Pest categorisation of Liriomyza sativae

Marie-Agnès Jacques

The Agricultural Research Service of the United States Department of Agriculture has maintained a continuous European effort in classical biological control of exotic pests in the USA. The European Parasite Laboratory was established in France in 1919, while the European Weed Laboratory began operations in Rome in 1958. The two laboratories were merged in Montpellier in 1991 as the European Biological Control Laboratory (EBCL), becoming the primary overseas biocontrol laboratory of the USDA. The management of weeds, insect pests, and pathogens is an important feature of agricultural research programmes worldwide. These invasive species can lead to vast financial losses for countries engaged in agriculture. The overall goal of research at EBCL is to develop biological control technologies to be used to suppress invading weeds and insect pests. This is done through expeditions to find natural enemies (insects, mites and pathogens), or phytophagous, parasitoid or predator species. These are characterized in careful experimentation in quarantine facilities and eventually developed as biological control agents. Current weed projects include studies on the Centaurea spp., Arundo donax, Vincetoxicum spp., Isatis tinctoria, Taeniatherum sp. and Dipsacus sp. Insect projects research Lygus bugs, the olive fruit fly, the vine mealybug, and the Asian long-horned beetle. The EBCL team is international and interdisciplinary. Entomology, plant and insect pathology, molecular biology and ecology are the main approaches of our biocontrol research. The team cooperates with universities and agencies worldwide.

Plant pathogens and invertebrates harmful to plants, collectively referred to as plant pests, continue to threaten food security. International cooperation and regulatory systems to inhibit the spread of plant pests began formally in 1878. Initially seven countries worked together and agreed phytosanitary measures against grape phylloxera, Phylloxera vastatrix (=Daktulosphaira vitifoliae). There are now 172 countries that are contracting parties to the International Plant Protection Convention, a treaty that aims to prevent the introduction and spread of pests of plants and plant products, and to promote appropriate measures for their control. Apparently contradictory interests between international trade, which has facilitated the spread of plant pests, and the protection of plants are mutually recognised in global trade and phytosanitary agreements. The principle that risk management measures should provide an appropriate level of protection without undue interference in trade was established within the plant protection agreements at the beginning of the 20th Century and is still fundamental to risk management policy today. Globally ten Regional Plant Protection Organizations facilitate more local cooperation and recommend the regulation of over 1,000 named quarantine plant pests. Member States of the European Union work together and regulate imported plant material on the grounds of plant health with each Member State taking into account the plant health concerns of every other Member State. However, decision making can be slow and border inspections poorly targeted. Close relationships between regulatory scientists and policy makers, focussed on agricultural and horticultural production, are changing to take a broader stakeholder community into consideration as decisions regarding the environment seek to draw upon a wider knowledge base. Challenges that impede the success of limiting international pest movement include increased international trade and climate change. International guidelines designed to prevent pest spread present challenges of their own if they remain difficult to implement.

SCIENTIFIC OPINION ADOPTED: 30 January 2020 doi: 10.2903/j.efsa.2020.6037 Pest categorisation of Liriomyza sativae EFSA Panel on Plant Health (PLH), Claude Bragard, Katharina Dehnen-Schmutz, Francesco Di Serio, Paolo Gonthier, s Jacques, Josep Anton Jaques Miret, Annemarie Fejer Justesen, Marie-Agne Christer Sven Magnusson, Panagiotis Milonas, Juan A Navas-Cortes, Stephen Parnell, Roel Potting, Philippe Lucien Reignault, Hans-Hermann Thulke, Wopke Van der Werf, , Ewelina Czwienczek, Franz Streissl and Antonio Vicent Civera, Jonathan Yuen, Lucia Zappala Alan MacLeod Abstract The EFSA Panel on Plant Health performed a pest categorisation of Liriomyza sativae (Diptera: Agromyzidae) for the EU. L. sativae (the cabbage or vegetable leaf miner; EPPO code: LIRISA) is a polyphagous pest native to the Americas which has spread to Africa, Asia and Oceania. L. sativae can have multiple overlapping generations per year. Eggs are inserted in the leaves of host plants. Three larval instars, which feed internally on ﬁeld vegetables (leaves and stems), follow. Then, the larva jumps into the soil where a fourth larval instar occurs immediately before pupation, which takes place in the soil. L. sativae is regulated in the EU by Commission Implementing Regulation (EU) 2019/2072 (Annex IIA). Within this Regulation, import of soil or growing medium as such or attached to plants for planting from third countries other than Switzerland is regulated. Therefore, entry of L. sativae pupae is prevented. However, immature stages on plants for planting (excluding seeds) and fresh leafy hosts for consumption, cut branches, ﬂowers and fruit with foliage provide potential pathways for entry into the EU. L. sativae has been repeatedly intercepted in the EU, especially in basil (Ocimum spp.). Climatic conditions and the wide availability of host plants provide conditions to support establishment in the EU, both in open ﬁelds and greenhouses. Impacts on ﬁeld vegetables and ornamentals as well as hosts in greenhouses would be possible. Phytosanitary measures are available to reduce the likelihood of entry. L. sativae satisﬁes the criteria that are within the remit of EFSA to assess for it to be regarded as a potential Union quarantine pest. Although human-assisted movement of vegetables is considered the main spread way for L. sativae, this agromyzid does not meet the criterion of occurring in the EU for it to be regarded as a potential Union regulated non-quarantine pest. © 2020 European Food Safety Authority. EFSA Journal published by John Wiley and Sons Ltd on behalf of European Food Safety Authority. Keywords: Agromyzid, European Union, pest risk, plant health, plant pest, quarantine, cabbage leaf miner, vegetable leaf miner Requestor: European Commission Question number: EFSA-Q-2019-00579 Correspondence: alpha@efsa.europa.eu www.efsa.europa.eu/efsajournal EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation Panel members: Claude Bragard, Katharina Dehnen-Schmutz, Francesco Di Serio, Paolo Gonthier, s Jacques, Josep Anton Jaques Miret, Annemarie Fejer Justesen, Alan MacLeod, Christer Marie-Agne Sven Magnusson, Panagiotis Milonas, Juan A Navas-Cortes, Stephen Parnell, Roel Potting, Philippe Lucien Reignault, Hans-Hermann Thulke, Wopke Van der Werf, Antonio Vicent Civera, Jonathan Yuen . and Lucia Zappala Suggested citation: EFSA PLH Panel (EFSA Panel on Plant Health), Bragard C, Dehnen-Schmutz K, Di Serio F, Gonthier P, Jacques MA, Jaques Miret JA, Justesen AF, Magnusson CS, Milonas P, NavasCortes JA, Parnell S, Potting R, Reignault PL, Thulke H-H, Van der Werf W, Vicent Civera A, Yuen J, L, Czwienczek E, Streissl F and MacLeod A, 2020. Scientiﬁc Opinion on the pest categorisation Zappala of Liriomyza sativae. EFSA Journal 2020;18(3):6037, 37 pp. https://doi.org/10.2903/j.efsa.2020.6037 ISSN: 1831-4732 © 2020 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 The EFSA Journal is a publication of the European Food Safety Authority, an agency of the European Union. www.efsa.europa.eu/efsajournal 2 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation Table of contents Abstract................................................................................................................................................... 1. Introduction................................................................................................................................ Background and Terms of Reference as provided by the requestor.................................................. 1.1. 1.1.1. Background ................................................................................................................................ 1.1.2. Terms of Reference ..................................................................................................................... 1.1.2.1. Terms of Reference: Appendix 1................................................................................................... 1.1.2.2. Terms of Reference: Appendix 2................................................................................................... 1.1.2.3. Terms of Reference: Appendix 3................................................................................................... 1.2. Interpretation of the Terms of Reference....................................................................................... 2. Data and methodologies .............................................................................................................. Data........................................................................................................................................... 2.1. 2.1.1. Literature search ......................................................................................................................... 2.1.2. Database search ......................................................................................................................... 2.2. Methodologies............................................................................................................................. Pest categorisation ...................................................................................................................... 3. Identity and biology of the pest.................................................................................................... 3.1. 3.1.1. Identity and taxonomy................................................................................................................. 3.1.2. Biology of the pest ...................................................................................................................... 3.1.3. Intraspeciﬁc diversity ................................................................................................................... 3.1.4. Detection and identiﬁcation of the pest ......................................................................................... Pest distribution .......................................................................................................................... 3.2. 3.2.1. Pest distribution outside the EU .................................................................................................... 