Colletotrichum acutatum (black spot of strawberry)
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- Risk of Introduction
- Hosts/Species Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Means of Movement and Dispersal
- Plant Trade
- Detection and Inspection
- Prevention and Control
- Distribution Maps
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IdentityTop of page
Preferred Scientific Name
- Colletotrichum acutatum Simmonds ex Simmonds
Preferred Common Name
- black spot of strawberry
Other Scientific Names
- Colletotrichum xanthii Halsted
International Common Names
- English: crown rot (of anemone and celery); leaf curl of anemone; post-bloom fruit drop of citrus; terminal crook disease (of pine)
- Spanish: antracnosis del fresón; manchas negras del fresón
- French: anthracnose du fraisier; taches noires du fraisier
- COLLAC (Glomerella acutata)
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Fungi
- Phylum: Ascomycota
- Subphylum: Pezizomycotina
- Class: Sordariomycetes
- Subclass: Sordariomycetidae
- Family: Glomerellaceae
- Genus: Colletotrichum
- Species: Colletotrichum acutatum
Notes on Taxonomy and NomenclatureTop of page
The classification of the genus Colletotrichum is currently very unsatisfactory, and several species occur on the principal economic host (strawberry) which are regularly confused. As well as C. acutatum, these include the Glomerella cingulata anamorphs C. fragariae and C. gloeosporioides, all of which can be distinguished by isoenzyme analysis (Bonde et al., 1991). Studies are continuing. Colletotrichum xanthii appears to be an earlier name for C. acutatum, but more research is necessary before it is adopted in plant pathology circles.
DescriptionTop of page
Colonies in culture are usually white, pale grey or pale orange, sometimes producing strong pinkish-purple pigments. Conidiomata are usually poorly developed, with few or no setae, especially in culture. Conidiogenous cells are roughly cylindrical, sometimes borne in weak clusters, and produce conidia successively from single loci. Conidia are 8-16 x 2.5-4 µm in size, fusiform, thin-walled, aseptate and hyaline. Appressoria are few in number, 6.5-11 x 4.5-7.5 µm in size, clavate to circular and light to dark brown.
Full descriptions are given by Dyko and Mordue (1979), Sutton (1980), Baxter et al. (1983) and Gunnell and Gubler (1992).
DistributionTop of page
Some country records may refer instead to the Glomerella cingulata-Colletotrichum fragariae aggregate.
A record of C. acutatum in Chile (EPPO, 2009; CABI/EPPO, 2010) published in previous versions of the Compendium has been removed as the pathogen in the original source (Peredo et al., 1979) is now confirmed as a separate species, Colletotrichum pseudoacutatum (Damm et al., 2012). C. acutatum is a quarantine pest for Chile (Servicio Agrícola y Ganadero, 2013).
Distribution TableTop of page
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/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|China||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Chongqing||Present||Chen et al., 2016|
|-Hainan||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Hong Kong||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Hubei||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Hunan||Present||Xia et al., 2011|
|-Jiangsu||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Liaoning||Present||Xu et al., 2013; EPPO, 2014|
|India||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Andhra Pradesh||Present||CABI/EPPO, 2010|
|-Assam||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Indian Punjab||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Tamil Nadu||Present||CABI/EPPO, 2010|
