United States Department of Agriculture and Plant Health Inspection Service Plant Protection and Quarantine

Importation of Persimmon, Thunb., as Fresh Fruit with Calyxes from into the United States

Risk Management Document

April 21, 2015

Plant Health Programs (PHP) Regulations, Permits and Manuals (RPM) Contact Person: David Lamb

Introduction

APHIS received a request to import persimmon fruits into the United States from the National Plant Protection Organization of Japan (NPPO). A pathway-initiated pest risk assessment (PRA) was prepared by APHIS’s Plant Protection and Quarantine (PPQ) to identify the unmitigated pest risks associated with importation of persimmon fruits with calyxes from Japan (USDA, 2013). The PRA was prepared based on pest interception data, scientific literature, and information provided by the Government of Japan. The PRA identified quarantine pests of D. kaki that occur in Japan and that could be introduced into the United States (continental United States, Alaska and Hawaii) in commercial consignments.

The PRA identified ten and nine fungi likely to follow the pathway of persimmons with calyxes from Japan.

Arthropods:

Mites Tenuipalpus zhizhilashviliae Reck Acari: Tenuipalpidae Conogethes punctiferalis (Guenée) Lepidoptera: Pyralidae Homonopsis illotana (Kennel) Lepidoptera: aeolopa Meyrick Lepidoptera: Tortricidae masinissa Meyrick Lepidoptera: Mealybugs Crisicoccus matsumotoi (Siraiwa) Hemiptera: Pseudococcidae Pseudococcus cryptus Hempel Hemiptera: Pseudococcidae Thrips Ponticulothrips diospyrosi Haga & Okajima Thysanoptera: Phlaeothripidae Scirtothrips dorsalis Hood Thysanoptera: Thripidae Thrips coloratus Schmutz Thysanoptera: Thripidae

Fungi:

Adisciso kaki Yamamoto et al. Ascomycetes: Amphisphaeriaceae Colletotrichum horii B. Weir & P.R. Johnst. Ascomycetes: Phyllachorales Cryptosporiopsis kaki (Hara) Weindlm. Ascomycetes, Incertae sedis) Mycosphaerella nawae Hiura & Ikata Ascomycetes: Mycosphaerellales Pestalotia diospyri Syd. and P. Syd. Ascomycetes: Xylariales Pestalotiopsis acaciae (Thümen) Yokoyama & Kaneko Ascomycetes: Xylariales Pestalotiopsis crassiuscula Steyaert Ascomycetes: Xylariales Phoma kakivora Hara Ascomycetes: Pleosporales Phoma loti Cooke Ascomycetes: Pleosporales

The PRA assigned High pest risk potentials to the arthropods Conogethes punctiferalis, Homonopsis illotana, Lobesia aeolopa, Pseudococcus cryptus, and Scirtothrips dorsalis and the

2 fungus Pestalotia diospyri. All other quarantine pests were rated Medium pest risk potential.

The proposed movement of persimmon fruits with calyxes from Japan, if approved, would be regulated by an amendment to existing fruit and vegetable import regulations (7 CFR §319.56). Pest risk management is the process of identifying ways to react to a perceived risk, evaluating the efficacy of these actions, and identifying the most appropriate options (IPPC, 2004). This document outlines phytosanitary measures and provides evidence of their efficacy in preventing the introduction of quarantine pests. The appropriate level of protection may be achieved through the application of a single phytosanitary measure, such as establishment of pest free areas, pest free place of production or a quarantine treatment, or a combination of measures in a systems approach.

APHIS PPQ Oversight and Operational Workplan

The NPPO of Japan and APHIS will develop an operational workplan that details the activities that the growers will carry out to meet the requirements of the systems approach. The Japan NPPO or their designate will be directly involved with the monitoring and auditing implementation of the systems approach. The NPPO of Japan will ensure that each grower has a pest surveillance and orchard pest control program and follows all requirements of this systems approach. The NPPO of Japan will ensure that all records related to program activities are maintained for at least 1 year and, as requested, provide them to APHIS for review. The NPPO of Japan may delegate oversight of program activities to independent auditing organizations.

Risk Management Measures

Persimmon fruits with calyxes from Japan may only be imported to the United States if they have been grown and packed using a systems approach including all of the following risk management measures:

1. Only commercial consignments of persimmons may be imported. Persimmons must be grown in approved places of production (orchards) that are registered with NPPO of Japan. The NPPO of Japan will approve all places of production and ensure they meet all of the requirements of the systems approach. NPPO of Japan will visit and inspect the places of production monthly, beginning at blossom drop and continuing until the end of the shipping season.

