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



# Importation of Fresh Mango **( Mangifera indica** **) Fruit from Australia into the**  **Continental United States** 

# Risk Management Docum **ent**

**June 23 , 201**  **1** Ver. 00 8

**United States Department of Agriculture Animal and Plant Health Inspection Service**  **Agency Contact: Donna.L.West@aphis.usda.gov**2

**Introduction** The Government of Australia (GOA) requested permission to import mango ( Mangifera indica L. ) fruit into the continental United States (U.S.). Mangoes are currently enterable into the U.S. from India, Mexico, Philippines, Thailand, Taiwan, and countries in Central and South America (7 CFR 319.56), and from the State of Hawaii (7 CFR 318.13

- 4f) after treatment with hot water, vapor heat or irradiation (USDA, 2009 b )

. Mangoes have not been imported from Australia before, so a pathway

- initiated commodity risk assessment was conducted. A list of mango pests in Australia was prepared based on (1) documents submitted by

the GOA, (2) United States Department of Agriculture (USDA)’s Animal and Plant Health Inspection Service (APHIS) records of intercepted pests, and (3) scientific literature. The pest risk assessment (PRA) docum ent, Importation of Fresh Fruit ofMango, Mangifera indica L. , from Australia into the Continental United States identified **thirteen** insects, **seven** fungi and **one** bacterium likel y to follow the pathway of fresh mango fruit from Australia (USDA , 20 11 ). The a ssessment is based on the assumption that , as part of standard post

- harvest practices , the mangoes are cleaned and washed in packing houses for sap removal and quality enhancement (USDA, 2011)

. Insects: Bactrocera aquilonis (May) (DIPTERA:Tephritidae) Bac trocera cucumis (French) (DIPTERA:Tephritidae) Bactrocera frauenfeldi (Schiner) (DIPTERA:Tephritidae) Bactrocera jarvisi (Tryon) (DIPTERA:Tephritidae) Bactrocera kraussi ( Hardy) (DIPTERA:Tephritidae) Bactrocera murrayi (Perkins) (DIPTERA:Tephritidae) Bactrocera neohumeralis (Hardy) (DIPTERA:Tephritidae) Bactrocera opiliae (Drew and Hardy) (DIPTERA:Tephritidae) Bactrocera tryoni (Froggatt) (DIPTERA:Tephritidae) Ceratitis capitata Wiedemann (D IP TERA:Tephritidae) Ceroplastes rubens Maskell ( HEMIPTERA :Coccidae) Coccus viridis (Green) ( HEMIPTERA :Coccidae) Sternochetus mangiferae (F.) ( COLEOPTERA : Curculionidae **)** Fungi: Cytosphaera mangiferae Died

. Fusarium spp. complex associated with M ango M alformation D isease Lasiodiplodia pseudotheobromae A.J.L. Phillips, A. Al ves & Crous Neofusicoccum mangiferae (Syd. & P. Syd.) Crous, Slippers & A.J.L. Phillips Neoscytalidium novaehollandia e Pavlic, T.I

. Burgess & M.J. Wingf. Phomopsis mangiferae S. Ahmad Pseudofusicoccum adansoniae Pavlic, T.I. Burgess & M.J. Wingf. Bac t eria : Xanthomonas campestris pv. mangiferaeindicae (Patel et al .) Robbs et al

. (Xanthomonadales: Xanthomonadaceae)3

The P RA of mangoes from Australia determined that risk is high for Ceroplastes rubens , Ceratitis capitata , and the nine fruit flies in the genu s Bactrocera ; medium for Coccus viridis, Cytosphaera mangiferae, Lasiodiplodia pseudotheobromae , Neofusicoccum mangiferae , Neoscytalidium novaehollandia e, Pseudofusicoccum adansoniae , Sternochetus mangiferae, and Xanthomonas campestris pv. mangiferaeindic ae ; and low for the Fusarium spp. complex associated with M ango M alformation D isease and Phomopsis mangiferae

