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

Risk Management Document

Importation of Banana, Musa spp., as Fresh, Hard Green Fruit from the to Guam, , and the Northern Mariana Islands

February 13, 2013

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

Introduction

A Pest Risk Assessment (PRA) was submitted by the Philippine Bureau of Plant Industry (BPI) to Animal and Plant Health Inspection Service (APHIS) in December 2005 in support of a market access request for Philippine green bananas to Guam (BPI, 2005). This pest risk assessment was prepared for Dole Philippines, Inc., Dole Asia Ltd., Makati, Philippines. In May 2007, BPI amended the market access request to include Hawaii and the Northern Mariana Islands.

APHIS reviewed the relevant literature and pest interception records and revised the PRA submitted by BPI (USDA, 2012a). The APHIS pest list identified 62 quarantine pests of banana which might potentially follow the pathway of fresh green bananas from the Philippines:

Taxa Pest Acari: Tenuipalpidae Brevipalpus californicus (Banks) Brevipalpus phoenicis (Geijskes) Coleoptera: Anthribidae Araecerus coffeae (Fabricius) Coleoptera: Cerambycidae alternans Wiedemann Coleoptera: Curculionidae Metamasius hemipterus Linnaeus Philicoptus waltoni (Boheman) Coleoptera: Scarabaeidae Scapanes australis Boisduval Diptera: Muscidae Atherigona orientalis Schiner Diptera: Tephritidae Bactrocera occipitalis (Bezzi) Bactrocera philippinensis Drew and Hancock Bactrocera musae (Tryon) Diptera: Stratiomyidae Hermetia illucens (Linnaeus) Hemiptera: Aphididae Rhopalosiphum padi Linnaeus Hemiptera: Coccidae Ceroplastes cirripediformis Comstock Ceroplastes rubens Maskell Coccus longulus (Douglas) Hemiptera: Coreidae Leptoglossus gonagra (Fabricius) Hemiptera: Diaspididae Aonidiella aurantii (Maskell) Aonidiella comperei McKenzie Aonidiella orientalis (Newstead) Aspidiotus coryphae Cockerell and Robinson Aspidiotus excisus Green Chrysomphalus aonidum (Linnaeus) Hemiberlesia lataniae (Signoret) Hemiberlesia palmae (Cockerell) Hemiberlesia rapax (Comstock)

2 Taxa Pest Lepidosaphes beckii (Newman) Lepidosaphes similis Beardsley Mycetaspis personata (Comstock) Parlatoria proteus (Curtis) Pinnaspis aspidistrae aspidistrae (Signoret) Pinnaspis buxi (BouchT) Pinnaspis musae Takagi Pinnsaspis strachani (Cooley) Pseudaulacaspis cockerelli (Cooley) Selenaspidus articulatus (Morgan) Unaspis citri (Comstock) Arthropods Hemiptera: Margarodidae Icerya aegyptiaca Douglas Icerya pulcher (Leonardi) Icerya seychellanum (Westwood) Hemiptera: Pentatomidae Tessaratoma papillosa (Drury) Hemiptera: Pseudococcidae Geococcus coffeae Green Maconellicoccus hirsutus (Green) Planococcus lilacinus (Cockerell) Pseudococcus cryptus Hempel Pseudococcus jackbeardsleyi Gimpel and Miller Pseudococcus longispinus (Targioni Tozzetti) Rastrococcus invadens Williams Rastrococcus spinosus (Robinson) Lepidoptera: Limacodidae Parasa lepida (Cramer) Lepidoptera: Noctuidae Agrotis ipsilon (Hufnagel) Spodoptera exigua (Hubner) Lepidoptera: Pyralidae Diaphania indica (Saunders) Orthoptera: Acrididae Chondracris rosea (DeGeer) Locusta migratoria (Linnaeus) Melicodes tenebrosa Walker Valanga nigricornis Burmeister Thysanoptera: Thripidae Hercinothrips femoralis (Reuter) Thrips florum Schmutz Thrips hawaiiensis (Morgan) Mollusca Achitinidae Achatina fulica Bowdich Weed Imperata cylindrica (L.) Beauv. Bacteria Burkholderiales: Ralstonia solanacearum (Smith) Yabuuchi et al., Burkholdericeae Race 2, Biovar 1

