The EFSA Journal (2008) 703, 1-21

Pest risk assessment made by France on Ceratocystis fimbriata 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-2006-091)

Adopted by written procedure on 30 April 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 pres 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 simplified 2 pest risk assessment conducted by France on Ceratocystis fimbriata Ellis & Halsted responsible for Ceratocystis canker of citrus with French Guiana, Guadeloupe, Martinique and Réunion considered as endangered area. C. fimbriata causes a very serious disease on many host plants. On citrus, it is reported in Colombia and Cuba to cause canker, dieback and wilt. The disease is systemic and can lead to the death of the plant. 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

1

2

For citation purposes: Scientific Opinion of the Panel on Plant Heath on a request from the European Commission on Pest risk assessment made by France on Ceratocystis fimbriata considered by France as harmful in French overseas departments of Guadeloupe, Martinique, French Guiana and Réunion. The EFSA Journal (2008) 703, 1-21 A simplified pest risk assessment contains in a “synthetic fiche” the information available allowing according to the risk assessor the assessment of the risk associated with the relevant organism (see the Terms of reference).

© European Food Safety Authority, 2008

Pest risk assessment made by France on Ceratocystis fimbriata

ISPM No. 11 3 : 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 Panel observes that statements in the document are not individually referenced. Some statements are not supported by data. This is particularly noted in relation to economic impact of the introduction of the pathogen. The document could not consider the recent literature published after 2003 on taxonomy of Ceratocystis spp. The Panel concludes that: •

The Panel agrees with the identification of the wood pathway, considering that the pathogen could transfer to a suitable host through infected host debris (e.g. sawdust) and by the help of insect vectors. The Panel considers that the probability of entry through host plants and vegetative propagation material would be moderate to high. The Panel notes that the highest risk for the citrus industry of the French overseas departments would be associated with the trade of host plants and vegetative propagation material or accompanying soil from areas where C. fimbriata is reported to cause disease on citrus (Colombia, Cuba). Main host crops of C. fimbriata in Colombia are citrus, coffee and cacao. The isolates pathogenic to cacao are now referred to the recently described species Ceratocystis cacaofunesta. In Cuba the reported hosts are citrus, coffee, taro and the naturalized ornamental tree Spathodea campanulata. The Panel also considers passenger traffic as an entry pathway.

•

The Panel, after taking into account the information provided in the document and additional consulted, concludes that the probability of establishment, once the pathogen enters the PRA area 4 , would be high.

•

The Panel agrees with the document that cultural practices may lead to a rapid spread after establishment.

•

The Panel agrees that the impact on citrus would be severe and considers that the disease could also affect coffee and perhaps other tree species.

•

The level of uncertainty is high for the following aspects: lack of studies on pathogenicity to citrus of isolates from other host plants and other regions; limited data published on yield losses; the level of economic and social consequences would depend on the range of affected host plants.

In agreement with the document, the Panel concludes that C. fimbriata is 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:

Ceratocystis fimbriata, French overseas departments, pest risk assessment, Réunion

3

ISPM International Standard for Phytosanitary Measures. ISPM No. 11: Pest risk analysis for quarantine pests, including analysis of environmental risks and living modified organisms. 4 PRA area is the area in relation to which a Pest Risk Analysis is conducted [FAO, 2007].

The EFSA Journal (2008) 703, 2-21

Pest risk assessment made by France on Ceratocystis fimbriata

TABLE OF CONTENTS Panel Members............................................................................................................................................1 Summary .....................................................................................................................................................1 Table of Contents ........................................................................................................................................3 Background as provided by the European Commission .............................................................................4 Terms of reference as provided by the European Commission...................................................................5 Acknowledgements .....................................................................................................................................5 Assessment ..................................................................................................................................................6 1. Introduction ........................................................................................................................................6 1.1. General introduction to Ceratocystis fimbriata .........................................................................6 1.2. The document under scrutiny.....................................................................................................7 1.3. Evaluation procedure .................................................................................................................7 1.4. General comments on the document..........................................................................................7 2. Evaluation of the pest risk assessment................................................................................................7 2.1. Pest categorization .....................................................................................................................7 2.1.1. Identity of pest.......................................................................................................................7 2.1.2. Presence or absence in PRA area...........................................................................................8 2.1.3. Regulatory status ...................................................................................................................8 2.1.4. Potential for establishment and spread in PRA area..............................................................8 2.1.5. Potential for economic consequences in PRA area ...............................................................8 2.1.6. Conclusion of pest categorization..........................................................................................8 2.2. Assessment of the probability of introduction and spread.........................................................8 2.2.1. Probability of entry of the pest ..............................................................................................8 2.2.1.1. Identification of pathways ............................................................................................8 2.2.1.2. Probability of the pest being associated with the pathway at origin...........................10 2.2.1.3. Probability of survival during transport or storage .....................................................11 2.2.1.4. Probability of pest surviving existing pest management procedures ..........................11 2.2.1.5. Probability of transfer to a suitable host .....................................................................11 2.2.1.6. Conclusion on the probability of entry .......................................................................12 2.2.2. Probability of establishment ................................................................................................12 2.2.2.1. Availability of suitable hosts, alternate hosts and vectors in the PRA area................12 2.2.2.2. Suitability of environment ..........................................................................................13 2.2.2.3. Cultural practices and control measures .....................................................................13 2.2.2.4. Other characteristics of the pest affecting the probability of establishment ...............14 2.2.2.5. Conclusion on the probability of establishment..........................................................14 2.2.3. Probability of spread after establishment ............................................................................14 2.2.4. Conclusion on probability of introduction and spread ........................................................14 2.3. Assessment of potential economic consequences ....................................................................15 2.3.1. Direct pest effects ................................................................................................................15 2.3.1.1. Crop quality and/or yield losses..................................................................................15 2.3.1.2. Control measures, efficacy and costs..........................................................................15 2.3.2. Indirect pest effects..............................................................................................................15 2.3.2.1. Loss of export markets................................................................................................15 2.3.2.2. Social consequences ...................................................................................................16 2.3.2.3. Environmental consequences......................................................................................16 2.3.3. Conclusion of the assessment of economic consequences ..................................................16 2.4. Comments on the conclusion of the pest risk assessment........................................................16 2.4.1. Degree of uncertainty ..........................................................................................................16 Conclusions and Recommendations..........................................................................................................17 Documentation provided to EFSA ............................................................................................................17 References .................................................................................................................................................18

