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



## Risk Managem **ent Document**


## Importation of Apples ( **Malus pumila**  **) from China**  **into the continental United States** 

**December 2 , 2013** 

**Plant Health Programs (PHP) Regulations, Permits and Manuals (RPM)**  **Contact Person : Marc E. Phillips** This document describes the risk management measures for the i mportation of fresh apple fruit,

Malus pumila Mill ., from China into th e c ontinental United States

. A qualitative, p athway

initiated pest risk assessment (PRA) , “ Importation of Apples ( Malus pumila ) from China into the continental United States ” (USDA, 2013 a) was developed in support of a request from China to export apples into the continental United States. The PRA was prepared based on pest interception data, the scientific literature, and information provi ded by the Government of China

. Entry of apples from China into the United States presents a risk of introduction of exotic plant pests. The PRA reported 21 ( 19 arthropods and 2 fung i ) quarantine pests that may follow the pathway of commercial shipments o f apples from China into the continental United States

. The PRA determined that the following pests are candidates for risk management, because they **met the threshold to likely cause unacceptable consequences of introduction** , and they received an overall **likelihood of introduction** risk rating **above** Negligible: **Pest type Taxonomy**  **Scientific name Likelihood of Introduction**  **overall rating** Arthropod Acari: Tenuipalpidae Cenopalpus pulcher (Canestrini & Fanzago) Medium Coleoptera: Curculionidae Rhynchites auratus (Scopoli) Medium Rhynchites bacchus (L.) Medium Rhynchites giganteus Krynicky Medium Rhynchites heros Roelofs Medium Diptera: Tephritidae Bactrocera dorsalis (Hendel) High Lepidoptera: Carposinidae Carposina sasakii Matsumura Medium Lepidoptera: Lyonetiidae Leucoptera malifoliella (Costa) High Lepidoptera: Pyralidae Cryptoblabes gnidiella (Millière) Medium Euzophera bigella (Zeller) Medium Euzophera pyriella Yang Medium Lepidoptera: Tortricidae Adoxophyes orana (Fischer von Röslerstamm) Medium Archips micaceana (Walker) Medium Argyrotaenia ljungiana (Thunberg) Medium Cydia funebrana (Treitschke) Medium Grapholita inopinata Heinrich Medium Spilonota albicana (Motschulsky) Medium Spilonota prognathana Snellen Medium Ulodemis trigrapha Meyrick Medium Fungi Ascomycetes: Helotiales Monilia polystroma van Leeuwen High Monilinia fructigena Honey High The PRA identified these pests as candidates for risk management and rated them Medium or High for probability

of introduction. L ow rated pests normally only require standard port

–of

-entry

inspection as a mitigation. Pests rated Medium and High for probability of introduction that have been identified in the PRA as candidates for risk management may require mitigations beyond standard port
- of

- entry inspection based on the biology of the pests. 

## Risk Managem **ent Measures :**  APHI S propose s that fresh apples from China m ay be imported into the United States under the following sy stems approach: 1. An operational workplan detailing the sy stems approach will be developed by the national plant protection organization (NPPO ) of China subject to approval b y APHIS. All oversight of the program will be done by the NPPO of China or their designate. The NPPO of China is expected to maintain program records for at least one year and provide them to APHI S upon request. APHIS reserves the right to require APHI S oversight visits in the event of pest interceptions or other problems. 2. Commercial consignments only may be exported. 3

. Apples must be grown at production sites (orchards) registered with the NPPO of China. The growers with registered production sites will be responsible for following the phy tosanitary measures agreed upon by APHIS and the NPPO of China, including appl yi ng control measures that are authorized for use in China and the United States of America to reduce pest p opulations. 4. The NPPO of China is responsible for ensuring that registered places of production are inspected twice every

season, with special emphasis on the control of quarantine pests listed above. 5. All apples must be bagged individuall y by the time they

reach 2cm in diameter. 6. Fallen fruit must be removed from orchards weekly

. 7 . Packinghouses must be registered with the NPPO of China and must have a s ys tem of box markings allowing traceback to individual production sites. 8 . Packinghouses must have a s ys tem of quality control of fruit , including culling to remove all leaves and any damaged or infested fruit. 9 . A ll a pples must undergo washing and waxing.10 . The NPPO of China must inspect a biometric sample of the packed

