Importation of Passion fruit (Passiflora spp.) from ... · Importation of Passion fruit (Passiflora...

Importation of Passion fruit (Passiflora spp.) from Ecuador

into the continental United States

A Qualitative, Pathway-Initiated Pest Risk Assessment

December 2, 2014

Version 2

Agency Contact:

Plant Epidemiology and Risk Analysis Laboratory

Center for Plant Health Science and Technology

United States Department of Agriculture

Animal and Plant Health Inspection Service

Plant Protection and Quarantine

1730 Varsity Drive, Suite 300

Raleigh, NC 27606

Pest Risk Assessment for Passiflora spp. from Ecuador

Ver. 2 December 2, 2014 i

Executive Summary

The Animal and Plant Health Inspection Service (APHIS) of the United States Department of

Agriculture (USDA) prepared this risk assessment document to examine plant pest risks

associated with importing commercially produced fruit of passion fruit, Passiflora spp.

(Passifloraceae), for consumption from Ecuador into the continental United States. Based on the

market access request from Ecuador, we considered the pathway to include the following

processes and conditions: harvest by hand and culling in the packinghouse. No washing or other

post-harvest treatments are indicated. All processes and conditions considered during the risk

assessment process become mandatory conditions for entry of the commodity.

Based on the scientific literature, port-of-entry pest interception data, and information from the

government of Ecuador, we developed a list of all potential pests with actionable regulatory

status for the continental United States that are known to occur in Ecuador and that are known to

be associated with the commodity plant species anywhere in the world. From this list, we

identified and further analyzed six organisms that have a reasonable likelihood of being

associated with the commodity following harvesting from the field and prior to any post-harvest

processing.

Of the pests selected for further analysis, we determined that the following are not candidates for

risk management, because there is no endangered area within the continental United States:

Anastrepha curitis and A. dissimilis (Diptera: Tephritidae).

We determined that the following pests are candidates for risk management, because they met

the threshold to likely cause unacceptable consequences of introduction, and they received

an overall likelihood of introduction risk rating above Negligible:

Pest type Taxonomy Scientific name Likelihood of Introduction

overall rating

Arthropods Diptera: Anastrepha fraterculus (Wiedemann) High

Tephritidae Anastrepha pseudoparallela Loew Medium

Anastrepha striata Schiner High

Ceratitis capitata (Wiedemann) Medium

Detailed examination and choice of appropriate phytosanitary measures to mitigate pest risk are

part of the pest risk management phase within APHIS and are not addressed in this document.


Ver. 2 December 2, 2014 ii

Table of Contents

Executive Summary ....................................................................................................................... i

1. Introduction ............................................................................................................................... 1 1.1. Background .......................................................................................................................... 1 1.2. Initiating event ...................................................................................................................... 1 1.3. Determination of the necessity of a weed risk assessment for the commodity .................... 2 1.4. Description of the pathway................................................................................................... 2

2. Pest List and Pest Categorization ............................................................................................ 3 2.1. Pests considered but not included on the pest list ................................................................ 4 2.2. Pest list ................................................................................................................................. 7

2.3. Pests selected for further analysis ...................................................................................... 15

3. Assessing Pest Risk Potential ................................................................................................. 16 3.1. Introduction ........................................................................................................................ 16

3.2. Assessment results .............................................................................................................. 17

4. Summary and Conclusions of Risk Assessment ................................................................... 31

5. Acknowledgements ................................................................................................................. 32

6. Literature Cited ...................................................................................................................... 32

7. Appendix A. Pests with non-actionable regulatory status .................................................. 41


Ver. 2 December 2, 2014 1

1. Introduction

1.1. Background

This document was prepared by the Plant Epidemiology and Risk Analysis Laboratory of the

Center for Plant Health Science and Technology, USDA Animal and Plant Health Inspection

Service (APHIS), Plant Protection and Quarantine (PPQ), to evaluate the risks associated with

the importation of commercially produced fresh fruit of passion fruit (Passiflora spp. L.) for

consumption from Ecuador into the continental United States.

The International Plant Protection Convention (IPPC) provides guidance for conducting pest risk

analyses. The methods used here are consistent with guidelines provided by the IPPC,

specifically the International Standard for Phytosanitary Measures (ISPM) on “Pest Risk

Analysis for Quarantine Pests, Including Analysis of Environmental Risks and Living Modified

Organisms” (IPPC, 2013). The use of biological and phytosanitary terms is consistent with the

“Glossary of Phytosanitary Terms” (IPPC, 2012).

Three stages of pest risk analysis are described in international standards: Stage 1, Initiation;

Stage 2, Risk Assessment; and Stage 3, Risk Management. This document satisfies the

requirements of Stages 1 and 2.

This is a qualitative risk assessment. We express the risk based on qualitative ratings for the

likelihood and consequences of pest introduction via imported passion fruit (granadilla) from

Ecuador. The details of the methodology and rating criteria are found in the Guidelines for Plant

Pest Risk Assessment of Imported Fruit and Vegetable Commodities, Version 6.0 (PPQ, 2012).

The appropriate risk management strategy for a particular pest depends on the risk posed by that

pest. Identification of appropriate phytosanitary measures to mitigate pest risk is undertaken in

Stage 3 (Risk Management) and is not covered in this risk assessment. Risk management will be

specified in a separate document.

1.2. Initiating event

The importation of fruits and vegetables for consumption into the United States is regulated

under Title 7 of the Code of Federal Regulations, Part 319.56 (7 CFR §319.56) (2012).

Currently, under this regulation, the entry of granadilla from Ecuador into the continental United

States is not authorized. This assessment was prepared in response to a request from Dr.

Francisco A. Jácome Robalino (Agencia Ecuatoriana de Aseguramiento de la Calidad del Agro –

AGROCALIDAD) to change the Federal Regulation to allow entry of Passiflora ligularis

(Robalino, 2009). Further consideration by APHIS and AGROCALIDAD resulted in an

expansion of this pest risk assessment to include all Passiflora species that may be exported

(Cabezas, 2013).



1.3. Determination of the necessity of a weed risk assessment for the commodity

In some cases, the imported commodity may have the potential of becoming invasive in the pest

risk analysis (PRA) area. The likelihood that this may happen is evaluated in a weed risk

assessment, conducted separately from the commodity risk assessment.

We determined that a weed risk assessment is not needed for granadilla because it is already

enterable into the PRA area from other countries. Passion fruit (Passiflora spp.) is authorized for

entry into the United States from Bermuda, from Tasmania in Australia (prohibited entry into

Hawaii), and from New Zealand (prohibited entry into Hawaii). Passion fruit is accepted from

Chile with treatment T102-b-2, a soapy water and wax treatment for the Chilean mite,

Brevipalpus chilensis (APHIS, 2013).