3.2.2. Pest distribution in the EU............................................................................................................ 3.3. Regulatory status ........................................................................................................................ 3.3.1. Regulation 2016/2031.................................................................................................................. 3.3.2. Legislation addressing the hosts of Liriomyza sativae ..................................................................... Entry, establishment and spread in the EU .................................................................................... 3.4. 3.4.1. Host range.................................................................................................................................. 3.4.2. Entry .......................................................................................................................................... 3.4.2.1. Interceptions .............................................................................................................................. 3.4.3. Establishment ............................................................................................................................. 3.4.3.1. EU distribution of main host plants ............................................................................................... 3.4.3.2. Climatic conditions affecting establishment .................................................................................... 3.4.4. Spread ....................................................................................................................................... 3.5. Impacts ...................................................................................................................................... 3.6. Availability and limits of mitigation measures ................................................................................. 3.6.1. Identiﬁcation of additional measures............................................................................................. 3.6.2. Additional control measures ......................................................................................................... 3.6.2.1. Additional supporting measures .................................................................................................... 3.6.2.2. Biological or technical factors limiting the effectiveness of measures to prevent the entry, establishment and spread of the pest ........................................................................................... 3.6.2.3. Biological or technical factors limiting the ability to prevent the presence of the pest on plants for planting ...................................................................................................................................... 3.7. Uncertainty ................................................................................................................................. Conclusions................................................................................................................................. 4. References............................................................................................................................................... Abbreviations ........................................................................................................................................... Glossary .................................................................................................................................................. Appendix A – Host plants for Liriomyza sativae. .......................................................................................... Appendix B – EU member state production of some L. sativae hosts ............................................................ Appendix C – Detailed global distribution of Liromyza sativae on the base of EPPO Global Database............... www.efsa.europa.eu/efsajournal 3 1 4 4 4 4 5 6 7 8 8 8 8 8 9 11 11 11 11 12 12 13 13 14 14 14 14 15 15 15 16 18 18 18 19 19 20 20 20 21 22 23 23 23 24 25 25 27 30 35 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation 1. Introduction 1.1. Background and Terms of Reference as provided by the requestor 1.1.1. Background Council Directive 2000/29/EC1 on protective measures against the introduction into the Community of organisms harmful to plants or plant products and against their spread within the Community established the previous European Union plant health regime. The Directive laid 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 was prohibited, was 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) 2016/20312 on protective measures against pests of plants, was adopted on 26 October 2016 and applied 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 categorisations 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 pest 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 2 3 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. 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. 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. www.efsa.europa.eu/efsajournal 4 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation 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. Anthonomus bisignifer (Schenkling) Anthonomus signatus (Say) Aschistonyx eppoi Inouye Carposina niponensis Walsingham Enarmonia packardi (Zeller) Enarmonia prunivora Walsh Grapholita inopinata Heinrich Hishomonus phycitis Leucaspis japonica Ckll. Listronotus bonariensis (Kuschel) Numonia pyrivorella (Matsumura) Oligonychus perditus Pritchard and Baker Pissodes spp. (non-EU) Scirtothrips aurantii Faure Scirtothrips citri (Moultex) Scolytidae spp. (non-EU) Scrobipalpopsis solanivora Povolny Tachypterellus quadrigibbus Say Toxoptera citricidas Kirk. Unaspis citri Comstock (b) Bacteria Citrus variegated chlorosis Erwinia stewartii (Smith) Dye Xanthomonas campestris pv. oryzae (Ishiyama) Dye and pv. oryzicola (Fang. et al.) Dye (c) Fungi Alternaria alternata (Fr.) Keissler (non-EU pathogenic isolates) €ller Anisogramma anomala (Peck) E. Mu Apiosporina morbosa (Schwein.) v. Arx Ceratocystis virescens (Davidson) Moreau Cercoseptoria pini-densiﬂorae (Hori and Nambu) Deighton Cercospora angolensis Carv. and Mendes Elsinoe spp. Bitanc. and Jenk. Mendes Fusarium oxysporum f. sp. albedinis (Kilian and Maire) Gordon Guignardia piricola (Nosa) Yamamoto Puccinia pittieriana Hennings Stegophora ulmea (Schweinitz: Fries) Sydow & Sydow Venturia nashicola Tanaka and Yamamoto (d) Virus and virus-like organisms Beet curly top virus (non-EU isolates) Black raspberry latent virus Blight and blight-like Cadang-Cadang viroid Citrus tristeza virus (non-EU isolates) Leprosis Little cherry pathogen (non- EU isolates) Naturally spreading psorosis Palm lethal yellowing mycoplasm Satsuma dwarf virus Tatter leaf virus Witches’ broom (MLO) Annex IIB (a) Insect mites and nematodes, at all stages of their development Anthonomus grandis (Boh.) Cephalcia lariciphila (Klug) Dendroctonus micans Kugelan Gilphinia hercyniae (Hartig) Gonipterus scutellatus Gyll. Ips amitinus Eichhof www.efsa.europa.eu/efsajournal Ips cembrae Heer Ips duplicatus Sahlberg €rner Ips sexdentatus Bo Ips typographus Heer Sternochetus mangiferae Fabricius 5 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation (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 2) Draeculacephala minerva Ball 3) Graphocephala atropunctata (Signoret) Group of Tephritidae (non-EU) such as: 1) Anastrepha fraterculus (Wiedemann) 2) Anastrepha ludens (Loew) 3) Anastrepha obliqua Macquart 4) Anastrepha suspensa (Loew) 5) Dacus ciliatus Loew 6) Dacus curcurbitae Coquillet 7) Dacus dorsalis Hendel 8) Dacus tryoni (Froggatt) 9) Dacus tsuneonis Miyake 10) Dacus zonatus Saund. 11) Epochra canadensis (Loew) 12) 13) 14) 15) 16) 17) 18) 19) 20) 21) Pardalaspis cyanescens Bezzi Pardalaspis quinaria Bezzi Pterandrus rosa (Karsch) Rhacochlaena japonica Ito Rhagoletis completa Cresson Rhagoletis fausta (Osten-Sacken) Rhagoletis indifferens Curran Rhagoletis mendax Curran Rhagoletis pomonella Walsh Rhagoletis suavis (Loew) (c) Viruses and virus-like organisms Group of potato viruses and virus-like organisms such as: 1) Andean potato latent virus 2) Andean potato mottle virus 3) Arracacha virus B, oca strain 4) Potato black ringspot virus 5) Potato virus T 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) 2) 3) 4) 5) 6) 7) Blueberry leaf mottle virus Cherry rasp leaf virus (American) Peach mosaic virus (American) Peach phony rickettsia Peach rosette mosaic virus Peach rosette mycoplasm Peach X-disease mycoplasm www.efsa.europa.eu/efsajournal 8) Peach yellows mycoplasm 9) Plum line pattern virus (American) 10) Raspberry leaf curl virus (American) 11) Strawberry witches’ broom mycoplasma 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 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation 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) Amauromyza maculosa (Malloch) Anomala orientalis Waterhouse Arrhenodes minutus Drury Choristoneura spp. (non-EU) Conotrachelus nenuphar (Herbst) Dendrolimus sibiricus Tschetverikov Diabrotica barberi Smith and Lawrence Diabrotica undecimpunctata howardi Barber Diabrotica undecimpunctata undecimpunctata Mannerheim Diabrotica virgifera zeae Krysan & Smith Diaphorina citri Kuway Heliothis zea (Boddie) Hirschmanniella spp., other than Hirschmanniella gracilis (de Man) Luc and Goodey Liriomyza sativae Blanchard Longidorus diadecturus Eveleigh and Allen Monochamus spp. (non-EU) Myndus crudus Van Duzee Nacobbus aberrans (Thorne) Thorne and Allen Naupactus leucoloma Boheman Premnotrypes spp. (non-EU) Pseudopityophthorus minutissimus (Zimmermann) Pseudopityophthorus pruinosus (Eichhoff) Scaphoideus luteolus (Van Duzee) Spodoptera eridania (Cramer) Spodoptera frugiperda (Smith) Spodoptera litura (Fabricus) Thrips palmi Karny Xiphinema americanum Cobb sensu lato (non-EU populations) Xiphinema californicum Lamberti and Bleve-Zacheo (b) Fungi Ceratocystis fagacearum (Bretz) Hunt Chrysomyxa arctostaphyli Dietel Cronartium spp. (non-EU) Endocronartium spp. (non-EU) Guignardia laricina (Saw.) Yamamoto and Ito Gymnosporangium spp. (non-EU) Inonotus weirii (Murril) Kotlaba and Pouzar Melampsora farlowii (Arthur) Davis Mycosphaerella larici-leptolepis Ito et al. Mycosphaerella populorum G. E. Thompson Phoma andina Turkensteen Phyllosticta solitaria Ell. and Ev. Septoria lycopersici Speg. var. malagutii Ciccarone and Boerema Thecaphora solani Barrus Trechispora brinkmannii (Bresad.) Rogers (c) Viruses and virus-like organisms virus Pepper mild tigre Squash leaf curl virus Euphorbia mosaic virus Florida tomato virus Tobacco ringspot virus Tomato ringspot virus Bean golden mosaic virus Cowpea mild mottle virus Lettuce infectious yellows virus www.efsa.europa.eu/efsajournal 7 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation (d) Parasitic plants Arceuthobium spp. (non-EU) Annex IAII (a) Insects, mites and nematodes, at all stages of their development Meloidogyne fallax Karssen Popillia japonica Newman Rhizoecus hibisci Kawai and Takagi (b) Bacteria Clavibacter michiganensis (Smith) Davis et al. ssp. Ralstonia solanacearum (Smith) Yabuuchi et al. sepedonicus (Spieckermann and Kotthoff) Davis et al. (c) Fungi €men Melampsora medusae Thu 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 Liriomyza sativae Blanchard 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 for the area of the EU excluding Ceuta, Melilla and the outermost regions of Member States referred to in Article 355(1) of the Treaty on the Functioning of the European Union (TFEU), other than Madeira and the Azores. Following the adoption of Regulation (EU) 2016/2031 on 14 December 2019 and the Commission Implementing Regulation (EU) 2019/2072 for the listing of EU regulated pests, the Plant Health Panel interpreted the original request (ToR in Section 1.1.2) as a request to provide pest categorisations for the pests in the Annexes of Commission Implementing Regulation (EU) 2019/2072. 