. According to our pest risk assessment guidelines ( USDA , 2000): for pests rated high, specific measures beyond port of entry inspection are stron gl y recommended ; for pests rated medium, specific measures beyond port of entry inspections may

be neces s ary ; and for pests rated as low, specific measures beyond port of entry inspections are not required. So, we are not recomending any specific mitigati on measure for Fusarium spp. complex associated with Mango Malformation Disease and Phomopsis mangiferae

. Australia proposed to treat mangoes with an APHIS

- approved irradiation treatment that would mitigate pathway

risks from the targeted insect pests, co ntinue appl ying post

harvest washing and cleaning practices that would mitigate risks from scale insects, and apply additional measures to mitigate risks from pathogens and other pests as required b y APHI S. All insect pests will be effectively neutralized 1 with the irradiation generic dose of 400 Gy

(USDA , 2006). The plant pathogens that are likel y to follow the pathway include six fungi, Cytosphaera mangiferae , Lasiodiplodia pseudotheobromae , Neofusicoccum mangiferae , Neoscytalidium novaehollandia e, Pseu dofusicoccum adansoniae , Phomopsis mangiferae and the Fusarium spp. complex associated with the Mango M alformation D isease , and one bacterium, Xanthomonas campestris pv. mangiferaeindicae

. These pathogens may not be effectivel y neutralized with irradiatio n and require additional measures. The proposed importation of mango fruit from Australia, if approved, would be regulated by an amendment to the existing fruits and vegetables regulations ( 7 CFR § 319.56 )

. This document outlines the phy tosanitary meas ures that APHI S will require if the proposed importation of mango es from Australia is approved , and documents the evidence used b y APHIS to conclude that these measures will effectively prevent the introduction of quarantine pests.
**Proposed Risk Mitigat ion Measures for Mangoes from Australia**  APHI S proposes that mango fruit from Australia may be imported into the continental United S tates only

under the following conditions: (a) The fruit must be commercially produced and part of a commercial consignment

. (b) The f ruit must be treated with irradiation by receiving a minimum absorbed dos e (MAD) of 400 Gy

and meet all other relevant requirements in 7 CFR 305. 9

1 A pes t is considered neutralized w hen it is killed, rendered sterile or its further development into an adult is stopped.4 including monitoring of the treatment b y APHIS inspectors. (c) One of the following options for the fungi ( Cytosphaera mangiferae, Lasiodiplodia pseudotheobromae , Neofusicoccum mangiferae , Neoscytalidium novaehollandia e, and Pseudofusicoccum adansoniae ) must be followed : (Option 1 ) the fruit must be treated with a broad spectrum post

- harvest fungicidal dip; or (Option 2 ) the fruit must originate from an orchard that was inspected prior to the beginning of harvest and the **orchard** was found free of the fungi of quarantine concern ; or (Option 3 ) the fruit must originate from an orchard that was treated with a broad spectrum fungicide during the growing season, inspected prior to harvest and the **fruit** wa s found free of the fungi of quarantine concern

. (d) Prior to departure from Australia, the fruit must be inspected by the national plant protection organization (NPPO ) of Australia and found free of Cytosphaera mangiferae, Lasiodiplodia pseudotheobromae , Neofusicoccum mangiferae , Neoscytalidium novaehollandia e, Pseudofusicoccum adansoniae and Xanthomonas campestris pv
. m angiferaeindicae. (e) If irradiation is applied outs ide the United States, e ach consignment of fruit must be inspected jointly

by APHI S and Australian officials and accompanied by a Phy tosanitary Certificate (PC) issued by the NPPO of Australia certifying that the fruit received the required irradiation tre atment. The PC must also include an additional declaration (AD) that , depending on the option implemented , would state: (1) "The fruit was subjected to a post

- harvest broad

- spectrum fungicidal dip," ( 2 ) "The fruit originated from an orchard that was insp ected prior to the beginning of harvest and the **orchard** was found free of fungi of quarantine concern " or ( 3 ) "The fruit was originated from an orchard treated with a broad

spectrum fungicide during the growing season, was inspected prior to harvest, and the **fruit** was found free of fungi of quarantine concern

