United States Department of Importation of spp. in Agriculture Approved Growing Media from

Animal and Denmark into the United States Health Inspection Service A Pathway-Initiated Pest Risk Assessment Plant Protection and Quarantine

July 30, 2012

Version 1 (Original)

Agency Contact: Plant Epidemiology and Risk Analysis Laboratory Center for Plant Health Science and Technology

United States Department of Agriculture Animal and Plant Health Inspection Service Plant Protection and Quarantine 1730 Varsity Drive, Ste. 300 Raleigh, NC 27606

Pest Risk Assessment for Campanula spp. from Denmark

Executive Summary

In this pathway-initiated commodity risk assessment, we examined the risks associated with the proposed importation of Campanula spp. established in APHIS-approved growing media from Denmark into the United States. We analyzed these pests using the methodology described in the USDA-APHIS-PPQ Guidelines for Pathway-Initiated Risk Analysis 5.02, which examine pest biology in the context of the Consequences of Introduction and the Likelihood of Introduction and estimate the baseline Pest Risk Potential, which is the risk in the absence of mitigation.

We analyzed the following pests: the leafminers, Liriomyza buhri Hering, L. strigata (Meigen), and Phytomyza campanulae Hendel; the whitefly, Aleyrodes lonicerae; the aphids, Aphis psammophila Szelegiewicz, Uroleucon campanulae (Kaltenbach), U. nigrocampanulae (Theobald), and U. rapunculoidis (Börner); the thrips, Thrips major Uzel; and the mollusk, Arianta arbustorum (L.). We rated the Pest Risk Potential of all of these pests as Medium.

All plants in growing media imported into the United States must be approved by APHIS and must comply with the requirements in 7 CFR 319.37-8, but specific additional phytosanitary measures may be necessary for pests with a Medium or High risk potential.

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Table of Contents

Executive Summary ...... ii 1. Background ...... 1 2. Risk Assessment ...... 1 2.1. Initiating Event: Proposed Action...... 1 2.2. Assessment of the Weed Potential of Campanula spp...... 2 2.3. Current Status and Pest Interceptions ...... 2 2.4. Pest Categorization ...... 3 2.5. Consequences of Introduction ...... 11 2.6. Likelihood of Introduction ...... 15 2.7. Pest Risk Potential and Conclusion ...... 17 3. Acknowledgements ...... 17 4. Literature Cited ...... 17

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1. Background

This document was prepared by the Plant Epidemiology and Risk Analysis Laboratory of the USDA Animal and Plant Health Inspection Service (APHIS), Plant Protection and Quarantine (PPQ), Center for Plant Health Science and Technology, in response to a request to evaluate the risks associated with the importation of commercially produced Campanula spp. plants (at least four months old) established in APHIS-approved growing media from Denmark into the United States.

The International Plant Protection Convention (IPPC) provides guidance for conducting pest risk analyses. The methods used here are consistent with guidelines provided by the IPPC, specifically the International Standard for Phytosanitary Measures (ISPM) on “Pest Risk Analysis for Quarantine Pests, Including Analysis of Environmental Risks and Living Modified Organisms” (IPPC, 2011a). The use of biological and phytosanitary terms is consistent with the “Glossary of Phytosanitary Terms” (IPPC, 2011a).

Three stages of pest risk analysis are described in international standards: Stage 1, Initiation; Stage 2, Risk Assessment; and Stage 3, Risk Management. This document satisfies the requirements of Stages 1 and 2.

This is a qualitative risk analysis; estimates of risk are expressed in terms of High, Medium, and Low pest risk potentials based on the combined ratings for specified risk elements (PPQ, 2000) related to the probability and consequences of importing Campanula spp. plants established in APHIS-approved growing media from Denmark. For the purposes of this assessment High, Medium, and Low probabilities will be defined as: High: More likely to occur than not to occur Medium: As likely to occur as not to occur Low: More likely not to occur than to occur

All plants in growing media imported into the United States must be approved by APHIS and must comply with all requirements in 7 CFR 319.37-8. Identification of additional phytosanitary measures to mitigate the risk, if any, for these pests is undertaken as part of Stage 3 (Risk Management).

2. Risk Assessment

2.1. Initiating Event: Proposed Action

We prepared this commodity-based, pathway-initiated pest risk assessment in response to a request for USDA authorization to allow the importation from Denmark of Campanula spp. with roots in approved growing media according to the requirements in 7 CFR 319.37-8. This also includes the written agreement that will be established between APHIS and the national plant protection organization of Denmark.

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2.2. Assessment of the Weed Potential of Campanula spp.

If the species considered for import poses a risk as a weed pest, then a “pest-initiated” risk assessment is conducted. The results of the screening for weed potential for Campanula spp. (Table 1) did not prompt a pest initiated risk assessment because Campanula plants are already present in the United States and are not reported as weeds.

Table 1. Process for determining weed potential of Campanula spp. The genus Campanula () is native to the temperate parts of the northern hemisphere and contains over 250 species (Page and Olds, 2001). Phase 1. Is the genus new to or not widely prevalent in the United States? (exclude plants grown under USDA permit in approved containment facilities) Native species of Campanula occur in the continental United States and are widely cultivated. No Campanula species are native to Puerto Rico, Hawaii, the U.S. Virgin Islands, or Guam (NGRP, 2012; NRCS, 2012). Phase 2. Answer Yes or No to the following questions: Is the genus listed in: No Geographical Atlas of World Weeds (Holm et al., 1997) No World's Worst Weeds (Holm et al., 1977) No Report of the Technical Committee to Evaluate Noxious Weeds; Exotic Weeds for Federal Noxious Weed Act (Gunn and Ritchie, 1982) No Economically Important Foreign Weeds (Reed, 1977) No Weed Science Society of America list (WSSA, 2007) No Is there any literature reference indicating weed potential (e.g., AGRICOLA, CAB, Biological Abstracts, AGRIS; search on “Campanula” combined with "weed")? Phase 3. Conclusion: Many species of this genus are present in the United States, and the answer to all of the questions is no; therefore, the commodity does not have weed potential.