2. Data and methodologies 2.1. Data 2.1.1. Literature search A literature search on Liriomyza sativae was conducted at the beginning of the categorisation in the ISI Web of Science bibliographic database, using the scientiﬁc name Liriomyza sativae as a search term. Relevant papers were reviewed, and further references and information were obtained from experts, as well as from citations within the references and grey literature. 2.1.2. Database search Pest information, on host(s) and distribution, was retrieved from the European and Mediterranean Plant Protection Organization (EPPO) Global Database (EPPO, 2019a,b) 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) www.efsa.europa.eu/efsajournal 8 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation 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 Liriomyza sativae, following guiding principles and steps presented in the EFSA guidance on quantitative pest risk assessment (EFSA PLH Panel, 2018) and in the International Standard for Phytosanitary Measures No 11 (FAO, 2013) and No 21 (FAO, 2004). This work was initiated 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 regulated nonquarantine pest (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 ToR received by the European Commission. In addition, for each conclusion, the Panel provides a short description of its associated uncertainty. Table 1 presents 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 an 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 an 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. 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 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 nonquarantine 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 an RNQP. (A regulated nonquarantine pest must be present in the risk assessment area) Criterion of pest categorisation www.efsa.europa.eu/efsajournal 9 EFSA Journal 2020;18(3):6037 Liriomyza sativae: 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 nonquarantine pest 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) 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! Potential for consequences in the EU territory (Section 3.5) Would the pests’ introduction have an economic or environmental impact on the EU territory? Is spread mainly via speciﬁc plants for planting, rather than via natural spread or via movement of plant products or other objects? Is entry by natural spread from Clearly state if plants for EU areas where the pest is planting is the main pathway! present possible? Does the presence of the pest Would the pests’ introduction on plants for planting have an have an economic or economic impact as regards environmental impact on the the intended use of those protected zone areas? plants for planting? Available measures (Section 3.6) 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? Criterion of pest categorisation Regulatory status (Section 3.3) 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 able to enter into, become established in, and spread within, the protected zone areas? Are there measures available to prevent the entry into, establishment within or spread of the pest within the protected zone areas such that the risk becomes mitigated? Are there measures available to prevent pest presence on plants for planting such that the risk becomes mitigated? Is it possible to eradicate the pest in a restricted area within 24 months (or a period longer than 24 months where the biology of the organism so justiﬁes) after the presence of the pest was conﬁrmed in the protected zone? Conclusion of pest categorisation (Section 4) A statement as to whether (1) all criteria assessed by EFSA above for consideration as a potential quarantine pest were met and (2) if not, which one(s) were not met A statement as to whether (1) all criteria assessed by EFSA above for consideration as potential protected zone quarantine pest were met, and (2) if not, which one(s) were not met A statement as to whether (1) all criteria assessed by EFSA above for consideration as a potential RNQP were met, and (2) if not, which one (s) were not met The Panel will not indicate in its conclusions of the pest categorisation whether to continue the risk assessment process, but following the agreed two-step approach, will continue only if requested by the risk managers. However, during the categorisation process, experts may identify key elements and knowledge gaps that could contribute signiﬁcant uncertainty to a future assessment of risk. It would be useful to identify and highlight such gaps so that potential future requests can speciﬁcally target the major elements of uncertainty, perhaps suggesting speciﬁc scenarios to examine. www.efsa.europa.eu/efsajournal 10 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation 3. Pest categorisation 3.1. Identity and biology of the pest 3.1.1. Identity and taxonomy Is the identity of the pest established, or has it been shown to produce consistent symptoms and to be transmissible? Yes, the identity of Liriomyza sativae is well established. Liriomyza sativae Blanchard 1938 is an insect of the order Diptera, family Agromyzidae. This species, native to the Americas, was originally described from specimens obtained from infested leaves of lucerne (Medicago sativa L.) collected in Argentina (CABI, 2019). However, it was inadvertently redescribed twice (Scheffer and Lewis, 2005). Its common English names include cabbage leaf miner, tomato leaf miner and vegetable leaf miner (EPPO GD, 2019). This species has many junior synonyms (CABI, 2019; EPPO GD, 2019; FAO, 2016): Agromyza subpusilla Frost, 1943); Liriomyza canomarginis Frick, 1952; L. guytona Freeman, 1958; L. lycopersicae Pla & de la Cruz, 1981; L. minutiseta Frick, 1952; L. munda Frick, 1957; L. propepusilla Frost, 1954; L. pullata Frick, 1952; and L. verbenicola Hering, 1951. The EPPO code (Griessinger and Roy, 2015; EPPO, 2019a,b) for this species is LIRISA4 (EPPO GD, 2019). According to Scheffer and Lewis (2005), there has been a long history of taxonomic confusion regarding L. sativae, which together with numerous misidentiﬁcations, make the literature on this species before the 1970s difﬁcult to interpret. 3.1.2. Biology of the pest Although nearly all Liriomyza species are host-speciﬁc, Liriomyza sativae is one of the few Agromyzidae of economic importance considered to be truly polyphagous (Parrella, 1987; Kang et al., 2009). Indeed, this species is considered a pest of many vegetable and ﬂower crops (Spencer, 1973a, b, 1990). Larvae feed internally on plants, often as leaf and stem miners, thus the common name of leaf miner. L. sativae is a multivoltine species which cannot survive cold areas except in greenhouses. In warm climates (including glasshouses), this species can breed continuously, with many overlapping generations per year (Capinera, 2017; CABI, 2019). Eggs, which are inserted into plant tissue just beneath the leaf surface (Capinera, 2017), hatch in 2–8 days depending on temperature (Parrella, 1987). Many eggs can be laid on the same leaf. A lower development threshold for this stage was estimated to be 7°C (Webb and Smith, 1970). First instar larvae start feeding immediately after hatching and will continue feeding until they reach the third instar. At this stage, the larva cuts a semicircular slit in the mined leaf and usually exits the mine, jumps off the leaf and burrows into the soil to a depth of only a few centimetres to form a puparium (Capinera, 2017). A fourth non-feeding larval instar occurs between puparium formation and pupation (Parrella, 1987). The lower development threshold of this stage has been estimated to be in the range 4.6–7.9°C (Oatman and Michelbacher, 1959; Webb and Smith, 1970). The pupal stage may take 7–14 days at temperatures between 20 and 30°C (Leibee, 1982). At lower temperatures, emergence is delayed and this stage becomes the overwintering stage (Parrella, 1987). Indeed, pupae can endure some time at freezing temperatures. The LT50 of 4-day-old puparia exposed to 0, 5, and 10°C is around 9 days, 2 days, and less than 1 hour, respectively (Zhao and Kang, 2000). Immature development time takes around 25 days at 15°C. At optimal temperatures (30°C), the whole cycle is completed in about 15 days (Capinera, 2017). One day after emergence, adults become sexually active. They can mate several times for up to a month post-emergence before dying (Capinera, 2017). Adults feed on plant exudates, e.g. caused by oviposition. Females often make feeding punctures without depositing eggs and only about 15% of 4 An EPPO code, formerly known as a Bayer code, is a unique identiﬁer linked to the name of a plant or plant pest important in agriculture and plant protection. Codes are based on genus and species names. However, if a scientiﬁc name is changed the EPPO code remains the same. This provides a harmonised system to facilitate the management of plant and pest names in computerised databases, as well as data exchange between IT systems (Griessinger and Roy, 2015; EPPO, 2019a,b). www.efsa.europa.eu/efsajournal 11 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation punctures contain viable eggs (Parrella et al., 1981). Mean fecundity ranges from 200 to 700 eggs per female, with a daily oviposition rate of 30–40 eggs, which decreases as females get older. Adult agromyzid ﬂies are not considered strong ﬂiers and tend to remain close to their target crops, only moving short distances between host plants. Although they can be passively dispersed over long distances by the wind (Malipatil et al., 2016), dispersal over long distances is attributed to humanassisted movement of planting material (EPPO GD, 2019). 