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<title>Importation of Fresh Tomato Fruit with Stems</title>
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<p><b>United States Department of Agriculture</b></p>
<p><b>Animal and Plant Health Inspection Service</b></p>
<p><b>Plant Protection and Quarantine</b></p>
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<p><b>Importation of Fresh Strawberry, <i>Fragaria</i> spp., Fruit with Flower Calyx and Short Stalk from Jordan into the Continental United States</b></p>
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<p><b>Risk Management Document</b></p>
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<p><b>May 24, 2010</b></p>
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<p><b>Plant Health Programs (PHP)</b></p>
<p><b>Regulations, Permits and Manuals (RPM)</b></p>
<p><b>Contact Person: Donna L. West</b></p>
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<p><b>Introduction</b></p>
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<p>The U.S. Department of Agriculture (USDA), Animal and Plant Health Inspection Service (APHIS) conducted a pest risk assessment in response to a request by Jordan’s Ministry of Agriculture, also referred to as Jordan’s National Plant Protection Organization (NPPO), to allow imports of fresh, field-grown strawberry (<i>Fragaria </i>spp.) fruit with calyces and short stalks from Jordan into the continental United States (PERAL, 2010).  Six pests of quarantine significance were identified as likely to be introduced into the continental United States via the fresh strawberry fruit.  This document evaluates and describes the appropriate pest risk management measures for these quarantine pests.</p>
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<p>The movement of fruits and vegetables from foreign countries into the United States is regulated in the U.S. Code of Federal Regulations (7 CFR § 319.56, 2010).  Currently, the entry of fresh strawberry fruit from Jordan is not authorized under these regulations.</p>
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<p>The pest risk assessment (PERAL, 2010) estimated the risk associated with the unmitigated importation of fresh strawberry fruit from Jordan and identified the following six quarantine pests of concern for strawberry fruit from Jordan:</p>
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<p><i>Cacoecimorpha pronubana</i> Hübner (Lepidoptera: Tortricidae)</p>
<p><i>Chrysodeixis chalcites</i> (Esper) (Lepidoptera: Noctuidae)</p>
<p><i>Eutetranychus orientalis</i> (Klein) (Acari: Tetranychidae)</p>
<p><i>Monilinia fructigena</i> Honey (Leotiomycetes: Helotiales)</p>
<p><i>Spodoptera littoralis</i> (Boisduval) (Lepidoptera: Noctuidae)</p>
<p><i>Thrips major</i> Uzel (Thysanoptera: Thripidae)</p>
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<p>All pests were identified as having a <b>High</b> risk potential.</p>
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<p>The volume of strawberries to be shipped from Jordan to the United States is estimated to be just under 30, 40-foot long maritime containers per year (PERAL, 2009), and shipment to the United States would be during the months of December through May (Matalka, 2004).</p>
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<p>Jordan intends to export the strawberry fruit with flower calyces and short stalks (Matalka, 2004).  Leaving the calyx on the fruit helps decrease perishability (PERAL, 2010).  </p>
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<p><b>Standard industry practices</b></p>
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<p>In Jordan, strawberries are produced in 500 m2 (0.124 acre) plastic tunnels and are under irrigation using drip irrigation (Abu-El Samen Hiasat, 2008).  There are no open field plantations, but multi-span plastic tunnels are used on a few farms (Abu-El Samen Hiasat, 2008).  </p>
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<p>In Jordan, integrated pest management (IPM) practices are used in strawberry production in collaboration with GTZ (German Agency for Technical Cooperation)-Germany IPM projects, which entail mainly the use of predators and parasites of insect pests and restricted pesticide applications (Abu-El Samen Hiasat, 2008).  Other pest management measures implemented in Jordan for export strawberries include exclusionary screening, crop scouting and trapping, and good ventilation (Matalka, 2004).</p>