2.3. Current Status and Pest Interceptions

In 1994, Denmark, in combination with Belgium, Israel, and the Netherlands, requested market access to the United States for a number of genera of live plants, including Campanula. No decision was reached. In 2010, the Danish Ministry of Food, Agriculture and Fisheries requested market access specifically for Campanula plants rooted in APHIS-approved growing media, as listed in 7 CFR 319.37-8. This risk assessment is in response to this request.

Between 1985 and 2012 several quarantine pests were intercepted 5 or more times on Campanula spp. from around the world, but none of those same pests were intercepted 5 or more times on any commodities from Denmark (PestID, 2012).

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2.4. Pest Categorization

2.4.1. Methodology In this process we determine if a pest has the characteristics of a quarantine pest or those of a regulated non-quarantine pest. Our procedures are based on ISPM 11 ((IPPC, 2009)). First, we develop a comprehensive list of potential quarantine pests known to occur in the country or region from which the commodity is to be exported and which are associated with the commodity. To be a quarantine pest the organism must be “of potential economic importance” and must not yet be present in the area being assessed, or if present, it should be under official control. Because all pests on the list are associated with the plant species, they are considered to be “of potential economic importance” (IPPC, 2009: ISPM #11). The listed pests may or may not also occur in the United States.

We list pests associated with Campanula spp. in Denmark below (Table 2). We produced the list based on evidence in the scientific literature, manuals on production, a list provided by the Danish Ministry of Food, Agriculture and Fisheries, and other sources of general information. This list identifies (1) the host status of the pests in the United States, (2) the generally affected plant part or parts, (3) the quarantine status of the pest with respect to the United States, (4) potential for commercial Campanula spp. in approved growing media to introduce the pest into the United States, and (5) pertinent citations for the distribution or the biology of the pest. Because of specific characteristics of biology and distribution, many organisms are eliminated from further consideration as sources of phytosanitary risk on Campanula spp. because they do not satisfy the IPPC definition of a quarantine pest. We shaded the quarantine pests identified as likely to follow the commodity pathway and selected for further analysis.

Even if non-quarantine pests are able to follow the pathway, phytosanitary measures against these pests would not be justified because the pests already occur in the United States. Information on plant part association and whether the pest is likely to follow the pathway is therefore not needed for non-quarantine pests. For the non-quarantine pests in Table 2, we put N/A (= Not Applicable) in the columns for “Plant Part(s) Association” and “Likely to Follow Pathway.”

Table 2. Pests associated with Campanula spp. in Denmark. For distribution information, DK = Denmark, HI = Hawaii, PR = Puerto Rico, and US = United States. Pest name Host status Distribution Quaran- Plant part Follow tine pest association Pathway ACARI Tetranychidae Bryobia praetiosa Koch Bolland et al., DK, US (Bolland et No N/A N/A 1998 al., 1998) Tetranychus urticae Bolland et al., DK, US (Bolland et No N/A N/A Koch 1998 al., 1998)

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Pest name Host status Distribution Quaran- Plant part Follow tine pest association Pathway ARTHROPODA Diptera: Agromyzidae Chromatomyia horticola Pitkin et al., 2012 (Pitkin et al., 2012) No (see Stem Yes (Goureau), 2.4.2 below) Liriomyza buhri Hering Bromaeus, 2011; DK (Bromaeus, Yes Stem (Spencer, Yes Spencer, 1990 2011) 1990) Liriomyza strigata Pitkin et al., 2012; DK (Pitkin et al., Yes Leaf (Pitkin et Yes (Meigen) Spencer, 1990 2012; Spencer, al., 2012; 1990) Spencer, 1990) Phytomyza campanulae Bromaeus, 2011; DK (Bromaeus, Yes Leaf (Pitkin et Yes Hendel Pitkin et al., 2012; 2011) al., 2012; Spencer, 1990 Spencer, 1990) Hemiptera: Aleyrodidae Aleyrodes lonicerae Mound and DK (Martin et al., Yes Leaf (Hill, 1987) Yes Walker Halsey, 1978 2000) Trialeurodes Mound and DK, US, HI, PR No N/A N/A vaporariorum Halsey, 1978 (Mound and Halsey, Westwood 1978) Hemiptera: Aphididae Aphis fabae Scopoli Osiadacz and DK, US (Blackman No N/A N/A Hałaj, 2011 and Eastop, 2000) Aphis psammophila Osiadacz and DK (Heie et al., Yes Leaf (Blackman Yes Szelegiewicz Hałaj, 2011 1997) and Eastop, 2000) Aulacorthum solani Blackman and Worldwide1 No N/A N/A (Kaltenbach) Eastop, 2000 (Blackman and Eastop, 2000) Dysaphis (Pomaphis) Heie, 1986 DK, US (CA) (Heie, Yes Leaf (Heie, 1992) Yes2 sorbi (Kaltenbach) 1992) Myzus ascalonicus Blackman and Worldwide No N/A N/A Doncaster Eastop, 2000 (Blackman and Eastop, 2000) Myzus persicae Sulzer Blackman and Worldwide No N/A N/A Eastop, 2000 (Blackman and Eastop, 2000) Neomyzus circumflexus Blackman and Worldwide No N/A N/A (Buckton) Eastop, 2000 (Blackman and Eastop, 2000) Rhopalosiphoninus Blackman and DK, US (Blackman No N/A N/A staphyleae (Koch) Eastop, 2000 and Eastop, 2000)

1 Unless otherwise noted, “Worldwide” includes both Denmark and the United States. 2 We did not analyze this pest further because it rarely attacks Campanula and is not considered a pest (Heie, 1986).

