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SCIENTIFIC OPINION ADOPTED: 27 September 2018 doi: 10.2903/j.efsa.2018.5442 Pest categorisation of Melampsora farlowii EFSA Panel on Plant Health (EFSA PLH Panel), Claude Bragard, Francesco Di Serio, Paolo Gonthier, Marie-Agn es Jacques, Josep Anton Jaques Miret, Anne Marie Fejer Justesen, Alan MacLeod, Christer Sven Magnusson, Panagiotis Milonas, Juan A. Navas-Cortes, Stephen Parnell, Roel Potting, Philippe L Reignault, Hans-Hermann Thulke, Wopke Van der Werf, Antonio Vicent, Jonathan Yuen, Lucia Zappal a, Johanna Boberg, Michael Jeger, Marco Pautasso and Katharina Dehnen-Schmutz Abstract Following a request from the European Commission, the EFSA Panel on Plant Health performed a pest categorisation of Melampsora farlowii, a well-defined and distinguishable fungus of the family Melampsoraceae. M. farlowii is the causal agent of a leaf and twig rust of hemlocks (Tsuga spp.) in eastern North America. The pathogen is regulated in Council Directive 2000/29/EC (Annex IAI) as a harmful organism whose introduction into the EU is banned. M. farlowii is not reported to be present in Europe and could enter the EU via host plants for planting and cut branches. Cones and fruits are listed as plant parts that can carry the pest in trade and transport, but are not regulated. The pathogen could establish in the EU, as climatic conditions are favourable and Tsuga spp. have been planted as ornamentals and in plantations in several EU countries. M. farlowii would be able to spread following establishment by human movement of host plants for planting and cut branches, as well as natural spread. Should the pathogen be introduced in the EU, impacts can be expected on Tsuga spp. plantations, ornamental trees and especially nurseries. Hemlock rust is considered a destructive rust attacking Tsuga spp., particularly Tsuga canadensis in nurseries. The main uncertainties concern whether the impact of the pathogen in plantations under European conditions could be different than observed in eastern North America, whether fruit/cones of Tsuga can be a pathway of entry, and the dissemination potential of the pathogen under European conditions. However, M. farlowii is found in North America in most of the natural distribution range of T. canadensis, suggesting little dispersal limitation of the pathogen. The criteria assessed by the Panel for consideration as a potential quarantine pest are met, whilst, for regulated non-quarantine pests, the criterion on the pest presence in the EU is not met. ©2018 European Food Safety Authority. EFSA Journal published by John Wiley and Sons Ltd on behalf of European Food Safety Authority. Keywords: European Union, forest pathology, hemlock twig rust, pest risk, plant pest, quarantine, tree health Requestor: European Commission Question number: EFSA-Q-2018-00039 Correspondence: [email protected] EFSA Journal 2018;16(10):5442www.efsa.europa.eu/efsajournal
Panel members: Claude Bragard, Katharina Dehnen-Schmutz, Francesco Di Serio, Paolo Gonthier, Marie-Agn es Jacques, Josep Anton Jaques Miret, Anne Marie Fejer Justesen, Alan MacLeod, Christer Sven Magnusson, Panagiotis Milonas, Juan A. Navas-Cortes, Stephen Parnell, Roel Potting, Philippe L. Reignault, Hans-Hermann Thulke, Wopke Van der Werf, Antonio Vicent, Jonathan Yuen and Lucia Zappal a. Suggested citation: EFSA PLH Panel (EFSA Panel on Plant Health), Bragard C, Di Serio F, Gonthier P, Jacques M-A, Jaques Miret JA, Fejer Justesen AM, MacLeod A, Magnusson CS, Milonas P, Navas-Cortes JA, Parnell S, Potting R, Reignault PL, Thulke H-H, Van der Werf W, Vicent A, Yuen J, Zappal a L, Boberg J, Jeger M, Pautasso M and Dehnen-Schmutz K, 2018. Scientific Opinion on the pest categorisation of Melampsora farlowii. EFSA Journal 2018;16(10):5442, 19 pp. https://doi.org/10.2903/j.efsa.2018.5442 ISSN: 1831-4732 ©2018 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. Reproduction of the images listed below is prohibited and permission must be sought directly from the copyright holder: Figure 1: © EPPO; Figure 2: © European Union; Figure 3: © Bugwood.org The EFSA Journal is a publication of the European Food Safety Authority, an agency of the European Union. Melampsora farlowii: pest categorisation www.efsa.europa.eu/efsajournal 2 EFSA Journal 2018;16(10):5442