The EFSA Journal (2008) 703, 3-21

Pest risk assessment made by France on Ceratocystis fimbriata

BACKGROUND AS PROVIDED BY THE EUROPEAN COMMISSION 5 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, l0.7.2000, p. l), as last amended by Commission Directive 2006/35/EC (OJ L88, 25.3.2006, 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 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 pest risk assessments 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 pest risk assessments among the 130 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 pest risk assessment have been made: a full pest risk assessment for harmful organisms for which the probability of introduction into the French overseas departments is high with economic important crops and a simplified pest risk assessment for organisms for which the probability of introduction is extremely low. 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, 281-305). 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 pest risk assessment (EPPO Bulletin 23, 191-198). The guidelines are based on many years experience of EPPO experts in the EPPO Panel on pest risk assessment and the EPPO Panel on phytosanitary measures. They conform with the International Standards on Phytosanitary Measures ISPM No. 11 (Guidelines for quarantine pests) and use the terms of ISPM No 5 (Glossary of phytosanitary terms). The simplified pest risk assessment contains in a “synthetic fiche” the information available allowing the assessment of the risk associated with the relevant organism. 5

Submitted by the European Commission, ref. SANCO E/1/VE/svi D(2006)510488

The EFSA Journal (2008) 703, 4-21

Pest risk assessment made by France on Ceratocystis fimbriata

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 pest risk assessments made by France on organisms which are considered by France as harmful in 4 French overseas departments, i.e. Guadeloupe, French Guiana, Martinique and Reunion, 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, Thomas C. Harrington, David Jones, David Makowski, Luisa Manici, Angelo Porta Puglia, Robert Steffek, Anita Strömberg, and Irene Vloutoglou.

The EFSA Journal (2008) 703, 5-21

Pest risk assessment made by France on Ceratocystis fimbriata

ASSESSMENT

1.

Introduction

This document presents the opinion of the Panel on Plant Health on the pest risk assessment conducted by France on Ceratocystis fimbriata Ellis & Halsted with French Guiana, Guadeloupe, Martinique and Réunion considered as endangered areas. 1.1.

General introduction to Ceratocystis fimbriata

Ceratocystis fimbriata can cause serious disease on many host plants. Ceratocystis fimbriata in different parts of the world (CABI, 2007). There are several apparently host-specialized strains that are sometimes called ‘types’, ‘races’ or ‘forms’ (Baker et al., 2003; Harrington, 2000; Wellman, 1972), and many of these have proven or may prove to be distinct species. Webster and Butler (1967) considered such types as members of a single, highly variable species. However, isolates from some hosts and some regions are genetically unique (Baker et al., 2003; Barnes et al., 2001; Johnson et al., 2002; Marín et al., 2003; Santini and Capretti, 2000). The pathogen attacking Platanus spp. formerly designated as a separate form, C. fimbriata f. platani, based on its host specificity (Walter et al., 1952), has been raised from a form to species, Ceratocystis platani (Baker Engelbrecht and Harrington, 2005). Similarly, a new species Ceratocystis cacaofunesta has been described, which includes former C. fimbriata isolates from cacao from Ecuador, Brazil, Colombia and Costa Rica (Baker Engelbrecht and Harrington, 2005). Another form, occurring on Acacia mearnsii and species of Protea in South Africa, is now considered a separate species, Ceratocystis albofundus (Wingfield et al., 1996); Ceratocystis variospora found on Quercus (Davidson, 1944), is similar to C. fimbriata (Hunt, 1956) and, although previously considered by Upadhyay (1981) a synonym of C. fimbriata, is confirmed as a separate species (Johnson et al., 2005). It appears therefore that the species C. fimbriata in the broad sense is a complex of many species, each with a distinct host range and geographic distribution (CABI, 2007). Harrington (2000) proposed that the cryptic species within the C. fimbriata complex fall into three broad geographic clades, the North American, the Latin American and the Asian clades. Both rDNA and allozyme analyses support these three major clades (Baker et al., 2003; Harrington, 2000; Johnson et al., 2005). The few reports of C. fimbriata on citrus are from the Caribbean region, where the Latin American clade appears to be indigenous (Baker et al., 2003; Baker Engelbrecht et al., 2005). The disease on citrus is particularly severe in Colombia, and isolates from citrus and coffee there were confirmed to belong in the Latin American clade (Baker et al., 2003; Marín et al., 2003). The disease on citrus was reported in 1994 in Colombia, threatening citrus production in the Colombian coffee growing areas of the country. The damage was most serious on cv. Tahiti lime and on orange trees causing wilt/dieback and canker, spreading in the sapwood centrifugally in a black “flame” shape that may be visible on trunk surface and in tree cross sections (Mourichon, 1994). The disease features internal discoloration of the woody tissues of the trunk or main branches or throughout most of the tree. The dark discoloration of the xylem often spreads from the base of the trunk to the top of the tree. The first disease symptoms (leaf wilt) often correspond to widespread underlying internal discoloration and cankers on the branches and main stem. The disease is systemic and can lead to the death of the plant (CABI, 2007). In Cuba a severe outbreak of C. fimbriata causing wilting of Mexican lime (Citrus aurantifolia) was observed in 1972 in the Banes region of the Oriente province, (Rodriguez and Alfonso, 1978), but the Panel could not find any report on the success of the subsequent eradication program and on the current state of the disease caused by C. fimbriata on citrus in The EFSA Journal (2008) 703, 6-21

Pest risk assessment made by France on Ceratocystis fimbriata

Cuba. There is one unconfirmed report from Argentina on the occurrence of the disease on lemon trees (De Alcain and Marmelicz, 1984). The pathogen C. fimbriata can be easily isolated by cultural methods from the infected plant parts and identified as C. fimbriata in the broad sense based on morphology (Moller and DeVay, 1968; Rayner, 1970). In planta molecular or serological diagnostic techniques have not been developed, but there are DNA sequences of ITS-rDNA and other genes unique to C. fimbriata, and these could be developed for diagnosis (CABI, 2007, Harrington et al., 2001; Witthuhn et al., 2000). 1.2.

The document under scrutiny

The assessment of risks of the organism is presented by the French risk assessors in a so-called simplified pest risk assessment, which contains in a “synthetic fiche” the information available allowing according to the risk assessor the assessment of the risk associated with the relevant organism. The simplified pest risk assessment follows the principal sections of ISPM No. 11 but also contains descriptive sections, e.g. geographical distribution, host plants and description of damage. Based on this document France requested C. fimbriata be added to the list of harmful organisms in Directive 2000/29/EC. 1.3.