. " Additionally , the PC must include an AD stating : "The fruit in this consignment was inspected prior to shipment and found free of Cytosphaera mangiferae, Lasiodiplodia pseudotheobromae , Neofusicoccum mangiferae , Neoscytalidium novaehollandia e, Pseudofusicoccum adansoniae and Xanthomonas campestris pv
. mangiferaeindicae ." (f) If irradiation is to be applied upon arrival in the United States, e ach consignment of fruit must be inspected by GOA inspectors prior to departure and accompanied by a PC issued by

the NPPO of Australia with an AD that , depending on the option chosen , would state: (1) "The fruit was subjected to a post

- harvest broad

spectrum fungicidal dip," ( 2 ) "The fruit was originated from an orc hard inspected prior to the beginning of harvest and the **orchard** was found free of fungi of quarantine concern " or ( 3 ) "The fruit was originated from an orchard treated with a broad

- spectrum fungicide during the growing season, was inspected prior to harve st, and the **fruit** was found free of fungi of quarantine concern

. " Additionally , the PC must also include an AD stating : "The fruit in this consignment was inspected prior to shipment and found free of Cytosphaera5 mangiferae, Lasiodiplodia pseudotheobromae , Neofusicoccum mangiferae , Neoscytalidium novaehollandia e, Pseudofusicoccum adansoniae, and Xanthomonas campestris pv . mangiferaeindicae ." (g) Fruits imported into the United States will also be subject to inspection at the port of entry

. **Evidence for the Effective Removal of Pests of Concern from the Pathway**  The following paragraph s summarize key mitigation measures for mango fruit from Australia and provides a general discussion of their efficacy

. They also discuss the evidence APHI S uses to determine that the measures described in Section **B** effectivel y remove pests of concern from the pathway. **Insects:** A minimum absorbed dose of 400 Gy is required by

U.S. regulations ( 7 CFR 305. 9 ) and has been determined by APHIS to be adequate to neutralize or mitig ate risks of all insect pests excluding adults and pupae in the order Lepidoptera. None of the 13 insect pests identified in the PRA as likely to follow the pathway (USDA, 2011) belong to the order Lepidoptera. Therefore the generic irradiation treatment is a valid treatment for all the insect pests of concern. Thirteen of the 21 pests likely to follow the pathway

are insects. There are no records of importing irradiated mangoes from Australia, but records since 2000 of interstate movement of mangoes fr om H awaii into the United S tates after treatment with 300 Gy irradiation dose show no interceptions of quarantine pests (USDA, 200 9 a). Over 300 consignments of Indian mangoes irradiated with 400 Gy entered into the United States since the program began in 2007 and no pest of quarantine significance has been reported (USDA , 200 9 a). Although the pest complex in Hawaii or India may be different from that described for Australian mangoes, the 400 Gy minimum absorbed dose has been determined to be effective ag ainst all insect pests except adults and pupae of the order Lepidoptera (USDA , 2006).
**Pathogens: Fungi:**  The PRA determined that the five pathogens, Cytosphaera mangiferae, Lasiodiplodia pseudotheobromae , Neofusicoccum mangiferae , Neoscytalidium novaehollandia e, Pseudofusicoccum adansoniae ( fung i ) and Xanthomonas campestris pv . mangiferaeindica (bacterium), have a medium pest risk potential , whereas the two other pathogens, Fusarium spp. associated with M ango M alformation D isease and Phomopsis mangiferae (fung i ) , have a low pest risk potential. According to our pest risk assessment guidelines (PPQ, 2000) , for pests rated with low pest risk potential , specific measures beyond port of entry inspections are not required

.6

In fection b y Cytosphaera mangiferae in the field causes a tan lesion that develop s at the stem end of the fruit after a “zonate” leaf spot initially appears on the leaves (Johnson & Hyde, 1992; Peterson, 1986 ; MAF , 2003 ). The leaf spot sy mptoms first appear as water
- soaked circular spots that later develop tan centers with dark brown borders. On the fruit, th e fungus causes slow