3.1.3. Intraspeciﬁc diversity The existence of a host race of L. sativae on melons (misidentiﬁed as L. pictella) was reported by Parrella (1987). Later, Scheffer and Lewis (2005) found distinct mitochondrial clades in different L. sativae populations from native (the Americas) and invaded areas (Asia), which suggested that L. sativae could be a cryptic species complex. Interestingly, only one clade seemed to be invasive on a worldwide scale. However, this study was not conclusive and further research is needed to clarify the situation. 3.1.4. Detection and identiﬁcation of the pest Are detection and identiﬁcation methods available for the pest? Yes, there are standard protocols for detection and identiﬁcation of L. sativae (EPPO, 2005; FAO, 2016). Moreover, taxonomic keys for the identiﬁcation of L. sativae exist (Spencer and Steyskal, 1986). There are almost 400 species in the genus Liriomyza (Kang et al., 2009; EPPO GD, 2019), of which around 140 are found naturally in Europe (Seymour, 1994; de Jong et al., 2014). According to EPPO (EPPO GD, 2019), the adult ﬂies of all these minute species (1–3 mm long) look very similar. From above, they are seen to be mostly black, with a bright yellow scutellum in most species. As a result, separating these species can be difﬁcult. Diagnosticians have to distinguish indigenous and naturalised Liriomyza spp. from quarantine agromyzid species. FAO developed a diagnostic protocol for these species including morphological and molecular tools for both adults and immature stages of this ﬂy (ISPM 27; FAO 2016). EPPO also produced a standard for L. sativae (PM 7/53; EPPO, 2005). A summary of the most remarkable features in these diagnostic protocols follows: • Detection Symptoms: Feeding punctures and leaf mines are usually the ﬁrst and most obvious signs of the presence of Liriomyza spp. Mines remain intact and relatively unchanged over a period of weeks. Mine conﬁguration is affected by the host, by the physical and physiological condition of each leaf and by the number of larvae mining the same leaf. Therefore, species identiﬁcation from mine conﬁguration alone is not advisable, especially for polyphagous Liriomyza spp. like L. sativae. Adults: Small free-ﬂying minute ﬂies (1.3–2.3 mm in body length, 1.3–2.3 mm in wing length; females slightly larger than males), which can be observed on leaf surfaces while producing feeding and oviposition punctures. Species-speciﬁc characteristics of L. sativae include bright-yellow scutellum, shining black prescutum and scutum and inner vertical setae usually standing on yellow ground. Accurate identiﬁcation, though, requires dissection of male terminalia (see below). Immature stages: Egg: Elliptical, 0.20–0.30 9 0.10–0.15 mm, off-white and slightly translucent, and inserted into plant tissue. Larva: headless maggots up to 3 mm long when mature. First instar larvae are colourless when hatching but turn yellowish as they grow older. Later larval instars are yelloworangish. Third instars abandon the mine and usually burrow into the soil (a few centimetres deep) where a fourth and last non-feeding larval instar occurs. Petitt (1990) provided characters to distinguish the larval instars of L. sativae. www.efsa.europa.eu/efsajournal 12 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation Puparium: Elliptical, 1.5 9 0.75 mm, slightly ﬂattened ventrally, reddish-brown, located a few centimetres deep into the soil. • Identiﬁcation Morphological identiﬁcation: Because the morphological characters used to diagnose species are based on male genitalia (particularly the distiphallus, the terminal part of the aedeagus), adult males are needed in order to conﬁrm species identiﬁcation. There are no adequate keys for the species-level identiﬁcation of adult females (which are often identiﬁable with certainty to genus level only), eggs, larvae or pupae. Molecular identiﬁcation: Various polymerase chain reaction (PCR)-based molecular tests have been used to identify Liriomyza species, including PCR-restriction fragment length polymorphism (RFLP), endpoint PCR using species-speciﬁc primers, real-time PCR and DNA sequence comparison. Considering the speciﬁc limitations of molecular tests, a negative molecular test result does not exclude the possibility of positive identiﬁcation by morphological tests. In fact, it is advisable to combine morphology and molecular-based identiﬁcation methods for accurate species identiﬁcation. 3.2. Pest distribution 3.2.1. Pest distribution outside the EU Liriomyza sativae is endemic to the Americas. Although originally limited to this continent, it is now found in many areas of Africa, Asia and Oceania (Figure 1). It is not clear whether it may be present in the European part of Turkey. According to EPPO GD (2019), in Turkey, L. sativae is restricted to the regions of the Aegean and south east Anatolia. However, the original information dates from 2005 (C ß ıkman and Civelek, 2005). Figure 1: Global distribution map for Liriomyza sativae (extracted from the EPPO Global Database updated 30/01/2020 accessed on 17/2/2020) Appendix C shows the details about the worldwide pest presence and absence on the base of EPPO Global Database accessed on 17/11/2019. www.efsa.europa.eu/efsajournal 13 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation 3.2.2. Pest distribution in the EU Is the pest present in the EU territory? If present, is the pest widely distributed within the EU? No, L. sativae is not present in the EU territory (EPPO GD, 2019) 3.3. Regulatory status 3.3.1. Regulation 2016/2031 Liriomyza sativae is listed in Annex II of Commission Implementing Regulation (EU) 2019/20725 and of Regulation (EU) 2016/2031 of The European Parliament. Details are presented in Table 2. Table 2: Liriomyza sativae in Commission Implementing Regulation (EU) 2019/2072 Annex II List of Union quarantine pests and their respective codes Part A: Pests not known to occur in the Union territory Quarantine Pests and their codes assigned by EPPO C. Insects and mites 37. Liriomyza sativae Blanchard [LIRISA] 3.3.2. Legislation addressing the hosts of Liriomyza sativae Regulated hosts and commodities that may involve L. sativae in Annexes of Commission Implementing Regulation (EU) 2019/2072 are shown in Table 3. Table 3: Annex VII 8 5 List of plants, plant products and other objects, originating from third countries and the corresponding special requirements for their introduction into the Union territory in Commission Implementing Regulation (EU) 2019/2072 List of plants, plant products and other objects, originating from third countries and the corresponding special requirements for their introduction into the Union territory Plants, plant products and other objects CN codes* Origin Special requirements Plants for planting of herbaceous species, other than bulbs, corms, plants of the family Poaceae, rhizomes, seeds, tubers, and plants in tissue culture ex 0602 10 90 0602 90 20 ex 0602 90 30 ex 0602 90 50 ex 0602 90 70 ex 0602 90 91 ex 0602 90 99 ex 0704 10 00 ex 0704 90 10 ex 0704 90 90 ex 0705 11 00 ex 0705 19 00 ex 0705 21 00 ex 0705 29 00 ex 0706 90 10 ex 0709 40 00 ex 0709 99 10 ex 0910 99 31 ex 0910 99 33 Third countries where Liriomyza sativae (Blanchard) and (. . .) are known to occur Ofﬁcial statement that the plants have been grown in nurseries and: (a) originate in an area established by the national plant protection organisation in the country of origin as being free from Liriomyza sativae (Blanchard) (. . .) in accordance with relevant International Standards for Phytosanitary Measures which is mentioned on the phytosanitary certiﬁcate referred to in Article 71 of Regulation (EU) No 2016/2031, under the rubric ‘Additional declaration’, or (b) originate in a place of production, established by the national plant protection organisation of the country of origin as being free from Liriomyza sativae Commission Implementing Regulation (EU) 2019/2072 of 28 November 2019 establishing uniform conditions for the implementation of Regulation (EU) 2016/2031 of the European Parliament and the Council, as regards protective measures against pests of plants, and repealing Commission Regulation (EC) No 690/2008 and amending Commission Implementing Regulation (EU) 2018/2019. OJ L 319, 10.12.2019, p. 1–279. www.efsa.europa.eu/efsajournal 14 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation Annex VII List of plants, plant products and other objects, originating from third countries and the corresponding special requirements for their introduction into the Union territory (Blanchard) (. . .) in accordance with the relevant International Standards for Phytosanitary Measures, and which is mentioned on the phytosanitary certiﬁcate referred to in Article 71 of Regulation (EU) No 2016/2031, under the rubric ‘Additional declaration’, and declared free from Liriomyza sativae (Blanchard) (. . .) on ofﬁcial inspections carried out at least monthly during the three months prior to export, or (c) immediately prior to export, have been subjected to an appropriate treatment against Liriomyza sativae (Blanchard) (. . .) and have been ofﬁcially inspected and found free from Liriomyza sativae (Blanchard) (. . .). Details of the treatment referred in point (c) shall be mentioned on the phytosanitary certiﬁcate referred to in Article 71 of Regulation (EU) No 2016/2031 28 Cut ﬂowers of Chrysanthemum L., Dianthus L., Gypsophila L. and Solidago L., and leafy vegetables of Apium graveolens L. and Ocimum L. 0603 12 00 0603 14 00 ex 0603 19 70 0709 40 00 ex 0709 99 90 Third countries Ofﬁcial statement that the cut ﬂowers and the leafy vegetables: (a) originate in a country free from Liriomyza sativae (Blanchard) (. . .), or (b) immediately prior to their export, have been ofﬁcially inspected and found free from Liriomyza sativae (Blanchard) (. . .)). *: Further details on the CN codes is provided in Annex XI of Commission Implementing Regulation (EC) 2019/2072. 3.4. Entry, establishment and spread in the EU 3.4.1. Host range Liriomyza sativae is a highly polyphagous species, with more than 60 host plants in 18 different botanical families: Amaranthaceae, Apiaceae, Asteraceae, Brassicaceae, Caryophyllaceae, Chenopodiaceae, Convolvulaceae, Cucurbitaceae, Euphorbiaceae, Fabaceae, Lamiaceae, Liliaceae, Malvaceae, Moringaceae, Poaceae, Polemoniaceae, Solanaceae and Tropaeolaceae (Appendix A). Hosts include cultivated monocots (e.g. maize, sorghum) and dicots (e.g. potatoes, cabbages, sugar beet, melons), and ornamentals (e.g. dahlia, phlox), as well as plants considered as weeds in America (e.g. the nightshade, Solanum americanum and Spanish needles, Bidens alba). As a Union quarantine pest, its introduction into the EU is banned irrespective of the host plant. 