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 evaluation of the French document was conducted on the basis of an English translation from an original submission in French, which remains the reference document. 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 pest risk assessment, this has been noted. 1.4.

General comments on the document

The document comprises 4 pages and includes a list of 9 references in bibliography, but statements made in the document are not individually referenced. Many issues have not been dealt with in detail, despite the availability of relevant information at the time of conducting the original assessment. The document was compiled in July 2003 and therefore required updating. Since then, the knowledge on taxonomy, host range and geographic distribution of C. fimbriata has changed substantially. 2.

Evaluation of the pest risk assessment

2.1.

Pest categorization

2.1.1.

Identity of pest

The document identifies the pest as the species Ceratocystis fimbriata Ellis & Halsted. The common name of the disease cited in the document is Ceratocystis canker of citrus. The Panel agrees that the identity of the pathogen should be Ceratocystis fimbriata Ellis & Halsted. The EFSA Journal (2008) 703, 7-21

Pest risk assessment made by France on Ceratocystis fimbriata

The taxonomical position of the pathogen is: Fungi, Ascomycota, Sordariomycetes, Hypocreomycetidae, Microascales, Ceratocystidaceae, Ceratocystis. Anamorph: Thielaviopsis (Paulin-Mahady et al., 2002). It is a member of the Latin American clade of the C. fimbriata complex (Baker et al., 2003; Harrington, 2000; Johnson et al., 2002). C. fimbriata has a wide range of hosts. Reports on Citrus spp. at the moment are only confirmed from Colombia (Capera-Borja et al., 1995a and b; Mourichon, 1994) and Cuba (Rodriguez and Alfonso, 1978). The Colombian isolates from citrus are genetically related to the coffee isolates from Colombia (Barnes et al., 2001, Marín et al., 2003). 2.1.2.

Presence or absence in PRA area

C. fimbriata is not known to be present in the PRA area. 2.1.3.

Regulatory status

C. fimbriata is not regulated in the PRA area and in the European Union. The EU directive 2000/29/EC only regulates C. fimbriata f. platani on plane trees (now C. platani). 2.1.4.

Potential for establishment and spread in PRA area

C. fimbriata is established in areas with a wide range of climatic conditions (CABI, 2007). Host plants (citrus, coffee, etc.) are grown in all the French overseas departments and the pathogen can spread by human activities and insect vectors. Therefore, C. fimbriata has the potential for establishment and spread in the PRA area. 2.1.5.

Potential for economic consequences in PRA area

C. fimbriata causes serious dieback disease of citrus in Colombia. According to Mourichon (1994), 10% of citrus crops in Colombia are affected. The pathogen is also found in Colombia on coffee – its severity and incidence has increased significantly in recent years, resulting in substantial losses for resource-poor farmers (Marín et al., 2003). The Cuban outbreak of C. fimbriata in citrus orchards of the Oriente province in the 70’s was described as severe (Rodriguez and Alfonso, 1978), but data on current incidence were not found. C. fimbriata therefore has a potential for economic consequences in the PRA area. 2.1.6.

Conclusion of pest categorization

C. fimbriata is not present in the PRA area and has a potential for establishment, spread and economic consequences in the PRA area. 2.2.

Assessment of the probability of introduction and spread

2.2.1.

Probability of entry of the pest

2.2.1.1.

Identification of pathways

The document identifies as pathways wood samples or contaminated earth particles and considers that, as there is no information on the existence of citrus-specific forms, attention should be paid to all the susceptible hosts of C. fimbriata, mentioning twenty different species or genera.

The EFSA Journal (2008) 703, 8-21

Pest risk assessment made by France on Ceratocystis fimbriata

The Panel notes that some of the listed species are no longer considered to be hosts of C. fimbriata but are hosts of newly described or recognized species of Ceratocystis [Platanus acerifolia, Platanus orientalis, Platanus occidentalis and Platanus racemosa are hosts of C. platani (Baker Engelbrecht and Harrington, 2005); Theobroma cacao is host of C. cacaofunesta (Baker Engelbrecht and Harrington, 2005); Acacia mearnsii is host of C. albofundus; Populus is host of C. populicola (Johnson et al., 2005)]. Current recognised host families and host genera of C. fimbriata are (CABI, 2007; Harrington, 2000): Anacardiaceae (Mangifera); Annonaceae (Annona); Apiaceace (Daucus); Araceae (Alocasia, Colocasia, Syngonium, Xanthosoma); Bignoniaceae (Spathodea); Brassicaceae (Mancoa); Caesalpiniaceae (Cassia); Convolvulaceae (Ipomoea); Euphorbiaceae (Hevea, Manihot); Fabaceae (Crotalaria, Erythrina); Fagaceae (Fagus); Mimosaceae (Acacia, Inga); Moraceae (Ficus); Myrtaceae (Eucalyptus, Pimenta); Punicaceae (Punica); Rubiaceae (Coffea); Rutaceae (Citrus); Sterculiaceae (Herrania, Theobroma); Verbenaceae (Gmelina). Limited evidence is currently available on the host specificity of the citrus isolates of C. fimbriata. In the geographical areas where the citrus isolates are reported, i.e. Colombia and Cuba, the reported host genera of C. fimbriata are respectively Citrus, Coffea, Theobroma and Inga (CABI, 2007), and Citrus, Coffea, Colocasia and Spathodea (CABI, 2007; Prieto et al., 1981). The Colombian coffee and citrus isolates of C fimbriata are genetically closely related (Barnes et al., 2001; Marín et al., 2003) and Colombian isolates from coffee and cacao have been shown to be pathogenic to citrus (Marín et al., 2006), C. fimbriata is not reported on citrus from other citrus producing countries, where C. fimbriata is present. There is only one unconfirmed report from Argentina on the occurrence of the disease on lemon trees (De Alcain and Marmelicz, 1984). Therefore, the Panel considers that the risk for the citrus production of the French overseas departments is mainly associated with the reported hosts of C. fimbriata from Colombia and Cuba. The Panel agrees with the document that the movement of infected wood and of contaminated soil are potential pathways for the entry of C. fimbriata into the PRA area. Wood packaging material was also considered to be the entry pathway for the species C. platani into Italy during the second world war (Panconesi, 1981). Therefore, there is a possibility that C. fimbriata could be introduced into the PRA area on logs, wood chips and lumber of susceptible hosts (CABI, 2007). The soil pathway is currently blocked as import of soil is banned for both the French overseas departments (JORF, 1992) and the EU (Council Directive 2000/29/EC). However, if the current regulations are lifted, soil could represent a potential pathway for the entry of the pathogen into the PRA area. The Panel considers that, since the document was issued, it has become more widely recognized that vegetative plant propagation material is a primary pathway for the introduction of C. fimbriata into new areas. This is especially true of members of the Latin American clade of the complex, i.e., C. fimbriata, C. platani and C. cacaofunesta. Because there may be extensive mycelial growth within a plant before symptoms appear, propagative cuttings may be an effective pathway of dispersal. Infected Syngonium cuttings were the apparent means of spread of the Syngonium form of the fungus throughout the greenhouse industry (Thorpe et al., 2005; Walker et al., 1988). C. fimbriata has also been found in both symptomatic and apparently healthy eucalyptus cuttings in a Brazilian eucalyptus plantation (Harrington, 2000). Cuttings, roots and corms are used to propagate many other common hosts of C. fimbriata, including Theobroma, Ipomoea and Colocasia, and this may facilitate long-distance transport of the fungus. The Ipomoea form of the fungus, which is probably native to Latin America, is likely spread on storage roots (Baker et al., 2003). It has been assumed that strains of C. fimbriata from Brazil were introduced to Oman and Pakistan on infected mango plants or soil accompanying the plants and the disease is causing serious losses in these countries (van Wyk The EFSA Journal (2008) 703, 9-21

