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



## Risk Managem **ent Document**



## Importation of Fresh Pepper

**– Capsicum annuum**  **L., Capsicum baccatum**  **L., Capsicum chinense**  **Jacq .**  **, Capsicum**  **frutescens L., and**  **Capsicum pubescens Ruiz & Pav.** 

**– Fruit**  **with Stems from Central Ameri ca into the United States** 

**September 1 3**  **, 2010**

**Plant Health Programs (PHP) Regulations, Permits and Manuals (RPM)**  **Contact Person: David Lam**  **b**Rev: 7

**Introduction** This risk management document was prepared by the Animal and Plant Health Inspection Service (APHI S ) to provide risk management strategies for the importation of peppers from Central America (Costa Rica, El Salvador, Guatemala, Honduras, Nicaragua and Panama) following the development of a commodity

- based, pathway

- initiated risk analy sis ( PRA) that was conducted by the APHI S (USDA, 2009)

. In 2004, APHI S prepared a PRA to examine plant pest risks associated with the importation of fresh pepper ( Capsicum spp., specificall y the domesticated species Capsicum annuum L., C. baccatum L., C. chin ense Jacq
. , C. frutescens L. , and C. pubescens Ruiz & Pav. ) fruit with stems in response to a request by the governments of Costa Rica, El Salvador, Guatemala, Honduras and Nicaragua (USDA , 2004)

. In 2008 in response to a request from Panama , APHI S update d the pest risk assess ment document, and included Panama as an exporting country ( USDA, 2009)

. T h e PRA considered the risk associated with the import ation of several species of Capsicum ( C. annuum , C. baccatum , C. chinense, and C. frutescens ) because o f taxonomic uncertainty regarding the species status ( Walsh and Hoot, 2001 ) and because wild populations of C. annuum merge with populations of C. frutescens and C. chinense ( Eshbaugh, 1993 ). There is a wide overlap of common name usage among all domesticated Capsicum species ( Bosland, 1996 ), so two other cultivated species ( C. baccatum and C. pubescens ) were also included in the PRA (USDA, 2009)

. Tit le 7 of the Code of Federal Regulations 319 Part 56 ( 7 CFR § 319., 2007 ) provides regulatory authority for the importation of fruits and vegetables from foreign sources into the United States. The PRA lists 12 quarantine pests that may follow the pathway of fresh peppers fruit with stems from Costa Rica, El Salvador, Guatemala, Honduras, Nicaragua and Panama into the United States (USDA, 2009) . The pests include eight insects, one bacterium , one fungus , and two viruses

. **Insects** Anastrepha ludens (Loew) (Diptera: Tephritidae)

- Mexfly Ceratitis capitata Wiedemann ( Diptera: Tep hritidae )

- Medfl y Faustinus ovatipennis (Champion) ( Coleoptera: Curculionidae )

- weevil Liriomyza huidobrensis (Blanchard) ( Diptera: Agromy zidae )

– pea leafminer Neoleucinodes elegantalis (Guenée) ( Lepidoptera: Crambidae )

– tomato fruit borer Phenacoccus parvus Morrison ( Hemiptera: Pseudococcidae )

– lantana mealy bug Planococcus minor (Maskell) ( Hemiptera: Pseudococcidae )

– passion vine mealy bug Thrips palmi Karny ( Th ysanoptera: Thripidae )

– melon thrips **Bacterium** Ralstonia solanacearum race 3 biovar 2 (S mith) Yabuuchi et al. ( Burkholderiales ) **Fungus**Rev: 7

Puccinia pampeana Speg. (Urediniom ycet es: Uredinales )

– rust fungus **Viruses** Andean potato mottle virus (APMoV) ( Comoviridae ) Tomato severe leaf curl virus (ToSL CV) ( Geminiviridae ) \ The pest risk potential was rated **Low** for the bacterium and **H igh**  of all of other pests.