3.4.2. Entry Is the pest able to enter into the EU territory? Yes, L. sativae has been repeatedly intercepted in different commodities entering into the EU. The main pathways are fruit and vegetables and cut ﬂowers and branches with foliage. Plants for planting can also constitute a pathway. www.efsa.europa.eu/efsajournal 15 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation Liriomyza sativae is a polyphagous species and its different life stages could use different pathways to enter the EU, as noted in Table 4. Table 4: Potential pathways for Liriomyza sativae and existing mitigations Pathways Life stage Plants for planting (excluding seeds) Eggs and larvae Cut ﬂowers and branches with foliage Eggs and larvae Fruits and vegetables Eggs and larvae Soil & growing media Pupae Hitchhiking adults Adults Relevant mitigations [e.g. prohibitions (Annex VI) or special requirements (Annex VII)] Annex VII applies only to Chrysanthemum, Dianthus, Gypsophila and Solidago other ornamental hosts exist such as Phlox and Dahlia Annex VII applies to Apium graveolens and Ocimum Annex VI of Commission Implementing Regulation 2019/2072 bans the introduction of soil and growing medium as such into the Union from third countries other than Switzerland Speciﬁc regulations apply to soil/growing medium attached to plants for planting for vitality The soil/growing medium pathway can be considered as closed, as import of soil/growing medium as such from third countries other than Switzerland is banned from entering into the EU (Annex VI). If necessary, for vitality, when attached to plants for planting, speciﬁc regulations are in place for import (Annex VII). With the implementation of the Plant Health Regulation (EC 2016/2031), consignments of almost all fruits and vegetables require a phytosanitary certiﬁcate indicating that they have been inspected and are free from harmful organisms before entry into the EU. 3.4.2.1. Interceptions There are 624 records of L. sativae interceptions in the Europhyt database between 1996 and November 2019 (accessed 17/11/2019). Most of these interceptions refer to basil (Ocimum spp.) (Figure 2) and to commodities imported from Thailand (Figure 3). L. sativae has been intercepted in many EU countries (Europhyt, 2019) because it is transported with plant material (Capinera, 2017). 56% of interceptions refer to fruit and vegetables (Europhyt classiﬁcation code 140), 39% to cut ﬂowers and branches with foliage (code 120). The remaining 5% corresponds to other living plants (codes !, 102, and 122). The number of interceptions substantially decreased between 1997 and 2003, and then again starting in 2009 (Figure 4). The average number of interceptions between 2009 and 2018 was 25.2 per year. However, without information on the number of inspections made, it is difﬁcult to interpret interception data. www.efsa.europa.eu/efsajournal 16 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation Apium graveolens Gypsophila sp. Ocimum americanum Ocimum basilicum Ocimum sp. Ocimum tenuiflorum Others Figure 2: Host plants where L. sativae was intercepted between 1996 and 2019 (n = 624). Hosts where the pest was intercepted less than 10 times have been grouped as ‘Others’. This category includes Amaranthus sp., Amaranthus viridis, Artemisia dracunculus, Brassica alboglabra, Brassica sp., Cassia sp., Cestrum sp., Chrysantemum sp., Coriandrum sativum, Dendranthema sp., Dianthus sp., Gypsophila sp., Ipomoea sp., Momordica charantia, Moringa oleifera, Solanum sp., Solidago sp., Spinacia sp., Trigonella sp. and Trigonella foenum-graecum Israel Laos Vietnam India Malaysia Others Kenya Suriname Kazakhstan Thailand Figure 3: Countries of origin of the commodity where L. sativae was intercepted between 1996 and 2019 (n = 624). Countries from which the pest was intercepted less than 10 times have been grouped as ‘Others’. This category includes Congo, Colombia, Dominican Republic, Ecuador, Egypt, Ethiopia, Ghana, Iran, Jordan, Sri Lanka, Morocco, Mexico, Nigeria, Pakistan, Tanzania and Uganda www.efsa.europa.eu/efsajournal 17 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation Figure 4: Annual number of interceptions of L. sativae between 1996 and 2019 (n = 624) 3.4.3. Establishment Is the pest able to become established in the EU territory? Yes, biotic and abiotic conditions are conducive for the establishment of L. sativae in some parts of the EU where potential hosts occur (either cultivated or not). 3.4.3.1. EU distribution of main host plants Many potential hosts of L. sativae (Appendix A) would be available to this insect in the EU. Because of the high polyphagy of this Dipteran, many crops widely grown in the EU, including those grown in glasshouses, could support the reproduction and immature development of this insect (Table 5). Table 5: EU 28 crop production (2014–2018) of the main host plants affected by Liriomyza sativae Crop 2014 2015 2016 2017 Brassicas : 273.77 273.01 279.90 2018 Lettuces Tomatoes 96.03 248.09 93.95 254.43 91.19 247.00 91.00 241.07 Cucumbers Gourds and pumpkins 37.31 : 33.51 : 32.43 : 31.91 : : : Muskmelons 76.46 73.73 73.27 72.60 : Watermelons 75.56 76.39 75.29 76.47 : : 88.33 243.44 ‘:’ data not available. 3.4.3.2. Climatic conditions affecting establishment The distribution of L. sativae in its native range in the Americas, extending from Canada to Argentina and Chile, covers a large area where all climate types also occurring in the EU can be found (Figure 5). Therefore, we assume that climatic conditions in the EU would not limit the ability of L. sativae to establish. www.efsa.europa.eu/efsajournal 18 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation €ppen–Geiger climate type zones (MacLeod and Korycinska, 2019). In its native range in Figure 5: Ko the Americas, L. sativae is established from Canada to Argentina and Chile (dotted rectangle), a zone including all climate types also occurring in the EU 3.4.4. Spread Is the pest able to spread within the EU territory following establishment? Yes, adults can ﬂy. However, L. sativae seems not to be a good ﬂyer. It can be passively dispersed by wind currents. RNQPs: Is spread mainly via speciﬁc plants for planting, rather than via natural spread or via movement of plant products or other objects? Yes, wide-scale and international spread of L. sativae seems to be mostly dependent on human-mediated movement of plants. As pointed out in Section 3.1.2, agromyzid ﬂies are not considered strong ﬂiers and tend to remain close to their host crops, only moving short distances between host plants. Although they can be passively dispersed over long distances by the wind (Malipatil et al., 2016), dispersal over long distances is attributed to human-assisted moving of infested host plant material (EPPO GD, 2019). 3.5. Impacts Would the pests’ introduction have an economic or environmental impact on the EU territory? Yes, the introduction of L. sativae would most probably have an economic impact in the EU through qualitative and quantitative effects on agricultural production. RNQPs: Does the presence of the pest on plants for planting have an economic impact, as regards the intended use of those plants for planting?6 Yes, should L. sativae be present in plants for planting, an economic impact on their intended use would be expected. According to CABI (2019), L. sativae is the most serious of the agromyzid pests, causing severe damage and loss of yield in many southern states of the US and also in South America. Damage to the 6 See Section 2.1 on what falls outside EFSA’s remit. www.efsa.europa.eu/efsajournal 19 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation plant is caused in several ways: (i) by the stippling that results from punctures made by females with their ovipositor for feeding on sap and laying eggs; (ii) by the internal mining by the larvae; (iii) by allowing microorganisms to enter the leaf through the feeding punctures and (iv) by mechanical transmission of some plant viruses (Malipatil et al., 2016). Young plants are particularly susceptible to damage and consequent reduced efﬁciency or death, while older plants may also be seriously damaged through leaf loss due to many mines occurring in each leaf (CABI, 2019). Losses of 80% have been reported for celery in Florida and up to 80% in lucerne in Argentina (Spencer, 1973b). 30– 60% yield increases were reported by Sharma et al. (1980), who studied the value of controlling this pest in squash in California. L. sativae is difﬁcult to eradicate because of its ability to survive in many weed plants which normally occur in areas adjacent to crop ﬁelds (CABI, 2019). Liriomyza sativae can mechanically transmit the Potyviridae Celery Mosaic Virus and Watermelon Mosaic Virus in experimental conditions (Zitter and Tsai, 1977). However, the same authors say that ‘the likelihood of achieving natural spread of potyviruses by leaf miners is at best remote’. Legislation does not address these viruses which are widespread and not regulated in the EU (EPPO GD, 2019). 3.6. Availability and limits of mitigation measures 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, the existing measures (see sections 3.3 and 3.4.2) can mitigate the risks of entry, establishment, and spread within the EU. As a pest listed in Annex IIA, its introduction and spread in the EU is banned irrespective of what it may be found on. RNQPs: Are there measures available to prevent pest presence on plants for planting such that the risk becomes mitigated? Yes, sourcing plants and plant parts from PFA would mitigate the risk. 3.6.1. Identiﬁcation of additional measures Phytosanitary measures are currently applied to soil. Some host plants are listed in the import prohibitions of Annex VI (e.g. Fragaria and Poaceae from speciﬁed third countries) or in speciﬁc requirements in Annex VII of Commission Implementing Regulation 2019/2072 (see Sections 3.3 and 3.4.2). 