Since the PRA was developed APHIS has deregulated several pests including:

3 Chaetanaphothrips signipennis (Bagnall), Planococcus minor (Maskell) and (Wiedemann) and these pests have been removed from the RMD (USDA, 2012b). The pests listed in this RMD are all expected to be excluded from the pathway of fresh hard green bananas by mitigation measures that are standard industry practices in the Philippines (BPI, 2005; USDA, 2012a). The mitigation measures expected to exclude these pests are from the following list provided to APHIS by BPI (BPI, 2005).

Industry Standard Practices

A list of industry standard practices for banana production in the Philippines was submitted to APHIS by BPI (BPI, 2005). BPI indicated that these are standard industry practices, and they will mitigate all risk from pests in green bananas from the Philippines. These practices include the following:

a) Use of tissue culture (tc) seedlings in new plantings. Tc seedlings are relatively free from and disease pests. b) Excellent weed management to limit proliferation of insect and disease pests. c) Pseudostem sanitation to eliminate refuse and breeding sites of insect pests. d) Fruit obstruction removal (FOR) to prevent fruit damage as well as eliminate bridges that may be utilized by the pests to infest the fiuit. e) Insecticidal bud injection to kill the banana flower thrips. f ) Insecticide spray on the pseudostem to eliminate insect pests i.e., mealybugs, aphids, etc. g) Regular bunch spray containing insecticide to prevent mealybugs and scale from colonizing the developing fruit bunch. This spray would eliminate fruit flies if present. h) Chlorpyrifos-impregnated polyethylene (PE) bags are used to cover the fruit bunches after bunch spray to further prevent mealybug, scale and fruit fly insect infestation on the fruit. Bags also prevent from disease infections. i) Additional Chlorpyrifos-impregnated PE material (in a form of "strip" or "square") is installed on the fruit as additional control against insect pests when needed. j) Bunches for harvest are identified or tagged one (1) day before harvest in an operation called "pre-calibration". Bunches, in the process, are inspected likewise for the presence of insect pests. Bunches with mealybugs, scales, other insect and disease damage are discarded during harvest. k) Upon arrival of the fruit at the packing plant, fruit bunches are sprayed with highpressure water to eliminate any possible, although highly improbable, mealybug infestation. 1) While bunches are waiting to be de-handed, the “fruit inspector” in the packing plant will check for insect damage, particularly mealybug infestation, on individual bunches. m) During de-handing, individual hands are thoroughly inspected by the "de-hander" for possible mealybug infestation and any other evidence of insect damage.

4 n) After de-handing, individual hands are thoroughly cleaned with soap and water by the fruit selectors and further brushed with high-pressure water to eliminate possible infestation of mealybugs. o) The individual hands are again inspected to confirm freedom from mealybugs and other insects during weighing and immediately before packing inside the box. p) Unused pallets and those that are clean, dry and free from trash, soil, weed seeds and non-weed contaminants are utilized by the industry. q) Fruits stay in the wharf no more than 3 hours before being loaded in the vessel or into cold storage. Wharf areas are maintained, kept clean and are situated away from population areas and farms. Regular cleaning of wharf is done to prevent any source of contamination on exportable fruits. r) Vessels are cleaned with the recommended disinfectant before loading. Some vessels use ozone for disinfection between loads.

Some of these practices are viewed as necessary by APHIS and will be included as required risk mitigations. APHIS will also require some additional mitigations that are not on this list provided by BPI.

Risk Management Measures - Systems approach for green bananas

The following mitifgation measures are required for the systems approach for fresh green bananas. Monitoring and Oversight. The NPPO of the Philippines must provide a workplan to APHIS that details the activities that the NPPO of Philippines will, subject to APHIS’ approval of the workplan, carry out to meet the requirements of the systems approach and specific quarantine treatments that may be required. APHIS will be directly involved with BPI in monitoring and auditing implementation of the systems approach and/or any quarantine treatments.

