Citrus Black Spot
Johann van der Vyver: Technical Sales Director: Africa Region
The pathogen causing Citrus Black Spot (CBS) is a fungus generally referred to as Phyllosticta citricarpa (McAlpine) van der Aa, which is the anamorph stage of the fungus. The teleomorph stage is Guignardia citricarpa KeiIy. The pathogen was first noticed and described in Australia more than 120 years ago.
Today CBS affects all commercial citrus types to a certain degree in the global summer rainfall regions. Lemons, limes, mandarins and late-maturing sweet oranges are the most susceptible. Nu-Film 17 however, has shown significant value as part of a control program.
Economic Importance
Although the disease affects the rind of fruit, causing lesions, it does not result in fruit decay or affect the internal fruit quality. Severely affected fruit may drop prematurely from the tree, reducing production.
The biggest economic importance of CBS is that the European Union does not allow the importation of citrus with CBS symptoms. Despite continuous negotiations, discussions, and different opinions between the EU and citrus producing countries (with CBS) regarding the viability and potential occurrence of CBS in Europe, challenges remain.
The disallowance may have the following economic impact for citrus exporting countries (should shipments contain fruit with CBS symptoms):
- Destroying / rerouting of shipments with CBS symptoms.
- Reduced profit (instead of being exported, fruit are sent to local markets or being processed).
- Increased disease control measures.
Symptomology
Fruit symptoms vary greatly; to the extent that lesions are referred to as A, B, C, and D types.
Type A
Symptoms include hard shot and shot-hole spot, which are circular, depressed, brick red lesions with brown to black margins and grey necrotic tissue in the center. Pycnidia (asexual fruiting bodies of the fungi) are usually, but not always present in these spots.
Although hard spot lesions are the most typical symptoms of black spot, the causal fungus is isolated from them at low frequencies. Hard spot is a preharvest symptom and develops on the sunny side of the fruit.
Type B
Symptoms are characterized by false melanose spots or speckled blotch (dark brown stippling). They appear early on green fruit and do not contain pycnidia. These symptoms may develop into Type A symptoms towards the end of the season.
Type C
Freckle spots are a sign of severe infection. It may develop into virulent spots late in the season or during storage. These spots are orange to red, round, depressed and 1 mm (0.04 inch) in diameter. They enlarge into craters of up to 3 mm (0.12 inch). Pycnidia can be present.
Type D
Symptoms are virulent, spreading or galloping spots. These spots are sunken and irregular in shape. It occurs on heavily infected fruit towards the end of the season. Under conditions of high humidity numerous pycnidia develop.
(Photos from G.C. Schutte)
Leaf and stem symptoms are not as common as fruit symptoms, especially in well-managed orchards. Symptoms are more common on lemon types, which are more susceptible than other citrus types. Lesions begin as small reddish-brown lesions that are slightly raised. With age they become round sunken necrotic spots with gray centers and prominent margins that are brick-red to chocolate brown
Phenology
Phyllosticta citricarpa produces ascospores in pseudothecia (ascocarps) and conidia in pycnidia as inoculum sources. Ascospores from dead leaves on the orchard floor are the main source of inoculum. Ascospores are not found on fruit, green leaves and twigs in the canopy.
Conidia can be found in dead twigs (not green twigs), green leaves (mainly lemons) and diseased fruit as well as on fallen leaves.
Windborne ascospores are generally dispersed under field conditions over longer distances (c. 25 m) and are associated with the spread of CBS between trees. Conidia are dispersed over shorter distances (less than 80 cm) through washing-down.
This is responsible for the spread of CBS within a tree canopy. Conidia (in pycnidia) on fruit do no not survive for long periods.
Pseudothecia develop between 40 to 180 days after leaf drop. The number of days depend primarily on the frequency of wetness and prevailing temperatures. In cool areas it’s possible that dead leaves decompose before pseudothecia.
Ascospore release is triggered by frequently occurring rainfall with temperatures in the range of 22 to 30°C (71.6 to 86°F). The optimal temperature range for the fungus is 25 to 27°C (77 to 80.6°F).
The critical period for infection starts at fruit set when it rains, especially when fruit remains wet for 8 or more hours. Fruit remains susceptible for 4 to 5 months, after which infection no longer takes place.
Inoculum availability during the summer depends on warm, wet and humid conditions favorable for infection, as well as the age of the fruit in relation to its susceptibility to infection. When an ascospore germinates, it produces a germ tube called an appressorium.
From the appressorium, a thin infection peg penetrates the cuticle and expands into a small mass of mycelium between the cuticle and the epidermal wall. The fungus remains in this latent state until the fruit becomes fully grown or mature, when it may grow further into the rind tissue and produce a black spot symptom – hence the name.
Symptom development on mature fruit is enhanced by rising temperatures, high light intensity, drought and poor tree vigor. CBS is more prone on older trees.
Control
Commercial control of CBS can only be achieved by using plant protection products. The efficacy thereof can be enhanced through cultural practices. These are agricultural practices to avoid or limit the risk of infection. Implementation of these practices is a consideration of practicalities and economics.
Cultural Practices
- Use uninfected trees from nurseries in black-spot free regions. Infected nursery trees spread the inoculum through infected leaves.
- Since ascospores from dead leaves on the orchard floor are the main source of inoculum, any method that removes dead leaves reduces the inoculum.
- Mulching of the orchard floor with a suitable material such as grass cuttings. Mulching accelerates the decomposition of the leaves bearing the ascocarps, causing a reduction in inoculum. Timing of mulching is extremely important. It should be applied after leaf drop.