1.4. Description of the pathway

The IPPC (2011) defines a pathway as “any means that allows the entry or spread of a pest.” In

the context of commodity pest risk assessments, the pathway is the commodity to be imported,

together with all the processes the commodity undergoes that may have an impact on pest risk. In

this risk assessment, the specific pathway of concern is the importation of fresh fruit of passion

fruit (Passiflora spp. L.) for consumption from Ecuador into the continental United States; the

movement of this commodity provides a potential pathway for the introduction and/or spread of

plant pests.

The following description of this pathway focuses on the conditions that may affect plant pest

risk, including morphological and physiological characteristics of the commodity, as well

processes the commodity will undergo from production in Ecuador through importation and

distribution in the continental United States. These conditions provided the basis for creating the

pest list and assessing the likelihood of introduction of the pests selected for further analysis;

therefore, all components of the pathway, as they are described below, should be considered

mandatory conditions for importation of the commodity.

1.4.1. Description of the commodity

The granadilla plant is a vine. Its leaves are 8 to 16 cm in length, cordiform, glabrous, and

slightly purple on the underside (Leon, 1987). In the Andes, it is usually grown between 1600

and 2200 meters above sea level. Commercial-size plantations exist in the countries where it is

grown (Bernal, 1994). It is very well known and liked, and quite common and popular in the

Andean countries, but with few exceptions, it is not grown outside of this region.

The fruit is 6-7.5 cm long, broad-elliptic, green with purple tint and has tiny whitish dots when

unripe. When ripe, the fruit is orange-yellow with white specks (Morton, 1987). The exterior is a

little hard and brittle, and the interior of the mesocarp is cottony soft (Leon, 1987). The pulp is

mucilaginous, whitish, translucent, and juicy and has within it 200 to 250 blackish seeds per fruit

(CRFG, 2009).



1.4.2. Production and harvest procedures in the exporting area

Outside of harvesting of fruit by hand (Rodas, 2012), no information regarding production and

harvesting procedures in Ecuador was specified.

1.4.3. Post-harvest procedures in the exporting area

In the packinghouse, fruit is culled and classified according to size, weight, ripeness, and

external physical appearance (Rodas, 2012). No washing is performed, in an effort to reduce fruit

damage (Rodas, 2012). Fruits are packed in cardboard boxes for shipment (Rodas, 2012).

1.4.4. Shipping and storage conditions

Shipping and storage conditions were not specified by Ecuador. However, according to

McGregor (1987), passion fruit is typically shipped at 7-10°C (45-50°F) at 95 percent relative

humidity. In these conditions, transit and storage life for passion fruit is expected to be 3-5 weeks

(McGregor, 1987).

1.4.5. Summary of the pathway

The figure below summarizes the pathway of concern: the importation of fresh fruit of passion

fruit (Passiflora spp.) for consumption from Ecuador into the continental United States.

Figure 1. Pathway diagram for imports of Passiflora spp. from Ecuador into the continental

United States.

2. Pest List and Pest Categorization

In this section, we identify the plant pests with actionable regulatory status for the continental

United States that could potentially become established in the continental United States as a

result of the importation of passion fruit (Passiflora spp.) from Ecuador, and we determine which

of these pests meet the criteria for further analysis. Pests are considered to be of regulatory

significance if they are actionable at U.S. ports-of-entry. Actionable pests include quarantine

pests, pests considered for or under official control, and pests that require evaluation for

regulatory action.



2.1. Pests considered but not included on the pest list

2.1.1. Pests with weak evidence for association with the commodity or for presence in the export

area

Anastrepha grandis: This insect is listed as a pest of Passiflora alata with no references

provided (Weems, 1990). A few other sources indicate that this host association may be

considered doubtful (e.g., Norrbom et al., 2012; USDA Fruit Fly Host Plant Database). No other

indication of host association could be found; therefore, this species is not included on the pest

list.

Anastrepha obliqua: This insect is listed as a pest of Passiflora quadrangularis with no

references provided (CABI, 2013; Maes, 2004). Weems and Steck (2012) state that A. obliqua

has been reared experimentally from P. quadrangularis. Anastrepha obliqua is a major pest,

widespread in Mexico, Central and South America, and the West Indies (CABI, 2013). Research

regarding the host range and impact for this species is abundant. Despite this, no field host

associations could be found, and this species is not included on the pest list.

Ascochyta passiflorae: Ascochyta passiflorae was intercepted with fruit of Passiflora species in

baggage or store from Ecuador 113 times between 1984 and 1998 (PestID, 2013), with no

records more recent than 1998. Based on a thorough literature review, including review of

specific recent Passiflora diseases reports (e.g., Fischer and Rezende, 2008; Joy and Sherin,

2012; Liberato and Zerbini, n.d.; Lozano et al., 2007), we were unable to find any information

indicating that A. passiflorae is considered to be a pest in Passiflora production. The lack of field

evidence suggests that this is a post-harvest disease potentially associated with Passiflora. There

is no information available regarding the pathogenicity of A. passiflorae. Additionally, there

appears to be some taxonomic confusion, as indicated by the following note in the Fungal

Databases: “This species was excluded by Melnik (1977) from Ascochyta, but its generic affinity

is unknown” (Farr and Rossman, 2013). For these reasons, A. passiflorae is not considered to be

a pest in commercial production of Passiflora and is not included on the list.

Dasiops brenneri: This species is described as a pest of Passiflora flowers in Ecuador (García,

2011). However, no describing authority could be determined, and the name may not be valid.

For this reason, it is not included on the pest list.

2.1.2. Organisms with non-actionable regulatory status

We found evidence of the organisms listed in Appendix A being associated with passion fruit

and being present in the Ecuador; however, because these organisms have non-actionable

regulatory status for the continental United States, we did not include them in Table 2 of this risk

assessment.

2.1.3. Organisms identified only to the genus level

In commodity import risk assessments, the taxonomic unit for pests selected for evaluation

beyond the pest categorization stage is usually the species (IPPC, 2011), as assessments focus on

organisms for which biological information is available. Therefore, generally, we do not assess

risk for organisms identified only to the genus level, in particular if the genus in question is

reported in the import area. Often there are many species within a genus, and we cannot know if



the unidentified species occurs in the import area and, consequently, whether it has actionable

regulatory status for the import area. On the other hand, if the genus in question is absent from

the import area, any unidentified organisms in the genus can have actionable status; however,

because such an organism has not been fully identified, we cannot properly analyze its likelihood

and consequences of introduction.

