Scientific Opinion of the Panel on Plant Health. Adopted by written procedure on 12 March 2008

Transcription

1 The EFSA Journal (2008) 668, 1-22 Pest risk assessment made by France on Fusarium oxysporum. f. sp. cubense considered by France as harmful in French overseas departments of French Guiana, Guadeloupe, Martinique and Réunion 1 Scientific Opinion of the Panel on Plant Health (Question No EFSA-Q ) Adopted by written procedure on 12 March 2008 PANEL MEMBERS Richard Baker, David Caffier, James William Choiseul, Patrick De Clercq, Erzsébet Dormannsné-Simon, Bärbel Gerowitt, Olia Evtimova Karadjova, Gábor Lövei, Alfons Oude Lansink, David Makowski, Charles Manceau, Luisa Manici, Dionyssios Perdikis, Angelo Porta Puglia, Jan Schans, Gritta Schrader, Robert Steffek, Anita Strömberg, Kari Tiilikkala, Johan Coert van Lenteren and Irene Vloutoglou SUMMARY Following a request from the European Commission, the Panel on Plant Health was asked to deliver a scientific opinion on 30 pest risk assessments made by France on organisms which are considered by France as harmful in four French overseas departments, i.e. French Guiana, Guadeloupe, Martinique and Réunion. In particular, the Panel was asked whether these organisms can be considered as harmful organisms for the endangered area of the above departments, in the meaning of the definition mentioned in Article 2.1. (e) of Directive 2000/29/EC and thus potentially eligible for addition to the list of harmful organisms in Directive 2000/29/EC. This document presents the opinion of the Panel on Plant Health on the full 2 pest risk assessment conducted by France on Fusarium oxysporum Schlecht. f. sp. cubense (E.F. Smith) W.C. Snyder & H.S. Hansen with French Guiana, Guadeloupe, Martinique and Réunion considered as endangered area. F. oxysporum f. sp. cubense is responsible for Fusarium wilt (also known as Panama disease), which is one of the most destructive diseases of banana world-wide. Control of the disease is restricted to husbandry measures and cultivar resistance. F. oxysporum f. sp. cubense has been divided into races based on its pathogenicity on reference host cultivars. Among the most significant races of F. oxysporum f. sp. cubense pathogenic to edible banana, race 1 affects mainly the cultivar Gros Michel, race 2 affects bananas of the Bluggoe sub-group, race 4 affects all cultivars in the Cavendish sub-group grown in subtropical 1 For citation purposes: Scientific Opinion of the Panel on Plant Health on a request from the European Commission on Pest risk assessment made by France on Fusarium oxysporum. f. sp. cubense considered by France as harmful in French overseas departments of French Guiana, Guadeloupe, Martinique and Réunion. The EFSA Journal (2008) 668, The full pest risk assessments have been made according to the Guidelines for the European and Mediterranean Plant Protection Organisation (EPPO) pest risk assessment scheme in EPPO Standard PM 5/3 (1) (EPPO Bulletin 27, ). European Food Safety Authority, 2008

2 climates plus cultivars susceptible to races 1 and 2. F. oxysporum f. sp. cubense race 4 is commonly known as subtropical race 4. F. oxysporum f. sp. cubense tropical race 4 (hereinafter T4) is a new variant, which was recognised in the early 1990s and is responsible for serious losses of cultivars in the Cavendish subgroup in some areas of tropical South East Asia. Both races 1 and 2 are reported to be endemic in the PRA area 3, while races 4 and T4 are not known to be present. Race 4 has been under quarantine regulation since 1992 for French Guiana, Guadeloupe, Martinique and Réunion. 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 : Pest risk analysis for quarantine pests, including analysis of environmental risks and living modified organisms (2004) by the International Plant Protection Convention (FAO, 2007b). Following a detailed analysis of the material provided in the pest risk assessment and after additional study of published information on the pathogen and the disease it causes, the Panel observes that: The document only cites one reference, which is a review article. As a consequence, statements in the pest risk assessment are not individually referenced or supported by verifiable scientific data. The risk assessor identifies the pest as F. oxysporum f.sp. cubense, which implies that all races are under consideration. However most of the document focuses only on races 4 and T4. This confuses the identity of the subject organism of the pest risk assessment. F. oxysporum f.sp. cubense, races 1 and 2 are reported to be present in most departments defined as the PRA area (i.e. French Guiana, Guadeloupe and Martinique) and are not reported to be under official control in the document. Races 4 and T4 are not known to be present in the PRA area. The Panel concludes that: Only the races 4 and T4 fulfil the criteria for a quarantine pest 5, as they are not known to occur in the PRA area and have the potential for establishment and spread and for negative economic consequences in the PRA area. In agreement with the document, the probability of entry of F. oxysporum f.sp. cubense races 4 and T4 into the PRA area on conventional planting material, from countries where the disease is present, would be high if present import restrictions were rescinded. In agreement with the document, the probability of establishment for F. oxysporum f.sp. cubense race 4, which attacks Cavendish cultivars in the subtropics, would be low, except for those parts of the PRA area with subtropical climate, where the probability for establishment of race 4 would be high. The probability of establishment for F. oxysporum f.sp. cubense race T4, which is able to attack Cavendish cultivars in the tropics, would be high (rather than moderate ), as most of 3 PRA area is the area in relation to which a Pest Risk Analysis is conducted [FAO, 2007a]. 4 ISPM International Standard for Phytosanitary Measures. ISPM No. 11: Pest risk analysis for quarantine pests, including analysis of environmental risks and living modified organisms. 5 A quarantine organism is a pest of potential economic importance to the area endangered thereby and not yet present there, or present but not widely distributed and being officially controlled [FAO, 1990; revised FAO, 1995; IPPC 1997]. The EFSA Journal (2008) 668, 2-22

