesions produce more conidia than similar lesions on fruit (Seif and Hillocks, 1993), it is most likely that they constitute the main source of infection during disease spread in infected areas.

Survival mechanisms are unknown; the fungus probably survives in dormant lesions on infected material until the onset of conditions conducive to sporulation.

No physiological specialization is known in this pathogen. In his study of vegetative compatibility groups among isolates from Angola, Ragazzi (1997) found their distribution in the population to be homogeneous. There was little variation in the disease caused by 10 isolates used in inoculations in Cameroon (Kuate et al., 1997).

Climate

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ClimateStatusDescriptionRemark
Af - Tropical rainforest climate Preferred > 60mm precipitation per month
Am - Tropical monsoon climate Preferred Tropical monsoon climate ( < 60mm precipitation driest month but > (100 - [total annual precipitation(mm}/25]))
Aw - Tropical wet and dry savanna climate Preferred < 60mm precipitation driest month (in winter) and < (100 - [total annual precipitation{mm}/25])
BS - Steppe climate Tolerated > 430mm and < 860mm annual precipitation
BW - Desert climate Tolerated < 430mm annual precipitation

Means of Movement and Dispersal

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Natural Dispersal

Wind-borne conidia are the apparent sole means of natural dispersal. No sexual form is known. The possibility of wild hosts of the fungus should be examined (Kuate, 1998).

Vector Transmission

Insect transmission may occur, but is not reported.

Accidental Introduction

Human transport of infected fruit and propagating material has undoubtedly played some role in the spread of the fungus in Africa (Sief and Hillocks, 1993; Kuate, 1998).

Plant Trade

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

Impact Summary

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CategoryImpact
Economic/livelihood Negative

Economic Impact

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P. angolensis causes a significant disease of citrus, the most devastating effect being the premature abscission of young fruit and leaves. The development of even a few fruit lesions renders the fruit unmarketable. A yield loss of 50-100% is not uncommon in most disease-affected areas (Menyonga, 1971; Brun, 1972; Seif and Kungu, 1989). The loss of leaves and desiccation of shoots can have a significant debilitating effect on the tree, which will affect subsequent fruit yields (Kuate, 1998). In some areas, farmers have abandoned citrus plantings or replaced them with other crops (Seif and Hillocks, 1993; Kuate, 1998; Kassahun et al., 2006).

Risk and Impact Factors

Top of page Invasiveness
  • Invasive in its native range
  • Proved invasive outside its native range
  • Has a broad native range
  • Highly mobile locally
  • Has high reproductive potential
  • Reproduces asexually
Impact outcomes
  • Host damage
  • Negatively impacts agriculture
  • Negatively impacts livelihoods
Impact mechanisms
  • Pathogenic
Likelihood of entry/control
  • Highly likely to be transported internationally accidentally
  • Difficult to identify/detect as a commodity contaminant
  • Difficult to identify/detect in the field

Diagnosis

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Sequences of the ITS1, ITS2 and 5.8s regions of ribosomal DNA are available in GenBank for comparison (NCBI, 2009).

Detection and Inspection

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The lower sides of leaves should be examined for the dark sporulation of the fungus in grey to brown sunken lesions with yellow halos; the lesions are also visible from the upper surface (Kuate, 1998). Mature fruits also bear sunken brown lesions with a yellow halo, with sporulation occurring under wet or humid conditions.

Similarities to Other Species/Conditions

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At an early stage, the lesions caused by P. angolensis on leaves appear similar to those of citrus canker caused by the bacterium Xanthomonas campestris pv. citri. They differ in being flat or shrunken, rather than raised (Seif and Hillocks, 1993). Canker lesions on leaves also have a yellow halo, but are distinguished by a water-soaked margin around the spot (Brlansky, 1988), as are the flat lesions caused by other bacterial pathogens of Citrus (Duan et al., 2009).

The fungus Guignardia citricarpa also causes spots on leaves and/or fruits of Citrus in Africa, Asia, Australia, and South America. The lesions of the disease, called ‘black spot’, may resemble those produced by P. angolensis, particularly on lemon leaves or take the form of ‘freckle spots’ or red-brown bordered, irregular, sunken, necrotic spots. Small, globose, black, fungal pycnidia, containing single-celled colourless spores, are often produced in these spots (Kotze, 1988).

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.

SPS Measures

Prevention of the transport of infected trees and fruit from contaminated areas is an important measure for inhibiting the spread of the pathogen in and from Africa (Kuate, 1998). The most significant citrus production in Africa, near the Mediterranean in North Africa and in the Republic of South Africa, occurs in countries currently outside of the range of distribution of P. angolensis (Sief and Hillocks, 1993). Vicent and Garcia-Jimenez (2008) suggest that the relative aridity of the Mediterranean climate may make it unsuitable for wind-disseminated pathogens such as P. angolensis; the periods of interrupted leaf wetness provided by dew in Spain might be sufficient for infection. This fungus is an A1 level restricted organism for Europe (EPPO, 2009).