Pest risk assessment made by France on Ceratocystis fimbriata

et al., 2007). The recent introduction of C. platani to Greece may have been in infected nursery stock of London plane (Ocasio et al., 2007). C. cacaofunesta is thought to have been introduced through plant propagation material into several research stations in Central and South America (Engelbrecht et al., 2007). Thorpe et al. (2005) suggested that dispersal by humans of host specialized populations of C. fimbriata from Araceae is likely to have occurred on cuttings or corms. C. populicola was likely introduced into Poland in the late 1970s in planting stock of Populus spp. (Johnson et al., 2005). There is no record of spread of C. fimbriata associated with seed (CABI, 2007). The Panel considers that the citrus plant propagation material pathway is currently blocked for the French overseas departments (JORF, 1992) and the EU Council Directive 2000/29/EC in Annex III forbids introduction of “plants of Citrus L., Fortunella Swingle, Poncirus Raf. and other hybrids, other than fruits and seeds”. However there is no ban on plant propagation material of other hosts of C. fimbriata. The Panel considers that the movement of fruit is not a pathway of entry, as the pathogen does not infect the fruit, although it may be present in the peduncles. However, Council Directive 2000/29/EC in Annex IV has a general regulation that fruit of Citrus L., Fortunella Swingle, Poncirus Raf. and their hybrids originating from third countries should be free of peduncles and leaves. The document mentions that the pathogen may spread by insects and by movement of infected host debris. The primary insect vectors are fungal-feeding insects (Nitidulidae, Coleoptera) that are not associated with particular plants (Thorpe et al., 2005). Ambrosia beetles such as Xyleborus and Hypocryphalus species may facilitate the dispersal of the fungus by tunnelling through infested wood and expelling frass with fungal spores (CABI, 2007; Isla and Ravelo, 1989). Ascopores are probably spread naturally by insects and are not likely airborne. Airborne disperal of conidia is also not likely, except in insect frass (Iton, 1960, Ocasio et al., 2007). Rainsplash dispersal of conidia has not been documented (CABI, 2007). The pathogen is also transmitted through various kinds of infected host debris. Infected insect frass and sawdust can be spread by wind, rain or running water (CABI, 2007). The document does not mention the passenger traffic as an entry pathway. The Panel is of the opinion that passenger traffic should have been considered by the assessors. According to the document, Guadeloupe and Martinique call for particular attention owing to the proximity of citrus-growing areas in which the disease has been reported (Cuba). The Panel notes that similar attention might apply to the citrus crops in French Guiana, as the disease has been reported on citrus in Colombia. The Panel considers that the citrus orchards of Réunion are not likely to be threatened by natural spread of citrus infecting strains of the pathogen, due to geographical isolation. All the French overseas departments can be threatened by introduction of the pathogen by human activities (e.g. movement of infected host plant propagation material, logs, lumber, etc). 2.2.1.2.

Probability of the pest being associated with the pathway at origin

C. fimbriata has a very large host range (CABI, 2007) (see section 1.1. and 2.2.1.1.). However, C. fimbriata has been confirmed on citrus only in Colombia and Cuba, therefore the probability of association of C. fimbriata pathogenic to citrus is higher with pathways originating from these countries.

The EFSA Journal (2008) 703, 10-21

Pest risk assessment made by France on Ceratocystis fimbriata

C. fimbriata has been reported to severely attack citrus in Colombia (Mourichon, 1994). An other important host of C. fimbriata in Colombia is coffee (Marín et al., 2003). Although C. fimbriata has been isolated from cacao wounds, Baker Engelbrecht and Harrington (2005) attributed the disease on cacao, known as ‘mal de machete’ (Engelbrecht et al., 2007), to the new species C. cacaofunesta. Other hosts of C. fimbriata in Colombia include species of the genus Inga of the Mimosaceae family (CABI, 2007; Marín Montoya and Wingfield, 2006). C. fimbriata causes one of the most important diseases of coffee in Colombia (Marín et al., 2003). The Colombian isolates from citrus are genetically related to the coffee isolates (Barnes et al., 2001). Marín et al. (2006) reported that pathogenicity tests on coffee, cacao and citrus plants, using isolates from these hosts, showed that they could infect and cause disease on all three hosts inoculated, without indication of host specialization amongst the isolates tested. C. fimbriata has been described in Cuba on citrus, coffee, taro (Colocasia esculenta) and the ornamental tree Spathodea campanulata (Isla and Ravelo, 1989; Prieto et al., 1981; Rodriguez and Alfonso, 1975; Thorpe et al., 2005; Triana and Diaz, 1989), but the Panel could not find any information regarding the host specificity of these isolates. Epidemics on citrus were reported by Rodriguez and Alfonso (1978), but the Panel could not find any report on the current status of the disease caused by C. fimbriata on citrus in Cuba. The Panel considers that there is high probability of C. fimbriata pathogenic to citrus being associated with plants and vegetative plant propagation material of reported hosts from Colombia and Cuba. 2.2.1.3.