- spreading, tan lesions th at form initially on the stem end of the fruits and eventually spread onto the shoulder of the fruit. It can be distinguished from other fungi by the conidiomata it produces , which appear as dark pinpoints within the tan lesions ( Johnson et al. , 1993; Plo etz et al. , 1994). The fungi of quarantine concern belonging to the Family Botryosph eraceae ( Lasiodiplodia pseudotheobromae , Neofusicoccum mangiferae , Neoscytalidium novaehollandia e, and Pseudofusicoccum adansoniae ) cause watery rot that starts at the ste m end of the fruit and then pro gresses throughtout the rest of the fruit (Sakalidis et al ., 2011) , which exhibits as blemished or damaged fruit

. Host infection general l y occurs following phy sical damage or general stress (Slippers & Wingfield, 2007) , whic h may

lea d to large parts of the host plant dying . This is easil y detectable in the fiel d. H owever , fungi may be endophy

tic and express on fruits after harvest (Sakalidis et al ., 2011; Slippers & Wingfield, 2007)

. These mango pathogens can be transporte d in infected fruit or planting material, and pruning equipment can also aid in their transmission (Sakalidis et al ., 2011). In Australia, spraying of mango plants with broad spectrum fungicides during the growing season is a common practice to control fungal diseases. Additionally , the fruit that are blemished and damaged are culled by hand in the field and during the processing of commercial mango fruit. M ango fruit undergo a post

- harvest fungicide treatment as well as cleaning and washing (USDA, 2011)

. These practices , coupled with good agricultural practices, effectivel y help remov e the pathogens of concern from the pathway

. Since the intended use of mango s imported into the United States is for consumption, the probability that infec ted fruit will co me in contact with suceptible hosts and lead to disease stablishement is very low. As discussed below, pre

- harvest field inspection, o rchard application of broad spectrum fungicide , or post
- harvest fungicidal dip are required as one of three options to mi tigate the risk th e s e fungal pathogen may cause post
- harvest infections. Risk Mitgation Option 1 : The fruit is subjected to a post

- harvest broad spectrum fungicidal dip. The broad spectrum fungicidal dip treatment is one of the required options to treat Indian mangoes for Cytopshaera mangiferae , Macrophoma mangiferae , and Xanthomonas camprestris pv. mangferaeindica and , when coupled with a pre

- export inspection of the fruit , is considered sufficient to mitigate the pathway risk (USDA , 200 9 a). Shipme nt of Australian mangoes would require a PC with an AD stating that: “The fruit in this consignment was subjected to a broad spectrum fungicidal dip, inspected during the pre

- clearance activities, and found free of Cytosphaera mangiferae,7

Lasiodiplodia pse udotheobromae , Neofusicoccum mangiferae , Neoscytalidium novaehollandia e, and Pseudofusicoccum adansoniae

. ” Specificall y listing the pests on the AD o f the PC alerts APHI S inspectors to the specific pests of concern. Risk Mitigation Option 2 : A pre

- harvest or growing season inspection of the orchard coupled with pre

export inspection of the fruit are required

. Cytosphaera mangiferae and the fungi in the Botryosphaeriaceae can be easily seen and detected in the field on mango leaves and fruit during pr e - harvest inspection . Post

- harvest diseases do not occur without the presence of fungal s ymptoms on leaves in the field. The inspection must occur at a time prior to the beginning of harvest as determined b y mutual agreement between APHI S and the Austral ian NPPO for s ymptoms of Cytosphaera mangiferae and the fungi in the Botryosphaeriaceae

. Shipments of fruit must be accompanied by a PC with an AD stating that: “The fruit in this consignment originat e d from an orchad that was inspected prior to the beginning of harvest and the **orchard** was found free of Cytosphaera mangiferae, Lasiodiplodia pseudotheobromae , Neofusicoccum mangiferae , Neoscytalidium novaehollandia e, and Pseudofusicoccum adansoniae .” Risk Mitigation Option 3 : Orchard application of b road spectrum fungicide spray s protects fruit from infection by aerial spores produced on leaves or stems (Jarvis, 1992). An orchard treatment and orchard inspection, when coupled with a pre