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<p>The strawberry fruit for export to the continental United States would undergo the following harvest and post-harvest practices, as described by Abu-El Samen Hiasat (2008):</p>
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<p>· At harvest, the fruit are collected in “field boxes” and undergo an initial grading in the field. </p>
<p>· Within one hour, the fruit are transported by refrigerated trucks to warehouses.</p>
<p>· At the warehouse in the quality control room, the fruit are graded, and unwanted fruit are removed.  </p>
<p>· The fruit are then placed in “exportation boxes” of different sizes depending on the destination requirements, but generally in containers of 250-400 g holding one layer of fruit.</p>
<p>· The boxes are placed into perforated cardboard cases and then stored in the pre-cooling room (0oC) for 30-60 minutes. </p>
<p>· The boxes are then moved to cold rooms (0-5 oC), where they are stored for 24-48 hours.</p>
<p>· The fruit are then transported in refrigerated trucks to the airport and are air shipped to their destination.  The fruit would be shipped from Jordan to the United States on 12-14 hour, non-stop flights.</p>
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<p><b>Risk Management Measures</b></p>
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<p>APHIS proposes that fresh strawberry fruit grown in Jordan may be imported into the continental United States only under the following conditions:      </p>
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<p>A) Each consignment of strawberry fruit must be accompanied by a Phytosanitary Certificate (PC) issued by Jordan’s NPPO bearing the following Additional Declaration (AD): “The strawberry fruit in this consignment were grown in Jordan and were inspected and found free of the quarantine pests.”</p>
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<p>B) Strawberry fruit must be imported as commercial consignments only.</p>
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<p>C) Port of entry inspection.</p>
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<p><b>Rationale for Risk Management Measures</b></p>
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<p>According to the USDA guidelines for pathway initiated pest risk assessments (USDA, 2000), specific phytosanitary measures, supplemental to port-of-entry inspection, are strongly recommended for pests given a ‘High’ pest risk potential.</p>
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<p>According to PPQ regulations and import decision history documents (APHIS, 2009; PERAL, 2010), PPQ has long permitted the entry of strawberry fruit for consumption from many countries (e.g., Israel, Turkey, Spain, France, Austria, etc.) where the above pests of concern occur (Bolland et al., 1998; CABI, 2007; CABI/EPPO, 1997; Fauna Europaea Web Service, 2009; Zhang, 1994), as early as the 1940’s or 50’s for some countries.  Despite this import history, the quarantine pests of concern have never been intercepted at U.S. ports-of-entry in commercial strawberry fruit (PestID, 2009).  The lack of interception suggests that, in general, commercial strawberry fruit for export are unlikely to contain the identified quarantine pests.  </p>
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<p>The quarantine pests (PERAL, 2010) occur primarily externally on their hosts and the presence or symptoms can be readily detected with visual inspection.  </p>
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<p>The larvae of the tortricid insect <i>Cacoecimorpha pronubana</i> grow up to 19 or 20 mm in length (CABI, 2007; Hill, 1987).  The eggs, larvae, and pupae occur externally on leaves, where they are visible to the naked eye (CABI, 2007). The larvae feed externally on their hosts, mainly on the leaves and flowers, making numerous holes, rolling leaves, and forming a dense silken mass around the attacked plant parts (CABI, 2007; Hill, 1983, 1987; Meijerman & Ulenberg, 2000; Van Der Geest & Evenhuis, 1991).  On strawberries, the larvae may attack the fruit beneath the shelter of the calyx (Meijerman & Ulenberg, 2000); therefore, inspection for this insect should include inspection beneath the calyx, looking for larvae, feeding damage, webbing and frass. </p>