Probability of survival during transport or storage

The fungus survives and continuously grows on plant propagation material during transit. In wood and in soil, C. fimbriata produces aleurioconidia (chlamydospores) that can survive long periods (CABI, 2007). The probability of survival during transport and storage is therefore high. 2.2.1.4.

Probability of pest surviving existing pest management procedures

Asymptomatic infected vegetative plant propagation material could go undetected at visual inspections. Soil accompanying plants may also harbour the fungus and therefore go undetected at border inspection. The pathways of citrus plant propagation material and soil are currently blocked because of existing prohibitions on the importation both for the French overseas departments and the EU (see section 2.2.1.2.). The wood treatments are indicated in the Council Directive 2000/29/EC and more detailed in ISPM No. 15 IPPC Standard (heat treatment 56°C for 30 minutes, kiln-drying below 20% moisture content, de-barking, fumigation by methyl bromide at different temperatures, by phosphine, sulphuryl fluorid, carbonyl sulphide, chemical pressure impregnation, different irradiation methods and controlled atmosphere) in the case of import of wood material into EU Member States from third countries (FAO, 2007c). There is no information on the survival of chlamydospores of C. fimbriata in wood (logs, lumbers, etc) and wood packaging material that have been subjected to these treatments. 2.2.1.5.

Probability of transfer to a suitable host

Infected plant propagation material or soil would likely transfer the pathogen to the vicinity of a suitable host. The EFSA Journal (2008) 703, 11-21

Pest risk assessment made by France on Ceratocystis fimbriata

The pathogen could also be transferred from wood or wood packaging material to a suitable host in insect frass or sawdust or on cutting tools and other equipment (CABI, 2007). The primary vector insects (Nitidulidae, Coleoptera) are fungal feeding insects that are not associated with particular plants (Thorpe et al., 2005) and Ambrosia beetles, which facilitate the spread of the disease (CABI, 2007; Isla and Ravelo, 1989; Ocasio-Morales et al., 2007) are also present in the PRA area (Kairo et al., 2003) and they could therefore contribute to the transfer of the pathogen to a suitable host. 2.2.1.6.

Conclusion on the probability of entry

According to the French document, the probability of C. fimbriata entry on the citrus-growing pathway is low to moderate, but the polyphagous nature of the pathogen and the lack of information on any host specificity increases the risk of the pathogen’s entry into the PRA area. However, only chlamydospore-bearing wood samples or contaminated earth particles are considered as possible introduction pathways. The Panel agrees with the identification of the wood pathway, considering that the pathogen could transfer to a suitable host through infected host debris (e.g. sawdust) and by the help of insect vectors. However, the Panel considers that the probability of entry through host plants and vegetative propagation material would be moderate to high. The Panel notes that the highest risk for the citrus industry of the French overseas departments would be associated with the trade of host plants and vegetative propagation material or accompanying soil from areas where C. fimbriata is reported to cause disease on citrus (Colombia, Cuba). Main reported hosts of C. fimbriata in Colombia are citrus, coffee and cacao. The isolates pathogenic to cacao are now referred to the recently described species C. cacaofunesta. In Cuba the reported hosts are citrus, coffee, taro and the naturalized ornamental tree S. campanulata. The Panel also considers passenger traffic as an entry pathway. 2.2.2. 2.2.2.1.

Probability of establishment Availability of suitable hosts, alternate hosts and vectors in the PRA area

According to the document, orange trees and Tahiti limes as well as grapefruit grown in the relevant PRA area are highly susceptible, though there is inadequate information on levels of varietal susceptibility. The Panel found no literature reporting grapefruit (Citrus × paradisi) being susceptible to C. fimbriata. The disease was observed in Colombia on Tahiti limes (Citrus aurantifolia), tangelos (Citrus × tangelo), mandarines (C. reticulata) and sweet oranges (C. sinensis) (Capera-Borja et al., 1995 a and b; Mourichon, 1994) and in Cuba on Mexican lime (Citrus aurantifolia) (Rodriguez and Alfonso, 1978). According to a study performed in Colombia, species and varieties of citrus varied in susceptibility to a citrus strain of C. fimbriata (Paez Redondo and Castaño Zapata, 2001). Among rootstocks, only the white grapefruit (Toronja blanca) did not show any internal or external symptoms. The genotypes Swingle citrumelo (Citrus × paradisi Macf. × Poncirus trifoliata L. Raf.), Sunki × Jacobson and Sunki × English showed resistance, The most susceptible rootstocks were sweet orange, Rangpur lime (Citrus × limonia Osbeck), Cleopatra mandarin (Citrus reshini Hort. ex Tan.) and ‘Volkamer’ lemon (Citrus volkameriana Pasq.). Among the citrus varieties, only grapefruit (Toronja) Ruby red showed resistance. ‘Valencia’ orange, pajarito lime, Mexican lime, Oneco mandarin and Minneola tangelo were susceptible.

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Pest risk assessment made by France on Ceratocystis fimbriata

The Panel notes that Citrus species are grown in the whole PRA area. In Martinique, the citrus growing area has been estimated to be 327 ha with production of 1891 tonnes in 2006 (Agreste, 2007a). The main species is sweet orange accounting for 82% of the total area. A small area is devoted to grapefruit and pumelo (Citrus maxima) (11%) and lemon (Citrus limon) and limes (7%) (FAOSTAT, 2008 6 ). In Guadeloupe, the citrus growing area has been estimated to be 359 ha with a yearly production of 6225 tonnes. The main citrus species are sweet orange (100 ha), limes (140 ha), mandarin (60 ha) and grapefruit (50 ha) (Agreste, 2007b). In 2004, the area of citrus crop in French Guiana is reported as 1455 (INSEE, 2007). The main species are lemon and limes (Tahiti and Mexican lime) and sweet oranges, accounting for 44% and 42% of the total citrus area, respectively. A small area is devoted to tangerine, mandarin and clementine (11%), while grapefruit and pummelo only accounts for 3% of the total citrus production area (FAOSTAT, 2008). In Réunion, approximately 301 ha of citrus groves were cultivated in 2006 (Agreste, 2007c), with tangerine, mandarin and clementine grown on 50%, lemon and limes on 34% and sweet orange on 16% of the total citrus area (FAOSTAT, 2008). In 2006, family gardens occupied 1080 ha in Martinique (Agreste, 2007a), 615 ha in Guadeloupe (Agreste, 2007b) and 2890 ha in Réunion (Agreste, 2007c). These plots may also be planted with citrus along with other crops. No recent data were found on the area of family gardens in French Guiana. Among other hosts, coffee is grown in the French overseas departments. In Réunion, Coffea arabica var. Laurina, a local coffee variety Bourbon pointu is object of a vast experimental program 7 . Coffea liberica is sometimes cultivated in the south of the island (Verdcourt 1989). In Guadeloupe, in 2006, coffee is grown on 125 ha (Agreste, 2007b). Coffee is reported as present also in Martinique (Fournet, 2002) and French Guiana (Hoff et al., 2007). Host plants of the genus Inga (Mimosaceae) are present in natural vegetation or cultivated in all the French overseas departments (Cons. Bot. Nat. de Mascarn, 2007; Fournet, 2002; Hoff et al., 2007). Insect vectors are present in the PRA area (see section 2.2.1.5.). 2.2.2.2.