In light of these issues, we usually do not include organisms identified only to the genus level in

the main pest list. Instead, we address them separately in this sub-section. The information here

can be used by risk managers to determine if measures beyond those intended to mitigate fully

identified pests are warranted. Often, however, the development of detailed assessments for

known pests that inhabit a variety of ecological niches, such as internal fruit feeders or foliage

pests, allows effective mitigation measures to eliminate the known organisms as well as similar

but incompletely identified organisms that inhabit the same niche.

Table 1. Organisms identified to the genus level that are reported on Passiflora spp. in Ecuador and that

have actionable or undetermined regulatory status.

Pest name Evidence of

presence on

Passiflora spp.

in Ecuador

Genus

present in

continental

United

States?

Regulatory

status1

Plant part(s)

association2

On harvested

plant

part(s)?3

Remarks

ARTHROPODS

Acari: Tetranychidae

Tetranychus

spp.

Rogg, 2000 Yes (CABI,

2013)

U Leaves (Rogg,

2000)

No

Coleoptera: Chrysomelidae

Epitrix sp. Friesen et al.,

2008

Yes (CABI,

2013)

U Leaves (Friesen

et al., 2008)

No

Lactica sp. Friesen et al.,

2008

Yes (Furth,

2006)

U Flowers, leaves

(Friesen et al.,

2008)

No

Paralactica sp. Friesen et al.,

2008

No A Flowers, leaves

(Friesen et al.,

2008)

No

Coleoptera: Curculionidae

Naupactus sp. Rogg, 2000 Yes (Dixon,

2008)

U Stem (Rogg,

2000)

No

1 A=Actionable, U=Undetermined. If the genus does not occur in the continental United States, the organism has actionable

status. If the genus occurs in the continental United States, the organism has undetermined regulatory status, because we

cannot know if the unidentified species is one that occurs in the continental United States. 2 The plant part(s) listed are those for the plant species under analysis. If the information is extrapolated, such as from plant

part association on other plant species, this is noted. 3 “Yes” indicates the pest has a reasonable likelihood of being associated with the harvested plant part(s).




presence on

Passiflora spp.

in Ecuador

Genus

present in

continental

United

States?

Regulatory

status1

Plant part(s)

association2

On harvested

plant

part(s)?3

Remarks

Diptera: Lonchaeidae

Dasiops spp. Rogg, 2000 Yes

(MacGowan

, 2013)

U Flower buds

(Aguiar-

Menezes et al.,

2002)

No

Neosilba sp. Friesen et al.,

2008

Yes

(MacGowan

, 2013)

U Immature fruit

(Friesen et al.,

2008)

No

Diptera: Mycetophilidae

Mycetophila

spp.

Friesen et al.,

2008

Yes

(Cresswell,

2009)

U Flower buds

(Friesen et al.,

2008)

No

Diptera: Tephritidae

Anastrepha spp. Rogg, 2000;

MAG-IICA,

2001

Yes (CABI,

2013)

U Fruit (CABI,

2013)

Yes

Hemiptera: Cicadellidae

Empoasca spp. García, 2011 Yes (CABI,

2013)

U Leaves (García,

2011)

No

Hymenoptera: Apidae

Trigona sp. Rogg, 2000 No A Flowers (Rogg,

2000)

No

Hymenoptera: Formicidae

Solenopsis spp. Rogg, 2000 Yes (CABI,

2013)

U Flowers, roots

(Rogg, 2000)

No

Lepidoptera: Noctuidae

Copitarsia sp. Friesen et al.,

2008

No A Flower buds,

leaves (Friesen

et al., 2008)

No

Lepidoptera: Nymphalidae

Agraulis spp. García, 2011 Yes (CABI,

2013)

U Leaves (García,

2011)

No

Heliconius sp. Rogg, 2000 Yes (Beltrán

et al., 2010)

U Leaves (Aguiar-

Menezes et al.,

2002)

No

BACTERIA

Xanthomonas

sp.

MAG-IICA,

2001

Yes (CABI,

2013)

U Leaves, fruit

(Goncalves and

Rosato, 2000)

Yes

FUNGI

Ascochyta sp. García, 2011 Yes (CABI,

2013)

U Leaves (García,

2011)

No




presence on

Passiflora spp.

in Ecuador

Genus

present in

continental

United

States?

Regulatory

status1

Plant part(s)

association2

On harvested

plant

part(s)?3

Remarks

Botrytis sp. MAG, 1986;

MAG-IICA,

2001; Rogg,

2000

Yes (CABI,

2013)

U Immature fruit

(Kagiwata,

1990)

No Affected fruit

fall from the

tree

(Kagiwata,

1990) and are

not likely to

be harvested.

Colletotrichum

sp.

MAG, 1986;

MAG-IICA,

2001

Yes (CABI,

2013)

U Leaf, flowers,

immature fruit,

stem (Fischer

and Rezende,

2008)

No Symptoms on

fruit are

conspicuous

(Fischer and

Rezende,

2008), and

infested fruit

are not likely

to remain

with the

consignment.

Fusarium sp. MAG-IICA,

2001

Yes (CABI,

2013)

U Leaves (Fischer

and Rezende,

2008)

No

Mycosphaerella

sp.

García, 2011 Yes (CABI,

2013)

U Stem (García,

2011)

No

Phomopsis sp. MAG, 1986 Yes (CABI,

2013)

U Leaves, stems,

fruit (Fischer

and Rezende,

2008)

Yes

Pseudomonas

sp.

MAG-IICA,

2001

Yes (CABI,

2013)

U Leaves

(Manicom et al.,

2003)

No

NEMATODES

Helicotylenchus

sp.

García, 2011 Yes (CABI,

2013)

U Roots (García,

2011)

No

Meloidogyne sp. García, 2011;

MAG, 1986;

Rogg, 2000

Yes (CABI,

2013)

U Roots (CABI,

2013)

No

2.2. Pest list

In Table 2, we list the actionable pests associated with passion fruit that occur in Ecuador. The

list comprises those actionable pests that occur in Ecuador on any host and are reported to be

associated with Passiflora spp. whether in Ecuador or elsewhere in the world. For each pest, we



indicate 1) the part of the imported plant species with which the pest is generally associated, and

2) whether the pest has a reasonable likelihood of being associated, in viable form, with the

commodity following harvesting from the field and prior to any post-harvest processing. We

developed this pest list based on the scientific literature, port-of-entry pest interception data, and

information provided by the government of Ecuador. Pests in shaded rows are pests identified for

further evaluation, as we consider them reasonably likely to be associated with the harvested

commodity; we summarize these pests in a separate table (Table 3).

