Volume 22, Issue 3 e8657
SCIENTIFIC OPINION
Open Access

Commodity risk assessment of Cornus alba and Cornus sanguinea plants from the UK

EFSA Panel on Plant Health (PLH)

Corresponding Author

EFSA Panel on Plant Health (PLH)

Correspondence:[email protected]Search for more papers by this author
Claude BragardPaula BaptistaElisavet Chatzivassiliou

Elisavet Chatzivassiliou

Search for more papers by this author
Francesco Di SerioPaolo GonthierJosep Anton Jaques Miret

Josep Anton Jaques Miret

Search for more papers by this author
Annemarie Fejer Justesen

Annemarie Fejer Justesen

Search for more papers by this author
Alan MacLeodChrister Sven MagnussonPanagiotis MilonasJuan A. Navas-CortesStephen ParnellPhilippe Lucien Reignault

Philippe Lucien Reignault

Search for more papers by this author
Emilio StefaniHans-Hermann ThulkeWopke Van der WerfAntonio Vicent CiveraJonathan YuenLucia ZappalàRaghavendra Reddy MandaOlaf Mosbach SchulzParaskevi KariampaAntigoni AkrivouSpyridon AntonatosDespoina BerisJane DebodeChristos KritikosMaria KormpiCharles ManceauDimitrios PapachristosChrysavgi ReppaCiro GardiRoel Potting
First published: 12 March 2024
Adopted: 1 February 2024
Appendix C is available under the  Supporting Information section.

Abstract

The European Commission requested the EFSA Panel on Plant Health to prepare and deliver risk assessments for commodities listed in Commission Implementing Regulation (EU) 2018/2019 as ‘high risk plants, plant products and other objects’. Taking into account the available scientific information, including the technical information provided by the applicant country, this Scientific Opinion covers the plant health risks posed by the following commodities: Cornus alba and Cornus sanguinea bare-root plants and rooted plants in pots up to 7 years old imported into the EU from the UK. A list of pests potentially associated with the commodities was compiled. The relevance of any pest was assessed based on evidence following defined criteria. Four EU quarantine pests (Meloidogyne fallax, Phytophthora ramorum (non-EU isolates), tobacco ringspot virus, and tomato ringspot virus) and one EU non-regulated pest (Discula destructiva), were selected for further evaluation. For the selected pests, the risk mitigation measures implemented in the technical dossier from the UK were evaluated taking into account the possible limiting factors. For these pests, an expert judgement is given on the likelihood of pest freedom taking into consideration the risk mitigation measures acting on the pest, including uncertainties associated with the assessment. The degree of pest freedom varies among the pests evaluated, with P. ramorum being the pest most frequently expected on the imported C. alba and C. sanguinea plants. The Expert Knowledge Elicitation indicated, with 95% certainty, that between 9823 and 10,000 bare-root C. alba and C. sanguinea plants per 10,000 will be free from P. ramorum.

1 INTRODUCTION

1.1 Background and Terms of Reference as provided by European Commission

1.1.1 Background

The Plant Health Regulation (EU) 2016/2031,1 on the protective measures against pests of plants, has been applied from December 2019. Provisions within the above Regulation are in place for the listing of ‘high risk plants, plant products and other objects’ (Article 42) on the basis of a preliminary assessment, and to be followed by a commodity risk assessment. A list of ‘high risk plants, plant products and other objects’ has been published in Regulation (EU) 2018/2019.2 Scientific Opinions are therefore needed to support the European Commission and the Member States in the work connected to Article 42 of Regulation (EU) 2016/2031, as stipulated in the terms of reference.

1.1.2 Terms of Reference

In view of the above and in accordance with Article 29 of Regulation (EC) No 178/2002,3 the Commission asks EFSA to provide Scientific Opinions in the field of plant health.

In particular, EFSA is expected to prepare and deliver risk assessments for commodities listed in the relevant Implementing Act as ‘high risk plants, plant products and other objects’. Article 42, paragraphs 4 and 5, establishes that a risk assessment is needed as a follow-up to evaluate whether the commodities will remain prohibited, removed from the list and additional measures will be applied or removed from the list without any additional measures. This task is expected to be ongoing, with a regular flow of dossiers being sent by the applicant required for the risk assessment.

Therefore, to facilitate the correct handling of the dossiers and the acquisition of the required data for the commodity risk assessment, a format for the submission of the required data for each dossier is needed.

Furthermore, a standard methodology for the performance of ‘commodity risk assessment’ based on the work already done by Member States and other international organizations needs to be set.

In view of the above and in accordance with Article 29 of Regulation (EC) No 178/2002, the Commission asked EFSA to provide Scientific Opinion in the field of plant health for Cornus alba and Cornus sanguinea plants from the UK taking into account the available scientific information, including the technical dossier provided by the UK.

1.2 Interpretation of the Terms of Reference

The EFSA Panel on Plant Health (from this point onwards referred to as ‘the Panel') was requested to conduct a commodity risk assessment of C. alba and C. sanguinea plants from the UK following the Guidance on commodity risk assessment for the evaluation of high-risk plant dossiers (EFSA PLH Panel, 2019) taking into account the available scientific information, including the technical information provided by the UK. In accordance with the Agreement on the withdrawal of the United Kingdom of Great Britain and Northern Ireland from the European Union and the European Atomic Energy Community, and in particular Article 5(4) of the Windsor Framework in conjunction with Annex 2 to that Framework, for the purposes of this Opinion, references to the United Kingdom do not include Northern Ireland.

The EU quarantine pests that are regulated as a group in the Commission Implementing Regulation (EU) 2019/20724 were considered and evaluated separately at species level.

Annex II of Implementing Regulation (EU) 2019/2072 lists certain pests as non-European populations or isolates or species. These pests are regulated quarantine pests. Consequently, the respective European populations, isolates or species are non-regulated pests.

Annex VII of the same Regulation, in certain cases (e.g. point 32) makes reference to the following countries that are excluded from the obligation to comply with specific import requirements for those non-European populations, isolates or species: Albania, Andorra, Armenia, Azerbaijan, Belarus, Bosnia and Herzegovina, Canary Islands, Faeroe Islands, Georgia, Iceland, Liechtenstein, Moldova, Monaco, Montenegro, North Macedonia, Norway, Russia (only the following parts: Central Federal District (Tsentralny federalny okrug), Northwestern Federal District (SeveroZapadny federalny okrug), Southern Federal District (Yuzhny federalny okrug), North Caucasian Federal District (Severo-Kavkazsky federalny okrug) and Volga Federal District (Privolzhsky federalny okrug)), San Marino, Serbia, Switzerland, Turkey, Ukraine, and the UK (except Northern Ireland5).

Consequently, for those countries,
  1. Any pests identified, which are listed as non-European species in Annex II of Implementing Regulation (EU) 2019/2072 should be investigated as any other non-regulated pest.
  2. Any pest found in a European country that belongs to the same denomination as the pests listed as non-European populations or isolates in Annex II of Implementing Regulation (EU) 2019/2072, should be considered as European populations or isolates and should not be considered in the assessment of those countries.

Pests listed as ‘Regulated Non-Quarantine Pest’ (RNQP) in Annex IV of the Commission Implementing Regulation (EU) 2019/2072, and deregulated pests (i.e. pest which were listed as quarantine pests in the Council Directive 2000/29/EC and were deregulated by Commission Implementing Regulation (EU) 2019/2072) were not considered for further evaluation. In case a pest is at the same time regulated as a RNQP and as a protected zone quarantine pest, in this Opinion it should be evaluated as quarantine pest.

In its evaluation the Panel:
  • Checked whether the provided information in the technical dossier (from this point onwards referred to as ‘the Dossier’) provided by the applicant (UK, Department for Environment Food and Rural Affairs – from this point onwards referred to as ‘DEFRA’) was sufficient to conduct a commodity risk assessment. When necessary, additional information was requested to the applicant.
  • Selected the relevant Union quarantine pests and protected zone quarantine pests [as specified in Commission Implementing Regulation (EU) 2019/2072,6 from this point onwards referred to as ‘EU quarantine pests’] and other relevant pests present in the UK and associated with the commodity.
  • Did not assess the effectiveness of measures for Union quarantine pests for which specific measures are in place for the import of the commodity from the UK in Commission Implementing Regulation (EU) 2019/2072 and/or in the relevant legislative texts for emergency measures and if the specific country is in the scope of those emergency measures. The assessment was restricted to whether or not the applicant country implements those measures.
  • Assessed the effectiveness of the measures described in the Dossier for those Union quarantine pests for which no specific measures are in place for the importation of the commodity from the UK and other relevant pests present in the UK and associated with the commodity.

Risk management decisions are not within EFSA's remit. Therefore, the Panel provided a rating based on expert judgement on the likelihood of pest freedom for each relevant pest given the risk mitigation measures proposed by DEFRA of the UK.

2 DATA AND METHODOLOGIES

2.1 Data provided by DEFRA of the UK

The Panel considered all the data and information in the Dossier provided by DEFRA of the UK in April 2023. The Dossier is managed by EFSA.

The structure and overview of the Dossier are shown in Table 1. The number of the relevant section is indicated in the Opinion when referring to a specific part of the Dossier.

TABLE 1. Structure and overview of the Dossier.
Dossier section Overview of contents Filename
1.0 Technical dossiers

Cornus alba commodity information final.pdf

Cornus sanguinea commodity information final.pdf

2.0 Pest list Cornus pest list_checked_UK.xlsx
3.0 Nursery distribution map

Cornus_alba_distribution_map.pdf

Cornus_sanguinea_distribution_map.pdf

4.0 List of plants produced in the Cornus nurseries

Cornus_alba_producers_sample_product_list_UK.xlsx

Cornus_sanguinea_producers_sample_product_list_UK.xlsx

2.2 Literature searches performed by DEFRA

The data and supporting information provided by DEFRA of the UK formed the basis of the commodity risk assessment. Table 2 shows the main data sources used by DEFRA of the UK to compile the Dossier (Dossier Sections 1.0 and 2.0).

TABLE 2. Databases used in the literature searches by the DEFRA of the UK.
Database Platform/link
Aphids on the World's Plants https://www.aphidsonworldsplants.info/
Aphid Species File https://aphid.speciesfile.org/
The American Phytopathological Society https://www.apsnet.org/Pages/default.aspx
Beetles of Britain and Ireland https://www.coleoptera.org.uk/
Biological Records Centre https://www.brc.ac.uk/
British Bugs https://www.britishbugs.org.uk/gallery.html
British Leafminers https://www.leafmines.co.uk/html/plants.htm
CABI Crop Protection Compendium https://www.cabi.org/cpc/
CABI Plantwise Knowledge Bank https://www.plantwise.org/knowledgebank/
CABI Publishing https://www.cabi.org/what-we-do/publishing/
Checklist of Aphids of Britain https://influentialpoints.com/aphid/Checklist_of_aphids_in_Britain.htm
Database of the World's Lepidopteran Hostplants https://www.nhm.ac.uk/our-science/data/hostplants/
EPPO Global Database https://gd.eppo.int/
Field Mycology https://basidiochecklist.science.kew.org/BritishFungi/index.htm
Flat Mites of the World https://idtools.org/tools/1074/index.cfm
The Fungal Records Database of Britain and Ireland https://www.frdbi.info/
Global Biodiversity Information Facility https://www.gbif.org/
Indian Council of Agricultural Research – National Bureau of Agricultural Insect Resources https://www.nbair.res.in/
Index Fungorum https://www.indexfungorum.org/
3I Interactive Keys and Taxonomic Databases https://dmitriev.speciesfile.org/
L'Inventaire national du patrimoine naturel https://inpn.mnhn.fr/accueil/index
MycoBank https://www.mycobank.org/
National Collection of Plant Pathogenic Bacteria https://www.fera.co.uk/ncppb
NBA Atlas https://species.nbnatlas.org/
Norfolkmoths https://www.norfolkmoths.co.uk/
Plant Parasites of Europe https://bladmineerders.nl/
Scalenet https://scalenet.info/
The British Mycological Society Fungal Records Database https://www.britmycolsoc.org.uk/field_mycology/fungal_recording
The GB Checklist of Fungal Names https://basidiochecklist.science.kew.org/BritishFungi/GBCHKLST/gbchklst.htm
The Leaf and Stem Mines of British Flies and Other Insects https://www.ukflymines.co.uk/
The Sawflies (Symphyta) of Britain and Ireland https://www.sawflies.org.uk/
UK Butterflies https://www.ukbutterflies.co.uk/index.php
UK Moths https://ukmoths.org.uk/
UK Plant Health Information Portal https://planthealthportal.defra.gov.uk/
USDA Forest Service https://www.srs.fs.usda.gov/
USDA Fungal Database https://nt.ars-grin.gov/fungaldatabases/

2.3 Literature searches performed by EFSA

Literature searches in different databases were undertaken by EFSA to complete a list of pests potentially associated with the genus Cornus. The following searches were combined: (i) a general search to identify pests reported on the genus Cornus in the databases, and subsequently (ii) a tailored search to identify whether the above pests are present or not in the UK. The searches were run on 9 May 2023. No language, date or document type restrictions were applied in the search strategy.

The Panel used the databases indicated in Table 3 to compile the list of pests associated with the genus Cornus. As for Web of Science, the literature search was performed using a specific, ad hoc, established search string (see Appendix B). The string was run in ‘All Databases’ with no range limits for time or language filters.

TABLE 3. Databases used by EFSA for the compilation of the pest list associated with Cornus spp.
Database Platform/link
Aphids on World Plants https://www.aphidsonworldsplants.info/C_HOSTS_AAIntro.htm
CABI Crop Protection Compendium https://www.cabi.org/cpc/
Database of Insects and their Food Plants https://www.brc.ac.uk/dbif/hosts.aspx
Database of the World's Lepidopteran Hostplants https://www.nhm.ac.uk/our-science/data/hostplants/search/index.dsml
EPPO Global Database https://gd.eppo.int/
EUROPHYT https://webgate.ec.europa.eu/europhyt/
Global Biodiversity Information Facility https://www.gbif.org/
Google Scholar https://scholar.google.com/
Leafminers https://www.leafmines.co.uk/html/plants.htm
Nemaplex https://nemaplex.ucdavis.edu/Nemabase2010/PlantNematodeHostStatusDDQuery.aspx
Plant Parasites of Europe https://bladmineerders.nl/
Plant Pest Information Network https://www.mpi.govt.nz/news-and-resources/resources/registers-and-lists/plant-pest-information-network/
Plant Viruses Online https://www1.biologie.uni-hamburg.de/b-online/e35/35tmv.htm#Range
Scalenet https://scalenet.info/associates/
Spider Mites Web https://www1.montpellier.inra.fr/CBGP/spmweb/advanced.php
USDA ARS Fungal Database (version 2021) https://nt.ars-grin.gov/fungaldatabases/fungushost/fungushost.cfm
Web of Science: All Databases (Web of Science Core Collection, CABI: CAB Abstracts, BIOSIS Citation Index, Chinese Science Citation Database, Current Contents Connect, Data Citation Index, FSTA, KCI-Korean Journal Database, Russian Science Citation Index, MEDLINE, SciELO Citation Index, Zoological Record)

Web of Science

https://www.webofknowledge.com

World Agroforestry https://www.worldagroforestry.org/treedb2/speciesprofile.php?Spid=1749
The American Phytopathological Society https://www.apsnet.org/Pages/default.aspx

Additional searches, limited to retrieve documents, were run when developing the Opinion. The available scientific information, including previous EFSA opinions on the relevant pests and diseases and the relevant literature and legislation (e.g. Regulation (EU) 2016/2031; Commission Implementing Regulations (EU) 2018/2019; (EU) 2018/2018; and (EU) 2019/2072), was taken into account.

2.4 Methodology

When developing the Opinion, the Panel followed the EFSA Guidance on commodity risk assessment for the evaluation of high-risk plant dossiers (EFSA PLH Panel, 2019).

In the first step, pests potentially associated with the commodity in the country of origin (EU-regulated pests and other pests) that may require risk mitigation measures are identified. The EU non-regulated pests not known to occur in the EU were selected based on evidence of their potential impact in the EU. After the first step, all the relevant pests that may need risk mitigation measures were identified.

In the second step, if applicable, the implemented risk mitigation measures for each relevant pest are evaluated.

A conclusion on the pest freedom status of the commodity for each of the relevant pests, if any, are determined and uncertainties identified using expert judgements.

Pest freedom was assessed by estimating the number of infested/infected:
  1. Bare-root plants (single or up to 50 plants per bundle) out of 10,000 exported plant units.
  2. Rooted plants in pots/cells (single or up to 5 plants per bundle) out of 10,000 exported plant units.

2.4.1 Commodity data

Based on the information provided by DEFRA of the UK, the characteristics of the commodity are summarised in Section 3 of this Opinion.

2.4.2 Identification of pests potentially associated with the commodity

To evaluate the pest risk associated with the importation of the commodity from the UK, a pest list was compiled. The pest list is a compilation of all identified plant pests reported as associated with all species of Cornus based on information provided in the Dossier Sections 1.0 and 2.0 and on searches performed by the Panel. The search strategy and search syntax were adapted to each of the databases listed in Table 3, according to the options and functionalities of the different databases and Centre for Agriculture and Bioscience International (CABI) keyword thesaurus.

The scientific names of the host plants (i.e. Cornus) were used when searching in the European and Mediterranean Plant Protection Organization (EPPO) Global database (EPPO GD, online) and CABI Crop Protection Compendium (CABI, online). The same strategy was applied to the other databases (see Table 3) excluding EUROPHYT and Web of Science. The notifications of interceptions of EU member states were consulted for the years 2009 to 2023 (EUROPHYT, online, from 2009 to 2020 and TRACES-NT, online, from May 2020 to March 2023, Accessed: 14 November 2023). To check whether Cornus spp. can act as a pathway, all notifications (all origins) for Cornus spp. were evaluated. For each selected pest, it was checked if there were any notification records for UK (all commodities).

The search strategy used for Web of Science Databases was designed combining English common names for pests and diseases, terms describing symptoms of plant diseases and the scientific and English common names of the commodity and excluding pests which were identified using searches in other databases. The established search string is detailed in Appendix B and was run on 9 May 2023.

The titles and abstracts of the scientific papers retrieved were screened, and the pests associated with Cornus genus were included in the pest list. The pest list was eventually further compiled with other relevant information (e.g. EPPO code per pest, taxonomic information, categorisation and distribution) useful for the selection of the pests relevant for the purposes of this Opinion.

The compiled pest list (see Microsoft Excel® in Appendix C) includes all identified pests that use the genus Cornus as a host.

The evaluation of the compiled pest list was done in two steps: first, the relevance of the EU quarantine pests was evaluated (Section 4.1); second, the relevance of any other plant pest was evaluated (Section 4.2).

2.4.3 Listing and evaluation of risk mitigation measures

All proposed risk mitigation measures were listed and evaluated. When evaluating the likelihood of pest freedom at origin, the following types of potential infestation/infection sources for C. alba and C. sanguinea in nurseries were considered (see also Figure 1):
  • Pest entry from surrounding areas,
  • Pest entry with new plants/seeds,
  • Pest spread within the nursery.
Details are in the caption following the image
Conceptual framework to assess likelihood that plants are exported free from relevant pests.

Source: EFSA PLH Panel (2019).

Information on the biology, estimates of likelihood of entry of the pest into the nursery and spread within the nursery, and the effect of the measures on a specific pest is summarised in pest data sheets compiled for each pest selected for further evaluation (see Appendix A).

2.4.4 Expert knowledge elicitation

To estimate the pest freedom of the commodities, an Expert Knowledge Elicitation (EKE) was performed following EFSA guidance (Annex B.8 of EFSA Scientific Committee, 2018).

The specific question for EKE was defined as follows: ‘Taking into account (i) the risk mitigation measures listed in the Dossier, and (ii) other relevant information (reported in the specific pest datasheets), how many of 10,000 plants, either single or in bundles will be infested with the relevant pest/pathogen when arriving in the EU?’

The risk assessment considers bare-root plants (Figure 2A,B) (bundles of 25 or 50 for seedlings or transplants; bundles of 5, 10 or 15 for whips; or single bare-root trees) and rooted plants in pots/cells (Figures 3A,B, 4) (single or up to 5 plants per bundle [Figure 3B]).

Details are in the caption following the image
Field-grown (A) C. alba and (B) C. sanguinea for bare-root plant production

(Source: Dossier Section 1.0).

Details are in the caption following the image
(A) Cell-grown plants grown on metal frames; (B) Cell-grown plants bundled prior to dispatch of C. alba and C. sanguinea plants (Source: Dossier Section 1.0).
Details are in the caption following the image
Rooted plants in pots grown in plastic trays on top of gravel

(Source: Dossier Section 1.0).

Before the elicitation, the pests were grouped if they had similar characteristics, such as: closely taxonomically related; biology/life history; behavioural ecology; effect of management measures (e.g. mesh size); plant/pathogen/vector (if applicable) interactions.

The uncertainties associated with the EKE were taken into account and quantified in the probability distribution applying the semi-formal method described in section 3.5.2 of the EFSA PLH Guidance on quantitative pest risk assessment (EFSA PLH Panel, 2018). Finally, the results were reported in terms of the likelihood of pest freedom. The lower 5% percentile of the uncertainty distribution reflects the opinion that pest freedom is, with 95% certainty, above this limit.

3 COMMODITY DATA

3.1 Description of the commodity

The commodity consists of the following type of deciduous plants of C. alba or C. sanguinea (Table 4, Figures 2-42-4):

TABLE 4. Type of C. alba and C. sanguinea plants to be exported to the EU (Dossier Section 1.0).
Type of plants Age Stem diameter (cm) Height (cm)
Bare-root plants (whips*) 1–3 years old 0.4–1.0 20–120
Bare-root plants 2–7 years old 0.4–4.0 20–150
Cell-grown plants (small containers) 1–2 years old 0.4–1.0 20–60
Rooted plants in pots 1–5 years old 1.0–4.0 20–150
  • * Whips are slender, unbranched trees that can be bare-root or containerised.

Rooted plants in pots may be exported with leaves, depending on the timing of the export and the life cycle of the species. Bare-root plants exported to the EU may also have some leaves at the time of export, in particular when exported in November (Dossier Section 1.0).

According to International Standards for Phytosanitary Measures (ISPM) 36 (FAO, 2019), the commodity can be classified as ‘bare-root plants’ or ‘rooted plants in pots’.

According to the Dossier Section 1.0, the trade volume for both C. alba and C. sanguinea are listed in Table 5.

TABLE 5. Trade volume and seasonal timing for C. alba and C. sanguinea plants.
Type of plant Number of items Seasonal timing
Bare-root plants 10,000 (C. sanguinea), 15,000 (C. alba) October to April
Rooted plants in pots 20,000 (C. sanguinea), 25,000 (C. alba) Mainly September to May
Trade of all plant types will mainly be to Northern Ireland and the Republic of Ireland.
  • Bare-root plants will be lifted from late autumn until early spring (October to April), as this is the best time to move/export dormant plants (Dossier Section 1.0).
  • Rooted plants in pots can be moved/exported at any time in the year to fulfil consumer demand, but more usually from September to May. These will probably be destined for amenity or garden centre trade rather than nurseries (Dossier Section 1.0).

3.2 Description of the production areas

The nurseries producing the commodity are distributed in the Eastern part of Great Britain. All nurseries are registered as professional operators with the UK National Plant Protection Organization (NPPO), either by the Animal and Plant Health Agency (APHA) in England and Wales or by the Scottish Government, and are authorised to issue UK plant passports and phytosanitary certificates for export (Dossier Section 1.0).

Producers do not set aside separate areas for export production. All plants within UK nurseries are grown under the same phytosanitary measures, meeting the requirements of the UK Plant Passporting regime (Dossier Section 1.0). The production areas designated for export to the EU are indicated in the map below (Figure 5).

Details are in the caption following the image
Location of the nurseries designated for export of C. alba and C. sanguinea to the European Union

(Source: Dossier Section 1.0).

Nurseries

The minimum and maximum sizes of nurseries growing C. alba and C. sanguinea for export are as follows.
  • Container grown stock: minimum 8 ha/maximum 150 ha.
  • Field-grown stock (for bare-root plants): maximum 325 ha.

The exporting nurseries grow a range of other plant species. The production area where C. alba and C. sanguinea plants are grown is around 1%–5% of the total area of the nurseries. None of the nurseries expected to export to the EU produce plants from grafting; they use seed (no certification) and seedlings (UK plant passports); therefore, there are no mother plants of C. alba and C. sanguinea present in the nurseries. None of the nurseries expected to export to the EU have mother plants of other tree species present in the nurseries. Approximately 20% of the nurseries likely to export to the EU also sell plants within the UK to final users as ornamental plants, for example to the Local Authorities/Landscape Architects (Dossier Section 1.0).

As the plants are intended for outdoor cultivation, only early growth stages are normally maintained under protection, such as young plants/seedlings, where there is an increased vulnerability due to climatic conditions, including frost. The commodity to be exported should therefore be regarded as outdoor grown. Growth under protection is primarily to protect against external climatic conditions rather than protection from pests. The early stages of plants grown under protection are maintained in plastic polytunnels or in glasshouses, which typically consist of a metal or wood frame construction and glass panels (Dossier Section 1.0).

Surrounding area

Exporting nurseries are predominately situated in rural areas. The surrounding land is mainly arable farmland, with some pasture for animals and small areas of woodland. Hedges are often used to define field boundaries and grown along roadsides (Dossier Section 1.0).

Arable crops

These are rotated in line with good farming practice but could include oilseed rape (Brassica napus), wheat (Triticum), barley (Hordeum vulgare), turnips (Brassica rapa subsp. rapa), potatoes (Solanum tuberosum) and maize (Zea mays) (Dossier Section 1.0).

Pasture

Predominantly ryegrass (Lolium) (Dossier Section 1.0).

Woodland

Woodlands tend to be a standard UK mixed woodland, with a range of UK native trees such as oak (Quercus robur), pine (Pinus), poplar (Populus), ash (Fraxinus), sycamore (Acer pseudoplatanus), holly (Ilex), Norway maple (Acer platanus) and field maple (Acer campestre) (Dossier Section 1.0).

Hedges

Hedges are made up of a range of species, including hazel (Corylus avellana), yew (Taxus baccata), holly (Ilex), ivy (Hedera), alder (Alnus glutinosa), laurel (Prunus laurocerasus), hawthorn (Crataegus), blackthorn (Prunus spinosa) and leylandii (Cupressus x leylandii) (Dossier Section 1.0).

The map provided (Figure 5) included the locations of those nurseries that have contributed the technical information required to prepare the dossier. While these nurseries are likely to be responsible for most UK movements to Northern Ireland and the EU, the information they have contributed is intended to be representative of general industry practice. As with any market access application submitted in line with IPPC guidance, we assume, unless specifically stated otherwise, that the application is made at the country-to-country level. It may therefore be possible that other nurseries in the UK could produce these commodities and would want to export in the future. Such nurseries would need to meet the import requirements set out in any subsequent EU legislation as the nurseries that have contributed technical information to the dossiers.

3.3 Production and handling processes

3.3.1 Source of planting material

The starting material is a mix of seeds and seedlings depending on the nursery. Some seedlings may be obtained from the EU (mostly the Netherlands). This is the only source of the plants obtained from abroad (Dossier Section 1.0).

C. alba seeds purchased in the UK are not covered by a certification scheme; seedlings sourced in the UK are certified with UK Plant Passports; seedlings from the EU countries are certified with phytosanitary certificates (Dossier Section 1.0).

C. sanguinea seeds purchased in the UK may be certified under the Forestry Commission's Voluntary Scheme for the Certification of Native Trees and Shrubs. This allows certification of seeds not covered by Schedule 1 of The Forest Reproductive Material (Great Britain) Regulations 2002 (legislation.gov.uk) (Dossier Section 1.0).

3.3.2 Production cycle

The growing conditions are as follows (as defined in Annex 1 of ISPM 36 (FAO, 2019)):
  • Grown outdoors/in the open air in containers (cells and pots) on protected plastic membranes, or on raised benches to prevent contact with the soil;
  • Field grown.

Cell-grown trees may be grown in cells at one plant per cell. These may be grown under protection initially; however, most plants will be field grown, or field grown in containers.

Any plants in pots with organic growing medium being exported from the UK to the EU need to meet the requirements for growing media in EU Regulation 2019/2072, Annex VII, and the UK already has exports to EU MS meeting this requirement.

In the production or procurement of plants, the use of growing media is assessed for the potential to harbour and transmit plant pests. Growers use virgin peat or peat-free compost, which is a mixture of coir, tree bark, wood fibre etc. This compost is heat-treated by commercial suppliers during production to eliminate pests and diseases. It is supplied in sealed bulk bags or shrink-wrapped bales and stored off the ground on pallets, these are completely hygienic and free from contamination. Where delivered in bulk, compost is kept in a dedicated bunker, either indoors or covered by tarpaulin outdoors, and with no risk of contamination with soil or other material (Dossier Section 1.0).