3.6.2. Additional control measures Potential additional control measures are listed in Table 6. Table 6: 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 Control measure summary information sheet if available) Risk component (entry/ establishment/ spread/impact) Entry, Growing plants in Description of possible exclusion conditions that could be isolation implemented to isolate the crop from pests and if applicable relevant establishment, spread, impact vectors, e.g. a dedicated structure such as greenhouses Crop rotation, associations and density, weed/ volunteer control Impact Crop rotation, associations and density, weed/volunteer control are used to prevent problems related to pests and are usually applied in various combinations to make the habitat less favourable for pests The measures deal with (1) allocation of crops to ﬁeld (over time and space) (multi-crop, diversity cropping) and (2) to control weeds and volunteers as hosts of pests/vectors Nitrogen level and reﬂective mulches are sometimes said to inﬂuence leaf miner populations, but responses have not been consistent (Chalfant et al., 1977; Hanna et al., 1987). Placement of row covers over cantaloupe has been reported to prevent damage by L. sativae (Orozco-Santos et al., 1995) www.efsa.europa.eu/efsajournal 20 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation Information sheet title (with hyperlink to Control measure summary information sheet if available) Heat and cold treatments Risk component (entry/ establishment/ spread/impact) Entry, spread, Controlled temperature treatments aimed to kill or inactivate pests impact without causing any unacceptable prejudice to the treated material itself. The measures addressed in this information sheet are: autoclaving; steam; hot water; hot air; cold treatment All stages are killed within a few weeks by cold storage at 0°C. Newly laid eggs are, however, the most resistant stage and it is recommended that cuttings of infested ornamental plants be maintained under normal glasshouse conditions for 3–4 days after lifting to allow eggs to hatch. Subsequent storage of the plants at 0°C for 1–2 weeks should then kill off the larvae of leaf miner species (Webb and Smith, 1970) Chemical treatments on crops including reproductive material Foliar application of insecticides is often frequent in susceptible crops. Impact Insecticide susceptibility varies greatly both spatially and temporally. Many insecticides are no longer effective. Insecticides are disruptive to naturally occurring biological control agents, and leaf miner outbreaks are sometimes reported to follow chemical insecticide treatment for other insects (Capinera, 2017) Resistant plants are used to restrict the growth and development of a Impact Use of resistant and tolerant plant speciﬁed pest and/or the damage they cause when compared to species/varieties susceptible plant varieties under similar environmental conditions and pest pressure It is important to distinguish resistant from tolerant species/varieties Some crops vary in susceptibility to leaf mining. This has been noted, e.g. in cultivars of tomato, cucumber, cantaloupe, and beans (Hanna et al., 1987). However, the differences tend to be moderate, and not adequate for reliable protection (Capinera, 2017) õBiological control The parasitoids of L. sativae are not speciﬁc (Capinera, 2017) and usually attack other (i.e. Coleoptera, Hymenoptera, Lepidoptera) and behavioural manipulation Impact 3.6.2.1. Additional supporting measures Potential additional supporting measures are listed in Table 7. Table 7: Selected supporting measures (a full list is available in EFSA PLH Panel et al., 2018) in relation to currently unregulated hosts and pathways. Supporting measures are organisational measures or procedures supporting the choice of appropriate risk reduction options that do not directly affect pest abundance Information sheet title (with Supporting measure summary hyperlink to information sheet if available) Inspection and trapping Risk component (entry/ establishment/ spread/impact) Inspection is deﬁned as the ofﬁcial visual examination of plants, plant Entry products or other regulated articles to determine if pests are present or to determine compliance with phytosanitary regulations (ISPM 5).The effectiveness of sampling and subsequent inspection to detect pests may be enhanced by including trapping and luring techniques Laboratory testing Examination, other than visual, to determine if pests are present using ofﬁcial diagnostic protocols. Diagnostic protocols describe the minimum requirements for reliable diagnosis of regulated pests www.efsa.europa.eu/efsajournal 21 Entry EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation Information sheet title (with hyperlink to Supporting measure summary information sheet if available) Risk component (entry/ establishment/ spread/impact) Certified and approved premises Entry Mandatory/voluntary certiﬁcation/approval of premises is a process including a set of procedures and of actions implemented by producers, conditioners and traders contributing to ensure the phytosanitary compliance of consignments. It can be a part of a larger system maintained by a National Plant Protection Organization in order to guarantee the fulﬁlment of plant health requirements of plants and plant products intended for trade. Key property of certiﬁed or approved premises is the traceability of activities and tasks (and their components) inherent the pursued phytosanitary objective. Traceability aims to provide access to all trustful pieces of information that may help to prove the compliance of consignments with phytosanitary requirements of importing countries Sampling According to ISPM 31, it is usually not feasible to inspect entire consignments, so phytosanitary inspection is performed mainly on samples obtained from a consignment. It is noted that the sampling concepts presented in this standard may also apply to other phytosanitary procedures, notably selection of units for testing. For inspection, testing and/or surveillance purposes the sample may be taken according to a statistically based or a non-statistical sampling methodology An ofﬁcial paper document or its ofﬁcial electronic equivalent, consistent with the model certiﬁcates of the IPPC, attesting that a consignment meets phytosanitary import requirements (ISPM 5) a) export certiﬁcate (import) b) plant passport (EU internal trade) To avoid the introduction of L. sativae EPPO (EPPO, 1990) recommends that propagating material (except seeds) of Capsicum, carnations, celery, chrysanthemums, Cucumis, Gerbera, Gypsophila, lettuces, Senecio hybridus and tomatoes from countries where the pest occurs must have been inspected at least every month during the previous 3 months and found free from the pests. A phytosanitary certiﬁcate should be required for cut ﬂowers and for vegetables with leaves. Phytosanitary certiﬁcate and plant passport Entry Entry Certiﬁcation of reproductive material (voluntary/ ofﬁcial) – Entry Surveillance – Entry 3.6.2.2. Biological or technical factors limiting the effectiveness of measures to prevent the entry, establishment and spread of the pest • • • • • Minute size of all developmental stages of L. sativae Mobility of adults Egg and larval stages within and protected by plant tissue Long pupal stage occurring in the soil Control with insecticides is usually complicated by the insect’s biology, including the ability of Liriomyza spp. to develop resistance to insecticides (Parrella, 1987). www.efsa.europa.eu/efsajournal 22 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation 3.6.2.3. Biological or technical factors limiting the ability to prevent the presence of the pest on plants for planting • • Fast development time High reproductive capability 3.7. Uncertainty There are no uncertainties affecting the conclusions of this pest categorisation. 4. Conclusions L. sativae satisﬁes the criteria that are within the remit of EFSA to assess for it to be regarded as a potential Union quarantine pest. L. sativae does not meet the criteria of occurring in the EU for it to be regarded as a potential Union regulated non-quarantine pest. Pest categorisation’s conclusions are presented in the Table 8. Table 8: 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) 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 Identity of the pests (Section 3.1) The identity of Liriomyza sativae is well established and there are taxonomic keys available for its identiﬁcation to species level The identity of Liriomyza sativae is well established and there are taxonomic keys available for its identiﬁcation to species level Absence/presence of the pest in the EU territory (Section 3.2) Regulatory status (Section 3.3) L. sativae is not present in the EU L. sativae is not present in the EU. Therefore, it does not fulﬁl this criterion to be regulated as a RNQP The pest is listed in Annex IIA Commission Implementing Regulation (EU) 2019/2072 There are no grounds to consider its status as a quarantine pest is to be revoked Pest potential for entry, establishment and spread in the EU territory (Section 3.4) L. sativae could enter into, become established in, and spread within, the EU territory. The main pathways are: Fresh leafy hosts for consumption, cut branches, fruit and ﬂowers with foliage, leafy plants for planting The pests’ introduction would most probably have an economic impact in the EU Although adults can ﬂy, natural spread is not considered its main dispersal mode but human-assisted transport (including plants for planting) There are measures available to prevent the entry into, establishment within or spread of the pest within the EU (i.e. sourcing plants from PFA) All criteria assessed by EFSA above for consideration as a potential quarantine pest are met with no uncertainties There are measures available to prevent pest presence on plants for planting (i.e. sourcing plants from PFA, PFPP) Criterion of pest categorisation Potential for consequences in the EU territory (Section 3.5) Available measures (Section 3.6) Conclusion on pest categorisation (Section 4) www.efsa.europa.eu/efsajournal Key uncertainties Should L. sativae be present on plants for planting, an economic impact on its intended use would be expected Although the criterion of plants for planting being the main means of spread for consideration as a RNQP is met, the criterion of the pest being present in the EU territory, which is a prerequisite for consideration as a potential RNQP, is not met 23 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation Criterion of pest categorisation Aspects of assessment to focus on/ scenarios to address in future if appropriate 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 None References CABI, 2019. Invasive species compendium. Avilable online: https://www.cabi.org/isc/datasheet/30960 [Accessed: 19 Novrmber 2019] Capinera JL, 2017. Featured Creatures: Liriomyza sativae Blanchard (Insecta: Dipetra: Agromyzidae). Available online: http://entnemdept.ufl.edu/creatures/veg/leaf/vegetable_leafminer.htm [Accessed: 21 Novemeber 2019]. Chalfant RB, Jaworski CA, Johnson AW and Summer DR, 1977. Reﬂective ﬁlm mulches, millet barriers, and pesticides: effects on watermelon mosaic virus, insects, nematodes, soil-borne fungi, and yield of yellow summer squash. Journal of the American Society of Horticultural Science, 102, 11–15. C ß ıkman E and Civelek HS, 2005. Contributions to the leaf miner fauna from Turkey, with four new records. Phytoparasitica, 33, 391–396. 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, 1990. Speciﬁc quarantine requirements. EPPO Technical Documents No. 1008. EPPO, 2005. Data sheets on Quarantine Pests. Liriomyza sativae. EPPO, 2019a. EPPO codes. Available online: https://www.eppo.int/RESOURCES/eppo_databases/eppo_codes EPPO, 2019b. How to use the EPPO Global Database?. Available online: https://gd.eppo.int/media/files/general_ user-guide_2019_09.pdf EPPO (European and Mediterranean Plant Protection Organization), online. EPPO Global Database. Available online: https://gd.eppo.int [Accessed: 09 January 2019]. 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), 2016. ISPM (International standards for phytosanitary measures) No 27. Diagnostic protocols for regulated pests. DP 16: Genus Liriomyza. Available online: https://www.ippc.int/static/media/ﬁles/publication/en/2017/01/DP_16_2016_En_2017-01-30.