Pest categorisation of Cadang-Cadang viroid

SCIENTIFIC OPINION ADOPTED: 27 June 2017 doi: 10.2903/j.efsa.2017.4928 Pest categorisation of Cadang-Cadang viroid EFSA Panel on Plant Health (PLH), Michael Jeger, Claude Bragard, David Caffier, Thierry Candresse, Katharina Dehnen-Schmutz, Gianni Gilioli, Jean-Claude Gregoire, Josep Anton Jaques Miret, Alan MacLeod, Maria Navajas Navarro, Bj€ orn Niere, Stephen Parnell, Roel Potting, Trond Rafoss, Vittorio Rossi, Gregor Urek, Ariena Van Bruggen, Wopke Van der Werf, Jonathan West, Elisavet Chatzivassiliou, Stephan Winter, Gabor Hollo and Thierry Candresse Abstract The EFSA Panel on Plant Health performed a pest categorisation of Cadang-Cadang viroid for the European Union (EU) territory. Coconut cadang-cadang viroid (CCCVd) is a well-known viroid for which efficient molecular detection assays are available. It is transmitted by vegetative multiplication of infected hosts, by seed and pollen and, possibly, by the action of unknown vector(s). CCCVd is reported from a few countries in Asia and is not known to occur in the EU. It therefore does not meet one of the criteria for being a Union regulated non-quarantine pest. The host range of CCCVd is restricted to Arecaceae species (palms), in particular coconut and it is listed on all known hosts in Annex IIAI of Directive 2000/29/EC. CCCVd is expected to be able to enter in the EU and to be able to establish in the open in the southernmost regions of the EU and elsewhere under protected cultivation. It has the potential to subsequently spread via plants for planting and possibly other mechanisms. CCCVd is able to cause severe symptoms in some Arecaceae species while others seem less affected. The potential impact of CCCVd if introduced in the EU is very difficult to assess. Given that the spread potential is, as for other viroids, likely to be limited, the potential impact is estimated to be limited in extent but this judgement is affected by large uncertainties. Overall, CCCVd meets all the criteria evaluated by EFSA to qualify as Union quarantine pest. The main knowledge gaps concern (1) the relationships between CCCVd-related RNAs and CCCVd, (2) the origin and volume of the trade in palm seeds and plants for planting imported in the EU (3) the efficiency of natural spread under EU conditions and (4) host status and susceptibility of many palm species grown in the EU. ©2017 European Food Safety Authority. EFSA Journal published by John Wiley and Sons Ltd on behalf of European Food Safety Authority. Keywords: cadang-cadang viroid, cadang-cadang disease, orange spotting disease, CCCVd, palm, coconut, Arecaceae Requestor: European Commission Question number: EFSA-Q-2017-00201 Correspondence: [email protected] EFSA Journal 2017;15(7):4928www.efsa.europa.eu/efsajournal Panel members: Claude Bragard, David Caffier, Thierry Candresse, Elisavet Chatzivassiliou, Katharina Dehnen-Schmutz, Gianni Gilioli, Jean-Claude Gregoire, Josep Anton Jaques Miret, Michael Jeger, Alan MacLeod, Maria Navajas Navarro, Bj€ orn Niere, Stephen Parnell, Roel Potting, Trond Rafoss, Vittorio Rossi, Gregor Urek, Ariena Van Bruggen, Wopke Van der Werf, Jonathan West and Stephan Winter. Suggested citation: EFSA Panel on Plant Health (PLH), Jeger M, Bragard C, Caffier D, Candresse T, Dehnen-Schmutz K, Gilioli G, Gregoire J-C, Jaques Miret JA, MacLeod A, Navajas Navarro M, Niere B, Parnell S, Potting R, Rafoss T, Rossi V, Urek G, Van Bruggen A, Van der Werf W, West J, Chatzivassiliou E, Winter S, Hollo G and Candresse T, 2017. Scientific Opinon on the pest categorisation of Cadang-Cadang viroid. EFSA Journal 2017;15(7):4928, 23 pp. https://doi.org/10.2903/j.efsa.2017.4928 ISSN: 1831-4732 ©2017 European Food Safety Authority. EFSA Journal published by John Wiley and Sons Ltd on behalf of European Food Safety Authority. This is an open access article under the terms of the Creative Commons Attribution-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited and no modifications or adaptations are made. The EFSA Journal is a publication of the European Food Safety Authority, an agency of the European Union. Cadang-Cadang viroid: pest categorisation www.efsa.europa.eu/efsajournal 2 EFSA Journal 2017;15(7):4928 Table of contents Abstract................................................................................................................................................... 1 1. Introduction................................................................................................................................4 1.1. Background and Terms of Reference as provided by the requestor.................................................. 4 1.1.1. Background ................................................................................................................................4 1.1.2. Terms of Reference ..................................................................................................................... 4 1.1.2.1. Terms of Reference: Appendix 1................................................................................................... 5 1.1.2.2. Terms of Reference: Appendix 2................................................................................................... 6 1.1.2.3. Terms of Reference: Appendix 3................................................................................................... 7 1.2. Interpretation of the Terms of Reference....................................................................................... 8 2. Data and methodologies .............................................................................................................. 9 2.1. Data........................................................................................................................................... 9 2.1.1. Literature search ......................................................................................................................... 9 2.1.2. Database search ......................................................................................................................... 9 2.2. Methodologies............................................................................................................................. 9 3. Pest categorisation ...................................................................................................................... 