Plants for bare-root plant production are planted from late autumn until early spring (November to March); rooted plants in pots can be planted at any time of year, though winter is most common. Flowering occurs during late spring (April to June), depending upon the variety and weather conditions (Dossier Section 1.0) (Table 6).

Lifting:
  • Bare-root plants will be harvested in winter. The plants are then root-washed on site and stored prior to export. Bare-root plants exported to the EU may also have some leaves at the time of export, in particular when exported in November (Dossier Section 1.0).
  • Rooted plants in pots can be traded at any point in the year. These plants may be exported with leaves, depending on the timing of the export and the life cycle of the species (Dossier Section 1.0).
TABLE 6. Period of the year when the commodity is produced and the phenology of the crop (including sowing/planting, flowering and harvesting periods).
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
Planting
Flowering
Leaf drop
Lifting

The irrigation is done on a need basis and could be overhead, sub-irrigation or drip irrigation. Water used for irrigation can be drawn from several sources, the mains supply, bore holes or from rainwater collection/water courses. Growers are required to assess water sources, irrigation and drainage systems used in the plant production for the potential to harbour and transmit plant pests. Water is routinely sampled and sent for analysis. No quarantine pests have been found so far (Dossier Section 1.0).

Growers must assess weeds and volunteer plants for the potential to host and transmit plant pests and have an appropriate programme of weed management in place at the nursery (Dossier Section 1.0). Growing areas are kept clear of non-cultivated herbaceous plants. In access areas, non-cultivated herbaceous plants are kept to a minimum and only exist at nursery boundaries. Non-cultivated herbaceous plants grow on less than 1% of the nursery area (Dossier Section 1.0).

General hygiene measures are undertaken as part of routine nursery production, including disinfection of tools and equipment between batches/lots. Tools are disinfected after operation on a stock and before being used on a different plant species. The tools are dipped and wiped with a clean cloth between trees to reduce the risk of virus and bacterial transfer between subjects. Virkon S (active substances: potassium peroxymonosulfate and sodium chloride) was reported as the most commonly used disinfectant. Growers keep records, allowing traceability for all plant material handled (Dossier Section 1.0).

Plant material is regularly monitored for plant health issues. This monitoring is carried out by trained nursery staff via regular crop walking and records kept of this monitoring. Qualified agronomists also undertake regular crop walks to verify the producer's assessments. Curative or preventative actions are implemented together with an assessment of phytosanitary risk. Unless a pest can be immediately and definitively identified as non-quarantine growers are required to treat it as a suspect quarantine pest and notify the competent authority (Dossier Section 1.0).

Additional specific phytosanitary measures apply against Phytophthora ramorum (EU QP (Non-EU isolates)). At growing sites, infected plants are destroyed, and potentially infected plants are ‘held’ (prohibited from moving). The UK has a containment policy in the wider environment, with official action taken to remove infected trees. As part of an annual survey of ornamental retail and production sites (frequency of visits determined by a decision matrix), P. ramorum is inspected on common host plants. An additional inspection, during the growing period, is carried out at plant passport production sites. Inspections are carried out in a survey of 300 non-woodland wider environment sites annually (Dossier Section 1.0).

Pest and disease pressures vary from season to season. Biological control or chemical treatments are reported to be applied when required and depend on the situation at that time (disease pressure, growth stage etc., and environmental factors) (Dossier Section 1.0).

There are no specific measures/treatments against soil pests. However, containerised plants are grown in trays on top of protective plastic membranes to prevent contact with soil. Membranes are regularly refreshed when needed. Alternatively, plants may be grown on raised galvanised steel benches stood on gravel as a barrier between the soil and bench feet and/or concreted surfaces (Dossier Section 1.0, Point 5.1).

3.3.3 Export procedure

The UK NPPO carries out inspections and testing (where required by the country of destination's plant health legislation) to ensure all requirements are fulfilled and a valid phytosanitary certificate with the correct additional declarations is issued (Dossier Section 1.0).

The following processes are typical of all exporting nurseries.

Bare-root plants are lifted and washed free from soil with a low-pressure washer in the outdoors nursery area away from packing/cold store area. In some cases, the plants may be kept in a cold storage for up to 5 months after harvesting prior to export (Dossier Section 1.0).

Prior to export, bare-root plants may be placed in bundles, depending on the size of the plants (25 or 50 for seedlings or transplants; 5, 10 or 15 for whips; or single bare-root trees). They are then wrapped in polythene and packed and distributed on ISPM 15 certified wooden or metal pallets (FAO, 2018) (Figure 6). Alternatively, they may be placed in pallets, which are then wrapped in polythene. Small-volume orders may be packed in waxed cardboard cartons or polythene bags and dispatched via courier (Dossier Section 1.0).

Rooted plants in pots are transported on Danish trolleys for smaller containers or ISPM 15 certified pallets, or individually in pots for larger containers. Small-volume orders may be packed in waxed cardboard cartons or polythene bags and dispatched via courier (Dossier Section 1.0) (Figure 6).

The preparation of the commodities for export is carried out inside the nurseries in a closed environment, for example packing shed (Dossier Section 1.0).

Plants are transported by lorry (size dependent on load quantity). Sensitive plants will occasionally be transported by temperature-controlled lorry if weather conditions during transit are likely to be very cold (Dossier Section 1.0).

Details are in the caption following the image
The preparation of the plants for export to the EU (Source: Dossier Section 1.0).

4 IDENTIFICATION OF PESTS POTENTIALLY ASSOCIATED WITH THE COMMODITY

The search for potential pests associated with Cornus spp. rendered 887 species (see Microsoft Excel® file in Appendix C).

4.1 Selection of relevant EU quarantine pests associated with the commodity

The EU listing of Union quarantine pests and protected zone quarantine pests (Commission Implementing Regulation (EU) 2019/2072) is based on assessments concluding that the pests can enter, establish, spread and have potential impact in the EU.

The 18 EU quarantine species that are reported to use Cornus spp. as a host plant were evaluated (Table 7) for their relevance of being included in this Opinion.

TABLE 7. Overview of the evaluation of the 18 EU quarantine pest species known to use Cornus species as host plants for their relevance for this Opinion.
No. Pest name according to EU legislationa EPPO code Group Pest present in the UK Cornus confirmed as a host (reference) Pest can be associated with the commodity (NA = not assessed) Pest relevant for the opinion
1 Anoplophora chinensis ANOLCN Insects No Cornus sp. (EPPO GD) NA No
2 Anthonomus quadrigibbus TACYQU Insects No Cornus sericea (EPPO GD) NA No
3 Choristoneura conflictana ARCHCO Insects No Cornus alternifolia (EPPO GD) NA No
4 Choristoneura rosaceana CHONRO Insects No Cornus sp., Cornus florida, Cornus racemosa (EPPO GD) NA No
5 Euwallacea fornicatus sensu lato XYLBFO Insects No Cornus controversa (EPPO GD) NA No
6 Lopholeucaspis japonica LOPLJA Insects No Cornus controversa, Cornus florida, Cornus kousa, Cornus macrophylla, Cornus mas, Cornus officinalis, Cornus x rutgergensis (artificial hybrid of Cornus kousa and Cornus florida) (EPPO GD) NA No
7 Lycorma delicatula LYCMDE Insects No Cornus sp., Cornus controversa, Cornus florida, Cornus kousa, Cornus officinalis (EPPO GD) NA No
8 Meloidogyne chitwoodi MELGCH Nematodes No Cornus sanguinea (NEMAPLEX) NA No
9 Meloidogyne fallax MELGFA Nematodes Yes Cornus sanguinea (NEMAPLEX) Yes Yes
10 Oemona hirta OEMOHI Insects No Cornus nattallii (EPPO GD) NA No
11 Phyllosticta solitaria PHYSSL Fungi No Cornus walteri (USDA) NA No
12 Phymatotrichopsis omnivora PHMPOM Fungi No Cornus drummondii, Cornus florida (EPPO GD) NA No
13 Phytophthora ramorum PHYTRA Oomycetes Yes Cornus capitata, Cornus hybrids, Cornus kousa (EPPO GD) Yes Yes
14 Rhagoletis mendax RHAGME Insects No Cornus canadensis (WoS) NA No
15 Rhagoletis pomonella RHAGPO Insects No Cornus florida (WoS) NA No
16 Tobacco ringspot virus TRSV00 Viruses Yes Cornus florida, Cornus racemosa, Cornus sericea (EPPO GD) Yes Yes
17 Tomato ringspot virus TORSV0 Viruses Yes Cornus florida (Encyclopedia of Plant Viruses and Viroids) Yes Yes
18 Xylella fastidiosa XYLEFA Bacteria No Cornus florida (WoS) NA No
  • a Commission Implementing Regulation (EU) 2019/2072.
The relevance of an EU quarantine pest for this Opinion was based on evidence that:
  1. the pest is present in the UK;
  2. the commodity is a host of the pest;
  3. one or more life stages of the pest can be associated with the specified commodity.

Pests that fulfilled all criteria are selected for further evaluation.

Of the 18 EU quarantine pest species evaluated, four pests were selected for further assessment.

4.2 Selection of other relevant pests (non-quarantine in the EU) associated with the commodity

The information provided by the UK, integrated with the search performed by EFSA, was evaluated in order to assess whether there are other relevant pests potentially associated with the commodity species present in the country of export. For these potential pests that are non-regulated in the EU, pest risk assessment information on the probability of entry, establishment, spread and impact is usually lacking. Therefore, these pests were also evaluated to determine their relevance for this Opinion based on evidence that:
  1. the pest is present in the UK;
  2. the pest is (i) absent or (ii) has a limited distribution in the EU;
  3. Cornus spp. is a host of the pest;
  4. one or more life stages of the pest can be associated with the Cornus spp.;
  5. the pest may have an impact in the EU.
For non-regulated species with a limited distribution (i.e. present in one or a few EU member states) and fulfilling the other criteria (i.e. c, d and e), and either one of the following conditions should be additionally fulfilled for the pest to be further evaluated:
  • official phytosanitary measures have been adopted in at least one EU member state;
  • any other reason justified by the working group (e.g. recent evidence of presence).

Based on the information collected, 869 potential pests (non-EU quarantine) known to be associated with Cornus spp. were evaluated for their relevance to this Opinion.

Species were excluded from further evaluation when at least one of the conditions listed above (a–e) was not met. Details can be found in the Appendix C (Microsoft Excel® file). One of the evaluated EU non-quarantine pests, Discula destructiva, was selected for further evaluation.

4.3 Summary of pests selected for further evaluation

Five pests that were identified to be present in the UK and having potential for association with Cornus plants designated for export to the EU are listed in Table 8. The efficacy of the risk mitigation measures applied to the commodity was evaluated for these selected pests.

TABLE 8. List of relevant pests selected for further evaluation.
No. Current scientific name EPPO code Taxonomic information Group Regulatory status
1 Meloidogyne fallax MELGFA Rhabditida, Meloidogynidae Nematodes EU Quarantine Pest
2 Phytophthora ramorum PHYTRA Peronosporales, Peronosporaceae Oomycetes EU Quarantine Pest
3 Tobacco ringspot virus TRSV00 Secoviridae, Nepovirus Viruses EU Quarantine Pest
4 Tomato ringspot virus TORSV0 Secoviridae, Nepovirus Viruses EU Quarantine Pest
5 Discula destructiva DISCDE Diaporthales, Gnomoniaceae Fungi Not regulated in the EU

5 RISK MITIGATION MEASURES

For the selected pests (Table 8), the Panel evaluated the likelihood that it could be present in the C. alba and C. sanguinea nurseries by evaluating the possibility that the commodity in the export nurseries is infested either by:
  • Introduction of the pest from the environment surrounding the nursery;
  • Introduction of the pest with new plants/seeds;
  • Spread of the pest within the nursery.

The information used in the evaluation of the effectiveness of the risk mitigation measures is summarised in pest data sheets (see Appendix A).

5.1 Risk mitigation measures applied in the UK

With the information provided by the UK (Dossier Sections 1.0, 2.0, 3.0, & 4.0), the Panel summarised the risk mitigation measures (see Table 9) that are implemented in the production nursery.

TABLE 9. Overview of implemented risk mitigation measures for C. alba and C. sanguinea plants designated for export to the EU from the UK.
No. Risk mitigation measure Evaluation and uncertainties
1 Registration of production sites All nurseries are registered as professional operator with the UK NPPO, by the APHA and is authorised to issue UK plant passports (Dossier Section 1.0)
2 Certified plant material Seeds of C. alba are not certified, while seeds of C. sanguinea purchased in the UK may be certified under the Forestry Commission's Voluntary Scheme for the Certification of Native Trees and Shrubs. Seedlings for Cornus spp. production sourced in the UK are certified with UK Plant Passports; seedlings from the EU countries are certified with phytosanitary certificates (Dossier Section 1.0)
3 Certification of substrates (rooted plant in pots) Rooted plants in pots: In the production or procurement of these plants, the use of growing media is assessed for the potential to harbour and transmit plant pests. Growers most commonly use virgin peat or peat-free compost, which is a mixture of coir, tree bark, wood fibre etc. The compost is heat-treated by commercial suppliers during production to eliminate pests and diseases. It is supplied in sealed bulk bags or shrink-wrapped bales and stored off the ground on pallets, these are completely hygienic and free from contamination. Where delivered in bulk, compost is kept in a dedicated bunker, either indoors or covered by tarpaulin outdoors, and with no risk of contamination with soil or other material (Dossier Section 1.0)
4 Surveillance, monitoring and sampling

In the last 3 years there has been a substantial level of inspection of registered Cornus spp. producers, both in support of the Plant Passporting scheme (checks are consistent with EU legislation, with a minimum of once a year for authorised operators) and as part of the Quarantine Surveillance programme (Great Britain uses the same framework for its surveillance programme as the EU). The Competent Authority inspects crops at least once a year to check if they meet the standards set out in the guides (Dossier Section 1.0).

UK(GB) surveillance is based on visual inspection with samples taken from symptomatic material, and where appropriate, samples are also taken from asymptomatic material (e.g. plants, tubers, soil, watercourses) (Dossier Section 1.0)

5 Hygiene measures According to the Dossier Section 1.0, all the nurseries have plant hygiene and housekeeping rules and practices in place, which are communicated to all relevant employees. The rules will be dependent on the plants handled and the type of business but will include:
  • Growing media
  • Weed management
  • Water usage
  • Cleaning and sterilisation
  • Waste treatment and disposal
  • Visitors
6 Irrigation water quality and/or treatments Growers are required to assess water sources, irrigation and drainage systems used in the plant production for the potential to harbour and transmit plant pests. Water is routinely sampled and sent for analysis. No quarantine pests have been found (Dossier Section 1.0)
7 Application of pest control products Crop protection is achieved using a combination of measures including approved plant protection products, biological control or physical measures. Plant protection products are only used when necessary and records of all plant protection treatments are kept (Dossier Section 1.0)
8 Washing of the roots (bare-root plants) Bare-root plants are lifted from the field in winter and then root-washed on site and stored prior to export (Dossier Section 1.0)
9 Inspections and management of plants before export

The UK NPPO carries out inspections and testing where required by the country of destination's plant health legislation, to ensure all requirements are fulfilled and a valid phytosanitary certificate with the correct additional declarations is issued

Separate to any official inspection, plant material is checked by growers for plant health issues before dispatch

Special provision for inspection of P. ramorum is in place

5.2 Evaluation of the current measures for the selected pests including uncertainties

The relevant risk mitigation measures acting on the selected pests were identified. Any limiting factors on the efficacy of the measures were documented. All the relevant information, including the related uncertainties deriving from the limiting factors used in the evaluation, is summarised in the pest datasheets provided in Appendix A.

Based on this information, an expert judgement has been given for the likelihood of pest freedom of the commodity, taking into consideration the risk mitigation measures acting on the pest and their combination.

An overview of the evaluation of the selected pests is given in the sections below (Sections 5.2.1, 5.2.45.2.4). The outcome of EKE on pest freedom after the evaluation of the proposed risk mitigation measures is summarised in the Section 5.2.5.

5.2.1 Overview of the evaluation of Meloidogyne fallax

Overview of evaluation of Meloidogyne fallax for the bare-root plants
Rating of the likelihood of pest freedom Pest free with some exceptional cases (based on the median)
Percentile of the distribution 5% 25% Median 75% 95%
Proportion of pest-free plants 9849 out of 10,000 plants 9930 out of 10,000 plants 9973 out of 10,000 plants 9993 out of 10,000 plants 10,000 out of 10,000 plants
Proportion of infested plants 0 out of 10,000 plants 7 out of 10,000 plants 27 out of 10,000 plants 70 out of 10,000 plants 151 out of 10,000 plants
Summary of the information used for the evaluation

Possibility that the pest could become associated with the commodity

M. fallax is a polyphagous nematode with a wide host range, including several major horticultural and agricultural crops and a few species of trees, shrubs and herbaceous plants. The pest can spread via passive human-assisted transport with plants for planting with infested roots, infested soil and/or growing media, and possibly via contaminated tools and machinery. The bare-root Cornus spp. plants could become infested during their growth in the field soil

Measures taken against the pest and their efficacy

General measures taken by the growers are effective against the nematode. These measures include (a) registration of production sites; (b) the use of certified plant material; (c) surveillance, monitoring and sampling; (d) hygiene measures; (e) irrigation water testing; and (f) inspection and management of plants before export

Shortcomings of current measures/procedures

No major shortcomings were identified in the evaluation. If all the described measures are implemented correctly, it is unlikely that the pest is present on the exported Cornus spp. plants

Main uncertainties

– The efficacy of pest detection in the Plant Passport scheme is not known.

– The frequency of inspection of root systems for nematodes.

– The efficiency of the hygiene measures, especially concerning the cleaning of the machinery and the possible movement of soil within the nursery.

– In case of irrigation water, the frequency and the method used for the detection of this pest.

Overview of evaluation of Meloidogyne fallax for the rooted plants in pots
Rating of the likelihood of pest freedom Pest free with few exceptional cases (based on the median)
Percentile of the distribution 5% 25% Median 75% 95%
Proportion of pest-free plants 9963 out of 10,000 plants 9981 out of 10,000 plants 9991 out of 10,000 plants 9997 out of 10,000 plants 10,000 out of 10,000 plants
Proportion of infested plants 0 out of 10,000 plants 3 out of 10,000 plants 9 out of 10,000 plants 19 out of 10,000 plants 37 out of 10,000 plants
Summary of the information used for the evaluation

Possibility that the pest could become associated with the commodity

M. fallax is a polyphagous nematode with a wide host range, including several major horticultural and agricultural crops and a few species of trees, shrubs and herbaceous plants. The pest can enter into the nurseries and spread within the nurseries with passive human-assisted transport with plants for planting with infested roots, infested soil and growing media, and possibly via contaminated tools and machinery. The rooted Cornus spp. plants in pots could become infested when in contact with infested soil

Measures taken against the pest and their efficacy

General measures taken by the nurseries are effective against the nematode. These measures include (a) registration of production sites; (b) the use of certified plant material; (c) the use of certified (heat-treated) growing media; (d) surveillance, monitoring and sampling; (e) hygiene measures (avoid contact with soil); (f) irrigation water testing; and (g) inspection and management of plants before export

Shortcomings of current measures/procedures

No major shortcomings were identified in the evaluation. If all the described measures are implemented correctly, it is unlikely that the pest is present on the exported Cornus spp. plants

Main uncertainties

– The efficacy of pest detection in the plant passport scheme is not known.

– The temperature–time of the heat treatment of the growing media and the efficacy on M. fallax are not known. In another species (Meloidogyne incognita), egg sacs protect eggs and juveniles from heat, and 72°C for 4 days is required sanitation. The heat tolerance of M. fallax is not known.

– The frequency of inspection of root systems for nematodes.

– The efficiency of the hygiene measures, especially concerning the cleaning of the machinery and the possible movement of soil within the nursery.

– In case of irrigation water, the frequency and the method used for the detection of this pest.

5.2.2 Overview of the evaluation of Phytophthora ramorum

Overview of evaluation of Phytophthora ramorum for the bare-root plants
Rating of the likelihood of pest freedom Pest free with some exceptional cases (based on the median)
Percentile of the distribution 5% 25% Median 75% 95%
Proportion of pest-free plants 9823 out of 10,000 plants 9908 out of 10,000 plants 9968 out of 10,000 plants 9994 out of 10,000 plants 9999 out of 10,000 plants
Proportion of infected plants 1 out of 10,000 plants 6 out of 10,000 plants 32 out of 10,000 plants 92 out of 10,000 plants 177 out of 10,000 plants
Summary of the information used for the evaluation

Possibility that the pest could become associated with the commodity

P. ramorum is present in the UK; it has been found in most regions of the UK, but it is more often reported in wetter, western regions. P. ramorum has a wide host range. The possible entry of P. ramorum from the surrounding environment may occur through wind, water and infested soil propagules on the feet of animals/humans entering the field (if any). The pathogen can also enter with new seedlings of Cornus spp. and new plants of other species used for plant production in the nurseries

Measures taken against the pest and their efficacy

P. ramorum is a quarantine pest in the UK and is under official control. General measures taken by the growers are effective against this pathogen. These measures include (a) registration of production sites; (b) the use of certified plant material; (c) surveillance, monitoring and sampling; (d) hygiene measures; (e) irrigation water testing; (f) washing of the roots of the bare-root plants; (g) application of pest control products; and (h) inspection and management of plants before export

Shortcomings of current measures/procedures

No major shortcomings were identified in the evaluation. If all the described measures are implemented correctly, it is unlikely that the pest is present on the exported Cornus spp. plants

Main uncertainties

– It is not clear if the propagation material of alternative host is covered in the certification of plant material scheme.

– The efficiency of the hygiene measures, especially concerning the cleaning of the machinery and the possible movement of soil within the nursery.

– In case of irrigation water, the frequency and the method used for the detection of the pathogen.

– The health status of the other plant species cultivated/traded in the nurseries.

Overview of evaluation of Phytophthora ramorum for the rooted plants in pots
Rating of the likelihood of pest freedom Pest free with few exceptional cases (based on the median)
Percentile of the distribution 5% 25% Median 75% 95%
Proportion of pest-free plants 9971 out of 10,000 plants 9984 out of 10,000 plants 9992 out of 10,000 plants 9996 out of 10,000 plants 9999 out of 10,000 plants
Proportion of infected plants 1 out of 10,000 plants 4 out of 10,000 plants 8 out of 10,000 plants 16 out of 10,000 plants 29 out of 10,000 plants
Summary of the information used for the evaluation

Possibility that the pest could become associated with the commodity

P. ramorum is present in the UK; it has been found in most regions of the UK, but it is more often reported in wetter, western regions. P. ramorum has a wide host range. The possible entry of P. ramorum from the surrounding environment to the nurseries may occur through wind, water and infested soil propagules on the feet of animals/humans entering the nurseries. The pathogen can also enter the nurseries with new seedlings of Cornus spp. and new plants of other species used for plant production in the nurseries

Measures taken against the pest and their efficacy

P. ramorum is a quarantine pest in the UK and is under official control. General measures taken by the nurseries are effective against this pathogen. These measures include (a) registration of production sites; (b) the use of certified plant material; (c) the use of certified growing media; (d) surveillance, monitoring and sampling; (d) hygiene measures; (e) irrigation water testing; (f) application of pest control products; and (g) inspection and management of plants before export

Shortcomings of current measures/procedures

No major shortcomings were identified in the evaluation. If all the described measures are implemented correctly, it is unlikely that the pest is present on the exported Cornus spp. plants

Main uncertainties

– It is not clear if the propagation material of alternative host is covered in the certification of plant material scheme.

– The efficiency of the hygiene measures, especially concerning the cleaning of the machinery and the possible movement of soil within the nursery.

– In case of irrigation water, the frequency and the method used for the detection of the pathogen.

5.2.3 Overview of the evaluation of nepoviruses

Overview of evaluation of nepoviruses [tobacco ringspot virus (TRSV) and tomato ringspot virus (ToRSV)] for the bare-root plants
Rating of the likelihood of pest freedom Pest free with few exceptional cases (based on the median)
Percentile of the distribution 5% 25% Median 75% 95%
Proportion of pest-free plants 9970 out of 10,000 plants 9986 out of 10,000 plants 9995 out of 10,000 plants 9999 out of 10,000 plants 10,000 out of 10,000 plants
Proportion of infected plants 0 out of 10,000 plants 1 out of 10,000 plants 5 out of 10,000 plants 14 out of 10,000 plants 30 out of 10,000 plants
Summary of the information used for the evaluation

Possibility that the pest could become associated with the commodity

TRSV and ToRSV have a wide natural host range. They are widely transmitted by the nematode vectors belonging to the genus Xiphinema. Species of Xiphinema vectoring these viruses are not known to occur in the UK, although there is no evidence of TRSV/ToRSV eradication. Their occurrence in the UK is restricted to Pelargonium (ornamentals) at very low levels. Infected plants may not show symptoms, and TRSV/ToRSV can still establish via seed and pollen transmission. TRSV/ToRSV can also establish by clonal vegetative propagation of infected mother plants. Although potted plants are isolated from soil, bare-root plants are field grown; hence, TRSV/ToRSV can be naturally transmitted by Xiphinema vectors, which may be present in undetected populations.

Measures taken against the pest and their efficacy

In the UK, TRSV is a quarantine pest, and ToRSV is a regulated non-quarantine pest with 0% tolerance on findings on propagating material of ornamental plants and fruit propagating material and fruit plants intended for fruit production. Thus, there is a set of standard precautions to ensure that no plants other than certified plants are present in the production facilities. General measures taken by the growers are effective against these viruses/vectors. These measures include (a) registration of production sites; (b) the use of certified plant material; (c) surveillance, monitoring and sampling; (d) hygiene measures; (e) irrigation water testing; (f) washing of the roots in case of the bare-root plants; and (g) inspection and management of plants before export.

Shortcomings of current measures/procedures

No major shortcomings were identified in the evaluation. If all the described measures are implemented correctly it is unlikely that the pest is present on the exported Cornus spp. plants.

Main uncertainties

– The presence of small undetected populations of nematode vectors.

– The efficiency of the detection and sampling strategies in detecting asymptomatic infections.

– The health status of the other plant species cultivated/traded in the nurseries.

Overview of evaluation of nepoviruses [TRSV and TORSV] for the rooted plants in pots
Rating of the likelihood of pest freedom Almost always pest free (based on the median)
Percentile of the distribution 5% 25% Median 75% 95%
Proportion of pest-free plants 9996 out of 10,000 plants 9997 out of 10,000 plants 9998 out of 10,000 plants 9999 out of 10,000 plants 10,000 out of 10,000 plants
Proportion of infected plants 0 out of 10,000 plants 1 out of 10,000 plants 2 out of 10,000 plants 3 out of 10,000 plants 4 out of 10,000 plants
Summary of the information used for the evaluation

Possibility that the pest could become associated with the commodity

TRSV and ToRSV have a wide natural host range. They are widely transmitted by nematode vectors belonging to the genus Xiphinema. Species of Xiphinema vectoring these viruses are not known to occur in the UK, although there is no evidence of TRSV/ToRSV eradication. Its occurrence in the UK is restricted to Pelargonium (ornamentals) at very low levels. Infected plants may not show symptoms, and TRSV/ToRSV can still establish via seed and pollen transmission. TRSV/ToRSV can also establish by clonal vegetative propagation of infected mother plants. Although potted plants are isolated from soil, bare-root plants are field grown; hence, TRSV/ToRSV can be naturally transmitted by nematode vectors, which may be present in undetected populations.

Measures taken against the pest and their efficacy

TRSV is a quarantine pest in the UK, and ToRSV is a regulated non-quarantine pest with 0% tolerance on findings on propagating material of ornamental plants and fruit propagating material and fruit plants intended for fruit production. Thus, there is a set of standard precautions to ensure that no plants other than certified plants are present in the production facilities. General measures taken by the nurseries are effective against these viruses/vectors. These measures include (a) registration of production sites; (b) the use of certified plant material; (c) the use of certified growing media; (d) surveillance, monitoring and sampling; (d) hygiene measures; (e) irrigation water testing; and (f) inspection and management of plants before export.

Shortcomings of current measures/procedures

No major shortcomings were identified in the evaluation. If all the described measures are implemented correctly, it is unlikely that the pest is present on the exported Cornus spp. plants

Main uncertainties

– The presence of small undetected populations of nematode vectors.

– The efficiency of the detection and sampling strategies in detecting asymptomatic infections.

– The health status of the other plant species cultivated/traded in the nurseries, including the possible nematode (vector) infestation of the growing media.