|-Uttar Pradesh||Present||CABI/EPPO, 2010|
|Indonesia||Present||CABI/EPPO, 2010; EPPO, 2014|
|Iran||Present||Zafari and Hamadani, 2009; Mousakhah and Khodaparast, 2012|
|Israel||Present||CABI/EPPO, 2010; EPPO, 2014|
|Japan||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Honshu||Present||CABI/EPPO, 2010; EPPO, 2014|
|Korea, Republic of||Present||CABI/EPPO, 2010; EPPO, 2014|
|Malaysia||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Peninsular Malaysia||Present||CABI/EPPO, 2010|
|Nepal||Present||CABI/EPPO, 2010; EPPO, 2014|
|Saudi Arabia||Present||Ammar and El-Naggar, 2011|
|Sri Lanka||Present||CABI/EPPO, 2010; EPPO, 2014|
|Taiwan||Present||CABI/EPPO, 2010; EPPO, 2014|
|Thailand||Present||CABI/EPPO, 2010; EPPO, 2014|
|Turkey||Present||CABI/EPPO, 2010; EPPO, 2014|
|Egypt||Present||CABI/EPPO, 2010; EPPO, 2014|
|Ethiopia||Present||CABI/EPPO, 2010; EPPO, 2014|
|Kenya||Present||CABI/EPPO, 2010; EPPO, 2014|
|Nigeria||Present||CABI/EPPO, 2010; EPPO, 2014|
|South Africa||Present||CABI/EPPO, 2010; EPPO, 2014|
|Tanzania||Present||CABI/EPPO, 2010; EPPO, 2014|
|Tunisia||Present||Sayeh et al., 2016|
|Zimbabwe||Present||CABI/EPPO, 2010; EPPO, 2014|
|Canada||Restricted distribution||CABI/EPPO, 2010; EPPO, 2014|
|-British Columbia||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Manitoba||Present||CABI/EPPO, 2010; EPPO, 2014|
|-New Brunswick||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Nova Scotia||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Ontario||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Quebec||Present||CABI/EPPO, 2010; EPPO, 2014|
|USA||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Arkansas||Present||CABI/EPPO, 2010; EPPO, 2014|
|-California||Present||CABI/EPPO, 2010; Swain et al., 2012; EPPO, 2014|
|-Connecticut||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Florida||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Louisiana||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Michigan||Present||CABI/EPPO, 2010; Rodriguez-Salamanca et al., 2012|
|-Mississippi||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Missouri||Present||CABI/EPPO, 2010; EPPO, 2014|
|-New Mexico||Present||French et al., 2013; EPPO, 2014|
|-New York||Present||CABI/EPPO, 2010; EPPO, 2014|
|-North Carolina||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Ohio||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Oklahoma||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Pennsylvania||Present||Pollok et al., 2012|
|-Rhode Island||Present||CABI/EPPO, 2010|
|-South Carolina||Present||CABI/EPPO, 2010|
Central America and Caribbean
|Belize||Present||CABI/EPPO, 2010; EPPO, 2014|
|Costa Rica||Present||CABI/EPPO, 2010; EPPO, 2014|
|Dominica||Present||CABI/EPPO, 2010; EPPO, 2014|
|Dominican Republic||Present||CABI/EPPO, 2010; EPPO, 2014|
|Saint Lucia||Present||CABI/EPPO, 2010|
|Argentina||Restricted distribution||CABI/EPPO, 2010; Sir et al., 2012; EPPO, 2014|
|Brazil||Restricted distribution||CABI/EPPO, 2010; EPPO, 2014|
|-Minas Gerais||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Rio Grande do Sul||Present||CABI/EPPO, 2010|
|-Santa Catarina||Present||CABI/EPPO, 2010|
|-Sao Paulo||Present||CABI/EPPO, 2010; EPPO, 2014|
|Chile||Absent, invalid record||CABI/EPPO, 2010; EPPO, 2014|
|Colombia||Present||CABI/EPPO, 2010; EPPO, 2014|
|Ecuador||Present||CABI/EPPO, 2010; EPPO, 2014|
|Uruguay||Present||CABI/EPPO, 2010; Alaniz et al., 2012; EPPO, 2014|
|Venezuela||Present||Cedeño et al., 2007; CABI/EPPO, 2010; EPPO, 2014|
|Austria||Present, few occurrences||CABI/EPPO, 2010; EPPO, 2014|
|Belgium||Present||CABI/EPPO, 2010; EPPO, 2014|