- out apples for pe sts

and disease. The sample size for this inspection will be specified in the workplan. 1 1 . The NPPO must issue a Phy tosanitary Certificate indicating that the consignment was inspected and found free of pests 1 2

. An APHI S approved treatment is required for fruit produced south of 3 3rd parallel, to mitigate Bactrocera dorsalis fruit flies. Currently the only APHIS approved treatment for Bactrocera dorsalis in apples is T108

- a fumigation plus refrigeration of fruits , but any other treatment subsequentl y approved b y APHIS may be used. 1 3

. Upon detection of Monilinia fructigena or Monilia polystroma in a consignment for export, APHI S MAY reject the infected consignment and reject the production site for importation to the United States for the remainder of that season. If Monilinia fructigena or Monilia polystroma are detected in more than one registered production site in a Province , APHI S may

prohibit the importation into the United States of apples from the Province until an investigation is conducted and APHIS and the NPPO of China agree that appropriate remedial actions have been taken. Procedures for disqualification of production sites based on pest detections in export consignments will be detailed in the workp lan approved b y APHI S and the NPPO of China. 1 4 . The exportation to the United States of apples from the rejected production site may resume in the next growing season if an investigation is conducted and APHI S and the NPPO of China agree that appropriate remedial actions have been taken. 1 5 . The fruit will be inspected b y U.S. Customs and Border Protection at the first U.S. port of entry for pests and disease. 

## Efficacy of **Risk Managem ent Measures**  **:** All production sites will have to be registered with the NPPO of China. The required operational workplan will ensure that the NPPO of China will provide oversight to the production sites so that bagging of fruit will be applied consistentl y to all fruit. The NPPO will also monitor the production sites at least twice per season so that effective control of quarantine pests will be maintained. The packinghouses must also maintain traceback through box markings, so that any problem consignments can be trac ed bac k to the production sites and remedial action may be taken. China NPPO monitoring of pest populations will determine the need and timing of field controls and insure effective control of pests (Lewis, 1981). The operational details for monitoring and application of controls in the orchards, if needed, will be detailed in the workplan

. Of the 21 quaranti ne pests listed in the PRA (USDA, 2013 a), 19 are arthropods , of which 8 are Lepidoptera and 4 are weevils (Curculionidae)

. The required bagging of the individual fruit at2cm in diameter will prevent these Lepidoptera and Coleoptera pests from infesting the apples.

China has imported certain pear s pecies using bagging as a mitigation for Lepidoptera since 1998. In 15 years o f importation there have been only 15 interceptions of Lepidoptera and 0 interceptions of Curculionidae indicating that bagging is an effective mitigation for these pests (AQAS, 2013). In addition to the bagging, APHIS requires packing house culling and an inspection of apples b y the NPPO of China. L epidoptera pests of apples leave obvious feeding damage, holes and frass in the fruit. Standard industry packinghouse procedures as culling and a phy tosanitary inspection will remove these visible pests from the pathway . If pests are found upon port
- of

- entry inspection, traceback will allow removal of problem production sites from the program. The pear leaf miner, Leucoptera malifoliella , was intercepted in significant numbers in apples import ed from Franc e in 1985 (AQAS , 2013) . This led to restriction s on imports of apples and the previous requirement for pre

- clearance. The current sy stems approach will require removal of all leaves , packinghouse culling and packinghouse inspections , which together will effectivel y remove this leaf miner from the pathway of fresh fruit. Currently the onl y APH IS approved treatment for Bactrocera dorsalis in apples is T108