3 the endangered area has a tropical climate and no commercial Cavendish cultivars resistant to race T4 have yet been developed or tested in the French overseas departments. In agreement with the document, the potential economic impacts of races 4 and T4 would be high. Plantations of dessert bananas for export and smallholdings and family gardens producing fruit for the local market or for home-consumption would suffer severe yield losses. Concerning social impacts, for Guadeloupe and Martinique there could be a reduction in employment in commercial plantations, whilst a potential disruption of subsistence production and consumption patterns could occur among smallholders and family gardens. The Panel, based on the information provided in the document and on additional literature consulted, concludes that F. oxysporum f.sp. cubense races 4 and T4 are appropriate for evaluation of pest risk management options for the endangered areas of French Guiana, Guadeloupe, Martinique and Réunion, and thus potentially eligible for addition to the list of harmful organisms in Directive 2000/29/EC. Key words: banana, Cavendish sub-group, French overseas departments, Fusarium oxysporum. f. sp. cubense race 4, Fusarium wilt, Musa spp., Panama disease, pest risk assessment, tropical race 4 The EFSA Journal (2008) 668, 3-22

4 TABLE OF CONTENTS Panel Members...1 Summary...1 Table of Contents...4 Background as provided by the European Commission...5 Terms of reference as provided by the European Commission...6 Acknowledgements...6 Assessment Introduction General introduction to Fusarium oxysporum f. sp. cubense The document under scrutiny Evaluation procedure General comments on the document Methodology applied for the risk assessment Evaluation of the pest risk assessment Pest categorization Identity of pest Presence or absence in PRA area Regulatory status in PRA area Potential for establishment and spread in PRA area Potential for economic consequences in PRA area Conclusion of pest categorization Assessment of the probability of introduction and spread Probability of entry of the pest Identification of pathways Probability of pest being associated with the pathway at origin Probability of survival during transport or storage Probability of the pest surviving existing pest management procedures Probability of transfer to a suitable host Conclusion of entry Probability of establishment Availability of suitable hosts, alternate hosts and vectors in the PRA area Suitability of environment Cultural practices and control measures Conclusion of the probability of establishment Probability of spread after establishment Conclusion on probability of introduction and spread Assessment of potential economic consequences Direct pest effects Crop quality and/or yield losses Control measures, efficacy and costs Indirect pest effects Export markets Social consequences Environmental consequences Conclusion of the assessment of economic consequences Comments on the conclusion of the pest risk assessment Degree of uncertainty...17 Conclusions and Recommendations...17 Documentation provided to EFSA...19 References...19 The EFSA Journal (2008) 668, 4-22

5 BACKGROUND AS PROVIDED BY THE EUROPEAN COMMISSION 6 The current Community plant health regime is established by Council Directive 2000/29/EC on protective measures against the introduction into the Community of organisms harmful to plants or plant products and against their spread within the Community (OJ L169, l , p. l), as last amended by Commission Directive 2006/35/EC (OJ L88, , p. 9). The Directive lays down, amongst others, the technical phytosanitary provisions to be met by plants and plant products and the control checks to be carried out at the place of origin on plants and plant products destined for the EC or moved within the EC, the list of harmful organisms whose introduction into or spread within the EC is prohibited and the control measures to be carried out at the outer border of the EC on arrival of plants and plant products. A harmful organism is defined in its Article 2.1.(e) as: any species, strain or biotype of plant, animal or pathogenic agent injurious to plants or plant products. However, the provisions of the Directive are at present not yet applicable to trade in plants and plant products between the French overseas departments and the remainder of the Community. In view of the special nature of the agricultural production of the French overseas departments, additional protective measures justified on grounds of the protection of health and life of plants and plant products therein should be given. France has therefore prepared for 4 departments (Guadeloupe, Guyana, Martinique and Réunion 130 pest risk analyses (PRA) on organisms which are considered by France as harmful for the most important crops grown in these departments, such as banana, sugar cane, pine apple, rice, coffee, orchids, Palmae, etc. These PRAs cover a wide range of harmful organisms, such as insects and mites (54), fungi (14), bacteria (20) and virus (42). In accordance with the discussions on this topic in the meeting of the Standing Committee on Plant Health on 27 and 28 April 2006, it was agreed that in a first phase France would select 30 PRAs among the 130 PRAs initially transmitted. They cover harmful organisms (insects, mites, fungi, bacteria and virus) affecting citrus fruit and bananas grown in the above departments. Two types of PRA have been made: a full PRA for harmful organisms for which the probability of introduction into the French overseas departments is high with economic important crops and a simplified PRA for organisms for which the probability of introduction is extremely low. The full PRAs have been made according to the Guidelines for the European and Mediterranean Plant Protection Organisation (EPPO) pest risk assessment scheme in EPPO Standard PM 5/3 (1) (EPPO Bulletin 27, ). This scheme aims at assessing the potential risk of a particular pest (or harmful organism) for a clearly defined area through a quantitative evaluation of that risk based on questions to which replies are given on a 1-9 scale. Expert judgement is used in interpreting the replies. Moreover for each of the 130 harmful organisms a data sheet containing the most important data on the organism has been made according to the EPPO Standard PM 5/1 (1) on Checklist of information required for PRA (EPPO Bulletin 23, ). The guidelines are based on many years experience of EPPO experts in the EPPO Panel on PRA and the EPPO Panel on phytosanitary measures. They conform with the International Standards on Phytosanitary Measures ISPM No. 11 (Guidelines on PRA for quarantine pests) and use the terms of ISPM No 5 (Glossary of phytosanitary terms). The simplified PRAs contain in a synthetic fiche the information available allowing the assessment of the risk associated with the relevant organism. 6 Submitted by the European Commission, ref. SANCO E/1/VE/svi D(2006) The EFSA Journal (2008) 668, 5-22