|Bulgaria||Restricted distribution||CABI/EPPO, 2010; EPPO, 2014|
|Czech Republic||Restricted distribution||CABI/EPPO, 2010; Víchová et al., 2013; EPPO, 2014|
|Denmark||Present||CABI/EPPO, 2010; EPPO, 2014|
|Estonia||Absent, confirmed by survey||EPPO, 2014|
|Finland||Restricted distribution||CABI/EPPO, 2010; EPPO, 2014|
|France||Present||CABI/EPPO, 2010; EPPO, 2014|
|-France (mainland)||Present||CABI/EPPO, 2010|
|Germany||Present, few occurrences||CABI/EPPO, 2010; EPPO, 2014|
|Greece||Present||Iliadi et al., 2018|
|Hungary||Present, few occurrences||Irinyi and Kövics, 2008; CABI/EPPO, 2010; EPPO, 2014|
|Ireland||Present, few occurrences||EPPO, 2014|
|Italy||Present||CABI/EPPO, 2010; Mari et al., 2012; EPPO, 2014; Vitale and Infantino, 2014; Vitale et al., 2015; Frisullo et al., 2016|
|-Italy (mainland)||Present||CABI/EPPO, 2010|
|-Sicily||Present||Polizzi et al., 2011|
|Lithuania||Present, few occurrences||CABI/EPPO, 2010; EPPO, 2014|
|Malta||Restricted distribution||CABI/EPPO, 2010; EPPO, 2014|
|Montenegro||Present||Latinovic et al., 2012; EPPO, 2014|
|Netherlands||Present||NPPO of the Netherlands, 2013; CABI/EPPO, 2010; EPPO, 2014|
|Norway||Present||CABI/EPPO, 2010; EPPO, 2014|
|Portugal||Present||CABI/EPPO, 2010; EPPO, 2014|
|Serbia||Present||CABI/EPPO, 2010; EPPO, 2014|
|Slovenia||Present, few occurrences||CABI/EPPO, 2010; EPPO, 2014|
|Spain||Restricted distribution||CABI/EPPO, 2010; EPPO, 2014|
|-Spain (mainland)||Present||CABI/EPPO, 2010|
|Sweden||Present, few occurrences||CABI/EPPO, 2010; EPPO, 2014|
|Switzerland||Present||CABI/EPPO, 2010; Michel et al., 2011; Michel et al., 2013; EPPO, 2014|
|UK||Restricted distribution||CABI/EPPO, 2010; Baroncelli et al., 2014; EPPO, 2014|
|-Channel Islands||Present||CABI/EPPO, 2010; EPPO, 2014|
|-England and Wales||Restricted distribution||CABI/EPPO, 2010; EPPO, 2014|
|-Northern Ireland||Present||CABI/EPPO, 2010|
|-Scotland||Absent, intercepted only||CABI/EPPO, 2010|
|Australia||Present||CABI/EPPO, 2010; EPPO, 2014|
|-New South Wales||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Queensland||Present||CABI/EPPO, 2010; EPPO, 2014|
|-South Australia||Present||CABI/EPPO, 2010|
|-Victoria||Present||CABI/EPPO, 2010; EPPO, 2014|
|-Western Australia||Present||CABI/EPPO, 2010; EPPO, 2014|
|New Zealand||Present||CABI/EPPO, 2010; EPPO, 2014|
|Papua New Guinea||Present||CABI/EPPO, 2010|
|Vanuatu||Present||CABI/EPPO, 2010; EPPO, 2014|
Risk of IntroductionTop of page
C. acutatum has not been considered to be a quarantine pest by EPPO or any other regional plant protection organization. A certain ambiguity remains on its geographical distribution and impact on the strawberry crop, due to confusion with other Colletotrichum spp. In several countries of mainland Europe, the names C. fragariae or C. gloeosporioides have been used for all fungi causing anthracnose on strawberry. C. acutatum was only described on strawberry in the 1960s (Simmonds, 1966) and it is not clear whether its subsequent appearance as a strawberry pathogen in the literature is due to geographical spread of a pathogen which previously had a restricted distribution, to the rise in importance of a pathogen which was previously insignificant, or simply to the clarification of a taxonomic situation which was previously confused. As C. acutatum attacks several other crops without being a serious cause of concern, and indeed many other plant species, it does not appear logical to attempt to control it by international phytosanitary measures. In addition, identification in imported consignments presents difficulties because of the confusion with related species. Pathogen-free certification of strawberry planting material seems the best approach.