2. Growers must adhere to orchard control programs approved by NPPO of Japan for control of arthropods and fungi of quarantine concern. This IPM program includes monitoring and treatments for major pests, including plant pathogens, in the orchards following field practices jointly agreed by APHIS and NPPO of Japan.

3. Packinghouses must be registered with NPPO of Japan. During the time each packinghouse is in use for shipping persimmons to the United States, fruit for export to the United States must

3 be segregated from other fruit. The packinghouse may only accept fruit for export to the United States from registered, approved places of production. NPPO of Japan will audit packinghouse operations to verify that the packinghouses are complying with the requirements of the systems approach. If NPPO of Japan finds that a place of production or packinghouse is not complying with the requirements of the systems approach, no fruit from the place of production or packinghouse will be eligible for export to the United States until NPPO of Japan conducts an investigation and appropriate remedial actions have been implemented.

4. Any damaged, disease-infected, -infested, or deformed fruit and fruits with surface pests must be culled before or during packing. Culled fruit must be removed from the packinghouse.

5. Box markings identifying each orchard and packing house will be required so that consignments can be traced back to groves or places of production.

6. A biometric sample (jointly agreed upon by NPPO of Japan and APHIS) of persimmon fruit must be inspected following any post-harvest processing. A biometric sample will be visually inspected for quarantine pests including fungal diseases, and a portion of the fruit will be cut open to detect internal pests. If quarantine pests are found, the entire lot of fruit will be prohibited from export under the systems approach to the United States.

7. Consigments must be accompanied by a Phytosanitary Certificate with Additional Declaration stating “Fruit in this consignment was inspected and found free of quarantine pests; the consignment was produced under and meets all the components of the systems approach".

8. All persimmons imported into the United States are subject to inspection for pests of quarantine concern at the port of entry by Customs and Border Protection (CBP) of the Department of Homeland Security (DHS).

Efficacy of Risk Management Measures

A systems approach made up of multiple mitigations can provide an alternative to single measure mitigation, such as a standalone quarantine treatment, to meet the appropriate level of phytosanitary protection, or can be developed to provide phytosanitary protection in situations in which no single measure is available (IPPC, 2002). For example, Hass avocados from Mexico have been produced and exported to the United States under a systems approach for Stenoma catenifer, seed and stem weevils and fruit flies. The Mexican avocado program included a field program to maintain pest free and pest low prevalence areas. The systems approach combines field inspection for pests with cutting of samples at the packing house, and sampling by CBP at the first port of entry to the United States. Since 2004, approximately 181,000 consigments totaling over 3.2 million metric tons of Hass avocadoes from Mexico have been imported into the United States (AQAS, 2014). None of the pests have ever been intercepted in commercial consigments of avocados under the systems approach since Mexico was granted market access in 1997 (AQAS, 2014). Based on the success of this program, APHIS has modified it and removed or modified components that are not required to remove pests from the pathway.

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The systems approach of risk management measures for Japan persimmons includes:

 Workplan and oversight with orchard and packing facility certification and traceback  Orchard control of key pests  Culling all pest-infested and damaged persimmons at the packing house  Sampling of packed persimmons will include cutting of some fruit to inspect for internally feeding Lepidoptera larvae and visual inspection for diseases  Phytosanitary Certificate with an Additional Declaration stating freedom of pests of concern  U.S. port of entry inspection.

The NPPO of Japan or their designate will provide oversight to the systems approach through a workplan that details the growers’ responsibilities. The NPPO of Japan will ensure that each grower follows the field and industry practices jointly agreed by APHIS and NPPO of Japan and follows all requirements of this systems approach. Any grower that does not comply with the required pest management will not be allowed to export. APHIS may monitor the places of production if necessary. If any pest problems are found at port of entry inspections, the consignment can be traced back to the packinghouse and place of production (orchard).

High pest populations are a contributing factor to the failure of systems approaches. By monitoring pest populations using appropriate orchard pest controls, high pest populations are avoided. The pest control used for persimmons in Japan will follow the guidelines jointly agreed by APHIS and NPPO of Japan. These guidelines are mandatory for persimmon producers in Japan who wish to export their persimmons. These guidelines include monitoring orchards for key pests and control of these pests using recommended chemical treatments at appropriate times when persimmons are most vulnerable to damage or infestation; i.e., at fruit drop and immediately before harvest.

