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



## Risk Management Document

**Im portation of Fresh**  **Citrus Fruit, including Sweet Orange (**  **Citrus sinensis (L.) Osb**  **eck ), Lemon (**  **C. limon (L.)**  **Burm. f.), Mandarin (**  **C. reticulata Blanco,**  **C. clementina Hort. ex Tanaka,**  **C. deliciosa Ten.,**  **C. unshiu Marc**  **ow. ),**  **Citrus Hybrids, and**  **the Citrus**  **- Related Gen**  **us Fortunella**  **( F.**  **japonica (**  **Thunb. )**  **Sw ingle** **, F. margarita (Lour.) Swing**  **le ), from Uruguay**  **into the**

**Continental United States**

**December 1 6**  **, 2012** 

**Plant Health Programs (PHP) Regulations, Permits and Manuals (RPM**  **) Contact Person:**  **Meredith Jones**2



### Introduction Currently , importation of fresh Citrus and Fortunella fruit from Uruguay into the United States is not authorized by 7 CFR§319.56
. The Plant Protection Division of the Dirección General de Servicios Agrícolas (DGSA), Ministerio de Ganadería , Agricultura y Pesca (MGAP) from Uruguay prepared a pest risk assessment (PRA) for th e importation of species of Citrus and Fortunella fruit from Uruguay into the continental United States in support of a market access request. The Plant Epidemiology and Risk Analy sis Laboratory

(PERAL) of the United States Department of Agriculture (USDA) , Animal and Plant Health Inspection Service (APHIS) , Plant Protection and Quarantine (PPQ) , Center for Plant Health Science and Technology (CPHST) reviewed and revised this pest risk assessment for the importation of commercially produced fresh Citrus and Fortunella fruit from Uruguay into the continental United States
. Based on the pest risk assessment (USDA, 2012 ), six pests that could be associated with fresh Citrus and Fortunella fruit imported from Uruguay were determined to be of quarantine significance for the United States: Tephritidae ( f

ruit f lies) Anastrepha fraterculus (Wiedemann) , South American fruit fl y Ceratitis capitata (Wiedemann) , Mediterranean fruit fly (Medfly) Lepidoptera Cryptoblabes gnidiella (Millière), Honeydew moth Gymnandrosoma aurantianum (Lima), Citrus borer Fungi Elsinoë australis (Bitanc
. & Jenkins ), causal agent of Sweet o range s cab disease (SOS) Bacteria Xanthomonas citri subsp. citri (ex Hasse 1915) Gabriel et al . 19 89 [sy n.: X. axonopodis pv. citri (Vauterin, et al. ) ] , causal agent of Citrus c anker disease (Xcc ) The risk rating s for all of the insect pests w ere **high .**  The rating s for the fungus (SOS) and the bacterium (Xcc) w ere **medium .**  Although a very low incidence of one of the plant pathogen s may

enter on an occasional s ymptomatic fruit, the evidence indicates that it is highly

unlikel y that any of these plant pathogens could become establish ed via the pathway of commercial Citrus and Fortunella (USDA, 2012 )
. In a previous revision of the PRA, Guignardia citricarpa Kiely was included as a quarantine pathogen likely to follow the pathway . However , a PRA conducted by APHI S (USDA
- APHIS, 2010 b ; USD, 2009b; USDA, 2009c) concluded that fresh or dried citrus3

fruit is not epidemiologically significant as a pathway

for the introduction of citrus black spot ( CBS ) because the combination of conditions required for disease transmission fro m harvested fruit are highl y unlikely
. APHIS therefore consider that fruit which is surface disinfected and treated with fungicides before shipment reduces the pest risk potential by reducing the prevalence of CBS and other pathogens affected fruit in commercial consignments
. 

### Standard Industry Practices The standard industry

practices are listed in the PRA (USDA, 2012 ). Some of these practices will be required as part of the s ys tems approach proposed for exportation of Citrus and Fortunella to the continental United States. 