The inclusion of C. acutatum (and other Colletotrichum spp.) among the species covered by a strawberry certification scheme would ensure that healthy planting material is traded nationally and internationally. A suitable scheme has been recommended by EPPO (OEPP/EPPO, 1994).
Hosts/Species AffectedTop of page
The species has a very wide host range, but is economically most important on strawberries.
C. acutatum can apparently affect almost any flowering plant, especially in warm temperate or tropical regions, although its host range needs further clarification. It has rarely been noted on other than agricultural or forestry land.
Growth StagesTop of page Post-harvest
SymptomsTop of page
The spread of the disease is often so rapid that by the time symptoms are noticed, the crop is in serious danger. For strawberry, fruit and occasionally petiole rots may be noticed, with sunken, water-soaked spots enlarging to cover the whole fruit within 2-3 days, with dark-brown fruit bodies producing pink spore masses. For other crops such as anemone and celery, crown rots and leaf curl may be the principal symptoms. In pine seedlings, the developing leaves around the apical bud are affected, with small, brown lesions appearing and rapidly extending. Severe stunting is eventually caused as the uninfected tissue beneath the apex continues to develop.
List of Symptoms/SignsTop of page
|Fruit / lesions: scab or pitting|
|Leaves / leaves rolled or folded|
|Stems / rot|
|Stems / stunting or rosetting|
Biology and EcologyTop of page
The conidia germinate to form appressoria on plant surfaces, from which penetration hyphae develop into plant cells. Infection may occur through almost any plant surface, but for the particularly susceptible herbaceous species such as strawberry and anemone, the crown with its relatively humid microclimate is often favoured. In suitable conditions, the fungus can grow rapidly inside the plant and cause severe symptoms very quickly, but in other circumstances the fungus may be quiescent inside host tissues for a period, in some cases only becoming apparent after harvest. Once the fungus has developed sufficiently inside the plant, dark fruit-bodies are produced, causing typical anthracnose symptoms. Conidia are formed liberally, and are normally dispersed by watersplash (Yang et al., 1992). They may lie dormant in the soil for some time, often overwintering in this fashion. Survival is longest under relatively cool, dry conditions (Eastburn and Gubler, 1992). The fungus can also remain dangerous for long periods in dead plant material on the surface or buried in the soil.
Although the disease in strawberry crops tends to be more virulent in warm climates, where damage can be devastating, it frequently has its origins in cooler conditions where propagating material is grown (Opgenorth et al., 1989; Wilson et al., 1990; Sutton, 1992). The disease may possibly occur in all countries where strawberries are cultivated. However, it is reported to be absent from the premises of most major strawberry propagators in the UK, and it may be possible to exclude the fungus from these sites despite its presence elsewhere in the areas concerned. There is little information on the biology of C. acutatum other than for strawberry crops.
In some crops, notably mango (Liu et al., 1986) and tamarillo (Yearsley et al., 1988), C. acutatum causes postharvest diseases of fruits.
Means of Movement and DispersalTop of page
Most natural transmission is probably by conidia, although appressoria, hyphal fragments and appressorium-like thick-walled cells may also play a part (Nair et al., 1983). Local dispersal seems to be at least mostly by water-splash (Yang et al., 1990), with propagules sometimes overwintering in soil to affect strawberry crops planted in subsequent years (Eastburn and Gubler, 1990).
Long-distance transmission due to human influence is probably widespread, and has contributed to the rapid spread of the fungus in recent years. The disease is frequently intercepted on strawberry material imported into the UK.
Plant TradeTop of page
|Plant parts liable to carry the pest in trade/transport||Pest stages||Borne internally||Borne externally||Visibility of pest or symptoms|
|Bark||hyphae; spores||Yes||Yes||Pest or symptoms usually invisible|
|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 invisible|
|Leaves||hyphae; spores||Yes||Yes||Pest or symptoms usually visible to the naked eye|
|Roots||hyphae||Yes||Pest or symptoms usually invisible|
|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|
|Growing medium accompanying plants|
ImpactTop of page
The disease is significant worldwide on strawberry (on which it is considered the second most important pathogen after Botrytis cinerea), and also on a few other crops such as anemones. The disease on pine may not now be so severe as in recent years, judging from the decline in research papers. Little detailed information on economic losses is available. In France, the disease has caused up to 80% losses of unsprayed strawberry crops, especially of ever-bearing cultivars (Denoyes and Baudry, 1991). Crops sprayed for B. cinerea control have suffered much less. In the UK, where the disease is statutorily notifiable, presence forces the burning of crops and fumigation of the soil.
