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



# Risk Management Document

Importation Mango Fruit, Mangifera indica , from

Jamaica into th e Continental United States

March 20, 2013

Plant Health Programs (PHP) Regulations, Permits and Manuals ( RPM )

Contact Person: Tony Román1

Introduction

USDA Animal and Plant Health Inspection Service (APHIS), Plant Protection and Quarantine (PPQ) prepared a Pest Risk Assessment ( PRA ) to evaluate the risks associated with the importation of commercially produced mango, Mangifera indica L.

, as fresh fruit from Jamaica

into the continental United States in response to a 2009 market access request fro m Jamaica (MAFJA, 2009; USDA, 2011 a ). APHIS developed the PRA for Jamaica mango based on pests

listed in the Jamaica market access request (MAFJA, 2009) , pest interception records and

available scientific literature (USDA, 20 11 a )

.

Five pests of quarantine significance were identified in the PRA , which could reasonably be expected to follow the pathway of fresh mangos imported into the continental United States from

Jamaica

. The pests of quarantine concern that can follow the pathway of mango fruit include:

Arthropods Anastrepha obliqua (Ma cquart) (Diptera: Tephritidae)

- West Indian fruit fly Anastrepha suspensa (Loew) (Diptera: Tephritidae)

- Caribbean fruit fly

Coccus moestus De Lotto ( Hemiptera: Coccidae)

- Moestus soft scale

Fungi Phomopsis mangiferae S. Ahmad (Ascomycetes: Diapor thales)

- stem end rot of mango

Bacteria Xanthomonas campestris pv. m angiferaeindicae (Patel et al . 1948) Robbs et al . 1974

– mango bacterial black spot

The pest risk assessment identified a cumulative pest risk potential of High for the fruit flies

Anas trepha obliqua and A. suspensa and Medium for the soft scale C occus moestus and plant pathogens Phomopsis mangifera, and Xanthomonas campestris pv. m angiferaeindicae

. According to the APHIS Guidelines for Pathway

- Initiated Pest Risk Assessments Version 5. 02 ( USDA , 2000), it is strongly recommended that pests receiving a rating of High are mitigated by phytosanitary measures in addition to standard port of entry inspection. Pest s rated medium may require additional phytosanitary measures beyond standard po rt of entry inspection.

APHIS will only allow the importation of commercial consignments of mangos

. The mango fruit

will be imported into the United States under the s imilar conditions as current imports of mangos

from Central America and South America

. Currently mangos from Central and South America may be imported into the United States with hot water treatment for fruit flies, or from APHIS recognized pest free areas that are free of fruit flies.

Ri sk m anagement measures2

APHIS proposes that m angos from Jamaica may be imported into the continental United States under the following conditions:

1. Only commercial consignments of mango
, M a n g i fer a indica , may be imported

. All growers must be registered with the National Plant Protection Organiz ation ( NPPO ) of Jamaica

.

2. The mangos must be treated with a n APHIS approved treatment for Anastrepha spp. fruit flies. The following treatments are available in the APHIS treatment manual for Anastrepha spp. fruit flies (USDA, 2011b)

.

A. H ot water t reatment

, T102

- a

. Each consignment of fruit treated with t he APHIS

approved hot water treatment must be pre

- cleared by APHIS inspectors in Jamaica . T he

treatment must be carried out under the supervision and direction of APHIS and e ach shipment must be in spected jointly by APHIS and the Jamaica NPPO inspectors

.

B. Irradiation treatment

, T105

. The fruit must be irradiated with a minimum absorbed

dose of 150 Gy for fruit flies and follow the requirements of 7 CFR parts 305 and 319. If the approved irradi ation treatment is applied outside the United States, e ach consignment

of fruit must be pre

- cleared by APHIS inspector s in Jamaica . If irradiation is to be applied upon arrival in the United States, e ach consignment of fruit must be inspected by

Jamaica i nspectors prior to departure and accompanied by a P hytosanitary C ertificate (PC) issued by the NPPO of Jamaica. Mangos intended to be irradiated in the United States must be shipped in packaging that prevents escape of any fruit fly larvae or adults.

3

. The mangos must be safeguarded from exposure to fruit flies from the time of treatment to export, including packag ing which prevent s access by fruit flies and other injurious insect pests. The package containing the mangos may not contain any other fru it, including mangos not qualified for importation into the United States.

4 T he fruit must be subject to a pre

- or post

- harvest fungicidal application unless the mango fruit originate from orchards which are inspected and found free of diseases

.

