United States Department of Agriculture

Animal and Plant Health Inspection Service

Plant Protection and Quarantine

Risk Management Document

Importation of Fresh Citrus Fruit, including Sweet Orange 

(Citrus sinensis (L.) Osbeck), Lemon (C. limon (L.) Burm. f.), 

Mandarin (C. reticulata Blanco, C. clementina Hort. ex Tanaka,

C. deliciosa Ten., C. unshiu Marcow.), Citrus Hybrids, and the 

Citrus-Related Genus Fortunella (F. japonica (Thunb.) 

Swingle, F. margarita (Lour.) Swingle), from Uruguay into the 

Continental United States

December 16, 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 the

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 

Analysis 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 (fruit flies)

Anastrepha fraterculus (Wiedemann), South American fruit fly

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 orange scab disease 

(SOS)

Bacteria

Xanthomonas citri subsp. citri (ex Hasse 1915) Gabriel et al. 1989 [syn.: X.

axonopodis pv. citri (Vauterin, et al.)], causal agent of Citrus canker disease 

(Xcc)

The risk ratings for all of the insect pests were high. The ratings for the fungus (SOS) 

and the bacterium (Xcc) were medium. Although a very low incidence of one of the

plant pathogens may enter on an occasional symptomatic fruit, the evidence indicates that 

it is highly unlikely that any of these plant pathogens could become established 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 APHIS 

(USDA-APHIS, 2010b; USD, 2009b; USDA, 2009c) concluded that fresh or dried citrus 
3

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 from 

harvested fruit are highly 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 systems approach proposed for exportation of 

Citrus and Fortunella to the continental United States. 

Pest Risk Management Measures 

1. Only commercially 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 systems approach.

2. DGSA must provide an operational workplan to APHIS that details the activities 

and responsibilities that DGSA will, subject to APHIS’ approval of the workplan, 

carry out to meet the requirements of the systems approach. APHIS will be 

directly involved with DGSA in monitoring and auditing implementation of the 

systems approach.

3. If DGSA 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 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 fly and Lepidoptera 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 

practically 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. DGSA will regularly visit and inspect places of production through the exporting 

season, starting thirty days 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 

phytosanitary control programs, reviewing them at least once a year, and 

maintaining all forms and documents related to activities in groves and packing 

houses in the export program. APHIS may monitor places of production, 

packinghouses and records if necessary.

9. All fruit imported into the United States must be accompanied by a phytosanitary

certificate (PC) with an additional declaration (AD) issued by DGSA stating that 

the fruit in the consignment are free of all quarantine insects (South American 

fruit fly, Med fly, Honeydew moth and Citrus borer) and have been produced in 

accordance with the requirements of the systems approach.

10. APHIS will inspect fruit consignments at the port of entry to the United States.

11. DGSA must monitor and audit the harvesting system and ensure that during the 

time the packinghouse is in use for exporting fruit to the United States, the 

packinghouse may only 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 azoxystrobin) at labeled rates, and waxed at packinghouses.

13. DGSA will certify that places of production from exporting orchards have 

effective fruit fly trapping programs, and follow pest control guidelines, when 

necessary, to reduce regulated pest populations. The personnel conducting the 

trapping and pest surveys must be hired, trained, and supervised by DGSA or 

personnel authorized by the DGSA. 

14. Beginning at least 1 year before harvest begins and continuing throughout the 

year, trapping in the orchards for fruit fly monitoring must be at a density of at 

least 2 traps per km2in commercial production areas, with at least 2 traps placed 

in each place of production. Traps should be baited with APHIS-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 fly is

trapped, pesticide bait treatments must be applied in the affected place of 

production in order for the place of production to remain eligible to export fruit.

16. DGSA must keep records of fruit fly 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 (except 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 APHIS 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 by a pest-proof screen or plastic 

tarpaulin while in transit to the packinghouse and while awaiting packing. All 

openings to the outside of the packinghouse must be covered by 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 the 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 by APHIS 

and DGSA, 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 single 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 phytosanitary 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 they 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 essential 

components of good agricultural practices and are mainstays 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 (Gómez 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 systems 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. APHIS may monitor the production areas and packing houses 

if necessary.