**Table 1. Pest**  **geographic distribution**

Costa Rica El Salvador Guatemala Honduras Nicaragua Panama Anastrepha ludens X X X X X X Ceratitis capitata X X X X X X Faustinus ovatipennis X X Liriomyza huidobrensis X X X X X X Neoleucinodes elegantalis X X Phenacoccus parvus X X X Planococcus minor X X X Thrips palmi X X X X X X Ralstonia solanacearum race 3 biovar 2 X X Puccinia pampeana X X Andean potato mottle virus (APMoV) X X X Tomato severe leaf curl virus (ToSL CV) X X XRev: 7

**Risk Mitigation Measures**  The current requirements for the importation of peppers from certain Central American countries are listed in the Code of Federal Regulations § 31 9.56

- 40 **.** The addition of Panama as an importing country in the PRA (USDA, 2009) did not significantl y change the pest list and therefore the risk mitigations are the same

. In the revised PRA , Capsicum sp . is reported as a minor host for Opogana sacchari (banana moth)

. However , there have been no interceptions of O

. sacchari associated with Capsicum sp . imports. Therefore , Opogona sacchari is now listed a s not follow ing the pathway of fresh pepper fruit s, and has been removed from the list of pests that are inspected for in the risk mitigations below

. T omato yellow mosaic virus has also been dropped from the previous list of pests (see USDA, 2009) and the Bacterial wilt ( Ralstonia solanacearum race 3 biovar 2 ) , and T omato severe leaf curl virus were added to the pest list ( see USDA, 2009)

. In reference to item “c” below, the PRA indicated that the only field host of Mexican fruit fly

( A. ludens ) is C

. pubescens

. Capsicum annuum is a host of A. Ludens , and other Anastrepha sp p. , such as A. distincta , A

. o blique , and A. serpentine , but only under laboratory

conditions with artificial infestation ; so those species were not included in the PRA and hence mitigation measures are not included in the risk management document. The PRA found no evidence that A

. lu dens or the other species affect C

. annuum in the field. Since f ruit of Ralstonia solanacearum race 3 biovar 2 susceptible solanaceous crops, such as peppers and tomatoes , only rarel y contain the pathogen (Sanchez

- Perez et al ., 200 8 ) , the pest risk potential is considered to be low (USDA, 2009)

. T he United S tates currently allows import s of tomatoes and pepper fruits from Central American countries where R. solanacearum R3 B2 occurs . APHIS regulates the importation of plant s for planting ( 7 CFR 319.37

- 2 ) but do es not regulate the importation of fruits. No mitigation for Ralstonia solanacearum race 3 biovar 2 is required. **Mitigation measures for the importation of p epper**  **fruit s**  **with steams from certain Central**  **Am erican countries**  **(7 CFR 319.56 -**  **40) .**  Fresh pepper ( Capsicum spp.) fruits with stems may be imported into the United States from Costa Rica, El Salvador, Guatemala, Honduras , Nicaragua and Panama only under the following conditions and in accordance with all other applicable provisions of this subpart: (a) For peppers of the species Capsicum annuum , Capsicum baccatum , Capsicum chinense, and Capsicum frutescens from areas free of Me diterranean fruit fl y (Medfl y) entry requirements are as follows: (1) The peppers must be grown and packed in an area that has been determined by APHI S to be free of Medfl y in accordance with the procedures described in §319.56

– 5 of this subpart. (2) A pre

- harvest inspection of the growing site must be conducted b y the national plant protection organization (NPPO) of the exporting country for the pests that occur in those countries (from table 1 ), the weevil Faustinus ovatipennis , pea leafminer, tomato fruit borer, lantana meal ybug, passionvine meal ybug, melon thrips, the rust fungus Puccinia pampeana , and the viruses An dean potato mottle virus and Tomato severe leaf curl virus ) ; if any of these pests ,Rev: 7

or other quarantine pests, are found to be infesting or infecting the production site, the NPPO may not allow export from that production site until the NPPO has determined that risk mitigation has been achieved. (3) The peppers must be packed in insect

- proof cartons or containers or covered with insect

proof mesh or plastic tarpaulin at the packinghouse for transit to the United States. These safeguards must remain intact until arrival in the United States. (4) The exporting country's NPPO is responsible for export certification, inspection, and issuance of phy tosanitary certificates. Each consignment of peppers must be accompanied by a phy tosanitary certificate issued by the NPPO and bearing the declaration, “These peppers were grown in an area recognized to be free of Medfl y and have been inspected and found free of the pests listed in the requirements.” (b) For peppers of the species Capsicum annuum , Capsicum baccatum , Capsicum chinense , Capsicum frutescens , and Capsicum pubescens from areas in which Medfly is present: (1) The peppers must be grown in approved production sites registered with the NPPO of the exporting country . Initial approval of the production sites wi ll be completed jointly by the exporting country's NPPO and APHIS. The exporting country's NPPO will visit and inspect the production sites monthly, starting 2 months before harvest and continuing through until the end of the shipping season. APHI S may mon itor the production sites at any time during this period. (2) Pepper production sites must consist of pest