5

. Ea ch consignment must be inspected jointly by inspectors from APHIS and the national plant protection organization (NPPO) of Jamaica and accompanied by a Phytosanitary Certificate ( PC ) issued by NPPO of Jamaica certifying that the c onsignment was inspected a nd received the mandatory treatment . The PC mus t also include an additional declaration (AD) stating : “ T he

mangos in this consignment were inspected and found free of Phomopsis mangiferae and Xanthomonas campestris pv. mangiferaeindicae and received the re quired hot water treatment or

received irradiation treatment with 150 Gy as the minimum absorbed dose

. ”

6

. Each consignment is subject to inspection at the U

. S

. ports of entry.3

Evidence for the Effective Removal of Pests of Concern from the Pathwa y

Commercial consignments include fruit that has been grown to high standards of quality, subjected to pest control, sort ed for quality, subjected to culling, and post harvest treatments to maintain quality. Cultural, chemical, or mechanical means (e.g., field sanitation, pre

- harvest application of pesticides, resistant cultivars) should be used to eliminate pests from fields or prevent fruit infestation. Sanitation, such as removing and discarding fallen fruit and pesticide applications, as essential com ponents of good agricultural practices, are mainstays of commercial fruit production (e.g., Kirk et al ., 2001). Commercially produced fruit is thus far less likely to contain quarantine pests (USDA, 2011c).

Hot water treatments have been used to disinfes t mangos of fruit flies since 1987 (Sharp , 1994 )

. M any countries in Central and South America including Brazil, Costa Rica, Dominican Republic, Ecuador, Guatemala, Haiti, Honduras, Mexico, Nicaragua, Peru and Venezuela export mangos to the United States u sing hot water immersion treatment

. In the last three years, between 350 and 400 thousand metric tons of mangos have been imported into the United States each year from these countries, almost all using the T102a hot water treatment. The treatment is

con sidered an effective treatment for Anastrepha spp. fruit flies (USDA , 2011b)

.

The 150 gy dose was adopted by APHIS as effective against all species of Tephritid fruit flies ( IAEA, 2004 ). Irradiation has been used successfully to import fruits and vegetab les from India, Mexico, T hailand, Vietnam and other countries as well as for moving fruit interstate from Hawaii. No live fruit flies have been found in shipments of irradiated fruit, in part because of the oversight APHIS provides to these programs.

Saf eguarding provides a physical barrier to re

- infestation by fruit flies and other pests. This may include tarps, insect proof boxes or containers and double door entries to packinghouses or other

facilities. Safeguarding movement of fruit from the field t o the packinghouse, and subsequently to the place of export is standard procedure for export programs in countries where fruit flies

occur.

Any infestations of scale insects would be culled by the packing house. The hot water dip will

kill all scale i nsects on the surface of the mangos (Gould & McGuire, 2000; Hara et al ., 1996)

. Inspection at the port of entry will also readily detect scale insects

, so that fruit intended for irradiation can be inspected to detect any infestations of soft scales.

T he PRA determined that the fungus Phomopsis mangiferae h as a medium pest risk potential

. A ccording to the Guidelines for Pathway

- Initiated Pest Risk Assessment s V ersion 5.02 (USDA, 2000), for pest s rated with medium pest risk

, specific phytosanitary measu res may be necessary. Phomopsis mangiferae produces dark lesions at the stem end that penetrate the mesocarp (Ploetz,

2003 ) ; the lesions may resemble stem

- end anthracnose cause d by Colletotrichum gloeosporioides , but the latter lesions usually penetrate th e mesocarp not deeper than 10

- 20 mm and are covered by pink spore masses of the pathogen (Ploetz, 2003)

. These lesions are easily identified by inspector s at packing houses as well as at the port of entry.4

APH I S is requiring that

, unless mango fruit or iginated from orchards inspected and found free of diseases, mang o fruit must be subjected to a pre

- or post

- harvest fungicidal application. The work plan shall incorporate details on fungicide and methodology of application. Pre

- or post

harvest fungicida l application s are already being successfully used to mitig ate fungal diseases for

mangos imported from India and Pakistan into the United States ( 7 CFR § 319.56

- 46).

Bacterial black spot or black canker caused by Xanthomonas campestris pv

. mangiferaein dica occurs in Australia, Brazil, China, India, Japan, Pakistan, R é union, South Africa

, Sudan , and Taiwan ( CABI , 2005). Since the pathogen moves only short distances in wind

- blown aerosols (usually within orchards), the long

- distance spread of the pathoge n depends almost entirely upon

the movement of diseased propagati ve material. True seed transmission has not been

demonstrated (Manicom & Pruvost, 1994 ; Gagnevin & Pruvost, 2001). T his bacterial pathogen is not generally considered as a post harvest diseas e (Johnson, 1994; Singh, 2000). The pathogen is an epiphytic colonist of leaves (Manicom, 1986; Pruvost et al. , 1990), buds (Pruvost et al.

, 1993) and fruit (Pruvost & Luisetti, 1991). Infection usually occurs through wounds and less often through stomat a (Ploetz et al ., 1994).