### Pest Risk **M anagement**  **M easures**  1. Only commerciall y grown fruit from approved places of production that are registered with DGSA, the Uruguayan National Plant Protection Organization (NPPO), will be exported to the United States. The DGSA will ensure that growers are participating in the program and following the guidelines. Packinghouses must also be registered and approved by the DGSA and meet the requirements of the sy stems approach. 2. DGSA must provide an operational workplan to APHI S that details the activities and responsibilities that DGSA will, subject to APHI S’ approval of the workplan, carry out to meet the requirements of the s ys tems approach. APHI S will be directly involved with DG SA in monitoring and auditing implementation of the sy stems approach
. 3. If DGSA finds that a place of production or packinghouse is not compl yi ng with the requirements of the sy stems approach, no fruit from the place of production or packinghouse will be el ig ible for export into the United States until APHIS and DGSA conduct an investigation and appropriate remedial actions have been implemented
. 4. Plant litter and fallen fruit must be removed from the place of production to remove potential fruit fl y and Lep idoptera host material. Fallen fruit must not be included in field containers of fruit brought to the packing house to be packed for export. 5. Fruit must be imported in commercial consignments only and the fruit must be practicall y free of leaves, twigs and other plant parts, except for stems that are less than one inch long and attached to the fruit.4

6. The identity

and origin of the fruit must be maintained throughout the process

-- from the grove, through the packing house , and through the exporting process to the United States

-- for traceability back to the place of production. 7. DG SA will regularl y visit and inspect places of production through the exporting season, starting thirty

day s before harvest and continuing until the end of the shipping season , to ensure that the growers are following the export protocols. 8. DGSA will provide oversight for all program activities including monitoring phy tosanitary control programs, reviewing them at least once a ye ar, and maintaining all forms and documents relat ed to activities in groves and packing houses in the export program. APHI S may monitor places of production, packinghouses and records if necessary
. 9. All fruit imported into the United States must be accompanied b y a phyt osanitary certificate (PC) with an additional declaration (AD) issued b y DGSA stating that the fruit in the consignment are free of all quarantine insects (South American fruit fly , Med fl y, Honeydew moth and Citrus borer) and have been produced in accordance with the requirements of the s y stems approach. 10. APHI S will inspect fruit consignments at the port of entry to the United States
. 11. D G SA must monitor and audit the harvesting s ys tem and ensure that during the time the packinghouse is in use for exporting fruit to the United States, the packinghouse may

onl y accept fruit from registered, approved places of production. 12. Fruit must be washed, brushed, surface disinfected in accordance with 7 CFR part 305 and according to treatment schedules listed in the PPQ Treatment Manual, treated with fungicide ( e.g. imazalil, thiabendazole or combination of fludioxonil plus azox ys trobin) at label ed rates, and waxed at packinghouses. 13. DGSA will certify

that places of production from exporting orchards have effective fruit fl y trapping programs, and follow pest control guidelines, when necessary , to reduce regulated pest populations. The personnel conducting the trapping and pest survey s must be hired, trained, and supervised by DGSA or personnel authorized b y the DGSA. 14. Beginning at least 1 ye ar b efore harvest begins and continuing throughout the ye ar, trapping in the orchards for fruit fl y monitoring must be at a density of at least 2 traps per km2 in commercial production areas , with at least 2 traps placed in each place of production. Traps sho uld be baited with APHI S
- approved baits and serviced at least once every two weeks.5

15. If more than 0.7 FTD (number of fruit flies per trap per day) of either fruit fl y is trapped, pesticide bait treatments must be applied in the affected place of productio n in order for the place of production to remain eligible to export fruit. 16. DGSA must keep records of fruit fl y detections for each trap and make the records available to APHIS upon request. The records must be maintained for at least 1 year. 17. Fruit (exc ept lemon fruit) may be imported into the United States only if it is treated in accordance with 7 CFR part 305 with an approved quarantine treatment for Ceratitis capitata and Anastrepha fraterculus listed in the PPQ Treatment Manual and monitored by an official authorized by APHIS per APHIS policy
. 18. Lemon fruit may

be shipped without a quarantine treatment if it is harvested green between May

15 and August 31. The lemons must be shipped with an Additional Declaration: “The lemons have been harvested green between May 15 and August 31”. If the lemons are harvested outside of this window, or harvested yellow, they must be treated with an approved quarantine treatment in accordance with 7 CFR part 305 for Ceratitis capitata (as listed in the PPQ Treatment Manual) and monitored by

an official authorized by APHIS per APHI S policy
. 19. Fruit must be packed within 24 hours of harvest in a pest