- exclusionary greenhouses, which must have double self

- closing doors and have all other openings and vents covered with 1.6 mm (or less) screening. (3) Registered sites must contain traps for the detection of Medfl y both within and around the production site. (i) Traps with approved protein bait must be placed inside the greenhouses at a density of four traps per hectare, with a minimum of two traps per greenhouse. Traps must be serviced on a weekl y basis. (ii) If a single Medfly

is detected inside a registered production site or in a consignment, the registered production site will lose its ability to export peppers to the United States until APHI S and the exporting country's NPPO mutually determine that risk mitigation is achieved. (iii) Medfly

traps with an approved lure must be placed inside a buffer area 500 meters wide around the registered production site, at a density of 1 trap per 10 hectare s and a minimum of 10 traps. These traps must be checked at least every 7 day s. At least one of these traps must be near the greenhouse. Traps must be set for at least 2 months before export and trapping must continue to the end of the harvest. (iv) Capture of 0.7 or more Medflies per trap per week will delay or suspend the harvest, depending on whether harvest has begun, for consignments of peppers from that production siteRev: 7

until APHI S and the exporting country's NPPO can agree that the pest risk has been mitigated. (v) The greenhouse must be inspected prior to harvest for the weevil Faustinus ovatipennis , pea leafminer, tomato fruit borer, lantana meal ybug, passionvine meal ybug, melon thrips, the rust fungus Puccinia pampeana , and the viruses Andean potato mottle virus and Tomato severe leaf curl virus (if present in the country , according to table 1 ) . If any of these pests or other quarantine pests are found to be generally infesting or infecting the greenhouse, export from that production site will be h alted until the exporting country's NPPO determines that the pest risk has been mitigated. (4) The exporting country's NPPO must maintain records of trap placement, checking of traps, and any Medfl y captures. The exporting country's NPPO must maintain an APHI S

- approved quality control program to monitor or audit the trapping program. The trapping records must be maintained for APHIS' review. (5) The peppers must be packed within 24 hours of harvest in a pest

- exclusionary packinghouse. The peppers must be safeguarded b y an insect

- proof mesh screen or plastic tarpaulin while in transit to the packinghouse and while awaiting packing. Peppers must be packed in insect

- proof cartons or containers, or covered with insect

- proof mesh or plastic tarpaulin for trans it to the United States. These safeguards must remain intact until arrival in the United States or the consignment will be denied entry into the United States. (6) During the time the packinghouse is in use for exporting peppers to the United States, the packinghouse may

accept peppers onl y from registered approved production sites. (7) The exporting country's NPPO is responsible for export certification, inspection, and issuance of phy tosanitary certificates. Each consignment of peppers must be accompani ed b y a phy tosanitary certificate issued by

the NPPO of the exporting country bearing the declaration, “These peppers were grown in an approved production site and the consignment has been inspected and found free of the pests listed in the requirements.” The shipping box must be labeled with the identity

of the production site. (c) For peppers of the species Capsicum pubescens from areas in which Mexican fruit fly (Mexfly) is considered to exist: (1) The peppers must be grown in approved production sites registered with the NPPO of the exporting country . Initial approval of the production sites will be completed jointly by the exporting country's NPPO and APHIS. The exporting country's NPPO must visit and inspect the production sites monthly, starting 2 m onths before harvest and continuing through until the end of the shipping season. APHI S may monitor the production sites at any time during this period. (2) Pepper production sites must consist of pest

- exclusionary greenhouses, which must have double self

- closing doors and have all other openings and vents covered with 1.6 mm (or less) screening. (3) Registered sites must contain traps for the detection of Mexfly both within and around theRev: 7

production site. (i) Traps with approved protein bait must be pla ced inside the greenhouses at a density of four traps per hectare, with a minimum of two traps per greenhouse. Traps must be serviced on a weekl y basis. (ii) If a single Mexfly

is detected inside a registered production site or in a consignment, the regis tered production site will lose its ability to ship under the s ys tems approach until APHI S and the exporting country's NPPO mutually determine that risk mitigation is achieved. (iii) Mexfly