Table 2. Actionable pests reported on Passiflora spp. (in any country) and present in Ecuador (on any

host).


presence in

Ecuador

Host status Plant part(s)

association4

On

harvested

plant

part(s)?5

Remarks

ARTHROPODS

Coleoptera: Chrysomelidae

Diabrotica

speciosa (Germar)

MAG, 1986 Walsh, 2003 Flowers, roots of

various host plants

(Walsh, 2003)

No


Philonis

passiflorae O'Brien

Rogg, 2000 Aguiar-Menezes et

al., 2002; Rogg,

2000

Stem (Aguiar-

Menezes et al.,

2002; Rogg, 2000)

No

Coleoptera: Meloidae

Epicauta atomaria

(Germar)


al., 2002

Leaf (Aguiar-

Menezes et al.,

2002)

No

Diptera: Drosophilidae

Zapriothrica nr

salebrosa Wheeler

Friesen et al.,

2008

Aguiar-Menezes et

al., 2002; Friesen

et al., 2008

Flower buds

(Aguiar-Menezes et

al., 2002; Friesen et

al., 2008)

No

4 The plant part(s) listed are those for the plant species under analysis. If the information is extrapolated, such as from plant

part association on other plant species, this is noted. 5 “Yes” indicates simply that the pest has a reasonable likelihood of being associated with the harvested commodity; the level

of pest prevalence on the harvested commodity (low, medium, or high) is qualitatively assessed in Risk Element A1 as part of

the likelihood of introduction assessment (section 3).




presence in

Ecuador


association4

On

harvested

plant

part(s)?5

Remarks

Zapriothrica nr

nudiseta Wheeler

Friesen et al.,

2008

Friesen et al., 2008 Flower buds,

immature fruit

(Friesen et al., 2008)

No This pest may be

found associated

with immature

fruit (Friesen et

al., 2008);

however, it is

primarily

associated with

host flowers

(Casanas-Arango

et al., 1996) and

is not expected

to be associated

with mature fruit

at harvest.


Dasiops caustonae

Norrbom and

McAlpine

Friesen et al.,

2008

Ávila et al., 2012;

Friesen et al., 2008

Immature fruit


No This is an

external pest

(Friesen et al.,

2008) not

expected to be

associated with

mature fruit at

harvest.

Dasiops curubae

Steyskal

Friesen et al.,

2008

Aguiar-Menezes et

al., 2002; Ávila et

al., 2012; Friesen

et al., 2008;

Gallego and

Velez, 1992

Flower buds


No

Neosilba pendula

(Bezzi) (= Silba

pendula (Bez.))


al., 2002

Flower buds

(Aguiar-Menezes et

al., 2002)

No

Diptera: Tephritidae

Anastrepha curitis

Stone

García, 2011 Aguiar-Menezes et

al., 2002; Gallego

and Velez, 1992;

García, 2011;

Zucchi and

Moraes, 2008

Fruit (García, 2011) Yes

Anastrepha

dissimilis Stone

Tigrero and

Salas, 2009

Aguiar-Menezes et

al., 2002; Zucchi

and Moraes, 2008

Fruit (Aguiar-

Menezes et al.,

2002)

Yes




presence in

Ecuador


association4

On

harvested

plant

part(s)?5

Remarks

Anastrepha

fraterculus

(Wiedemann)

Rogg, 2000;

Uchôa, 2012

Aguiar-Menezes et

al., 2002; Pirovani

et al., 2010;

Uramoto et al.,

2004; Zucchi and

Moraes, 2008

Fruit (Aguiar-

Menezes et al.,

2002)

Yes

Anastrepha

pseudoparallela

(Loew)

Tigrero and

Salas, 2009;

Uchôa, 2012

Aguiar-Menezes et

al., 2002; Raga et

al., 2011; Uchôa,

2012; Uramoto et

al., 2004; Zucchi

and Moraes, 2008

Fruit (Aguiar-

Menezes et al.,

2002)

Yes

Anastrepha striata

Schiner

CABI, 2013;

Carrejo and

González, 1994;

Uchôa, 2012

Aguiar-Menezes et

al., 2002; da Silva

et al., 2009;

Uchôa, 2012;

Zucchi and

Moraes, 2008

Fruit (Aguiar-

Menezes et al.,

2002)

Yes

Ceratitis capitata

(Wiedemann)

CABI, 2013;

Uchôa, 2012;

Rogg, 2000

Aguiar-Menezes et

al., 2002; CABI,

2013; Hill, 1983;

Liquido et al.,

1991; Raga et al.,

2011; Rogg, 2000

Fruit (Hill, 1983) Yes

Hemiptera: Aleyrodidae

Aleurocanthus

woglumi Ashby

Mound and

Halsey, 1978

CABI, 2013;

Evans, 2008;

Maes, 2004;

Mound and

Halsey, 1978

Leaves and stems of

various host plants

(CABI, 2013).

No This pest is

present in

Florida, Hawaii,

and Texas

(CABI, 2013).

Hemiptera: Pseudococcidae

Pseudococcus

landoi

(Balachowsky)

Ben-Dov et al.,

2013

Ben-Dov et al.,

2013

Leaves of various

host plants (Gimpel

and Miller, 1996)

No

Heteroptera: Coreidae

Anisoscelis

foliacea marginella

(Dallas)


al., 2002;

Rodrigues et al.,

2007; Rogg, 2000

Flowers and

immature fruit

(Rodrigues et al.,

2007; Rogg, 2000)

No This is an

external pest

(Aguiar-

Menezes et al.,

2002) not

expected to be

associated with

mature fruit at

harvest.




presence in

Ecuador


association4

On

harvested

plant

part(s)?5

Remarks

Diactor bilineatus

(Fabricius)


al., 2002; Rogg,

2000

Flowers and

immature fruit

(Rogg, 2000)

No This is an

external pest

(Aguiar-

Menezes et al.,

2002) not

expected to be

associated with

mature fruit at

harvest.

Holymenia

clavigera (Herbst)

Rogg, 2000 Rodrigues et al.,

2007; Rogg, 2000

Flowers and

immature fruit

(Rodrigues et al.,

2007; Rogg, 2000)

No This is an

external pest

(Aguiar-

Menezes et al.,

2002) not

expected to be

associated with

mature fruit at

harvest.

