Scientific Opinion on the risk of Phyllosticta citricarpa (Guignardia citricarpa) for the EU territory with identification and evaluation of risk reduction options


Panel on Plant Health
EFSA Journal
EFSA Journal 2014;12(2):3557 [243 pp.].
Panel members at the time of adoption
Richard Baker, Claude Bragard, Thierry Candresse, Gianni Gilioli, Jean-Claude Grégoire, Imre Holb, Michael John Jeger, Olia Evtimova Karadjova, Christer Magnusson, David Makowski, Charles Manceau, Maria Navajas, Trond Rafoss, Vittorio Rossi, Jan Schans, Gritta Schrader, Gregor Urek, Johan Coert van Lenteren, Irene Vloutoglou, Stephan Winter and Wopke van der Werf.

The Panel wishes to thank: Richard Baker, Andrew Hart, Diego Intrigliolo, David Makowski, Marco Pautasso, Trond Rafoss, Jan Schans, Wopke van der Werf and Antonio Vicent for the preparatory work on this scientific opinion, the hearing expert Eduardo Primo Millo and EFSA staff: Giuseppe Stancanelli, Olaf Mosbach Schulz, Francesca Riolo, Jose Cortinas Abrahantes, Ewelina Czwienczek, Tilemachos Goumperis and Marilia Ioannou, for the support provided to this scientific opinion.

Opinion of the Scientific Committee/Scientific Panel
On request from
European Commission
Question Number
30 January 2014
21 February 2014
European Food Safety Authority (EFSA), Parma, Italy
Download Article (3.89 MB)

The Panel conducted a risk assessment of Phyllosticta citricarpa for the EU. P. citricarpa causes citrus black spot (CBS) and is absent from the EU. Under the scenario of absence of specific risk reduction options against P. citricarpa, the risk of entry of P. citricarpa was rated as likely for citrus plants for planting and citrus fruit with leaves, moderately likely for citrus fruit without leaves, unlikely for citrus leaves for cooking and very unlikely for Tahiti lime fruit without leaves. Establishment was rated as moderately likely because susceptible hosts are widely available and environmental conditions in many EU citrus-growing areas are suitable (with high uncertainty) for P. citricarpa ascospore production, dispersal and infection.  Current fungicide treatments will not prevent establishment. Environmental favourability is increased by the use of sprinkler and micro-sprinkler irrigation in some EU citrus-growing locations. Spread with trade was rated as moderately likely. Model results indicate that CBS epidemics are most likely to develop in EU citrus-growing areas in late summer to early autumn and in some locations also in late spring to early summer. CBS is expected to affect mainly lemons and late-maturing sweet orange and mandarin varieties, with moderate negative consequences for the production of fresh fruit, but with environmental impact of additional fungicide treatments. Negative consequences would be minor for early-maturing citrus varieties and minimal for citrus for processing. Uncertainty concerning the consequences is high, mainly because of the lack of data on critical climate response parameters for the pathogen but also because information on impact in areas at the limits of the current distribution is scarce. Since eradication and containment are difficult, phytosanitary measures should focus on preventing entry. Current phytosanitary measures are evaluated to be effective, with the exception of pest-free production sites.


The European Commission requested EFSA to prepare a pest risk assessment of the citrus black spot (CBS) fungus Guignardia citricarpa Kiely (all strains pathogenic to Citrus), to identify risk reduction options and to evaluate their effectiveness in reducing the risk to plant health posed by this organism in the EU territory. EFSA was also requested to carry out an evaluation of the effectiveness of the present EU requirements for Guignardia citricarpa in reducing the risk of introduction of this harmful organism into the EU. Furthermore, EFSA was requested to assess the risk associated with Citrus latifolia plants, including fruit, for the entry of this organism into the EU.

Following a request from the European Commission, the EFSA’s Scientific Panel on Plant Health (PLH) had undertaken in the summer 2013 a public consultation on the draft Scientific Opinion on the risk to plant health of Phyllosticta citricarpa (Guignardia citricarpa)for the EU territory.  The comments received during the public consultation were taken into account and the Scientific Opinion was revised accordingly.