Cultural Control and Sanitary Measures

The following disease management methods have been recommended (Seif and Kungu, 1989):

- Collection and destruction by burying and/or burning of all fallen fruit and leaves in affected orchards. This may drastically reduce the inoculum pressure in the field.

- Planting of windbreaks around the citrus orchards to minimize the impact of wind, which is the primary dispersal agent for spores.

- Discouraging inter-planting in affected orchards composed of mature producing trees, fostering a microclimate of relatively cool temperatures and high relative humidity (RH), thus preventing disease development.

- Judicious pruning of shoots, particularly those that have died back, to allow light penetration into and free aeration within the tree canopy, thus making the environment in the phyllosphere less conducive to disease development, i.e. shorter leaf-wetness period, lower RH, moderate temperatures.

Pretorious and Holtz (2008) recommend the removal of neglected orchards in Zimbabwe to reduce inoculum.

Chemical Control

The most effective fungicides tested on fruit and leaf spot of citrus in Cameroon were copper oxide and benomyl (Menyonga, 1971; Rey et al., 1988). Others found to be effective were mancozeb, tridemorph, triadimenol and propiconazole (Rey et al., 1988). Applications of mancozeb in the rainy season were not effective in Zimbabwe (Pretorius and Holtz, 2008).

Use of benomyl alone may lead to the development of resistant strains of the fungus (Kuate, 1998). Treatments with benomyl, alternated with copper-based fungicides, may be applied at 2-week intervals beginning a week after the onset of rains (Sief and Hillocks, 1993). A further three fortnightly applications with copper-based fungicides, followed by one of benomyl, can be made when the fruits are the size of golf balls (approximately 3 cm diameter). Sief and Hillocks (1997) recommend spraying after rainfall, rather than on a fixed schedule, because rain stimulates spore production and favours infection (see Kuate et al., 1994).

Of the newer triazole fungicides, fluzilazole provided the best control of disease in the field, whereas tebuconazole was not as effective as a copper hydroxide formulation (Sief and Hillocks, 1997). Pretorius and Holtz (2008) reported that a trifloxystrobin + mancozeb + mineral spray oil combination, applied in November, January and March, provided the best control of the disease on foliage in Zimbabwe. A mixture of benomyl and chlorothalonil applied at 15-day intervals was most effective in controlling the disease on the leaves of sweet orange in Ethiopia, compared to a mixture of benomyl and copper hydroxide or any of the fungicides alone (Kassahun et al., 2006).

Some recent attention has focused on the possibility of using natural oils, which should be relatively cheap, available, and safer in the environment, in place of synthetic chemicals. Oils extracted from the skin of fruits of more resistant species of Citrus: Citrus latifolia (lime) and Citrus limon (lemon), reduced the growth of an isolate of the pathogen more than the extracts of susceptible species did (Jazet et al., 2002). Furthermore, among the oil extracts of 22 varieties of cultivated Citrus, those of the more disease-tolerant varieties were the most effective in reducing radial growth of the fungus in culture, but those of the susceptible varieties were more effective in inhibiting sporulation (Kuate et al., 2006). Oil extracts from the leaves of two Eucalyptus species had minimum inhibitory concentrations (MICs) of 6000 and 6500 ppm (Jazet et al., 2008). Essential oils of the bottlebrush plants, Callistemon citrinus and Callistemon rigidus, showed similar activity (Dongmo et al., 2009). Lime-leaf oil extract had an MIC of 1600 ppm, with both fungistatic and fungitoxic effects (Dongmo et al., 2008), and oils of Citrus aurantifolia (Key lime) had MICs of 1400 to 1500 ppm (Dongmo et al., 2009). The antifungal activity of certain fractions of the lime oil appeared to be due to their high content of neral and geranial. Of the extracts reported so far, those of the grass Cymbopogon citratus were most effective at inhibiting fungal growth in the laboratory, with activity at 600 ppm comparable to that of a fungicide (Tchinda et al., 2009).

Host Resistance

Cultivated species and varieties vary in susceptibility to the fungus and effects of the disease (Bella-Manga et al., 1999; Sief and Hillocks, 1999). Use and development of resistant varieties would benefit growers with small orchards or a few trees, who cannot afford fungicide treatments (Mohammed Yesuf, 2007). Nevertheless, progress in this effort is hindered by an absence of strong resistance, loss of apparent resistance in different ecological zones or in different seasons, and the need to evaluate the susceptibilities of leaves and fruits (Kuate, 1998).

Gaps in Knowledge/Research Needs

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Additional knowledge is needed of the conditions that favour infection and sporulation. Sources of resistance should be sought among the wild species of Citrus and related genera, whereas the role of wild hosts in the persistence and spread of the pathogen in Africa should be explored.

References

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06/11/09 Updated by:

Systematic Mycology & Microbiology Laboratory, USDA-ARS, 10300 Baltimore Ave., Beltsville, MD 20705, USA

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