Heteroptera: Tingidae

Corythaica

cyathicollis (Costa)

Rogg, 2000 Schaefer and

Panizzi, 2000

Leaves of various

host plants (Schaefer

and Panizzi, 2000)

No

Gargaphia

lunulata (Mayr)

Rogg, 2000 Gallego and

Velez, 1992;

Rogg, 2000

Leaves (Rogg, 2000) No

Heteroptera: Isoptera

Microcerotermes

arboreus Emerson

Bahder et al.,

2009

Dominguez-Gil

and McPheron,

1992

Roots, stems

(Dominguez-Gil and

McPheron, 1992)

No

Lepidoptera: Arctiidae

Turuptiana

sanguinipectus

Seitz

Friesen et al.,

2008

Friesen et al., 2008 Leaves (Friesen et

al., 2008)

No

Lepidoptera: Gracillariidae

Acrocercops sp.

near pylonias

Friesen et al.,

2008


al., 2008)

No


Copitarsia

consueta (Walker)


al., 2002; Gallego

and Velez, 1992

Flowers (Aguiar-

Menezes et al.,

2002)

No

Spodoptera litura

Fabricius

Rogg, 2000 Robinson et al.,

2001

Leaves of various

host plants (CABI,

2013)

No




presence in

Ecuador


association4

On

harvested

plant

part(s)?5

Remarks

Lepidoptera: Notodontidae

Cyanotricha

necyria Felder

Friesen et al.,

2008; MAG,

1986

Friesen et al.,

2008; MAG, 1986

Leaves (Friesen et

al., 2008)

No

Josia fluonia Druce Friesen et al.,

2008


al., 2008)

No

Josia ligata group Friesen et al.,

2008


al., 2008)

No


Dione glycera C &

R Felder

Friesen et al.,

2008; MAG,

1986

Aguiar-Menezes et

al., 2002; Friesen

et al., 2008;

Gallego and

Velez, 1992;

MAG, 1986

Leaves (Friesen et

al., 2008)

No

Eueides aliphera

(Godart)

Willmott and

Hall, 2013

Aguiar-Menezes et

al., 2002; Young,

1978

Leaves (Aguiar-

Menezes et al.,

2002)

No

Eueides isabella

(Stoll)

Rogg, 2000;

Willmott and

Hall, 2013

Aguiar-Menezes et

al., 2002; Rogg,

2000; Young,

1978

Leaves (Aguiar-

Menezes et al.,

2002)

No

Eueides lybia

(Fabricius)

Willmott and

Hall, 2013

Brown, 1981;

Young, 1978

Leaves (Young,

1978)

No

Eueides procula

Doubleday (=

Heliconius

procula)

Willmott and

Hall, 2013

Causton et al.,

2000

Leaves (Causton et

al., 2000)

No

Eueides vibilia

Godart

Willmott and

Hall, 2013

Mallet and

Longino, 1982

Leaves (Mallet and

Longino, 1982)

No

Heliconius

clysonymus

Latreille

Willmott and

Hall, 2013

Brown, 1981 Leaves (Brown,

1981)

No

Heliconius cydno

Doubleday

Beltrán and

Brower, 2008;

Willmott and

Hall, 2013

Beltrán and

Brower, 2008

Leaves (Aguiar-

Menezes et al.,

2002)

No

Heliconius erato

(Linnaeus)

Willmott and

Hall, 2013

Aguiar-Menezes et

al., 2002

Leaves (Aguiar-

Menezes et al.,

2002)

No

Heliconius hecale

Fabricius (=

Papilio hecale)

Willmott and

Hall, 2013


1981)

No




presence in

Ecuador


association4

On

harvested

plant

part(s)?5

Remarks

Heliconius

hecalesia Hewitson

Willmott and

Hall, 2013


1981)

No

Heliconius

ismenius Latreille

Willmott and

Hall, 2013


1981)

No

Heliconius

melpomene

(Linnaeus)

Willmott and

Hall, 2013


1981)

No

Heliconius sapho

(Drury) Syn:

Papilio sapho

Willmott and

Hall, 2013


1981)

No

Heliconius sara

Fabricius (=

Papilio sara)

Willmott and

Hall, 2013

Aguiar-Menezes et

al., 2002; Brown,

1981

Leaves (Aguiar-

Menezes et al.,

2002)

No

Heliconius

telesiphe

Doubleday

Willmott and

Hall, 2013


1981)

No

Philaethria dido

(Linnaeus)

Constantino and

Salazar, 2010;

Willmott and

Hall, 2013

Aguiar-Menezes et

al., 2002

Leaves (Aguiar-

Menezes et al.,

2002)

No

Lepidoptera: Pyralidae

Pyrausta

perelegans

Hampson

Friesen et al.,

2008

Aguiar-Menezes et

al., 2002; Friesen

et al., 2008;

Gallego and

Velez, 1992

Flower buds, young

fruit, stem tips

(larvae) (Aguiar-

Menezes et al.,

2002; Friesen et al.,

2008)

No This is an

external pest

(Aguiar-

Menezes et al.,

2002) not

expected to be

associated with

mature fruit at

harvest. This

pest was also

introduced and

released into

Hawaii as a

biological

control agent for

Passiflora weed

species.




presence in

Ecuador


association4

On

harvested

plant

part(s)?5

Remarks

BACTERIA

Xanthomonas

axonopodis pv.

passiflorae

(Pereira)

Gonçalves &

Rosato (= X.

campestris pv.

passiflorae

(Pereira) Dye)

Rogg, 2000 Joy and Sherin,

2012; Manicom et

al., 2003; Rogg,

2000

Leaves, seeds

(Manicom et al.,

2003), fruit (Fischer

and Rezende, 2008;

Goncalves and

Rosato, 2000)

No Infection of the

fruit by X.

axonopodis pv.

passiflorae

causes fruit to

fall prior to

maturation or

causes lesions

that are

conspicuous

(Fischer and

Rezende, 2008).

Infected fruit are

not likely to

remain with the

consignment.

FUNGI

Alternaria

passiflorae J.H.

Simmonds

MAG-IICA, 2001 Fischer and

Rezende, 2008;

MAG-IICA, 2001;

Manicom et al.,

2003

Leaves, fruit, stem

(Fischer and

Rezende, 2008)

No This pest is

present in

Florida and

Hawaii (Farr and

Rossman, 2013).

Spots on fruit are

conspicuous

(Fischer and

Rezende, 2008)

and infected fruit

are not likely to

remain with the

consignment.

Asterina

megalospora Berk.

& M.A. Curtis

Wellman, 1977 Farr and Rossman,

2013; Wellman,

1977

Leaves (Farr and

Rossman, 2013)

No

Asterina tacsoniae

Pat.

Wellman, 1977 Farr and Rossman,

2013; Wellman,

1977

Leaves (based on

affected plant parts

for other Asterina

species on various

hosts) (Farr and

Rossman, 2013)

No




presence in

Ecuador


association4

On

harvested

plant

part(s)?5

Remarks

Irenopsis

passiflorae Hansf.