11 3.1. Identity and biology of the pest.................................................................................................... 11 3.1.1. Identity and taxonomy................................................................................................................. 11 3.1.2. Biology of the pest ...................................................................................................................... 11 3.1.3. Intraspecific diversity................................................................................................................... 12 3.1.4. Detection and identification of the pest......................................................................................... 12 3.2. Pest distribution .......................................................................................................................... 12 3.2.1. Pest distribution outside the EU.................................................................................................... 12 3.2.2. Pest distribution in the EU............................................................................................................ 13 3.3. Regulatory status ........................................................................................................................ 13 3.3.1. Council Directive 2000/29/EC ....................................................................................................... 13 3.3.2. Legislation addressing plants and plant parts on which on which Cadang-Cadang viroid is regulated .13 3.3.3. Emergency measures for Rhynchophorus ferrugineus (Olivier) (red palm weevil) ............................. 14 3.4. Entry, establishment and spread in the EU .................................................................................... 16 3.4.1. Host range.................................................................................................................................. 16 3.4.2. Entry.......................................................................................................................................... 16 3.4.3. Establishment ............................................................................................................................. 16 3.4.3.1. EU distribution of main host plants ............................................................................................... 16 3.4.4. Spread ....................................................................................................................................... 17 3.4.4.1. Vectors and their distribution in the EU (if applicable) .................................................................... 17 3.5. Potential or observed impacts in the EU ........................................................................................ 17 3.5.1. Potential pest impacts.................................................................................................................. 17 3.5.1.1. Direct impacts of the pest............................................................................................................ 17 3.5.2. Observed pest impacts in the EU.................................................................................................. 18 3.6. Availability and limits of mitigation measures ................................................................................. 18 3.6.1. Biological or technical factors limiting the feasibility and effectiveness of measures to prevent the entry, establishment and spread of the pest .................................................................................. 19 3.6.2. Control methods.......................................................................................................................... 19 3.7. Uncertainty ................................................................................................................................. 19 4. Conclusions................................................................................................................................. 19 References............................................................................................................................................... 22 Abbreviations ........................................................................................................................................... 23 Cadang-Cadang viroid: pest categorisation www.efsa.europa.eu/efsajournal 3 EFSA Journal 2017;15(7):4928 1. Introduction 1.1. Background and Terms of Reference as provided by the requestor 1.1.1. Background Council Directive 2000/29/EC 1 on protective measures against the introduction into the Community of organisms harmful to plants or plant products and against their spread within the Community establishes the present European Union plant health regime. The Directive lays down the phytosanitary provisions and the control checks to be carried out at the place of origin on plants and plant products destined for the Union or to be moved within the Union. In the Directive’s 2000/29/EC annexes, the list of harmful organisms (pests) whose introduction into or spread within the Union is prohibited, is detailed together with specific requirements for import or internal movement. Following the evaluation of the plant health regime, the new basic plant health law, Regulation (EU) 2016/2031 2 on protective measures against pests of plants, was adopted on 26 October 2016 and will apply from 14 December 2019 onwards, repealing Directive 2000/29/EC. In line with the principles of the above mentioned legislation and the follow-up work of the secondary legislation for the listing of EU regulated pests, EFSA is requested to provide pest categorizations of the harmful organisms included in the annexes of Directive 2000/29/EC, in the cases where recent pest risk assessment/pest categorisation is not available. 