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 .............................................................................................................. 8 2.1. Data........................................................................................................................................... 8 2.1.1. Literature search ......................................................................................................................... 8 2.1.2. Database search ......................................................................................................................... 8 2.2. Methodologies............................................................................................................................. 8 3. Pest categorisation ...................................................................................................................... 10 3.1. Identity and biology of the pest.................................................................................................... 10 3.1.1. Identity and taxonomy................................................................................................................. 10 3.1.2. Biology of the pest ...................................................................................................................... 10 3.1.3. Intraspecific diversity................................................................................................................... 11 3.1.4. Detection and identification of the pest......................................................................................... 11 3.2. Pest distribution .......................................................................................................................... 11 3.2.1. Pest distribution outside the EU.................................................................................................... 11 3.2.2. Pest distribution in the EU............................................................................................................ 12 3.3. Regulatory status ........................................................................................................................ 12 3.3.1. Council Directive 2000/29/EC ....................................................................................................... 12 3.3.2. Legislation addressing the hosts of Melampsora farlowii ................................................................. 13 3.4. Entry, establishment and spread in the EU .................................................................................... 13 3.4.1. Host range.................................................................................................................................. 13 3.4.2. Entry.......................................................................................................................................... 13 3.4.3. Establishment ............................................................................................................................. 13 3.4.3.1. EU distribution of main host plants ............................................................................................... 13 3.4.3.2. Climatic conditions affecting establishment.................................................................................... 14 3.4.4. Spread ....................................................................................................................................... 14 3.5. Impacts...................................................................................................................................... 15 3.6. Availability and limits of mitigation measures ................................................................................. 16 3.6.1. Identification of additional measures............................................................................................. 16 3.6.1.1. Additional control measures ......................................................................................................... 16 3.6.1.2. Biological or technical factors limiting the feasibility and effectiveness of measures to prevent the entry, establishment and spread of the pest .................................................................................. 16 3.6.1.3. Biological or technical factors limiting the ability to prevent the presence of the pest on plants for planting...................................................................................................................................... 16 3.7. Uncertainty ................................................................................................................................. 16 4. Conclusions................................................................................................................................. 17 References............................................................................................................................................... 18 Glossary .................................................................................................................................................. 19 Abbreviations ........................................................................................................................................... 19 Melampsora farlowii: pest categorisation www.efsa.europa.eu/efsajournal 3 EFSA Journal 2018;16(10):5442