The NPPO of Japan or their designate will ensure that all packinghouses follow the requirements of the systems approach. The packinghouses must segregate export fruit from all other fruit. The packinghouses will cull all deformed, disease-infected or arthropods-infested persimmons. This will prevent pests from entering the pathway of export to the United States.

Adisciso kaki naturally infected leaves and calyces begin to show symptoms, black lesions expand rapidly, leading to necrosis and finally defoliation (Yamamoto et al., 2012). Immature fruiting structures form on the underside of infected leaves relatively early in the infection cycle and likely complete their development on fallen leaves to produce more ascospores as inoculum to infect new leaves (Yamamoto et al., 2012).

Symptoms of Colletotrichum horii (persimmon anthracnose) are easily recognized. The fungus infects fruits throughout the entire fruit-growing season. In young fruits, the lesions are often circular or oval, 3-8 mm diameter, purple to dark purple, and occasionally slightly depressed. As the disease progresses, fruit lesions may reach up to 2 cm in diameter (Xie et al., 2010). Under dry conditions the disease lesions are sunken and a longitudinal crack often occurs through the

5 center of the fruit (Zhang, 2008). These symptoms can be readily recognized during field and packinghouses inspections.

Cryptosporiopsis kaki attacks persimmon branches (Weindlmayr, 1964) and fruit (Watson, 1971). Mycosphaerella nawae causes necrotic spots on leaves, chlorosis and early defoliation. Leaf lesions and defoliation caused by infection induce premature fruit maturation and abscission, resulting in serious economic losses (Vicent et al., 2011).

Pestalotia diospyri caused lesions on sepals (calyces), fruit, and leaves, causing defoliation, as well as damaging stem cankers (Alves et al., 2011). Pestalotiopsis acacia and Pestalotiopsis crassiuscula infection produces a ring-spot disease on leaves and calyxes of young fruits of persimmon (Yasuda et al., 2003), presumably reducing fruit quality to some degree. In severe cases, leaves may be shed prematurely.

Infection of fruit of Phoma kakivora produces circular or irregularly-shaped lesions or stains (10- 15 mm in diameter) composed of numerous small, black spots (Yamada, 1966), presumably reducing fruit yield and quality. Sepals and leaves also may exhibit the spots. Fruit and stems of Diospyros kaki can be infected by Phoma loti (Kishi, 1998), so presumably could reduce fruit yield and quality.

Fruits attacked by Conogethes punctiferalis appear discoloured, scorched, and are covered with brown excretion mass around holes. An early symptom of C. punctiferalis attacks is the appearance of a pattern of small, irregularly spaced holes. These symptoms can be readily recognized during inspections (CABI, 2015). Pseudococcus cryptus the mealybug settles under the sepal, where it feeds on the fruit; the honeydew produced causes black knots to appear on the fruit (George & Nissen, 2002). Most Tortricdae are not normally internal feeders on fruit. Larvae of Tortricidae are leaf rollers that will feed on any part of the plant they come into contact with including the surface of the fruit. Pupae, eggs and larvae are normally found on the leaves (Williams, 2000). Damage by thrips ranges from the slight disruption of the tissues to total deformation and disruption. The growing tip of the plant and young leaves, especially the axillary leaves, are the main points of attack. The damage is due to continuous sucking of the cell sap, leading to necrosis of the cell tissues (CABI, 2015). The above symptoms caused by arthropods are easily recognized during inspections and damaged fruits can be culled during packing house procedures prior to packing. Routine orchard controls that include monitoring and applications of pesticides as needed will keep the pest populations under control.

NPPO of Japan will inspect a biometric sample of the persimmons and certify that they have been produced under the requirements of the systems approach and are free of quarantine pests and diseases. The inspection will include cutting a portion of the persimmons to look for any internally feeding and visual inspection for diseases.

Japan persimmons produced under this systems approach will be inspected by CBP at the first port of entry to the United States. Infested/infected consignments will be rejected, and traceback will be done by APHIS and NPPO of Japan to identify and correct problems, including removal of the packinghouse and orchard from the Japan persimmon program. The sampling of fruit, including cutting, will give warning if any portion of the systems approach is failing.