1.1.2. Terms of Reference EFSA is requested, pursuant to Article 22(5.b) and Article 29(1) of Regulation (EC) No 178/2002 3 , to provide scientific opinion in the field of plant health. EFSA is requested to prepare and deliver a pest categorisation (step 1 analysis) for each of the regulated pests included in the appendices of the annex to this mandate. The methodology and template of pest categorisation have already been developed in past mandates for the organisms listed in Annex II Part A Section II of Directive 2000/29/EC. The same methodology and outcome is expected for this work as well. The list of the harmful organisms included in the annex to this mandate comprises 133 harmful organisms or groups. A pest categorisation is expected for these 133 pests or groups and the delivery of the work would be stepwise at regular intervals through the year as detailed below. First priority covers the harmful organisms included in Appendix 1, comprising pests from Annex II Part A Section I and Annex II Part B of Directive 2000/29/EC. The delivery of all pest categorisations for the pests included in Appendix 1 is June 2018. The second priority is the pests included in Appendix 2, comprising the group of Cicadellidae (non-EU) known to be vector of Pierce’s disease (caused by Xylella fastidiosa), the group of Tephritidae (non-EU), the group of potato viruses and virus-like organisms, the group of viruses and virus-like organisms of Cydonia Mill., Fragaria L., Malus Mill., Prunus L., Pyrus L., Ribes L., Rubus L. and Vitis L. and the group of Margarodes (non-EU species). The delivery of all pest categorisations for the pests included in Appendix 2 is end 2019. The pests included in Appendix 3 cover pests of Annex I part A section I and all pests categorisations should be delivered by end 2020. For the above mentioned groups, each covering a large number of pests, the pest categorisation will be performed for the group and not the individual harmful organisms listed under “such as” notation in the Annexes of the Directive 2000/29/EC. The criteria to be taken particularly under consideration for these cases, is the analysis of host pest combination, investigation of pathways, the damages occurring and the relevant impact. Finally, as indicated in the text above, all references to ‘non-European’should be avoided and replaced by ‘non-EU’and refer to all territories with exception of the Union territories as defined in Article 1 point 3 of Regulation (EU) 2016/2031. 1 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. OJ L 169/1, 10.7.2000, p. 1–112. 2 Regulation (EU) 2016/2031 of the European Parliament of the Council of 26 October 2016 on protective measures against pests of plants. OJ L 317, 23.11.2016, p. 4–104. 3 Regulation (EC) No 178/2002 of the European Parliament and of the Council of 28 January 2002 laying down the general principles and requirements of food law, establishing the European Food Safety Authority and laying down procedures in matters of food safety. OJ L 31/1, 1.2.2002, p. 1–24. Cadang-Cadang viroid: pest categorisation www.efsa.europa.eu/efsajournal 4 EFSA Journal 2017;15(7):4928 1.1.2.1. Terms of Reference: Appendix 1 List of harmful organisms for which pest categorisation is requested. The list below follows the annexes of Directive 2000/29/EC. Annex IIAI (a) Insects, mites and nematodes, at all stages of their development Aleurocantus spp. Numonia pyrivorella (Matsumura) Anthonomus bisignifer (Schenkling) Oligonychus perditus Pritchard and Baker Anthonomus signatus (Say) Pissodes spp. (non-EU) Aschistonyx eppoi Inouye Scirtothrips aurantii Faure Carposina niponensis Walsingham Scirtothrips citri (Moultex) Enarmonia packardi (Zeller) Scolytidae spp. (non-EU) Enarmonia prunivora Walsh Scrobipalpopsis solanivora Povolny Grapholita inopinata Heinrich Tachypterellus quadrigibbus Say Hishomonus phycitis Toxoptera citricida Kirk. Leucaspis japonica Ckll. Unaspis citri Comstock Listronotus bonariensis (Kuschel) (b) Bacteria Citrus variegated chlorosis Xanthomonas campestris pv. oryzae (Ishiyama) Dye and pv. oryzicola (Fang. et al.) Dye Erwinia stewartii (Smith) Dye (c) Fungi Alternaria alternata (Fr.) Keissler (non-EU pathogenic isolates) Elsinoe spp. Bitanc. and Jenk. Mendes Anisogramma anomala (Peck) E. M€ uller Fusarium oxysporum f. sp. albedinis (Kilian and Maire) Gordon Apiosporina morbosa (Schwein.) v. Arx Guignardia piricola (Nosa) Yamamoto Ceratocystis virescens (Davidson) Moreau Puccinia pittieriana Hennings Cercoseptoria pini-densiflorae (Hori and Nambu) Deighton Stegophora ulmea (Schweinitz: Fries) Sydow & Sydow Cercospora angolensis Carv. and Mendes Venturia nashicola Tanaka and Yamamoto (d) Virus and virus-like organisms Beet curly top virus (non-EU isolates) Little cherry pathogen (nonEU isolates) Black raspberry latent virus Naturally spreading psorosis Blight and blight-like Palm lethal yellowing mycoplasm Cadang-Cadang viroid Satsuma dwarf virus Citrus tristeza virus (non-EU isolates) Tatter leaf virus Leprosis Witches’broom (MLO) Annex IIB (a) Insect mites and nematodes, at all stages of their development Anthonomus grandis (Boh.) Ips amitinus Eichhof Cephalcia lariciphila (Klug) Ips cembrae Heer Dendroctonus micans Kugelan Ips duplicatus Sahlberg Gilphinia hercyniae (Hartig) Ips sexdentatus B€ orner Gonipterus scutellatus Gyll. Ips typographus Heer Sternochetus mangiferae Fabricius Cadang-Cadang viroid: pest categorisation www.efsa.europa.eu/efsajournal 5 EFSA Journal 2017;15(7):4928 (b) Bacteria Curtobacterium flaccumfaciens pv. flaccumfaciens (Hedges) Collins and Jones (c) Fungi Glomerella gossypii Edgerton Hypoxylon mammatum (Wahl.) J. Miller Gremmeniella abietina (Lag.) Morelet 1.1.2.2. Terms of Reference: Appendix 2 List of harmful organisms for which pest categorisation is requested per group. The list below follows the categorisation included in the annexes of Directive 2000/29/EC. Annex IAI (a) Insects, mites and nematodes, at all stages of their development Group of Cicadellidae (non-EU) known to be vector of Pierce’s disease (caused by Xylella fastidiosa), such as: 1) Carneocephala fulgida Nottingham 3) Graphocephala atropunctata (Signoret) 2) Draeculacephala minerva Ball Group of Tephritidae (non-EU) such as: 1) Anastrepha fraterculus (Wiedemann) 12) Pardalaspis cyanescens Bezzi 2) Anastrepha ludens (Loew) 13) Pardalaspis quinaria Bezzi 3) Anastrepha obliqua Macquart 14) Pterandrus rosa (Karsch) 4) Anastrepha suspensa (Loew) 15) Rhacochlaena japonica Ito 5) Dacus ciliatus Loew 16) Rhagoletis completa Cresson 6) Dacus curcurbitae Coquillet 17) Rhagoletis fausta (Osten-Sacken) 7) Dacus dorsalis Hendel 18) Rhagoletis indifferens Curran 8) Dacus tryoni (Froggatt) 19) Rhagoletis mendax Curran 9) Dacus tsuneonis Miyake 20) Rhagoletis pomonella Walsh 10) Dacus zonatus Saund. 