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 are 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. Melampsora farlowii: pest categorisation www.efsa.europa.eu/efsajournal 4 EFSA Journal 2018;16(10):5442
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 Aleurocanthus 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 cembrae Heer Cephalcia lariciphila (Klug) Ips duplicatus Sahlberg Dendroctonus micans Kugelan Ips sexdentatus B€ orner Gilphinia hercyniae (Hartig) Ips typographus Heer Gonipterus scutellatus Gyll. Sternochetus mangiferae Fabricius Ips amitinus Eichhof (b) Bacteria Curtobacterium flaccumfaciens pv. flaccumfaciens (Hedges) Collins and Jones Melampsora farlowii: pest categorisation www.efsa.europa.eu/efsajournal 5 EFSA Journal 2018;16(10):5442
(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 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 Melampsora farlowii: pest categorisation www.efsa.europa.eu/efsajournal 6 EFSA Journal 2018;16(10):5442
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 (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. Melampsora farlowii: pest categorisation www.efsa.europa.eu/efsajournal 7 EFSA Journal 2018;16(10):5442
(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 Melampsora farlowii 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 regulated non-quarantine pest (RNQP) for the area of the EU. 2. Data and methodologies 2.1. Data 2.1.1. Literature search A literature search on M. farlowii was conducted at the beginning of the categorisation in the ISI Web of Science bibliographic database, using the scientific name of the pest as well as its synonyms as search terms. The literature on the pest is limited (CABI, 2018), and most if not all available papers have been reviewed by the Panel. 2.1.2. Database search Pest information, on host(s) and distribution, was retrieved from the European and Mediterranean Plan Protection Organization (EPPO) Global Database (EPPO, 2018) and relevant publications. Data about the 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 (Statistical Office of the European Communities). The Europhyt database was consulted for pest-specific notifications on interceptions and outbreaks. Europhyt is a web-based network run by the Directorate General for Health and Food Safety (DG SANTE) of the European Commission, 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 Member States (MS) and the phytosanitary measures taken to eradicate or avoid their spread. 2.2. Methodologies The Panel performed the pest categorisation for M. farlowii, following guiding principles and steps presented in the EFSA guidance on quantitative pest risk assessment (EFSA PLH Panel, 2018) 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 quantitative pest risk assessment in the EU (EFSA PLH Panel, 2018), this work was started following an evaluation of the EU 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 in accordance with 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 Melampsora farlowii: pest categorisation www.efsa.europa.eu/efsajournal 8 EFSA Journal 2018;16(10):5442
as a quarantine pest or as a RNQP. If one of the criteria is not met, the pest will not qualify. A pest that does not qualify as a quarantine pest may still qualify as a RNQP that 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 regard 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, whereas addressing social impacts is outside the remit of the Panel, in agreement with the EFSA guidance on quantitative pest risk assessment (EFSA PLH Panel, 2018). Table 1: Pest categorisation criteria under evaluation, as 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 Criterion in Regulation (EU) 2016/2031 regarding Union quarantine pest Criterion in Regulation (EU) 2016/2031 regarding protected zone quarantine pest (articles 32–35) Criterion in Regulation (EU) 2016/2031 regarding Union regulated non-quarantine pest Identity of the pest (Section 3.1) Is the identity of the pest established, or has it been shown to produce consistent symptoms and to be transmissible? Is the identity of the pest established, or has it been shown to produce consistent symptoms and to be transmissible? Is the identity of the pest established, or has it been shown to produce consistent symptoms and to be transmissible? Absence/presence of the pest in the EU territory (Section 3.2) Is the pest present in the EU territory? If present, is the pest widely distributed within the EU? Describe the pest distribution briefly! Is the pest present in the EU territory? If not, it cannot be a protected zone quarantine organism Is the pest present in the EU territory? If not, it cannot be a regulated non-quarantine pest. (A regulated nonquarantine pest must be present