5.2.4 Overview of the evaluation of Discula destructiva

Overview of evaluation of Discula destructiva for the bare-root plants
Rating of the likelihood of pest freedom Pest free with some exceptional cases (based on the median)
Percentile of the distribution 5% 25% Median 75% 95%
Proportion of pest-free plants 9925 out of 10,000 plants 9961 out of 10,000 plants 9979 out of 10,000 plants 9990 out of 10,000 plants 9996 out of 10,000 plants
Proportion of infected plants 4 out of 10,000 plants 10 out of 10,000 plants 21 out of 10,000 plants 39 out of 10,000 plants 75 out of 10,000 plants
Summary of the information used for the evaluation

Possibility that the pest could become associated with the commodity

D. destructiva is present and widespread in the UK. D. destructiva is known to infect several plants belonging to the genus Cornus, including C. alba. The fungus may remain in a dormant stage for extended periods in leaves, twigs, leaf debris and branches. D. destructiva persists in cankers on the trunks and branches of its hosts, or in twigs or dead leaves carrying conidiomata. Furthermore, several species of arthropods are known to acquire and transport even for long distances viable conidia of D. destructiva, thereby contributing to the spread of dogwood anthracnose.

Measures taken against the pest and their efficacy

General measures taken by the growers are effective against this pathogen. These measures include (a) registration of production sites; (b) the use of certified plant material; (c) surveillance, monitoring and sampling; (d) hygiene measures; (e) application of pest control products; and (f) inspection and management of plants before export.

Shortcomings of current measures/procedures

No major shortcomings were identified in the evaluation. If all the described measures are implemented correctly, it is unlikely that the pest is present on the exported Cornus spp. plants.

Main uncertainties

– It is not clear if the inspection of registered Cornus spp. producers include and will report this pathogen.

– The efficiency of the hygiene measures, especially concerning the cleaning of the machinery.

– Latent, asymptomatic infections are likely to occur in the propagating plant material, and D. destructiva cannot be detected. In addition, infection of seeds is not visible or easy to detect.

– The frequency and efficacy of the treatment (application of pest control products) on the pathogen are unknown.

Overview of evaluation of Discula destructiva for the rooted plants in pots
Rating of the likelihood of pest freedom Pest free with some exceptional cases (based on the median)
Percentile of the distribution 5% 25% Median 75% 95%
Proportion of pest-free plants 9902 out of 10,000 plants 9949 out of 10,000 plants 9971 out of 10,000 plants 9985 out of 10,000 plants 9995 out of 10,000 plants
Proportion of infected plants 5 out of 10,000 plants 15 out of 10,000 plants 29 out of 10,000 plants 51 out of 10,000 plants 98 out of 10,000 plants
Summary of the information used for the evaluation

Possibility that the pest could become associated with the commodity

D. destructiva is present and widespread in the UK. D. destructiva is known to infect several plants belonging to the genus Cornus, including C. alba. The fungus may remain in a dormant stage for extended periods in leaves, twigs, leaf debris and branches. D. destructiva persists in cankers on the trunks and branches of its hosts, or in twigs or dead leaves carrying conidiomata. Furthermore, it is likely that the fungus could be present in the neighbouring environment of the nursery and enter the nursery mainly via insects and seeds, which can transmit the fungus. Several species of arthropods are known to acquire and transport even for long distances viable conidia of D. destructiva, thereby contributing to the spread of dogwood anthracnose.

Measures taken against the pest and their efficacy

General measures taken by the nurseries are effective against this pathogen. These measures include (a) registration of production sites; (b) the use of certified plant material; (c) surveillance, monitoring and sampling; (d) hygiene measures; (e) application of pest control products; and (f) inspection and management of plants before export.

Shortcomings of current measures/procedures

No major shortcomings were identified in the evaluation. If all the described measures are implemented correctly, it is unlikely that the pest is present on the exported Cornus spp. plants.

Main uncertainties

– It is not clear if the inspection of registered Cornus spp. producers include and will report this pathogen.

– The efficiency of the hygiene measures, especially concerning the cleaning of the machinery.

– Latent, asymptomatic infections are likely to occur in the propagating plant material, and D. destructiva cannot be detected. In addition, infection of seeds is not visible or easy to detect.

– The frequency and efficacy of the treatment (application of pest control products) on the pathogen are unknown.

5.2.5 Outcome of EKE

Table 10 and Figure 7 show the outcome of the EKE regarding pest freedom after the evaluation of the currently proposed risk mitigation measures for the selected pests.

TABLE 10. Assessment of the likelihood of pest freedom following evaluation of current risk mitigation measures against pests on C. alba and C. sanguinea plants designated for export to the EU. In panel A, the median value for the assessed level of pest freedom for each pest is indicated by ‘M', the 5% percentile is indicated by ‘L' and the 95% percentile is indicated by ‘U'. The percentiles together span the 90% uncertainty range regarding pest freedom. The pest freedom categories are defined in panel B of the table.
Number Group Pest species Sometimes pest free More often than not pest free Frequently pest free Very frequently pest free Extremely frequently pest free Pest free with some exceptional cases Pest free with few exceptional cases Almost always pest free
1 Nematodes Meloidogyne fallax/bare-root plants L M U
2 Nematodes Meloidogyne fallax/rooted plants in pots L M U
3 Fungi Phytophthora ramorum/bare-root plants L M U
4 Fungi Phytophthora ramorum/rooted plants in pots L M U
5 Virus Nepoviruses (ToRSV & TRSV)/bare-root plants L M U
6 Virus Nepoviruses (ToRSV & TRSV)/rooted plants in pots LMU
7 Fungi Discula destructiva/bare-root plants L M U
8 Fungi Discula destructiva/rooted plants in pots L M U
Details are in the caption following the image
The elicited certainty (y-axis) of the number of pest-free C. alba and C. sanguinea plants (x-axis; log-scaled) out of 10,000 plants designated for export to the EU introduced from the UK for all evaluated pests visualised as descending distribution function. Horizontal lines indicate the percentiles (starting from the bottom 5%, 25%, 50%, 75% and 95%).

Figure 8 provides an explanation of the descending distribution function describing the likelihood of pest freedom after the evaluation of the currently proposed risk mitigation measures for P. ramorum on Cornus spp. Bare-root plants designated for export to the EU.

Details are in the caption following the image
The explanation of the descending distribution function describing the likelihood of pest freedom after the evaluation of the currently proposed risk mitigation measures for C. alba and C. sanguinea bare-root plants designated for export to the EU based on the example of P. ramorum.

PANEL A

Pest freedom category Pest fee plantsout of 10,000 Legend of pest freedom categories
Sometimes pest free ≤ 5000 L Pest freedom category includes the elicited lower bound of the 90% uncertainty range
More often than not pest free 5000– ≤ 9000 M Pest freedom category includes the elicited median
Frequently pest free 9000– ≤ 9500 U Pest freedom category includes the elicited upper bound of the 90% uncertainty range
Very frequently pest free 9500– ≤ 9900
Extremely frequently pest free 9900– ≤ 9950
Pest free with some exceptional cases 9950– ≤ 9990
Pest free with few exceptional cases 9990– ≤ 9995
Almost always pest free 9995– ≤ 10,000

PANEL B

6 CONCLUSIONS

There are five pests (Meloidogyne fallax, Phytophthora ramorum (non-EU isolates), tobacco ringspot virus, tomato ringspot virus and Discula destructiva) identified to be present in the UK and considered to be potentially associated with the C. alba and C. sanguinea plants imported from the UK and relevant for the EU. The likelihood of the pest freedom after the evaluation of the implemented risk mitigation measures for bare roots and rooted C. alba and C. sanguinea plants in pots designated for export to the EU was estimated.

For M. fallax, the likelihood of pest freedom for bare-root C. alba and C. sanguinea plants following evaluation of current risk mitigation measures was estimated as ‘pest free with some exceptional cases’ with the 90% uncertainty range reaching from ‘very frequently pest free’ to ‘almost always pest free’. The EKE indicated, with 95% certainty, that between 9849 and 10,000 bare-root C. alba and C. sanguinea plants per 10,000 will be free from M. fallax. The likelihood of pest freedom for rooted C. alba and C. sanguinea plants in pots was estimated ‘pest free with few exceptional cases’ with the 90% uncertainty range reaching from ‘pest free with some exceptional cases’ to ‘almost always pest free’. The EKE indicated, with 95% certainty, that between 9963 and 10,000 rooted C. alba and C. sanguinea plants in pots per 10,000 will be free from M. fallax.

For P. ramorum, the likelihood of pest freedom for bare-root C. alba and C. sanguinea plants following evaluation of current risk mitigation measures was estimated as ‘pest free with some exceptional cases’ with the 90% uncertainty range reaching from ‘very frequently pest free’ to ‘almost always pest free’. The EKE indicated, with 95% certainty, that between 9823 and 10,000 bare-root C. alba and C. sanguinea plants per 10,000 will be free from P. ramorum. The likelihood of pest freedom for rooted C. alba and C. sanguinea plants in pots was estimated ‘pest free with few exceptional cases’ with the 90% uncertainty range reaching from ‘pest free with some exceptional cases’ to ‘almost always pest free’. The EKE indicated, with 95% certainty, that between 9971 and 10,000 rooted C. alba and C. sanguinea plants in pots per 10,000 will be free from P. ramorum.

For selected nepoviruses (tobacco ringspot virus and tomato ringspot virus), the likelihood of pest freedom for bare-root C. alba and C. sanguinea plants following evaluation of current risk mitigation measures was estimated as ‘pest free with few exceptional cases’ with the 90% uncertainty range reaching from ‘pest free with some exceptional cases’ to ‘almost always pest free’. The EKE indicated, with 95% certainty, that between 9970 and 10,000 bare-root C. alba and C. sanguinea plants per 10,000 will be free from the selected nepoviruses. The likelihood of pest freedom for rooted C. alba and C. sanguinea plants in pots was estimated ‘almost always pest free’ with the 90% uncertainty range reaching from ‘almost always pest free’ to ‘almost always pest free’. The EKE indicated, with 95% certainty, that between 9996 and 10,000 rooted C. alba and C. sanguinea plants in pots per 10,000 will be free from selected nepoviruses.

For D. destructiva, the likelihood of pest freedom for bare-root C. alba and C. sanguinea plants following evaluation of current risk mitigation measures was estimated as ‘pest free with some exceptional cases’ with the 90% uncertainty range reaching from ‘extremely frequently pest free’ to ‘almost always pest free’. The EKE indicated, with 95% certainty, that between 9925 and 10,000 bare-root C. alba and C. sanguinea plants per 10,000 will be free from D. destructiva. The likelihood of pest freedom for rooted C. alba and C. sanguinea plants in pots was estimated ‘pest free with some exceptional cases’ with the 90% uncertainty range reaching from ‘extremely frequently pest free’ to ‘pest free with few exceptional cases’. The EKE indicated, with 95% certainty, that between 9902 and 10,000 rooted C. alba and C. sanguinea plants in pots per 10,000 will be free from D. destructiva.

ABBREVIATIONS

  • APHA
  • Animal and Plant Health Agency
  • CABI
  • Centre for Agriculture and Bioscience International
  • DEFRA
  • Department for Environment Food and Rural Affairs
  • EKE
  • Expert Knowledge Elicitation
  • EPPO
  • European and Mediterranean Plant Protection Organization
  • FAO
  • Food and Agriculture Organization
  • ISPM
  • International Standards for Phytosanitary Measures
  • NPPO
  • National Plant Protection Organization
  • PLH
  • Plant Health
  • PRA
  • Pest Risk Assessment
  • PZQPs
  • Protected Zone Quarantine Pests
  • RNQPs
  • Regulated Non-Quarantine Pests
  • UK
  • United Kingdom
  • GLOSSARY

  • Control (of a pest)
  • Suppression, containment or eradication of a pest population (FAO, 1995, 2017).
  • Entry (of a pest)
  • Movement of a pest into an area where it is not yet present, or present but not widely distributed and being officially controlled (FAO, 2017).
  • Establishment (of a pest)
  • Perpetuation, for the foreseeable future, of a pest within an area after entry (FAO, 2017).
  • Impact (of a pest)
  • The impact of the pest on the crop output and quality and on the environment in the occupied spatial units.
  • Introduction (of a pest)
  • The entry of a pest resulting in its establishment (FAO, 2017).
  • Measures
  • Control (of a pest) is defined in ISPM 5 (FAO, 2017) as ‘Suppression, containment or eradication of a pest population’ (FAO, 1995). Control measures are measures that have a direct effect on pest abundance. Supporting measures are organisational measures or procedures supporting the choice of appropriate risk mitigation measures that do not directly affect pest abundance.
  • Pathway
  • Any means that allows the entry or spread of a pest (FAO, 2017).
  • Phytosanitary measures
  • Any legislation, regulation or official procedure having the purpose to prevent the introduction or spread of quarantine pests, or to limit the economic impact of regulated non-quarantine pests (FAO, 2017).
  • Protected zone
  • A Protected zone is an area recognised at EU level to be free from a harmful organism, which is established in one or more other parts of the Union.
  • Quarantine pest
  • A pest of potential economic importance to the area endangered thereby and not yet present there, or present but not widely distributed and being officially controlled (FAO, 2017).
  • Regulated non-quarantine pest
  • A non-quarantine pest whose presence in plants for planting affects the intended use of those plants with an economically unacceptable impact and which is therefore regulated within the territory of the importing contracting party (FAO, 2017).
  • Risk mitigation measure
  • 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 risk mitigation measure may become a phytosanitary measure, action or procedure according to the decision of the risk manager.
  • Spread (of a pest)
  • Expansion of the geographical distribution of a pest within an area (FAO, 2017).
  • ACKNOWLEDGEMENTS

    The EFSA would like to extend its sincere appreciation for the invaluable contributions made by trainees Raghavendra Reddy Manda and Paraskevi Kariampa.

      CONFLICT OF INTEREST

      If you wish to access the declaration of interests of any expert contributing to an EFSA scientific assessment, please contact [email protected].

      REQUESTOR

      European Commission

      QUESTION NUMBERS

      EFSA-Q-2023-00329, EFSA-Q-2023-00330

      COPYRIGHT FOR NON-EFSA CONTENT

      EFSA may include images or other content for which it does not hold copyright. In such cases, EFSA indicates the copyright holder, and users should seek permission to reproduce the content from the original source.

      PANEL MEMBERS

      Claude Bragard, Paula Baptista, Elisavet Chatzivassiliou, Francesco Di Serio, Paolo Gonthier, Josep Anton Jaques Miret, Annemarie Fejer Justesen, Alan MacLeod, Christer Sven Magnusson, Panagiotis Milonas, Juan A. Navas-Cortes, Stephen Parnell, Roel Potting, Philippe L. Reignault, Emilio Stefani, Hans-Hermann Thulke, Wopke Van der Werf, Antonio Vicent Civera, Jonathan Yuen and Lucia Zappalà.

      Notes

    1. 1 Regulation (EU) 2016/2031 of the European Parliament of the Council of 26 October 2016 on protective measures against pests of plants, amending Regulations (EU) 228/2013, (EU) 652/2014 and (EU) 1143/2014 of the European Parliament and of the Council and repealing Council Directives 69/464/EEC, 74/647/EEC, 93/85/EEC, 98/57/EC, 2000/29/EC, 2006/91/EC and 2007/33/EC. OJ L 317, 23.11.2016, pp. 4–104.
    2. 2 Commission Implementing Regulation (EU) 2018/2019 of 18 December 2018 establishing a provisional list of high risk plants, plant products or other objects, within the meaning of Article 42 of Regulation (EU) 2016/2031 and a list of plants for which phytosanitary certificates are not required for introduction into the Union, within the meaning of Article 73 of that Regulation C/2018/8877. OJ L 323, 19.12.2018, pp. 10–15.
    3. 3 Regulation (EC) No 178/2002 of the European Parliament and of the Council of 28 January 2002 laying down the general principles and requirements of food law, establishing the European Food Safety Authority and laying down procedures in matters of food safety. OJ L 31, 1.2.2002, pp. 1–24.
    4. 4 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, pp. 1–279.
    5. 5 In accordance with the Agreement on the withdrawal of the United Kingdom of Great Britain and Northern Ireland from the European Union and the European Atomic Energy Community, and in particular Article 5(4) of the Protocol on Ireland/Northern Ireland in conjunction with Annex 2 to that Protocol, for the purposes of this Opinion, references to Member States include the United Kingdom in respect of Northern Ireland.
    6. 6 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, pp. 1–279.
    7. APPENDIX A: Datasheets of pests selected for further evaluation

      A.1 Meloidogyne fallax

      A.1.1 Organism information

      Taxonomic information

      Current valid scientific name: Meloidogyne fallax

      Synonyms: Meloidogyne chitwoodi (Baexem) B-type. Name used in the EU legislation: Meloidogyne fallax Karssen [MELGFA]

      Order: Rhabditida

      Family: Meloidogynidae

      Common name: false Columbia root-knot nematode, root gall nematode

      Name used in the Dossier: Meloidogyne fallax

      Group Nematodes
      EPPO code MELGMA
      Regulated status

      The pest is listed in Annex II of Regulation (EU) 2019/2072 as Meloidogyne fallax Karssen [MELGFA]

      The pest is included in the EPPO A2 list (EPPO, online_a)

      M. fallax is quarantine in Morocco, Moldova and Norway. It is on A1 list of Argentina, Bahrain, Brazil, Egypt, Georgia, Kazakhstan, Russia, Ukraine and EAEU (=Eurasian Economic Union – Armenia, Belarus, Kazakhstan, Kyrgyzstan and Russia). It is on A2 list of COSAVE (=Comite de Sanidad Vegetal del Cono Sur – Argentina, Brazil, Chile, Paraguay, Peru and Uruguay) (EPPO, online_b). M. fallax is also quarantine pest in the USA (Kantor et al., 2022)

      In the UK, M. fallax is regulated non-quarantine pest on potato only, as this is considered to be the main host at risk (EPPO, online_b; DEFRA, online), and it is regulated quarantine pest in Northern Ireland (DEFRA, online)

      Pest status in the UK M. fallax is present in the UK (CABI, online; EPPO, online_c) with a restricted distribution in England and Wales, being more present in the western areas of UK. There are no findings associated to trees. M. fallax was also detected in Northern Ireland in 2011 (EPPO, 2015); however, its presence is currently not confirmed. The pest is present and shows symptoms on sport turf in UK that could act as source for a wider spread
      Pest status in the EU Not relevant for EU Quarantine pests
      Host status on Cornus

      Cornus spp. is reported as a host plant for M. fallax (Nemaplex, online; den Nijs LJMF et al., 2004)

      PRA information Available Pest Risk Assessments:
      • Pest risk assessment for the European Community plant health: a comparative approach with case studies. Cases: Meloidogyne chitwoodi and M. fallax. (MacLeod et al., 2012);
      • UK Risk Register Details for M. fallax (DEFRA, online);
      • Scientific Opinion on the commodity risk assessment of Acer spp. plants from New Zealand (EFSA PLH Panel, 2020).
      Other relevant information for the assessment
      Biology

      M. fallax is a highly polyphagous root-knot nematode first described from the Netherlands and mostly distributed in temperate regions of the world. It is present in Africa (South Africa), Asia (Indonesia), Europe (Belgium, France, Germany, the Netherlands, Switzerland, Sweden, UK), Oceania (Australia, New Zealand) and South America (Chile) (EPPO, online_c; CABI, online). According to MacLeod et al. (2012), M. fallax may be more widespread because it is frequently confused with similar species as M. hapla and M. chitwoodi, and not causing clear external symptoms on host plants

      M. fallax has three development stages: eggs, juveniles (four stages) and adults. The nematode mainly reproduces parthenogenetically, and sexual reproduction can possibly occur under adverse conditions; like other Meloidogyne species, M. fallax has 1–3 generations per year depending on temperature and host availability (EFSA, 2019; MacLeod et al., 2012). Females lay up to 800–1000 eggs in gelatinous masses (egg sacs) on the root surface, in galls and tubers. Hatching can occur at temperatures below 10°C, so that M. fallax is considered cryophilic (EFSA PLH Panel, 2020; MacLeod et al., 2012). The second-stage juveniles move in the soil and penetrate host roots, start feeding on cortical tissues, inducing giant cells as a feeding site and the formation of root galls (root-knots); they become sedentary and develop to successive stages by quick moults. The nematode can stay infective in the soil for long time, being also able to survive for more than 300 days at temperatures of 5 and 10°C, and 140 days at higher temperatures (15–25°C). Survival and infectivity may also be related to high soil humidity (100% survival with 98% RH), although in moderate dry soil conditions, M. fallax may survive for more than 9 weeks (MacLeod et al., 2012)

      As other nematode species living in the soil, M. fallax has only little spread capacity, the juvenile stages moving 1–2 m maximum per year depending on the type of soil, water availability and other parameters (EFSA, 2019). Water could also disperse the nematode (mainly eggs and juveniles) at short distances. The human-assisted spread on medium-long distance is very frequent and effective by passive transport. Possible pathways are mainly plants for planting with infected roots; tubers and bulbs; soil and growing media; contaminated tools, machinery, shoes and packaging material (EFSA 2019)

      Symptoms Main type of symptoms

      M. fallax is a root-knot nematode. Heavily infested plants show stunting and yellowing on above-ground parts and galling on roots (Moens et al., 2009; MacLeod et al., 2012; EFSA, 2019). Symptoms of root-knot nematodes on hardwood trees may show as slow growth, sparse foliage, chlorotic leaves and crown dieback (Riffle, 1963). Symptoms on roots vary with species but should be visible as galls in advanced infections

      On potato tubers, M. fallax causes numerous small pimple-like areas on the surface. These are caused by tuber infection in the second juvenile generation (EPPO, 2019)

      No specific information about symptoms on Cornus sp. was found

      Presence of asymptomatic plants At the early stages of infection, plants may not show any apparent symptoms on the above-ground parts and do not show galls on the roots. In some cases, plants are wilted and lack vigour. The main impact of the pest is on root growth, and on the quality and growth of the plant (EFSA, 2019; Moens et al., 2009; MacLeod et al., 2012)
      Confusion with other pests

      M. fallax is morphologically very similar to M. chitwoodi and may also be easily confused with other species as M. hapla and M. minor, often found in the same habitat. M. fallax cannot be identified on the basis of galls only, since other soil nematode cause similar damage and some insects and bacteria can induce comparable galls on roots as well (EFSA, 2019)

      The nematode can be identified by laboratory tests on morphometric characters, electrophoresis or sequencing/DNA barcoding (EPPO, 2016)

      Host plant range

      M. fallax is a polyphagous nematode with a wide host range, including several major horticultural and agricultural crops and a few species of trees, shrubs and herbaceous plants

      Main horticultural/agricultural hosts are: Apium graveolens, Allium porrum, Asparagus officinalis, Avena strigosa, Beta vulgaris, Cicorium endivia, Cynara scolymus, Daucus carota, Foeniculum vulgare, Fragaria ananassa, Hordeum vulgare, Lactuca sativa, Lycopersicum esculentum, Medicago sativa, Phaseolus vulgaris, Secale cereale, Solanum nigrum, S. tuberosum, Solanum spp., Triticum aestivum and Zea mays (CABI, online; EPPO, online_e; MacLeod et al., 2012)

      Woody hosts of M. fallax are Acer palmatum, Betula pendula, Cornus sanguinea, Laburnum anagyroides and Lonicera xylosteum (MacLeod et al., 2012; Nemaplex, online)

      For a more exhaustive list of hosts, see CABI (online), EPPO (online_e), Nemaplex (online), de Nijs et al. (2004) and MacLeod et al. (2012)

      Evidence that the commodity is a pathway Meloidogyne spp. nematodes, although rarely identified at species level, are frequently intercepted on plants for planting (EUROPHT/TRACES, online); therefore, the bare-root and potted plants of Cornus spp. are a possible pathway of entry for M. fallax
      Surveillance information According to the Dossier Section 1.0, M. fallax is not under official surveillance, and has no quarantine pest status in the UK

      A.1.2 Possibility of pest presence in the nursery

      A.1.2.1 Possibility of entry from the surrounding environment

      M. fallax is present in the UK territory with restricted distribution in agricultural lands and sports turf (EPPO, online).

      The nematode has a very limited capacity of movement in the soil (1–2 m) and can only spread by passive human-assisted transport with plants for planting with infected roots, infected soil and growing media, and possibly via contaminated tools and machinery. No other possibility of entry in the nurseries is known.

      Uncertainties:
      • The occurrence of the pest in south-eastern England.
      • Pest presence and pressure in the surrounding.

      Taking into consideration the above evidence and uncertainties, the Panel considers that it is possible for M. fallax to enter the nurseries from surrounding environment. In the surrounding area, suitable hosts are present, and the nematode can enter through the human-assisted spread of infested seedlings and infested soil accidentally introduced into the nurseries

      A.1.2.2 Possibility of entry with new plants/seed

      The starting materials are either seeds or seedlings. Seed purchased in the UK is not covered by a certification scheme; seedlings sourced in the UK are certified with UK Plant Passports; seedlings from the EU countries are certified with phytosanitary certificates. Some seedlings may be obtained from the EU (mostly the Netherlands). This is the only source of the plants obtained from abroad (Dossier Section 1.0). Seeds are not a pathway for the nematode.

      In addition to Cornus spp., the nurseries also produce other plants (Dossier Section 1.0). However, there is no information on how and where the plants are produced. Besides, M. fallax may also spread on soil adhering to the roots of non-host plants (MacLeod et al., 2012). Therefore, if the plants are first produced in another nursery, the nematode could possibly travel with them.

      The nurseries are using virgin peat or peat-free compost (a mixture of coir, tree bark, wood fibre etc.) as a growing media (Dossier Section 1.0). M. fallax is able to survive in the soil for a long time and therefore could potentially enter with infested soil/growing media. However, the growing media is heat-treated by commercial suppliers during production to eliminate pests and diseases (Dossier Section 1.0). In another species (Meloidogyne incognita), egg sacs protect eggs and juveniles from heat, and 72° C for 4 days is required sanitation. The heat tolerance of M. fallax is not known.

      Uncertainties:
      • No information is available on the origin of new plants used for plant production in the area of the nurseries.
      • No specific indication on how heat treatment is realised (temperature, time).

      Taking into consideration the above evidence and uncertainties, the Panel considers that it is possible for the nematode to enter the nurseries via the infected roots of new seedlings of Cornus spp. and the other plant species used for plant production in the area. The Panel considers the entry of the nematode with seeds and the growing media as not possible.

      A.1.2.3 Possibility of spread within the nursery

      Cornus spp. plants are either grown in containers (cells, pots, tubes etc.) outdoors in the open air or in fields.

      The nematode can infect other host plants that could be present in the nurseries.

      M. fallax can spread within the nurseries by movement of soil, water, infested plant material and infected tools, contaminated shoes and machinery. Tools used in the nurseries are disinfected after operation on a stock and before being used on a different plant species (Dossier Section 1.0); however, no information is available on the measures to reduce the risk of contamination of machinery, shoes or other material (i.e. package, bags etc.).

      Uncertainties:
      • Possibility that the pest can spread via contaminated soil adhering to shoes, machinery or other material.

      Taking into consideration the above evidence and uncertainties, the Panel considers that the spread of the nematode within the nurseries is possible either by movement of infested soil (also via machinery, shoes and other material), water or plant material.

      A.1.3 Information from interceptions

      In the EUROPHYT/TRACES-NT database, there are no records of interceptions of M. fallax on Cornus spp. from third countries or on any other plant from the UK.

      A.1.4 Evaluation of the risk mitigation measures

      In the table below (Table A.1), all risk mitigation measures currently applied in the UK are listed, and an indication of their effectiveness on M. fallax is provided. The description of the risk mitigation measures currently applied in the UK is provided in the Table 9.