21) Rhagoletis suavis (Loew) 11) Epochra canadensis (Loew) (c) Viruses and virus-like organisms Group of potato viruses and virus-like organisms such as: 1) Andean potato latent virus 4) Potato black ringspot virus 2) Andean potato mottle virus 5) Potato virus T 3) Arracacha virus B, oca strain 6) non-EU isolates of potato viruses A, M, S, V, X and Y (including Yo, Yn and Yc) and Potato leafroll virus Cadang-Cadang viroid: pest categorisation www.efsa.europa.eu/efsajournal 6 EFSA Journal 2017;15(7):4928 Group of viruses and virus-like organisms of Cydonia Mill., Fragaria L., Malus Mill., Prunus L., Pyrus L., Ribes L.,Rubus L. and Vitis L., such as: 1) Blueberry leaf mottle virus 8) Peach yellows mycoplasm 2) Cherry rasp leaf virus (American) 9) Plum line pattern virus (American) 3) Peach mosaic virus (American) 10) Raspberry leaf curl virus (American) 4) Peach phony rickettsia 11) Strawberry witches’broom mycoplasma 5) Peach rosette mosaic virus 12) Non-EU viruses and virus-like organisms of Cydonia Mill., Fragaria L., Malus Mill., Prunus L., Pyrus L., Ribes L., Rubus L. and Vitis L. 6) Peach rosette mycoplasm 7) Peach X-disease mycoplasm Annex IIAI (a) Insects, mites and nematodes, at all stages of their development Group of Margarodes (non-EU species) such as: 1) Margarodes vitis (Phillipi) 3) Margarodes prieskaensis Jakubski 2) Margarodes vredendalensis de Klerk 1.1.2.3. Terms of Reference: Appendix 3 List of harmful organisms for which pest categorisation is requested. The list below follows the annexes of Directive 2000/29/EC. Annex IAI (a) Insects, mites and nematodes, at all stages of their development Acleris spp. (non-EU) Longidorus diadecturus Eveleigh and Allen Amauromyza maculosa (Malloch) Monochamus spp. (non-EU) Anomala orientalis Waterhouse Myndus crudus Van Duzee Arrhenodes minutus Drury Nacobbus aberrans (Thorne) Thorne and Allen Choristoneura spp. (non-EU) Naupactus leucoloma Boheman Conotrachelus nenuphar (Herbst) Premnotrypes spp. (non-EU) Dendrolimus sibiricus Tschetverikov Pseudopityophthorus minutissimus (Zimmermann) Diabrotica barberi Smith and Lawrence Pseudopityophthorus pruinosus (Eichhoff) Diabrotica undecimpunctata howardi Barber Scaphoideus luteolus (Van Duzee) Diabrotica undecimpunctata undecimpunctata Mannerheim Spodoptera eridania (Cramer) Diabrotica virgifera zeae Krysan & Smith Spodoptera frugiperda (Smith) Diaphorina citri Kuway Spodoptera litura (Fabricus) Heliothis zea (Boddie) Thrips palmi Karny Hirschmanniella spp., other than Hirschmanniella gracilis (de Man) Luc and Goodey Xiphinema americanum Cobb sensu lato (non-EU populations) Liriomyza sativae Blanchard Xiphinema californicum Lamberti and Bleve-Zacheo Cadang-Cadang viroid: pest categorisation www.efsa.europa.eu/efsajournal 7 EFSA Journal 2017;15(7):4928 (b) Fungi Ceratocystis fagacearum (Bretz) Hunt Mycosphaerella larici-leptolepis Ito et al. Chrysomyxa arctostaphyli Dietel Mycosphaerella populorum G. E. Thompson Cronartium spp. (non-EU) Phoma andina Turkensteen Endocronartium spp. (non-EU) Phyllosticta solitaria Ell. and Ev. Guignardia laricina (Saw.) Yamamoto and Ito Septoria lycopersici Speg. var. malagutii Ciccarone and Boerema Gymnosporangium spp. (non-EU) Thecaphora solani Barrus Inonotus weirii (Murril) Kotlaba and Pouzar Trechispora brinkmannii (Bresad.) Rogers Melampsora farlowii (Arthur) Davis (c) Viruses and virus-like organisms Tobacco ringspot virus Pepper mild tigr e virus Tomato ringspot virus Squash leaf curl virus Bean golden mosaic virus Euphorbia mosaic virus Cowpea mild mottle virus Florida tomato virus Lettuce infectious yellows virus (d) Parasitic plants Arceuthobium spp. (non-EU) Annex IAII (a) Insects, mites and nematodes, at all stages of their development Meloidogyne fallax Karssen Rhizoecus hibisci Kawai and Takagi Popillia japonica Newman (b) Bacteria Clavibacter michiganensis (Smith) Davis et al. ssp. sepedonicus (Spieckermann and Kotthoff) Davis et al. Ralstonia solanacearum (Smith) Yabuuchi et al. (c) Fungi Melampsora medusae Th€ umen Synchytrium endobioticum (Schilbersky) Percival Annex I B (a) Insects, mites and nematodes, at all stages of their development Leptinotarsa decemlineata Say Liriomyza bryoniae (Kaltenbach) (b) Viruses and virus-like organisms Beet necrotic yellow vein virus 1.2. Interpretation of the Terms of Reference Cadang-Cadang viroid is one of a number of pests listed in the Appendices to the Terms of Reference (ToR) to be subject to pest categorisation to determine whether it fulfils the criteria of a quarantine pest or those of a Union regulated non-quarantine pest (RNQP) for the area of the European Union (EU) excluding Ceuta, Melilla and the outermost regions of Member States (MS) referred to in Article 355(1) of the Treaty on the Functioning of the European Union (TFEU), other than Madeira and the Azores. This pest categorisation covers Coconut cadang-cadang viroid (CCCVd). RNAs that hybridise with probes representing part or all of the genome of CCCVd sequence (so called ‘CCCVd-related RNAs’) Cadang-Cadang viroid: pest categorisation www.efsa.europa.eu/efsajournal 8 EFSA Journal 2017;15(7):4928 have been reported to occur in a number of palm species and other monocotyledons in the Pacific region and South-East Asia (Randles et al., 1980; Hanold and Randles, 1991b). However, there has generally been no unambiguous demonstration that these RNAs represent infectious CCCVd molecules. Although there are uncertainties, reports of the presence of CCCVd-related RNAs are therefore not considered in the present opinion as an indication of the presence of CCCVd. 2. Data and methodologies 2.1. Data 2.1.1. Literature search A literature search on Cadang-Cadang viroid was conducted at the beginning of the categorisation. Further references and information were obtained from citations within the references and from the grey literature. 2.1.2. Database search Pest information, on host(s) and distribution, was retrieved from the EPPO Global Database (EPPO, 2017). Data about import of commodity types that could potentially provide a pathway for the pest to enter the EU and about the area of hosts grown in the EU were obtained from EUROSTAT. The Europhyt database was consulted for pest-specific notifications on interceptions and outbreaks. Europhyt is a web-based network launched by the European Commission Directorate General for Health and Consumers (DG SANCO), and is a subproject of PHYSAN (Phyto-Sanitary Controls) specifically concerned with plant health information. The Europhyt database manages notifications of interceptions of plants or plant products that do not comply with EU legislation, as well as notifications of plant pests detected in the territory of the MSs and the phytosanitary measures taken to eradicate or avoid their spread. 