6 TERMS OF REFERENCE AS PROVIDED BY THE EUROPEAN COMMISSION EFSA is requested, pursuant to Article 29(1) and Article 22(5) of Regulation (EC) No 178/2002, to provide a scientific opinion on 30 PRAs made by France on organisms which are considered by France as harmful in 4 French overseas departments, i.e. Guadeloupe, French Guiana, Martinique and Réunion, and in particular whether these organisms can be considered as harmful organisms for the endangered area of the above departments in the meaning of the definition mentioned in Article 2.1.(e) of Directive 2000/29/EC and thus potentially eligible for addition to the list of harmful organisms in Directive 2000/29/EC. ACKNOWLEDGEMENTS The European Food Safety Authority wishes to thank the members of the Working Group for the preparation of this opinion James William Choiseul, Erzsébet Dormannsné-Simon, David R. Jones, Alfons Oude Lansink, David Makowski, Luisa Manici, Angelo Porta Puglia, Robert Steffek, Anita Strömberg and Irene Vloutoglou. The EFSA Journal (2008) 668, 6-22

7 ASSESSMENT 1. Introduction This document presents the opinion of the Panel on Plant Health on the pest risk assessment conducted by France on Fusarium oxysporum Schlecht. f. sp. cubense (E.F. Smith) W.C. Snyder & H.S. Hansen with French Guiana, Guadeloupe, Martinique and Réunion considered as endangered area General introduction to Fusarium oxysporum f. sp. cubense F. oxysporum. f. sp. cubense is a soil-borne fungus which is responsible for Fusarium wilt or Panama disease of banana. This disease is considered to be one of the most potentially destructive affecting bananas world-wide. In the 1940 s and 50 s the disease caused very significant damage to commercial banana plantations and resulted in the complete abandonment of the then industrial standard cultivar Gros Michel, for cultivars of the resistant Cavendish sub-group (Ploetz, 2000). Although there is some regional variation, currently, commercial banana growing relies upon Cavendish sub-group cultivars which, until recently, were not significantly affected by the disease (Ploetz, 2005). The term and concept of race has been used to classify strains of F. oxysporum f.sp. cubense since the mid 1900 s (Stover, 1962) and, although it is an imperfect measure of pathogen diversity in the complex, it provide useful information (Ploetz, 2006). The races of F. oxysporum f.sp. cubense are designated on the basis of their pathogenicity to different reference banana cultivars. Of these, the most significant are F. oxysporum f.sp. cubense race 1, which is pathogenic to the cultivar Gros Michel (AAA type) (Stover, 1962), F. oxysporum f.sp. cubense race 2 which affects bananas of the Bluggoe sub-group (ABB type, cooking bananas), F. oxysporum f.sp. cubense race 4, commonly known also as F. oxysporum f.sp. cubense subtropical race 4 (Grimbeek et al., 2001), which affects cultivars in the Cavendish sub-group (AAA type) in the subtropics where cold winter temperatures are thought to predispose Cavendish genotypes to race 4 (Su et al., 1986; Ploetz 2005a; Ploetz 2005b). F. oxysporum f.sp. cubense race 4 affects all Cavendish cultivars, those cultivars that are attacked by race 1 and 2 and diverse additional cultivars such as Pisang Mas (AA) (Ploetz and Pegg, 2000). F. oxysporum f.sp. cubense tropical race 4 (T4) was only identified in the early 1990 s (Pegg et al., 1993; Ploetz, 1994); it is distinguished from F. oxysporum f.sp. cubense race 4 because it is genetically distinct (Pegg et al., 1994; Bentley et al., 1998) and damages Cavendish sub-group in the tropics (Pegg et al., 1994; Ploetz, 2005b). F. oxysporum f.sp. cubense race 1 and 2, widespread in banana-growing regions of India, Asia, Africa, Australia, Central and South America, were under control in the 1960 s after the replacement of cultivar Gros Michel with the resistant sub-group Cavendish (Stover, 1962). Fusarium wilt on the Cavedish subgroup caused by F. oxysporum f.sp. cubense race 4 was reported in Canary and Madeira Islands, South Africa, Australia and in Taiwan (Ploetz and Pegg, 2000; Ploetz, 2005b). F. oxysporum f.sp. cubense race T4, the recently emerging variant, has been reported to affect Cavendish sub-group in a restricted areas of South East Asia (Malaysia and Indonesia) and in northern Australia (Ploetz, 2005). As described below in the paragraph on the vegetative compatibility groups (VCGs), some strains of the pathogen identified in Taiwan have been shown by VCGs analysis to belong to F. oxysporum f.sp. cubense race T4. The presence of F. oxysporum f.sp. cubense race T4 in Taiwan, which is The EFSA Journal (2008) 668, 7-22