The Panel on Plant Health (PLH) conducted the risk assessment following its guidance documents on a harmonised framework for pest risk assessment (EFSA Panel on Plant Health (PLH), 2010) and on evaluation of risk reduction options (EFSA Panel on Plant Health (PLH), 2012).

The Panel conducted the risk assessment in the absence of current and potential new risk reduction measures in place. The risk assessment therefore expresses the full risk posed by P. citricarpa to the EU territory corresponding to a situation in which all current EU citrus requirements listed in Council Directive 2000/29/EC (in Annexes II, III, IV and V) and Commission Decisions 2004/416/EC and 2006/473/EC are lifted without being replaced by any other risk reduction measures. The Panel undertook a simplified quantitative pathway analysis exercise for the trade of commercial citrus fruit in order to examine with further detail the various steps involved in a potential pathogen entry process and to support the qualitative ratings.

The risk assessment covers Guignardia citricarpa Kiely, which has since been renamed Phyllosticta citricarpa (McAlpine) Van der Aa. Other Phyllosticta species associated with citrus are not included.

After consideration of the evidence, the Panel reached the following conclusions:

With regard to the pest categorisation:

P. citricarpa is absent from the EU and has a potential for establishment and spread and for causing consequences in the risk assessment area.

With regard to the assessment of the risk to plant health for the EU territory:

Under the scenario in which all current EU requirements listed in Council Directive 2000/29/EC and Commission Decisions 2004/416/EC and 2006/473/EC are lifted, the conclusions of the pest risk assessment are as follows:


The probability of entry is rated as:

  • moderately likely for the citrus fruit trade pathway (medium uncertainty)
  • very unlikely for the Tahiti lime (Citrus latifolia) fruit trade pathway (high uncertainty)
  • unlikely for citrus fruit import by passengers traffic pathway (medium uncertainty)
  • likely for the citrus fruit with leaves trade pathway (medium uncertainty)
  • likely for the citrus plants for planting trade pathway (low uncertainty)
  • likely for the Tahiti lime (Citrus latifolia) plants for planting trade pathway (high uncertainty)
  • likely for the citrus plants for planting import by passengers traffic (medium uncertainty)
  • unlikely for the citrus leaves (medium uncertainty).


The probability of establishment is rated as moderately likely because of:

  • the widespread availability of susceptible hosts (no uncertainty)
  • the climate suitability for ascospores maturation, dispersal and infection of many EU citrus-growing areas in late summer and early autumn and for specific location also in late spring and early summer (high uncertainty)
  • cultural practices (fungicides) not preventing establishment (low uncertainty)
  • sprinkle and micro-sprinkle irrigation (still used in part of the EU citrus-growing areas) favouring establishment (low uncertainty)

Overall, the uncertainty on the probability of establishment is rated as high, mainly because of lack of knowledge of how P. citricarpa will respond under the EU climatic conditions. Although it is known which environmental factors are important to the organism in the various stages of the life cycle, there is insufficient scientific evidence to determine the exact thresholds of these factors required by the organism., e.g. temperature and wetness levels and durations. Further validation of the models applied by the Panel, especially for marginal areas within the current distribution of the citrus black spot disease, would be needed to reduce the uncertainty on the probability of establishment of P. citricarpa in the EU.


Natural spread of P. citricarpa is known to mainly happen by dispersal of airborne ascospores. There is little evidence about the dispersal distances of the pathogen by natural means, The pathogen is very likely to spread with human assistance along the commercial fruit and plants for planting pathways. However, because spread is defined as the expansion of the geographical distribution of a pest within an area, the rate of spread depends not only on the rapidity of movement and the number of spread pathways but also on the likelihood of finding a suitable environment for establishment. When the proportion of the citrus-growing areas identified as potentially suitable for P. citricarpa is taken into account, the Panel considered that a rating of moderately likely is most appropriate for spread.

Although there is uncertainty about the potential natural spread of ascospores carried by wind over long distances, this uncertainty does not concern the two main pathways of spread (intra-European trade of commercial fruit and plants for planting).