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/ Griessinger D and Roy AS, 2015. EPPO codes: a brief description. Available online: https://www.eppo.int/media/ uploaded_images/RESOURCES/eppo_databases/A4_EPPO_Codes_2018.pdf Hanna HY, Story RN and Adams AJ, 1987. Inﬂuence of cultivar, nitrogen, and frequency of insecticide application on vegetable leaf miner (Diptera: Agromyzidae) population density and dispersion on snap beans. Journal of Economic Entomology, 80, 107–110. de Jong Y, Verbeek M, Michelsen V, De Place Bjørn P, Los W, Steeman F, Bailly N, Basire C, Chylarecki P, Stloukal E, €ckler F, Kroupa A, Korb G, Hoffmann A, Ha €user C, Kohlbecker A, Mu €ller A, Gu €ntsch Hagedorn G, Wetzel FT, Glo A, Stoev P and Penev L, 2014. Fauna Europaea - all European animal species on the web. Biodiversity Data Journal, 2, e4034. https://doi.org/10.3897/BDJ.2.e4034. Available at https://fauna-eu.org/ [Accessed: 20 November 2019]. www.efsa.europa.eu/efsajournal 24 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation Kang L, Chen B, Wei JN and Liu TX, 2009. Roles of thermal adaptation and chemical ecology in Liriomyza distribution and control. Annual Review of Entomology, 54, 127–145. Leibee GL, 1982. Development of Liriomyza trifolii on celery. In: Schuster DJ (ed.). Proceedings of IFAS-Industry na Vista, Florida. pp. 35–41. Conference on Biology and Control of Liriomyza leaf miners. Lake Bue MacLeod A and Korycinska A, 2019. Detailing Koppen-Geiger climate zones at a country and regional level: a resource for pest risk analysis. EPPO Bulletin, 49, 73–82. Malipatil M, Blacket M, Wainer J, Ridland P and Reviewer Jones DC (Subcommittee on Plant Health Diagnostics), 2016. National Diagnostic Protocol for Liriomyza trifolii– NDP27 V1. Available online: http://plantbiosecuritydia gnostics.net.au/resource-hub/priority-pest-diagnostic-resources/ [Accessed: 21 November 2019]. Oatman ER and Michelbacher AE, 1959. The melon leaf miner Liriomyza pictella (Thomson) (Diptera: Agromyzidae).II. Ecological studies.. Journal of Economic Entomology, 52, 83–89. Orozco-Santos M, Perez-Zamora O and Lopez-Arriaga O, 1995. Floating row cover and transparent mulch to reduce insect populations, virus diseases and increase yield in cantaloupe. Florida Entomologist, 78, 493–501. Parrella MP, 1987. Biology of Liriomyza. Annual Review of Entomology, 32, 201–224. Parrella MP, Robb KL and Bethke JA, 1981. Oviposition and pupation of Liriomyza trifolii (Burgess). See Ref., 87, 5a–55. Petitt FL, 1990. Distinguishing larval instars of the vegetable leaf miner Liriomyza sativae (Diptera: Agromyzidae). Florida Entomologist, 73, 280–286. Scheffer SJ and Lewis ML, 2005. Mitochondrial phylogeography of vegetable pest Liriomyza sativae (Diptera: Agromyzidae): Divergent clades and invasive populations. Annals of the Entomological Society of America, 98, 181–186. Seymour PR, 1994. Taxonomy and morphological identiﬁcation. 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Journal of Economic Entomology, 63, 1359–1361. Zhao YX and Kang L, 2000. Cold tolerance of the leaf miner Liriomyza sativae (Dipt., Agromyzidae). Journal of Applied Entomology, 124, 185–189. Zitter TA and Tsai JH, 1977. Transmission of three potyviruses by the leaf miner Liriomyza sativae (Diptera: Agromyzidae). Plant Disease Reporter, 61, 1025–1029. Abbreviations EPPO FAO IPPC ISPM MS PCR PLH PZ RFLP RNQP TFEU ToR European and Mediterranean Plant Protection Organization Food and Agriculture Organization International Plant Protection Convention International Standards for Phytosanitary Measures Member State polymerase chain reaction EFSA Panel on Plant Health Protected Zone Restriction fragment length polymorphism Regulated non-quarantine pest Treaty on the Functioning of the European Union Terms of Reference Glossary Containment (of a pest) Control (of a pest) www.efsa.europa.eu/efsajournal Application of phytosanitary measures in and around an infested area to prevent spread of a pest (FAO, 1995, 2017) Suppression, containment or eradication of a pest population (FAO, 1995, 2017) 25 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation Entry (of a pest) Eradication (of a pest) Establishment (of a pest) Greenhouse Impact (of a pest) Introduction (of a pest) Measures Pathway Phytosanitary measures Protected zones (PZ) Quarantine pest Regulated non-quarantine pest Risk reduction option (RRO) Spread (of a pest) www.efsa.europa.eu/efsajournal 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) Application of phytosanitary measures to eliminate a pest from an area (FAO, 2017) Perpetuation, for the foreseeable future, of a pest within an area after entry (FAO, 2017) The term ‘greenhouse’ is used in the current opinion as deﬁned by EPPO (https://gd.eppo.int/taxon/3GREEL) as a walk-in, static, closed place of crop production with a usually translucent outer shell, which allows controlled exchange of material and energy with the surroundings and prevents release of plant protection products (PPPs) into the environment. A similar deﬁnition is also given in EFSA Guidance Document on protected crops (2014) https://efsa.onlinelib rary.wiley.com/doi/epdf/10.2903/j.efsa.2014.3615 The impact of the pest on the crop output and quality and on the environment in the occupied spatial units The entry of a pest resulting in its establishment (FAO, 2017) 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 Any means that allows the entry or spread of a pest (FAO, 2017) 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) 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 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) 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) 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 Expansion of the geographical distribution of a pest within an area (FAO, 2017) 26 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation Appendix A – Host plants for Liriomyza sativae. EPPO GD (accessed 17/11/2019) CABI (accessed 17/11/2019) Other sources Host plant Family Abelmoschus esculentus (okra) Malvaceae Main Allium Liliaceae Amaranthaceae Main Other Amaranthus Amaranthus viridis Amaranthaceae Amaranthaceae Wild/Weed Apium graveolens (celery) Arachis hypogaea (groundnut) Apiaceae Fabaceae Minor Artemisia dracunculus Asteraceae Aster Asteraceae Other Beta vulgaris var. saccharifera (sugar beet) Bidens alba Chenopodiaceae Main Asteraceae Weed (Capinera, 2017) Brassica alboglabra Brassicaceae Europhyt (this opinion) Brassica oleracea (cabbages, cauliﬂowers) Brassicaceae Main Brassica rapa cultivar group Mizuna Brassicaceae Brassica rapa subsp. rapa (turnip) Brassicaceae Main Main Europhyt (this opinion) Main Main Europhyt (this opinion) Main Cajanus cajan (pigeon pea) Brassicaceae (cruciferous crops) Fabaceae Main Capsicum (peppers) Capsicum annuum (bell pepper) Solanaceae Solanaceae Main Main Cassia sp. Fabaceae Minor Europhyt (this opinion) Cestrum (jessamine) Solanaceae Chrysanthemum Asteraceae Cicer arietinum (chickpea) Fabaceae Other Citrullus lanatus (watermelon) Coriandrum sativum Cucurbitaceae Apiaceae Main Cucumis Cucumis melo (melon) Cucurbitaceae Cucurbitaceae Minor Minor Cucumis sativus (cucumber) Cucurbita (pumpkin) Cucurbitaceae Cucurbitaceae Minor Cucurbita maxima (giant pumpkin) Cucurbita pepo (marrow) Cucurbitaceae Cucurbitaceae Dahlia hybrids Cucurbitaceae (cucurbits) Asteraceae Dahlia pinnata (garden dahlia) Datura (thorn-apple) Asteraceae Solanaceae Daucus carota (carrot) Dendranthema x grandiﬂorum Apiaceae Asteraceae www.efsa.europa.eu/efsajournal Other Europhyt (this opinion) Europhyt (this opinion) Major Main Main Main Main Main Main Minor Other Other Main Minor 27 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation Host plant Family Dendranthema x grandiﬂorum Asteraceae Fabaceae (leguminous plants) EPPO GD (accessed 17/11/2019) CABI (accessed 17/11/2019) Minor Minor Main Dianthus sp. Caryophyllaceae Gypsophila sp. Caryophyllaceae Gossypium (cotton) herbaceous ornamental plants Malvaceae Indigofera (indigo) Ipomoea sp. Fabaceae Convolvulaceae Other Lactuca sativa (lettuce) Lathyrus Asteraceae Fabaceae Minor Main Other Lathyrus odoratus (sweet pea) Medicago sativa (lucerne) Fabaceae Fabaceae Minor Main Main Melilotus (melilots) Momordica charantia Fabaceae Cucurbitaceae Moringa oleifera Moringaceae Europhyt (this opinion) Europhyt (this opinion) Main Minor Europhyt (this opinion) Other Europhyt (this opinion) Europhyt (this opinion) Nicotiana tabacum (tobacco) Solanaceae Main Ocimum basilicum (basil) Phaseolus (beans) Lamiaceae Fabaceae Main Main Phaseolus lunatus Phaseolus vulgaris (common bean) Fabaceae Fabaceae Phlox Physalis (Groundcherry) Polemoniaceae Solanaceae Pisum (pea) Pisum sativum (pea) Fabaceae Fabaceae Minor Main Main Raphanus sativus (radish) Ricinus communis (castor bean) Brassicaceae Euphorbiaceae Minor Main Other Minor Main Solanum americanum Solanaceae Solanaceae Solanum lycopersicum (tomato) Solanum melongena (aubergine) Solanaceae Solanaceae Major Minor Main Main Solanum tuberosum (potato) Solidago sp. Solanaceae Asteraceae Major Main Sorghum bicolor Spinacia oleracea (spinach) Poaceae Chenopodiaceae Minor Minor Symphyotrichum novi-belgii Trifolium (clovers) Asteraceae Fabaceae Minor Trigonella foenum-graecum Fabaceae Trigonella sp. Fabaceae Tropaeolum majus Tropaeolaceae www.efsa.europa.eu/efsajournal Other sources Minor Minor Main Other Other Weed (Capinera, 2017) Europhyt (this opinion) Main Main Europhyt (this opinion) Europhyt (this opinion) Incidental 28 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation Family EPPO GD (accessed 17/11/2019) Vicia faba Vigna (cowpea) Fabaceae Fabaceae Minor Minor Zea mays (maize) Poaceae Host plant Vegetable plants www.efsa.europa.eu/efsajournal CABI (accessed 17/11/2019) Other sources Minor Main Main 29 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation Appendix B – EU member state production of some L. sativae hosts EU28 crop production in standard humidity Eurostat (Area (cultivation/harvested/production) (1,000 ha) (accessed 11.11.2019) Brassicas Area\year European Union – 28 countries 2014 2015 2016 2017 2018 : 273.77 273.01 279.9 : Austria Belgium 1.76 8.58 1.64 8.73 1.57 8.98 1.53 9.82 1.44 9.58 Bulgaria Croatia : 0.94 2.11 1.66 3.03 1.67 1.85 2.13 2.13 1.98 Cyprus Czech Republic 0.13 1.68 0.12 1.71 0.14 1.77 0.15 1.64 0.16 1.47 Denmark Estonia : 0.3 1.65 0.3 1.87 0.28 2.07 0.29 2.18 0.38 Finland France 1.27 26.89 1.22 26.09 1.21 26.23 1.49 26.39 1.46 26 Germany Greece 19.53 9.73 18.7 7.15 18.8 6.32 20.09 5.89 18.84 6.22 Hungary Ireland 4.46 1.9 4.37 1.9 4.43 1.82 4.24 1.68 3.55 1.78 Italy Latvia : 0.9 30.26 1 29.74 0.8 29.81 0.6 : 0.7 Lithuania Luxembourg 2.41 0 2.04 0.01 2.22 0.01 1.99 0.01 2.16 0.03 Malta Netherlands 0 10.08 0 9.65 0 10.27 0 11.14 0 10.85 Poland Portugal 43.3 10.57 44 8.71 39.98 10.17 40.69 9.35 41.58 9.47 Romania Slovakia 31.45 0 32.41 0.55 30.76 0.6 30.9 