8 mainly subtropical, can be explained as banana production areas in Taiwan have relatively warm winters and are technically in the tropics (Ploetz, 2005b). Both F. oxysporum f.sp. cubense races 1 and 2 are endemic in the French overseas departments (CAB International, 1999), while races 4 and T4 are not known to be present. F. oxysporum f.sp. cubense race 4 has been under quarantine regulation since 1992 for French Guiana, Guadeloupe, Martinique and Réunion. The principal means of F. oxysporum f.sp. cubense spread is by infected suckers or rhizome pieces used for planting. The organism can also spread by contaminated soil attached to planting material or farm machinery and by water running through infested soil. However, these means are of more significance in terms of local spread (Ploetz and Pegg, 2000). Propagation by means of vitroplants will eliminate F. oxysporum f.sp. cubense from the early stages of the planting material production process. However, in order to ensure that plants are disease free, vitroplants must be hardened-off in F. oxysporum f.sp. cubense-free nursery soil prior to transfer to banana plantations (Subramaniam, 1970; Ploetz, 2006). Control of Fusarium wilt by chemical methods is generally ineffective. The most effective and sustainable means of control is to grow cultivars with resistance to local races of the pathogen (Moore et al., 2001). The genetic diversity that occurs within F. oxysporum f.sp. cubense has been first determined using VCGs, which divided F. oxysporum f.sp. cubense into at least 21 groups. (Ploetz and Correll, 1988). The majority of the isolates belonged to two major VCGs, each containing more than one race of the pathogen. Minor VCGs have a limited geographical distribution, among them VCGs , which correspond to the population of the pathogen identified as T4 from South-East Asia (Pegg et al., 1994; Ploetz, 1994). VCG analysis has also revealed that some strains of the pathogen attacking Cavendish in Taiwan actually belong to F. oxysporum f.sp. cubense T4 and not to F. oxysporum f.sp. cubense race 4 as first believed (Moore et al., 2001). To date it is not known which VCGs predominate on Cavendish in Taiwan (Ploetz, 2005b). The more recent studies using restriction fragment length polymorphism (RFLP) of genomic DNA divided F. oxysporum f.sp. cubense strains into two main clades with a differing genetic stability (Koenig et al., 1997; Bentley et al., 1998). These findings were confirmed by studies based on DNA sequencing analysis (O Donnel et al., 1998; O Donnel and Cigelnik, 1999), which, also in this case, could not find correlation between their analysis and the existing race structure in F. oxysporum f.sp. cubense. In all cases, these findings further support the genetic diversity of the pathogen already observed by VCGs. The evaluation of resistance of banana cultivars to F. oxysporum f.sp. cubense, requires laborious in vivo assessments. Inoculation on susceptible genotypes has been for a long time the only means of distinguishing F. oxysporum f.sp. cubense races. In addition to the time and labour required by these tests, disease symptoms expression is affected by several factors including inoculum concentration, edaphic conditions and temperature (Backeman et al., 1962; Brake et al., 1995). The diagnostic polymerase chain reaction (PCR) test for detection of F. oxysporum f.sp. cubense races has been investigated by several researchers in the 1990 s (Thomas et al., 1994; Edel et al., 2000) The document under scrutiny The assessment of risks of the organism in subject is presented by the French risk assessors in a full pest risk assessment made according to the Guidelines for the European and Mediterranean Plant Protection Organisation (EPPO) pest risk assessment scheme [EPPO The EFSA Journal (2008) 668, 8-22

9 Standard PM 5/3 (1)]. Risk management options are not included and therefore the document is only a pest risk assessment and not a pest risk analysis. Based on this document France requested F. oxysporum f.sp. cubense be added to the list of harmful organisms in Directive 2000/29/EC Evaluation procedure The Panel examined in detail the documents provided, and considered the accuracy and quality of the information 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) by the International Plant Protection Convention (FAO, 2007b). The evaluation of the French document was conducted on the basis of an English translation from an original submission in French, which remains the reference language. Detailed comments have been made only for the questions where it was considered that the French assessment is incorrect or could be improved. Where the Panel has uncovered new information that supports the French document, this has been noted. While the literature has been checked and additional data has been sought, no new analysis has been undertaken. The Panel has noted where it considers the risk scores provided by France to be too low or too high but has not suggested an exact score General comments on the document The document under scrutiny was produced in 2003, it comprises 25 pages and is organised in two parts: Part I. provides the information required for the pest risk assessment of F. oxysporum f.sp. cubense for the areas of the French Guiana, Guadeloupe, Martinique and Réunion based on EPPO Standard PM 5/1(1) Part II. provides the pest risk assessment of the organism in subject based on PM 5/3(1) In relation to the structure and the quality of the document, the Panel found that: The risk assessor identifies the pest as F. oxysporum f.sp. cubense, which implies that all races are under consideration. However most of the document F. oxysporum f.sp. cubense causes only on F. oxysporum f.sp. cubense races 4 and T4. This is misleading and makes the identity of the subject organism of the pest risk assessment unclear. The document only cites one reference, which is a review article (Ploetz and Pegg, 2000) in a book on banana diseases (Jones, 2000). As a consequence, statements in the pest risk assessment are not individually referenced or supported by verifiable scientific data Methodology applied for the risk assessment The Panel considered the methodology used in the risk assessment provided in Part 2 of the document and concluded that: The document does not completely analyse the new situation that would arise in the pest risk assessment area if the current regulations controlling banana imports were to be rescinded, although this aspect has been mentioned. The probabilities of entry, establishment and spread, and the potential impacts (economic, social, environmental) of the pathogen in the pest risk assessment area should have been The EFSA Journal (2008) 668, 9-22