2.2. Methodologies The Panel performed the pest categorisation for Cadang-Cadang viroid, following guiding principles and steps presented in the EFSA guidance on the harmonised framework for pest risk assessment (EFSA PLH Panel, 2010) and as defined in the International Standard for Phytosanitary Measures No 11 (FAO, 2013) and No 21 (FAO, 2004). In accordance with the guidance on a harmonised framework for pest risk assessment in the EU (EFSA PLH Panel, 2010), this work was initiated following an evaluation of the EU’s plant health regime. Therefore, to facilitate the decision-making process, in the conclusions of the pest categorisation, the Panel addresses explicitly each criterion for a Union quarantine pest and for a Union RNQP in accordance with Regulation (EU) 2016/2031 on protective measures against pests of plants, and includes additional information required as per the specific terms of reference received by the European Commission. In addition, for each conclusion, the Panel provides a short description of its associated uncertainty. Table 1presents the Regulation (EU) 2016/2031 pest categorisation criteria on which the Panel bases its conclusions. All relevant criteria have to be met for the pest to potentially qualify either as a quarantine pest or as a RNQP. If one of the criteria is not met, the pest will not qualify. Note that a pest that does not qualify as a quarantine pest may still qualify as a RNQP which needs to be addressed in the opinion. For the pests regulated in the protected zones only, the scope of the categorisation is the territory of the protected zone, thus the criteria refer to the protected zone instead of the EU territory. It should be noted that the Panel’s conclusions are formulated respecting its remit and particularly with regards to the principle of separation between risk assessment and risk management (EFSA founding regulation (EU) No 178/2002); therefore, instead of determining whether the pest is likely to have an unacceptable impact, the Panel will present a summary of the observed pest impacts. Economic impacts are expressed in terms of yield and quality losses and not in monetary terms, while addressing social impacts is outside the remit of the Panel, in agreement with EFSA guidance on a harmonised framework for pest risk assessment (EFSA PLH Panel, 2010). Cadang-Cadang viroid: pest categorisation www.efsa.europa.eu/efsajournal 9 EFSA Journal 2017;15(7):4928 3.4. Entry, establishment and spread in the EU 3.4.1. Host range All hosts of CCCVd belong to the Arecaceae family (owing to historical usage, the family is also referred to as Palmae as in directive 2000/29/EC), 6 a large family of ca. 181 genera and 2,600 perennial species of trees and shrubs (Christenhusz and Byng, 2016). There is only one report of a Poaceae species (Chloris) as a host of CCCVd (CABI, 2015) but the Panel was unable to identify the source of this information and to verify it. Cocos nucifera (coconut palm) is the main host of CCCVd, with all commercial varieties cultivated in the Philippines being susceptible. A wide number of Arecaceae species such as Aiphanes horrida, Aiphanes minima, Allagoptera arenaria, Arenga pinnata, Borassus flabellifer, Caryota mitis, Caryota urens, Corypha umbraculifera, Corphya utan, Dictyosperma album, Elaeis guineensis, Gaussia attenuata, Howea belmoreana, Howea forsteriana, Latania lontaroides, Livistona australis, Livistona rotundifolia, Metroxylon sagu, Neodypsis decaryi, Neodypsis leptocheilos, Ravenea rivularis, Syagrus schizophylla, Trachycarpus fortunei are natural hosts of CCCVd (EPPO GD; CABI, 2015; Wu et al., 2013). Experimental hosts identified after artificial inoculation include Adonidia merrillii,Areca catechu, Chrysalidocarpus lutescens,Corypha elata, Dypsis lutescens, Oreodoxa regia, Phoenix dactylifera, Ptychosperma macarthurii, Roystonea regia (EPPO GD; Imperial et al., 1985; Hanold and Randles, 1991a; Randles and Rodriguez, 2003) and possibly Maranta species (the later cited in CABI, 2015, but the Panel was unable to verify this information provided without indication on the original source). CCCVd-related RNAs have been detected in Elaeis guineensis and Corypha elata in the Philippines (Randles et al., 1980), as well as in members of Arecaceae, Pandanaceae, Zingiberaceae, Marantaceae and Commelinaceae in some south-west Pacific regions (Hanold and Randles, 1991b). But as stated elsewhere, the relationships between CCCVd-related RNAs and CCCVd have never been satisfactorily clarified. CCCVd is regulated in all of its Arecaceae hosts (Palmae species, see paragraph 3.3.1). However, there is some uncertainty concerning the report of Chloris as a host (CABI, 2015; see above). 3.4.2. Entry The main pathway for entry identified by the Panel is the trade of palm seeds or of plants for planting of susceptible Arecaceae species. Within the EU, many nurseries commercialise young palms for ornamental use and it is likely that those are either imported as small plants or grown in the EU from imported seeds. According to the ISEFOR database, 7 between the year 2000 and 2011 among several Arecaceae species, coconut plants were imported from Philippines (30 plants), Malaysia (1393 plants) and Sri Lanka (92 plants). Therefore, CCCVd is able to enter EU with at least coconut plants and the same applies to other susceptible palm species imported from those infected countries. 3.4.3. Establishment 3.4.3.1. EU distribution of main host plants In general, viroids have no other environmental constrains than those of their hosts. Palms, the hosts of CCCVd, are distributed in the tropical regions of the world with a few species adapted either to somewhat temperate or dry and arid conditions (Eiserhardt et al., 2011). The only palm species that grow naturally on the European mainland are the European fan palm (Chamaerops humilis, with a distribution mainly in coastal areas of the western half of the Mediterranean basin) and the Cretan Is the pest able to enter into the EU territory? YES, CCCVd could potentially enter EU via palm seeds or live plants imported as ornamentals. Is the pest able to become established in the EU territory? YES, Several Arecaceae species are produced and are widely used as ornamentals for landscaping in southern Europe. 