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<p>The larvae of the noctuid insect <i>Chrysodeixis chalcites </i>can grow up to 34 to 38 mm in length, and the pupae are 20 mm long (CABI, 2007).  The eggs, larvae, and pupae occur externally on fruit and leaves of their hosts and are visible to the naked eye (CABI, 2007); symptoms of larval feeding include leaf rolling, defoliation, skeletonized leaves, webbing, and frass (CABI, 2007; Hill, 1983).  At the prepupal stage, the larva makes a cocoon in which it pupates (CABI, 2007), which should be easy to detect during inspection.  </p>
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<p>The larvae of the noctuid, <i>Spodoptera littoralis</i> grow up to 40 to 50 mm in length (CABI, 2007; PPQ, 2002).  Pupation occurs in the soil (CABI, 2007), so they would not be associated with fruit and associated calyxes.  The larvae mainly feed externally on the leaves of its hosts, creating obvious symptoms (large holes of irregular shape, leaf shredding, skeletonization, and frass) (Avidov & Harpaz, 1969; CABI, 2007; PPQ, 2002).  The larvae may bore into the fruit of some hosts, but this feeding behavior makes the fruit unmarketable (Avidov & Harpaz, 1969; CABI, 2007).  </p>
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<p>Although <i>Thrips major</i> can attack fruit, it mainly attacks flowers (Buxton & Easterbrook, 1988; Dyadechko, 1977; Easterbrook, 1991, 2000; Hill, 1987; Lewis, 1997); this feeding behavior decreases the likelihood of <i>T. major</i> being in the pathway of commercial fruit.  Indeed, agricultural inspectors have never intercepted this thrips species with any commercial fruit at U.S. ports-of-entry (PestID, 2009).  When it does attack fruit, it causes bronzing of the skin of the fruit (Easterbrook, 2000).  Symptoms associated with thrips on strawberry fruit include bronzing and distortion of the fruit  (Steiner & Goodwin, 2005), which can be detected during fruit inspection.   </p>
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<p><i>Eutetranychus orientalis</i> is primarily a leaf feeder (Avidov & Harpaz, 1969; CABI, 2007; Hill, 1987; PPQ, 2002).  It also attacks fruit if infestations levels are high (Avidov & Harpaz, 1969).  On both leaves and fruit, damage by this mite results in obvious symptoms: chlorotic appearance on leaves and fruit, pale yellow streaks, lesions, abnormal colors, webbing, honeydew, and sooty mold (Avidov & Harpaz, 1969; CABI, 2007; Hill, 1987; PPQ, 2002; van den Berg <i>et al.</i>, 2001).  </p>
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<p>Infection by <i>Monilinia fructigena</i> can be easily observed, as this fungus produces visible rots on the fruits of its hosts.  On ripe fruit, the first symptoms are small, superficial, circular brown spots that rapidly turn to rotting, and the entire fruit eventually turns brown and decays (CABI, 2007; Ioos et al., 2009).  Often the sprouting tufts of mycelium and conidia are arranged in concentric rings on the fruit surface (Ioos et al., 2009).  Green fruit may have latent infections of the disease, but these often become active just before or after harvest (Ioos et al., 2009), therefore, would likely be detected during post-harvest processing and inspection and/or during port-of-entry inspection.  If infection is not apparent at port-of-entry, the fact that the fruit is for consumption (not propagation) makes it highly unlikely that the pathogen would be spread to natural hosts.  </p>
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<p>Additionally, good agricultural practices can effectively suppress or eliminate pests from fields or prevent infestation. Successful control programs typically include monitoring, cultural, biological, and chemical components.  As described above, all these components are used as part of Jordan’s IPM practices for the production of export strawberries.   </p>