10 clearly outlined for each of the French overseas departments, because of their specific geographic locations. A number of estimates provided in Part 2 (Pest Risk Assessment) cannot be justified or substantiated by the information provided in Part 1 of the document. The method of combining risk ratings and ascribing an overall risk rating is not defined and assumes equal weighting to the questions. 2. Evaluation of the pest risk assessment 2.1. Pest categorization Identity of pest In Part 1, the risk assessor identifies the pest as F. oxysporum f. sp. cubense and states that the taxonomy of the pathogen distinguishes various physiological races. The French document in Part 2 pest risk assessment (Stage 1. Initiation) defines F. oxysporum f. sp. cubense as a single taxonomic entity. While the pest definition of the French document in the title and in the introductions of Part 1 and Part 2 suggests to the readers that all races of F. oxysporum f.sp. cubense are under consideration, the pest risk assessment (Part 2), from the section on pest categorisation to the end of document, focuses on races 4 and T4. This appears inconsistent and causes confusion. The races of F. oxysporum f.sp. cubense under consideration in the French document should have been better defined for a clear identification of the pest. F. oxysporum f.sp. cubense can be adequately identified and distinguished both at species and at race level (Leslie and Summerell, 2006). Both races 4 and T4 are the only F. oxysporum f.sp. cubense races which can attack banana varieties of the Cavendish subgroup. F. oxysporum f.sp. cubense race T4 can be distinguished from race 4 because it is genetically distinct (Pegg et al., 1994; Bentley et al., 1998), and damages Cavendish sub-group in the tropics (Pegg et al., 1994; Ploetz, 2005b) Presence or absence in PRA area The French document states in Part 1 that F. oxysporum f.sp. cubense race 1 and 2 are present in three of the four French overseas department: French Guiana, Guadeloupe and Martinique. In the pest categorisation of the part 2, it also states that the F. oxysporum f.sp. cubense races 4 and T4 do not occur in the PRA area. The Panel agrees that F. oxysporum f.sp. cubense race 1 and 2 are reported to be present in French Guiana, Guadeloupe and Martinique (Stover, 1962), while races 4 and T4 are not known to occur in the PRA area Regulatory status in PRA area The French document reports in Part 1 that the current rules for the French overseas departments have placed F. oxysporum f.sp. cubense race 4 in the quarantine list since 1992 (JORF 16/02/1992, Annex I B). An overview of current quarantine regulations for F. oxysporum f.sp. cubense races 4 and T4 in the most important banana producing countries would have been useful. For example, current The EFSA Journal (2008) 668, 10-22

11 Australian regulations list F. oxysporum f.sp. cubense race T4 as a quarantine pest (AQIS, 2007a; 2007b). F. oxysporum f.sp. cubense races 1 and 2, which are reported as present in the French Guiana, Guadeloupe and Martinique, are not reported to be under official control in the document Potential for establishment and spread in PRA area Part 2 of the French document defines the eco-climatic conditions of highland areas in Guadeloupe and Réunion as suitable for establishment of F. oxysporum f.sp. cubense race 4 and whole of PRA area as suitable for F. oxysporum f.sp. cubense race T4. The PLH Panel agrees with this evaluation of potential for establishment of F. oxysporum f.sp. cubense races 4 and T4, considering the current geographical distribution of these races in countries with similar climates and the fact that susceptible Cavendish bananas are grown in all the French overseas departments Potential for economic consequences in PRA area Part 2 of the French document defines the organism under consideration as having potential economic consequences in the PRA area. As susceptible banana cultivars are grown in the PRA area and Fusarium wilt is one of the most destructive banana diseases, the Panel agrees that F. oxysporum f.sp. cubense races 4 and T4 have the potential for negative economic consequences after entry and establishment Conclusion of pest categorization Considering that F. oxysporum f.sp. cubense races 1 and 2 are present and not reported as having a limited distribution and/or being under official control, the Panel concludes that only the F. oxysporum f.sp. cubense races 4 and T4 fulfil the criteria for a quarantine pest according to the ISPM No. 5 and 11 requirements (FAO, 2007a and b). F. oxysporum f.sp. cubense races 4 and T4 are not known to occur in the PRA area and have the potential for establishment, spread and negative economic consequences in the PRA area Assessment of the probability of introduction and spread Probability of entry of the pest Identification of pathways The main pathway considered by the risk assessor is plant propagation material other than vitroplants. The Panel observes that the type of propagation material described in the document as classic seedling pathway should have been specified in detail (i.e. the import of suckers, rhizomes or rhizome pieces), but agrees with the high risk of this pathway. The Panel agrees with the assessor s statement that the use of F. oxysporum f.sp. cubense-free vitroplants should minimise the risk of introduction. The soil pathway is mentioned but not discussed in the document because the current regulation bans its import. The Panel observes that F. oxysporum f.sp. cubense can survive in the soil for many years (Subramaniam, 1970), thus this pathway could represent a high risk. Infected plant material illegally imported by passengers on aircraft or ships is another pathway of F. oxysporum f.sp. cubense races 4 and T4 identified in the document but considered negligible due to current regulation. The Panel is of the opinion that the difficulties of The EFSA Journal (2008) 668, 11-22