Suitability of environment

The document refers on the occurrence of the pathogen in Colombia and Cuba indicating that the environmental conditions in Cuba, where the disease is reported, are similar to those prevailing in Guadeloupe and Martinique. C. fimbriata already occurs in areas with a similar climate, such as Cuba and Colombia, and has become established in new areas with a wide range of climatic conditions (CABI, 2007). Therefore the Panel considers that the environmental conditions in the French overseas departments are suitable for the establishment of the pathogen. 2.2.2.3.

Cultural practices and control measures

Fungicides may be used to treat propagation material (Daines, 1971; Yang et al. 2000). However, only the use of pathogen-free vegetative plant propagation material can prevent the movement of the pathogen. Use of resistant rootstocks (grapefruit, Swingle citrumelo, Sunki × Jacobson and Sunki × English) may help in preventing the establishment of the disease. 6

The total area grown in 2006 with citrus in the French overseas department in FAOSTAT differs from the total area reported from Agreste 7 http://www.cafe-reunion.com/-Programme-Experimental-.html (accessed on 30 April 2008)

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2.2.2.4.

Other characteristics of the pest affecting the probability of establishment

C. fimbriata is a soil borne pathogen. It can persist in soil through thick-walled and durable aleurioconidia (chlamydospores) for long periods in the absence of suitable hosts. It also can survive in insect frass, wood fragments and in river water (CABI, 2007). Some degree of host specificity has been found within C. fimbriata sensu latu, but isolates from a given population or region often vary substantially in the disease levels found in inoculated hosts (Baker et al., 2003). Different levels of pathogenicity have been described among Colombian isolates of C. fimbriata from coffee, with some causing death of more than 90% and other killing less than 5% of the inoculated coffee plants (Marín et al., 2003). 2.2.2.5.

Conclusion on the probability of establishment

The document estimates the probability of C. fimbriata establishment in the PRA area as moderate in the “Conclusions of the pest risk assessment” and as “moderate to high” in the Summary box (first page). The Panel, after taking into account the information provided in the document and additional consulted, concludes that the probability of establishment, once the pathogen enters the PRA area, would be high. 2.2.3.

Probability of spread after establishment

The pathogen can be spread by machinery and farm equipment including pruning and cutting tools, by soil, or infected plant material. Infested insect frass and sawdust can be spread by wind, rain or running water. Fungal-feeding insects (Nitidulidae, Coleoptera) not associated with particular plants (Thorpe et al., 2005) and Ambrosia beetles, such as Xyleborus and Hypocryphalus species, that tunnel through infested wood and expel frass with fungal spores (CABI, 2007; Isla and Ravelo, 1989; Ocasio-Morales et al., 2007), may further facilitate the dispersal of the pathogen. The fungus can also be spread by vegetative propagation material taken from infected mother plants. 2.2.4.

Conclusion on probability of introduction and spread

The Panel agrees with the identification of the wood pathway, considering that the pathogen could transfer to a suitable host through infected host debris (e.g. sawdust) and by the help of insect vectors. The Panel considers that the probability of entry through host plants and vegetative propagation material would be moderate to high. The Panel notes that the highest risk for the citrus industry of the French overseas departments would be associated with the trade of host plants and vegetative propagation material or accompanying soil from areas where C. fimbriata is reported to cause disease on citrus (Colombia, Cuba). Main reported hosts crops of C. fimbriata in Colombia are citrus, coffee and cacao. The isolates pathogenic to cacao are now referred to the recently described species C. cacaofunesta. In Cuba the reported hosts are citrus, coffee, taro and the naturalized ornamental tree S. campanulata. The Panel also considers passenger traffic as an entry pathway. The Panel, after taking into account the information provided in the document and additional consulted, concludes that the probability of establishment, once the pathogen enters the PRA area, would be high. The Panel agrees with the document that cultural practices may lead to a rapid spread after establishment.

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2.3.

Assessment of potential economic consequences

2.3.1.

Direct pest effects

2.3.1.1.

Crop quality and/or yield losses

Host plant species of C. fimbriata are grown in the PRA area (see section 2.2.2.1.) with citrus and coffee being particularly at risk. The Panel considers that the main risk to citrus crops of the French overseas departments would be represented by C. fimbriata strains pathogenic to citrus in Colombia and in Cuba. C. fimbriata is reported to cause in these countries a rapid dieback and death of citrus plants (Capera-Borja et al., 1995a and b; Mourichon, 1994; Rodriguez and Alfonso, 1978). According to Mourichon (1994), C. fimbriata was reported to attack 10 % of citrus crops in Colombia and threaten citrus production in the Colombian coffee-growing regions. However it is not clear if this percentage refers to the number of infected trees, the surface affected or the number of orchards with plants showing symptoms. Capera-Borja et al. (1995a and b) also report that, in the central coffee-producing area of Colombia, 1-10% of the surface of technically-advanced citrus groves (which cover 8000 ha scattered in the whole area) was affected by the disease. According to Castrillon (1995, cited in Páez-Redondo and Castaño Zapata, 2001), the disease has caused in Colombia a reduction of 637 ha of the area under citrus (about 8% of total citrus area) and a yearly fruit yield reduction of 22,295 tons. In a Colombian experimental field, when citrus plants were planted on a naturally infected soil, 12 years old plants showed an high percentage of mortality (Onecco mandarin 64%; Valencia orange 51%), while in three years old trees the percentages were lower (Minneola tangelo 6%, Valencia orange 3%) (Castrillon and Urrea, 1999). The Cuban outbreak of C. fimbriata in citrus orchards of the Oriente province in the 70’s was described as severe (Rodriguez and Alfonso, 1978), but data on exact yield loss and disease incidence were not found by the Panel. Quarantine and burning of infected trees failed to control the disease, therefore it was recommended a complete eradication in the area of the outbreak (Rodriguez and Alfonso, 1978). However, the Panel could not find further information on the application and results of this measure. In Colombia, C. fimbriata is also a particularly important disease of coffee (Pontis, 1951). Different levels of pathogenicity have been described among Colombian isolates of C. fimbriata from coffee, with some causing death of more than 90% and other killing less than 5% of the inoculated coffee plants (Marín et al., 2003). 2.3.1.2.