- a , fumigation plus refrigeration of fruits , but any other treatment subsequently approved by

APHIS may be used. Cold treatment T

- 10 8

- a is an a pproved APHI S treatment for Bactrocera dorsalis (USDA, 2013 b ). Th is fumigation plus cold treatment has been used for many years on different fruit/country combinations and will ensure the mortality of all Bactrocera dorsalis larvae. Monilinia fructigena is the most common cause of fruit rot in fruit orchards, causing characteristic brown rot sy mptoms with conidial pustules often i n concentric circles (CABI, 2013 ). Field inspections, packinghouse inspections, and the Phy tosanitary Certificate stating disease freedom are considered sufficient mitigation measures for the fungal diseases. Field sanitation of removing fallen fruit is required under this sy ste ms approach, and this will remove fruit from the field which would otherwise provide host material for pests of concern. Culling at the packing house is a standard industry practice which removes all obviously blemished, diseased and insect

- in fested frui ts from the pathway

. Registration of places of production and packinghouses will allow trace back and auditing. Any problem places of production and packinghouses can be removed from the export program unless they comply with mitigations. Apples produce d under this sy stems approach will also be subject to inspection by Department of Homeland Security, Customs and Border Protection (CBP) at the United States port of entry. In fected and/or i nfested fruit will be rejected, and trace back will be don e by APHIS and the NPPO of China to identify and correct problems including removal of the packinghouse or place of production from the export program. The requirements of a phytosanitary certificate issue d by

the NPPO of China will document that the con signment is a product of the exporting country . A ph yt osanitary certificate will also provide ph yt osanitary

security by requiring the NPPO of China to conduct inspections for pests of quarantine concern.

## Summary:

Most of the pests on the pest list have never been intercepted at ports of entry in commercial fruit shipments. Standard commercial practices are suff icient to mitigate many pests. The sy stems approach of field and packing house measures described above will remove all other pests from the pathway. Requiring bagging of fruit, removal of leaves, packinghouse culling and inspection will ensure that the Lepidoptera and Curculionidae pests will be removed from the pathway of fresh apples

. APHI S has determined that the listed risk management meas ures, along with the requirement of a phyt osanitary certificate and the port of entry inspection, will mitigate the risk of pest introduction s on apples from China into the continental United States. 

## Author **s :**  José R. Hernández, Ph.D. Senior Risk Manager

- Plant Pathology Walter P. Gould, Ph.D. Senior Risk Manager

– Entomology Devaiah A. Muruvanda, Ph.D. Senior Risk Manager

– Entomology


## References:
AQAS. 2013. Pest Interception Database (PestID )

. United States Department of Agriculture, Animal and Plant Health Inspection Service, Plant Protection and Quarantine (PPQ) . Accessed October, 2013. CABI. 2013. Crop Protection Compendium. Commonwealth Agricultural Bureau International (CABI), Wallingford, UK. Hadidi , A., M. Barba, T. Candresse, and W. Jelkmann

. 2011. Virus and Virus

- like Diseases of Pome and Stone Fruit

. APS Press , St. Paul, MN

. p. 341

- 359. Lewis, T. 1981. Pest monitoring to aid insecticide use. Philosophical Transactions of the Royal Society , London. 295 (1076): 153

- 162. USDA. 2013 a . Importation of Apples ( Malus pumila ) from China into the continental United States . Animal and Plant Health Inspection Service, Center for Plant Health Science and Technology , Plant Epidemiology and Risk Analy sis L aboratory , Raleigh, NC. 311 pp.U SDA. 2013 b

. USDA Treatment Manual.

http://www.aphis.usda.gov/import_export/plants/manuals/ports/downloads/treatment.pdf Accessed December 2013. Watson, A.J. 1971. Foreign bacterial and fungus diseases of food, forage, and fiber crops : An annotated list

. United States Department of Agriculture , Agricultural Research Service . 111 pp

.