in the risk assessment area.) Regulatory status (Section 3.3) If the pest is present in the EU but not widely distributed in the risk assessment area, it should be under official control or expected to be under official control in the near future The protected zone system aligns with the pest free area system under the International Plant Protection Convention (IPPC) The pest satisfies the IPPC definition of a quarantine pest that is not present in the risk assessment area (i.e. protected zone) Is the pest regulated as a quarantine pest? If currently regulated as a quarantine pest, are there grounds to consider its status could be revoked? Pest potential for entry, establishment and spread in the EU territory (Section 3.4) Is the pest able to enter into, become established in, and spread within, the EU territory? If yes, briefly list the pathways! Is the pest able to enter into, become established in, and spread within, the protected zone areas? Is entry by natural spread from EU areas where the pest is present possible? Is spread mainly via specific plants for planting, rather than via natural spread or via movement of plant products or other objects? Clearly state if plants for planting is the main pathway! Potential for consequences in the EU territory (Section 3.5) Would the pests’ introduction have an economic or environmental impact on the EU territory? Would the pests’introduction have an economic or environmental impact on the protected zone areas? Does the presence of the pest on plants for planting have an economic impact, as regards the intended use of those plants for planting? Melampsora farlowii: pest categorisation www.efsa.europa.eu/efsajournal 9 EFSA Journal 2018;16(10):5442
3.6. Availability and limits of mitigation measures 3.6.1. Identification of additional measures Phytosanitary measures are currently applied to the host species of M. farlowii (see Section 3.3.2). 3.6.1.1. Additional control measures Potential additional control measures are listed in Table 4. 3.6.1.2. Biological or technical factors limiting the feasibility and effectiveness of measures to prevent the entry, establishment and spread of the pest •Infection is not limited to small trees or the lower parts of large trees, but can also occur copiously on the top of large trees (Hepting and Toole, 1939). •Excluding the pathogen from nurseries by removing and burning all infected twigs and cones before growth starts in the spring would be difficult to achieve (Hepting and Toole, 1939). •Use of fungicides in nurseries may mask symptom development. 3.6.1.3. Biological or technical factors limiting the ability to prevent the presence of the pest on plants for planting •Nursery-grown trees provide especially good conditions for hemlock rust development because of the trimming of the trees, their proximity to each other and the resulting extensive areas of compact foliage (Hepting and Toole, 1939). 3.7. Uncertainty •There is little available literature on this pathogen. •There is relatively limited information on the distribution and abundance of host trees in Europe. •There is uncertainty on whether fruit/cones of Tsuga can be a pathway of entry. 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, there is an import prohibition in place for the main pathway Tsuga plants (see Sections 3.3,3.4.2 and 3.6.1) RNQPs: Are there measures available to prevent pest presence on plants for planting such that the risk becomes mitigated? Yes, should the pathogen be introduced in the EU, production of plants for planting in pest free areas can prevent pest presence on plants for planting. Table 4: Selected control measures (a full list is available in EFSA PLH Panel, 2018) for pest entry/ establishment/spread/impact in relation to currently unregulated hosts and pathways. Control measures are measures that have a direct effect on pest abundance Information sheet title (with hyperlink to information sheet if available) Control measure summary Risk component (entry/ establishment/spread/ impact) Chemical treatments on crops including reproductive material Treatments with triadimefon, neem oil or mancozeb once when buds break and twice at 7-/14-day intervals (Kenaley and Hudler, 2010) Impact Crop rotation, associations and density, weed/ volunteer control Avoiding planting pure stands of Tsuga spp. can reduce impacts Where disease is severe, planting of susceptible hemlocks should be avoided as inoculum produced within infected nursery beds or cultures will persist (Kenaley and Hudler, 2010) Impact Melampsora farlowii: pest categorisation www.efsa.europa.eu/efsajournal 16 EFSA Journal 2018;16(10):5442