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Pest name Host status Distribution Quaran- Plant part Follow tine pest association Pathway Uroleucon campanulae Heie, 1995; DK (Andreev et al., Yes Leaf (Blackman Yes (Kaltenbach) Osiadacz and 2011; Heie, 1986) and Eastop, Hałaj, 2011 2000), stem, flower (Heie, 1995) Uroleucon Heie, 1995; DK (Andreev et al., Yes Leaf (Blackman Yes nigrocampanulae Osiadacz and 2011; Heie, 1994) and Eastop, (Theobald) Hałaj, 2011 2000); (Heie, 1995) Uroleucon rapunculoidis Heie, 1995; DK (Heie, 1995; Yes Flower, stem Yes (Börner) Osiadacz and Nieto Nafría et al., (Heie, 1995) Hałaj, 2011 2011) Lepidoptera: Tortricidae Cnephasia asseclana Pitkin et al., 2012 (Pitkin et al., 2012) No (see (Denis & 2.4.2 Schiffermüller) below) Cnephasia incertana Pitkin et al., 2012 (Pitkin et al., 2012) No (see (Treitschke) 2.4.2 below) Thysanoptera: Thripidae Frankliniella occidentalis Danish Plant DK (Danish Plant No N/A N/A (Pergande) Directorate, 2011 Directorate, 2011) Thrips major Uzel PestID, 2012 DK (Vierbergen and Yes Leaf (PestID, Yes zur Strassen, 2004) 2012) Thrips tabaci Lindeman Pirone, 1978 (Hansen, 1988) No N/A N/A MOLLUSKS Agriolimacidae Deroceras agreste (L.) Stahl, 1888 DK (WAD, 2012); No N/A N/A [= Limax agresteis] US (Archer, 1939; Richards, 1934) Arionidae Arion ater (L.) [= A. Barnes and Weil, Northern Europe No N/A N/A empiricorum Férussac] 1945 (Cain and Williamson, 1958; Kono et al., 1977) Helicidae Arianta arbustorum [= Stahl, 1888 (Steenberg, 1911) Yes Leaf Yes Helix arbustorum (Baur and (Linnæus, 1758)] Raboud, 1988) Cepaea hortensis Stahl, 1888 Western Europe, US No N/A N/A (Müller) [= Helix (Jones et al., 1977) hortensis Müller (Murray, 1963)]

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Pest name Host status Distribution Quaran- Plant part Follow tine pest association Pathway Succineidae Oxyloma elegans (Risso) DEFRA, 2003 DK (Kerney and No (non- N/A N/A [= O. pfeifferi Cameron, 1979; actionable) (Rossmässler); Rognes, 1991) (PestID, Succinea pfeifferi 2012) Rossmässler (Rossmässler, 1835)] NEMATODES Aphelenchoides fragariae Knight et al., 2002 DK, US (CABI, No N/A N/A (Ritzema - Bos) 2012) Christie BACTERIA Rhizobium radiobacter CABI, 2012 DK, restricted No N/A N/A (Beijerinck & van distribution (CABI, Delden) Young et al. 2012) [= Agrobacterium radiobacter (Beijerinck & van Delden) Conn] Rhodococcus fascians Buchwald, 1946; DK (Buchwald, Yes (HI Leaf (Putnam and Yes3 (Tilford) Goodfellow Putnam and 1946; CABI, 2012); and PR) Miller, 2006) Miller, 2006 Continental US (Putnam and Miller, 2006) FUNGI Ascochyta–like spores Danish Plant DK (Danish Plant Undeter- N/A N/A Directorate, 2011 Directorate, 2011) mined Botrytis cinerea Pers. : Farr and Rossman, DK, US (Farr and No N/A N/A Fr. Teleomorph: 2012 Rossman, 2012) Botryotinia fuckeliana (de Bary) Whetzel Botrytis sp. Danish Plant DK (Danish Plant Undeter- N/A N/A Directorate, 2011 Directorate, 2011) mined Coleosporium Wick and DK (CABI, 2012); Yes (HI, Flowers, leaves Yes3 tussilaginis (Pers.) Dicklow, 1999 Continental US (Farr PR) (CABI, 2012) Lev. in C. d'Orb [= C. and Rossman, 2012); campanulae (Pers.) G. (Petrillo, 2012) Winter [Alternate State): Peridermium orientale Cooke] Corticum rolfsii Curzi Farr and Rossman, DK (CABI, 2012), No N/A N/A [Anamorph: 2012 US (Farr and Sclerotium rolfsii Rossman, 2012) Sacc.]