      TABLE A.1. Evaluation of the risk mitigation measures.
      Number Risk mitigation measure Effect on the pest Evaluation and uncertainties
      1 Registration of production sites Yes

      All nurseries are registered as professional operator with the UK NPPO, by the APHA and is authorised to issue UK plant passports (Dossier Section 1.0)

      Evaluation: The registration of production sites is expected to contribute in reducing the phytosanitary risks within the facility

      Uncertainties: none

      2 Certified plant material Yes

      Seeds of C. alba are not certified, while seeds of C. sanguinea purchased in the UK may be certified under the Forestry Commission's Voluntary Scheme for the Certification of Native Trees and Shrubs. Seedlings for Cornus spp. production sourced in the UK are certified with UK Plant Passports; seedlings from the EU countries are certified with phytosanitary certificates. Seedlings could be a pathway for the nematode especially with regard to early, symptomless infections

      Evaluation: M. fallax is an regulated non-quarantine pests (RNQP) for UK on potato only. Inspections associated to the release of Plant Passport may help in reducing infestations. Seeds are not a pathway for M. fallax

      Uncertainties: The efficacy of pest detection in the Plant Passport scheme is not known

      3 Growing media composition and treatment Yes

      In the production or procurement of plants, the use of growing media is assessed for the potential to harbour and transmit plant pests. Growers most commonly use virgin peat or peat-free compost, which is a mixture of coir, tree bark, wood fibre etc. The compost is heat-treated by commercial suppliers during production to eliminate pests and diseases. It is supplied in sealed bulk bags or shrink-wrapped bales and stored off the ground on pallets, these are completely hygienic and free from contamination. Where delivered in bulk, compost is kept in a dedicated bunker, either indoors or covered by tarpaulin outdoors, and with no risk of contamination with soil or other material (Dossier Section 1.0)

      Evaluation: The measures for growing media can reduce infestation rates

      Uncertainties: The temperature–time of the heat treatment of the growing media and the efficacy on M. fallax. In another species (M. incognita), egg sacs protect eggs and juveniles from heat, and 72°C for 4 days is required sanitation. The heat tolerance of M. fallax is not known

      4 Surveillance, monitoring and sampling Yes

      In the last 3 years there has been a substantial level of inspection of registered Cornus spp. producers, both in support of the Plant Passporting scheme (checks are consistent with EU legislation, with a minimum of once a year for authorised operators) and as part of the Quarantine Surveillance programme (Great Britain uses the same framework for its surveillance programme as the EU). The Competent Authority inspects crops at least once a year to check if they meet the standards set out in the guides (Dossier Section 1.0)

      UK(GB) surveillance is based on visual inspection with samples taken from symptomatic material, and where appropriate, samples are also taken from asymptomatic material (e.g. plants, tubers, soil, watercourses) (Dossier Section 1.0)

      Evaluation: This measure can reduce the infestation rates

      Uncertainties: The frequency of inspection of root systems

      5 Hygiene measures Yes

      All nurseries have plant hygiene and housekeeping rules and practices in place, which are communicated to all relevant employees. The rules will be dependent on the plants handled and the type of business but will include:

      • Growing media
      • Weed management
      • Water usage
      • Cleaning and sterilisation
      • Waste treatment and disposal
      • Visitors

      Evaluation: This measure can reduce the infestation rates

      Uncertainties: The efficiency of the hygiene measures especially concerning the cleaning of the machinery and the with the possible movement of soil within the nursery

      6 Irrigation water quality and/or treatments Yes

      Growers are required to assess water sources, irrigation and drainage systems used in the plant production for the potential to harbour and transmit plant pests. Water is routinely sampled and sent for analysis. No quarantine pests have been found (Dossier Section 1.0)

      Evaluation: The irrigation water is routinely checked and can reduce the risk

      Uncertainties: The frequency and the method used for the detection of the pest

      7 Application of pest control products Yes

      Crop protection is achieved using a combination of measures including approved plant protection products, biological control or physical measures. Plant protection products are only used when necessary and records of all plant protection treatments are kept. (Dossier Section 1.0)

      Evaluation: There is no indication of use of nematicides

      Uncertainties: No

      8 Root washing No

      Bare-root plants are lifted from the field in winter and then root-washed on site and stored prior to export

      Evaluation: Root washing can remove infective juveniles of M. fallax, occurring in adhering soil, but has no effect on nematode stages inside roots

      Uncertainties: Using low-pressure water for cleaning the roots may not fully be effective in removing the M. fallax

      9 Inspections and management of plants before export Yes

      The UK NPPO carries out inspections and testing where required by the country of destination's plant health legislation, to ensure all requirements are fulfilled and a valid phytosanitary certificate with the correct additional declarations is issued

      Separate to any official inspection, plant material is checked by growers for plant health issues before dispatch

      Evaluation: Helpful in reducing rates of infestation

      Uncertainties: The frequency of inspection of root system

      A.1.5 Overall likelihood of pest freedom for Cornus spp. plants (bare-root and rooted plants in pots)

      A.1.5.1 Reasoning for a scenario which would lead to a reasonably low number of infested Cornus spp. plants (bare-root and rooted plants in pots)

      • M. fallax has restricted distribution in the UK. It is more prevalent in the Western part of the UK (more humid/suitable) than in the Eastern part (dry), where the nurseries are located.
      • M. fallax exhibits limited reproductive activity on Cornus spp.
      • The symptoms of the nematode infestation are clearly visible on the leaves.
      • Low spread rate of nematodes in the nursery.
      • Seeds are not a pathway for M. fallax, and the seedlings of Cornus spp. are certified with the UK plant passport.
      • The growing medium is heat-treated and separated from soil.
      • Tools are properly disinfected.
      • Root washing removes the soil.
      • Irrigation water is regularly checked.
      • Official inspection before the export.

      A.1.5.2 Reasoning for a scenario which would lead to a reasonably high number of infested Cornus spp. plants (bare-root and rooted plants in pots)

      • M. fallax is widespread in the UK.
      • Cornus is an experimental host/host.
      • The knots are not easily visible on roots, making the detection difficult.
      • There may not be clear symptoms on the plants, and it is easy to confuse with other species.
      • Woody host plants may be present in the surrounding environment.
      • There can be a human-assisted spread of nematode in the nursery.
      • Unclear check for nematodes in case of propagation material.
      • Heat treatment may not be efficient as the heat tolerance of M. fallax is not known.
      • Disinfection of machinery is unknown, so there can be a movement of soil.
      • Root washing may not completely remove the soil; therefore, it is not effective against the pest.
      • Overhead irrigation/excess water may spread M. fallax.
      • No application of nematicides.
      • Unclear details and efficiency of inspection before the export of Cornus spp. plants.

      A.1.5.3 Reasoning for a central scenario equally likely to over- or underestimate the number of infested Cornus spp. plants (bare-root and rooted plants in pots) (median)

      The scenario assumes a limited presence of the pest in the nurseries and the surroundings and that the plants are exposed to the nematode for only a short period of time. The movement of soil from the surrounding into the nurseries is not expected to be significant.

      A.1.5.4 Reasoning for the precision of the judgement describing the remaining uncertainties (1st and 3rd quartile/interquartile range)

      The limited information on occurrence of the pests in the UK, including the nurseries and the surroundings, results in a high level of uncertainties for infestation rates below the median. Otherwise, the pest pressure from the surroundings is expected to be low giving less uncertainties for rates above the median.

      A.1.6 Elicitation outcomes of the assessment of the pest freedom for Meloidogyne fallax

      The elicited and fitted values for M. fallax agreed by the Panel are shown in Tables A.2A.5 and in Figures A.1, A.2

      TABLE A.2. Elicited and fitted values of the uncertainty distribution of pest infestation by M. fallax per 10,000 bare-root Cornus spp. plants.
      Percentile 1% 2.5% 5% 10% 17% 25% 33% 50% 67% 75% 83% 90% 95% 97.5% 99%
      Elicited values 0 10 20 75 200
      EKE 0.0134 0.0782 0.296 1.13 3.03 6.67 11.79 27.2 51.9 69.6 93.3 121 151 176 200
      • Note: The EKE results are the BetaGeneral (0.52062, 2.3955, 0, 255) distribution fitted with @Risk version 7.6.
      Details are in the caption following the image
      (A) Elicited uncertainty of pest infestation per 10,000 bare-root Cornus spp. plants (histogram in blue–vertical blue line indicates the elicited percentile in the following order: 1%, 25%, 50%, 75%, 99%) and distributional fit (red line); (B) uncertainty of the proportion of pest-free plants per 10,000 (i.e. = 1 – pest infestation proportion expressed as percentage); (C) descending uncertainty distribution function of pest infestation per 10,000 plants.
      Details are in the caption following the image
      (A) Elicited uncertainty of pest infestation per 10,000 rooted Cornus spp. plants in pots (histogram in blue–vertical blue line indicates the elicited percentile in the following order: 1%, 25%, 50%, 75%, 99%) and distributional fit (red line); (B) uncertainty of the proportion of pest-free plants per 10,000 (i.e. = 1 – pest infestation proportion expressed as percentage); (C) descending uncertainty distribution function of pest infestation per 10,000 plants.

      Based on the numbers of estimated infested bare-root Cornus spp. plants, the pest freedom was calculated (i.e. = 10,000 – number of infested plants per 10,000). The fitted values of the uncertainty distribution of the pest freedom are shown in Table A.3.

      TABLE A.3. The uncertainty distribution of plants free of M. fallax per 10,000 bare-root Cornus spp. plants calculated by Table A.2.
      Percentile 1% 2.5% 5% 10% 17% 25% 33% 50% 67% 75% 83% 90% 95% 97.5% 99%
      Values 9800 9925 9980 9990 10,000
      EKE results 9800 9824 9849 9879 9907 9930 9948 9973 9988 9993 9997 9998.9 9999.7 9999.9 10,000
      • Note: The EKE results are the fitted values.
      TABLE A.4. Elicited and fitted values of the uncertainty distribution of pest infestation by M. fallax per 10,000 rooted Cornus spp. plants in pots.
      Percentile 1% 2.5% 5% 10% 17% 25% 33% 50% 67% 75% 83% 90% 95% 97.5% 99%
      Elicited values 0 4 8 20 50
      EKE 0.053 0.170 0.411 1.00 1.96 3.37 5.03 9.21 15.0 18.9 24.2 30.2 37.4 43.5 50.1
      • Note: The EKE results are the BetaGeneral (0.78848, 3.8978, 0, 76) distribution fitted with @Risk version 7.6.

      Based on the numbers of estimated infested rooted Cornus spp. plants in pots,, the pest freedom was calculated (i.e. = 10,000 – number of infested plants per 10,000). The fitted values of the uncertainty distribution of the pest freedom are shown in Table A.5

      TABLE A.5. The uncertainty distribution of plants free of M. fallax per 10,000 rooted Cornus spp. plants in pots calculated by Table A.4.
      Percentile 1% 2.5% 5% 10% 17% 25% 33% 50% 67% 75% 83% 90% 95% 97.5% 99%
      Values 9950 9980 9992 9996 10,000
      EKE results 9950 9957 9963 9970 9976 9981 9985 9991 9995 9997 9998 9999 9999.6 9999.8 9999.9
      • Note: The EKE results are the fitted values.

      A.1.7 References

      CABI (Centre for Agriculture and Bioscience International). (online). Datasheet Meloidogyne fallax (false Columbia root-knot nematode). https://www.cabi.org/cpc/datasheet/33241

      DEFRA (Department for Environment, Food and Rural Affairs), (online). UK risk register details for Meloidogyne fallax. https://planthealthportal.defra.gov.uk/pests-and-diseases/uk-plant-health-risk-register/viewPestRisks.cfm?cslref=164540

      DEFRA (Department for Environment Food and Rural Affairs). (2017). The nematode Meloidogyne fallax in sports turf: Symptoms, biosecurity, guidance and control. Plant Pest Factsheet, 5 pp. https://planthealthportal.defra.gov.uk/assets/factsheets/Meloidogyne-fallax-turf-biosecurity-guide-revision-date.pdf

      den Nijs, L. J. M. F., Brinkman, H., & van der Sommen, A. T. C. (2004). A Dutch contribution to knowledge on phytosanitary risk and host status of various crops for Meloidogyne chitwoodi Golden et al., 1980 and M. fallax Karssen, 1996: An overview. Nematology, 6, 303–312. https://doi.org/10.1163/1568541042360492

      EFSA (European Food Safety Authority), den Nijs, L., Camilleri, M., Diakaki, M., Schenk, M., & Vos, S. (2019). Pest survey card on Meloidogyne chitwoodi and Meloidogyne fallax. EFSA supporting publication, EN-1572. https://doi.org/10.2903/sp.efsa.2019.en-1572

      EFSA PLH Panel (EFSA Panel on Plant Health), Bragard, C., Dehnen-Schmutz, K., Di Serio, F., Jacques, M.-A., Jaques Miret, J. A., Justesen, A. F., MacLeod, A., Magnusson, C. S., Milonas, P., Navas-Cortes, J. A., Parnell, S., Potting, R., Reignault, P. L., Thulke, H.-H., Van der Werf, W., Civera, A. V., Yuen, J., Zappalà, L., … Gonthier, P., (2020). Scientific Opinion on the commodity risk assessment of Acer spp. plants from New Zealand. EFSA Journal, 18(5), 6105. https://doi.org/10.2903/j.efsa.2020.6105

      EPPO (European and Mediterranean Plant Protection Organisation). (2015). Meloidogyne fallax detected in sports turf in United Kingdom. EPPO Reporting Service No. 10-2015. https://gd.eppo.int/reporting/article-5137

      EPPO (European and Mediterranean Plant Protection Organisation). (2016). Diagnostics. PM 7/41 (3). Meloidogyne chitwoodi and M. fallax. EPPO Bulletin, 46, 171–189.

      EPPO (European and Mediterranean Plant Protection Organisation). (2019). Phytosanitary procedures. PM 3/69 (2) Meloidogyne chitwoodi and M. fallax sampling potato tubers for detection. EPPO Bulletin, 49, 486–487.

      EPPO (European and Mediterranean Plant Protection Organisation). (online_a). EPPO A2 List of pests recommended for regulation as quarantine pests, version 2021-09. https://www.eppo.int/ACTIVITIES/plant_quarantine/A2_list

      EPPO (European and Mediterranean Plant Protection Organisation). (online_b). Meloidogyne fallax (MELGFA), Categorization. https://gd.eppo.int/taxon/MELGFA/categorization

      EPPO (European and Mediterranean Plant Protection Organisation). (online_c). Meloidogyne fallax (MELGFA), Distribution. https://gd.eppo.int/taxon/MELGFA/distribution

      EPPO (European and Mediterranean Plant Protection Organisation). (online_d). Meloidogyne fallax (MELGFA), Reporting. https://gd.eppo.int/taxon/MELGFA/reporting

      EPPO (European and Mediterranean Plant Protection Organisation). (online_e). Meloidogyne fallax (MELGFA), Hosts. https://gd.eppo.int/taxon/MELGFA/hosts

      EUROPHYT. (online). European Union Notification System for Plant Health Interceptions – EUROPHYT. http://ec.europa.eu/food/plant/plant_health_biosecurity/europhyt/index_en.htm

      Nemaplex. (online). Nemaplex, Howard Ferris, Department of Entomology and Nematology, University of California (The Nematode-Plant Expert Information System). https://nemaplex.ucdavis.edu/

      Kantor, M., Handoo, Z., Kantor, C., & Carta, L. (2022). Top ten most important U.S.-regulated and emerging plant-parasitic nematodes. Horticulturae, 8(208), 1–26. https://doi.org/10.3390/horticulturae8030208

      MacLeod, A., Anderson, H., Follak, S., van der Gaag, D. J., Potting, R., Pruvost, O., Smith, J., Steffek, R., Vloutoglou, I., Holt, J., Karadjova, O., Kehlenbeck, H., Labonne, G., Reynaud, P., Viaene, N., Anthoine, G., Holeva, M., Hostachy, B., Ilieva, Z., … Wesemael, W. (2012). Pest risk assessment for the European Community plant health: A comparative approach with case studies. Cases: Meloidogyne chitwoodi and M. fallax. EFSA Supporting publication, EN-319. www.efsa.europa.eu/publications

      Moens, M., Perry, R. N., & Starr, J. L. (2009). Meloidogyne species–a diverse group of novel and important plant parasites. In: Perry, R. N., Moens, M., Starr, J. L., (eds.). Root-Knot Nematodes. CABI, California, USA, 1–17. https://doi.org/10.1079/9781845934927.0001

      Riffle, J. W. (1963). Meloidogyne ovalis (Nematoda: Heteroderidae), A new species of root-knot nematode. Helminthological Society of Washington, 30(2), 287–292.

      TRACES-NT. (online). TRAde Control and Expert System. https://webgate.ec.europa.eu/tracesnt

      A.2 Phytophthora ramorum

      A.2.1 Organism information

      Taxonomic information

      Current valid scientific name: Phytophthora ramorum

      Synonyms: –

      Name used in the EU legislation: Phytophthora ramorum (non-EU isolates) Werres, De Cock & Man in ‘t Veld [PHYTRA]

      Order: Peronosporales

      Family: Peronosporaceae

      Common name: Sudden oak death (SOD), ramorum bleeding canker, ramorum blight, ramorum leaf blight, twig and leaf blight

      Name used in the Dossier: Phytophthora ramorum

      Group Oomycetes
      EPPO code PHYTRA
      Regulated status

      P. ramorum is listed in Annex II of Commission Implementing Regulation (EU) 2019/2072 as Phytophthora ramorum (non-EU isolates) Werres, De Cock & Man in ‘t Veld [PHYTRA]. The EU isolates of P. ramorum are listed as regulated non-quarantine pest (RNQP)

      P. ramorum is included in the EPPO A2 list (EPPO, online_a)

      P. ramorum is quarantine in Canada, Israel, Mexico, Morocco and the United Kingdom. It is on A1 list of Brazil, Chile, Egypt, Kazakhstan, Türkiye and EAEU (=Eurasian Economic Union: Armenia, Belarus, Kazakhstan, Kyrgyzstan and Russia) (EPPO, online_b)

      Pest status in the UK

      P. ramorum is present in the UK (Brown and Brasier, 2007; Dossier Sections 1.0 and 2.0; CABI, online; EPPO, online_c)

      According to the Dossier Section 2.0, P. ramorum is present in the UK (non-EU isolates): not widely distributed and under official control. It has been found in most regions of the UK, but it is more often reported in wetter, western regions

      Pest status in the EU P. ramorum is present in the EU and it is currently reported in the following EU Member States: Belgium, Croatia, Denmark, Finland, France, Germany, Ireland, the Netherlands, Poland, Portugal and Slovenia (EPPO, online_c)
      Host status on Cornus Some Cornus species are reported as natural hosts of the pathogen and Cornus sanguinea showed susceptibility (low) (Cave et al., 2008; EPPO, online; Goss et al., 2011)
      PRA information

      Pest Risk Assessments available:

      • Risk analysis for P. ramorum Werres, de Cock & Man in't Veld, causal agent of sudden oak death, ramorum leaf blight and ramorum dieback (Cave et al., 2008);
      • Risk analysis of P. ramorum, a newly recognised pathogen threat to Europe and the cause of sudden oak death in the USA (Sansford et al., 2009);
      • Scientific opinion on the pest risk analysis on P. ramorum prepared by the FP6 project RAPRA (EFSA PLH Panel, 2011);
      • Pest risk management for P. kernoviae and P. ramorum (EPPO, 2013);
      • UK Risk Register Details for P. ramorum (DEFRA, online_a).

      Risk analysis for P. ramorum Werres, de Cock & Man in't Veld, causal agent of sudden oak death, ramorum leaf blight and ramorum dieback. US Department of Agriculture, Animal and Plant Health Inspection Service, Raleigh, NC (Cave et al., 2008)

      Other relevant information for the assessment
      Biology

      P. ramorum is most probably native to East Asia (Jung et al., 2021; Poimala and Lilja, 2013). The pathogen is present in Asia (Japan, Vietnam), Europe (Belgium, Croatia, Denmark, Finland, France, Germany, Guernsey, Ireland, Luxembourg, the Netherlands, Norway, Poland, Portugal, Slovenia, the UK), North America (Canada, US) and South America (Argentina) (EPPO, online_c). So far, there are 12 known lineages of P. ramorum: NA1 and NA2 from North American, EU1 from Europe (including the UK) and North America (Grünwald et al., 2009), EU2 from Northern Ireland and western Scotland (Van Poucke et al., 2012), IC1 to IC5 from Vietnam and NP1 to NP3 from Japan (Jung et al., 2021)

      P. ramorum is heterothallic oomycete species belonging to clade 8c (Blair et al., 2008) with two mating types: A1 and A2 (Boutet et al., 2010)

      Phytophthora species generally reproduce through: (a) dormant (resting) spores, which can be either sexual (oospores) or asexual (chlamydospores); and (b) fruiting structures (sporangia), which contain zoospores (Erwin and Ribeiro, 1996)

      P. ramorum produces sporangia on the surfaces of infected leaves and twigs of host plants. These sporangia can be splash-dispersed to other close or carried by wind and rain to longer distances. The sporangia germinate to produce zoospores that penetrate and initiate an infection on new hosts. In infected plant material the chlamydospores are produced and can serve as resting structures (Davidson et al., 2005; Grünwald et al., 2008). Trunk cankers (e.g. on Quercus, Fagus) are not known to support sporulation and therefore do not transmit the pathogen (DEFRA, online_a). The pathogen is also able to survive in soil (Shishkoff, 2007). In the west of Scotland, it persisted in soil for at least 2 years after its hosts were removed (Elliot et al., 2013). Oospores were only observed in pairing tests under controlled laboratory conditions (Brasier and Kirk, 2004). Optimal temperatures under laboratory conditions were 16–26°C for growth, 14–26°C for chlamydospore production and 16–22°C for sporangia production (Englander et al., 2006)

      P. ramorum is mainly a foliar pathogen; however, it was also reported to infect shoots, stems and occasionally the roots of various host plants (Grünwald et al, 2008, Parke and Lewis, 2007). According to Brown and Brasier (2007), P. ramorum commonly occupies xylem beneath phloem lesions and may spread within xylem and possibly recolonise the phloem from the xylem. P. ramorum can remain viable within xylem for two or more years after the overlying phloem had been excised

      P. ramorum can disperse by aerial dissemination, water, movement of infested plant material and soil containing propagules on footwear, tires of trucks and mountain bikes or the feet of animals (Brasier, 2008; Davidson et al., 2002)

      Infected foliar hosts can be a major source of inoculum, which can lead to secondary infections on nearby host plants. Important foliar hosts in Europe are Rhododendron spp. and Larix kaempferi (Brasier and Webber, 2010, Grünwald et al., 2008).

      Possible pathways of entry for P. ramorum are plants for planting (excluding seed and fruit) of known susceptible hosts; plants for planting (excluding seed and fruit) of non-host plant species accompanied by contaminated attached growing media; soil/growing medium (with organic matter) as a commodity; soil as a contaminant; foliage or cut branches; susceptible (isolated) bark; and susceptible wood (EFSA PLH Panel, 2011).

      P. ramorum caused rapid decline of Lithocarpus densiflorus and Quercus agrifolia in forests of California and Oregon (Rizzo et al., 2005) and Larix kaempferi in plantations of southwest England (Brasier and Webber, 2010)

      Symptoms Main type of symptoms

      P. ramorum causes different types of symptoms depending on the host species and the plant tissue infected

      According to DEFRA (online_a) P. ramorum causes three different types of disease:

      1. ‘Ramorum bleeding canker’ – cankers on trunks of trees, which emit a dark ooze. As they increase in size they can lead to tree death.
      2. ‘Ramorum leaf blight’ – infection of the foliage, leading to discoloured lesions on the leaves.
      3. ‘Ramorum dieback’ – shoot and bud infections which result in wilting, discolouration and dying back of affected parts.

      Symptoms on Cornus capitata and C. kousa x C. capitata have been described as leaf blight (DEFRA, online_b).

      Presence of asymptomatic plants

      If roots are infected by P. ramorum, the plants can be without above-ground symptoms for months until developmental or environmental factors trigger disease expression (Roubtsova and Bostock, 2009; Thompson et al., 2021)

      Application of some fungicides may reduce symptoms and therefore mask infection, making it more difficult to determine whether the plant is pathogen-free (DEFRA, online_a)

      Confusion with other pests

      Various symptoms caused by P. ramorum can be confused with other pathogens, such as canker and foliar symptoms caused by other Phytophthora species (P. cinnamomi, P. cambivora, P. citricola and P. cactorum); leaf lesions caused by rust in early stages; leafspots caused by sunburn; and dieback of twigs and leaves caused by Botryosphaeria dothidea (Davidson et al., 2003)

      P. ramorum can be easily distinguished from other Phytophthora species based on morphology (Grünwald et al., 2008) and molecular tests

      Host plant range

      P. ramorum has a very wide host range, which is expanding

      Main host plants include Camellia spp., Larix decidua, L. kaempferi, Pieris spp., Rhododendron spp., Syringa vulgaris, Viburnum spp. and the North American trees species, Lithocarpus densiflorus and Quercus agrifolia (EPPO online_d)

      Further proven hosts confirmed by Koch's postulates are Abies grandis, A. magnifica, Acer circinatum, A. macrophyllum, A. pseudoplatanus, Adiantum aleuticum, A. jordanii, Aesculus californica, A. hippocastanum, Arbutus menziesii, Arbutus unedo, Arctostaphylos columbiana, Agrostis glauca, A. hooveri, A. manzanita, A. montereyensis, A. morroensis, A. pilosula, A. pumila, A. silvicola, A. viridissima, Calluna vulgaris, Castanea sativa, Ceanothus thyrsiflorus, Chamaecyparis lawsoniana, Chrysolepis chrysophylla, Cinnamomum camphora, Cornus kousa, Cornus hybrids, Corylus cornuta, Fagus sylvatica, Frangula californica, Frangula purshiana, Fraxinus excelsior, Gaultheria procumbens, G. shallon, Griselinia littoralis, Hamamelis virginiana, Heteromeles arbutifolia, Kalmia spp., Larix × eurolepis, Laurus nobilis,, Lonicera hispidula, Lophostemon confertus, Loropetalum chinense, Magnolia × loebneri, M. oltsopa, M. stellata, Mahonia aquifolium, Maianthemum racemosum, Parrotia persica, Photinia fraseri, Phoradendron serotinum subsp. macrophyllum, Photinia × fraseri, Prunus laurocerasus, Pseudotsuga menziesii var. menziesii,, Quercuscerris, Q. chrysolepis, Q. falcata Q. ilex, Q. kelloggii, Q. parvula var. shrevei,, Rosa gymnocarpa, Salix caprea, Sequoia sempervirens,, Taxus baccata, Trientalis latifolia, Umbellularia californica, Vaccinium myrtillus, V. ovatum, V. parvifolium and Vinca minor (APHIS USDA, 2022; Cave et al., 2008; EPPO, online d)

      Reported evidence of impact P. ramorum is an EU quarantine pest
      Evidence that the commodity is a pathway P. ramorum is continuously intercepted in the EU on different plant species intended for planting (EUROPHYT/TRACES-NT, online), and according to EFSA PLH Panel (2011), P. ramorum can travel with plants for planting. Therefore, plants for planting of Cornus are possible pathway for P. ramorum
      Surveillance information

      P. ramorum at growing sites: infested plants are destroyed, and potentially infested plants are ‘held’ (prohibited from moving). The UK has a containment policy in the wider environment, with official action taken to remove infected trees (Dossier Section 1.0)

      As part of an annual survey at ornamental retail and production sites (frequency of visits determined by a decision matrix), P. ramorum is inspected on common host plants. An additional inspection, during the growing period, is carried out at plant passport production sites. Inspections are carried out at a survey to 300 non-woodland wider environment sites annually (Dossier Sections 1.0)

      A.2.2 Possibility of pest presence in the nursery

      A.2.2.1 Possibility of entry from the surrounding environment

      P. ramorum is present in the UK, it has been found in most regions of the UK, but it is more often reported in wetter, western regions (Dossier Sections 1.0 and 2.0).

      The possible entry of P. ramorum from surrounding environment to the nurseries may occur through aerial dissemination, water and animals (Davidson et al., 2002).

      P. ramorum has a wide host range and can infect a number of different plants. Suitable hosts of P. ramorum like Fagus spp., Ilex spp., Quercus spp., Taxus spp., Castanea spp., spp. (especially L. kaempferi), Magnolia spp., Prunus spp., Quercus spp., spp., Rosa spp., Salix spp., Syringa spp. and Viburnum spp. are present in the areas surrounding the nurseries (Dossier Section 1.0).

      Uncertainties:
      • The dispersal range of P. ramorum sporangia.
      • No information available on the distance of the nurseries to sources of pathogen in the surrounding environment.

      Taking into consideration the above evidence and uncertainties, the Panel considers that it is possible for the pathogen to enter the nurseries from surrounding environment. In the surrounding area, suitable hosts are present, and the pathogen can spread by wind, rain and infested soil propagules on the feet of animals entering the nurseries.

      A.2.2.2 Possibility of entry with new plants/seeds

      The starting materials are either seeds or seedlings. Seedlings are either from the UK or the EU (the Netherlands) (Dossier Section 1.0). Seeds are not a pathway for the pathogen.

      In addition to Cornus spp. plants, the nurseries also produce other plants (Dossier Section 6.0). Out of them, there are many suitable hosts for the pathogen (such as Abies spp., Acer spp., Aesculus spp., Arbutus spp., Calluna spp., Castanea spp., Fagus spp., Viburnum spp. etc.). However, there is no information on how and where the plants are produced. Therefore, if the plants are first produced in another nursery, the pathogen could possibly travel with them.

      For the potted plants, the nurseries are using virgin peat or peat-free compost (a mixture of coir, tree bark, wood fibre etc.) as a growing media (Dossier Section 1.0). P. ramorum is able to survive in soil (Shishkoff, 2007) and therefore could potentially enter with infested soil/growing media. However, the growing media is certified and heat-treated by commercial suppliers during production to eliminate pests and diseases (Dossier Section 3.0).

      Uncertainties:
      • No information is available on the origin of plants other than Cornus spp. used for plant production in the nurseries.
      • The effectiveness of removing all soil with a low-pressure washer.

      Taking into consideration the above evidence and uncertainties, the Panel considers that it is possible for the pathogen to enter the nurseries with new seedlings of Cornus spp. and new plants of other species used for plant production in the area. The Panel considers the entry of the pathogen with seeds and the growing media as not possible.