The phytosanitary certificate with additional declaration requires DGSA to conduct an 

inspection and certify that the citrus fruit are free of quarantine insects (South American 

fruit fly, Medfly, honeydew moth and citrus 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 currently approved by USDA for Xcc and SOS

decontamination of regulated citrus fruit moved within the United States: sodium 

hypochlorite, SOPP (sodium orthophenyl phenate) and peroxyacetic acid (CFR, 2006; 

USDA, 2011b; USDA APHIS. 2010a.). Various studies demonstrated the effectiveness 

of these disinfectants in reducing numbers of X. citri subsp. citri cells or similar bacteria 
7

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

al., 2000; Rybak & Canteros, 2001; CFR, 2006; CFR, 2007). The same surface 

disinfectants were recently approved by USDA for SOS (USDA, 2011a). Packing house 

treatments such as waxing, surface disinfection 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. Traceback and registered production sites allow backtracking of pest problems and remedial 

mitigation or removal of production sites or areas from the program.

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 surface 

disinfectant in accordance with 7 CFR part 305, and be free of leaves, twigs, and other 

debris. In October 2009, APHIS amended these regulations to remove some previous 

restrictions based on a pest risk analysis that concluded that "commercially packed 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, interstate movement of citrus fruit from SOS infested areas requires that 

fruit must be washed, brushed, surface disinfected (with at least one approved treatment), 

fungicide treated with labeled rates of imazalil, thiabendazole or combination of 

fludioxonil plus azoxystrobin and waxed at packinghouses (USDA, 2011a). Equivalent 

measures will be required for importation of Citrus and Fortunella fruit from Uruguay.

Citrus fruits except lemons may only 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 by cold treatment 

(Schedule T108-a) are all approved for disinfesting citrus of Ceratitis capitata and 

Anastrepha fraterculus (USDA, 2011b). 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 lowering 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, 2008), and 

research has shown that if lemons 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, 2012).

Based on the pest damage symptoms, 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, 2011b, 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 citrus from Uruguay.

Summary

APHIS believes that the risk management measures discussed in this document will 

provide an appropriate level of phytosanitary protection against the pests of quarantine 

concern associated with the importation of fresh Citrus and Fortunella 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 carefully examined field practices and 

procedures to determine which ones provide the most effective means of preventing the 

spread of citrus canker disease via the movement of commercial citrus fruit. The RMA 

treatments 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; USDA, 2011a).

Trapping and bait spraying will further ensure that fruit fly populations will be low. 

Packinghouse culling and fruit removal from orchards will remove any senescent fruit,

which are more likely to be hosts to fruit flies.

Gymnandrosoma auranianum 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, 2012). 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 by APHIS in citrus fruit 

(AQAS-PestID, 2012). Based on the pest damage symptoms, inspection and culling will 

remove Lepidoptera pests from the pathway (Parra et al., 2001; 2004; Silva & Mexia, 

1999).
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Uruguay has exported citrus fruits to the European Union for many years. The 

phytosanitary measures currently in place in Uruguay (USDA, 2012) for export to the 

European Union have been proposed by Uruguay to be the basis for a systems approach 

for the importation of citrus fruit to the continental United States. APHIS agrees with 

some of the proposed measures and proposes additional measures, which are included in

the system approach described here.

In addition to the systems approach in Uruguay, Customs and Border Protection officials 

will inspect fruit from Uruguay at ports of entry to prevent symptomatic or infested fruit 

from entering the United States.

 

Authors

Walter Gould Ph.D. 

Senior Risk Manager

José R. Hernández Ph.D.

Risk Manager
10

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Parra, J. R. P., J. M. S. Bento, M. S. Garcia, P. T. Yamamoto, E. F. Vilela, and W. S. 

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clementina Hort. ex Tanaka, C. deliciosa Ten., C. unshiu Marcow.), Citrus Hybrids, and 

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Appendix 1. 

Table 1. The mitigations that are effective for each pest. All mitigations are necessary as part of the 

systems 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 

aurantianum

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 X
Table 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