3 Although this pest may follow the pathway, we did not further analyze it. See section 2.4.2 for a full discussion.

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Pest name Host status Distribution Quaran- Plant part Follow tine pest association Pathway Cyathus olla Batsch : Lind, 1913, DK (Lind, 1913); Yes (HI) Stem, roots Yes3 Pers Vesterholt et al., Continental US, PR (Shinners- 2003 (Farr and Rossman, Carnelley et al., 2012) 2002) Erysiphe pisi var. pisi D. Farr and Rossman, DK, Continental US Yes (HI Leaves (Farr and Yes3 C. [= Erysiphi 2012 (Farr and Rossman, and PR) Rossman, 2012) communis (Wallr. : Fr.) 2012) Schltdl.] Fusarium oxysporum Danish Plant DK, US (Farr and No N/A N/A Schltdl. : Fr. Directorate, 2011 Rossman, 2012) Fusarium graminearum Lind, 1913 DK (Lind, 1913); Yes (HI Leaves, flower Yes3 Schwabe [Teleomorph Continental US (Farr and PR) (Farr and Gibberella zeae and Rossman, 2012) Rossman, 2012) (Schwein. : Fr.) Petch; = G. saubinetii (Mont.) Sacc] Golovinomyces Wick and DK, US (Farr and No N/A N/A cichoracearum (DC.) Dicklow, 1999 Rossman, 2012) V.P. Heluta [= Erysiphe cichoracearum DC] Hendersonia Lind, 1913 DK (Lind, 1913); Yes (HI Stems (Farr and Yes3 sarmentorum Westend. Continental US (Farr and PR) Rossman, 2012) and Rossman, 2012) Leptosphaeria doliolum Lind, 1913 DK (Lind, 1913); Yes (HI Leaves, stems Yes3 (Pers.) Ces. & De Not. Continental US (Farr and PR) (Farr and and Rossman, 2012) Rossman, 2012); dead stems (Lind, 1913) Macrophomina Farr and Rossman, DK (Chakraborty et No N/A N/A phaseolina (Tassi) 2012 al., 2011),US (Farr Goid. and Rossman, 2012) Myrothecium roridum Danish Plant DK (Danish Plant No N/A N/A Tode : Fr. Directorate, 2011 Directorate, 2011; Farr and Rossman, 2012; Richardson, 1990); US (Farr and Rossman, 2012) Phytophthora cryptogea Thinggaard, 1995 DK(CABI, 2012; Yes (HI Roots Yes3 Pethybridge & Lafferty Richardson, 1990), and PR) (Thinggaard, Continental US (Farr 1995) and Rossman, 2012 Phytophthora sp. Danish Plant DK(Danish Plant Undeter- N/A N/A Directorate, 2011 Directorate, 2011) mined

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Pest name Host status Distribution Quaran- Plant part Follow tine pest association Pathway Pleospora herbarum Farr and Rossman, DK (Lind, 1913); Yes (PR) Leaves (Farr and Yes3 (Pers. : Fr.) Rabenh.; 2012; Lind, 1913 Continental US, HI Rossman, 2012) Anamorph: (Farr and Rossman, Stemphylium herbarum 2012) E.G. Simmons Pleospora tarda E.G. Humphreys-Jones DK (Hernandez- No N/A N/A Simmons Anamorph: and Gibbons, 1971 Perez and du Toit, Stemphylium 2006); US (Farr and botryosum Wallr.; = Rossman, 2012) Macrosporium commune Rabenh. Pythium sp. Danish Plant DK (Danish Plant Undeter- N/A N/A Directorate, 2011 Directorate, 2011) mined Ramularia macrospora Lind, 1913; Farr DK (Lind, 1913); Yes (HI Leaves (Jelitto Yes3 Fresen. and Rossman, Continental US (Farr and PR) and Schacht, 2012 and Rossman, 2012) 1990) Rhizoctonia solani Kühn Farr and Rossman, DK; US (Farr and No N/A N/A 2012 Rossman, 2012) Sclerotinia sclerotiorum CABI, 2012; DK (CABI, 2012); No N/A N/A (Lib.) deBary Garibaldi et al., US (Farr and 2002; Wick and Rossman, 2012); Dicklow, 1999 (CABI, 2012) Synchytrium aureum J. Farr and Rossman, DK, US (CA, NY, Yes (HI Leaves (Farr and Yes3 Schröt. 2012 MA, PA. TX, WA. and PR) Rossman, 2012) WI, WY) (Farr and Rossman, 2012) Synchytrium globosum Farr and Rossman, DK (Farr and Yes (HI Leaves (Farr and Yes3 J. Schröt. 2012 Rossman, 2012; and PR) Rossman, 2012) Karling, nd); Continental US (Farr and Rossman, 2012); VIRUSES & VIROIDS Apple mosaic ilarvirus Sokmen et al., DK, US (CABI, No N/A N/A (ApMV) 2005; Sokmen et 2012) al., 2008 Cucumber mosaic virus Wick and DK (Noordam et al., No N/A N/A (CMV) Dicklow, 1999; 1965); US (CABI, Noordam et al., 2012) 1965 PARASITIC PLANTS Orobanche minor Sm. Murphy, 1972 in DK, limited Yes, Roots No4 CABI, 2012 distribution (CABI, Federal 2012) Noxious Weed

4 We did not further analyze this parasitic plant because it is highly unlikely to be present in greenhouse production.

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2.4.2. Pest List Discussion Non-specific pest identification. The biological hazard of organisms identified only to the genus level is not directly assessed in this document. International Standard for Phytosanitary Measures No. 11 states that “[t]he identity of the pest should be clearly defined to ensure that the assessment is being performed on a distinct organism, and that biological and other information used in the assessment is relevant to the organism in question” (IPPC, 2009). Risk assessments generally consider organisms defined to the species level only, unless a genus containing potential pests is not present in the importing country. Three fungi fit this category (genus present in the importing country) and were not further analyzed: Botrytis sp., Pythium sp. and Phytophthora sp. (Table 2).

Non-pests. We judged the following organisms to be no threat based on available information.

The fly, Chromatomyia horticola (Goureau), is a leafminer that can feed on Campanula (Pitkin et al., 2012), but is not actually a pest (Spencer, 1973).

The moths, Cnephasia asseclana (Denis & Schiffermüller) and C. incertana (Treitschke), have been recorded feeding on Campanula, but are rarely encountered (Pitkin et al., 2012).