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<p>Based on the above evidence and lack of interceptions of pests of concern (PestID, 2009) as well as their obvious symptoms, the appropriate level of phytosanitary security will be attained by requiring a Phytosanitary Certificate issued by Jordan’s NPPO with an Additional Declaration stating that the consignment has been inspected and found free of quarantine pests.</p>
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<p><b>Summary</b></p>
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<p class="normal_(Web)">The pest risk assessment for strawberry fruit with calyces and short stalks from Jordan only addressed the pest risk associated with the commodity being imported into the continental United States.  As such, importation and movement into areas outside the continental United States would be prohibited by permit conditions.  </p>
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<p>The requirement of a Phytosanitary Certificate from Jordan’s NPPO will document that the importation is a product of Jordan, and the Additional Declaration provides phytosanitary security by requiring Jordan’s NPPO to conduct inspections for the quarantine pests of concern.  These inspections double the number of inspections each strawberry consignment receives by requiring phytosanitary inspections in addition to the normal packing house quality inspections.  </p>
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<p>Importations of strawberries from Jordan will also be subject to inspection at the port-of-entry in the continental United States.  Depending on the interception levels of the pests of concern, a reevaluation of the risk management measures needed to attain the appropriate level of phytosanitary security may occur.   </p>
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<p><b>Authors</b></p>
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<p>Leah C. Millar, Entomologist/Risk Analyst, USDA, APHIS, PPQ, Center for Plant Health Science and Technology</p>
<p>José R. Hernández, Ph.D., Plant Pathologist/Risk Manager, USDA, APHIS, PPQ, Regulations, Permits & Manuals</p>
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<p><b>Reviewers</b></p>
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<p>Devaiah A. Muruvanda, Ph.D., Entomologist/Senior Risk Manager, USDA, APHIS, PPQ, Regulations, Permits & Manuals</p>
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<p>Donna L. West, Senior Import Specialist, USDA, APHIS, PPQ, Regulations, Permits & Manuals</p>
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<p>Brendon Reardon, Assistant Trade Director, USDA, APHIS, PPQ, Phytosanitary Issues Management</p>
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<p><b>References</b></p>
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<p>7 CFR § 319.56. 2010. U.S. Code of Federal Regulations, Title 7, Part 319 (7 CFR § 319.56 - Foreign Quarantine Notices), Subpart 56 (7 CFR § 319.56 - Fruits and Vegetables).</p>
<p>Abu-El Samen Hiasat, F. 2008. Strawberry production in Jordan and shipping conditions of strawberries from Jordan. Personal communication to O. P. Parfait on March 9, 2008, from F. Abu-El Samen Hiasat (Jordan University of Science and Technology).  Archived at the PERAL Library, Raleigh, NC.</p>
<p>APHIS. 2009. Fruits and Vegetables Import Requirements (FAVIR) Database. United States Department of Agriculture, Animal and Plant Health Inspection Service (APHIS). https://epermits.aphis.usda.gov/manual/index.cfm?ACTION=pubHome. (Archived at PERAL).</p>
<p>Avidov, Z., and I. Harpaz. 1969. Plant pests of Israel. Israel Universities Press, Jerusalem. 549 pp.</p>
<p>Bolland, H. R., J. Gutierrez, and C. H. W. Flechtmann. 1998. World catalogue of the spider mite family (Acari: Tetranychidae). Brill, Boston. 392 pp.</p>
<p>Buxton, J. H., and M. A. Easterbrook. 1988. Thrips as a probable cause of severe fruit distortion in late-season strawberries. Plant Pathology 37(2):278-280.</p>
<p>CABI. 2007. Crop Protection Compendium. Commonwealth Agricultural Bureau International (CABI), Wallingford, UK.</p>
<p>CABI/EPPO. 1997. Quarantine pests for Europe, second edition: data sheets on quarantine pests for the European Union and for the European and Mediterranean Plant Protection Organization. CAB International (CABI) and the European and Mediterranean Plant Protection Organization (EPPO), Oxon, UK. 1425 pp.</p>