•The potential dispersal range under European conditions of M. farlowii basidiospores is unknown. However, M. farlowii is found in North America in most of the natural distribution range of T. canadensis and T. caroliniana, thus suggesting little dispersal limitation of the pathogen. •There is uncertainty about whether the impact of the pathogen in plantations under European conditions could be different than observed in Eastern North America. 4. Conclusions M. farlowii meets the criteria assessed by EFSA for consideration as potential quarantine pests (Table 5). 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 nonquarantine pest Key uncertainties Identity of the pest (Section 3.1) The identity of M. farlowii as a species is clear The identity of M. farlowii as a species is clear None Absence/presence of the pest in the EU territory (Section 3.2) The pest is not reported to be present in the EU The pest is not reported to be present in the EU None Regulatory status (Section 3.3) M. farlowii is regulated by Council Directive 2000/29/EC (Annex IAI) as a harmful organism whose introduction into, and spread within, all Member States shall be banned M. farlowii is regulated by Council Directive 2000/29/EC (Annex IAI) as a harmful organism whose introduction into, and spread within, all Member States shall be banned None Pest potential for entry, establishment and spread in the EU territory (Section 3.4) Entry: the pest could enter the EU via host plants for planting and cut branches. Cones and fruits are listed as plant parts that can carry the pest in trade and transport Establishment: the hosts are non-native but are present in several EU MS. Climatic conditions are favourable in the risk assessment area Spread: the pest could spread following establishment by movement of host plants for planting and cut branches, as well as natural spread Plants for planting are not the main pathway of spread, given the potential contribution of cut branches and natural spread The dissemination potential of the fungus under European conditions is largely unknown There is uncertainty on whether fruit/cones of Tsuga can be a pathway of entry Potential for consequences in the EU territory (Section 3.5) The introduction of M. farlowii would have economic and environmental impacts in Tsuga spp. plantations, ornamental trees and especially nurseries The introduction of the pest could have an impact on the intended use of plants for planting There is uncertainty about whether the impact of the pathogen in plantations under European conditions could be different than observed in eastern North America Melampsora farlowii: pest categorisation www.efsa.europa.eu/efsajournal 17 EFSA Journal 2018;16(10):5442
References Arthur JC, 1962. Manual of the rusts in United States and Canada. Purdue Research Foundation, Purdue, Indiana, USA. CABI, 2018. Datasheet on Melampsora farlowii (hemlock rust). CAB International, Crop Protection Compendium. Available online: https://www.cabi.org/cpc/datasheet/33287 [Accessed September 2018] EFSA PLH Panel (EFSA Panel on Plant Health), Jeger M, Bragard C, Caffier D, Candresse T, Chatzivassiliou E, Dehnen-Schmutz K, 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, Winter S, Hart A, Schans J, Schrader G, Suffert M, Kertesz V, Kozelska S, Mannino MR, Mosbach-Schulz O, Pautasso M, Stancanelli G, Tramontini S, Vos S and Gilioli G, 2018. Guidance on quantitative pest risk assessment. EFSA Journal 2018;16(8):5350, 86 pp. https://doi.org/10.2903/j.efsa.2018.5350 EPPO (European and Mediterranean Plant Protection Organization), 1997. Data sheets on quarantine pests: Melampsora farlowii. In: Smith IM, McNamara DG, Scott PR, Holderness M (eds.), Quarantine Pests for Europe, 2nd Edition. CABI/EPPO, Wallingford. 1425 pp. EPPO (European and Mediterranean Plant Protection Organization), 2018. EPPO Global Database. Available online: https://gd.eppo.int [Accessed April 2018] FAO (Food and Agriculture Organization of the United Nations), 1995. ISPM (International standards for phytosanitary measures) No 4. Requirements for the establishment of pest free areas. Available online: https:// www.ippc.int/en/publications/614/ FAO (Food and Agriculture Organization of the United Nations), 2004. ISPM (International Standards for Phytosanitary Measures) 21—Pest risk analysis of regulated non-quarantine pests. FAO, Rome, 30 pp. Available online: https:// www.ippc.int/sites/default/files/documents//1323945746_ISPM_21_2004_En_2011-11-29_Refor.pdf FAO (Food and Agriculture Organization of the United Nations), 2013. ISPM (International Standards for Phytosanitary Measures) 11—Pest risk analysis for quarantine pests. FAO, Rome, 36 pp. Available online: https://www.ippc.int/sites/default/files/documents/20140512/ispm_11_2013_en_2014-04-30_201405121523-494. 