The aphid, Dysaphis sorbi, rarely feeds on Campanula spp., and is not a pest (Heie, 1992).

Doubtful host associations or distributions. Pest interceptions may be evidence that a pest is present in a particular country, but a few interceptions over the course of 20 years, especially if only in passenger baggage, are insufficient evidence that a pest is present in a country or attacks a commodity. Passengers may transit several countries before arriving in the United States, and inspectors or identifiers may make errors while processing large volumes of passengers or shipments. Likewise, commodities carried may not be commercial quality produce.

Aphelenchoides ritzemabosi (Schwartz) Steiner & Buhrer is a pest of Campanula but is no longer in Denmark (CABI, 2012), so we did not include it on the pest list.

Phytophthora porri is a quarantine pest of the United States (PestID, 2012). A single isolate is reported on Allium porrum from Denmark (MycoBank, 2012), and P. porri is reported only once on Campanula in the United Kingdom (Legge, 1951). Although infection by the Campanula P. porri strain resulted in reduced plant quality and death of Campanula, it failed to infect leek; likewise isolates from leek failed to infect Campanula (Legge, 1951). The single isolate reported in Denmark is unlikely to infect Campanula and therefore we did not list this pathogen.

Plum pox virus was detected five times on Prunus nursery stock between 2008 to 2011 in Denmark; eradication was pursued in each case and the nurseries placed under quarantine (IPPC, 2011b; Poulsen, 2012). We also found only one reference of over 30 years ago to Campanula as a natural host of plum pox virus (Kroll, 1973). Accordingly, we did not list this pest.

Leptosphaeria plemeliana, Pyrenopeziza radians, and Ramularia campanulae-latifolia were each only reported once from Denmark, a long time ago (Lind, 1913). Without further

Ver. 1 (Orig.) July 30, 2012 9 Pest Risk Assessment for Campanula spp. from Denmark detections, we consider that insufficient evidence for its presence in the exporting country. Therefore we did not list these fungi in the pest list above.

Unlikely to survive in tropical areas. The Plant Hardiness Zones listed for commercial species and cultivars of Campanula primarily range between 3-9, but a few cultivars are rated for use in zones to 10 (Page and Olds, 2001). Commercial Campanula spp. are primarily temperate species and are unlikely to survive, or become establish in tropical environments. Several pathogens of Campanula are not present in Hawaii, Puerto Rico, or other tropical locations in the United States (Table 2). However, no native species of Campanula were identified for Hawaii, Puerto Rico, the U.S. Virgin Islands or Guam ((USDA ARS, 2012)). The plant hardiness zones for Hawaii are primarily 11-13, with areas of zones 9-10 on the largest island (Magarey et al., 2008a). The Plant Hardiness Zone for Puerto Rico, Guam and the U.S. Virgin islands is 13, with a small area of zone 12 in Puerto Rico (Magarey et al., 2008a). These places are therefore inhospitable to most Campanula. The florist industry does currently ship Campanula for indoor use to Hawaii, but it is unlikely, as for cut flowers, that these plants would provide a pathway leading to the establish or spread of any of these pathogens.Therefore we listed the following pathogens above (Table 2), but did not further analyze them in this risk assessment for the reasons just stated: Coleosporium tussilaginis, Cyathus olla, Erysiphe pisi var. pisi, Fusarium graminearum, Hendersonia sarmentorum, Leptosphaeria doliolum, Phytophthora cryptogea, Pleospora herbarum, Ramularia macrospora, Rhodococcus fascians, Synchytrium aureum, and S. globosum.

2.4.3. Quarantine pests that are likely to follow the pathway In this risk assessment we identify and characterize the main sources of uncertainty. These include the use of a developing or evolving process (Orr et al., 1993), the approach used to combine risk elements (Bier, 1999; Morgan and Henrion, 1990), and the evaluation of risk by comparisons to lists of factors within the guidelines (Kaplan, 1991; Orr et al., 1993). Sources of uncertainty in this analysis stem from the quality of the biological information, which includes increased uncertainty whenever biological information is lacking on the regional flora and fauna (Gallegos and Bonano, 1993) and the inherent biological variation within a population of organisms (Morgan and Henrion, 1990). To address this uncertainty, we only analyzed the quarantine pests that can reasonably be expected to follow the pathway, i.e., be included in commercial shipments of Campanula plants (Table 3).

Table 3. Pests considered for further evaluation. Type Pest Insects Diptera: Liriomyza buhri Agromyzidae Liriomyza strigata Phytomyza campanulae Hemiptera: Aleyrodidae Aleyrodes lonicerae Hemiptera: Aphididae Aphis psammophila Uroleucon campanulae Uroleucon nigrocampanulae Uroleucon rapunculoidis

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Type Taxonomy Pest Thysanoptera: Thripidae Thrips major Mollusk Helicidae Arianta arbustorum

2.5. Consequences of Introduction

The undesirable consequences that may occur from the introduction of quarantine pests are assessed in this section. For each quarantine pest, the potential consequences of introduction are rated using five Risk Elements. These elements (Climate-Host Interaction, Host Range, Dispersal Potential, Economic Impact, and Environmental Impact) reflect the biology, host range, and climatic/geographic distribution of each pest and are supported by published biological information. For each element, pests are assigned a rating of Low (1 point), Medium (2 points) or High (3 points). Cumulative risk values are then calculated by adding the ratings. The following scale is used to interpret this total: Low (5-8 points), Medium (9-12 points), and High (13-15 points) and are summarized in Table 4. The ratings were determined using the criteria in the Guidelines for Pathway-Initiated Risk Assessments, Version 5.02 (PPQ, 2000).