traps with approved protein bait must be placed inside a buffer area 500 meters wide around the registered production site, at a density of 1 trap per 10 hectares and a minimum of 10 traps. These traps must be checked at least every 7 day s. At least one of these traps must be near the greenhouse. Traps must be set for at least 2 months before export, and trapping must continue to the end of the harvest. (iv) Capture of 0.7 or more Mexflies per trap per week will delay or suspend the harvest, depending on whether harvest has begun, for consignments of peppers from that p roduction site until APHI S and the exporting country's NPPO can agree that the pest risk has been mitigated. (v) The greenhouse must be inspected prior to harvest for the weevil Faustinus ovatipennis , pea leafminer, tomato fruit borer, lantana meal ybug, p assionvine meal ybug, melon thrips, the rust fungus Puccinia pampeana , and the viruses Andean potato mottle virus and Tomato severe leaf curl virus (if present in the country , according to table 1 ) . If any of these pests or other quarantine pests are found to be infesting or infecting the greenhouse, export from that production site will be halted until the exporting country's NPPO determines that the pest risk has been mitigated. (4) The exporting country's NPPO must maintain records of trap placement, che cking of traps, and any Mexfly captures. The exporting country's NPPO must maintain an APHI S

- approved quality control program to monitor or audit the trapping program. The trapping records must be maintained for APHIS' review. (5) The peppers must be packed within 24 hours of harvest in a pest

- exclusionary packinghouse. The peppers must be safeguarded b y an insect

- proof mesh screen or plastic tarpaulin while in transit to the packinghouse and while awaiting packing. Peppers must be packed in insect

- proof c artons or containers, or covered with insect

- proof mesh or plastic tarpaulin, for transit to the United States. These safeguards must remain intact until arrival or the consignment will be denied entry

into the United States. (6) During the time the packi nghouse is in use for exporting peppers to the United States, the packinghouse may

accept peppers onl y from registered approved production sites. (7) The exporting country's NPPO is responsible for export certification, inspection, and issuance of phy tosanitary certificates. Each consignment of peppers must be accompanied by a phy tosanitary certificate issued by

the NPPO of the exporting country bearing the declaration,Rev: 7

“These peppers were grown in an approved production site and have been inspected and fo und free of the pests listed in the requirements.” The shipping box must be labeled with the identity of the production site. **Efficacy of**  **Risk M itigation**  **Measures** Establishment of pest

- free places of production obviates the need for post

- harvest commo dity treatments to achieve phy tosanitary security ( IP PC 1996; 1999). Pest free places of production have been used successfully to prevent infestation by Mediterranean fruit fly (Medfl y) for peppers of the species Capsicum annuum , Capsicum baccatum , Capsi cum chinense, and Capsicum frutescens in Costa Rica, El Salvador, Guatemala, Honduras, and Nicaragua since 2005
. No pests of quarantine significance have been intercepted b y APHIS on peppers imported using this sy stems approach (Pest ID, 2008)

. Puccini a pampeana produce s conspicuous s ymptoms and signs (Agrios, 2004; Hernández & Hennen, 200 3; Lindquist, 1982 ) that are easil y recognizable on inspections in the Central American shipping country as well as at U.S. port s of entry inspections. Andean potato mottle virus and Tomato severe leaf curl virus were rated as high risk potential in the PRA , but their likelihood of establishment (contact with host material) is low . S ince they are not transmitted by seeds and transmitted mainly by vectors ( Diabrotica b alteata and Bemisia tabaci ) (Pernezn y et al., 2003), with historically few vector interceptions on peppers (USDA, 2009), we consider pre

harvest inspection of the growing site an appropriate mitigation. I f the sites are found to be infected, the NPPO may allow to export from the production site only after the determination that the risk mitigation has been achieved

. Central American fresh peppers produced under this sy stems approach will also be subject to packing house inspection and inspection by the D epartment of Homeland Security Customs and Border Protection (CBP) at the U.S. ports of entry
. In fested or infected fruit will be rejected, and traceback will be accomplished by APHIS and the NPPO of the originating country to identify and correct problems including removal of the packinghouse or area of produ ction from the export program. A sy stems approach can provide an alternative to single measures to meet the appropriate level of ph yt osanitary protection, or can be developed to provide phy tosanitary p rotection in situations in which no single measure is available (IPPC, 2002). Fresh peppers from Costa Rica, El Salvador, Guatemala, Honduras, and Nicaragua have been produced and exported to the United States under a s ys tems approach for fruit flies for over four ye ars (USDA, 2004) with no interceptions of program pests ( Pest ID , 200 8 ). Pest
- exclusionary

greenhouses remove pests from production sites ( 7 CFR § 319.56

- 40 (b) (2) ) and culling removes damaged and infest ed /infected fruit at the packing house