The NPPO of the Philippines must visit and inspect registered places of production starting when fruit bags are emplaced and continuing until the end of the shipping season, to verify that the growers are complying with the requirements of the systems approach including following pest management guidelines and fruit bagging.

In addition to conducting inspections at the packinghouses, the NPPO of the Philippines must monitor packinghouse operations to verify that the packinghouses are complying with the requirements of the systems approach.

If the NPPO of the Philippines determines 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 the NPPO of the Philippines conduct an investigation and appropriate remedial actions have been implemented.

The NPPO of the Philippines must review and maintain all forms and documents related to export program activities in places of production and packinghouses for at least 1 year and, as

5 requested, provide them to APHIS for review.

Registered places of production. Bananas must be grown in places of production that are registered with the NPPO of the Philippines. To register, the places of production must provide Philippine's NPPO with the following information: Grower, exporter, orchard, and places of production name, region, township, province, locality, area planted to each fruit, and approximate date of harvest. Registration must be renewed annually. The NPPO of the Philippines will certify that each place of production follows pest control guidelines to reduce regulated pest populations. APHIS may monitor the places of production if necessary. Registration of places of production will allow trace back to the places of production if pest problems are found on fruit shipped to the United States. Problem places of production can then be removed from the program until further mitigation measures have been taken to reduce pest populations.

Traceability. Harvested bananas must be placed in field cartons or containers that are marked to show the official registration number of the places of production. The place of production where the bananas were grown must remain identifiable when the fruit leaves the place of production, at the packinghouse, and throughout the export process. Fruit presented for inspection at the United States port of entry must be identified in the shipping documents accompanying each lot of fruit to specify the places of production or sites in which the fruit was produced, and the packing house or houses in which the fruit was processed. This identification must be maintained until the fruit is released for entry into the United States.

Place of production pest management program including covering bananas with pesticide impregnated bags. Each place of production must follow a pest management program specified by the NPPO to reduce populations of quarantine pests. This includes applying pesticides to reduce pest populations and bagging bananas after flower drop with plastic bags impregnated with pesticides. If at any time during the growing period when the bag is covering the fruit, the bag falls off, or the bag is torn so that fruit flies can enter, that fruit is no longer eligible for export to the United States.

Fruit fly population monitoring and management for low prevalence places of production. Low prevalence will be used as part of a systems approach to mitigate risk from Bactrocera species fruit flies. Procedures for the establishment and maintenance of areas of low pest prevalence must comply with international standards (NAPPO, 2003; IPPC, 2005). Beginning at least three months before harvest begins and continuing through the completion of harvest, trapping in the places production of banana for Bactrocera fruit fly species must be conducted with at least 1 trap per 0.2 km2 by the NPPO. APHIS-approved traps baited with APHIS- approved baits must be used and serviced at least once every 2 weeks. If more than 2.0 FTD (number of fruit flies per trap per day) fruit flies are trapped, pesticide bait treatments (or bait stations) must be applied in the affected place of production in order for the place of production to remain eligible to export bananas. The NPPO keeps records of fruit fly detections for each trap, updates the records each time the traps are checked, and makes the records available to APHIS inspectors upon request. The records must be maintained for at least 1 year after harvest.

6 Bananas harvested hard green (no color break or yellow visible). The bananas must be harvested at a mature green state. None of the bananas harvested for export may be at or past color break (turning yellow). Damaged fruit must not be harvested for export.

Safeguarding. Bananas must be safeguarded from exposure to fruit flies from harvest to export, including being packaged so as to prevent access by fruit fly and other injurious insect pests.

Packing houses. Packing houses must prevent the entry of pests (pest exclusionary packing houses) with double-door entry and other measures designed to exclude fruit flies and other pests of quarantine concern. The packinghouse operations for export of bananas must be monitored by Phillipine NPPO. No other fruit is allowed in a packing house during the time export fruit is being packed.