Endangered area

The risk assessment has identified parts of the EU where host plants are present and where, based on simulation results, the climatic conditions are suitable for ascospore maturation and release followed by infection.

Conclusions from simulations of the release of ascospores based on gridded interpolated climate data of the EU citrus-producing areas show that, in almost all years, ascospore release in the EU citrus growing areas will start early enough to coincide with climatic conditions that are conducive to infection in September and October. However, the simulations indicate that the onset of ascospore release in most areas will start too late to coincide with the climatic conditions conducive to infection in spring. Therefore, early-maturing citrus varieties might generally be infected in late summer and early autumn, which is when the availability of inoculum coincides with suitable conditions for infection. Owing to the long incubation time, fruits from these early varieties will be harvested before symptoms appear. The late-maturing oranges varieties and lemons are expected under such scenario to show CBS symptoms

There are some areas, however, such as locations in Portugal, southern Italy, Cyprus, the Greek islands, Malta and southern Spain, where development of ascospores is expected also in late spring and early summer months in part of the years simulated. In those years, it is expected that symptoms can develop on the fruit before harvest, and therefore have an impact on the fruit quality.

The uncertainty is high as indicated in the establishment section


The results from the simulation of ascospore maturation, release and infection show that citrus black spot will develop and express symptoms mainly in late-maturing sweet orange varieties and lemons grown within the endangered area. The expected consequences will be moderate for fresh fruit of late-maturing citrus varieties and lemons. There would a potential for reduction in disease incidence by chemical treatments, but this would cause environmental impacts because in most EU citrus-growing areas fungicides are not widely applied and the most effective fungicide products are not currently registered for use in citrus in the EU MSs. In addition, to export citrus fruit to areas where CBS is regulated, additional fungicide treatments in the orchards, official inspections, quality controls in packing houses and/or establishment of pest-free areas might be needed to meet the phytosanitary requirements of these countries.

The consequences for fresh fruit of early-maturing citrus varieties are assessed as minor. The impact on early-maturing varieties would be sporadic in time and space, limited to years with rainy springs and summers and/or to specific locations. However, the impact could be higher in areas where late spring and early summer infection, based on simulation results, is expected to be more frequent.

The consequences would be minimal for citrus for processing, as external lesions or spots on citrus fruit are not a quality issue for citrus for processing.

As for establishment, the uncertainties about consequences are high owing to the lack of information on key parameters in the epidemiological models and on the incubation period; the lack of knowledge about the rate of disease build-up for this pathogen; and the limited information available about the impact of the disease and the programmes of fungicide treatments in semi-arid areas within the current CBS area of distribution, e.g. Eastern Cape, where environmental conditions are more similar to those in the pest risk assessment area.

With regard to risk reduction options, the Panel notes that, for the reduction of the probability of entry of P. citricarpa, prohibition and import from pest-free areas have overall a high to very high effectiveness with moderate to high feasibility for all pathways. Prohibition of parts of the host also has high effectiveness and very high feasibility with regard to the prohibition of citrus fruit with leaves and peduncles. For the fruit pathway, systems approaches as well as the induction of precocious symptoms expression in latent infections also have high effectiveness and feasibility. For plants for planting, certification and pre- and post-entry quarantine systems were also found to have high effectiveness and feasibility.

For reduction of the probability of establishment and spread, the application of strict waste processing measures would be highly effective in reducing the potential transfer of P. citricarpa from infected citrus fruit, both for entry and spread, although with low feasibility. The effectiveness of eradication, as well as of containment, is assessed as low. The application of drip irrigation practices will moderately reduce the probability of establishment.

The effectiveness of current EU phytosanitary measures to reduce the risk of P. citricarpa introduction ranges from moderate to high, except for the pest free production site, for which the effectiveness is rated as low.

After establishment, P. citricarpa has not been eradicated anywhere and is reported to be very difficult to contain. Therefore risk reduction options to prevent the entry of the pathogen are evaluated as most effective. Should the disease be reported from the risk assessment area, limited options are available to reduce the risk of establishment and spread.

Phyllosticta citricarpa, Guignardia citricarpa, citrus black spot, European Union, pest risk assessment, risk reduction options
Print on demand
Number of Pages