. As part of a sy stems approach these measures are effective at lowering pest populations. No fruit flies have been intercepted on produce coming from pest exclusionary structures in any

of the programs for peppers or tomatoes. **Summary**Rev: 7

There are several risk management measures available for the high

- risk pests identified above that will permit the importation of pepper from Central America while satisfying the appropriate level of ph yt osanitary

protection for the United States. A s ys tems approach utili zing pest

exclusion greenhouse as described above , employing a combination of measures acting independentl y, also mitigates risk and provides an acceptable level of phytosanitary protection. P est
- free places of production as well as packinghouse and port of entry inspections provide the level of ph yt osanitary

security required b y the United States.
**Au thors**  Walter Gould, Senior Risk Manager APHI S

- PPQ Jos é R. Hern ández, Senior Risk Manager APHI S

- PPQ David B. Lamb, Import Specialist APHI S

- PPQ
**Referenc es** 
7 CFR § 319. 2007. Code of Federal Regulations, Title 7, Part 319 (7 CFR §319.56

- Fruit and Vegetable Quarantine Regulations). Agrios, G. N. 2004. Plant Pathology . Fifth Edition. Department of Plant Pathology University

of Florida, Elsevier Academic Press, San Diego. 922 pp. Bosland, P. W. 1996. Capsicums: Innovative uses of an ancient crop. Pages 479

- 487 in J. Janick, (ed.). Progress in new crops. ASHS Press, Arlington, VA. U.S.A. Eshbaugh, W. H. 1993. Peppers: History and exploitation of a seren dipitous new crop discovery

. Pages 132

- 139 in J. Janick and J. E. Simon, (eds.). New Crops. Wiley , New York, U.S.A. Hernández, J.R. and Hennen J.F. 2003. Rust fungi causing galls, witch’s brooms, and other abnormal plant growths in Northwestern Argentina. Mycologia 95:728

- 755. IPPC. 1996. Requirements for the establishment of pest free areas. International Standards for Phy tosanitary Measures No. 4. Rome: Secretariat of the International Plant Protection Convention, United Nations Food and Agriculture Organization.Rev: 7

IPPC. 1999. Requirements for the establishment of pest free places of production and pest free production sites. International Standards for Phy tosanitary Measures No. 10. Rome: Secretariat of the International Plant Protection Convention, Uni ted Nations Food and Agriculture Organization. IPPC. 2002. The use of integrated measures in a systems approach for pest risk management. International Standards for Phy tosanitary Measures No. 14. Rome: Secretariat of the International Plant Protection C onvention, United Nations Food and Agriculture Organization. Lindquist J.C. 1982. Royas de la República Argentina y zonas limítrofes. Instituto Nacional de Tecnología Agropecuaria. Buenos Aires. 574 pp. Pernezny , K., P. D. Roberts, J. F. Murphy , and N. P . Goldberg (eds.). 2003. Compendium of Pepper Diseases. APS Press, St. Paul, MN. PestID. 2008. Pest I dentification Database (PestID). United States Department of Agriculture, Animal and Plant Health Inspection Service, Plant Protection and Quarantine. http s://mokcs14.aphis.usda.gov/aqas/login.jsp. (Archived at PERAL). Sanchez Perez, A., L. Mejia, M. Fegan, and C. Allen. 2008. Diversity and distribution of Ralstonia solanacearum strains in Guatemala and rare occurrence of tomato fruit infection. Plant Path ology 57(2):320

- 331. USDA. 2004. Importation of fresh pepper fruit with steams ( Capsicum annum L. , C. fru tescens L., C. baccatum L., C. pubescens Ruiz & Pav., and C. chinense Jacq.) from Costa Rica, El Salvador, Guatemala, Honduras, and Nicaragua into the United States. A Qualitative, Pathway

- Initiated Risk Assessment. October 27, 2004. Plant Epidemiology and Risk Analy ses Laboratory , Center of Plant Health Science and Technology , Plant Protection and Quarantine. Ani m al and Plant Health Inspection Service. USDA . 2009. Importation of Fresh Pepper

- Capsicum annuum L., Capsicum baccatum L., Capsicum chinense Jacq, Capsicum frutescens L., and Capsicum pubescens Ruiz & Pav.

- Fruit with Stems from Central America into the United States. A Qualitative, Pathway

Initiated Risk Anal ys is. April 27 , 2009. Plant Epidemiology and Risk Analy sis Laboratory , Center for Plant Health Science and Technology , Plant Protection and Quarantine, Animal and Plant Health Inspection Service. Walsh, B. M., and S. B. Hoot. 2001. Phyl ogenetic relationships of Capsicum (Solanaceae) using DNA sequences from two noncoding regions: the chloroplast atpB

- rbcL spacer region and nuclear wax y introns. International Journal of Plant Sciences 1 62 :1409

- 1418.