      A.2.2.3 Possibility of spread within the nursery

      Cornus spp. plants are either grown in containers (cells, pots, tubes etc.) or in field. Cell-grown trees may be grown in greenhouses; however, most plants will be field grown, or grown in open air in containers (Dossier Section 1.0).

      The pathogen can infect other suitable plants (such as Abies spp., Aesculus spp., Castanea spp., Larix spp., Viburnum spp. etc.) present within the nurseries and hedges surrounding the nurseries (Prunus spp.) (Dossier Sections 1.0).

      P. ramorum can spread within the nurseries by aerial dissemination/water splash: via soil, water, movement of infested plant material (e.g. infested leaves) and animals/humans (Davidson et al., 2002).

      Uncertainties: None.

      Taking into consideration the above evidence and uncertainties, the Panel considers that the spread of the pathogen within the nurseries is possible either by aerial dissemination, animals, movement of infected plant material, soil or water.

      A.2.3 Information from interceptions

      In the EUROPHYT/TRACES-NT database, there are no records of interceptions of P. ramorum on Cornus spp. from third countries or on any other plant from the UK.

      A.2.4 Evaluation of the risk mitigation measures

      In the table below (Table A.6), all risk mitigation measures currently applied in the UK are listed, and an indication of their effectiveness on P. ramorum is provided. The description of the risk mitigation measures currently applied in the UK is provided in the Table 9.

      A.2.5 Overall likelihood of pest freedom for Cornus spp. plants (bare-root and rooted plants in pots)

      A.2.5.1 Reasoning for a scenario which would lead to a reasonably low number of infected Cornus spp. plants (bare-root and rooted plants in pots)

      • P ramorum outbreaks are more frequent in the Western part of the country (the nurseries are in the Eastern part).
      • The climate suitability for the pathogen in the Eastern UK, where the nurseries are located, is low (dryer climate compared to the Western part).
      • The pathogen has not been found on C. alba and C. sanguinea. Cornus alba has shown to be resistant to the pathogen in experiments.
      • The pathogen is causing clear symptoms (leave blight), and it is easy to detect.
      • There is official surveillance of Cornus spp. nurseries.
      • Seeds are not a pathway, seedlings of Cornus spp. are certified with the UK plant passport.
      • Clean new material is used for potted plants.
      • Root washing effectively removes the soil aggregates.
      • Irrigation water is regularly checked.
      • Some of the applied Plant Protection Products may be effective in controlling the pathogen.
      • Official inspections.

      A.2.5.2 Reasoning for a scenario which would lead to a reasonably high number of infected Cornus spp. plants (bare-root and rooted plants in pots)

      • P. ramorum is present in all regions of the UK (including nurseries).
      • Some Cornus species are natural hosts of the pathogen, and Cornus sanguinea showed susceptibility (low) in experiments.
      • Plants can be symptomless with a latent period of some months.
      • The pathogen can be confused with other Phytophthora species.
      • The measures adopted after the detection of the pathogen are unclear, nor results are reported; unclear efficiency.
      • Other host plants can be present in the surrounding.
      • Irrigation is applied (also overhead), and pathogens can be spread.
      • Contamination during production (in the nursery) is possible.
      • Root washing does not effectively remove the soil aggregates.
      • The Plant Protection Products used in the nurseries are not targeted to the control of P. ramorum.
      • Unclear details and efficiency of the inspections.

      A.2.5.3 Reasoning for a central scenario equally likely to over-or underestimate the number of infected Cornus spp. plants (bare-root and rooted plants in pots) (median)

      The scenario assumes a limited presence of the pathogen in the nurseries and the surroundings, and a limited susceptibility of Cornus spp. The pathogen is a regulated quarantine pest in the UK and under official control.

      A.2.5.4 Reasoning for the precision of the judgement describing the remaining uncertainties (1st and 3rd quartile/interquartile range)

      The limited information on the susceptibility of Cornus spp. and on the occurrence of the pathogen in the nurseries and the surroundings results in a high level of uncertainties for infestation rates below the median. Otherwise, the pest pressure from the surroundings is expected to be low, giving less uncertainties for rates above the median.

      A.2.6 Elicitation outcomes of the assessment of the pest freedom for Phytophthora ramorum

      The elicited and fitted values for P. ramorum agreed by the Panel are shown in Tables A.7A.10 and in Figures A.3, A.4.

      TABLE A.6. Evaluation of the risk mitigation measures.
      Number Risk mitigation measure Effect on the pest Evaluation and uncertainties
      1 Registration of production sites Yes

      All nurseries are registered as professional operator with the UK NPPO, by the Animal and Plant Health Agency (APHA) and is authorised to issue UK plant passports (Dossier Section 1.0)

      Evaluation: The registration of production sites is expected to contribute in reducing the phytosanitary risks within the facility

      Uncertainties: None

      2 Certified plant material Yes

      Seeds of C. alba are not certified, while seeds of C. sanguinea seed purchased in the UK may be certified under the Forestry Commission's Voluntary Scheme for the Certification of Native Trees and Shrubs. Seedlings for Cornus production sourced in the UK are certified with UK Plant Passports; seedlings from the EU countries are certified with phytosanitary certificates

      Evaluation: P. ramorum is a quarantine pest and targeted by this measure and could reduce the infection level. Seeds are not a pathway

      Uncertainties:

      – The details of the procedure are not clear

      – If propagation material of alternative hosts is covered is not clear

      3 Certification of substrates/ (rooted plant in pots) Yes

      Rooted plants in pots: In the production or procurement of these plants, the use of growing media is assessed for the potential to harbour and transmit plant pests. Growers most commonly use virgin peat or peat-free compost, which is a mixture of coir, tree bark, wood fibre etc. The compost is heat-treated by commercial suppliers during production to eliminate pests and diseases. It is supplied in sealed bulk bags or shrink-wrapped bales and stored off the ground on pallets, these are completely hygienic and free from contamination. Where delivered in bulk, compost is kept in a dedicated bunker, either indoors or covered by tarpaulin outdoors, and with no risk of contamination with soil or other material (Dossier Section 1.0)

      Evaluation: The measure is efficient in preventing the entry of the pathogen via the substrate into the nursery

      Uncertainties: None

      4 Surveillance, monitoring and sampling Yes

      In the last 3 years, there has been a substantial level of inspection of registered Cornus spp. producers, both in support of the Plant Passporting scheme (checks are consistent with EU legislation, with a minimum of once a year for authorised operators) and as part of the Quarantine Surveillance programme (Great Britain uses the same framework for its surveillance programme as the EU). The Competent Authority inspects crops at least once a year to check if they meet the standards set out in the guides (Dossier Section 1.0)

      UK(GB) surveillance is based on visual inspection with samples taken from symptomatic material, and where appropriate, samples are also taken from asymptomatic material (e.g. plants, tubers, soil, watercourses) (Dossier Section 1.0)

      Evaluation: The surveillance, monitoring and sampling can detect the pathogen

      Uncertainties:

      • The efficiency of the surveillance, monitoring and sampling
      • No results are reported.

      5 Hygiene measures Yes

      All nurseries have plant hygiene and housekeeping rules and practices in place, which are communicated to all relevant employees. The rules will be dependent on the plants handled and the type of business but will include:

      • Growing media
      • Weed management
      • Water usage
      • Cleaning and sterilisation
      • Waste treatment and disposal
      • Visitors

      Evaluation: These measures could be effective in reducing the risk of introduction and/or spread of the pathogen

      Uncertainties: The efficiency of the hygiene measures

      6 Irrigation water quality and/or treatments Yes

      Growers are required to assess water sources, irrigation and drainage systems used in the plant production for the potential to harbour and transmit plant pests. Water is routinely sampled and sent for analysis. No quarantine pests have been found (Dossier Section 1.0)

      Evaluation: The irrigation water is routinely checked and can reduce the risk

      Uncertainties: The frequency and the method used for the detection on the pathogen

      7 Application of pest control products Yes

      Crop protection is achieved using a combination of measures including approved plant protection products, biological control or physical measures. Plant protection products are only used when necessary and records of all plant protection treatments are kept. (Dossier Section 1.0).

      Evaluation: The listed treatments are not sufficiently effective against P. ramorum

      Uncertainties: The details about the products applied and the application scheme are unknown and the efficiency is unclear

      8 Washing of the roots (bare-root plants) Yes

      Bare-root plants are lifted from the field in winter and then root-washed on site and stored prior to expert

      Evaluation: The washing of the roots removes (parts of) the soil and thus also the pathogen

      Uncertainties: The effectiveness of the washing to remove all soil with the pathogen

      9 Inspections and management of plants before export Yes

      The UK NPPO carries out inspections and testing where required by the country of destination's plant health legislation, to ensure all requirements are fulfilled and a valid phytosanitary certificate with the correct additional declarations is issued

      Separate to any official inspection, plant material is checked by growers for plant health issues before dispatch

      Special provision for inspection of P. ramorum is in place

      Evaluation: The inspections and management of plants before export can detect the pathogen

      Uncertainties: The efficiency of the inspections

      TABLE A.7. Elicited and fitted values of the uncertainty distribution of pest infection by P. ramorum per 10,000 bare-root Cornus spp. plants.
      Percentile 1% 2.5% 5% 10% 17% 25% 33% 50% 67% 75% 83% 90% 95% 97.5% 99%
      Elicited values 1 10 20 100 200
      EKE 0.991 1.00 1.06 1.41 2.65 5.83 11.4 31.6 67.4 92.2 123 152 177 191 200
      • Note: The EKE results are the BetaGeneral (0.37655, 1.0565, 0.99, 207) distribution fitted with @Risk version 7.6.
      Details are in the caption following the image
      (A) Elicited uncertainty of pest infection per 10,000 bare-root plants Cornus spp. (histogram in blue–vertical blue line indicates the elicited percentile in the following order: 1%, 25%, 50%, 75%, 99%) and distributional fit (red line); (B) uncertainty of the proportion of pest-free plants per 10,000 (i.e. = 1 – pest infection proportion expressed as percentage); (C) descending uncertainty distribution function of pest infection per 10,000 plants.
      Details are in the caption following the image
      (A) Elicited uncertainty of pest infection per 10,000 rooted Cornus spp. plants in pots (histogram in blue–vertical blue line indicates the elicited percentile in the following order: 1%, 25%, 50%, 75%, 99%) and distributional fit (red line); (B) uncertainty of the proportion of pest-free plants per 10,000 (i.e. = 1 – pest infection proportion expressed as percentage); (C) descending uncertainty distribution function of pest infection per 10,000 plants.

      Based on the numbers of estimated infected bare-root Cornus spp. plants, the pest freedom was calculated (i.e. = 10,000 – number of infected plants per 10,000). The fitted values of the uncertainty distribution of the pest freedom are shown in Table A.8.

      TABLE A.8. The uncertainty distribution of plants free of P. ramorum per 10,000 bare-root Cornus spp. plants calculated by Table A.7.
      Percentile 1% 2.5% 5% 10% 17% 25% 33% 50% 67% 75% 83% 90% 95% 97.5% 99%
      Values 9800 9900 9980 9990 9999
      EKE results 9800 9809 9823 9848 9877 9908 9933 9968 9989 9994 9997 9998.6 9998.9 9999.00 9999.01
      • Note: The EKE results are the fitted values.
      TABLE A.9. Elicited and fitted values of the uncertainty distribution of pest infection by P. ramorum per 10,000 rooted Cornus spp. plants in pots.
      Percentile 1% 2.5% 5% 10% 17% 25% 33% 50% 67% 75% 83% 90% 95% 97.5% 99%
      Elicited values 0 4 8 16 40
      EKE 0.167 0.395 0.762 1.49 2.48 3.77 5.17 8.43 12.7 15.6 19.4 23.8 29.3 34.2 40.0
      • Note: The EKE results are the BetaGeneral (1.0764, 6.8505, 0, 80) distribution fitted with @Risk version 7.6.

      Based on the numbers of estimated infected rooted Cornus spp. plants in pots, the pest freedom was calculated (i.e. = 10,000 – number of infected plants per 10,000). The fitted values of the uncertainty distribution of the pest freedom are shown in Table A.10.

      TABLE A.10. The uncertainty distribution of plants free of P. ramorum per 10,000 rooted Cornus spp. plants in pots calculated by Table A.9.
      Percentile 1% 2.5% 5% 10% 17% 25% 33% 50% 67% 75% 83% 90% 95% 97.5% 99%
      Values 9960 9984 9992 9996 10,000
      EKE results 9960 9966 9971 9976 9981 9984 9987 9992 9995 9996 9997.5 9998.5 9999.2 9999.6 9999.8
      • Note: The EKE results are the fitted values.

      A.2.7 References

      APHIS USDA (Animal and Plant Health Inspection Service U.S. Department of Agriculture). (2022). APHIS Lists of Proven Hosts of and Plants Associated with Phytophthora ramorum. September 2022. 12 pp. https://www.aphis.usda.gov/plant_health/plant_pest_info/pram/downloads/pdf_files/usdaprlist.pdf

      Blair, J. E., Coffey, M. D., Park, S. Y., Geiser, D. M., & Kang, S. (2008). A multi-locus phylogeny for Phytophthora utilising markers derived from complete genome sequences. Fungal Genetics and Biology, 45(3), 266–277. https://doi.org/10.1016/j.fgb.2007.10.010

      Boutet, X., Vercauteren, A., Heungens, C., & Kurt A. (2010). Mating of Phytophthora ramorum: functionality and consequences. In: Frankel, S. J., Kliejunas, J. T., & Palmieri, K. M. (eds.), Proceedings of the Sudden Oak Death Fourth Science Symposium. Albany, CA: US Department of Agriculture, Forest Service, Pacific Southwest Research Station, 229, 97–100.

      Brasier C. (2008). Phytophthora ramorum + P. kernoviae = international biosecurity failure. In: Frankel, S. J., Kliejunas, J. T., Palmieri, K. M. (eds.), Proceedings of the sudden oak death third science symposium. USDA Forest Service, Pacific Southwest Research Station, Albany, CA: US Department of Agriculture, 214, 133–139.

      Brasier, C., & Kirk, S. (2004). Production of gametangia by Phytophthora ramorum in vitro. Mycological Research, 108(7), 823–827. https://doi.org/10.1017/s0953756204000565

      Brasier, C., & Webber, J. (2010). Sudden larch death. Nature, 466, 824–825. https://doi.org/10.1038/466824a

      Brown, A. V., & Brasier, C. M. (2007). Colonisation of tree xylem by Phytophthora ramorum, P. kernoviae and other Phytophthora species. Plant Pathology, 56(2), 227–241. https://doi.org/10.1111/j.1365-3059.2006.01511.x

      CABI (Centre for Agriculture and Bioscience International). (online). Phytophthora ramorum (Sudden Oak Death (SOD)). https://www.cabi.org/cpc/datasheet/40991

      Cave, G. L., Randall-Schadel, B., & Redlin, S. C. (2008). Risk analysis for Phytophthora ramorum Werres, de Cock & Man in’t Veld, causal agent of sudden oak death, ramorum leaf blight, and ramorum dieback. US Department of Agriculture, Animal and Plant Health Inspection Service, Raleigh, NC. 88 pp.

      Davidson, J. M., Rizzo, D. M., Garbelotto, M., Tjosvold, S., & Slaughter, G. W. (2002). Phytophthora ramorum and sudden oak death in California: II. Transmission and survival. In: Standiford, R. B., McCreary, D., & Purcell, K. L. (eds.). Proceedings of the fifth symposium on oak woodlands: Oaks in California's challenging landscape. San Diego, California, US Department of Agriculture, Forest Service, Pacific Southwest Research Station, 184, 741-749.

      Davidson, J. M., Werres, S., Garbelotto, M., Hansen, E. M., & Rizzo, D. M. (2003). Sudden oak death and associated diseases caused by Phytophthora ramorum. Plant Health Progress, 4(1), 12. https://doi.org/10.1094/php-2003-0707-01-dg

      Davidson, J. M., Wickland, A. C., Patterson, H. A., Falk, K. R., & Rizzo, D. M. (2005). Transmission of Phytophthora ramorum in mixed-evergreen forest in California. Phytopathology, 95, 587–596. https://doi.org/10.1094/phyto-95-0587

      DEFRA (Department for Environment, Food and Rural Affairs), (online_a). UK Risk Register Details for Phytophthora ramorum. https://planthealthportal.defra.gov.uk/pests-and-diseases/uk-plant-health-risk-register/viewPestRisks.cfm?cslref=23022

      DEFRA (Department for Environment, Food and Rural Affairs), (online_b). Fera list of natural hosts for Phytophthora ramorum with symptom and location. https://planthealthportal.defra.gov.uk/assets/uploads/P-ramorum-host-list-finalupdate-NOV-20-15.pdf

      EFSA PLH Panel (EFSA Panel on Plant Health). (2011). Scientific Opinion on the Pest Risk Analysis on Phytophthora ramorum prepared by the FP6 project RAPRA. EFSA Journal, 9(6), 2186. https://doi.org/10.2903/j.efsa.2011.2186

      Elliot, M., Meagher, T. R., Harris, C., Searle, K., Purse, B. V., & Schlenzig, A. (2013). The epidemiology of Phytophthora ramorum and P. kernoviae at two historic gardens in Scotland. In: Frankel, S. J., Kliejunas, J. T., Palmieri, K. M., & Alexander, J. M. (eds.). Sudden oak death fifth science symposium. Albany, CA, USA: US Department of Agriculture, Forest Service, Pacific Southwest Research Station, 23–32.

      Englander, L., Browning, M., & Tooley, P. W. (2006). Growth and sporulation of Phytophthora ramorum in vitro in response to temperature and light. Mycologia, 98(3), 365–373. https://doi.org/10.3852/mycologia.98.3.365

      EPPO (European and Mediterranean Plant Protection Organisation). (2013). Pest risk management for Phytophthora kernoviae and Phytophthora ramorum. EPPO, Paris. https://www.eppo.int/QUARANTINE/Pest_Risk_Analysis/PRA_intro.htm

      EPPO (European and Mediterranean Plant Protection Organisation). (online_a). EPPO A2 List of pests recommended for regulation as quarantine pests, version 2021-09. https://www.eppo.int/ACTIVITIES/plant_quarantine/A2_list

      EPPO (European and Mediterranean Plant Protection Organisation). (online_b). Phytophthora ramorum (PHYTRA), Categorization. https://gd.eppo.int/taxon/PHYTRA/categorization

      EPPO (European and Mediterranean Plant Protection Organisation). (online_c). Phytophthora ramorum (PHYTRA), Distribution. https://gd.eppo.int/taxon/PHYTRA/distribution

      EPPO (European and Mediterranean Plant Protection Organisation). (online_d). Phytophthora ramorum (PHYTRA), Host plants. https://gd.eppo.int/taxon/PHYTRA/hosts

      EPPO (European and Mediterranean Plant Protection Organisation). (online_e). Phytophthora ramorum (PHYTRA), Photos. https://gd.eppo.int/taxon/PHYTRA/photos

      Erwin, D. C., & Ribeiro, O. K. (1996). Phytophthora diseases worldwide. St. Paul, Minnesota: APS Press, American Phytopathological Society, 562.

      EUROPHYT. (online). European Union Notification System for Plant Health Interceptions – EUROPHYT. https://ec.europa.eu/food/plant/plant_health_biosecurity/europhyt/index_en.htm

      Goss, E. M., Larsen, M., Vercauteren, A., Werres, S., Heungens, K., & Grunwald, N. J. (2011). Phytophthora ramorum in Canada: Evidence for migration within North America and from Europe. Phytopathology, 101, 166-171.

      Grünwald, N. J., Goss, E. M., & Press, C. M. (2008). Phytophthora ramorum: a pathogen with a remarkably wide host range causing sudden oak death on oaks and ramorum blight on woody ornamentals. Molecular Plant Pathology, 9(6), 729–740. https://doi.org/10.1111/j.1364-3703.2008.00500.x

      Grünwald, N. J., Goss, E. M., Ivors, K., Garbelotto, M., Martin, F. N., Prospero, S., Hansen, E., Bonants, P. J. M., Hamelin, R. C., Chastagner, G., Werres, S., Rizzo, D. M., Abad, G., Beales, P., Bilodeau, G. J., Blomquist, C. L., Brasier, C., Brière, S. C., Chandelier, A., … Widmer, T. L. (2009). Standardising the nomenclature for clonal lineages of the sudden oak death pathogen, Phytophthora ramorum. Phytopathology, 99(7), 792–795.

      Jung, T., Jung, M. H., Webber, J. F., Kageyama, K., Hieno, A., Masuya, H., Uematsu, S., Pérez-Sierra, A., Harris, A. R., Forster, J., Rees, H., Scanu, B., Patra, S., Kudláček, T., Janoušek, J., Corcobado, T., Milenković, I., Nagy, Z., Csorba, I., Bakonyi, J., & Brasier, C. M. (2021). The destructive tree pathogen Phytophthora ramorum originates from the laurosilva forests of East Asia. Journal of Fungi, 7(3), 226, 32 pp. https://doi.org/10.3390/jof7030226

      Parke, J. L., & Lewis, C. (2007). Root and stem infection of Rhododendron from potting medium infested with Phytophthora ramorum. Plant Disease, 91, 1265–1270. https://doi.org/10.1094/pdis-91-10-1265

      Poimala, A., & Lilja, A. (2013). NOBANIS – Invasive Alien Species Fact Sheet – Phytophthora ramorum. From: Online Database of the European Network on Invasive Alien Species. 14 pp. https://www.nobanis.org/globalassets/speciesinfo/p/phytophthora-ramorum/phytophthora_ramorum.pdf

      Rizzo, D. M., Garbelotto, M., & Hansen, E. M. (2005). Phytophthora ramorum: integrative research and management of an emerging pathogen in California and Oregon forests. Annual Review of Phytopathology, 43(1), 13.1–13.27. https://doi.org/10.1146/annurev.phyto.42.040803.140418

      Roubtsova, T. V., & Bostock, R. M. (2009). Episodic abiotic stress as a potential contributing factor to onset and severity of disease caused by Phytophthora ramorum in Rhododendron and Viburnum. Plant Disease, 93(9), 912–918. https://doi.org/10.1094/pdis-93-9-0912

      Sansford, C. E., Inman, A. J., Baker, R., Brasier, C., Frankel, S., de Gruyter, J., Husson, C., Kehlenbeck, H., Kessel, G., Moralejo, E., Steeghs, M., Webber, J., & Werres, S. (2009). Report on the risk of entry, establishment, spread and socio-economic loss and environmental impact and the appropriate level of management for Phytophthora ramorum for the EU. Deliverable Report 28. EU Sixth Framework Project RAPRA. 310 pp.

      Shishkoff, N. (2007). Persistence of Phytophthora ramorum in soil mix and roots of nursery ornamentals. Plant Disease, 91(10), 1245–1249. https://doi.org/10.1094/pdis-91-10-1245

      Thompson, C. H., McCartney, M. M., Roubtsova, T. V., Kasuga, T., Ebeler, S. E., Davis, C. E., & Bostock, R. M. (2021). Analysis of volatile profiles for tracking asymptomatic infections of Phytophthora ramorum and other pathogens in Rhododendron. Phytopathology, 111(10), 1818–1827. https://doi.org/10.1094/phyto-10-20-0472-r

      TRACES-NT. (online). TRAde Control and Expert System. https://webgate.ec.europa.eu/tracesnt

      Van Poucke, K., Franceschini, S., Webber, J., Vercauteren, A., Turner, J. A., Mccracken, A. R., Heungens, K., & Brasier, C. (2012). Discovery of a fourth evolutionary lineage of Phytophthora ramorum: EU2. Fungal Biology, 116, 1178–1191. https://doi.org/10.1016/j.funbio.2012.09.003

      A.3 Nepoviruses [tomato ringspot virus (ToRSV) and tobacco ringspot virus (TRSV)]

      A.3.1 Organism information

      Taxonomic information

      Order: Picornavirales

      Family: Secoviridae

      Genus: Nepovirus

      Reasons for clustering: The below listed viruses belong in the same genus (Nepovirus) and they share the same biology and epidemiology characteristics.

      The cluster contains tomato ringspot virus (ToRSV) and tobacco ringspot virus (TRSV).

      1. Tomato ringspot virus (ToRSV)

      Synonyms: ToRSV, Tomato ringspot, Tomato ringspot nepovirus.

      Name used in the EU legislation: Tomato ringspot virus [ToRSV]

      Category: Virus

      (Proposed) Species: Nepovirus lycopersici

      Common name: ringspot of tomato, union necrosis of apple, chlorosis mosaic of raspberry, chlorosis of pelargonium, stem pitting of Prunus, yellow vein of grapevine.

      Name used in the Dossier: Tomato ringspot virus (ToRSV)

      1. Tobacco ringspot virus (TRSV)

      Synonyms: TRSV, Tobacco ringspot, Tobacco ringspot nepovirus.

      Name used in the EU legislation: Tobacco ringspot virus [TRSV00]

      Category: Virus

      Order: Picornavirales

      Family: Secoviridae

      Genus: Nepovirus

      Species: Nepovirus nicotianae

      Common name: ringspot of tobacco

      Name used in the Dossier: Tobacco ringspot virus (TRSV)

      Group Viruses and Viroids
      EPPO code The EPPO code for tomato ringspot virus (ToRSV) is ToRSV0 and for tobacco ringspot virus (TRSV) is TRSV00
      Regulated status ToRSV and TRSV are both listed as EU Quarantine pests (Annex II, Part A of Commission Implementing Regulation (EU) 2019/2072); Pests not known to occur in the EU Union territory (2019)
      Pest status in UK

      ToRSV is reported as ‘Present, few occurrences’ (EPPO, online a) or absent, eradicated (CABI, 2015). TRSV is reported as ‘Present, few occurrences’ (EPPO, online b)

      According to the UK NPPO (EPPO, online a), both nepoviruses are present at very low levels, ToRSV only detected in pelargonium (ornamental) and TRSV in pelargonium (ornamental) and anemome (wild plant) in the UK (DEFRA, 2018a, 2018b)

      Pest status in the EU Not relevant for EU Quarantine pest
      Host status on Cornus spp. Cornus spp. is reported as host of ToRSV (Encyclopedia for Viruses and Viroids) while Cornus florida, C. racemossa and C. sericea are reported as hosts of TRSV (EPPO, Onlinec,d)
      PRA information

      Rapid Pest Risk Analysis (PRA) for Tobacco ringspot virus (TRSV) (DEFRA, 2018a)

      Rapid Pest Risk Analysis for ToRSV in UK (DEFRA, 2018b)

      Scientific Opinion on the pest categorization of non-EU viruses and viroids of Cydonia Mill., Malus Mill. and Pyrus L. (EFSA PLH Panel, 2019a)

      Scientific Opinion on the pest categorization of non-EU viruses and viroids of Vitis L. (EFSA PLH Panel, 2019b)

      Other relevant information for the assessment
      Biology

      ToRSV and TRSV are bipartite positive-sense RNA viruses belonging in the Nepovirus genus, Secoviridae family (Sanfaçon et al., 2006)

      Transmission

      Both ToRSV and TRSV are transmitted by the ectoparasitic dagger nematodes in the Xiphinema americanum sensu lato group; both are transmitted by X. americanum sensu stricto, X. californicum, X. intermedium, X. rivesi and X. tarjanense, while the species X. bricolense and X. inaequale are additionally reported to transmit ToRSV (EFSA PLH Panel, 2018). Nepoviruses are transmitted by both the adult and larval stages of X. americanum (sensu lato), being acquired within 1 h and can be inoculated into healthy plants within 1 h (Stace-Smith, 1984). However, usually nepoviruses can be acquired in less than 15 min and persist up to several years when nematodes are not feeding (Fuchs et al., 2017). Local spread of nepoviruses due to the nematode vectors activity is slow and appear in parches. In raspberry plantings, the average rate of ToRSV spread is ca. 2 m per year (Converse & Stace-Smith, 1971)

      Seed transmission has been proved for ToRSV in soybean, strawberry, raspberry, pelargonium and Taraxacum officinale and pollen transmission to seed in pelargonium (Stace-Smith, 1984). TRSV can be seed transmitted in at least 12 species of herbaceous (crop and weed) hosts, such as soybean and cucumber, and by pollen in some species (Stace-Smith, 1985; Card et al., 2007; Rowhani et al., 2017). However, no seed/pollen transmission has been reported for these nepoviruses in woody hosts (EFSA PLH Panel, 2013)

      Uncertainly on biology

      The vector ability of additional nematode species

      The seed and pollen transmission of nepoviruses in woody plants

      Host range and distribution of host plants in the environment:

      In nature, ToRSV occurs mostly in vegetable and perennial crops, including ornamental and woody plants, such as Solanum lycopersicum (tomato), Cucumis sativus (cucumber), Nicotiana tabacum (tobacco), Solanum tuberosum (potato), Vitis vinifera (grapevine), Vaccinium corymbosum (blueberry), Fragaria vesca (strawberry), Pelargonium domesticum (geranium), raspberry (Rubus idaeus), Rubus fruticosus, Rubus sp. (blackberry), Malus sp. (apple), Hosta sp., Aquilegia vulgaris, Delphinium sp., Fragaria ananassa, Fraxina americana, Gladiolus sp., Heleborus foetidus, Hydrangea macrophylla, Iris sp., Punica granatum, Phaseolus vulgaris, Prunus persica, Prunus sp., Rosa sp., Trifolium sp., Vigna unguiculate, Viola cornuta; to these hosts ToRSV cause systemic infections (Stace-Smith, 1984; Powell et al., 1984; Samuitienė & Navalinskienė, 2001; Sanfaçon et al., 2006; EFSA PLH Panel, 2013; EPPO, 2013). Furthermore, ToRSV can infect weeds, including Taraxacum officinale, Rumex acetosella, Stellaria spp., among other 21 species (Mountain et al., 1983; Powell et al., 1984). In addition, the experimental host range of ToRSV is very wide, including species in more than 35 dicotyledonous and monocotyledonous families (Stace-Smith, 1984)

      TRSV infects also a wide range of herbaceous and woody hosts and can cause significant yield loss in soybeans (Glycine max), tobacco (Nicotiana tabacum), Vaccinium spp. and Cucurbitaceae (Stace-Smith, 1985). In addition, many other hosts have also been found naturally infected, such as Anemone, apples (Malus domestica), aubergines (Solanum melongena), blackberries (Rubus fruticosus), Capsicum, cherries (Prunus avium), Cornus, Fraxinus, Gladiolus, grapes (Vitis vinifera), Iris, Lupinus, Mentha, Narcissus pseudonarcissus, pawpaws (Carica papaya), Pelargonium, Petunia, Sambucus and various weeds (Gonsalves, 1988)

      Uncertainly on host range

      The actual host range of most nepoviruses

      Ecology and biology of the vectors:

      Nematodes belonging to the X. americanum sensu lato group are migratory ectoparasites of plant roots. All nematode stages are found in soil, but there is no specialised survival stage except in X. pachtaicum, which may survive under dry conditions in an anhydrobiotic state. Their life cycle lasts approximately 1 year, and they are assumed to reproduce parthenogenetically; males do not exist or are extremely rare. Optimum temperatures for reproduction are 20–24°C. Some species are important vectors of some American nepoviruses, including TRSV and ToRSV (EFSA PLH Panel, 2018)

      Symptoms Main type of symptoms

      ToRSV occurs in nature mostly in perennial plants, and it is associated with serious diseases of fruit and ornamental crops. Infected grapevines exhibit stunted shoot growth, shortened internodes, leaf ringspot and mottling, reduced size of fruit clusters and abortion of many berries, as well as thickened, spongy phloem tissue with numerous necrotic pits. In Malus, ToRSV causes graft union necrosis, woody pitting and decline in apples. In stone fruit trees, stem pitting and decline (in peach and cherry), yellow bud mosaic (in peach and almond) and brown line and decline (in plum) are observed. The red raspberry plants of some cultivars showing decline in vigour, stunting and significant fruit yield and quality reduction. Infected Rubus plants often die 4–5 years after infection (EFSA PLH Panel 2019a). Infected tomato plants may exhibit a conspicuous curling and shoot terminal necrosis, while younger leaves develop brown, clearly defined necrotic rings and sinuous lines with petioles often marked with necrotic streaks and rings. Tomato fruits may develop faint to conspicuous, grey to brown, corky, superficial and frequently concentric rings or portions of rings (EPPO, 2013).