- Maintain tree vigor. Trees in a poor condition are more prone to CBS infection.
Plant Protection Products
Plant protection products referred to below are based on international registration of products, scientific research, as well as information, publications and recognized professional recommendations available at the time of this publication.
Contact Fungicides
The use of contact fungicides has to be carefully timed to coincide with the critical infection period. The latent infection phase of black spot, which occurs between the cuticle and the epidermis of the rind, is out of reach of contact fungicides due to their inability to penetrate the rind.
Spray programs comprising these fungicides must be aimed at prevention of/protection against fungal infection. Recommended intervals between sprays must not be exceeded. The maximum period that the different contact fungicides can protect fruit at registered concentrations, is as follows:
- Dithiocarbamates: Such as mancozeb and maneb + zinc oxide = 25 days protective.
- Copper: 35 days protective.
Systemic Fungicides
These fungicides are capable of penetrating the epidermis and the cuticle, killing mycelium present. Existing lesions can also heal once the infection is eliminated.
The maximum period that the different contact fungicides can protect fruit (at registered concentrations) is as follow:
- Strobilurins: Such as azoxystrobin, pyraclostrobin and trifloxystrobin = 42 days protective. Have the advantage of limited curative action. In some cases up to 3 days. Although the use in a mixture with a fungicide of an unrelated mode of action is recommended (often registered as such), recent published scientific research indicates a low risk for resistance development.
- Benzimidazoles: Such as benomyl and carbendazim = 42 days protective. Have the advantage of a long curative ability = 28 days (rate dependent). Important: High risk for resistance development. If registered, use in a mixture with a fungicide of an unrelated mode of action or try to avoid more than one application per season. Monitor possible resistance regularly.
Other Fungicides
A recent addition to fungicides registered for the control of CBS is dipotassium phosphate. In South Africa it is registered for use in spray program with strobilurins (azoxystrobin and pyraclostrobin).
To assist with the critical timing of fungicides for the control of CBS, spore trapping and the recording of rainfall, dew periods and temperature can be used to determine the time and intensity of ascospore release.
An example of such a successful commercial system in South Africa is CRI-PhytRisk (www.cri-phytrisk.co.za/). It is a free online warning system that supports farmers with information about citrus black spot (CBS) risks, weather forecasts as well as the suitability of conditions for spraying fungicides.
Miller Product Use Within Citrus Black Spot Programs
During the last 3 citrus production seasons in South Africa Nu-Film 17 was successfully trialed in the following spray program for the control of CBS:
| PRODUCTS | Contact fungicide | Contact fungicide + Strobilurin + Nu-Film 17 | Contact fungicide + Strobilurin + Nu-Film 17 | Contact fungicide |
| TIME OF APPLICATION | Start | 3 weeks later | 6 weeks later | 6 weeks later |
Proven Nu-Film 17 attributes (during and after application) contributing to the successful incorporation into spray programs for the control of CBS are:
- Improved fungicide deposition on trees and fruit through reduction of volatility, spray drift, and improved adhesion of spray.
- More uniform spreading of spray deposit on trees and fruit.
- Improved retention of fungicide after application through improved rain fastness, reduced UV and heat degradation of active ingredients.
- A micro-encapsulated matrix that forms with the fungicide active ingredient. As the outer layers of the matrix degrades over time, contact fungicides are released on the plant surface for re-activation and distribution. Systemic fungicides within the matrix remain in a liquid stage for continuous availability and absorption into the plant.
Acknowledgements
Special thank you to Dr. G.C. Schutte ad Mr. C. Kotze for supplying literature, comments and sharing of valuable experience and insight.
LITERATURE CITED
Dewdney, M. Presentation: Citrus black spot management. https://crec.ifas.ufl.edu/extension/black_spot/PDF/Black%20spot%20management%20round%20table.pdf
EFSA Panel on Plant Health (PLH). 2014. Scientific Opinion on the risk of Phyllosticta citricarpa (Guignardia citricarpa) for the EU territory with identification and evaluation of risk reduction options.
EFSA. 2018. Citrus black spot: new evidence reviewed.
Guarnaccia, V., Gehrmann T., Silva-Junior, G.J., Fourie, P.H., Haridas, S., Vu, D., Spatafora, J., Martin, F.M., Robert, V., Grigoriev, I.V., Groenewald, J.Z. and Crous, P.W. 2019. Phyllosticta citricarpa and sister species of global importance to citrus.
Kotze, J.M. 1981. Epidemiology and Control of Citrus Black Spot in South Africa. Plant Disease 65 (12): 945–950.
Moyo, P and Fourie, P.H. 2019. CRI Cutting Edge No 262: Recent CRI-PhytRisk improvements.
Moyo, P. Van Niekerk, J. Carstens, E. and Fourie, P.H. 2021. CRI Cutting Edge No 329: Citrus Black Spot Spray Programmes 2021 – 2022.
Schutte, G.C. 2009. Black spot. In Chapter 6: Foliar and fruit diseases. Citrus Research International.
Van Niekerk, J. and Moyo, P. Citrus Research International Citrus Black Spot Research Summary 2015-2020.
Stammler, G., Schutte, G.C., Speakman, J., Miessner, S. and Crous, P.W. 2013. Phyllosticta species on citrus: Risk estimation of resistance to QoI fungicides and identification of species with cytochrome b gene sequences. Crop Protection 48: 6 – 12.
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