Post-harvest processing. After harvest all damaged or diseased fruits must be culled at the packinghouse. Fruit will be washed with a high pressure water spray, dehanded and washed with soap and water. Fruit for export must be packed into new, clean boxes, crates or other packing materials.

NPPO Inspection. Fruit must be inspected in the Philippines at an APHIS-approved inspection site under the direction of BPI inspectors, following any post-harvest processing. A sample of boxes from each consignment must be selected by BPI at a rate to be mutually agreed upon by BPI and APHIS. The fruit from these boxes must be visually inspected for quarantine pests. A portion of the fruit being inspected must be cut to detect internally feeding quarantine pests.

Phytosanitary certificate. Each consignment of fruit must be accompanied by a phytosanitary certificate issued by the NPPO of the Philippines that contains an additional declaration stating that “the fruit in the consignment was grown and packed in accordance with the approved systems approach and inspected and found free of quarantine pests”.

Port of Entry Inspection. Fruit must be inspected at the first United States port of entry by Customs and Border Protection (CBP) inspectors from the Department of Homeland Security (DHS). A sample of boxes from each consignment will be inspected for quarantine pests. If significant intereceptions of quarantine pests occur, APHIS may ask BPI to suspend those places of production pending the result of an investigation by BPI when they may either be removed from the program or required to take remedial measures.

Efficacy of Risk Management Measures

There are several measures available for mitigating the pests of concern from bananas from the Philppines. The measures chosen for risk management on bananas from the Philippines are summarized in Table 1.

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Table 1. Summary of risk management measures that are components of a systems approach for bananas from the Philippines to Guam, Hawaii and the Northern Mariana Islands. Measure(s) Pests Efficacy Monitoring and All pests, but must be These measures are standard for many import Oversight used in conjunction with programs and assist in maintaining quality of the other measures as part of program. a systems approach. Registered Places of All pests, but must be Places of production are registered to effectively Production used in conjunction with maintain quality control and traceback. other measures as part of a systems approach. Traceability All pests, but must be Traceability allows track back to places of production used in conjunction with if pests are found by inspection at the port of arrival other measures as part of to the United States. Places of production with a systems approach. quarantine pests can be removed from the program. Places of production All pests, but must be Registration of places of production is required to Registration used in conjunction with manage places of production requirements and other measures as part of restrict access to the program to qualified sites. a systems approach. Commercially grown consignments from registered places of production use good agricultural practices to reduce or eliminate pests. APHIS pest interception database indicates that commercial consignments are much less likely to have pest interceptions than non-commercial consignments or passenger baggage. Place of production registration is part of traceability that allows track back to places of production if pests are found by inspection at the port of arrival to the United States. Places of production with pests of quarantine concern can be removed from the program. Place of production All pests, but must be Pesticide impregnated bags are industry standard pest management used in conjunction with practices in Central and South America production of program including other measures as part of bananas (Matlock & de la Cruz, 2003; Polidoro et al., bananas covered with a systems approach. 2008; Simmonds, 1966). These bags reduce the pesticide impregnated Bagging also mitigates number of quarantine pests that may follow the bags. against all pests pathway of bananas. Bagging also mitigates the and some diseases such bacterial disease Ralstonia solanacearum Race 2 as Ralstonia Biovar 1 (Hayward, 2006; Jones, 2000; PCARRC, solanacearum. 2006; Soguilon et al., 1995).