<p>Dyadechko, N. P. 1977. Thrips or Fringe-Winged Insects (Thysanoptera) of the European Part of the USSR. Amerind Publishing Co., New Delhi, India. 344 pp.</p>
<p>Easterbrook, M. A. 1991. Species of thrips associated with flowers of late-flowering strawberries. Entomologist 110(1):5-10.</p>
<p>Easterbrook, M. A. 2000. Relationships between the occurrence of misshapen fruit on late-season strawberry in the United Kingdom and infestation by insects, particularly the European tarnished plant bug, <i>Lygus rugulipennis</i>. Entomologia Experimentalis et Applicata 96(1):59-67.</p>
<p>Fauna Europaea Web Service. 2009. Fauna Europaea version 2.0: Distribution of <i>Thrips major</i>. http://www.faunaeur.org/. (Archived at PERAL).</p>
<p>Hill, D. S. 1983. Agricultural insect pests of the tropics and their control. Cambridge University Press, New York, NY. xii+ 746 pp.</p>
<p>Hill, D. S. 1987. Agricultural insect pests of temperate regions and their control. Cambridge University Press, New York, NY. 659 pp.</p>
<p>Ioos, R., K. Hughes, A. Mackie, and M. Braithwaite. 2009. Plant Biosecurity Toolbox (PaDIL): Diagnostic Methods for Apple Brown Rot <i>Monilinia fructigena</i>. Cooperative Research Centre for National Plant Biosecurity (CRCNPB). Last accessed December 29, 2009, http://www.padil.gov.au/pbt/index.php?q=node/22&pbtID=79.</p>
<p>Katbeh-Bader, M. R. 2010. Response letter to USDA concerning the Jordan strawberry pest risk assessment. Personal communication to M. Bandla on February 24, 2010, from International Phytosanitary Expert, Head of Phytosanitary Division, Ministry of Agriculture, Ammam, Jordan.</p>
<p>Lewis, T. 1997. Thrips as crop pests. CAB International, New York, NY. 740 pp.</p>
<p>Matalka, M. S. 2004. Market access request for baby cucumber, white marrows, beans, strawberries, <i>Capsicum</i>, and sugar and snap peas from Jordan to the United States. Embassy of the Hashemite Kingdom of Jordan, Washington, D.C. 17 pp.</p>
<p>Meijerman, L., and S. A. Ulenberg. 2000. Arthropods of economic importance - Eurasian Tortricidae. ETI BioInformatics http://ip30.eti.uva.nl/BIS/tortricidae.php. (Archived at PERAL).</p>
<p>PERAL. 2010. Importation of Fresh Strawberry, <i>Fragaria</i> spp., Fruit with Flower Calyx and Short Stalk from Jordan into the Continental United States: A Pathway-Initiated Risk Assessment, Revision 03. United States Department of Agriculture, Animal and Plant Health Inspection Service, Plant Protection and Quarantine, Center for Plant Health Science and Technology, Plant Epidemiology and Risk Analysis Laboratory (PERAL), Raleigh, NC. 61 pp.</p>
<p>PestID. 2009. Pest Identification Database (PestID). United States Department of Agriculture, Animal and Plant Health Inspection Service, Plant Protection and Quarantine. https://mokcs14.aphis.usda.gov/aqas/login.jsp. (Archived at PERAL).</p>
<p>PPQ. 2002. Electronic Files for Arthropods from Pests Not Known to Occur in the United States or of Limited Distribution and Insects Not Known to Occur in the United States. United States Department of Agriculture, Animal and Plant Health Inspection Service, Plant Protection and Quarantine (PPQ), Policy and Program Development, Risk Analysis Systems. 941 pp.</p>
<p>Steiner, M. Y., and S. Goodwin. 2005. Management of thrips (Thysanoptera: Thripidae) in Australian strawberry crops: within-plant distribution characteristics and action thresholds. Australian Journal of Entomology 44:175-185.</p>
<p>USDA. 2000. Guidelines for Pathway-Initiated Pest Risk Assessments, Version 5.02. Plant Protection and Quarantine, Animal and Plant Health Inspection Service, United States Department of Agriculture.</p>
<p>van den Berg, M. A., E. A. de Villiers, and P. H. Joubert. 2001. Pests and beneficial arthropods of tropical and non-citrus subtropical crops in South Africa. Institute for Tropical and Subtropical Crops, Nelspruit, South Africa. 525 pp.</p>
<p>Van Der Geest, L. P. S., and H. H. Evenhuis. 1991. Tortricid pests: their biology, natural enemies, and control (World crop pests 5). Elsevier, Amsterdam; New York. xviii, 808 pp.</p>
<p>Zhang, B. C. 1994. Index of economically important Lepidoptera. CAB International, Wallingford, U.K. 599 pp.</p>
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