Control measures, efficacy and costs

C. fimbriata could raise additional costs of control (costs of sanitation, phytosanitary measures) but the extra costs are difficult to estimate because some of the measures (removing of diseased plants) could be part of the normal cultivation process. 2.3.2. 2.3.2.1.

Indirect pest effects Loss of export markets

The Panel considers that the introduction of C. fimbriata into French Guiana, Guadeloupe, Martinique and Réunion is unlikely to affect export markets, as citrus production in these departments, according to the French document, is mainly for the local market.

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There is also no coffee export from the French overseas departments. However in Réunion the local variety Bourbon pointu (a mutation of the Bourbon variety, appeared in Réunion island in 1771) is very much appreciated for the aroma and it is object of a vast experimental program aiming for the development of coffee plantations for the export market 8 . The introduction of C. fimbriata could compromise a potential niche export. 2.3.2.2.

Social consequences

There is no information on social consequences of the introduction of C. fimbriata into the French overseas departments. Citrus is grown on a small area in the French overseas departments, however, there could be potential social consequences, in case, once introduced, the pathogen would attack also coffee and other crops. 2.3.2.3.

Environmental consequences

The document does not provide any information regarding the presence and distribution of host species of C. fimbriata in natural vegetations in French Guiana, Guadeloupe, Martinique and Réunion. The Panel considers that, in areas where C. fimbriata has been introduced, the damage is primarily to planted species and not to native vegetation. However, recently, a species of the same genus, C. platani, which normally attacks amenity plane trees, has been reported to cause substantial mortality of native P. orientalis in Greece (Ocasio-Morales et al., 2007). 2.3.3.

Conclusion of the assessment of economic consequences

According to the document the economic impact of any introduction of C. fimbriata into French overseas departments would be high. The Panel agrees that the impact on citrus would be severe and that the disease could also affect coffee and perhaps other species. 2.4.

Comments on the conclusion of the pest risk assessment

The document concludes that C. fimbriata must be classified as a quarantine organism for French Guiana, Guadeloupe, Martinique and Réunion. The Panel considers C. fimbriata appropriate for stage 3 of Pest Risk Analysis, i.e. the evaluation of pest risk management options for the four French overseas departments. 2.4.1.

Degree of uncertainty

The document notes that the level of uncertainty is moderate and is bound up with the probability of establishment. The Panel is of the opinion that the level of uncertainty is high especially for the following aspects: •

8

Coffee isolates from Colombia are reported to be pathogenic to citrus. (Marín et al., 2006). C. fimbriata isolates pathogenic to coffee have also been reported from other countries of Central America and northwestern South America (Baker et al., 2003; Pontis, 1951), but it is not known whether these coffee isolates are pathogenic to citrus.

http://www.cafe-reunion.com/Programme-experimental-sur-le.html (accessed on 30 April 2008)

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Pest risk assessment made by France on Ceratocystis fimbriata •

Based on reports in neighbouring regions, such as Brazil (Baker et al., 2003; Harrington, 2000), it can not be excluded that other suitable hosts of C. fimbriata of lesser economic importance may be present in Colombia, and that vegetative propagation material from these other hosts may also be a pathway for introduction.

•

There is uncertainty on the level of economic and social consequences depending on how many host plants C. fimbriata would be able to affect, once introduced.

CONCLUSIONS AND RECOMMENDATIONS The Panel observes that statements in the document are not individually referenced. Some statements are not supported by data. This is particularly noted in relation to economic impact of the introduction of the pathogen. The document could not consider the recent literature published after 2003 on taxonomy of Ceratocystis spp. The Panel concludes that: •

The Panel agrees with the identification of the wood pathway, considering that the pathogen could transfer to a suitable host through infected host debris (e.g. sawdust) and by the help of insect vectors. The Panel considers that the probability of entry through host plants and vegetative propagation material would be moderate to high. The Panel notes that the highest risk for the citrus industry of the French overseas departments would be associated with the trade of host plants and vegetative propagation material or accompanying soil from areas where C. fimbriata is reported to cause disease on citrus (Colombia, Cuba). Main host crops of C. fimbriata in Colombia are citrus, coffee and cacao. The isolates pathogenic to cacao are now referred to the recently described species C. cacaofunesta. In Cuba the reported hosts are citrus, coffee, taro and the naturalized ornamental tree S. campanulata. The Panel also considers passenger traffic as an entry pathway.

•

The Panel, after taking into account the information provided in the document and additional consulted, concludes that the probability of establishment, once the pathogen enters the PRA area, would be high.

•

The Panel agrees with the document that cultural practices may lead to a rapid spread after establishment.

•

The Panel agrees that the impact on citrus would be severe and considers that the disease could also affect coffee and perhaps other tree species.

•

The level of uncertainty is high for the following aspects: lack of studies on pathogenicity to citrus of isolates from other host plants and other regions; limited data published on yield losses; the level of economic and social consequences would depend on the range of affected host plants.

In agreement with the document, the Panel concludes that C. fimbriata is 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.

DOCUMENTATION PROVIDED TO EFSA 1. Letter, dated 14 July 2006 with ref. SANCO E/1/VE/svi D(2006) 510488 from P. Testori Coggi to C. Geslain-Lanéelle. The EFSA Journal (2008) 703, 17-21