6 http://www.bgbm.org/IAPT/Nomenclature/Code/SaintLouis/0022Ch3Sec2a018.htm 7 Database developed within the FP7 Project ‘Increasing Sustainability of European Forests: Modelling for Security Against Invasive Pests and Pathogens under Climate Change’. Cadang-Cadang viroid: pest categorisation www.efsa.europa.eu/efsajournal 16 EFSA Journal 2017;15(7):4928 date palm (Phoenix theophrasti, endemic to Crete (Greece) and a few east Aegean islands) (Vamvoukakis, 1988). Many other palm species and mainly Chamaerops species,Canary palm (Phoenix canariensis) and date palm (Phoenix dactylifera) as well as Washingtonia robusta and Washingtonia filinera are widely used as ornamentals for landscaping in southern Europe (Cohen, 2017). The only known palm commercial cultivation for non-ornamental purposes in Europe is that of date palm (P. dactylifera) in Elche, Spain (38°170N) (Ferry et al., 2002) an area in the extreme northern latitude for its distribution (Abdelouahhab and Arias-Jimenez, 1999). Several palm species are widely grown in the EU under protected cultivation conditions for ornamental purposes. Spain produces about 2 million palm trees annually with Phoenix canariensis (1.2 million plants) being the predominant species, followed by other species such as P. dactylifera, Phoenix reclinata,W. filifera,W. robusta,Chamaerops humilis and Trachycarpus fortunei. (Armengol et al., 2005). There is also a significant ornamental palm production in nurseries in the Marche region of Italy (Nardi et al., 2009). In addition, the species Trachycarpus fortune is an ornamental species that is sometime grown in the open up to more northern latitudes (e.g. southern Switzerland) Gian das. Therefore, CCCVd is able to establish in the EU as there are some hosts grown in unprotected cultivation in southern Europe while many of them are grown in protected cultivation in more northern regions of the EU. However, there are some uncertainties concerning the sensitivity of the European native palm species (European fan palm and Cretan date palm) to CCCVd. The same applies to several other palm species grown for ornamental purposes in the EU. 3.4.4. Spread 3.4.4.1. Vectors and their distribution in the EU (if applicable) CCCVd systematically invades its hosts (see Section 3.1.2) and therefore can be transmitted through vegetative propagation practiced either by offshoot or tissue culture applied for some palm species e.g. date palm (Abdelouahhab and Arias-Jimenez, 1999). On the other hand, low rates of pollen and seed transmission of CCCVd, can be also responsible for pathogen movement (Hanold and Randles, 1991a; Pacumbaba et al., 1994) but this mechanism is expected to be significant only for species able to reproduce naturally under conditions prevailing in the EU. This applies in particular to the European fan palm and the Cretan date palm. In the infected areas in the Philippines, the extend and the patterns of natural spread cannot be fully explained by vegetative and pollen or seed transmission suggesting that the main mean of spread is still unknown (Pacumbaba et al., 1994). Therefore, additional mechanisms of spread cannot be excluded, but the uncertainties on this specific aspect are obviously very large. 3.5. Potential or observed impacts in the EU 3.5.1. Potential pest impacts 3.5.1.1. Direct impacts of the pest Coconut palms are severely affected by CCCVd. The disease is characterised by a slow progression of symptoms, closely associated with the progress of the infection and the presence of the different molecular forms of the viroid (Mohamed et al., 1982). It results eventually in the death of the diseased coconut trees (Randles and Rodriguez, 2003). First symptoms appear 1–2 years after the first detection of the viroid; nuts become rounded and scarified with an increasing incidence, while only at a later stage chlorotic (or water-soaked) spots appear on the leaves, inflorescences are stunted with tip necrosis and Is the pest able to spread within the EU territory following establishment? Yes. However, the spread is likely to be limited and with large uncertainties as the principal mode of spread may still be unknown. How: Through production and trade of plants for planting. Also through pollen and seeds of susceptible Arecaceae species. Would the pests’introduction have an economic or environmental impact on the EU territory? YES. Cadang-Cadang viroid: pest categorisation www.efsa.europa.eu/efsajournal 17 EFSA Journal 2017;15(7):4928 show loss of some male florets. As disease progresses, symptoms become more severe, there is a decline in fruit production as fewer nuts, spathe and inflorescences are produced, leaf spot numbers increase and coalesce while plant appear chlorotic, stunted, with a progressive decline, and eventually die. Susceptibility to the viroid decreases with the age of the plant (Velasco, 1997). CCCVd is considered to be a serious economic threat for coconut, causing their premature decline and death (Hanold and Randles, 1991a). It was estimated that in the Philippines about 40 million palms have died from cadang-cadang with a loss of about US$100 per infected palm due to lost production and delay in replacement (Randles and Rodriguez, 2003). The impact of the coconut lamina-depleting ‘brooming’ disease associated with the presence of single mutations (Rodriguez and Randles, 1993; Rodriguez and Randles, 1993) and the orange spotting disease, possibly associated with the occurrence of CCCVd variants in African oil palm in Malaysia (Vadamalai et al., 2006), is not yet estimated. Most species in the Arecaceae family that have been successfully inoculated with CCCVd, for example betel nut (Areca catechu) and palmera (Chrysalidocarpus lutescens), develop severe yellow leaf spotting. Other species such as buri palm (Corypha elata), oil palm (Elaeis guineensis), royal palm (Oreodoxa regia) and Manila palm (Adonidia merrillii) were also stunted (Imperial et al., 1985). 