8 Table 1. Summary of risk management measures that are components of a systems approach for bananas from the Philippines to Guam, Hawaii and the Northern Mariana Islands. Measure(s) Pests Efficacy Fruit fly population Bactrocera spp. fruit flies Several species of Bactrocera including Bactrocera monitoring and musae, B. occipitalis, and B. philippinensis are management for low present in the Philippines that may attack bananas. prevalence places of Bananas and especially green bananas are generally production. considered to be poor hosts to most species of fruit flies; however, B. musae is recorded as attacking green bananas. Fruit fly trapping and management is a key component part of low prevalence systems approaches for many commodities including tomatoes and peppers grown in pest exclusionary structures, and the papaya systems approach from Central and South America (Title 7, Code of Federal Regulations, 319.56-25, 28, 31 and 40). Bananas harvested Bactrocera spp. fruit flies Harvesting bananas at a hard green stage is a hard green (no color standard industry practice for banana production in break or yellow Central and South America, Hawaii, and most of the visible). world. Ripe bananas are much more likely to be infested with Tephritid fruit flies (Armstrong, 1983; 2001; Allwood & Drew, 1996). Safeguarding – fruit is Bactrocera spp. fruit flies Safeguarding is standard for any import program protected during where the fruit is a host to fruit flies. Most fruits transit from infestation become more susceptible to infestation after harvest by pests. and safeguarding prevents infestation, for example tomatoes from various countries and Mexican avocados (Title 7, Code of Federal Regulations, 319.56-28 and 30). Packinghouses All pests, but specifically Pest exclusionary packinghouses are a standard for Bactrocera spp. fruit APHIS requirement for import programs where the flies. fruit is fruit fly host material, for example the Mexican avocado program uses this risk mitigation (Title 7, Code of Federal Regulations, 319.56-30). Postharvest All pests, but must be Banana postharvest processing includes washing Processing used in conjunction with that removes surface pests such as mites, scale other measures as part of insects, mealybugs and any other surface feeding a systems approach. pests, and culling that removes any visible pests and damaged and diseased fruit (BPI, 2005). NPPO inspection All pests, but must be Inspections are recognized as an important part of a used in conjunction with pest management program (Kahn & Mathur 1999). other measures as part of Trained inspectors can recognize infestations of a systems approach. pests and the damage or diseases they cause to the fruits which would allow detection of these pests in some cases (CABI, 2007; NAPPO, 1998; USDA, 1982; USDA, 2004; Whittle, 1986) Phytosanitary All pests, but must be Requiring a phytosanitary certificate requires the certification used in conjunction with NPPO to inspect the bananas for pests. other measures as part of a systems approach.

9 Table 1. Summary of risk management measures that are components of a systems approach for bananas from the Philippines to Guam, Hawaii and the Northern Mariana Islands. Measure(s) Pests Efficacy Phytosanitary All pests, but must be Inspections are recognized as an important part of a inspection at port of used in conjunction with pest management program (Kahn and Mathur, entry other measures as part of 1999). Trained inspectors can recognize infestations a systems approach. of pest and the damage or disease they cause to the fruits which would allow detection of these pests in some cases (CABI, 2007; NAPPO, 1998; USDA, 1982; USDA, 2004; Whittle, 1986).

Summary

Bananas are exported from Central and South America and Hawaii using most of the components described in this systems approach for bananas from the Philippines. Over 3.8 to 4 million metric tons of bananas have been imported into the United States every year from 2003 to 2007 (NASS, 2008). Given the huge amount of fruit imported, the number of pest interceptions is very small, with about 1,400 interceptions of actionable quarantine pests in that time period for bananas worldwide (AQAS-PestID, 2012). The majority of these interceptions are mealybugs, scarabeid and weevils. The Scarabeids and weevils intercepted are not internally feeding on bananas, but are adult hitchhikers. Mealybugs are external feeders that are readily detected by inspection at the port of entry.

APHIS has intercepted only four of the 62 quarantine pests listed in the PRA (AQAS-PestID, 2012) in bananas from all sources including passenger baggage and commercial cargo in the past five years. These interceptions include Metasimius hemipterus, Maconellicoccus hirsutus and Planococcus lilacinus; however, the volume of bananas imported is very large. APHIS has no records of interceptions of Ralstonia solanacearum on bananas from any source (AQAS-PestID. 2012). In the proposed Philippine banana systems approach, any place of production with interceptions of quarantine pests can be either removed from the program or required to take remedial measures.