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Summary

A systems approach, employing a combination of measures acting independently, if properly implemented, mitigates risk and provides an acceptable level of phytosanitary protection. There are several mitigations including orchard monitoring and control of pests, culling, inspection and post-harvest quarantine treatments that, when combined, will remove all quarantine pests from the pathway. In addition, traceback will allow preventative actions should any problems occur with the systems approach.

Authors

José R. Hernández, Ph.D., Senior Risk Manager Plant Pathology APHIS-PPQ

Devaiah A. Muruvanda, Ph.D., Senior Risk Manager Entomology APHIS-PPQ

References

Alves, G., F. S. Verbiski, T. J. Michalides, and L. L. May-de-Mio. 2011. First report of Pestalotiopsis diospyri causing canker on persimmon trees. Revista Brasileira de Fruticultura 33(3):1019-1022.

AQAS. 2014. Agricultural Quarantine Activity System Pest Interception Database. USDA- APHIS-PPQ. Last accessed May 2014. CABI. 2015. www.CABI.org

George, A.P. and R.J. Nissen. 2002. Persimmon, pp. 65-124. In T.K. Bose, S.K. Mitra, and D. Sanyal (eds.). Fruits: Tropical and Subtropical. Vol. II, 3rd rev. ed. Calcutta: Naya Udyog.

IPPC. 2002. The use of integrated measures in a systems approach for pest risk management. International Standards for Phytosanitary Measures No. 14. Rome: Secretariat of the International Plant Protection Convention, United Nations Food and Agriculture Organization.

IPPC. 2004. Pest risk analysis for quarantine pests, including analysis of environmental risks and living modified organisms. International Standards for Phytosanitary Measures No. 11. Rome: Secretariat of the International Plant Protection Convention, United Nations Food and Agriculture Organization.

Kishi, K. (ed.). 1998. Plant Diseases in Japan. Tokyo: Zenkoku Nöson Kyöiku Kyökai.

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USDA. 2007. Risk Management Document: Removal of Anastrepha Fruit Fly Trapping Requirements from Mexican ‘Hass’ Avocados for Importation into the United States. USDA-APHIS-PPQ. Dec. 13, 2007. 4 pp.

USDA. 2013. Importation of Persimmon, Diospyros Kaki Thunb., as Fresh Fruit with Calyxes from Japan into the United States. A Qualitative, Pathway-initiated Risk Assessment. USDA-APHIS-PPQ Center for Plant Health Science and Technology - Plant Epidemiology and Risk Analysis Laboratory. 99 pp.\

Vicent, A., D. D. M. Bassimba, and D. S. Intrigliolo. 2011. Effects of temperature, water regime and irrigation system on the release of ascospores of Mycosphaerella nawae, causal agent of circular leaf spot of persimmon. Plant Pathology 60:890-898.

Watson, A.J. 1971. Foreign bacterial and fungus diseases of food, forage, and fiber crops: an annotated list. USDA Agric. Handbk. 418.

Weindlmayr, J. 1964. Beiträge zu einer Revision der Gattung Myxosporium Link. 2. Mitteilung. Sydowia 18(1-6): 26-32.

Williams, D. 2000. Light Brown Apple in Orchards. Agriculture Notes. AG93. http://www.dpi.vic.gov.au/dpi/nreninf.nsf/9e58661e880ba9e44a256c640023eb2e/83d05641197a e4adca256f0f0020f3f0/$FILE/ag0093.pdf

Xie L., Zhang J-Z, Cai L., and Hyde D. 2010. Biology of Colletotrichum horii, the causal agent of persimmon anthracnose. Mycologia 1(4): 242-253.

Yamada, S. 1966. The stain on Japanese persimmon fruits caused by Phoma kakivora. Bull. Hort. Res. Stn. Japan Ser. B 5: 133-138.

Yamamoto, J., Tanaka, K, Ohtaka, N. and Sato, N. 2012. Black leaf spot of Japanese persimmon (Diospyros kaki), a new disease caused by Adisciso kaki sp. nov. Journal of General Plant Pathology 78:99-105.

Yasuda, F., T. Kobayashi, H. Watanabe, and H. Izawa. 2003. Addition of Pestalotiopsis spp. to leaf spot pathogens of Japanese persimmon. J. Gen. Plant Pathol. 69(1): 29-32.

Zhang J-Z. 2008. Anthracnose of persimmon caused by Colletotrichum gloeosporioides in China. Asian Australian J. Plant Sci. Biotechnol. 2 (2): 50-54.

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