- export inspection of the fruit and a P C with an AD stating th at fruit was inspected and found free of Cytosphaera mangiferae and the fungi in the Botryosphaeriaceae, are considered sufficient to mitigate the pathway risk of th e s e fungal pathogen s . Specificall y listing the pests on the AD o f the PC alerts APHI S inspect ors to look for the specific pests of concern. The AD will state: “The fruit in this consignment originat e d from an orchard that was treated with a broad spectrum fungicide during the growing season, was inspected prior to harvest, and the **fruit** was found free of Cytosphaera mangiferae Lasiodiplodia pseudotheobromae , Neofusicoccum mangiferae , Neoscytalidium novaehollandia e, and Pseudofusicoccum adansoniae .” **Bacteria:** Bacterial black spot or black canker caused b y Xanthomonas campestris pv . mangiferaein dica , occurs in Australia, Brazil, India, Pakistan, Taiwan, Reunion, Sudan and South Africa (CPC , 2005). Since the pathogen moves only short distances in wind

- blown aerosols (usually within orchards), the long

- distance spread of the8

pathogen depends almos t entirely upon the movement of infected plants (Manicom & Pruvost, 1994). Sy mptoms 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 gumm y 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 packinghouse would most likely

detect this pathogen. This bacterial pathogen is not generall y considered to cause a post
- harvest disease (Johnson, 1994; Singh , 2000). "The pathogen is an epiph ytic colonist of leav es (Pruvost et al. , 1990), buds (Pruvost et al. , 1993) and fruit (Pruvost & Luisetti, 1991). Infection occurs through wounds and, less often, through stomata" (Ploetz, 1997). This pest is rated as medium risk in the PRA. According to our pest risk as sessment guidelines , pests rated as medium may require specific mitigation measures beyond port of entry

inspection. Visual inspection of the fruit at the packinghouse w ill detect this pathogen. Inspection of the fruit prior to shipment and a PC with an AD that stating that the fruit was inspected and found free of evidence of the bacterium are recommended to remove this pest from the pathway

. All shipments require the following AD : ” The fruit in this consignment was inspected during pre

- clearance activi ties and found free of Xanthomonas campestris pv
. mangiferaeindicae .” As part of the U.S. requirements governing the use of irradiation as a phyt osanitary treatment (7 CFR 305. 9 ), APHI S and the NPPO of Australia will jointly develop an operational work p lan. The work plan shall incorporate details of treatment and preclearance activities , including inspection , of articles that APHI S may perform before or after the treatment. Chemical treatment and i nspection of mango fruit s for the presence of pests no t targeted b y irradiation during preclearance activities will further ensure that the pests of concern are removed from the pathway

.
**Conclusion** The phy tosanitary requirements described above include treatment to Australia’s mango fruit with irradiation using a minimum absorbed dose of 400 Gy , a pre - harvest inspection of the orchard by the Australian NPPO, treatment of the orchard with a broad spectrum fungicide during the growing season, or post
- harvest fungicidal dip of fruit, and a preclearance inspection for pests not targeted b y the irradiation treatment. APHI S concludes that , based on the evaluation of effectiveness of these measures directed against the pests of concern, the safeguards of 7 CFR § 319.56, and the9

additional mitigations described in this document , will result in the effective removal of the pests of concern identified by the PRA (USDA , 200 11 ) from the pathway of the importing fresh mango fruit from Australia.

**Authors** José R. Hernández Senior Risk Manager

- Plant Pathoilogy Walter Gould Senior Risk Manager

- Enthomology

**References** CPC. 2005

. Crop Protection Compendium 2005. CAB International, Wallingford, UK. Gagnevin, L. and I. Pruvost. 2001. Epidemiology and Control of Mango Bacterial Black Spot. Plant Disease 85: 928

- 935. Jarvis, W.R. 1992. Managing Diseases in Greenhouse Crops. APS Press, St. Paul, Minnesota, p. 130. Johnson, G., T. Cooke, A. Mead, G.I. Johnson, A.W. Cooke and A.J. Mead. 1993. In fection and quiescence of mango stem

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Pruvost, O., A. Couteau and J. Luisetti. 1990. Development of bacterial black spot of mangoes and epiph ytic populations of the pathogen ( Xanthomonas campestris pv. mangiferaeindicae ) under natural conditions in Reunion I sland. Fruits Paris 45 (2): 125

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