Recent studies in Australia showed that C. acutatum caused losses of 25-50% in celery crops in Queensland (Wright and Heaton, 1991).
Detection and InspectionTop of page No rapid methods exist, although early results from a detection system using monoclonal antibodies are promising. Current tests involve either inoculation of apples with strawberry petioles or paraquat treatment of petioles to stimulate sporulation of the pathogen (Cook, 1993). These tests are time-consuming and labour-intensive.
Prevention and ControlTop of page
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.
The only serious research on control has been in connection with strawberry crops. Some success was reported in New Zealand by spraying with dichlofluanid and a captan-benomyl mixture (Cheah and Soteros, 1984), with various chemicals in Australia (Washington et al., 1992), and in South Africa with captan (van Zyl, 1985). Recently in the USA, studies showed that no acceptable fungicide is effective (Milholland, 1989). Fungicide-resistant strains of related species have been reported in the USA and Japan (Chikuo and Kobayashi, 1991; McInnes et al., 1992). There have been considerable efforts in the USA to develop resistant strawberry cultivars, but limited success has been achieved due to the presence of varied races within the species (Delp and Milholland, 1981; Smith, 1985; Smith and Black, 1990; McInnes et al., 1992). Gupton and Smith (1991) have suggested some potentially useful directions for further research.
In the UK, the disease is rare owing to strict quarantine controls and a policy of destroying affected crops and fumigating soil. McInnes et al. (1992) found that nursery material derived from tissue culture which was free from the related species C. fragariae and planted in isolated fields remained healthy, suggesting that careful selection of disease-free stock and soil sterilization in affected beds might be at least as effective as attempting chemical control.
In celery crops, Wright and Heaton (1991) found both a variation in cultivar susceptibility and amenability to chemical control of the disease. For anemone, disease incidence decreased with storage of corms (Doornik and Booden, 1990), and treatment by soaking with hot water proved effective (Doornik, 1990). Yearsley et al. (1988) found that dipping of tamarillos in imazalil and prochloraz reduced the incidence of postharvest disease caused by C. acutatum. However, dipping strawberry plants in hot water or fungicides did not eliminate the disease.
For pine, regular applications of prochloraz have been found to be effective, as has dichlofluanid (Vanner, 1990).
ReferencesTop of page
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Ammar MI, El-Naggar MA, 2011. Date palm (Phoenix dactylifera L.) fungal diseases in Najran, Saudi Arabia. International Journal of Plant Pathology, 2(3):126-135. http://scialert.net/fulltext/?doi=ijpp.2011.126.135&org=12
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Denoyes B, Baudry A, 1991. Characterization of species of Colletotrichum isolated from strawberry in France, taxonomy and pathogenicity abstract. Strawberry Diseases and Breeding for Varietal Resistance International Workshop, Bordeaux 1991.
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Iliadi, M. K., Tjamos, E. C., Antoniou, P. P., Tsitsigiannis, D. I., 2018. First report of Colletotrichum acutatum causing anthracnose on olives in Greece., 102(4), 820-821. http://apsjournals.apsnet.org/loi/pdis doi: 10.1094/PDIS-09-17-1451-PDN
Irinyi L, Kövics GJ, 2008. The first occurrence of Colletotrichum acutatum on strawberry in Hungary. (A Colletotrichum acutatum elsodouble acute~ hazai elodouble acute~fordulása szamócán.) In: 13. Tiszántúli Növényvédelmi Fórum, 15-16 October 2008, Debrecen, Hungary [ed. by Dávid, I.\Kövics, G. J.]. Debrecen, Hungary: Debreceni Egyetem, Agrártudományi Centrum, Mezögazdaságtudományi Kar, 66-77.
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