65%20KB.pdf FAO (Food and Agriculture Organization of the United Nations), 2017. ISPM (International standards for phytosanitary measures) No 5. Glossary of phytosanitary terms. Available online: https://www.ippc.int/en/ publications/622/ Hepting GH and Toole ER, 1939. The hemlock rust caused by Melampsora farlowii. Phytopathology, 29, 463–473. Kenaley SC and Hudler GW, 2010. Hemlock twig rust caused by Melamspora farlowii (Arth.) Davis. Cornell University Factsheet, Ithaca, NY, USA. p. 2. Peel MC, Finlayson BL and McMahon TA, 2007. Updated world map of the K€ oppen-Geiger climate classification. Hydrology and Earth System Sciences Discussions, 4, 439–473. 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 nonquarantine pest Key uncertainties Available measures (Section 3.6) Import prohibition of host plants for planting is an available measure to reduce the risk of introduction Avoiding planting pure stands of Tsuga spp. can reduce impacts Production of plants for planting in pest free areas can prevent pest presence on plants for planting None Conclusion on pest categorisation (Section 4) The criteria assessed by the Panel for consideration of M. farlowii as a potential quarantine pest are met The criterion on the pest presence in the EU is not met Aspects of assessment to focus on/scenarios to address in future if appropriate The main uncertainties concern whether the impact of the pathogen in plantations under European conditions could be different than observed in eastern North America and the dissemination potential of the pathogen under European conditions. However, M. farlowii is found in North America in most of the natural distribution range of T. canadensis and T. caroliniana, thus suggesting little dispersal limitation of the pathogen The present categorisation has explored most if not all of the limited available literature on these uncertainties Melampsora farlowii: pest categorisation www.efsa.europa.eu/efsajournal 18 EFSA Journal 2018;16(10):5442
Glossary Containment (of a pest) Application of phytosanitary measures in and around an infested area to prevent spread of a pest (FAO, 1995, 2017) Control (of a pest) Suppression, containment or eradication of a pest population (FAO, 1995, 2017) Entry (of a pest) Movement of a pest into an area where it is not yet present, or present but not widely distributed and being officially controlled (FAO, 2017) Eradication (of a pest) Application of phytosanitary measures to eliminate a pest from an area (FAO, 2017) Establishment (of a pest) Perpetuation, for the foreseeable future, of a pest within an area after entry (FAO, 2017) Impact (of a pest) The impact of the pest on the crop output and quality and on the environment in the occupied spatial units Introduction (of a pest) The entry of a pest resulting in its establishment (FAO, 2017) Measures Control (of a pest) is defined in ISPM 5 (FAO 2017) as ‘Suppression, containment or eradication of a pest population’(FAO, 1995) Control measures are measures that have a direct effect on pest abundance Supporting measures are organisational measures or procedures supporting the choice of appropriate Risk Reduction Options that do not directly affect pest abundance Pathway Any means that allows the entry or spread of a pest (FAO, 2017) Phytosanitary measures Any legislation, regulation or official procedure having the purpose to prevent the introduction or spread of quarantine pests, or to limit the economic impact of regulated non-quarantine pests (FAO, 2017) Protected zones (PZ) A Protected zone is an area recognised at EU level to be free from a harmful organism, which is established in one or more other parts of the Union. Quarantine pest A pest of potential economic importance to the area endangered thereby and not yet present there, or present but not widely distributed and being officially controlled (FAO, 2017) Regulated non-quarantine pest A non-quarantine pest whose presence in plants for planting affects the intended use of those plants with an economically unacceptable impact and which is therefore regulated within the territory of the importing contracting party (FAO, 2017) Risk reduction option (RRO) A measure acting on pest introduction and/or pest spread and/or the magnitude of the biological impact of the pest should the pest be present. A RRO may become a phytosanitary measure, action or procedure according to the decision of the risk manager Spread (of a pest) Expansion of the geographical distribution of a pest within an area (FAO, 2017) Abbreviations DG SANTE Directorate General for Health and Food Safety EASIN European Alien Species Information Network EPPO European and Mediterranean Plant Protection Organization FAO Food and Agriculture Organization GBIF Global Biodiversity Information Facility IPPC International Plant Protection Convention JRC Joint Research Centre MS Member State PLH EFSA Panel on Plant Health RNQP regulated non-quarantine pest RRO Risk Reduction Option ToR Terms of Reference Melampsora farlowii: pest categorisation www.efsa.europa.eu/efsajournal 19 EFSA Journal 2018;16(10):5442