Farr and

Rossman, 2013

Farr and Rossman,

2013

Leaves (based on

affected plant parts

for other Irenopsis

species on various

hosts) (e.g., Faria et

al., 2008;

Hosagoudar and

Sabeena, 2010)

No

Mycena citricolor

(Berk. & M.A.

Curtis) Sacc.

CABI, 2013 Wellman, 1977 Leaves (Wellman,

1977)

No This pest is

present in

Florida (CABI,

2013).

Pseudocercospora

calospilea (Syd.)

Deighton (=

Cercospora

calospilea Syd.)

Farr and

Rossman, 2013

Farr and Rossman,

2013; Wellman,

1977

Leaf spot (Wellman,

1977)

No

MOLLUSK

Lissachatina fulica

(Bowdich)

Borrero et al.,

2009

Raut and Barker,

2002

Whole plant (Raut

and Barker, 2002)

No This pest is

present in

Florida (PAS,

2013a).

Lissachatina

fulica is a large

mollusk. It is

highly unlikely

to remain with

fruit through

hand-harvesting

and culling as

described in

section 1.4.

2.3. Pests selected for further analysis

We identified six pests for further analysis (Table 3). All of these organisms are actionable pests

for the continental United States and have a reasonable likelihood of being associated with the

fruit at the time of harvest and remaining with the commodity, in viable form, throughout the

harvesting process.



Table 3. Pests selected for further analysis.

Pest type Taxonomy Scientific name

Arthropod Diptera: Tephritidae Anastrepha curitis

Anastrepha dissimilis

Anastrepha fraterculus

Anastrepha pseudoparallela

Anastrepha striata

Ceratitis capitata

3. Assessing Pest Risk Potential

3.1. Introduction

For each pest selected for further analysis, we estimate its overall pest risk potential. Risk is

described by the likelihood of an adverse event, the magnitude of the consequences, and

uncertainty. In this risk assessment, we first determine for each pest if there is an endangered

area within the import area. The endangered area is defined as the portion of the import area

where ecological factors favor the establishment of the pest and where the presence of the pest

will result in economically important losses. Once an endangered area has been determined, the

overall risk of each pest is then determined by two separate components: 1) the likelihood of its

introduction into the endangered area on the imported commodity (i.e., the likelihood of an

adverse event), and 2) the consequences of its introduction (i.e., the magnitude of the

consequences). In general, we assess both of these components for each pest. However, if we

determine that the risk of either of these components is negligible, it is not necessary to assess

the other, as the overall pest risk potential would be negligible regardless of the result of the

second component. In other words, if we determine that the introduction of a pest is unlikely to

have unacceptable consequences, we do not assess its likelihood of being introduced. Likewise,

if we determine there is negligible likelihood of a pest being introduced, we do not assess its

consequences of introduction.

The likelihood and consequences of introduction are assessed using different approaches.

For the consequences of introduction, we determine if the pest meets the threshold (Yes/No) of

likely causing unacceptable consequences of introduction. This determination is based on

estimating the potential consequences of introduction in terms of physical losses (rather than

monetary losses). The threshold is based on a proportion of damage rather than an absolute value

or amount. Pests that are like to impact at least 10 percent of the production of one or more hosts

are deemed “threshold pests.”

For likelihood of introduction, which is based on the likelihoods of entry and establishment, we

qualitatively assess risk using the ratings Negligible, Low, Medium, and High. The risk factors

comprising the model for likelihood of introduction are interdependent and, therefore, the model

is multiplicative rather than additive. Thus, if any one risk factor is rated as Negligible, then the

overall likelihood will be Negligible. For the overall likelihood of introduction risk rating, we

define the different categories as follows:



High: Pest introduction is highly likely to occur.

Medium: Pest introduction is possible, but for that to happen, the exact combination of

required events needs to occur.

Low: Pest introduction is unlikely to occur because one or more of the required events

are unlikely to happen, or the full combination of required events is unlikely to

align properly in time and space.

Negligible: Pest introduction is highly unlikely to occur given the exact combination of

events required for successful introduction.

3.2. Assessment results

3.2.1. Anastrepha curitis

A full pest analysis for A. curitis is not needed because the endangered area is negligible.

We present the results of this assessment in the table below.

Determination of the portion of the continental United States endangered by Anastrepha

curitis

Climatic suitability Anastrepha curitis is known only from Amazonas and Para, Brazil (Dutra

et al., 2013) and Ecuador (García, 2011). Based on a comparison with

USDA Plant Hardiness Zones (Magarey et al., 2008), establishment

would only occur in Plant Hardiness Zones 12 and 13. We conclude that

suitable environmental conditions would only exist within protected areas

(e.g., glasshouses) in the continental United States.

Defined

Endangered Area

We determined that no portion of the continental United States is likely

to be endangered by Anastrepha curitis because no portion of the PRA

area is likely to be climatically suitable for the pest’s continued survival.

3.2.2. Anastrepha dissimilis

A full pest analysis for A. dissimilis is not needed because the endangered area is negligible.

We present the results of this assessment in the table below.


dissimilis

Climatic suitability Anastrepha dissimilis is present throughout Brazil (Zucchi and Moraes,

2008) and in Ecuador (Tigrero and Salas, 2009). A comparison with the

USDA Plant Hardiness Zones (Magarey et al., 2008) indicates that

establishment may occur in Plant Hardiness Zones 10-13, inclusive of

Florida and some limited portions of southern Texas and Louisiana.

Potential hosts at

risk in PRA Area

The only known host plants for A. dissimilis are Passiflora species

(Aguiar-Menezes et al., 2002; Zucchi and Moraes, 2008). Passiflora

species may be found throughout the southern United States (NRCS,

2013).

Economically

important hosts at

riska

Anastrepha dissimilis has been reported on a number of Passiflora

species (Aguiar-Menezes et al., 2002; Zucchi and Moraes, 2008). In the

continental United States, Passiflora species may be grown for fruit



(limited production), as ornamentals, or as a groundcover (CABI, 2013;

CRFG, 2009; McGuire, 1999).

Pest potential on

economically

important hosts at

risk

The pest potential of A. dissimilis on Passiflora species in the continental

United States is considered negligible. Records indicate that it has not

been recorded from commercially important Passiflora species, and the

pest is therefore not considered economically significant (Norrbom et al.,

2012).

Defined

Endangered Area

We determined that no portion of the continental United States is likely

to be endangered by Anastrepha dissimilis because the pest does not pose

a threat to any hosts of economic, environmental, or social importance in

the PRA area. a As defined by ISPM No. 11, supplement 2, “economically” important hosts refers to both commercial and non-

market (environmental) plants (IPPC, 2011).