- exclusionary packinghouse or stored in a degreening chamber in a pest

- exclusionary packinghouse. Fruit must be safeguarded b y a pest - proof screen or plastic tarpaulin while in transit to the packin ghouse and while awaiting packing. All openings to the outside of the packinghouse must be covered b y screening with openings of not more than 1.6 mm or by some other barrier that prevents pests from entering. The packinghouse must have double doors at th e entrance to the facility and at the interior entrance to the area where Citrus and Fortunella fruits are packed. Fruit must be packed in insect

- proof cartons or containers, or covered with insect

- proof mesh or a plastic tarpaulin for transport to the United States. These safeguards must remain intact until the fruit arrive in the United States. 20. Fruit must be inspected by DGSA, or personnel authorized by DGSA, following post - harvest processing. A biometric sample, to be jointly determined b y APHI S and D GSA, will be visually inspected, and a portion of the fruit will be cut open to detect internal pests, such as fruit flies and Lepidoptera larvae. 21. If a s ingle Lepidoptera egg or larva of Cryptoblabes gnidiella or Gymnandrosoma aurantianum in or on any citrus or Ceratitis capitata in lemon is found during inspection, the entire lot of fruit will be prohibited from export to the United States, and the place of production will be suspended from the export program until appropriate mitigation measures, agreed upon by DGSA and APHIS, have been taken.6



### Evidence of Effective Removal of Pests of Concern from the Pathway Orchard registration with DGSA allows trace

- back to place of production and correction of phy tosanitary issues or removal of places of production from the fruit exportation program. Orchard registration ensures that DGSA will provide oversight and that registered places of production follow the export program. Since the fruit never loses its identity (all fruit remain traceable back to the grove th ey originated ; the place of production), origin can be determined even after the fruit has reached the consumer distribution outlets and other points of sale
. Sanitation measures , such as removing and discarding fallen fruit , are esse ntial components of good agricultural practices and are mainstay s of commercial fruit production (Kirk et al ., 2001; USDA , 2007a). Removal of fallen fruits removes insect host material, which helps to maintain low pest populations (Verghese et. al. , 2004; Judd & Gardiner, 2005). Removal of inoculum, as litter and fallen fruits, is also an effective way to reduce disease occurrence (Van der Plank, 1963 ; 1975). This procedure targets SOS, but also will reduce Xcc inoculum (G ó mez et. al ., 2006; Gottwald et al ., 2002; USDA, 2009a; USDA, 2009b ). DGSA already has an adequate monitoring program in effect that is used for citrus export to the European Union ( USDA, 2012 ). A similar sy stem s approach including recording and trace

- back will be required. DGSA will certify that exporting orchards have effective fruit fly trapping programs, and follow control guidelines, when necessary , to reduce regulated pest populations. APHI S may monitor the production areas and packing houses if necessary
. The p hy tosanitary c ertificate with additional d eclaration requires DGSA to conduct an inspection and certify

that the citrus fruit are free of quarantine insects (South American fruit fly , Medfl y, h oneydew moth and c itrus borer) . This raises the awareness of those requirements for our port of entry inspection. Many