According to BPI, bananas are currently exported from the Philippines to Japan using part of the systems approach listed here (BPI, 2005). According to BPI, no quarantine pests have been intercepted using this approach.

APHIS concludes that commercial consignments of Philippine bananas may safely be imported into Guam, Hawaii and the Northern Mariana Islands without the risk of introducing pests using the combination of the mitigations in the systems approach listed above.

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Authors

José R. Hernández, Ph.D. Senior Risk Manager Regulations, Permits and Manuals

Walter Gould, Ph.D. Senior Risk Manager Regulations, Permits and Manuals

References

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11 Kahn, R. P. and S. B. Mathur. 1999. Containment Facilities and Safeguards. American Phytopathological Society, St. Paul, MN. 213 pp. Matlock, R.B. and R. de la Cruz. 2003. Ants as indicators of pesticide impacts in banana. Environmental Entomology 32: 816-829. NAPPO. 1998. Surveillance for quarantine fruit flies (in a portion of a generally infested area). NAPPO Regional Standards for Phytosanitary Measures No. 10. Ottawa: Secretariat of the North American Plant Protection Organization. NAPPO. 2003. Guidelines for the Establishment, Maintenance and Verification of Areas of Low Pest Prevalence for Insects. NAPPO Regional Standards for Phytosanitary Measures No. 20. Ottawa: Secretariat of the North American Plant Protection Organization. NASS. 2008. National Agricultural Statistics Service. Hawaii bananas annual summary 2007. http://www.nass.usda.gov/hi/fruit/xban07.pdf PCARRD. 2006. Control of “bugtok” disease in “saba” banana. Philippine Organic Agriculture Information Network. Philippine Council for Agriculture, Forestry and Natural Resources Research and Development. Accessed June 27, 2011 at: http://pcarrd.dost.gov.ph/phil- organic/Technologies/control%20bugtok.htm. Polidoro, B.A., R.M. Dahlquist, L.E. Castillo, M.J. Morra, E. Somarriba and N.A. Bosque-Pérez. 2008. Pesticide application practices, pest knowledge, and cost-benefits of plantain production in the Bribri-Cabécar Indigenous Territories, Costa Rica. Environmental Research 108: 98-106. Simmonds, N. E. 1966. Bananas. 2nd edition. Longman, London. 512 pp. Soguilon, C. E., Magnaye, L. V., and Natural, M. P. 1995. Bugtok Disease of Banana. Musa Disease Fact Sheet No 6. International Network for the Improvement of Banana and Plantain, Montpellier, France. USDA. 1982. Pests Not Known to Occur in the United States or of Limited Distribution, No. 24: Rice Cutworm. USDA, APHIS, PPQ, Hyattsville, MD. 8 pp. USDA. 2000. Guidelines for Pathway-Initiated Pest Risk Assessments. Version 5.02. USDA, APHIS, PPQ. Riverdale, MD. 30 pp. USDA. 2004. Agricultural Quarantine Inspection Monitoring (AQIM) Handbook. USDA- APHIS, PPQ; http://www.aphis.usda.gov/ppq/manuals/port/AQIM_Chapters.htm [accessed July 2009]. USDA. 2012a. Importation of Banana, Musa spp., as Fresh, Hard Green Fruit from the Philippines to Guam, Hawaii and the Northern Mariana Islands. January, 2012 Rev. 002. USDA, APHIS, PPQ, CPHST, Raleigh, NC. 52 pp. USDA. 2012b. Official Control - The Federally Recognized State Managed Phytosanitary Program. Pests No Longer Regulated per FRSMP Evaluation. http://www.aphis.usda.gov/plant_health/plant_pest_info/frsmp/non-reg-pests.shtml access October 2012. Whittle, K. 1986. Pests Not Known to Occur in the United States or of Limited Distribution No. 74: Cabbage Moth- Mamestra brassicae L. September 1986. USDA, APHIS, PPQ. Hyattsville, MD. 15 pp.

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