0.51 32.08 0.44 Slovenia Spain : : 0.91 38.84 0.97 42.16 0.97 45.98 0.94 46.99 Sweden 1.18 1.18 1.2 1.4 1.38 27 26.88 26 27.3 25.6 United Kingdom : data not available. Lettuces Area\year 2014 2015 2016 2017 2018 European Union – 28 Austria 96.03 1.41 93.95 1.32 91.19 1.45 91 1.39 : 1.31 Belgium Bulgaria 1.25 0.29 1.33 0.18 1.29 0.12 1.28 0.29 1.18 0.24 Croatia Cyprus 0.1 0.08 0.2 0.15 0.28 0.28 0.2 0.19 0.25 0.18 Czech Republic Denmark 0.18 0.67 0.14 0.61 0.15 0.42 0.59 0.56 0.62 0.53 Estonia Finland 0 0.65 0 0.65 0 0.7 0 0.59 0 0.67 France 8.96 8.84 8.86 8.6 8.43 www.efsa.europa.eu/efsajournal 30 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation Area\year 2014 2015 2016 2017 2018 Germany 6.7 6.56 6.5 7.09 6.93 Greece Hungary 4.76 0.31 3.67 0.37 3.56 0.4 3.29 0.34 3.31 0.28 Ireland Italy 0.3 19.78 0.3 18.58 0.31 15.67 0.26 15.66 0.26 : Latvia Lithuania 0 0.22 0 0.24 0 0.27 0 0.24 0 0.25 Luxembourg Malta 0.01 0 0.01 0 0.02 0 0.02 0 0.02 0 Netherlands Poland 3.51 1.7 3.48 1.8 3.52 2.31 3.45 2.78 3.35 2.53 Portugal Romania 2.42 0.15 2.15 0.16 2.18 0.15 2.28 0.14 1.93 0.15 Slovakia Slovenia 0.2 0.67 0.04 0.73 0.02 0.75 0.02 0.74 0.01 0.71 Spain Sweden 33.87 1.85 34.31 1.71 35.65 1.63 34.51 1.7 33.67 1.81 6 6.43 4.7 4.8 4.8 United Kingdom : data not available. Tomatoes Area\Year 2014 2015 2016 2017 2018 248.09 254.43 247 241.07 243.44 Austria Belgium 0.19 0.51 0.19 0.51 0.18 0.51 0.18 0.52 0.2 0.55 Bulgaria Croatia 3.59 0.32 3.28 0.42 4.2 0.37 5.01 0.45 4.52 0.49 Cyprus Czech Republic 0.21 0.28 0.27 0.2 0.22 0.34 0.26 0.24 0.26 0.3 Denmark Estonia 0.04 0 0.03 0 0.03 0.01 0.03 0 0.03 0 248.09 0.11 254.43 0.11 247 0.11 241.07 0.11 243.44 0.1 France Germany 5.83 0.33 5.69 0.33 5.65 0.34 5.75 0.37 5.74 0.4 Greece Hungary 17.26 1.88 15.25 2.26 14.01 2.08 13.32 2.19 16.02 2.5 0.01 103.11 0.01 107.18 0.01 96.78 0.01 92.67 0.01 100.9 0 0.54 0 0.49 0 0.57 0 0.55 0 0.57 Luxembourg Malta 0 0 0 0 0 0 0 0 0 0 Netherlands Poland 1.78 13.5 1.76 13.8 1.78 12.42 1.79 12.64 1.79 13.11 Portugal Romania 18.46 24.43 18.66 24.84 20.85 22.71 20.87 22.21 15.83 22.97 Slovakia Slovenia 0.51 0.23 0.57 0.19 0.68 0.21 0.6 0.2 0.59 0.19 European Union – 28 countries European Union – 28 countries Finland Ireland Italy Latvia Lithuania www.efsa.europa.eu/efsajournal 31 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation Area\Year 2014 2015 2016 2017 2018 Spain Sweden 54.75 0.04 58.13 0.04 62.72 0.04 60.85 0.04 56.13 0.04 0.2 0.23 0.2 0.2 0.18 2018 United Kingdom : data not available. Cucumbers Area\year 2014 2015 2016 2017 European Union – 28 37.31 33.51 32.43 31.91 : Austria Belgium 0.21 0.04 0.21 0.04 0.19 0.06 0.19 0.06 0.2 0.06 Bulgaria Croatia 0.73 0.14 0.71 0.13 0.73 0.16 0.67 0.11 0.93 0.09 Cyprus Czech Republic 0.22 0.05 0.2 0.03 0.2 0.05 0.19 0.04 0.19 0.05 Denmark Estonia 0.05 0.1 0.05 0.1 0.05 0.09 0.04 0.1 0.04 0.1 Finland France 0.96 1.56 0.09 1.56 0.08 1.64 0.08 1.71 0.1 1.68 Germany Greece 0.33 2.34 0.34 1.85 0.37 1.85 0.37 1.88 0.39 1.89 Hungary Ireland 0.23 0.01 0.25 0.01 0.4 0.01 0.38 0.01 0.31 0.01 Italy Latvia 2.02 0.1 1.89 0.1 1.84 0 1.79 0.1 : 0.1 Lithuania Luxembourg 1.17 0 0.96 0 1.13 0 1.08 0 1.11 0 Malta Netherlands 0 0.6 0 0.55 0 0.54 0 0.6 0 0.59 Poland Portugal 10.6 0.19 10.1 0.22 9.49 0.13 9.19 0.11 9.17 0.13 Romania Slovakia 6.44 0.05 5.73 0.05 5.7 0.05 5.44 0.05 6.04 0.05 Slovenia Spain 0.08 8.9 0.06 8.1 0.06 7.44 0.06 7.48 0.06 7.5 Sweden 0.08 0.09 0.09 0.08 0.09 United Kingdom 0.1 0.1 0.1 0.1 0.1 2014 2015 2016 2017 2018 European Union – 28 Austria : 0.5 : 0.5 : 0.55 : 0.6 : 0.7 Belgium Bulgaria 0.21 0 0.3 2.44 0.51 11.76 0.51 1.87 0.46 1.57 Croatia Cyprus 0.09 0 0.27 0 0.16 0 0.21 0 0.14 0 Czech Republic Denmark 0 0 0 0 0 0 0 0 0 0 Estonia 0 0 0 0 0 : data not available. Gourds and pumpkins Area\year www.efsa.europa.eu/efsajournal 32 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation Area\year 2014 2015 2016 2017 2018 Finland 0.01 0.01 0.02 0.03 0.04 France Germany 3.85 3.23 3.83 3.49 4.08 3.99 4.31 4.48 4.21 4.15 Greece Hungary 0 0.96 0 0.73 0 1.17 0 1.39 0 1.54 0 : 0 : 0 0 0 0 0 : 0.1 0.1 0.2 0.1 0.2 0.13 0.1 0.22 0.1 0.21 Luxembourg Malta 0 0 0 0 0.01 0 0.02 0 0.01 0 Netherlands Poland 0.29 1.1 0.82 1.3 0.82 1.34 0.93 1.66 0.76 1.69 Portugal Romania 3.25 3.36 3.06 2.46 2.94 1.29 2.95 1.18 2.86 1.23 Slovakia Slovenia 0 : 2.25 : 2.87 : 0.67 : 0.21 : Spain Sweden 2 0.12 2.89 0.12 3.17 0.12 3.74 0.19 4.05 0.2 0 0 0 0 0 Ireland Italy Latvia Lithuania United Kingdom : data not available. Muskmelons Area\time 2014 2015 2016 2017 European Union – 28 countries 2018 76.46 73.73 73.27 72.6 : Austria Belgium 0.02 0 0.02 0 0.02 0 0.02 0 0.03 0 Bulgaria Croatia 0.48 0.1 0.66 0.11 1.75 0.17 2.67 0.15 2.77 0.22 Cyprus Czech Republic 0.14 0 0.17 0 0.15 0 0.15 0 0.15 0 0 0 0 0 0 0 0 0 0 0 Finland France 0 14.1 0 14.02 0 14.17 0 14.16 0 13.41 Germany Greece 0 4.72 0 4.22 0 3.91 0 4.03 0 3.74 Hungary Ireland 0.59 0 0.8 0 0.83 0 0.64 0 0.57 0 Italy Latvia 25.03 0 24.8 0 24.72 0 24.17 0 : 0 Lithuania Luxembourg 0 0 0 0 0 0 0 0 0 0 Malta Netherlands 0 0 0 0 0 0 0 0 0 0 Poland Portugal 0 3.26 0 2.56 0 2.08 0 1.84 0 1.94 Romania Slovakia 4.19 0.04 4.18 0.04 4.73 0.04 4.26 0.03 4.26 0.01 Denmark Estonia www.efsa.europa.eu/efsajournal 33 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation Area\time 2014 2015 2016 2017 2018 Slovenia Spain 0 23.79 0.01 22.14 0.02 20.69 0.01 20.47 0.01 19.03 Sweden 0 0 0 0 0 United Kingdom 0 0 0 0 0 Area\Year 2014 2015 2016 2017 2018 European Union – 28 countries Austria 75.56 0 76.39 0 75.29 0 76.47 0 : 0 Belgium Bulgaria 0 2.86 0 3.21 0 4.74 0 4.82 0 4.32 Croatia Cyprus 0.69 0.6 0.61 0.53 0.68 0.47 0.68 0.44 0.97 0.43 Czech Republic Denmark 0 0 0 0 0 0 0 0 0 0 Estonia Finland 0 0 0 0 0 0 0 0 0 0 France Germany 0.8 0 0.89 0 0.91 0 0.93 0 0.94 0 Greece Hungary 12.54 6.12 11.41 6.02 10.76 5.41 11.13 5.27 9.62 5.09 Ireland Italy 0 11.42 0 11.58 0 12.01 0 12.84 0 : Latvia Lithuania 0 0 0 0 0 0 0 0 0 0 Luxembourg Malta 0 0 0 0 0 0 0 0 0 0 Netherlands Poland 0 0 0 0 0 0 0 0 0 0 Portugal Romania 0.87 21.55 1.05 21.81 1.11 19.9 1.11 19.09 0.93 17.8 Slovakia Slovenia 0.15 0 0.12 0.03 0.14 0.02 0.12 0.01 0.06 0.01 Spain Sweden 17.95 0 19.15 0 19.16 0 20.03 0 20.4 0 0 0 0 0 0 : data not available. Watermelons United Kingdom : data not available. www.efsa.europa.eu/efsajournal 34 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation Appendix C – Detailed global distribution of Liriomyza sativae on the base of EPPO Global Database Continent Country Africa Cameroon Present, no details Congo Egypt Absent, unreliable record Present, no details Ethiopia Kenya Absent, unreliable record Present, no details Morocco Nigeria Absent, unreliable record Present, no details South Africa Sudan Absent, unreliable record Present, no details Tanzania Uganda Absent, unreliable record Absent, unreliable record Zimbabwe Antigua and Barbuda Present, restricted distribution Present, no details Argentina Bahamas Present, widespread Present, restricted distribution Barbados Brazil Present, restricted distribution Present, restricted distribution Americas State Status Ceara Parana Present, no details Present, no details Pernambuco Rio de Janeiro Present, no details Present, no details Rio Grande do Norte Present, no details Present, restricted distribution Ontario Chile Present, no details Present, restricted distribution Colombia Costa Rica Present, restricted distribution Present, no details Cuba Dominica Present, no details Present, no details Dominican Republic French Guiana Present, no details Present, no details Guadeloupe Jamaica Present, no details Present, restricted distribution Martinique Mexico Present, widespread Present, no details Montserrat Netherlands Antilles Present, no details Present, no details Nicaragua Panama Present, no details Present, no details Peru Puerto Rico Present, restricted distribution Present, no details Saint Lucia St Kitts-Nevis Present, no details Present, no details St Vincent and the Grenadines Suriname Present, widespread Absent, unreliable record Trinidad and Tobago Present, no details Canada www.efsa.europa.eu/efsajournal 35 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation Continent Country State United States of America Asia Status Present, restricted distribution Alabama Arizona Present, no details Present, no details Arkansas California Present, no details Present, no details Florida Georgia Present, no details Present, no details Hawaii Indiana Present, no details Present, no details Louisiana Maryland Present, no details Present, no details New Jersey Ohio Present, no details Present, no details Pennsylvania South Carolina Present, no details Present, no details Tennessee Texas Present, no details Present, no details Venezuela Bangladesh Present, restricted distribution Present, widespread Cambodia China Absent, unreliable record Present, widespread Anhui Fujian Present, no details Present, no details Guangdong Hainan Present, no details Present, no details Hebei Henan Present, no details Present, no details Hunan Shanxi Present, no details Present, no details Sichuan Yunnan Present, no details Present, no details Zhejiang Present, no details Present, restricted distribution Uttar Pradesh Present, no details Present, no details Java Iran Present, no details Present, widespread Israel Japan Present, no details Present, restricted distribution India Indonesia Honshu Kyushu Present, restricted distribution Present, restricted distribution Ryukyu Archipelago Jordan Present, restricted distribution Present, no details Lao Malaysia Absent, unreliable record Present, no details West Oman Present, no details Present, no details Pakistan Sri Lanka Present, no details Present, no details www.efsa.europa.eu/efsajournal 36 EFSA Journal 2020;18(3):6037 Liriomyza sativae: Pest categorisation Continent Europe Oceania Country State Status Thailand Uzbekistan Present, restricted distribution Present, restricted distribution Viet Nam Yemen Present, widespread Present, few occurrences Belgium Croatia Absent, intercepted only Absent, conﬁrmed by survey Estonia Finland Absent, conﬁrmed by survey Absent, intercepted only Lithuania Netherlands Absent, conﬁrmed by survey Absent, conﬁrmed by survey Poland Slovenia Absent, invalid record Absent, no pest record Turkey* United Kingdom Present, restricted distribution Absent, intercepted only American Samoa Australia Present, widespread Present, restricted distribution Queensland Cook Islands Present, restricted distribution Present, restricted distribution French Polynesia Guam Present, no details Present, restricted distribution Micronesia New Caledonia Present, no details Present, restricted distribution Northern Mariana Islands Samoa Present, no details Present, widespread Vanuatu Present, no details *: Although Turkey is included in Europe, L. sativae has been reported only from Asian locations see Section 3.2.1. www.efsa.europa.eu/efsajournal 37 EFSA Journal 2020;18(3):6037

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