of these pests have stages that are visible upon inspection, or cause visible damage ( Parra et al. , 2001 ; 2004; Silva & Mexia, 1999 ). Customs and Border Protection agricultural inspectors receive specific instruction for detecting quarantine pests and are instructed to inspect for insects , mites and insect/mites damage, and disease blemishes (USDA , 2011c ). Pre
- harvest grove inspections reduce the likelihood that infested fruit is harvested and transported to the packinghouse (USDA, 2006; Kinney , 2007). Three surface disinfectants are currentl y approved by USDA for Xcc and SOS decontamination of regulated citrus fruit moved within the United States: sodium hy pochlorite, SOPP (sodium orthophenyl phenate) and perox ya cetic acid ( CFR, 2006; USDA, 2011b ; USDA APHI S. 2010 a . )
. Various studies demonstrated the effectiveness of these disinfectants in reducing numbers of X. citri subsp. citri cells or similar bacteria7

to low or undetectable levels (Obata et al., 1969; Brown & Schubert, 1987; Canteros et al., 2000; Ry

bak & Canteros, 2001; CFR, 2006; CFR, 2007 )
. The same surface di sinfectants were recently approved by

USDA for SOS (USDA, 2011 a)
. Packing house treatments such as waxing, surface di sinfection and fungicide dip (USDA, 2011a) , should be effective in reducing the viability of any Elsinoë australis propagules
. Washing and brushing removes insects from fruit (Vincent et al ., 2003 )
. Culling citrus fruit removes fruit with visible signs of insect damage. Removal of any damaged or blemished fruit reduces the risk that pests will be exported to the United States. Trace

back and registered production sites allow backtracking of pest problems and remedial mitigation or removal of production site s or area s from the p rogram. The regulations governing the interstate movement of citrus fruit from Florida with respect to citrus canker (7 CFR 301.75

- 7) require that the fruit be packed in a commercial packinghouse operating under a compliance agreement, treated with a surf ace disinfectant in accordance with 7 CFR part 305, and be free of leaves, twigs, and other debris. In October 2009, APHI S amended these regulations to remove some previous restrictions based on a pest risk analy sis that concluded that " commerciall y packe d and disinfected fresh citrus fruit is not an epidemiologically significant pathway for the introduction and spread of Xcc," the causal agent of citrus canker. Domestically , i nterstate movem ent of citrus fruit from SOS infested areas requires that fruit must be washed, brushed, surface disinfected (with at least one app roved treatment), fungicide treated with label ed rates of imazalil , thiabendazole or combination of fludioxonil plus azoxystrobin and waxed at packinghouses (USDA, 2011 a)
. Equivalent measures will be required for importation of Citrus and Fortunella fruit from Uruguay
. Citrus fruits except lemons may onl y be exported from Uruguay if they are subject to an approved quarantine treatment. Methyl bromide fumigation (Schedule T101

- j

- 2
- 1 ), cold treatment (Schedule T107

- a), and methyl bromide fumigation followed b y cold treatment (Schedule T108

- a) are all approved for disinfesting citrus of Ceratitis capitata and Anastrepha fraterculus (USDA , 20 11b ). Exposure to methyl bromide may result in injury to the citrus fruit, and should be monitored carefully
. Under the combined fumigation and cold treatment, methyl bromide concentration and periods of fruit exposure to the gas are reduced, potentially

low ering the risk of fruit damage. Lemons may be shipped without quarantine treatment if they have been harvested green between May 15 and August 31”. Lemons are considered to be a poor host for fruit flies (USDA, 20 08 ) , and research has shown that if lemo ns are harvested green within this time period , when fruit fly populations are low, they are not hosts to fruit flies (Willink et al. , 2007). If the lemons are harvested outside of this window, or harvested yellow, they must be treated with an approved quarantine treatment. Cryptoblabes gnidiella primarily attacks fruit that have infestations of Homoptera species producing honey

dew (Silva & Mexia, 1999). Small Cryptoblabes gnidiella larvae feed on the honey

dew and do not attack the fruit until they have grown to a larger stage. Small larvae will be removed from the pathway by packing house washing and brushing.8

Cryptoblabes gnidiella has never been intercepted by APHIS in permit cargo citrus fruit (AQAS
- PestID, 20 1 2 ). Based on the pest damage sy mptoms , inspection and culling will remove Lepidoptera pests , including Cryptoblabes gnidiella and Gymnandrosoma aurantianum , from the pathway ( Parra et al. , 2001 ; 2004; Silva & Mexia, 1999)
. Quarantine treatments are effective in eliminating Ceratitis capitata and Anastrepha fraterculus from citrus fruits (USDA , 20 11b , Willink et al. , 2007 ). These treatments have been used successfully to mitigate pest risk for importing different types of fruits from many countries and may be used on citru s from Uruguay
. 