Symptoms of Xanthomonas campestris pv

. mangiferaeindica on mango fruit consist of fruit lesions that develop into water

- soaked halos, become raised, blacken and crack open (Ploetz et
al

. , 1994). These conspicuous lesions usually produce gummy exudates and are discernible with the naked eye (Johnson et al. , 1989). Fruit susceptibility increases over time and is highest during the month preceding harvest (Gagnevin & Pruvost, 2001). Visual inspection of the fruit at the packinghou se would most likely detect this pathogen. This pest is rated as medium risk in

the PRA (USDA, 2011a) . According to our 5.02 guidelines

, pests rated as medium risk may require specific mitigation measures beyond port of entry inspection.

Inspection is a primary tool for interdicting plant pests from entering the United States. APHIS and Customs and Border Protection (CBP) intercept 1.5 million prohibited plants and plant products and 40,000 to 50,000 plant pests per year by inspection (Cavey, 2003). T he requirement of a Phytosanitary Certificate (PC) ensures that the NPPO in the country of origin inspects the commodity and the Additional Declaration (AD) lists specific pests inspected for.

The additional declaration also alert s border inspectors in th e United States to the specific pests that might be present on the commodity.

Summary

The phytosanitary requi rements described above include commercial consignments, quarantine

treatments for fruit fl ies, inspections

, and phytosanitary certification for other quarantine pests.

Th is risk management document concludes that

, based on the evaluation of effectiveness of the measures directed against the quarantine pests

, the mitigations described will result in the effective removal of the pests of concern

, which were identified by the pest risk assessment (USDA, 20 11a ) for the importation of mangos from Jamaica into the continental United States

.5

Author s

Walter Gould, Ph.D Senior Risk Manager

- Entomology

José R. Hernández, Ph.D Senior Risk Manager

- Plant Patholo gy

Mitigation Measure Evidence for removal of pests from the pathway

1. Only commercial shipments may

be i mported. All growers must be registered with the Jamaican NPPO of the exporting country. Fruit in commercial orchards are grown using good agricultural practices which reduce pest populations. Registration of orchards allows trace back and removal from the export program of orchards with pest problems.

2. Treatment with either hot water dip T102a or irradiation T105 150gy

for fruit fl ies. Both treatments provide quarantine security for fruit flies (USDA, 2011b)

. Hot water treatment also mitigates s tem end rot caused by Phomopsis mangiferae (Ploetz, 2003)

. Hot water treatment mitigates against scale insects (Gould & McGuire, 2000; Har a et al., 1996).

3. Mangos must be safeguarded from exposure to fruit flies from

treatment to export, including being packaged so as to prevent access by fruit flies and other injurious insect

pests. Packing after treatment in a pest exclusionary house and safeguarding during transit reduces the exposure of harvested mangos to infestation by

maintainin g a pest exclusionary barrier.

4. The fruit must be subjected to a

pre

- or post

- harvest fungicidal application, unless mango fruit originated from orcha rds inspected

and found free of diseases. Pre

- and post

- harvest fungicidal applications reduces stem end rot (Ploetz, 2003).

5

. Each shipment of mangos must be accompanied by a phytosanitary certificate issued by NP PO bearing the following declaration: “ the mangos in this consignment were inspected and found free of Phomopsis mangiferae and Xanthomonas campestris pv. mangiferaeindicae and received the required hot water treatment or

received irradiation treatment with 150 Gy as the minimum absorbed

dose

. ” Requiring a Phytosanitary Certificate effectively ensures inspection by the NPPO for pests of concern. The additional declaration alerts inspectors at the United States port of entry to potential pests of concern.

6 . Each shipment of mangos is subje ct to inspection at the port of entry to the United States. Inspection ensures that various stages of any pest that are present will be detected; this is particularly effective against those pests whose later life stages are larger and more readily detecte d (Borror et al.

, 1989). Inspection will readily detect infestations of soft scales. Inspection is a primary method used by APHIS and CBP to interdict plant pests upon entry to the United States (Cavey, 2003).6

References

Borror, D. J., Triplehorn, C. A. and N. F. Johnson. 1989. Introduction to the study of insects,

6 th ed. Harcourt Brace Jovanovich College Publishers, TX. CABI. 2005. Crop Protection Compendium. CAB International, Wallingford, UK. http://www.cabicompendium.org/cpc/home.asp. Cavey, J .F. 2003. Mitigating introduction of invasive plant pests in the United States. p p . 350

– 361. ( Chapter 13 ) in Invasive Species: Vectors and Management Strategies, G.M. Ruiz and

J.T. Carlton eds. Island press , Washington DC

. Gagnevin, L. and Pruvost, I. 2001. Epidemiology and Control of Mango Bacterial Black Spot.

