Following a request from the European Commission, the Panel on Plant Health was asked to deliver a scientific opinion on a document titled “Citrus Black Spot: Pest Risk Assessment document for the review of current phytosanitary regulations pertaining to the export of fresh citrus fruit from the Republic of South Africa to the EU”, received in June 2000 from the national plant protection organisation of South Africa. In particular, the Panel was requested, pursuant to Article 29(1) and Article 22(5) of Regulation (EC) No 178/2002, to provide a scientific opinion on the pest risk assessment and additional supporting evidence provided by South Africa, with regard to the suitability of the European Union (EU) citrus fruit producing areas, the likelihood of an introduction, leading to an establishment, and the appropriateness of the level of protection under the existing management options. The Panel was also asked to identify whether effective options, alternative to those already present in Directive 2000/29/EC, could be suggested to prevent introduction of citrus black spot into the Community.
This document presents the opinion of the Panel on Plant Health on the pest risk assessment conducted by South Africa on Guignardia citricarpa with the EU citrus growing areas as endangered area.
Citrus black spot (CBS), caused by the fungus Guignardia citricarpa Kiely, is a leaf-spotting and fruit-blemishing disease affecting Citrus, Poncirus, Fortunella spp. and their hybrids. Except for sour orange and Tahiti limes, all commercially grown citrus species and cultivars are affected by the disease. Lemon is particularly susceptible and thus, in an unaffected area, the disease usually first appears on this species. CBS is present in citrus-producing areas in Asia, Oceania, Africa and South America, but it has never established in Europe, North America, Central America and the Caribbean region. Due to the external blemishes, CBS symptomatic citrus fruit is unsuitable for the fresh market. Severe infections may cause premature fruit drop, especially in years favourable for disease development and when fruit is held on the trees past peak maturity. In addition, asymptomatic fruit at harvest may still develop symptoms during transport or in storage. The pathogen is classified as a harmful organism for the European Community in Annex II part A Section I of the Council Directive 2000/29/EC.
The Panel examined in detail the risk assessment provided, and considered the accuracy and quality of the information provided and methods applied for pest risk assessment purposes. The review was based on the principles of the International Standard on Phytosanitary Measures ISPM No. 11: Pest risk analysis for quarantine pests including analysis of environmental risks and living modified organisms (2004) and the International Standard on Phytosanitary Measures ISPM No. 14: The use of integrated measures in a systems approach for pest risk management (2002), by the International Plant Protection Convention (IPPC) (FAO, 2007).
The Panel, has studied the pest risk assessment and additional supporting evidence supplied by South Africa, as well as new information collected by the Panel, and concludes the following.
1. With regard to the suitability of the EU citrus fruit producing areas for establishment of CBS in terms of their climatic conditions:
Based on (a) the evaluation of the application of CLIMEX (Paul et al., 2005), (b) the limitations of CLIMEX in predicting the potential distribution of pathogens such as G. citricarpa, (c) the relative climatic similarities between locations where CBS occurs in Eastern Cape Province and some locations where citrus is grown in the EU and (d) the results of the application of a generic infection model for foliar fungal pathogens, the Panel cannot agree with the conclusion by Paul et al. (2005) that the climate of the EU is unsuitable for the establishment of G. citricarpa.
2. With regard to the likelihood of an introduction, leading to an establishment, of CBS to the EU citrus fruit producing areas on CBS infected citrus fruit:
The Panel considers that G. citricarpa is associated with the citrus fruit in South Africa, is able to survive transport, storage and existing pest management procedures, especially in the form of quiescent infections and inconspicuous symptoms, and may be transferred to suitable hosts by means of splash dispersal from citrus black spot infected citrus fruit and peel. The Panel therefore concludes that G. citricarpa may enter the PRA area with infected citrus fruit. The Panel has also determined that, given the widespread distribution of susceptible hosts within the PRA area, cultural and climatic factors will not prevent the establishment of the pathogen.
The Panel concludes therefore that entry of G. citricarpa, leading to establishment in the EU citrus fruit production areas, on CBS infected citrus fruit is possible. The South African documents do not provide sufficient evidence to demonstrate that the importation of citrus fruit from infested areas is a very unlikely pathway for the introduction of G. citricarpa into these areas.
3. With regard to the appropriateness of the level of protection under the existing risk management options listed in Annex IV, Part A, Section I, point 16.4 of Council Directive 2000/29/EC:
Theoretically, the four existing risk management options are effective and in line with the IPPC principle of ‘equivalence’, but practical limitations may reduce their effectiveness. Option 16.4 (a) (pest free country) would be effective, but does not apply to South Africa. Option 16.4 (b) (pest free area) is effective in principle, but requires intensive continuous monitoring to maintain an accurate delimitation of this area. Information on such a monitoring programme was not provided to the Panel, so the effectiveness of this option could not be evaluated specifically for citrus fruit originating from South Africa. The Panel considered option 16.4 (c) (no symptoms in the field of production) to be not fully effective: the effectiveness depends on the intensity of the field inspection procedures in the field of production. Specification of the methods and level of accuracy of these inspection procedures is not required according to 2000/29/EC, and they are not specified by South Africa. The Panel considered option 16.4 (d) (appropriate field treatments) insufficiently effective, since no mitigating measure in the field, or combination of field treatments has been shown to fully prevent or eliminate fruit infections.
Observing the frequent interceptions of consignments of citrus fruit infested with G. citricarpa, originating from South Africa, the Panel concludes that the existing risk management options are not sufficient to prevent the entry of G. citricarpa.
The Panel observes that the existing measures apply to the whole territory of the European Community, where the movement of consignments of citrus fruit is not restricted. The Panel concludes that phytosanitary inspections and interceptions at all points of entry to the Community are appropriate in order to protect the citrus fruit growing areas. Therefore, the existing measures are in line with the IPPC principle of minimal impact.
Uncertainties associated with estimating the effectiveness of risk management options, which do not affect the Panel conclusions, may arise from lack of information on the sampling procedures that are part of various management options, and from insufficient data on the effectiveness of mitigation methods.
4. With regard to the identification of effective options, alternative to those already present in Directive 2000/29/EC, to prevent introduction of citrus black spot into the Community:
The Panel observes that post-harvest treatments of fruit are currently not listed as risk management options in Annex IV, Part A, Section I, point 16.4 of Council Directive 2000/29/EC. The combination of pre-harvest (field) treatments with post harvest treatments would further reduce, but not eliminate the risk of introduction. The Panel suggests including effective post-harvest treatments in option 16.4 (d). It is noted that, despite routine application of post-harvest treatment of citrus fruit by South Africa, frequent interceptions of infested consignments occur at the Community points of entry. The Panel suggests an investigation of the exact causes for infested consignments arrival at the EU border despite applied mitigation measures in South Africa.
For South Africa, as the country of origin, the Panel suggests that methods to accelerate citrus black spot symptoms development, combined with a standardised sampling scheme, could be applied in a pre-entry quarantine system to improve the detection of infested consignments before shipping.
For the European Community, the Panel suggests that demarcation of endangered and non-endangered areas could be combined with distinctive measures regarding end use and distribution of citrus fruit, that are less trade-restrictive.