3.5.2. Observed pest impacts in the EU CCCVd is not present in the EU; therefore, no impact is observed. For some species grown in the EU, such as the date palm (P. dactylifera), susceptibility has been experimentally demonstrated and some symptoms and damage could be expected should CCCVd be introduced. For other species grown it the EU, and in particular for the two species growing spontaneously in the EU (European fan palm and Cretan date palm), no information on susceptibility is available so that impact, if any, remains highly uncertain. None of the known hosts of CCCVd represents an important EU agricultural rop; however, a few of them are of high ornamental, landscape or cultural importance in the Mediterranean countries of the EU. A large number of those ornamental palms are produced in EU countries such as Spain and Italy (see Section 3.4.3.1) to be traded to the European markets, therefore they can be of considerable economic importance. On the other hand, three major heritage palm groves exist in the Mediterranean European countries, in Elche in Spain, Bordighera in Italy and Crete in Greece. The major one is that of Elche (Spain) that is made up of about 180,000 adult date palms, in an area of almost 400 ha. The total date fruit production in Elche is estimated to be 5,000 tonnes per year, of which only about 100 tonnes are sold for human consumption (Ferry et al. 1997 –cited in Ferry et al., 2002). However, the grove of date palm in Elche (Valencia) trees known as ‘Palmeral of Elche’was designated in 2000 as a World Heritage Site (http://whc.unesco.org/en/list/930). There are also a couple of additional historical groves in the same area of Spain, in Orihuela and Alicante, but they are not as large as the one in Elche (Su arez, 2010; Jacas et al., 2011). In Bordighera, in Italy, date palms have been cultivated since at least the 16th century for religious purposes, and even though their number has significantly dropped since the last century, they remain of high landscape significance. Other threatened native species may include the Cretan date palm (Phoenix theophrasti) that is present only in Crete (Greece) and a few east Aegean islands (Vamvoukakis, 1988) and is a species with a near threatened status (2006 IUCN Red List of Threatened Species). Overall, while several species grown in Europe and of commercial or cultural importance are known to be susceptible to CCCVd, information is lacking for other species, in particular the two European native palms. In addition, there are important uncertainties about how efficiently CCCVd would be able to spread in European palms. The potential impact of CCCVd if introduced in the EU is therefore very difficult to assess. Given that the spread potential is, as for other viroids, likely to be limited, the potential impact is estimated to be limited in extent but this judgement is affected by large uncertainties. 3.6. Availability and limits of mitigation measures Cadang-Cadang viroid is listed in Council Directive 2000/29/EC and it is regulated in all of its hosts 8 (see Section 3.4.1). The present legislation imposes several conditions on imported plants for planting Are there measures available to prevent the entry into, establishment within or spread of the pest within the EU such that the risk becomes mitigated? YES for entry: tightening of regulations to include seeds and to rely on CCCVd testing rather than on the unreliable observation of symptoms. 8 Chloris has been reported as a host but this assessment is associated with significant uncertainties. Cadang-Cadang viroid: pest categorisation www.efsa.europa.eu/efsajournal 18 EFSA Journal 2017;15(7):4928 of Arecaceae (Palmae) species. Specifically, these may be imported on the condition that ‘no symptoms of Cadang-Cadang viroid have been observed on the plants since the beginning of the last complete cycle of vegetation and that plants at the place of production which have shown symptoms giving rise to the suspicion of contamination by the organisms have been rogued out at that place’(Council Directive 2000/29/EC, Annex IV, Part A, Section I, 37b). In addition, the import into and movement within the EU of many palm species is subjected to specific requirements and inspections according to the emergency measures set with the Commission Decision 2007/365/EC for R. ferrugineus (see Section 3.4.1). In the field, symptoms of CCCVd may have an incubation period of up to 6 years and roguing is not effective in controlling the spread of the viroid (Randles and Rodriguez, 2003). Therefore, due to its reliance on the short-term observation of symptoms, the current plant health legislation is not considered fully efficient. Accordingly, the emergency measures for R. ferrugineus may only slightly improve the efficiency of the current legislation as CCCVd incubation period is longer than the surveillance period put in place. On the other hand, the current legislation does not take into account seeds, despite the fact that CCCVd is known to be seed-transmitted (Anon., 1982 –cited by Randles and Imperial, 1984; Pacumbaba et al., 1994). In addition, there are also uncertainties about whether imported coconuts would be considered as seeds or as fruits. 3.6.1. Biological or technical factors limiting the feasibility and effectiveness of measures to prevent the entry, establishment and spread of the pest •Existence of a long asymptomatic phase of up to 6 years in the field •Symptoms, especially the early ones, resemble those caused by abiotic stress or other pests •Seed and pollen transmission •Imperfect knowledge on the natural means of spread •Systemic pathogen transmitted by vegetative multiplication practices •No clear ecoclimatic limitations besides those applying to the host •The ambiguous status of CCCVd-related molecules affecting the host range and geographic distribution of CCCVd •Unavailability of genetic resistance and efficient control strategies. 3.6.2. Control methods Exclusion in the only method considered to be effective in controlling the spread of CCCVd. In the Philippines, the spread of Cadang-Cadang disease is managed by regulating movement of coconut products across internal quarantine boundaries (Carpio, 2011; -cited by Geering and Randles, 2012). Control by eradication has been unsuccessful, while replanting does not significantly affect disease spread, but only allow to maintain production in affected areas (Randles, 1987). No genetic resistance or tolerance is available in C. nucifera; all 93 tested coconut populations were susceptible to inoculation (Orolfo et al., 2000); however, some field resistance to natural infection may be available in some population (Randles and Rodriguez, 2003). 