Plant Disease 85: 928

- 935. Gould, W.P. and R.G. McGuire. 2000. Hot Water Treatment and Insecticidal Coatings for Disinfesting Limes of Mealybugs (Homoptera: Pseudococcidae) . J. Econ. Ento mol. 93:

1017

- 1020. Hara, A.H., T.Y. Hata, V.L. Tenbrink, B. K.

- S. Hu, and R.T. Kaneko. 1996. Postharvest heat treatment of red ginger flowers as a possible alternative to insecticidal dip. Postharvest Biology and Technology. 7: 137

- 144.

IAEA. 2004. Irr adiation as a phytosanitary treatment of food and agricultural commodities. Proceedings of a final research coordination meeting organized by the Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture 2002 . International Atomic Energy Agenc y. 189 pp. Johnson, G.I. 1994

. Stem

- end rot. In: Ploetz, R.C., Zentmyer, G. A., Nishijima, W., Rohrbach, K. and Ohr, H.D. (eds) Compendium of Tropical Fruit Diseases . APS Press, St. Paul, Minnesota, pp. 39

- 41. Johnson, G.I., I.F. Muirhead and L.M. Rappe l. 1989. Mango post

- harvest disease control: a review of research in Australia, Malaysia and Thailand. ASEAN Food Journal. 4 (4): 139

- 141. Kirk, K., Bessin, R., Hartman, J., O’Leary, J. and Strang, J. 2001. Total quality assurance: apple production: best m anagement practices. Kentucky Coop. Ext. Serv. ID

- 137. MAFJA. 2009. Information Requested for A Pest Risk Analysis for Mango ( Mangifera indica ) from Jamaica to the United States of America. Plant Risk Analysis Unit, Plant Quarantine/Produce and Inspection, Ministry of Agriculture and Fisheries

. Manicom, B. Q. 1986. Factors affecting bacterial black spot of mangoes caused by Xanthomonas campestris pv. Mangiferaeindicae. Ann. Appl. Biol. 109:129

- 135. Manicom, B.Q. and Pruvost, O.P. 1994

. Bacterial black spot. In: Ploetz, R.C. Zentmyer, G.A. Nishijima, W.T., Rohrbach, K.G. and Ohr, H.D. (eds) Compendium of Tropical Fruit

Diseases . APS Press, St. Paul, Minnesota, pp. 41

- 42. Ploetz, R.C. 2003. Diseases of tropical fruit crops. CAB International. 527 pp. Ploetz, R. C., Zentmyer, G. A., Nishijima, W. T., Rohrbach, K. G., and Ohr, H. D. 1994. Compendium of tropical fruit diseases. 88 pp. Pruvost, O., A. Couteau and J. Luisetti. 1990. Development of bacterial black spot of mangoes and epiphytic populations of the pathogen ( Xanthomonas campestris pv. mangiferaeindicae ) under natural conditions in Reunion Island. Fruits Paris. 45 (2): 125

- 140. Provust, O., Coutaeu, A. and Luisetti, J. 1993. Epiphytic survival of Xanthomonas campestris

pv. m angiferaeindicae on mango buds. Acta Horticulturae 341: 337

- 344.7

Pruvost, O. and J. Luisetti. 1991. Effect of time of inoculation with Xanthomonas campestris pv. mangiferaeindicae on mango fruits suscept ibility. Epiphytic survival of X. c. pv. mangiferaeindicae on mango fruits i n relation to disease development. Journal of Phytopathology. 133 (2): 139

- 151.

Sharp. J.L. 1994. Hot water immersion. p. 133

– 147 in Quarantine treatment of pests of food plants, J.L. Sharp and G.J. Hallman, eds. Westview Press, Boulder CO. Singh, R. S. 2000. Diseases of Fruit Crops. Science Publishers, Inc., Enfield, New Hampshire, pp. 153

- 182.

USDA . 2000. Guidelines for Pathway

- Initiated Pest Risk Assessments. Version 5.02. APHIS Plant Protection and Quarantine, Riverdale, Maryland.

USDA

. 20 11 a

. Importation of mango fruit

, M a ng i fer a indic a, from Jamaica into the Continental

United States

. A Qualitative, Pathway

- Initiated Pest Risk Assessment

. 64 pp. USDA. 201 1b . Treatment Manual. United States Department of Agriculture (USDA), Animal

and Plant H ealth Inspection Service (APHIS), Plant Protection and Quarantine (PPQ), Washington, D.C. http://www.aphis.usda.gov/import_export/plants/manuals/ports/treatment.sht ml Last

accessed July , 201 1.

USDA. 2011c. Plant Pest Risk Associated with Fruits and Vegetables in Passenger Baggage . A Risk Management Document. United States Department of Agriculture (USDA), Animal and Plant Health Inspection Service (APHIS), Plant Protection and Quarantine (PPQ), Washington, D.C. 9 pp.