3.2.3. Anastrepha fraterculus

We determined the overall likelihood of introduction to be High. We present the results of this

assessment in the table below.

We determined that the establishment of Anastrepha fraterculus in the continental United States

is likely to cause unacceptable impacts. We present the results of this assessment in the table

below.


fraterculus

Climatic suitability Anastrepha fraterculus occurs in North, Central, and South America and

the Caribbean, ranging from southern Texas to Argentina (Alberti et al.,

2008; CABI, 2013; Foote et al., 1993). More specifically, it occurs in

southern Texas (Rio Grande Valley), Mexico (restricted distribution),

Belize, Costa Rica, El Salvador, Guatemala, Honduras, Nicaragua,

Panama, Trinidad and Tobago, Argentina (restricted distribution),

Bolivia, Brazil, Colombia, Ecuador, Guyana, Paraguay, Peru, Suriname,

Uruguay, and Venezuela (CABI, 2013). This distribution covers a

temperature range corresponding to USDA Plant Hardiness Zones 8-11

(Magarey et al., 2008).

Potential hosts at

risk in PRA Area

Anastrepha fraterculus feeds on multiple genera in multiple plant

families, including Actinidiaceae (Actinidia), Anacardiaceae (Mangifera,

Spondias), Annonaceae (Annona), Combretaceae (Terminalia),

Ebenaceae (Diospyros), Juglandaceae (Juglans), Lauraceae (Persea),

Moraceae (Ficus), Myrtaceae (Eugenia, Psidium, Syzygium), Oleaceae

(Olea), Punicaceae (Punica), Rosaceae (Cydonia, Eriobotrya, Fragaria,

Malus, Prunus, Pyrus, Rubus), Rutaceae (Citrus, Fortunella), Sapotaceae

(Manilkara, Pouteria), Solanaceae (Solanum), and Vitaceae (Vitis)

(CABI, 2013; White and Elson-Harris, 1992).

Economically

important hosts at

riska

The A. fraterculus species complex may infest economically important

crops as apple, citrus, guava, and peaches (CABI, 2013; Weems, 2006).



Pest potential on

economically

important hosts at

risk

The A. fraterculus species complex damages economically important

plants (Weems, 2006). In Argentina and Mexico, A. fraterculus is

considered one of the most economically important fruit fly species

(Alberti et al., 2008; Aluja et al., 1987). The oviposition punctures

(“stings”) alone may render fruit unmarketable (Gould and Raga, 2002).

In Brazil, it is considered a major apple pest that requires chemical

control measures in commercial orchards (Sugayama et al., 1997). Yield

loss in organic peach production ranges from 40-98.3 percent (Rupp et

al., 2012).

Defined

Endangered Area

The area endangered by A. fraterculus comprises Plant Hardiness Zones

8-11, as this area is both climatically suitable and contains economically

important hosts. a As defined by ISPM No. 11, supplement 2, “economically” important hosts refers to both commercial and non-


Assessment of the likelihood of introduction of Anastrepha fraterculus into the endangered

area via the importation of passion fruit from Ecuador

Risk Element Risk Rating Uncertainty

Ratinga

Justification for rating and

explanation of uncertainty (and

other notes as necessary)

Likelihood of Entry

Risk Element A1: Pest

prevalence on the harvested

commodity (= the baseline

rating for entry)

High MC Anastrepha fraterculus is one of

the most common fruit flies

associated with passion fruit

(Aguiar-Menezes et al., 2002).

Eggs are laid within fruit and

larvae feed internally during

development (Aguiar-Menezes et

al., 2002). No standard industry

field practices beyond minimal

handling during harvest are known

(see section 1.4: Description of

pathway).

Risk Element A2: Likelihood

of surviving post-harvest

processing before shipment

High MC Fruit infested with fruit flies are

highly likely to escape detection

during culling (White and Elson-

Harris, 1992).


of surviving transport and

storage conditions of the

consignment

High MU No transport or storage conditions

have been provided that may

reduce the prevalence of A.

fraterculus on the fruit (see section

1.4: Description of pathway).

Typical shipping conditions for

passion fruit seem unlikely to

affect the pest population.




Ratinga




Risk Element A: Overall risk

rating for likelihood of entry

High N/A

Likelihood of Establishment

Risk Element B1: Likelihood

of coming into contact with

host material in the

endangered area

High C Anastrepha fraterculus feeds on

multiple genera in multiple plant

families (CABI, 2013; White and

Elson-Harris, 1992). Suitable hosts

are widely and regularly distributed

throughout the entire endangered

area.


of arriving in the endangered

area

High C More than 25 percent of the U.S.

population lives in the endangered

area.

Risk Element B: Combined

likelihood of establishment

High N/A

Overall Likelihood of Introduction

Combined likelihoods of

entry and establishment

High N/A

aC=Certain, MC=Moderately Certain, MU=Moderately Uncertain, U=Uncertain

Assessment of the consequences of introduction of Anastrepha fraterculus into the

continental United States (i.e., the PRA area)

Criteria Meets

criteria?

(Y/N)

Uncertainty

Ratinga




Direct Impacts

Risk Element C1: Damage

potential in the endangered

area

Yes MC Management strategies for the

different Anastrepha species vary

accordingly (Miller et al., 2013),

and current management

techniques in the United States

may not be sufficient for A.

fraterculus. Yield losses due to

infestations of A. fraterculus in

organic fruit production are

especially high, ranging from 40-

98.3 percent (Rupp et al., 2012). It

is likely that introduction of A.

fraterculus into the United States

would initiate additional specific

control programs that are likely to



Criteria Meets

criteria?

(Y/N)

Uncertainty

Ratinga




significantly increase the costs of

production.

Risk Element C2: Spread

potential

Yes C Anastrepha fraterculus has been

shown to successfully colonize

multiple new important crops, such

as apples when they were

introduced into Brazil (Sugayama

et al., 1998). Adults of A.

fraterculus can fly relatively long

distances in short periods

(Kovaleski et al., 1999). The

primary mode of international

spread is through the movement of

infested fruit (Botha et al., 2004;

CABI, 2013).

Risk Element C: Pest

introduction is likely to cause

unacceptable direct impacts

Yes

N/A

Trade Impacts

Risk Element D1: Export

markets at risk

N/A N/A

Risk Element D2: Likelihood

of trading partners imposing

additional phytosanitary

requirements

N/A N/A

Risk Element D: Pest is likely

to cause significant trade

impacts

N/A N/A

Conclusion

Is the pest likely to cause

unacceptable consequences in

the PRA area?