### Summary APHI S believes that the risk management measures discussed in this document will provide an appropriate level of phyt osanitary protection against the pests of quarantine concern associated with the importation of fresh Citrus and Fortun ella from Uruguay into the continental United States. The RMA (USDA, 2009b ; USDA, 2009c ) for interstate movement of citrus from the Xcc quarantine area within the United States carefull y examined field practices and procedures to determine which ones prov ide the most effective means of preventing the spread of citrus canker disease via the movement of commercial citrus fruit. The RMA treatment s achieve this goal. The measures that are proposed for importation of fruit from Uruguay are equivalent to those in regulations for interstate movement of citrus from Xcc and SOS quarantine areas in the United States. Sweet orange scab disease is easily controlled with field treatments and is further inhibited with post

- harvest treatments (EPPO

- CABI , 1997; USD A, 2011 a)
. Trapping and bait spraying w ill further ensure that fruit fly populations will be low. Packinghouse culling and fruit removal from orchards will remove any s enescent fruit , which are more likel y to be host s to fruit flies. Gymnandrosoma auran ianum is rare in commercial citrus in South America (USDA , 2007b ). G. auranianum has never been intercepted by APHIS in citrus fruit from any country (AQAS
- PestID , 201 2 )
. Cryptoblabes gnidiella primarily attacks fruit that has infestations of Homoptera species producing honey dew (Silva & Mexia, 1999). Small larvae feed on the honey

dew and do not attack the fruit until they have grown to a larger stage. Small larvae will be removed from the pathway by packing house washing and brushing. Cryptoblabes gnidiella has never been intercepted b y APH IS in citrus fruit (AQAS
- PestID , 201 2 ). Based on the pest damage sy mptoms, inspection and culling will remove Lepidoptera pests from the pathway ( Parra et al. , 2001 ; 2004; Silva & Mexia, 1999)
.9

Uruguay has exported citrus fruits to the European Union for many ye ars. The phy tosanitary measures currentl y in place in Uruguay (USDA, 2012 ) for export to the European Union have been proposed b y Uruguay to be the basis for a s ys tems approach for the importation of citrus fruit to the continental United States. APHI S agrees with some of the proposed measures and propose s additional measures , which are included in the sy stem approach described here. In addition to the sy stems approach in Uruguay , Customs and Border Protection officials will inspect fruit from Uruguay at ports of entry

to prevent s ymptomatic or infested fruit from entering the United States. 

### Authors Walter Gould Ph.D. Senior Risk Manager José R. Hernández Ph.D. Risk Manager10



### References AQAS
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- APHIS
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. Brown, G.E. and T.S. Schubert. 1987. "Use of Xanthomonas campestris pv. vesicatoria to evaluate surface disinfec tants for canker quarantine treatment of citrus fruit." Plant Disease 71(4): 319

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- 65204 Citrus Canker; Movement of Fruit From Quarantined Areas; Final Rule. Office of the Federal Register, National Archives and Records Administration, Washington, DC, USA. EPPO/CABI . 1997. Data sheet on quarantine pests: Elsinoë fawcettii and Elsinoë australi s. In I. M. Smith, D. G. McNamara, P. R. Scott, and M. Holderness, (eds.). Quarantine Pests for Europe. 2nd edition. CAB International, Wallingford, UK. G ó mez C. L . Brun, D. Chauffour, and D. De Le Vallée
. 2006. Effect of leaf litter management on scab development in an organic apple orchard. Agriculture, Ecosy stems & Environment 118: 249
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. http://www .plantmanagementnetwork.org/pub/php/review/citruscanker/
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complimentary

actions of mating disruption, tree banding and sterile insect technique: Five

- year study in organic orchards. Crop Protection 24: 718

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137. Obata, T., F. Tsuboi and S. Wakimoto. 1969. "Studies on the detection of Xanthomonas citri by phage technique and the surface sterilization of Unshu orange for export to the United States." Res. Bull. Plant Prot. Japan 7:26