2.5.1. Aleyrodes lonicerae Climate-Host Interaction. Aleyrodes lonicerae is present throughout Europe (Nieto Nafría et al., 2011) and parts of the Middle East (Mound and Halsey, 1978) through Plant Hardiness Zones 6-10 (Magarey et al., 2008b). Thus, we rated Climate-Host Interaction High for this species.

Host Range. Aleyrodes lonicerae has a broad host range across many families (Mound and Halsey, 1978), so we rated it High for the Host Range element.

Dispersal Potential. Aleyrodes lonicerae has multiple generations per year (Alford, 1991). Although whiteflies are often characterized as weak fliers, Bemisia tabaci was capable of dispersing considerable distances (Byrne, (1999). We rated the pest Medium.

Economic Impact. Aleyrodes lonicerae is an occasional and local pest that rarely requires control measures (Hill, 1987) so we rated it Low for economic impact.

Environmental Impact. No known hosts of Aleyrodes lonicerae (Mound and Halsey, 1978) are listed as threatened or endangered (USFW, 2012), but some genera fed on by A. lonicerae contain threatened or endangered species. These species are Campanula robinsiae, Cardamine micranthera, Euphorbia haeleeleana, E. telephioides, Geum radiatum, Hypericum cumulicola, Ribes echinellum, Spiraea virginiana, Thalictrum cooleyi, Viola chamissoniana, V. helenae, V. kauaiensis var. wahiawaensis, V. lanaiensis, and V. oahuensis. We rated this pest Medium for environmental impact.

2.5.2. Aphis psammophila Climate-Host Interaction. Aphis psammophila is present in Europe (Nieto Nafría et al., 2011) through Plant Hardiness Zones 6-8 (Magarey et al., 2008b), so we rated Climate-Host Interaction for this species as Medium.

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Host Range. Aphis psammophila is known to feed exclusively in the family Campanulaceae (Osiadacz and Hałaj, 2011). We rated this pest Low for the Host Range element.

Dispersal Potential. Aphids can disperse long distances in wind currents (Schmidt et al., 2012). A related species, Aphis fabae, had an average fecundity of 80 larvae per aphid (Cockbain, 1961). We rated this pest High for the Dispersal Potential element.

Economic Impact. We found no evidence that this species causes economic damage to Campanula spp., and Heie (1986 ) states that the species does not alter hosts. We rated this pest Low for this element.

Environmental Impact. One species of Campanula, Campanula robinsiae, is listed as endangered in (USFW, 2012), but since the aphid has little or no effect on its hosts, we expect no significant damage. We rated Environmental Impact Low for this pest.

2.5.3. Arianta arbustorum Climate-Host Interaction. This snail is distributed throughout Western Europe as far north as Norway and south to Austria and the Czech Republic Host Range (Field Museum, 2012). These areas correspond to Global Plant Hardiness Zones 6-8 (Magarey et al., 2008b). We rated this pest Medium for the Climate-Host Interaction element.

Host Range. Arianta arbustorum is an omnivorous feeder with a tendency to feed on fast- growing ephemerals and perennials (Hägele and Rahier, 2001). We rated this pest High for the Host Range element.

Dispersal Potential. Snails can produce between 5-200 young in a lifetime, depending upon the altitude, and the young may reach maturity in 1-9 years (Baur and Raboud, 1988). In a three- month study, snails moved an average of 1.5-4.9 meters and it was found that paved roads were a significant barrier to movement (Baur and Baur, 1990). We rated this pest Low for the Dispersal Potential element.

Economic Impact. In large numbers this species can cause economic damage to nurseries and home gardens (Lindqvist et al., 2010). Although widely studied, this snail does not seem to be generally regarded as an important pest. We rated this pest Medium for the Economic Impact element.

Environmental Impact. Arianta arbustorum is omnivorous, including soil and detritus feeding, and surface feeding on non-living substrates (Hägele and Rahier, 2001). It may chance to feed on some threatened or endangered species, but only as part of its varied diet. As such, the snail is unlikely to cause enough damage to any species to cause harm. We rated this pest Low for the Environmental Impact element.

2.5.4. Liriomyza buhri, L. strigata, and Phytomyza campanulae Climate-Host Interaction. We found little information about the leafminers P. campanulae and L. buhri, so we used an analysis of L. strigata for all three leafminers. The complete geographic distribution of L. strigata is unknown. It is found in the Palaearctic region, throughout Western

Ver. 1 (Orig.) July 30, 2012 12 Pest Risk Assessment for Campanula spp. from Denmark

Europe, but the eastern limit of its range is unknown (Spencer, 1973). Based on its known distribution, it could survive in four or more Plant Hardiness Zones of the United States (Magarey et al., 2008b). One or more of its potential hosts occurs in these zones (NRCS, 2012). We rated these pests High for the Climate-Host interaction element.

Host Range. Liriomyza strigata is a highly polyphagous species that feeds on over 180 genera in 31 different families. Main vegetable crops attacked include Beta vulgaris (Chenopodiaceae), Lactuca spp. (Compositae), and Pisum sativum L. (Fabaceae) (Spencer, 1973). We rated these pests High for the Host Range element.

Dispersal Potential. Species of Liriomyza have a relatively high biotic potential. Lifetime fecundity varies greatly by species, ranging between 100 and about 600 eggs per female (Parrella, 1987).

In general, leaf miners have minimal natural dispersal potential. Larvae remain inside the leaf onto which they hatched until they pupate (CABI, 2012). Adults do not disperse long distances on their own (Ozawa et al., 1999). They can be transported through wind currents, but because windborne transfer requires that suitable plant hosts be available at the destination during the relatively short lifespan of the fly, this is probably not a common method of dispersal (CABI, 2012). Movement of economic crop hosts, if containing early stages of the pest, may effectively transfer the species to new areas. However, despite having a large host range, including many crops, this species has a relatively restricted global distribution. We rated these pests Medium for the Dispersal Potential element.