12 enforcing the import ban in French Guiana mentioned in the document increases the risk of entry of the pathogen in the PRA area by this pathway Probability of pest being associated with the pathway at origin The Panel agrees with the high probability for association of the pest with conventional plant propagation material if F. oxysporum f.sp. cubense races 4 and T4 occur in the country of origin. The Panel agrees with the document that the probability for association of the pest with the vitroplants pathway is negligible, as such production systems are characterised by high sanitation practices. According to the FAO/IPGRI Technical Guidelines for the safe movement of Musa germplasm (Diekmann and Putter, 1996), all Musa germplasm should be moved in the form of tissue culture Probability of survival during transport or storage Plant propagation material is transported under conditions which favour the survival of the plant itself (e.g. air transport in cool boxes). Such conditions do not affect the survival of the pathogen. In addition, the pathogen can survive adverse conditions in soil or plant residues as chlamydospores (Stover, 1962). Therefore, the probability of survival of the pathogen during transport or storage would be high Probability of the pest surviving existing pest management procedures The current regulation in force in the French overseas departments bans the import of soil and of any Musa spp. plant material. The Panel understands that there is no probability of introducing the pathogen with vitroplants. F. oxysporum f.sp. cubense is a vascular pathogen and chemical control methods are ineffective (Ploetz and Pegg, 2000). In case of the lifting of the current regulation, the Panel observes that the probability of the pathogen escaping the border inspection is high for the conventional plant propagation material, as the pathogen can be present without visually detectable symptoms. Regarding the identification methods for inspection purposes, in Part 1 the document has briefly described the conventional and new molecular methods (RFLP and nucleotide sequence analysis) used for the detection of F. oxysporum f.sp. cubense. However without addressing the uncertainties coming from the nature of the host pathogen interaction and the effect of climate conditions and other abiotic factors on symptoms expression (Backeman et al., 1962; Ploetz et al., 1990; Brake et al., 1995; Viljoen, 2002). The Panel agrees with the conclusion of the French document in Part 1 that the only reliable method to confirm the pathogenic status of the isolates of F. oxysporum f.sp. cubense is experimental infection. This is correct because race designation currently relies entirely on symptoms development on reference cultivars under field conditions (Groenewalds, 2006). However, the French document adds that this method is rarely undertaken. The Panel observes that, in order to make the diagnosis of Fusarium wilt, it is necessary to isolate the fungus, identify the species and then perform the pathogenicity test (Leslie and Summerell, 2006). This method, although expensive and time consuming, remains the reference diagnostic procedure for F. oxysporum f.sp. cubense (Liberato et al., 2007). Consequently, all methods for rapid screening of plant material for the presence of specific F. oxysporum f.sp. cubense races (i.e PCR, VCGs) need to be always confirmed by pathogenicity tests. The EFSA Journal (2008) 668, 12-22

13 Finally the French document does not mention the method to distinguish races 4 and T4. These races can be clearly distinguished as F. oxysporum f.sp. cubense race T4 isolates damage Cavendish in the tropics (Ploetz, 2005b) and they are the only isolates corresponding to the two vegetative compatibility groups VCGs and (Pegg et al., 1994). The F. oxysporum f.sp. cubense isolates belonging to these two VCGs, and identified as race T4, have been shown to be highly genetically related among them and genetically distinguishable from the other VCGs of F. oxysporum f. sp. cubense (Bentley et al., 1998) Probability of transfer to a suitable host The probability of transfer of F. oxysporum f.sp. cubense races 4 and T4 from infected plant propagation material to a suitable host in the PRA area would be high, as these races, besides the susceptible Cavendish cultivars grown in the French overseas departments, can attack a wide range of cultivars. In agreement with the document, the pathogen would be able to spread from infected plants to neighbouring healthy hosts by contaminated soil adherent to shoes, farm machinery etc., or by surface water running through infested soil. The probability of transfer of F. oxysporum f.sp. cubense races 4 and T4 to a suitable host with contaminated soil would be high, considering the long survival of the pathogen as chlamydospores (Stover, 1962). Based on the above, the Panel concludes that the probability of transfer of F. oxysporum f.sp. cubense races 4 and T4 to a suitable host plant would be high Conclusion of entry In agreement with the document, the Panel considers that the probability of entry of F. oxysporum f.sp. cubense races 4 and T4 into the PRA area on conventional planting material, from countries where the disease is present, would be high if present import restrictions were rescinded Probability of establishment Availability of suitable hosts, alternate hosts and vectors in the PRA area The pest risk assessment clearly shows the importance of the Cavendish sub-group, which is susceptible to F. oxysporum f.sp. cubense races 4 and T4, in Guadeloupe and Martinique. It also mentions that Cavendish cultivars are grown on Réunion, but there is no information on the importance of the Cavendish sub-group in French Guiana. The Panel observed that it should have been emphasised here that F. oxysporum f.sp. cubense strains of races 4 and T4 can attack a wide range of cultivars including those susceptible to races 1 and 2, thus increasing the potential for economic loss amongst smallholders. The Panel confirmed the information included in the French document that host plants of F. oxysporum f.sp. cubense races 4 and T4 are widely distributed in plantations, smallholdings and private gardens in the PRA area. In 2006, dessert bananas of the Cavendish sub-group were produced commercially on 7300 ha in Martinique (Agreste, 2007a) and on 2240 ha in Guadeloupe (Agreste, 2007b). In the same year, in Réunion 500 ha were cultivated with bananas (Agreste, 2007c). Data from 2005 show 355 ha of bananas in French Guiana (INSEE 2007). Dessert banana, plantain and other cooking bananas are grown in the French overseas departements for household consumption in family gardens. The importance of this production is underpinned by food consumption data for Guadeloupe and Martinique (AFSSA, 2007). In 2006 family gardens occupy 1080 ha in Martinique, 615 ha in Guadeloupe and 2890 ha in The EFSA Journal (2008) 668, 13-22