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Parra, J. R. P., J. M. S. Bento, M. S. Garcia, P. T. Yamamoto, E. F. Vilela, and W. S. Leal. 2004. Development of a control alternative for the citrus fruit borer, Ecdytolopha aurantiana (L epidoptera, Tortricidae): from basic research to the grower. Revista Brasileira de Entomologia 48(4):561

- 567. Parra, J. R. P., P. K. Júnior, R. M. d. S. Molina, and M. d. L . Haddad. 2001. Effect of the Fruit Acidity

on the Development of the Citrus Fruit Borer. Entomologia 22(2):321

- 332. Ry bak, M. and B.I. Canteros. 2001. Populations of Xanthomonas axonopodis pv. citri in endemic areas. Plant Pathogenic Bacteria. De Boer, S. H. Netherlands, Kluwer Academic Publishers. Silva, E. B., A. Mexia. 1999. The pest complex Cryptoblabes gnidiella (Millière) (Lepidoptera: P yr alidae) and Planococcus citri (Risso) (Homoptera: Pseudococcidae) on sweet orange groves ( Citrus sinensis (L .) Osbeck) in Portugal: Interspecific association. Bol. San. Veg. Plagas. 25: 89

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. www.aphis.usda.gov/

plant_ health/ plant_pest_info/ citrus /downloads/chrp.pdf USDA. 2007a. Argentina Lemons ( Citrus limon ) for Fresh Market Export: USDA
APHI S
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. USDA APHIS and USDA ARS
. January

2008. 16 pp. http://www.aphis.usda.gov/pl ant_health/plant_pest_info/fruit_flies/downloads/medfly rep ort - da

- 2008
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USDA
. 201 1a
. APHIS
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. 3 pp. USDA. 20 11b
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- APHIS, PPQ; http://www.aphis.usda.gov/import_export/plants/manuals/ports/treatment.shtml accessed March 2011. USDA. 2011c
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- Related Genus Fortunella ( F. japonica (Thunb.) Swingle, F. margarita (L our.) Swingle), from Uruguay into the Continental United States
. A Qualitative, Pathway

Initiated Pest Risk Assessment. Version 9, 122 pp. USDA APHI S. 2010 a . Federal Domestic Quarantine Order: Elsinoë australis Bitanc. & Jenkins Causal Agent of Sweet Orange Scab (SOS) (DA

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- 2007. Estación Experimental Agroindustrial Obispo Colombres, Available in www.eeaoc.org.ar , Tucumán, Argentina.Appendix 1.

Table 1. The m itigations that are effective for each pest. All mitigations are necessary as part of the sy stems approach for the pest complex on Citrus from Uruguay
.

Pests that may

follow the pathway

of fresh citrus from Uruguay Mitigation Anastrepha

fraterculus Ceratitis

capitata Cryptoblabes

gnidiella Gymnandrosoma

aurantian um Elsinoë

australis (SOS) Xanthomonas

citri subsp. citri (Xcc ) 1 X X X X X X 2 X X X X X X 3 X X X X X X 4 X X X X 5 X X X X X X 6 X X X X X X 7 X X X X X X 8 X X X X X X 9 X X X X 10 X X X X X X 11 X X X X X X 12 X X 13 X X X X X X 14 X X 15 X X 16 X X 17 X X 18 X X 19 X X 20 X X X X X X 21 X X XTable 2. The mitigations that will be in the CFR

or the Operational Workplan (OWP) or both. Mitigation CFR or OWP or

Both 1 OWP 2 Both 3 OWP 4 Both 5 Both 6 OWP 7 OWP 8 OWP 9 Both 10 CFR 11 OWP 12 Both 13 OWP 14 OWP 15 OWP 16 OWP 17 Both 18 OWP 19 OWP 20 OWP 21 OWP