Economic Impact. Large populations of L. strigata are rarely found in a single plant (Spencer, (1973). Therefore, larval damage to mature plants is generally negligible, and young plants are not normally attacked. Chemical control programs are unlikely to be initiated against this pest, since those already in place for the control of other species of Liriomyza are likely to be equally effective against it. Therefore, the presence of this species is unlikely to significantly increase production costs. Introduction of the pest could cause the loss of regional and domestic markets since it is apparently not present in the Western Hemisphere, Africa, Asia, or the Pacific (CABI, 2012). We rated these pests Medium for the Economic Impact element.

Environmental Impact. Liriomyza strigata is highly polyphagous (Spencer, 1973) and could feed on plants listed as Threatened or Endangered (e.g., Campanula robinsiae, endangered in FL; Helianthus paradoxus, threatened in TX and NM; H. schweinitzii, endangered in NC and SC) (USFW, 2012). However, damage is unlikely to be more severe than that produced by native leafminers, nor is it likely to affect plant reproduction potential. Chemical control programs are unlikely to be initiated against this pest, since those already in place for the control of other pestiferous leaf miners, such as Liriomyza sativae Blanchard or L. trifolii (Burgess), are likely to be equally effective against L. strigata. However, this pest could be the target of biological control programs, as has occurred with other introduced Agromyzidae [e.g., Hawaii; (Culliney and Nagamine, 2000)]. We rated these pests Medium for the Environmental Impact element.

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2.5.5. Thrips major Climate-Host Interaction. Thrips major is found in Denmark (PestID, 2012), Iran (Alavi et al., 2007), Algeria, France, Corsica (Bornier, 1963), and England (Buxton and Easterbrook, 1988). These areas correspond to Global Plant Hardiness Zones 7-9 in the United States (Magarey et al., 2008b). We rated this pest Medium for the Climate-Host Interaction element.

Host Range. Thrips major is a polyphagous insect (Bornier, 1963). Hosts include Poaceae (Alavi et al., 2007), Citrus, Callnna, Achillea, Salix, Thalictrum, Lythrum, Buxinius, (Bornier, 1963), and Fragaria (Buxton and Easterbrook, 1988). We rated this pest High for the Host Range element.

Dispersal Potential. Thrips species are weak fliers, but their small size allows them to be carried long distances by wind currents (Lewis, 1997). Female thrips lay three to four eggs per day. Multiple generations are produced each year (Bornier, 1963). We rated this pest Medium for the Dispersal Potential element.

Economic Impact. Thrips major is a significant pest of nectarines in Italy, causing russeting on the fruit surface because of feeding at bloom (Tommasini et al., 2004). It causes cosmetic damage to citrus in North Africa (1963), and disfigures strawberries in England (Buxton and Easterbrook, 1988). However, flower thrips of other species like western flower thrips are commonly managed in the United States and we found no evidence that the addition of T. major would change management practices or costs. We rated this pest Medium for the Economic Impact element.

Environmental Impact. One species of Campanula, C. robinsiae, is listed as endangered in Florida (USFW, 2012). Environmental Impact is rated Medium for this pest.

2.5.6. Uroleucon campanulae, U. nigrocampanulae, and U. rapunculoidis Climate-Host Interaction. Uroleucon campanulae, U. nigrocampanulae, and U. rapunculoidis (Börner) are present in Europe (Nieto Nafría et al., 2011) through Plant Hardiness Zones 6-8 (Magarey et al., 2008b). Thus, we rated Climate-Host interaction for these species Medium.

Host Range. Uroleucon campanulae, U. nigrocampanulae, and U. rapunculoidis are known to feed exclusively in the family Campanulaceae (Osiadacz and Hałaj, 2011). We rated these pests Low for the Host Range element.

Dispersal Potential. Aphids can disperse long distances in wind currents (Schmidt et al., 2012). A related species, Uroleucon nigrotibiumo, had an average fecundity of 41 on its favored host plant (Moran, 1984). We rated these pests High for the Dispersal Potential element.

Economic Impact. We found no information about the economic impact of these species on Campanula spp. We rated these pests Low for this element.

Environmental Impact. One species of Campanula, C. robinsiae, is listed as endangered in Florida (USFW, 2012) but we found no information regarding the economic impact of Uroleucon spp. on their hosts, so Environmental Impact is rated Low for these pests.

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Table 4. Summary of the risk ratings and the cumulative Consequences of Introduction rating. Pest Climate- Host Dispersal Economic Environ- Cumulative Host Range Potential Impact mental risk rating Interaction impact (score) Aleyrodes lonicerae High (3) High (3) Med (2) Low (1) Med (2) Medium (11) Aphis psammophila Med (2) Low (1) High (3) Low (1) Low (1) Low (8) Arianta arbustorum Med (2) High (3) Low (1) Med (2) Low (1) Medium (9) Liriomyza strigata, L. High (3) High (3) Med (2) Med (2) Med (2) Medium (12) buhri, & Phytomyza campanulae Thrips major Med (2) High (3) Med (2) Med (2) Med (2) Medium (11) Uroleucon Med (2) Low (1) High (3) Low (1) Low (1) Low (8) campanulae, U. nigrocampanulae, & U. rapunculoidis a Low = 5-8 points, Medium = 9-12, and High = 13-15.

2.6. Likelihood of Introduction

The likelihood of introduction for a pest is rated relative to six factors, which include the quantity imported annually (PPQ, 2000). As per the Guidelines for Pathway-Initiated Risk Assessments, Version 5.02 (PPQ, 2000), the value for the Likelihood of Introduction is the sum of all the ratings, which we summarized in (Table 5).