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2. Phytosanitaire Analyse du Risque Phytosanitaire AGR-c3: Ceratocystis fimbriata Ellis et Halsted. Responsable de la maladie Chancre à Ceratocystis des Agrumes. Assessor: Xavier Mourichon, CIRAD, 2003. REFERENCES Agreste 2007a. Mémento agricole 2007 (résultats 2006). Agreste Martinique – La statistique agricole, Novembre 2007, 2 pp. Available from: http://agreste.agriculture.gouv.fr/IMG/pdf/D97208C01.pdf Agreste 2007b. L’agriculture guadeloupéenne en 2006 – Bilan. Statistique agricole annuelle. Comptes départementaux de l’agriculture. Agreste Guadeloupe, Novembre 2007 3: 24 pp. Document available on http://agreste.agriculture.gouv.fr/IMG/pdf/D97107A03.pdf Agreste 2007c. Mémento agricole et rural 2007 – La Réunion (résultats 2006). Agreste Réunion – La statistique agricole, Décembre 2007 11: 2 pp. Available from: http://agreste.agriculture.gouv.fr/IMG/pdf/D97407A15.pdf Baker CJ, Harrington TC, Kraus U and Alfenas AC 2003. Genetic variability and host specialization in the Latin American clade of Ceratocystis fimbriata. Phytopathology 93: 1274–1284. Baker Engelbrecht CJ and Harrington TC 2005. Intersterility, morphology and taxonomy of Ceratocystis fimbriata on sweet potato, cacao and sycamore. Mycologia 97(1): 57–69. Barnes I, Gaur A, Burgess T, Roux J, Wingfield BD and Wingfield MJ 2001. Microsatellite markers reflect intra-specific relationships between isolates of the vascular wilt pathogen Ceratocystis fimbriata. Molecular Plant Pathology 2: 319–325. CABI (CAB International) 2007. Crop Protection Compendium. Ceratocystis fimbriata Ellis & Halst., Ceratocystis blight. Available from: http://www.cabicompendium.org/cpc/datasheet.asp?CCODE=CERAFI&COUNTRY=0 as last updated on 07 March 2005 (accessed on 30 April 2008). Capera-Borja D, Leguizamon-Caycedo JE and Lopez-Rios A 1995a. Etiología y sintomatología del secamiento de los citricos en la zona cafetera central de Colombia. Cenicafé 46(2): 100– 111. Capera-Borja D, Leguizamon-Caycedo JE and Lopez-Rios A 1995b. El secamiento de los citricos en la zona cafetera central. Cenicafé Avances Tecnicos No. 212, 8 pp. Castrillon CA and Urrea CFJ 1999. Aspectos epidemiologicos sobre el secamiento de los citricos (Ceratocystis fimbriata Ellis. & Halsted and Hunt) en tres variedades comerciales. Fitopatologia Colombiana 23(1): 15–19. Conservatoire Botanique National de Mascarin (Boullet V. coord.) 2007. Index de la flore vasculaire de la Réunion (Trachéophytes) : statuts, menaces et protections. Version 2007.1 (mise à jour 12 juin 2007). Available from: http://flore.cbnm.org Council Directive 2000/29/EC of 8 May 2000 on protective measures against the introduction into the Community of organisms harmful to plants or plant products and against their spread within the Community. Daines RH 1971. The control of black rot of sweet potatoes by the use of fungicide dips at various temperatures. Phytopathology 61:1145–1146. Davidson RW 1944. Two American hardwood species of Endoconidiophora described as new. Mycologia 36: 300–306.

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De Alcain JC and Marmelicz LA 1984. Ceratocystis fimbriata – Ellis and Halst. A new lemon tree pathogen. Proceedings of International Society of Citriculture 1: 432–435. Engelbrecht CJB, Harrington HJ and Alfenas A 2007. Ceratocystis wilt of cacao – a disease of increasing importance. Phytopathology 97: 1648–1649. FAO (Food and Agriculture Organisation of the United Nations) 2007a. International standards for phytosanitary measures 1 to 29 (2007 edition), ISPM No. 5 Glossary on phytosanitary terms (2007), Rome, 63-86. FAO 2007b. International standards for phytosanitary measures 1 to 29 (2007 edition). ISPM No. 11 Pest risk analysis for quarantine pests including analysis of environmental risks and living modified organisms (2004), Rome, 135–160. FAO 2007c. International standards for phytosanitary measures 1 to 29 (2007 edition). ISPM No. 15 Guidelines for regulating wood packaging materials in international trade (2002) with modifications to Annex I (2006). Rome, 195–205. FAOSTAT 2008. ProdSTAT – Crops. Commodities/Countries, year 2006. Available from: http://faostat.fao.org/site/567/DesktopDefault.aspx?PageID=567 (accessed on 30 April 2008). Fournet J 2002. Flore illustrée des phanérogames de Guadeloupe et de Martinique. CIRAD, Montpellier - Gondwana Editions, Trinité. 2538 pp. Harrington TC 2000. Host specialization and speciation in the American wilt pathogen Ceratocystis fimbriata. Fitopatologia Brasileira 25S: 262–263. Harrington TC, McNew D, Steimel, Hofstra D and Farrel R 2001. Phylogeny and taxonomy of the Ophiostoma piceae complex and the Dutch elm disease fungi. Mycologia 93:111-136. Hoff M, Cremers G, Chevillotte H, De Granville JJ, Guérin V and Molino JF 2007. Base de données botaniques Aublet2 de l'Herbier de Guyane française (CAY). Available from: http://www.cayenne.ird.fr/aublet2 Hunt J 1956. Taxonomy of the Genus Ceratocystis. Lloydia 19: 1–59. Isla LH and Ravelo HG 1989. Spathodea campanulata Beauv., nueva planta hospedante de Ceratocystis fimbriata Ellis. & Halst. y Xyleborus spp. Centro Agricola 16 (2): 91–93. Iton EF 1960. Studies on a wilt disease of cacao at River Estate. II. Some aspects of wind transmission. In: Annual Report on Cacao Research, 1959-1960; 47–58 pp. INSEE (Institut National de la Statistique et des Études Économiques) 2007. Guyane : la région en faits et chiffres. Chiffres-clés: théme Agriculture/ Exploitations agricoles. Available from http://www.insee.fr/fr/insee_regions/guyane/rfc/chifcle_fiche.asp?ref_id=AGRTC001&tab_ id=1952 as last updated on August 2007 (accessed on 30 April 2008). Johnson JA, Baker CJ, Harrington TC and Nason JD 2002. Allozyme and DNA sequence analysis of Ceratocystis fimbriata isolates reveal geographic groupings and host associated lineages. Phytopathology 92: S40. Johnson JA, Harrington TC and Engelbrecht CJB 2005. Phylogeny and taxonomy of the NorthAmerican clade of the Ceratocystis fimbriata complex. Mycologia 97(5): 1067–1092. JORF (Journal Officiel de la République Française) 1992. Arrêté du 3 Décembre 1991 modifiant l’arrêté du 3 Septembre 1990 relatif au contrôle sanitaire des végétaux et produits végétaux. Journal Officiel de la République Française, 16 Février 1992, 2476–2503.

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