14 Réunion (Agreste, 2007a, b and c). In French Guiana, banana and plantain are among the associated crops of the shifting cultivation, which is practiced on 33 % of the total utilised agricultural area (PDR Guyane, 2007). Since the French document was issued, four weed species have been reported as additional hosts of F. oxysporum f.sp. cubense race T4 (Hennessy et al., 2005). Of these, Chloris inflata (syn. C. barbata), Euphorbia heterophylla and Tridax procumbens are reported to be present in French Guiana, Guadeloupe and Réunion (Fournet, 2002; Cons. Bot. Nat. de Mascaren, 2007; Hoff et al., 2007) Suitability of environment The Panel observes that more information on the climates of the PRA area, compared to climates where F. oxysporum f.sp. cubense races 4 and T4 occur, would have enabled a more accurate assessment of environmental conditions suitable for the establishment of these races. Even though F. oxysporum f.sp. cubense races 4 and T4 are distinguished by their ability to attack Cavendish subgroup in sub-tropical and tropical climates (Ploetz et al., 1990; Bentley et al., 1998), the Panel found that the impact of climate and edaphic condition on F. oxysporum f.sp. cubense races 4 and T4 pathogenicity expression was not sufficiently explained in Part 1 of the French document. The French document states that any plant material infected with F. oxysporum f.sp. cubense T4 is very likely to lead to the establishment of a pest population, while a plant infected with race 4 is moderately unlikely to lead to the establishment of a pest population, as it needs to be in one of the geographical areas with suitable climatic conditions. The Panel agrees with the high rating assigned for F. oxysporum f.sp. cubense race T4. However, the rating of moderately unlikely assigned to F. oxysporum f.sp. cubense race 4 is not supported by evidence in the document. The areas characterised by subtropical climatic conditions, suitable for F. oxysporum f.sp. cubense race 4 establishment, should have been more clearly defined in the document Cultural practices and control measures The Panel agrees with the document that chemical control is not effective in controlling F. oxysporum f.sp. cubense and that the control of the Panama disease relies on cultivar resistance and pathogen-free plant propagation material. Studies on genetic improvement of Musa spp., using conventional and non-conventional breeding tools available at the time of the original assessment (Hwang, and Tang, 2000; Mandal et al., 2001; Escalant et al., 2002; Jain and Swennen, 2004) were not considered in Part 1 of the French document. The Panel observes that, recently, Cavendish cultivars with resistance to Fusarium wilt have been developed by somaclonal variation. The resistant somaclonal variant Formosana has been propagated for commercial planting in Taiwan since 2002 (Hwang and Ko, 2004). This demonstrates the feasibility of using tissue culture to generate variation for selection of commercially acceptable resistant cultivars of Cavendish (Smith et al., 2006). No information is provided in the document on the current banana cropping systems in the French overseas department. Other characteristics of the pest affecting the probability of establishment The Panel agrees with the document that the pathogen can survive for several years in soil in absence of hosts. Moreover weeds, which are known to harbour the pathogen in Australia The EFSA Journal (2008) 668, 14-22

15 (Hennessy et al., 2005), are also reported as present at least in three French overseas departments (Fournet, 2002; Cons. Bot. Nat. de Mascaren, 2007; Hoff et al., 2007) Conclusion of the probability of establishment The Panel considers that the probability of F. oxysporum f.sp. cubense race T4 establishing in the PRA area would be high rather than moderate, as most of the PRA area is characterised by tropical climates, where F. oxysporum f.sp. cubense T4 strains are pathogenic, and susceptible banana cultivars are grown. The Panel agrees with the estimate of low assigned to the probability of establishment of F. oxysporum f.sp. cubense race 4, except for those part of the PRA area with subtropical climate, where the probability for establishment of race 4 would be high. A climate matching model would have been useful to define the parts of the PRA area suitable for F. oxysporum f.sp. cubense race Probability of spread after establishment The assessor considers the spread through natural means to be slow, but the spread by human assistance to be rapid. The possibility of containment is considered to be unlikely. The Panel agrees with this assessment, although natural spread in individual plantations could be more rapid following heavy rains. The assessor refers to infected planting material and contaminated waste as a main means of spread by human assistance but fails to mention the possibility of spread in contaminated soil on farm machinery or footwear Conclusion on probability of introduction and spread In agreement with the document, the probability of entry of F. oxysporum f.sp. cubense races 4 and T4 into the PRA area on conventional planting material, from countries where the disease is present, would be high if present import restrictions were rescinded. In agreement with the document, the probability of establishment for F. oxysporum f.sp. cubense race 4, which attacks Cavendish cultivars in the subtropics, would be low, except for those part of the PRA area with subtropical climate, where the probability for establishment of race 4 would be high. The probability of establishment for F. oxysporum f.sp. cubense race T4, which is able to attack Cavendish cultivars in the tropics, would be high rather than moderate, as most of the PRA area has a tropical climate and no commercial Cavendish cultivars resistant to race T4 have yet been developed or tested in the French overseas departments. The Panel agrees that the spread through natural means would be slow, but the spread by human assistance would be rapid Assessment of potential economic consequences Direct pest effects Crop quality and/or yield losses F. oxysporum. f. sp. cubense is a soil-borne fungus which is responsible for Fusarium wilt of banana, one of the most destructive disease affecting bananas world-wide. A relatively large share of the agricultural area of Guadeloupe and Martinique is devoted to banana production and a relatively small share in French Guiana and Réunion (see section 2.1). The EFSA Journal (2008) 668, 15-22