      TRSV causes a significant bud blight disease in soybeans (Glycine max), a necrotic ringspot disease in tobacco (Nicotiana tabacum) and Vaccinium spp., especially V. corymbosum, and Cucurbitaceae. Infected grapevine develops symptoms of decline with shortened internodes, small and distorted leaves and decreased berry yield. Foliar symptoms (chlorotic spots, rings or areas surrounded by necrotic tissues) may be induced in infected stone fruit trees (EFSA PLH Panel 2019a). In several ornamentals, TRSV infections also cause chlorotic and necrotic spots, streaks and ringspots (Samuitienė & Navalinskienė, 2001).

      Presence of asymptomatic plants Many virus hosts may be asymptomatic, depending on the virus strain or host species and/or variety or may not exhibit symptoms in the early stages of infection, especially under low temperature conditions. In addition, plants infected with nepoviruses may exhibit symptoms recovery (Ghoshala and Sanfaçon, 2015).
      Confusion with other pathogens/pests The geographical distribution, natural host range and vector relations of ToRSV and TRSV are closely parallel to each other (Stace-Smith, 1984 and 1985). The two viruses can be distinguished only in the laboratory by proper testing.
      Reported evidence of impact These nepoviruses are listed as EU Quarantine pest according to Annex II, Part A of Commission Implementing Regulation (EU) 2019/2072
      Pathways and evidence that the commodity is a pathway Nepoviruses infect their hosts, including Cornus spp. systemically; therefore, bare-root (including dormant) and potted plants for planting coming from a country where these nepoviruses occur can be the main pathway of entry. In addition, infected nematodes may be carried over in soil attached to bare-root plants or in potted plants (EFSA PLH Panel, 2019a, 2019b)
      Surveillance information

      ToRSV. According to the information dated on 2021 from EPPO, ToRSV has a restricted presence in the UK, with only a few reported occurrences in Pelargonium (ornamentals).

      A survey in 1979–1980 found that ToRSV was distributed throughout the UK pelargonium industry, but only a small number of infected cultivars were present on individual holdings. Surveys conducted in the late 1990s found that ToRSV was present in Pelargonium cultivars and was found in seven nurseries across 17 varieties. Surveys conducted in the early 2000s found eight positive findings for ToRSV. Recent survey indicates that ToRSV has not been eradicated, since it has been found in pelargonium from old nursery stock plants, despite the nematode vectors responsible for transmission are not known to occur in the UK (Defra, 2018b).

      TRSV. According to the information dated on 1984 and 2018 from CABI and EPPO, TRSV has a restricted presence in UK, with only a few reported occurrences.

      TRSV was first reported from an outbreak of Anemone necrosis in Somerset in 1957 (Hollings, 1965). In 1979, TRSV was detected in Pelargonium in the UK (Stone et al. 1980), and also from amenity grasses (Cooper and Edwards, 1985). In 2011, during pre-export testing, TRSV was found on lettuce seeds originated from France. Several findings have been reported in Pelargonium stocks in the UK, results of surveys reported in the Rapid Pest Risk Analysis for TRSV indicating no evidence of eradication, despite the nematode vectors responsible for transmission are not known to occur in the UK (Defra, 2018a).

      A.3.2 Possibility of pest presence in the nursery

      A.3.2.1 Possibility of entry from the surrounding environment

      ToRSV and TRSV have a wide natural host range. They are naturally transmitted by some nematode species of the Xiphinema americanum sensu lato group (EFSA PLH Panel, 2018). These species are not known to occur in UK, although there is no evidence of ToRSV and TRSV eradication (Defra, 2018). The occurrence of these viruses in the UK is restricted to ornamentals at very low levels (NPPO, 2021). Thus, there is a set of standard precautions to ensure that only certified plants are present in the production facilities. Seed and pollen transmission of these nepoviruses have been reported in some herbaceous species (Stace-Smith, 1984) but remains highly uncertain for woody hosts species (EFSA, 2019a, 2019b). Infected plants may not show symptoms, and both viruses can be established by vegetative propagation of infected mother plants. There have been no other records in the UK, on any other hosts, including Cornus spp.

      Uncertainties:
      • The presence of alternative hosts for nepoviruses in the surrounding of the nurseries.
      • The presence of small undetected populations of the vectors in, Xiphinema americanum sensu lato group.
      • The efficiency of nepoviruses transmission in woody plants including Cornus spp. trees.
      • The efficiency of the detection and sampling strategies in detecting asymptomatic infections.

      Taking into consideration the above evidence and uncertainties, the Panel considers that the possibility of entry into the nursery infecting Cornus spp. plants from surrounding orchards is unlikely.

      A.3.2.2 Possibility of entry with new plants/seeds

      Seed purchased in the UK is not covered by a certification scheme. Seedlings sourced in the UK are certified with UK Plant Passports; seedlings from the EU countries are certified with phytosanitary certificates.

      ToRSV and TRSV host range is wide, and despite some hosts can be infected asymptomatically, symptoms expression is often severe enough to ensure its detection. There is evidence that nepoviruses are capable of establishing via seed/pollen transmission in some herbaceous species (Stace-Smith, 1984; 1985) but remains highly uncertain for woody host species (EFSA, 2019a, 2019b). Nepoviruses can also spread via vegetatively propagated material.

      Uncertainties:
      • The efficiency of the detection and sampling strategies in detecting asymptomatic infections.
      • Certification scheme applied to the seedlings.
      • Seed and pollen transmission in woody plants including Cornus spp. trees.
      • The health status of other species possibly cultivated/traded in the nurseries, including possible nematode infestation of the growing media.

      Taking into consideration the above evidence and uncertainties, the Panel considers that the possibility of entry with new plants of other ornamental species must be considered.

      A.3.2.3 Possibility of spread within the nursery

      Cornus spp. plants are produced in open fields and under a certification scheme in nurseries, and they are monitored and inspected during the vegetation period. Although potted plants are isolated from soil, bare-root plants are field grown. ToRSV and TRSV are naturally transmitted by some nematode species in the X. americanum sensu lato group (EFSA PLH Panel, 2018), which may be present in undetected populations. Also, the virus may be transmitted by pollen. However, there is a lack of data on the efficiency of pollen transmission in woody plants.

      Uncertainties:
      • Seed and pollen transmission in woody plants including Cornus spp. trees.
      • The presence in the nursery of small undetected populations of vector species in the X. americanum sensu lato group.

      Taking into consideration the above evidence and uncertainties, the Panel considers that the spread of the pathogen within the nursery is possible but very unlikely.

      A.3.3 Information from interceptions

      In the EUROPHYT/TRACES-NT database, there are no records of interceptions of Nepoviruses on Cornus spp. from third countries or on any other plant from the UK.

      A.3.4 Evaluation of the risk mitigation measures

      In the table below (Table A.11), all risk mitigation measures currently applied in UK are listed, and an indication of their effectiveness on nepoviruses is provided. The description of the risk mitigation measures currently applied in UK is provided in the Table 9.

      A.3.5 Overall likelihood of pest freedom for Cornus spp. plants (bare-root and rooted plants in pots)

      A.3.5.1 Reasoning for a scenario which would lead to a reasonably low number of infected Cornus spp. plants (bare-root and rooted plants in pots)

      • The vectors of nepoviruses in the X. americanum sensu lato group is not reported in UK.
      • Nepoviruses are not present in the surrounding environment of the nurseries.
      • Low occurrence of nepoviruses, only in UK ornamental (pelargonium) production sites with vegetative reproduction.
      • There is no vegetative propagation of the Cornus spp. plants in the nursery.
      • No reported seed transmission of nepoviruses for woody plants.
      • The spreading capacity of nematodes therefore of the viruses they transmit is limited.
      • The traded Cornus species may be resistant/tolerant (ToRSV).
      • The symptoms of nepoviruses are consisted of rings on the leaves, easy to be visually detected either in field surveys and/or before export.

      A.3.5.2 Reasoning for a scenario which would lead to a reasonably high number of infected Cornus spp. plants (bare-root and rooted plants in pots)

      • Vector species in the X. americanum sensu lato group could be present in some undetected spots in the nursery or could be imported by propagation material of other plants with soil.
      • Cornus spp. are reported as natural hosts of nepoviruses.
      • Nepoviruses have a wide host range therefore, it is highly possible that other host species are also present in the nursery.
      • Nepovirus could efficiently spread via infected nematodes in the field and/or the use/exchange/spread of soil infested with infected nematodes, and/or transmission via pollen.
      • ToRSV can spread via pollen in weeds and seeds.
      • Asymptomatic infections are common for nepoviruses during the latent period of infection, in plants that recover with few symptoms and in dormant plants without leaves.
      • Asymptomatic infections remain unnoticed in visual inspections.
      • There are no surveys for nepoviruses in the surrounding environment.
      • Seeds from UK and not certified and nepoviruses could be pollen and seed transmitted in Cornus spp.

      A.3.5.3 Reasoning for a central scenario equally likely to over-or underestimate the number of infected Cornus spp.plants (bare-root and rooted plants in pots) (median)

      • ToRSV has not been reported in Cornus spp. in the UK, but only associated with the vegetative propagation of ornamental plants.
      • Presence of the nematode vectors is very unlikely.
      • Introduction of the virus from the surrounding areas or from propagation material within the nurseries is very unlikely.
      • The scenario assumes a limited presence of the nepoviruses in the nurseries and the surroundings, and a limited susceptibility of Cornus spp. ToRSV is RNQP in the UK and TRSV is a quarantine pest in the UK.

      A.3.5.4 Reasoning for the precision of the judgement describing the remaining uncertainties (1st and 3rd quartile/interquartile range)

      The limited information on the susceptibility of Cornus spp. and on the unknown status of the nepoviruses in the nurseries and the surroundings results in high level of uncertainties for infestation rates below the median.

      A.3.6 Elicitation outcomes of the assessment of the pest freedom for tomato ringspot virus and tobacco ringspot virus

      The elicited and fitted values for nepoviruses agreed by the Panel are shown in Tables A.12A.15 and in Figures A.5, A.6

      TABLE A.11. Evaluation of the risk mitigation measures.
      Number Risk mitigation measure Effect on the pest Evaluation and uncertainties
      1 Registration of production sites Yes

      All nurseries are registered as professional operator with the UK NPPO, by the Animal and Plant Health Agency (APHA) and is authorised to issue UK plant passports (Dossier Section 1.0)

      Evaluation: The registration of production sites is expected to contribute in reducing the phytosanitary risks within the facility

      Uncertainties: None

      2 Certified plant material Yes

      Seeds of C. alba are not certified, while seeds of C. sanguinea purchased in the UK may be certified under the Forestry Commission's Voluntary Scheme for the Certification of Native Trees and Shrubs. Seedlings for Cornus spp. production sourced in the UK are certified with UK Plant Passports; seedlings from the EU countries are certified with phytosanitary certificates

      Evaluation: Nepoviruses can be seed transmitted in some of their host plant species. ToRSV is a quarantine pest and targeted by this measure that could reduce the infection level

      Uncertainties:

      – The details of the procedure are not clear.

      – If propagation material of alternative hosts is covered is not clear.

      3 Certification of substrates/ (rooted plant in pots) Yes

      Rooted plants in pots: In the production or procurement of these plants, the use of growing media is assessed for the potential to harbour and transmit plant pests. Growers most commonly use virgin peat or peat-free compost, which is a mixture of coir, tree bark, wood fibre etc. The compost is heat-treated by commercial suppliers during production to eliminate pests and diseases. It is supplied in sealed bulk bags or shrink-wrapped bales and stored off the ground on pallets, these are completely hygienic and free from contamination. Where delivered in bulk, compost is kept in a dedicated bunker, either indoors or covered by tarpaulin outdoors, and with no risk of contamination with soil or other material (Dossier Section 1.0).

      Evaluation: The measure is efficient in preventing the entry of the pathogen via the substrate containing infected nematode vectors into the nursery

      Uncertainties: None

      4 Surveillance, monitoring and sampling Yes

      In the last 3 years there has been a substantial level of inspection of registered Cornus spp. producers, both in support of the Plant Passporting scheme (checks are consistent with EU legislation, with a minimum of once a year for authorised operators) and as part of the Quarantine Surveillance programme (Great Britain uses the same framework for its surveillance programme as the EU). The Competent Authority inspects crops at least once a year to check if they meet the standards set out in the guides (Dossier Section 1.0)

      UK(GB) surveillance is based on visual inspection with samples taken from symptomatic material, and where appropriate, samples are also taken from asymptomatic material (e.g. plants, tubers, soil, watercourses) (Dossier Section 1.0)

      Evaluation: The surveillance, monitoring and sampling can detect the symptoms (if present) of the pathogen.

      Uncertainties:

      • The efficiency of the surveillance, monitoring and sampling, especially in detecting asymptomatic infections.
      • No results are reported.

      5 Hygiene measures Yes

      All nurseries have plant hygiene and housekeeping rules and practices in place, which are communicated to all relevant employees. The rules will be dependent on the plants handled and the type of business but will include:

      • Growing media
      • Weed management
      • Water usage
      • Cleaning and sterilisation
      • Waste treatment and disposal
      • Visitors

      Evaluation: These measures could be effective in reducing the risk of introduction and/or spread of the pathogens and its infected nematode vectors

      Uncertainties: The efficiency of the hygiene measures

      6 Irrigation water quality and/or treatments Yes

      Growers are required to assess water sources, irrigation and drainage systems used in the plant production for the potential to harbour and transmit plant pests. Water is routinely sampled and sent for analysis. No quarantine pests have been found (Dossier Section 1.0).

      Evaluation: the irrigation water is routinely checked and this can reduce the risk via the spread of infected nematode vectors.

      Uncertainties:

      • The frequency and the method used for the detection of the nematode vectors.

      7 Application of pest control products Yes

      Crop protection is achieved using a combination of measures including approved plant protection products, biological control or physical measures. Plant protection products are only used when necessary and records of all plant protection treatments are kept. (Dossier Section 1.0).

      Evaluation: The listed treatments are not effective against the vectors of nepoviruses.

      Uncertainties: None.

      8

      Washing of the roots (bare-root plants)

      Yes

      Bare-root plants are lifted from the field in winter and then root-washed on site and stored prior to export.

      Evaluation: The washing of the roots removes (parts of) the soil and thus also the nematode-vector of nepoviruses (if present).

      Uncertainties: The effectiveness of the washing to completely remove soil with the nematodes.

      9 Inspections and management of plants before export Yes

      The UK NPPO carries out inspections and testing where required by the country of destination's plant health legislation, to ensure all requirements are fulfilled and a valid phytosanitary certificate with the correct additional declarations is issued.

      Separate to any official inspection, plant material is checked by growers for plant health issues before dispatch.

      Evaluation: The inspections and management of plants before export could detect the pathogen.

      Uncertainties: The efficiency of the inspections, especially to detect asymptomatic infections.

      TABLE A.12. Elicited and fitted values of the uncertainty distribution of pest infection by tomato ringspot virus and tobacco ringspot virus per 10,000 bare-root Cornus spp. plants.
      Percentile 1% 3% 5% 10% 17% 25% 33% 50% 67% 75% 83% 90% 95% 98% 99%
      Elicited values 0 2 4 15 40
      EKE 0.00269 0.0156 0.0593 0.225 0.607 1.33 2.36 5.45 10.4 13.9 18.7 24.1 30.3 35.2 40.0
      • Note: The EKE results are the BetaGeneral (0.52062, 2.3955, 0, 51) distribution fitted with @Risk version 7.6.
      Details are in the caption following the image
      (A) Elicited uncertainty of pest infection per 10,000 bare-root plants Cornus spp. (histogram in blue–vertical blue line indicates the elicited percentile in the following order: 1%, 25%, 50%, 75%, 99%) and distributional fit (red line); (B) uncertainty of the proportion of pest-free plants per 10,000 (i.e. = 1 – pest infection proportion expressed as percentage); (C) descending uncertainty distribution function of pest infection per 10,000 plants.
      Details are in the caption following the image
      (A) Elicited uncertainty of pest infection per 10,000 rooted Cornus spp. plants in pots (histogram in blue–vertical blue line indicates the elicited percentile in the following order: 1%, 25%, 50%, 75%, 99%) and distributional fit (red line); (B) uncertainty of the proportion of pest-free plants per 10,000 (i.e. = 1 – pest infection proportion expressed as percentage); (C) descending uncertainty distribution function of pest infection per 10,000 plants.

      Based on the numbers of estimated infected bare-root Cornus spp. plants, the pest freedom was calculated (i.e. = 10,000 – number of infected plants per 10,000). The fitted values of the uncertainty distribution of the pest freedom are shown in Table A.13.

      TABLE A.13. The uncertainty distribution of plants free of tomato ringspot virus and tobacco ringspot virus per 10,000 of bare-root Cornus spp. plants calculated by Table A.12.
      Percentile 1% 3% 5% 10% 17% 25% 33% 50% 67% 75% 83% 90% 95% 98% 99%
      Values 9960 9985 9996 9998 10,000
      EKE results 9960 9965 9970 9976 9981 9986 9990 9995 9997.6 9998.7 9999 9999.39 9999.94 9999.984 9999.997
      • Note: The EKE results are the fitted values.
      TABLE A.14. Elicited and fitted values of the uncertainty distribution of pest infection by tomato ringspot virus and tobacco ringspot virus per 10,000 rooted Cornus spp. plants in pots.
      Percentile 1% 3% 5% 10% 17% 25% 33% 50% 67% 75% 83% 90% 95% 98% 99%
      Elicited values 0 1 2 3 5
      EKE 0.0729 0.152 0.267 0.471 0.724 1.03 1.33 1.95 2.65 3.04 3.50 3.96 4.41 4.72 5.00
      • Note: The EKE results is the BetaGeneral (1.2575,2.033, 0, 5.48) distribution fitted with @Risk version 7.6.

      Based on the numbers of estimated infected rooted Cornus spp. plants in pots, the pest freedom was the pest freedom was calculated (i.e. = 10,000 – number of infected plants per 10,000). The fitted values of the uncertainty distribution of the pest freedom are shown in Table A.15

      TABLE A.15. The uncertainty distribution of plants free of tomato ringspot virus and tobacco ringspot virus per 10,000 rooted Cornus spp. plants in pots calculated by Table A.14.
      Percentile 1% 3% 5% 10% 17% 25% 33% 50% 67% 75% 83% 90% 95% 98% 99%
      Values 9995 9997 9998 9999 10,000
      EKE results 9995 9995 9995.6 9996 9996.5 9997 9997.4 9998 9998.7 9999 9999.3 9999.5 9999.7 9999.8 9999.93
      • Note: The EKE results are the fitted values.

      A.3.7 References list

      Converse, R. H., & R. Stage-Smith. (1971). Rate of spread and effect of Tomato ringspot virus on Red Raspberry in the field. Phytopathology, 61, 1104–1106.

      Cooper, J. I., & Edwards, M. L. (1985). Viruses found in a survey of amenity grasses in the UK. Mitteilungen, Biologischen Bundesanstalt fur Land- und Forstwirtschaft, Berlin-Dahlem, No. 228. 89–91.

      CABI (Centre for Agriculture and Bioscience International), (online). Tomato ringspot virus (ringspot of tomato). https://www.cabidigitallibrary.org/doi/10.1079/cabicompendium.54076

      Card, S. D., Pearson, M. N., & Clover, G. R. G. (2007). Plant pathogens transmitted by pollen. Australasian Plant Pathology, 36, 455–461.

      DEFRA (Department for Environment, Food and Rural Affairs). (2018a). Rapid Pest Risk Analysis (PRA) for: Tobacco ringspot virus (TRSV). 23 pp. https://pra.eppo.int/pra/6e693e88-1a57-4e43-9bea-823b143c8a8c

      DEFRA (Department for Environment, Food & Rural Affairs). (2018b). Rapid Pest Risk Analysis (PRA) for: Tomato ringspot virus (ToRSV). https://planthealthportal.defra.gov.uk/assets/pras/ToRSV-PRA4.pdf

      EFSA PLH Panel (EFSA Panel on Plant Health). (2013). Scientific opinion on the risks posed by Prunus pollen, as well as pollen from seven additional plant genera, for the introduction of viruses and virus-like organisms into the EU. EFSA Journal, 16(10):3375, 50 pp. https://doi.org/10.2903/j.efsa.2013.3375

      EFSA PLH Panel (EFSA Panel on Plant Health), Jeger, M., Bragard, C., Caffier, D., Candresse, T., Chatzivassiliou, E., Dehnen-Schmutz, K., Gilioli, G., Grgegoire, J.-C., Jaques Miret, J. A., MacLeod, A., Navajas Navarro, M., Parnell, S., Potting, R., Rafoss, T., Rossi, V., Urek, G., Van Bruggen, A., Van der Werf, W., West, J., … Niere, B. (2018). Scientific Opinion on the pest categorization of Xiphinema americanum sensu lato. EFSA Journal, 16(7):5298. https://doi.org/10.2903/j.efsa.2018.5298

      EFSA PLH Panel (EFSA Plant Health Panel), Bragard, C., Dehnen-Schmutz, K., Gonthier, P., Jacques, M.-A., Jaques Miret, J. A., Justesen, A. F., MacLeod, A., Magnusson, C. S., Milonas, P., Navas-Cortes, J. A., Parnell, S., Potting, R., Reignault, P. L., Thulke, H.-H., Van der Werf, W., Vicent Civera, A., Yuen, J., Zappalà, L., … Rubino, L. (2019a). Scientific Opinion on the pest categorization of non-EU viruses and viroids of Cydonia Mill., Malus Mill. and Pyrus L. EFSA Journal, 17(9), 5590. https://doi.org/10.2903/j.efsa.2019.5590

      EFSA PLH Panel (EFSA Plant Health Panel), Bragard, C., Dehnen-Schmutz, K., Gonthier, P., Jacques, M.-A., Jaques Miret, J. A., Justesen, A. F., MacLeod, A., Magnusson, C. S., Milonas, P., Navas-Cortes, J. A., Parnell, S., Potting, R., Reignault, P. L., Thulke, H.-H., Van der Werf, W., Vicent Civera, A., Yuen, J., Zappalà, L., … Rubino, L. (2019b). Scientific Opinion on the pest categorization of non-EU viruses and viroids of Vitis L. EFSA Journal, 17(9), 5669. https://doi.org/10.2903/j.efsa.2019.5669

      EPPO (European and Mediterranean Plant Protection Organisation), (2013). Tomato ringspot virus in fruit trees and grapevine: Inspection. Phytosanitary procedures. PM3/32 (2). Bulletin OEPP/EPPO Bulletin, 43(3), 397 https://doi.org/10.1111/epp.12073

      EPPO (European and Mediterranean Plant Protection Organisation). (online_a). Tomato ringspot virus (TORSV0), Distribution. https://gd.eppo.int/taxon/TORSV0/distribution

      EPPO (European and Mediterranean Plant Protection Organisation). (online_b). Tobacco ringspot virus (TRSV0), Distribution. https://gd.eppo.int/taxon/TRSV00/distribution/GB

      EPPO (European and Mediterranean Plant Protection Organisation). (online_c). Tobacco ringspot virus (TRSV0), Host plants. https://gd.eppo.int/taxon/TRSV00/hosts

      EPPO (European and Mediterranean Plant Protection Organisation). (online_d). Tomato ringspot virus (TORSV0), Host plants. https://gd.eppo.int/taxon/TORSV0/hosts

      EUROPHYT. (online). European Union Notification System for Plant Health Interceptions – EUROPHYT. https://ec.europa.eu/food/plant/plant_health_biosecurity/europhyt/index_en.htm

      FERA (The Food and Environment Research Agency). 2014. Rapid pest risk analysis for Xiphinema americanum s.l. (European populations). https://planthealthportal.defra.gov.uk/pests-and-diseases/uk-plant-health-risk-register/downloadExternalPra.cfm?id=4175

      Fucks, M., Schmitt-Keichinger, C., & Sanfaçon, H. (2017). A renaissance in nepovirus research provides new insights into their molecular interface with hosts and vectors. Advances in Virus Research, 97, 61–105. https://doi.org/10.1016/bs.aivir.2016.08.009

      Mountain, W., Powell, C., Forer, L., & Stouffer, R. (1983). Transmission of Tomato ringspot virus from dandelion via seed and dagger nematodes. Plant Disease, 67, 867–868. https://doi.org/10.1094/pd-67-867

      Powell, C., Forer, L., Stouffer, R., Cummins, J., Gonsalves, D., Rosenberger, D., Hoffman, J., & Lister, R. (1984). Orchard weeds as hosts of Tomato ringspot and Tobacco ringspot viruses. Plant Disease, 68, 242–244. https://doi.org/10.1094/pd-69-242

      Samuitienė, M., & Navalinskienė, M. (2001): Nepoviruses and their influence on field floriculture. Biologija, 4, 43–45.

      Sanfaçon, H., Zhang, G., Chisholm, J., Jafarpour, B., & Jovel, J. (2006). Molecular biology of Tomato ringspot nepovirus, a pathogen of ornamentals, small fruits and fruit trees. Floriculture, Ornamental and Plant Biotechnology, 540–547.

      Stace-Smith, R. (1984). Tomato ringspot virus, CMI/AAB Descriptions of Plant Viruses, No. 290, AAB, Wellesbourne (GB).

      Stace-Smith, R. (1985). Tobacco ringspot virus. CMI/AAB Descriptions of Plant Viruses, AAB, Wellesbourne (GB), 309, AAB, Wellesbourne (GB).