3.7. Uncertainty The Panel identified four mains sources of uncertainty in the present opinion: •Uncertainties on the relationships between CCCVd-related RNAs and CCCVd and therefore on host range and geographic distribution of CCCVd. •Uncertainties on the origin and volume of the trade in palm seeds and plants for planting imported in the EU. •Uncertainties about the efficiency of spread under EU conditions. •Lack of information on host status and susceptibility of many palm species grown in the EU and, in particular on susceptibility of the two species growing spontaneously in the EU. These uncertainties primarily affect two aspects of the present Pest Categorisation, the efficiency and extent to which CCCVd would be able to spread and the impact it would have if introduced in the EU. 4. Conclusions CCCVd meets the criteria required to satisfy the definition of a Union quarantine pest (Table 5). Cadang-Cadang viroid: pest categorisation www.efsa.europa.eu/efsajournal 19 EFSA Journal 2017;15(7):4928 Table 5: The Panel’s conclusions on the pest categorisation criteria defined in Regulation (EU) 2016/2031 on protective measures against pests of plants (the number of the relevant sections of the pest categorisation is shown in brackets in the first column Criterion of pest categorisation Panel’s conclusions against criterion in Regulation (EU) 2016/2031 regarding Union quarantine pest Panel’s conclusions against criterion in Regulation (EU) 2016/2031 regarding Union regulated non-quarantine pest Key uncertainties Identity of the pest (Section 3.1) The identity of the pest is well established; it can be identified with reliable and sensitive molecular diagnostic techniques The identity of the pest is well established; it can be identified with reliable and sensitive molecular diagnostic techniques Uncertainties concerning the relationship of CCCVd-related RNAs with CCCVd Absence/presence of the pest in the EU territory (Section 3.2) CCCVd is not known to occur in the EU territory CCCVd is not known to occur in the EU territory, therefore does not qualify as a Union RNQP Although not documented, some CCCVd isolates might be present in the EU Regulatory status (Section 3.3) CCCVd is currently regulated on Palmae (Arecaceae) plants for planting by 2000/29/EC. Emergency measures set with the Commission Decision 2007/365/EC for R. ferrugineus and many palm species may improve the efficiency of 2000/29/EC CCCVd is currently regulated on Palmae (Arecaceae) plants for planting by 2000/29/EC. Emergency measures set with the Commission Decision 2007/365/EC for R. ferrugineus and many palm species may improve the efficiency of 2000/29/EC No uncertainties Pest potential for entry, establishment and spread in the EU territory (Section 3.4) CCCVd could potentially enter, establish and spread in the EU. At least plants for planting and seeds of Arecaceae species represent possible pathways for the pest to enter and spread in the EU Plants for planting and seeds of Arecaceae species represent the main entry pathways and the main means of CCCVd spread over long distance Uncertainties on the origin and volume of the trade in palm seeds and plants for planting imported in the EU Uncertainties about the efficiency of spread under EU conditions Lack of information on host status of many palm species grown in the EU and, in particular on susceptibility of the two species growing spontaneously in the EU Potential for consequences in the EU territory (Section 3.5) The potential impact of CCCVd if introduced in the EU is very difficult to assess. Given that the spread potential is, as for other viroids, likely to be limited, the potential impact is estimated to be limited in extent but this judgement is affected by large uncertainties. Because of the limited spread potential of viroids the expected impact, is expected to be limited, but large uncertainties affect this assessment Lack of information on host status and susceptibility of many palm species grown in the EU and, in particular on susceptibility of the two species growing spontaneously in the EU Available measures (Section 3.6) Exclusion in the only method considered to be effective in controlling the spread of the pest. There are no efficient methods (e.g roguing, natural resistance or tolerance) for controlling CCCVd spread after its introduction in an area. Replanting is used only to maintain production in affected areas The ambiguous status of CCCVd-related molecules affects the host range and geographic distribution of CCCVd therefore hinders the efficiency of the measures Cadang-Cadang viroid: pest categorisation www.efsa.europa.eu/efsajournal 20 EFSA Journal 2017;15(7):4928 Criterion of pest categorisation Panel’s conclusions against criterion in Regulation (EU) 2016/2031 regarding Union quarantine pest Panel’s conclusions against criterion in Regulation (EU) 2016/2031 regarding Union regulated non-quarantine pest Key uncertainties Conclusion on pest categorisation (Section 4) CCCVd meets all the criteria evaluated by EFSA to qualify as a Union quarantine pest CCCVd does not meet the presence on the territory criterion and therefore does not qualify as a Union RNQP Aspects of assessment to focus on/scenarios to address in future if appropriate The main knowledge gaps concern (1) the relationships between CCCVd-related RNAs and CCCVd, (2) the origin and volume of the trade in palm seeds and plants for planting imported in the EU (3) the efficiency of natural spread under EU conditions and (4) host status and susceptibility of many palm species grown in the EU. 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Abbreviations CCCVd Coconut Cadang-Cadang viroid CTiVd Coconut tinangaja viroid EPPO European and Mediterranean Plant Protection Organization EU MS European Union Member State FAO Food and Agriculture Organization IPPC International Plant Protection Convention OS orange spotting PAGE polyacrylamide gel electrophoresis PLH EFSA Panel on Plant Health RA risk assessment RNQP regulated non-quarantine pest RPA ribonuclease protection assay RT-LAMP reverse transcription loop-mediated isothermal amplification RT-PCR reverse transcription polymerase chain reaction TFEU Treaty on the Functioning of the European Union ToR Terms of Reference Cadang-Cadang viroid: pest categorisation www.efsa.europa.eu/efsajournal 23 EFSA Journal 2017;15(7):4928