16 The Panel agrees with the document on the high potential impact of F. oxysporum f. sp. cubense races 4 and T4 on banana crops in the French overseas departments. Examples of recent outbreaks of races 4 and T4 would have better supported the conclusion in the document. In Taiwan, Fusarium wilt resulted in a ten fold decrease in the area grown with Cavendish banana between 1967 and 1990 (Hwang and Ko, 2004) Control measures, efficacy and costs The Panel agrees with the document that chemical control is not effective in controlling F. oxysporum f.sp. cubense and that the control of Fusarium wilt relies essentially on cultivar resistance and pathogen-free plant propagation material. The Panel agrees with the documents on the high costs required by the breeding programs for developing new commercial Cavendish cultivars resistant to race 4 and T4. In fact, considering the effect of environmental condition on disease expression and the genetic variability of F. oxysporum f. sp. cubense, even resistant varieties developed elsewhere need to be carefully tested in local conditions and with local strains of the pathogen (Koenig et al., 1997; Bentley et al., 1998). In Taiwan, it took almost 20 years to develop a new commercially acceptable resistant Cavendish cultivar (Hwang and Ko, 2004) Indirect pest effects Export markets Martinique exported a net total of 228,358 tonnes ( 178 mln euros) 7 of bananas in 2005, representing 93% of local production (Aumand, 2006). In 2004, 251,695 tonnes of bananas were exported, representing 89% of the total production of banana varieties intended for export (Agreste, 2006a). In Guadeloupe, the export of bananas was 65,730 tonnes in 2004 and 51,700 tonnes ( 37 mln euros) 7 in 2005, i.e. respectively 75% and 80% of the total production of banana varieties intended for export (Agreste, 2006b). In French Guiana and Réunion, banana production is for local consumption only (DAF Guyane, 2001; Le Jeannic, 2002). Banana production of Guadeloupe and Martinique is mainly exported, with the EU being the primary trading partner (Lassoudière, 2007). Under the current EU regulations (Directive 2000/29/EC), the introduction of F. oxysporum f.sp. cubense races 4 and T4 into the French overseas departments would not evoke quarantine restrictions to fruit trade. The Panel agrees with the French document that the introduction of F. oxysporum f.sp. cubense races 4 and T4 into Guadeloupe and Martinique would severely affect the quantity of bananas available for export, thus causing potential long-term loss of export markets Social consequences According to the document, the banana industry provides 7,000 direct jobs in Martinique and 10,000 direct and indirect jobs in Guadeloupe. The Panel considers that for Guadeloupe and Martinique, where dessert banana is widely grown for export, a decrease in the cultivation of banana as a result of the disease establishment could reduce employment possibilities for the local population. Plantain and cooking banana are important staple food and a large fraction is produced in gardens for family consumption (for Guadeloupe and Martinique see AFSSA, 2007). As banana production in smallholdings and family gardens would suffer from high yield losses, a 7 based on average prices at departure for the first semester 2005 (Agreste La statistique agricole. Le Bulletin. Séries chronologiques, 13, Guadeloupe, 1 er Semestre 2006, 4 pp.) The EFSA Journal (2008) 668, 16-22

17 potential disruption of subsistence production and consumption patterns could occur, causing negative social impacts. Similar social effects are possible also for shifting cultivation in French Guiana, where banana is one of the crops grown. There is uncertainty regarding the availability and the costs of substitution foods, should the yield of cooking banana and plantain be substantially reduced Environmental consequences Potential consequences associated with landscape changes due to a reduced presence of banana plants within commercial plantations and private gardens, after the establishment of Panama disease, have not been considered in the document. Alternatives to banana cultivation have not been identified and assessed Conclusion of the assessment of economic consequences The Panel concludes, in agreement with the document, that the potential economic impacts would be high. Plantations of dessert bananas for export and smallholdings and family gardens producing fruit for the local market or for home-consumption would suffer severe yield losses. Concerning social impacts, for Guadeloupe and Martinique there could be a reduction in employment in commercial plantations, whilst a potential disruption of subsistence production and consumption patterns could occur among smallholders and family gardens. There is uncertainty regarding the availability and the costs of substitution foods, should the yield of cooking banana and plantain be substantially reduced Comments on the conclusion of the pest risk assessment The general conclusion of the document is that Fusarium oxysporum f. sp. cubense (and more particularly races 4 and T4) must be included in the overseas departments lists of quarantine pests. However, as discussed in the pest categorisation section of this opinion, although Part 1, (pest identity) and Part 2 (conclusions) deal with F. oxysporum f. sp. cubense, the pest risk assessment focuses only on races 4 and T4, generating confusion on the subject of the assessment. Considering that races 1 and 2 are present and not reported as having a limited distribution and/or being under official control, the Panel opinion is that only the F. oxysporum f.sp. cubense races 4 and T4 fulfil the criteria for a quarantine pest and are appropriate for stage 3 of Pest Risk Analysis, i.e. the evaluation of pest risk management options for the 4 French overseas departments Degree of uncertainty Uncertainties are not addressed in the document. There is uncertainty regarding the availability and the costs of substitution foods, should the yield of cooking banana and plantain be substantially reduced. CONCLUSIONS AND RECOMMENDATIONS Following a detailed analysis of the material provided in the pest risk assessment made by France in July 2003 on F. oxysporum f. sp. cubense, which is considered by France as potentially harmful for the French overseas departments of French Guiana, Guadeloupe, The EFSA Journal (2008) 668, 17-22