2.6.1. Quantity imported annually We base this rating on the amount proposed by the country for export, converted into standard units of 40-foot-long shipping containers. Denmark’s NPPO anticipated that 450,000 plants valued at 1 million Euros would be shipped.. Denmark’s NPPO also noted that permission to import into the United States is likely to be linked with an increase in production in the future and subsequent increases in the volumes of imports. We do not expect more than 10 containers per year so all pests are rated Low for this element.

2.6.2. Availability of post-harvest treatments For this risk assessment we assume no treatments at the time of shipment so all pests were rated High for this element.

2.6.3. Survive shipment The plants are likely to be shipped at moderate temperatures and humidity, which are unlikely to adversely affect pest populations present on the shipments. Those conditions will not inhibit the growth of any of the quarantine pests. Therefore, we rated this element High for all pests.

2.6.4. Not detected at the port-of-entry Leafminer damage is quite apparent on leaves (Spencer, 1973) and would be fairly easy to detect. We therefore rated this element Low for Lyriomyza buhri, L. strigata and Phytomyza campanulae.

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The aphids, Aphis psammophila, Uroleucon campanulae, U. nigrocampanulae, and U. rapunculoidi, are small insects that may be difficult to find by inspectors, so we rated them High. A related pest to Aleyrodes lonicerae, A. proletella, is reported to carry a conspicuous white waxy layer (Hill, 1987), so this insect is rated Medium for this element.

Thrips major are very small, but are generally only found on flowers, which would render inspection easier. Non-flowering Campanula plants would not be at risk from T. major. We rated T. major Medium for this risk element.

Arianta arbustorum would produce obvious damage to leaves and flowers and would itself be highly visible. We rated this snail Low for this element.

2.6.5. Moved to a suitable habitat Liriomyza strigata, Aphis psammophila, Uroleucon campanulae, U. nigrocampanulae, and U. rapunculo, Thrips major, and Arianta arbustorum would likely be able to survive in Global Plant Hardiness Zones 6-8, an area covering a large portion of the continental United States (Magarey et al., 2008b) and are therefore rated High for this element. The current range of the other leafminers, Liriomyza buhri and Phytomyza campanulae, is narrower than that of L. strigata, but we analyzed the leafminers as a group, so they took the higher rating. Aleyrodes lonicerae can survive in plant hardiness zones 6-10, so is also rated High for this element.

2.6.6. Contact with Host Material All of the pests examined are likely to come into contact with host material if they enter the United States because infested Campanula plants are likely to be grown near other Campanula plants or near other hosts in outdoor settings. Additionally, close proximity in these environments is likely to facilitate dissemination of insects and insect vectors to other Campanula plants (Agrios, 1997; Pirone, 1978). We rated all pests High for this element.

Table 5. Summary of the Risk Ratings for the Likelihood of Introduction. Pest Quantity Survive Survive Not detected Moved Find Cumulative imported post- shipment at port-of- to a suitable risk ratingb annually harvest entry suitable hosts treatment habitat Aleyrodes lonicerae Low (1) High (3) High (3) Medium (2) High (3) High (3) High (15) Aphis psammophila Low (1) High (3) High (3) High (3) High (3) High (3) High (16) Arianta arbustorum Low (1) High (3) High (3) Low (1) High (3) High (3) Medium (14) Liriomyza buhri, L. Low (1) High (3) High (3) Low (1) High (3) High (3) Medium (14) strigata, & Phytomyza campanulae Thrips major Low (1) High (3) High (3) Med (2) High (3) High (3) High (15) Uroleucon campanulae, U. Low (1) High (3) High (3) High (3) High (3) High (3) High (16) nigrocampanulae, & U. rapunculoidis b Low = 6-9 points, Medium = 10-14 points, and High = 15-18 points.

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2.7. Pest Risk Potential and Conclusion

We analyzed the insects Aleyrodes lonicerae, Aphis psammophila, Liriomyza buhri, L. strigata, Phytomyza campanulae, Uroleucon campanulae, U. nigrocampanulae, U. rapunculoidis and Thrips major, and the snail Arianta arbustorum. The overall pest risk potential was Medium for all the pests analyzed. The overall pest risk potentials for the pests analyzed are listed below (Table 6). Specific phytosanitary measures may be necessary for pests with a Medium rating. Risk management measures are considered elsewhere, as part of the risk management phase.

Table 6. Pest Risk Potentials for quarantine pests of Campanula spp. from Denmark. Pest Consequences Likelihood of Pest risk potentiala of Introduction Introduction Aleyrodes lonicerae Medium (11) High (15) Medium (26) Aphis psammophila Low (8) High (16) Medium (24) Arianta arbustorum Medium (9) Medium (14) Medium (23) Liriomyza buhri, L. Medium (12) Medium (14) Medium (26) strigata, & Phytomyza campanulae Thrips major Medium (11) High (15) Medium (26) Uroleucon campanulae, Low (8) High (16) Medium (24) U. nigrocampanulae, & U. rapunculoidis a Low = 11-18 points, Medium = 19-26 points, and High 27-33 points.

3. Acknowledgements

Authors Shawn P. Robertson, Entomologist/Risk/Analyst, CPHST, PERAL (primary contact) Betsy Randall-Schadel, Plant Pathologist/Risk Analyst, CPHST, PERAL

Reviewers Cynthia Landry, Biologist/Risk Analyst, CPHST, PERAL Walter A Gutierrez, Plant Pathologist/Risk Analyst, CPHST, PERAL Ashley M. Jackson, Editorial Assistant, CPHST, PERAL

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