      TRACES-NT. (online). TRADE Control and Expert System. https://webgate.ec.europa.eu/tracesnt

      Stone, O. M. (1980). Nine viruses isolated from pelargonium in the United Kingdom. In V International Symposium on Virus diseases of Ornamental Plants 110 (pp. 177–182).

      A.4 Discula destructiva

      A.4.1 Organism information

      Taxonomic information

      Current valid scientific name: Discula destructiva Redlin (1991)

      (Index Fungorum, https://www.speciesfungorum.org/Names/SynSpecies.asp?RecordID=355233)

      Synonyms: –

      Name used in the EU legislation:

      Order: Diaporthales

      Family: Gnomoniaceae

      Common name: Dogwood anthracnose

      Name used in the Dossier: Discula destructiva

      Group Fungi
      EPPO code DISCDE
      Regulated status

      The pest is not regulated in the EU territory and not listed in Commission Implementing Regulation (EU) 2019/2072

      Formerly listed in the EPPO Alert List (2003–2007)

      Pest status in UK Present, widespread (EPPO, CABI; online)
      Pest status in the EU Present in Germany (few occurrences) and in Italy (restricted distribution) (EPPO, CABI; online)
      Host status on Cornus spp.

      Cornus florida (flowering dogwood) and C. nuttallii (Pacific dogwood) are the main hosts of D. destructiva and particularly susceptible. Cornus kousa, C. alternifolia and C. amomum are reported as relatively resistant hosts (Sherald et al., 1994), Cornus mas is considered resistant host (Stinzing and Lam, 2003).C. alba is mentioned as a host species by CABI (online), and Brown et al. (1996). There is no information about the host status of C. sanguinea

      Uncertainties: the host status of C. sanguinea

      PRA information EPPO (2005) Pest risk analysis Discula destructiva (draft) https://pra.eppo.int/pra/849c2c2f-939e-48dd-bcd4-9852aeb9c4b6
      Other relevant information for the assessment
      Biology

      The fungus may remain in a dormant stage for extended periods in leaves, twigs, leaf debris and branches (Baysal-Gurel et al., 2017). D. destructiva persists in cankers on the trunks and branches of its hosts, or in twigs or dead leaves carrying conidiomata. D. destructiva produces acervuli and subcuticular conidiomata on leaves and twigs of the host. Conidia are ellipsoidal and non-septate (Daughtrey and Hibben, 1994; Daughtrey et al., 1996). The sexual state of the fungus is unknown (Redlin, 1991). Conidia formed in conidiomata (acervuli) on cankers are dispersed by rain-splashing to newly expanded leaves during the spring, that are infected under humid conditions (CABI, 2020). Fruiting structures of D. destructiva form underneath leaf spots and on the surface of twig cankers. Huge amounts of conidia are formed inside and, in the spring, ooze out in slimy beige clusters. Short distance dispersal of the conidia occurs via rain splash. For long-distance dispersal, Colby et al. (1996) demonstrated that the coccinellid, Hippodamia convergens can transport viable conidia of D. destructiva externally for as many as 16 days under laboratory conditions. Several other species of arthropods have been found with viable conidia of the fungus in a natural environment in periods with humidity and cool temperatures. Of them, curculionids, formicids, hemipterans, homopterans and immature and adult orthopterans are mobile enough to move from tree to tree (Holt et al., 1998). Infected seeds could provide a mechanism for long-distance dispersal of D. destructiva by animals or birds by consuming infected fruits and excreting the seeds (Britton et al., 1993; Cornell University, Plant Disease Diagnostic Clinic, 2015).

      The fungus survives the winter in the host and leaf symptoms generally begin to occur in the early spring of the next year (Daughtrey and Hibben, 1994).

      Lesions on the leaves may remain as small spots, expand to form larger blotches or lead to the complete blighting of the leaf, spreading into the petiole and result in the infection of the shoot. At flowering, bracts are also infected. Conidia may infect the current season's shoots directly, forming small cankers which are usually rapidly delimited by callus tissue. However, shoots infected from previously blighted leaves develop more severe cankering and die back (CABI, online). The shoot dieback often results in the development of epicormic shoots on both branches and trunk, which become infected in turn. In cases of severe infection, young trees may die but, if conditions become less favourable for disease development in subsequent seasons, branch and trunk cankers may be contained and the tree recovers. D. destructiva is slow growing in culture and the identification process may take more than 2 weeks. It does not sporulate readily in conventional media, making morphological identification challenging (Daughtrey and Hibben, 1994). The optimal growth and sporulation in culture is at 21–24°C, with no growth occurring at 27°C. Infection is favoured by cool, wet spring and autumn, but can occur throughout the growing season. Predisposing factors for infection include low light intensity and drought stress (Daughtrey and Hibben, 1994, 1996; Erbaugh et al., 1995)

      Symptoms Main type of symptoms Initial symptoms include small leaf spots with a purple margin, which then progress into large necrotic blotches. In many cases, infected mature leaves die prematurely. Sometimes, they can remain attached to the stems after the usual leaf fall. Infection expands from leaves to small twigs and then to branches (CABI, online). Infected shoots show fruiting bodies of the fungus on the dead tissue. Twig and branch dieback start in the lower crown (hence the original name of the disease ‘lower branch dieback’). Numerous epicormic shoots often form at the base of the trunk or on branches of infected plants. These shoots frequently become infected and die, with infections advancing from the shoots into the trunk. D. destructiva causes cankers which can kill the tree. Cankers may not be present on all dead trees (Anderson et al., 1994). The fungus can kill dogwoods of all sizes, but it is particularly severe on young seedlings and in understorey forest dogwoods. Infection of dogwoods is most likely to occur during cool, wet weather in spring and fall, but can occur at any time during the growing season. Ornamentals especially those in open, sunny sites, may be disfigured without necessarily being killed (Anderson et al., 1994; Mielke and Daughtrey, 1989)
      Presence of asymptomatic plants Plants may be infected with the pathogen without exhibiting visible and conspicuous signs or symptoms of the disease. The fungus survives in the form of latent overwintering structures (conidiomata) on wood. The fungus may persist in a dormant stage for extended periods in aerial plant parts before the infection becomes visible and the presence of the pathogen detected (Baysal-Gurel et al., 2017)
      Confusion with other pathogens/pests

      In the early stages of the disease, the symptoms can be confused with:

      1. Spot anthracnose, caused by Elsinoe corni
      2. Leaf spots, caused by Septoria cornicola
      3. The dogwood twig borer Oberea tripunctata (Swederus)
      4. Mechanical injuries and drought

      (Anderson et al., 1994).

      D. destructiva was initially confused with the anamorph of Glomerella cingulata, already well known on this host. Various other fungi that cause leaf spots on Cornus (Elsinoë corni, species of Septoria, Ascochyta cornicola, Botryotinia fuckeliana), can be easily distinguished microscopically (CABI, online) or using molecular methods

      Host plant range The host plant range of the fungus includes: Cornus alba (red-barked dogwood), Cornus controversa (giant dogwood), Cornus sericea (red osier dogwood) and Cornus stolonifera (CABI, online)
      Evidence that the commodity can be a pathway

      Plant parts liable to carry the hyphae or conidia of the fungus are leaves, twigs and branches. Therefore, it is possible that the exported bare-root plants or potted plants of Cornus spp. can act as a pathway for D. destructiva

      Several records confirm that Cornus spp. are hosts of D. destructiva. Plants for planting or plant parts (wood, fruit, seeds), nursery stock and propagation material originated from infested areas are could carry the fungus via trade and transport (Daughtrey et al. 1996; Holt et al. 1998). The infection of plants and movement of infected tissues ensures the long-distance dispersal of the pathogen. D. destructiva can be disseminated through conidia on all aerial plant parts. Conidia production can be accelerated by rain and humidity (e.g. CABI, online; Redlin, 1991; Smith, 2021)

      Reported evidence of impact In the USA, a significant proportion of woodland dogwood populations has been killed. The disease now presents a considerable problem for nursery production of healthy plants (CABI, online)
      Surveillance information According to the Dossier Section 1.0, D. destructiva is not under official surveillance, and has no quarantine pest status in UK

      A.4.2 Possibility of pest presence in nursery

      A.4.2.1 Possibility of entry from the surrounding environment

      Considering that the pathogen has widespread distribution in the UK (EPPO, 2022) and hosts Cornus spp. (native or cultivated) are present, it is likely that the fungus could be present in the neighbouring environment of the nursery and enters the nursery mainly via insects or seeds who can transmit the fungus. Several species of arthropods are known to contribute to the spread of dogwood anthracnose, that can acquire and transport even for long distances viable conidia of D. destructiva. Assuming that there are no host plants present directly connected with the nursery that can act as an inoculum reservoir of the fungus, the main pathway of entry of the fungus from the surrounding environment is through insects.

      Uncertainties:

      The possible role of insects as vector of the disease. The possibility that wind-driven rain splash or aerial dispersal from host plants in the environment reach the nurseries.

      A.4.2.2 Possibility of entry with new plants/seeds

      Infected seed could be a pathway.

      Infected asymptomatic seedlings introduced into the nurseries can also be a pathway. The fungus has no regulatory status in the UK and therefore there are no compulsory testing for this fungus. Latent, asymptomatic infections are likely to occur in the propagating plant material and D. destructiva could not be detected. In addition, infection or infestation of seeds are not visible or easy to detect.

      Uncertainties:

      The detection of the asymptomatic infections in the propagation material.

      A.4.2.3 Possibility of spread within the nursery

      If D. destructiva has entered into the nursery the pathogen can spread to other plants through dispersal of conidia. Conidia can be dispersed from infected to healthy plant tissues via splash of water during irrigation or currents of air inside the nursery. If the environmental conditions (relative humidity and temperature) are favourable for disease development the pathogen thrives and spreads the disease.

      Planting of infected seeds, movement of soil with plant debris with fruiting bodies, deficient insect control, workers and tools may also contribute to the spread of the pathogen.

      Removal of symptomatic material would reduce the availability of inoculum reducing the probability of disease spread. Furthermore, the spread of the disease could be reduced if non-host plants are grown in the nursery.

      Uncertainties:

      There is uncertainty on the duration of a possible latent stage of the fungus and the early detection of D. destructiva on infected tissues.

      The proportion of host plants grown in the nurseries is not known.

      The proportion of host plants grown in the nurseries is not known.

      A.4.3 Information from interceptions

      There were no interceptions of Discula destructiva on commodities imported into the EU Member States from third countries (EUROPHYT and TRACES, online, [Accessed: 22 November 2023]). The disease in EPPO region was intercepted in 1995 by United Kingdom on imported Cornus florida from USA (EPPO, 2007).

      A.4.4 Evaluation of the risk mitigation measures

      In the table below (Table A.16), all risk mitigation measures currently applied in the UK are listed and an indication of their effectiveness on D. destructiva is provided. The description of the risk mitigation measures currently applied in the UK is provided in Table 9.

      A.4.5 Overall likelihood of pest freedom for Cornus spp. plants (bare-root and rooted plants in pots)

      A.4.5.1 Reasoning for a scenario which would lead to a reasonably low number of infected Cornus spp. plants (bare-root and rooted plants in pots)

      • The pathogen occurs only on a few Cornus species, where C. alba is a confirmed host but not a major host and while C. sanguinea is less susceptible.
      • There is high proportion of C. sanguinea (less susceptible) plants than C. alba.
      • The pathogen is widespread in the UK, but there is either a low pest pressure in the surroundings or that Cornus species are less susceptible to this pathogen.
      • The pathogen can spread only short distances by rain splash and there is no spread of the pathogen by insects.
      • In Spring, the infections develop visible symptoms on leaves and cankers are also present.
      • There is a regular monitoring for this pathogen.
      • Seedlings are partly sourced from the EU.
      • The combination of systemic and contact fungicides are effective against the leaf asymptomatic and symptomatic infections.
      • The nurseries are protected by the hedges that can reduce the risk of pathogen spread from the environment.
      • The drip system of irrigation is used.
      • Leaves on top of the soil are cleaned before export and official inspections before export are carried out and the symptoms of the infection are visible.

      A.4.5.2 Reasoning for a scenario which would lead to a reasonably high number of infected Cornus spp. plants (bare-root and rooted plants in pots)

      • All Cornus spp. are hosts for this pathogen and are widespread in UK (C. sanguinea less than C. alba).
      • There is high proportion of C. alba plants than C. sanguinea (less susceptible).
      • The pathogen is widespread in the UK with high pest pressure and the Cornus species are tolerant.
      • The pathogen spreads to long distances by insects, seeds and birds.
      • Latent or late (in autumn) infections occur without visible symptoms.
      • The symptoms may not develop visible symptomatic infections for longer time, and there can be confused with symptoms induced by other fungi.
      • The latent and late infections may be overlooked.
      • The seedlings can be asymptomatic and there is no obligatory testing.
      • The fungicides are not effective against cankers and the curative applications are not effective.
      • The pathogen can spread from the close environment via the wind or rain.
      • The overhead irrigation system is used (can spread the inoculum).
      • Infected debris can be on the soil.
      • Official inspections before export are carried out but asymptomatic plants, infections on dormant plants and early infections on branches and stems maybe overlooked.

      A.4.5.3 Reasoning for a central scenario equally likely to over-or underestimate the number of infected Cornus spp.plants (bare-root and rooted plants in pots) (median)

      The scenario assumes a limited presence of the pest in the nurseries and the surroundings. As there are no reports of impact in the UK, the pest pressure may not be so high. C. alba is a poor host and C. sanguinea is not a host and the nursery is protected by hedges. The symptoms on the leaves should make the detection easy.

      A.4.5.4 Reasoning for the precision of the judgement describing the remaining uncertainties (1st and 3rd quartile/interquartile range)

      The limited information on the status of the D. destructiva in the nurseries and the surroundings results in high level of uncertainties for infestation rates below the median.

      A.4.6 Elicitation outcomes of the assessment of the pest freedom for Discula destructiva

      The elicited and fitted values for D. destructiva agreed by the Panel are shown in Tables A.17A.20 and in Figures A.7, A.8.

      TABLE A.16. Evaluation of the risk mitigation measures.
      Number Risk mitigation measure Effect on the pest Evaluation and uncertainties
      1 Registration of production sites Yes

      All nurseries are registered as professional operator with the UK NPPO, by the Animal and Plant Health Agency (APHA) and is authorised to issue UK plant passports (Dossier Section 1.0)

      Evaluation: The registration of production sites is expected to contribute to reducing the phytosanitary risks within the facility

      Uncertainties: None

      2 Certified plant material Yes

      Seeds of C. alba are not certified, while seeds of C. sanguinea seed purchased in the UK may be certified under the Forestry Commission's Voluntary Scheme for the Certification of Native Trees and Shrubs. Seedlings for Cornus production sourced in the UK are certified with UK Plant Passports; seedlings from the EU countries are certified with phytosanitary certificates

      Evaluation: D. destructiva is not a quarantine and therefore there are no compulsory testing for this fungus. Seeds and seedlings can be a pathway

      Uncertainties: The duration of the asymptomatic phase in seedlings

      3 Certification of substrates/ (rooted plant in pots) No Rooted plants in pots: In the production or procurement of these plants, the use of growing media is assessed for the potential to harbour and transmit plant pests. Growers most commonly use virgin peat or peat-free compost, which is a mixture of coir, tree bark, wood fibre etc. The compost is heat-treated by commercial suppliers during production to eliminate pests and diseases. It is supplied in sealed bulk bags or shrink-wrapped bales and stored off the ground on pallets, these are completely hygienic and free from contamination. Where delivered in bulk, compost is kept in a dedicated bunker, either indoors or covered by tarpaulin outdoors, and with no risk of contamination with soil or other material (Dossier Section 1.0)
      4 Surveillance, monitoring and sampling Yes

      In the last 3 years there has been a substantial level of inspection of registered Cornus producers, both in support of the Plant Passporting scheme (checks are consistent with EU legislation, with a minimum of once a year for authorised operators) and as part of the Quarantine Surveillance programme (Great Britain uses the same framework for its surveillance programme as the EU). The Competent Authority inspects crops at least once a year to check if they meet the standards set out in the guides (Dossier Section 1.0)

      Evaluation: The fungus has no quarantine status in UK and in the EU

      Uncertainties: It is not clear if the inspection of registered Cornus spp. producers include and will report this pathogen

      5 Hygiene measures Yes

      All nurseries have plant hygiene and housekeeping rules and practices in place, which are communicated to all relevant employees. The rules will be dependent on the plants handled and the type of business but will include:

      • Growing media
      • Weed management
      • Water usage
      • Cleaning and sterilisation
      • Waste treatment and disposal
      • Visitors

      Evaluation: Pruning, water usage and waste treatment and disposal of plant residues measures could be effective in reducing the risk of introduction and/or spread of the pathogen.

      Uncertainties: The application and efficiency of the hygiene measures

      6 Irrigation water quality and/or treatments No

      Growers are required to assess water sources, irrigation and drainage systems used in the plant production for the potential to harbour and transmit plant pests. Water is routinely sampled and sent for analysis. No quarantine pests have been found (Dossier Section 1.0)

      Evaluation: Only the type of irrigation applied (overhead or sub-irrigation) is relevant for the spread of the pathogen

      Uncertainties: None

      7 Application of pest control products Yes

      Crop protection is achieved using a combination of measures including approved plant protection products, biological control or physical measures. Plant protection products are only used when necessary and records of all plant protection treatments are kept. (Dossier Section 1.0).

      Evaluation:

      • Combination of systemic and contact fungicides are used.
      • Fungicides are used as both preventive and curative purpose, depending on the situation.

      Uncertainties: The efficacy of the treatment on the pathogen is unknown

      8 Washing of the roots (bare-root plants) No Bare-root plants are lifted from the field in winter and then root-washed on site and stored prior to export
      9 Inspections and management of plants before export Yes

      The UK NPPO carries out inspections and testing where required by the country of destination's plant health legislation, to ensure all requirements are fulfilled and a valid phytosanitary certificate with the correct additional declarations is issued.

      Separate to any official inspection, plant material is checked by growers for plant health issues before dispatch.

      Evaluation: The inspections and management of plants before export can detect the disease only in symptomatic plants (symptoms on branches or stems/trunks).

      Uncertainties:

      • The efficiency of the inspections.
      • The possibility of detecting asymptomatic infected plants, symptoms on dormant plants and initial symptoms on branches and stems/trunks are unknown

      TABLE A.17. Elicited and fitted values of the uncertainty distribution of pest infection by D. destructiva per 10,000 bare-root Cornus spp. plants.
      Percentile 1% 2.5% 5% 10% 17% 25% 33% 50% 67% 75% 83% 90% 95% 97.5% 99%
      Elicited values 3 10 20 40 100
      EKE 3.00 3.26 3.77 4.99 6.90 9.65 12.8 20.8 31.8 39.2 49.1 60.6 74.5 86.6 100
      • Note: The EKE results is the BetaGeneral (0.82642, 4.4331, 2.87, 160) distribution fitted with @Risk version 7.6.
      Details are in the caption following the image
      (A) Elicited uncertainty of pest infection per 10,000 bare-root Cornus spp. plants (histogram in blue–vertical blue line indicates the elicited percentile in the following order: 1%, 25%, 50%, 75%, 99%) and distributional fit (red line); (B) uncertainty of the proportion of pest-free plants per 10,000 (i.e. = 1 – pest infection proportion expressed as percentage); (C) descending uncertainty distribution function of pest infection per 10,000 plants.
      Details are in the caption following the image
      (A) Elicited uncertainty of pest infection per 10,000 rooted Cornus spp. plants in pots (histogram in blue–vertical blue line indicates the elicited percentile in the following order: 1%, 25%, 50%, 75%, 99%) and distributional fit (red line); (B) uncertainty of the proportion of pest-free plants per 10,000 (i.e. = 1 – pest infection proportion expressed as percentage); (C) descending uncertainty distribution function of pest infection per 10,000 plants.

      Based on the numbers of estimated infected bare-root Cornus spp. plants, the pest freedom was calculated (i.e. = 10,000 – number of infected plants per 10,000). The fitted values of the uncertainty distribution of the pest freedom are shown in Table A.18.

      TABLE A.18. The uncertainty distribution of plants free of D. destructiva per 10,000 bare-root Cornus spp. plants calculated by Table A.17.
      Percentile 1% 2.5% 5% 10% 17% 25% 33% 50% 67% 75% 83% 90% 95% 97.5% 99%
      Values 9900 9960 9980 9990 9997
      EKE results 9900 9913 9925 9939 9951 9961 9968 9979 9987 9990 9993 9995 9996.2 9996.7 9997
      • Note: The EKE results are the fitted values.
      TABLE A.19. Elicited and fitted values of the uncertainty distribution of pest infection by D. destructiva per 10,000 rooted Cornus spp. plants in pots.
      Percentile 1% 2.5% 5% 10% 17% 25% 33% 50% 67% 75% 83% 90% 95% 97.5% 99%
      Elicited values 3.0 15.0 30.0 50.0 150.0
      EKE 3.00 4.02 5.46 8.03 11.3 15.3 19.5 29.3 42.1 50.9 63.0 77.9 97.8 117 143
      • Note: The EKE results is the BetaGeneral (1.3478, 377.97, 1.99, 10,000) distribution fitted with @Risk version 7.6.

      Based on the numbers of estimated infected rooted Cornus spp. plants in pots, the pest freedom was calculated (i.e. = 10,000 – number of infected plants per 10,000). The fitted values of the uncertainty distribution of the pest freedom are shown in Table A.20.

      TABLE A.20. The uncertainty distribution of plants free of D. destructiva per 10,000 rooted Cornus spp. plants in pots calculated by Table A.19.
      Percentile 1% 2.5% 5% 10% 17% 25% 33% 50% 67% 75% 83% 90% 95% 97.5% 99%
      Values 9850 9950 9970 9985 9997
      EKE results 9857 9883 9902 9922 9937 9949 9958 9971 9980 9985 9989 9992 9995 9996 9997
      • Note: The EKE results are the fitted values.

      A.4.7 References

      Anderson, R.L., Knighten, J.L., Windham, M., Langdon, K., Hendrix, F., and Roncadori R., (1994). Dogwood Anthracnose and its spread in the South. Forest Service Protection Report 26, p. 19.

      Baysal-Gurel F., Kabir N., Randaci A., (2017). Dogwood Anthracnose. College of Agriculture Tennessee State University.

      Britton. K.O., Roncadori R. W. and Hendrix.F.F. (1993). Isolation of Discula destructiva and other fungi from seeds of dogwood trees. Plant Disease, 77, 1026–1028.

      Brown, D. A., Windham, M. T., & Trigiano, R. N. (1996). Resistance to dogwood anthracnose among Cornus species. Journal of Arboriculture, 22, 83–86.

      CABI (Centre for Agriculture & Bioscience International), (online). Discula destructiva (anthracnose of dogwood). https://www.cabidigitallibrary.org/doi/10.1079/cabicompendium.20079

      Cornell University, Plant Disease Diagnostic Clinic, (2015). Dogwood Anthracnose: Discula destructiva. http://plantclinic.cornell.edu/factsheets/dogwoodanthracnose.pdf

      Daughtrey, M. L., & Hibben, C. R. (1994). Dogwood anthracnose: A new disease threatens two native Cornus species. Annual Review of Phytopathology, 61–73.

      Daughtrey, M. L., Hibben, C. R., Britton, K. O., Windham, M. T., & Redlin, S. C. (1996). Dogwood anthracnose: Understanding a disease new to North America. Plant Disease, 80(4), 349–358.

      EPPO (European and Mediterranean Plant Protection Organisation). (online). Discula destructiva (DISCDE). https://gd.eppo.int/taxon/DISCDE

      EPPO (European and Mediterranean Plant Protection Organisation). (2007). Mini data sheet on Discula destructiva. https://gd.eppo.int/taxon/DISCDE/documents

      EPPO (European and Mediterranean Plant Protection Organisation). (2005). PRA for Discula destructiva [EPPO, 2005-02-15]. https://pra.eppo.int/pra/849c2c2f-939e-48dd-bcd4-9852aeb9c4b6

      Erbaugh, D. K., Windham, M. T., Stodola, A. J. W., & Auge, R. M. (1995). Light intensity and drought stress as predisposition factors for dogwood anthracnose. Journal of Environmental Horticulture, 13(4), 186–189; 24.

      EUROPHYT. European Union Notification System for Plant Health Interceptions EUROPHYT. https://ec.europa.eu/food/plant/plant_health_biosecurity/europhyt/index_en.htm

      Gauthier, N. W., & Stolz, S. (2017). Flowering Dogwood Diseases. https://plantpathology.ca.uky.edu/files/ppfs-or-w-06.pdf

      Holt, H. L., Grant, J. F., & Windham, M.T. (1998). Incidence of arthropods infested with conidia of the dogwood anthracnose fungus, Discula destructiva Redlin, on flowering dogwoods in the natural environment. Journal of Entomological Science, 33(4), 329–335.

      Mielke, M.E., & M.L. Daughtrey. (1989). How to Identify and Control Dogwood Anthracnose. USDA Forest Service, Northeastern Area, Broomall, PA. NA GA-18: 8

      Redlin, S. C. (1991). Discula destructiva sp. nov., cause of dogwood anthracnose. Mycologia, 83(5), 633–642.

      Sherald, J. L., Stidham, T. M., & Roberts, L. E. (1994). Evaluation of eight species of Cornus for resistance to dogwood anthracnose. Journal of Environmental Horticulture, 12(2), 61–64.

      Smith, S. (2021). Anthracnose Diseases of Dogwood. https://www.uaex.uada.edu/publications/pdf/fsa-7564.pdf

      Stinzing, A., & Lang, K.J. (2003). Dogwood anthracnose. First detection of Discula destructiva on Cornus florida in Germany. Nachrichtenblatt des Deutschen Pflanzenschutzdienstes, 55(1), 1–5.

      APPENDIX B: Web of Science all databases search string

      In the table below, the search string for Cornus used in Web of Science is reported. Totally, 596 papers were retrieved. Titles and abstracts were screened, and 28 pests were added to the list of pests (see Appendix C) (Table B.1).

      TABLE B.1. String for Cornus.
      Web of Science All databases

      TOPIC:

      (“Cornus” OR “dogwood”)

      AND

      TOPIC:

      (“pathogen*” OR “pathogenic bacteria” OR “fung*” OR “oomycet*” OR “myce*” OR “bacteri*” OR “virus*” OR “viroid*” OR “insect$” OR “mite$” OR “phytoplasm*” OR “arthropod*” OR “nematod*” OR “disease$” OR “infecti*” OR “damag*” OR “symptom*” OR “pest$” OR “vector” OR “hostplant$” OR “host plant$” OR “host” OR “root lesion$” OR “decline$” OR “infestation$” OR “damage$” OR “symptom$” OR “dieback*” OR “die back*” OR “malaise” OR “aphid$” OR “curculio” OR “thrip$” OR “cicad$” OR “miner$” OR “borer$” OR “weevil$” OR “plant bug$” OR “spittlebug$” OR “moth$” OR “mealybug$” OR “cutworm$” OR “pillbug$” OR “root feeder$” OR “caterpillar$” OR “foliar feeder$” OR “virosis” OR “viruses” OR “blight$” OR “wilt$” OR “wilted” OR “canker” OR “scab$” OR “rot” OR “rots” OR “rotten” OR “damping off” OR “damping-off” OR “blister$” OR “smut” OR “mould” OR “mold” OR “damping syndrome$” OR “mildew” OR “scald$” OR “root knot” OR “root-knot” OR “rootkit” OR “cyst$” OR “dagger” OR “plant parasitic” OR “parasitic plant” OR “plant$parasitic” OR “root feeding” OR “root$feeding” OR “acari” OR “host$” OR “gall” OR “gall$” OR “whitefly” OR “whitefl*” OR “aleyrodidae” OR “thysanoptera” OR “moths” OR “scale” OR “scale$” OR “thripidae” OR “leafhoppers” OR “leafhopper$” OR “plant pathogens” OR “fungal” OR “aphididae” OR “Scolytinae” OR “bark beetle”’)

      NOT

      (“heavy metal$” OR “pollut*” OR “weather” OR “propert*” OR “probes” OR “spectr*” OR “antioxidant$” OR “transformation” OR “Secondary plant metabolite$” OR “metabolite$” OR “Postharvest” OR “Pollin*” OR “Ethylene” OR “Thinning” OR “fertil*” OR “Mulching” OR “Nutrient$” OR “human virus” OR “animal disease$” OR “plant extracts” OR “immunological” OR “purified fraction” OR “traditional medicine” OR “medicine” OR “mammal$” OR “bird$” OR “human disease$” OR “cancer” OR “therapeutic” OR “psoriasis” OR “blood” OR “medicinal ethnobotany” OR “Nitrogen-fixing” OR “patients” OR “Probiotic drugs” OR “Antioxidant” OR “Anti-Inflammatory” OR “plasma levels” OR “ethnomedicinal” OR “traditional uses of medicinal plants” OR “Antitumor” OR “Neuroprotective” OR “Hypoglycemic” OR “ozone sensitivity” OR “cardiotonic”)

      NOT

      TOPIC:

      Acanalonia conica” OR “Acanthosoma haemorrhoidale” OR “Acarosporium austriacum” OR “Acasis viretata” OR “Acherontia atropos” OR “Acleris cornana” OR “Acleris forbesana” OR “Acleris umbrana” OR “Acronicta americana” OR “Acronicta dactylina” OR “Acronicta funeralis” OR “Acronicta grisea” OR “Acronicta impleta” OR “Acrospeira mirabilis” OR “Acrospermum compressum” OR “Acrostaphylus pulvereus” OR “Actebia fennica” OR “Agnocoris reclairei” OR “Agnocoris rubicundus” OR “Agriopis aurantiaria” OR “Agriopis bajaria” OR “Allantus melanarius” OR “Alternaria alternata” OR “Alternaria tenuissima” OR “Altica cornivorax” OR “Ambrosiodmus rubricollis” OR “Amorbia humerosana” OR “Amphinema arachispora” OR “Amphipyra pyramidea” OR “Amphipyra pyramidoides” OR “Amphisphaerella alpigena” OR “Anavitrinella pampinaria” OR “Ancylis apicana” OR “Ancylis muricana” OR “Ancylis unculana” OR “Angerona prunaria” OR “Anisandrus sayi” OR “Anisota virginiensis” OR “Anoecia corni” OR “Anoecia cornicola” OR “Anoecia cornimaris” OR “Anoecia fulviabdominalis” OR “Anoecia furcate” OR “Anoecia haupti” OR “Anoecia himalayensis” OR “Anoecia ilicicola” OR “Anoecia japonica” OR “Anoecia major” OR “Anoecia oenotherae” OR “Anoecia takahashii” OR “Anoecia tanakai” OR “Anoecia vagans” OR “Anoplophora chinensis” OR “Antaeotricha leucillana” OR “Anthaxia fulgurans” OR “Anthaxia podolica” OR “Anthaxia salicis” OR “Anthaxia scutellaris” OR “Anthaxia semicuprea” OR “Antheraea polyphemus” OR “Anthocoptes cornicolus” OR “Anthocoptes platynotus” OR “Anthonomus quadrigibbus” OR “Anthostomella cornicola” OR “Anthostomella nitidula” OR “Antipspila metallella” OR “Antispila aurirubra” OR “Antispila cornifoliella” OR “Antispila freeman” OR “Antispila metallella” OR “Antispila petryi” OR “Antispila treitschkiella” OR “Aonidiella aurantii” OR “Aonidiella citrina” OR “Aphelenchoides fragariae” OR “Aphelia alleniana” OR “Aphis asclepiadis” OR “Aphis caliginosa” OR “Aphis cirsiioleracei” OR “Aphis cornifoliae” OR “Aphis fabae” OR “Aphis frangulae” OR “Aphis gossypi” OR “Aphis impatientis” OR “Aphis maculatae” OR “Aphis neogillette” OR “Aphis nigratibialis” OR “Aphis odinae” OR “Aphis salicariae” OR “Aphis spiraecola” OR “Apiognomonia errabunda” OR “Apiognomonia rigniacensis” OR “Apioporthe corni” OR “Aplopsora corni” OR “Arabis mosaic virus” OR “Archips argyrospila” OR “Archips podana” OR “Archips purpurana” OR “Archips rileyana” OR “Archips rosana” OR “Archips xylosteana” OR “Arctia caja” OR “Arcyria incarnata” OR “Argyrotaenia velutinana” OR “Armillaria mellea” OR “Artomyces pyxidatus” OR “Ascochyta cornicola” OR “Ascochyta medicaginicola” OR “Aspergillus flavus” OR “Asterococcus muratae” OR “Asteroma corni” OR “Asteromella bacteriiformis” OR “Asthena anseraria” OR “Athelia rolfsii” OR “Aulacaspis projecta” OR “Aulacorthum solani” OR “Aurantioporthe corni” OR “Aureobasidium pullulans” OR “Automeris io” OR “Baltazaria galactina” OR “Barrmaelia oxyacanthae” OR “Basiseptospora fallax” OR “Batophila fallax” OR “Belonolaimus longicaudatus” OR “Beltrania rhombica” OR “Bipolaris oryzae” OR “Biscogniauxia mediterranea” OR “Biston betularia” OR “Bitylenchus maximus” OR “Bjerkandera adusta” OR “Boczekiana celtidis” OR “Botryosphaeria dothidea” OR “Botrytis cinerea” OR “Broad bean wilt virus” OR “Bryobia praetiosa” OR “Bryobia ulmophila” OR “Byssomerulius corium” OR “Callimorpha dominula” OR “Callophrys rubi” OR “Calonectria morganii” OR “Caloptilia belfrageella” OR “Caloptilia burgessiella” OR “Caloptilia canadensisella” OR “Caloptilia cornusella” OR “Calycina vulgaris” OR “Camarographium koreanum” OR “Camarosporium incrustans” OR “Candidatus Phytoplasma asteris” OR “Candidatus Phytoplasma fragariae” OR “Capnodium citri” OR “Carcina quercana” OR “Carpatolechia decorella” OR “Carpocoris purpureipennis” OR “Carposina niponensis” OR “Catocala ultronia” OR “Celastrina argiolus” OR “Cenopalpus spinosus” OR “Cepphis advenaria” OR “Ceratobasidium ochroleucum” OR “Cerioporus scutellatus” OR “Ceriporia tarda” OR “Cerococcus parrotti” OR “Ceroplastes ceriferus” OR “Ceroplastes japonicus” OR “Ceuthospora corni” OR “Chalceopla dietziella” OR “Cheimophila salicella” OR “Cheirospora botryospora” OR “Cherry leaf roll virus” OR “Chionaspis corni” OR “Chionaspis lintneri” OR “Chionaspis salicis” OR “Chloroclystis v-ata” OR “Chondrostereum purpureum” OR “Choristoneura conflictana” OR “Choristoneura rosaceana” OR “Chrysobothris affinis” OR “Chrysobothris femorata” OR “Chrysomphalus dictyospermi” OR “Cilioplea coronata” OR “Cladosporium cladosporioides” OR “Cladosporium cornigenum” OR “Cladosporium herbarum” OR “Cladosporium sphaerospermum” OR “Clavaspis disclusa” OR “Clavaspis ulmi” OR “Clepsis persicana” OR “Clypeosphaeria mamillana” OR “Cnestus

      mutilatus” OR “Coccus hesperidum” OR “Coccus malloti” OR “Coleophora ahenella” OR “Coleophora albiantennaella” OR “Coleophora anatipennella” OR “Coleophora cornivorella” OR “Coleophora salicivorella” OR “Coleophora violacea” OR “Colletotrichum acutatum” OR “Colletotrichum gloeosporioides” OR “Colletotrichum godetiae” OR “Colotois pennaria” OR “Comstockaspis perniciosa” OR “Coniosporium peziza” OR “Conistra torrida” OR “Conoplea globosa” OR “Conoplea olivacea” OR “Coprinellus disseminatus” OR “Corniculariella urceola” OR “Corticium koleroga” OR “Corynespora cambrensis” OR “Coryneum corni-albae” OR “Coryneum corni-asperifoliae” OR “Cosmia trapezina” OR “Craneiobia corni” OR “Crepidotus epibryus” OR “Criconema demani” OR “Criconema mutabile” OR “Cristulariella corni” OR “Cristulariella depraedans” OR “Cristulariella moricola” OR “Cryptosphaeria moravica” OR “Cucumber mosaic virus” OR “Cucurbitaria callista” OR “Cydia molesta” OR “Cylindrocarpon ianthothele” OR “Cylindrosporium corni” OR “Cytospora corni” OR “Cytospora ceratosperma” OR “Cytospora fallax” OR “Cytospora leucosperma” OR “Cytospora populina” OR “Cytospora pruinose” OR “Cytospora pulcherrima” OR “Cytospora salicina” OR “Daedalea confragosa” OR “Daldinia vernicosa” OR “Daphnis nerii” OR “Daruvedia bacillata” OR “Dasystoma salicella” OR “Dematophora necatrix” OR “Dendrothele amygdalispora” OR “Diaporthe amygdali” OR “Diaporthe cornicola” OR “Diaporthe eres” OR “Diaporthe lagerstroemiae” OR “Diaporthe oncostoma” OR “Diaporthe pardalota” OR “Diaporthe rudis” OR “Diaspidiotus ancylus” OR “Diaspidiotus forbesi” OR “Diaspidiotus juglansregiae” OR “Diaspidiotus osborni” OR “Diaspidiotus ostreaeformis” OR “Diaspidiotus spiraspinae” OR “Diatrype albopruinosa” OR “Diderma radiatum” OR “Didymella glomerata” OR “Didymella pinodella” OR “Didymosphaeria decolorans” OR “Didymosphaeria oblitescens” OR “Diplodia corni” OR “Diplodia mamillana” OR “Diplodina macrospora” OR “Diptacus corni” OR “Discohainesia oenotherae” OR “Discosia artocreas” OR “Discostroma corticola” OR “Discostroma fuscellum” OR “Discula destructiva” OR “Dogwood mosaic nepovirus” OR “Dothichiza ambigua” OR “Dothiorella sarmentorum” OR “Dothioropsis corni” OR “Drepanopeziza populi” OR “Drosicha corpulenta” OR “Drosophila suzukii” OR “Dysmicoccus wistariae” OR “Eacles imperialis” OR “Echinosphaeria canescens” OR “Ectropis crepuscularia” OR “Edwardsiana diversa” OR “Elasmopalpus lignosellus” OR “Elsinoe corni” OR “Elsinoe fawcettii” OR “Empoasca decipiens” OR “Endopiza rhoifructana” OR “Ennomos subsignaria” OR “Eotetranychus cornicola” OR “Epiblema similana” OR “Epicoccum nigrum” OR “Epidiaspis leperii” OR “Epinotia lindana” OR “Erannis defoliaria” OR “Erannis tiliaria” OR “Erysiphe cornicola” OR “Erysiphe penicillate” OR “Erysiphe pulchra” OR “Erysiphe tortilis” OR “Euchlaena effecta” OR “Euchlaena irraria” OR “Euchlaena johnsonaria” OR “Euchlaena serrata” OR “Eucosma landana” OR “Eudeilinia herminiata” OR “Eugraphe sigma” OR “Eulecanium tiliae” OR “Eulithis xylina” OR “Eupithecia exiguata” OR “Euplexia benesimilis” OR “Euplexia lucipara” OR “Eupoecilia ambiguella” OR “Eupoecilia angustana” OR “Euproctis chrysorrhoea” OR “Euproctis similis” OR “Eurydema ornata” OR “Euthyatira pudens” OR “Eutrapela clemataria” OR “Eutypa flavovirens” OR “Eutypa lata” OR “Eutypa ludibunda” OR “Eutypa maura” OR “Eutypella stellulata” OR “Euwallacea fornicatus sensu lato” OR “Exidia cystidiata” OR “Exosporium occidentale” OR “Ferrisia gilli” OR “Flagelloscypha libertiana” OR “Floricola ulema” OR “Fomitiporia mediterranea” OR “Fusarium haematococcum” OR “Fusarium lateritium” OR “Fusarium oxysporum” OR “Fusarium sambucinum” OR “Fusarium solani” OR “Fuscoporia ferrea” OR “Fuscoporia ferruginosa” OR “Fuscoporia scruposa” OR “Fuscoporia torulosa” OR “Ganoderma applanatum” OR “Gliocephalotrichum simplex” OR “Globisporangium irregulare” OR “Globisporangium splendens” OR “Gloeodes pomigena” OR “Gloeosporium corni” OR “Glomopsis corni” OR “Glyphium corrugatum” OR “Gnophos furvata” OR “Godronia fuliginosa” OR “Graphiphora augur” OR “Grovesinia moricola” OR “Grovesinia pyramidalis” OR “Hainesia marsdeniae” OR “Halyomorpha halys” OR “Hapalocystis corni” OR “Haploa confusa” OR “Haploa lecontei” OR “Haradamyces foliicola” OR “Hedya corni” OR “Hedya nubiferana” OR “Helicobasidium mompa” OR “Helicotylenchus canadensis” OR “Helicotylenchus pseudorobustus” OR “Heliococcus osborni” OR “Heliococcus stachyos” OR “Helminthosporium velutinum” OR “Hemiberlesia cyanophylli” OR “Hemiberlesia diffinis” OR “Hemileuca nevadensis” OR “Hemithea aestivaria” OR “Hendersonia alternifoliae” OR “Hendersonia fiedleri” OR “Herpetogramma pertextalis” OR “Hesperumia sulphuraria” OR “Heterocampa biundata” OR “Heterocampa guttivitta” OR “Heterocampa subrotata” OR “Heterodera zeae” OR “Hoplolaimus stephanus” OR “Hyalophora cecropia” OR “Hydnophlebia chrysorhiza” OR “Hydrelia albifera” OR “Hydria undulata” OR “Hymenoscyphus serotinus” OR “Hypagyrtis unipunctata” OR “Hypena abalienalis” OR “Hypena bijugalis” OR “Hyphantria cunea” OR “Hyphoderma rimosum” OR “Hypoderma commune” OR “Hypomecis punctinalis” OR “Hypoxylon albocinctum” OR “Hypoxylon fuscum” OR “Hypoxylon rubiginosum” OR “Hysterium pulicare” OR “Hysterobrevium mori” OR “Hysteropatella prostii” OR “Icerya purchasi” OR “Ilyonectria destructans” OR “Incurvaria oehlmaniella” OR “Incurvaria pectinea” OR “Iridopsis larvaria” OR “Irpex lacteus” OR “Irpicomyces cornicola” OR “Jattaea allantospora” OR “Jattaea cornina” OR “Jodis lactearia” OR “Kretzschmaria frustulosa” OR “Lachnella corni” OR “Laestadia systema-solare” OR “Lambertella corni-maris” OR “Lasiocampa quercus” OR “Lasiodiplodia theobromae” OR “Lecanodiaspis prosopidis” OR “Leiosphaerella vexata” OR “Lepidosaphes corni” OR “Lepidosaphes kuwacola” OR “Lepidosaphes malicola” OR “Lepidosaphes tubulorum” OR “Lepidosaphes ulmi” OR “Lepidosaphes yanagicola” OR “Leptographium profanum” OR “Leptosphaeria borealis” OR “Leptosphaeria platycarpa” OR “Leptosphaeria rugosa” OR “Leptosphaeria vagabunda” OR “Leptostroma herbarum” OR “Leucostoma translucens” OR “Linospora carpini” OR “Linospora elata” OR “Liothrips austriacus” OR “Lithophane georgii” OR “Lithophane laticinerea” OR “Lithophane vivida” OR “Lobesia botrana” OR “Lobesia reliquana” OR “Lojkania decorticate” OR “Lomographa bimaculata” OR “Lophiostoma oreophilum” OR “Lophiostoma prominens” OR “Lophiostoma vagabundum” OR “Lopholeucaspis japonica” OR “Lycia rachelae” OR “Lycia ursaria” OR “Lycorma delicatula” OR “Lymantor aceris” OR “Lymantria dispar” OR “Lyomyces crustosus” OR “Machimia tentoriferella” OR “Macrophoma paniculata” OR “Macrophomina phaseolina” OR “Macrosiphum cornifoliae” OR “Macrosiphum euphorbiae” OR “Macrosiphum hamiltoni” OR “Macrosiphum manitobense” OR “Malacosoma americanum” OR “Malacosoma disstria” OR “Massaria gigantispora” OR “Massarina albocarnis” OR “Massarina polymorpha” OR “Massariovalsa sudans” OR “Melanaspis nigropunctata” OR “Melanaspis obscura” OR “Melanaspis tenebricosa” OR “Melanolophia canadaria” OR “Melanolophia imitata” OR “Melanomma aspegrenii” OR “Melanomma populicola” OR “Melaspilea proximella” OR “Meliola nidulans” OR “Meloidogyen fallax” OR “Meloidogyne chitwoodi” OR “Meloidogyne hapla” OR “Meloidogyne platani” OR “Melomastia mastoidea” OR “Merlinius brevidens” OR “Meruliopsis corium” OR “Mesocriconema xenoplax” OR “Metarranthis warnerae” OR “Metasphaeria fiedleri” OR “Microdiplodia papillosa” OR “Mollisia discolor” OR “Mollisia propinqua” OR “Mollisia rosae” OR “Monilinia corni” OR “Monilinia fructicola” OR “Monilinia fructigena” OR “Monochaetia cornicola” OR “Mononychellus caribbeanae” OR “Morrisonia confusa” OR “Mycosphaerella auerswaldii” OR “Mycosphaerella cornicola” OR “Mycosphaerella corni” OR “Mycosphaerella punctiformis” OR “Myrmaecium harperianum” OR “Myxosporium corni” OR “Myxosporium everhartii” OR “Myxosporium nitidum” OR “Myxosporium roumeguerei” OR “Myzus persicae” OR “Naeviopsis pusilla” OR “Nectria cinnabarina” OR “Nectria rehmiana” OR “Nectriella atrorubra” OR “Nemania albocincta” OR “Nemania serpens” OR “Neocoenorrhinus germanicus” OR “Neocucurbitaria cava” OR “Neocosmospora rehmiana” OR “Neofusicoccum luteum” OR “Neofusicoccum parvum” OR “Neofusicoccum ribis” OR “Neonectria coccinea” OR “Neonectria ditissima” OR “Neopinnaspis harperi” OR “Neopulvinaria innumerabilis” OR “Nigrospora oryzae” OR “Niptera stictella” OR “Noctua comes” OR “Noctua janthe” OR “Odontopera bidentata” OR “Oemona hirta” OR “Olethreutes connectus” OR “Olethreutes exaeresimum” OR “Olethreutes inornatana” OR “Olethreutes punctanum” OR
      “Olethreutes quadrifidum” OR “Olethreutes subnubilum” OR “Olethreutes valdanum” OR “Olethreutes versicolorana” OR “Oligia mactata” OR “Oligonychus coniferarum” OR “Oligonychus endytus” OR “Oligonychus propetes” OR “Operophtera brumata” OR “Orgyia antiqua” OR “Orgyia leucostigma” OR “Orientus ishidae” OR “Orthosia garmani” OR “Orthosia hibisci” OR “Orthotaenia undulana” OR “Ostropa barbara” OR “Otiorhynchus apenninus” OR “Otiorhynchus crataegi” OR “Ourapteryx sambucaria” OR “Palomena prasina” OR “Palthis angulalis” OR “Pammene rhediella” OR “Pandemis canadana” OR “Pandemis corylana” OR “Pandemis limitata” OR “Pandemis pyrusana” OR “Paramyrothecium roridum” OR “Parasa indetermina” OR “Paratylenchus projectus” OR “Parlatoreopsis chinensis” OR “Parlatoreopsis pyri” OR “Parlatoria octolobata” OR “Parlatoria oleae” OR “Parlatoria theae” OR “Parthenolecanium corni” OR “Passalora angelicae” OR “Passalora corni” OR “Passalora cornicola” OR “Patellaria clavispora” OR “Pavonia pavonia” OR “Pelionella kansui” OR “Penicillium brevicompactum” OR “Penicillium chrysogenum” OR “Penicillium citrinum” OR “Penicillium miczynskii” OR “Penicillium simplicissimum” OR “Penicillium spinulosum” OR “Penicillium thomii” OR “Peniophora cinerea” OR “Peniophora versiformis” OR “Peniophora violaceolivida” OR “Perenniporia tenuis” OR “Perenniporia unita” OR “Pero mizon” OR “Peroneutypa scoparia” OR “Pestalotia cornifolia” OR “Pestalotiopsis guepinii” OR “Pestalotiopsis mangiferae” OR “Pestalotiopsis microspora” OR “Pestalotiopsis monochaeta” OR “Pestalotiopsis versicolor” OR “Pestalotiopsis zahlbruckneriana” OR “Petunia asteroid mosaic virus” OR “Peyronellaea obtuse” OR “Pezicula corni” OR “Pezicula cornicola” OR “Pezicula cornina” OR “Pezicula ocellata” OR “Pezicula rubi” OR “Phaeoacremonium minimum” OR “Phaeoisariopsis pruni-grayanae” OR “Phaeosphaeria guttulata” OR “Phanerochaete laevis” OR “Phellinus igniarius” OR “Phenacoccus aceris” OR “Phialocephala fortinii” OR “Phigalia titea” OR “Phlebia fascicularia” OR “Phoma candidula” OR “Phoma corni-albae” OR “Phoma florida” OR “Phoma paniculata” OR “Phomopsis corni” OR “Phyllachora subcuticularis” OR “Phyllactinia corni” OR “Phyllactinia guttata” OR “Phyllobius glaucus” OR “Phyllobius pyri” OR “Phyllobius virideaeris” OR “Phyllocoptes depressus” OR “Phyllosticta capitalensis” OR “Phyllosticta corni-canadensis” OR “Phyllosticta cornicola” OR “Phyllosticta fallopiae” OR “Phyllosticta globifera” OR “Phyllosticta minima” OR “Phyllosticta pervincae” OR “Phyllosticta solitaria” OR “Phyllosticta starbaeckii” OR “Phyllosticta taurica” OR “Phymatotrichopsis omnivora” OR “Physalospora corni” OR “Physalospora everhartii” OR “Phytocoris longipennis” OR “Phytomyza agromyzina” OR “Phytophthora cactorum” OR “Phytophthora cinnamomi” OR “Phytophthora citricola” OR “Phytophthora citrophthora” OR “Phytophthora cryptogea” OR “Phytophthora megasperma” OR “Phytophthora nicotianae” OR “Phytophthora palmivora” OR “Phytophthora plurivora” OR “Phytophthora ramorum” OR “Pilidium lythri” OR “Pinnaspis hikosana” OR “Pinnaspis indivisa” OR “Placosphaeria cornicola” OR “Plagiostoma salicellum” OR “Plemyria georgii” OR “Pleomassaria swidae” OR “Pleospora atromaculans” OR “Pleospora laricina” OR “Pleuroceras tenellum” OR “Pochazia shantungensis” OR “Podosphaera corni” OR “Polia bombycina” OR “Polia nebulosa” OR “Polydrusus cervinus” OR “Polyphaenis sericata” OR “Pratylenchus crenatus” OR “Pratylenchus neglectus” OR “Pratylenchus penetrans” OR “Pratylenchus vulnus” OR “Probole alienaria” OR “Probole amicaria” OR “Probole nepiasaria” OR “Prociphilus cornifoliae” OR “Prosthecium platanoidis” OR “Pseudaonidia duplex” OR “Pseudaonidia paeoniae” OR “Pseudasiphonaphis corni” OR “Pseudaulacaspis biformis” OR “Pseudaulacaspis cockerelli” OR “Pseudaulacaspis pentagona” OR “Pseudocamarosporium corni” OR “Pseudomassaria corni” OR “Pseudomassaria foliicola” OR “Pseudomassaria necans” OR “Pseudomonas syringae pv. syringae” OR “Pseudovalsa titan” OR “Puccinia acuminata” OR “Puccinia porphyrogenita” OR “Pucciniastrum coriariae” OR “Pucciniastrum corni” OR “Pulvinaria acericola” OR “Pulvinaria corni” OR “Pulvinaria hazeae” OR “Pulvinaria hydrangeae” OR “Pulvinaria idesiae” OR “Pulvinaria kuwacola” OR “Pulvinaria nishigaharae” OR “Pulvinaria occidentalis” OR “Pulvinaria regalis” OR “Pyrrhocoris apterus” OR “Quaternaria dissepta” OR “Ramularia angustissima” OR “Ramularia gracilipes” OR “Ramularia stolonifer” OR “Refractohilum achromaticum” OR “Rhaphigaster nebulosa” OR “Rhizobium radiobacter” OR “Rhizobium rhizogenes” OR “Rhizochaete filamentosa” OR “Rhizoctonia anceps” OR “Rhizoctonia solani” OR “Rhopobota myrtillana” OR “Rhynchites germanicus” OR “Rhyparia purpurata” OR “Rosellinia aquila” OR “Rosellinia mammiformis” OR “Rotylenchus robustus” OR “Saccothecium sepincola” OR “Saissetia coffeae” OR “Saissetia miranda” OR “Samia cynthia” OR “Sanghuangporus ligneus” OR “Sarcinella heterospora” OR “Sarcinella pulchra” OR “Sarocladium kiliense” OR “Saturnia pavonia” OR “Schiffnerula corni” OR “Schizopora paradoxa” OR “Schizothyrium jamaicense” OR “Schizothyrium pomi” OR “Schizoxylon compositum” OR “Schizura concinna” OR “Schizura unicornis” OR “Sclerotinia sclerotiorum” OR “Sebacina incrustans” OR “Seimatosporium corni” OR “Seimatosporium salicinum” OR “Seiridium corni” OR “Seiridium cupressi” OR “Seiridium venetum” OR “Selenia dentaria” OR “Septobasidium bogoriense” OR “Septobasidium castaneum” OR “Septobasidium cokeri” OR “Septobasidium fumigatum” OR “Septobasidium pseudopedicellatum” OR “Septobasidium tanakae” OR “Septonema secedens” OR “Septoria canadensis” OR “Septoria cornicola” OR “Septoria corni-maris” OR “Septoria cornina” OR “Septoria floridae” OR “Septosporium fuliginosum” OR “Sheathospora cornuta” OR “Shevtchenkella bulgarica” OR “Shevtchenkella cornifoliae” OR “Shevtchenkella glabratae” OR “Simplicillium lanosoniveum” OR “Siphocoryne cornicolum” OR “Sirosporium corni” OR “Spatalistis bifasciana” OR “Sphaeropsis atra” OR “Sphaeropsis cornicola” OR “Sphaerulina cornicola” OR “Sphinx chersis” OR “Sphinx gordius” OR “Spilosoma lutea” OR “Spiramater grandis” OR “Spiramater lutra” OR “Sporidesmium toruloides” OR “Sporocadus cornicola” OR “Stagonopsis pallida” OR “Stauropus fagi” OR “Stephanitis pyri” OR “Stereum gausapatum” OR “Stereum gausapatum” OR “Stictis mollis” OR “Stictis sphaeroboloidea” OR “Stictis stigma” OR “Stictophacidium carniolicum” OR “Stigmina cornicola” OR “Sunira verberata” OR “Synanthedon geliformis” OR “Synanthedon scitula” OR “Synaxis jubararia” OR “Synchytrium aureum” OR “Synchytrium corni” OR “Syndemis afflictana” OR “Takahashia japonica” OR “Talaromyces assiutensis” OR “Talaromyces cecidicola” OR “Talaromyces trachyspermus” OR “Tegonotus acutilobus” OR “Teichospora ignavis” OR “Teichospora winteriana” OR “Tenthredo atra” OR “Tetracis cachexiata” OR “Tetranychus urticae” OR “Thaxteriella pezizula” OR “Thekopsora lanpingensis” OR “Thekopsora triangula” OR “Thelonectria discophora” OR “Thyridopteryx ephemeraeformis” OR “Thyrostroma cornicola” OR “Tilletiopsis lilacina” OR “Tobacco ringspot virus” OR “Togninia cornicola” OR “Tomato bushy stunt virus” OR “Tomato mosaic virus” OR “Tomato ringspot virus” OR “Tomato spotted wilt orthotospovirus” OR “Trametes gibbosa” OR “Trametes versicolor” OR “Trematosphaeria cornina” OR “Tremella lutescens” OR “Tremella mesenterica” OR “Trichoderma lixii” OR “Trichoferus campestris” OR “Trirhacus biokovensis” OR “Tylenchorhynchus claytoni” OR “Tympanis fasciculata” OR “Tympanopsis confertula” OR “Tyromyces chioneus” “Valsaria anserina” OR “Valsaria cornicola” OR “Vanderbylia fraxinea” OR “Velataspis dentata” OR “Venturia clintonii” OR “Venturia corni” OR “Venturia systema-solare” OR “Venusia pearsalli” OR “Verpa digitaliformis” OR “Vitreoporus dichrous” OR “Vuilleminia comedens” OR “Xanthotype sospeta” OR “Xanthotype urticaria” OR “Xenocriconemella macrodora” OR “Xenosporium berkeleyi” OR “Xestia ditrapezium” OR “Xestia triangulum” OR “Xiphinema americanum” OR “Xyleborinus saxesenii” OR “Xyleborus affinis” OR “Xyleborus dispar” OR “Xyleborus xylographus” OR “Xylodon radula” OR “Xylosandrus compactus” OR “Xylosandrus crassiusculus” OR “Xylosandrus germanus” OR “Zale aeruginosa” OR “Zale undularis” OR “Zaranga permagna” OR “Zygophiala jamaicensis” OR “Zythia aurantiaca”

      APPENDIX C: Excel file with the pest list of Cornus species

      Appendix C can be found in the online version of this output in the ‘supporting information section’.