Yes N/A


3.2.4. Anastrepha pseudoparallela

We determined the overall likelihood of introduction to be Medium. We present the results of

this assessment in the table below.

We determined that the establishment of Anastrepha pseudoparallela in the continental United

States is likely to cause unacceptable impacts. We present the results of this assessment in the

table below.




pseudoparallela

Climatic suitability Anastrepha pseudoparallela is present in Argentina, Brazil, Ecuador, and

Peru (Carroll et al., 2006; Uchôa, 2012). A comparison with the USDA

Plant Hardiness Zones (Magarey et al., 2008) indicates that establishment

may occur in Plant Hardiness Zones 10-13, inclusive of Florida and some

limited portions of southern Texas and Louisiana.

Potential hosts at

risk in PRA Area

Potential hosts for A. pseudoparallela include mango (Mangifera indica),

guava (Psidium guajava), and passion fruit (Passiflora spp.) (Uchôa,

2012), all of which may be found in Plant Hardiness Zones 10-13

(NRCS, 2013).

Economically

important hosts at

riska

Mango and guava are considered to be economically important crops

grown in the continental United States, specifically in Florida (Mossler

and Crane, 2012; Mossler and Crane, 2013).

Pest potential on

economically

important hosts at

risk

Anastrepha pseudoparallela is considered to be a fruit fly with “real

economic importance” on mango, guava, and passion fruit (Aguiar, 2012;

Uchôa, 2012). The lack of specific quantification of damage increases the

uncertainty of this conclusion.

Defined

Endangered Area

The area of the continental United States endangered by A.

pseudoparallela includes mango and guava in Plant Hardiness Zones 10-

11. a As defined by ISPM No. 11, supplement 2, “economically” important hosts refers to both commercial and non-


Assessment of the likelihood of introduction of Anastrepha pseudoparallela into the

endangered area via the importation of passion fruit from Ecuador


Ratinga




Likelihood of Entry




rating for entry)

High MC Anastrepha pseudoparallela is

considered to be a pest of various

Passiflora species in Ecuador

(Aguiar-Menezes et al., 2002;

Uchôa, 2012). Eggs are laid within

fruit and larvae feed internally

during development (Aguiar-

Menezes et al., 2002). No standard

industry field practices beyond

minimal handling during harvest

are known (see section 1.4:

Description of pathway).










Ratinga




Harris, 1992).




consignment



reduce the prevalence of A.

pseudoparallela on the fruit (see

section 1.4: Description of

pathway). Typical shipping

conditions for passion fruit seem

unlikely to affect the pest

population.



High N/A





endangered area

Medium C Anastrepha pseudoparallela is a

pest of Passiflora spp., mango, and

guava (Uchôa, 2012), and suitable

hosts are widely established in only

a limited portion of the endangered

area.



area

Low C Less than 10 percent of the U.S.


area.



Medium N/A




Medium N/A


Assessment of the consequences of introduction of Anastrepha pseudoparallela into the

continental United States (i.e., the PRA area)

Criteria Meets

criteria?

(Y/N)

Uncertainty

Ratinga




Direct Impacts



area

Yes MU Management strategies for the


accordingly (Miller et al., 2013), and

current management techniques in the

United States may not be sufficient

for A. pseudoparallela. General



Criteria Meets

criteria?

(Y/N)

Uncertainty

Ratinga




control practices for mango and guava

production in Florida do not indicate

specific fruit fly control measures

(Mossler and Crane, 2012, 2013).

While specific yield losses

attributable to infestations of A.

pseudoparallela could not be found, it

is considered to be a pest species in

South America (Aguiar, 2012; Uchôa,

2012). For these reasons, we estimate

that there is potential for significant

damage to occur in the endangered

area, but with moderate levels of

uncertainty.


potential

Yes MU There do not appear to be any

biological factors that may reduce the

spread potential of A. pseudoparallela

in the United States. As with other

Anastrepha species, the primary mode

of spread is likely through the

movement of infested fruit (Botha et

al., 2004; CABI, 2013).




Yes

N/A

Trade Impacts


markets at risk

N/A N/A




requirements

N/A N/A



impacts

N/A N/A

Conclusion



the PRA area?

Yes N/A




3.2.5. Anastrepha striata

We determined the overall likelihood of introduction to be High. We present the results of this

assessment in the table below.

We determined that the establishment of A. striata in the continental United States is likely to

cause unacceptable impacts. We present the results of this assessment in the table below.


striata

Climatic suitability Anastrepha striata is present in southern Mexico, most of Central

America, through South America to Peru, Bolivia, and Brazil (CABI,

2013; Hernández-Ortiz, 1992; Weems and Fasulo, 2012). A comparison

with the USDA Plant Hardiness Zones (Magarey et al., 2008) indicates

that establishment may occur in Plant Hardiness Zones 9-13.

Potential hosts at

risk in PRA Area

The primary host of Anastrepha striata is guava (Psidium guajava)

(Hernández-Ortiz, 1992), though it may also infest fruits of lime (Citrus

aurantifolia) and orange (Citrus sinensis) (Condor, 1973), Spondias

purpurea, and other Psidium species (Zucchi and Moraes, 2008), all of

which may be found in Plant Hardiness Zones 9-13 (NRCS, 2013).

Economically

important hosts at

riska

Guava and citrus are considered to be economically important hosts in

the United States (Mossler and Crane, 2012; NASS, 2011).

Pest potential on

economically

important hosts at

risk

Anastrepha striata is considered to be an important agricultural pest in

guava, limes, and oranges (Aluja et al., 1987; Condor, 1973; Weems and

Fasulo, 2012). In general, A. striata does not appear to be considered a

pest of primary economic importance (Weems and Fasulo, 2012), though

significant damage may occur in dooryard plantings or other plants in the

environment. Anastrepha species are considered to be the most serious

fruit fly pests in Central and South America (CABI, 2013); therefore, we

consider it likely that A. striata would have significant economic impacts

on potential host species in the continental United States.

Defined

Endangered Area

The endangered area encompasses areas where guava and citrus are

grown in Plant Hardiness Zones 9-11. a As defined by ISPM No. 11, supplement 2, “economically” important hosts refers to both commercial and non-


Assessment of the likelihood of introduction of Anastrepha striata into the endangered area

via the importation of passion fruit from Ecuador


Ratinga




Likelihood of Entry




High MC Anastrepha striata may be found

commonly associated with various

Passiflora species (Aguiar-




Ratinga




rating for entry) Menezes et al., 2002). Eggs are

laid within fruit, and larvae feed

internally during development

(Aguiar-Menezes et al., 2002). No

standard industry field practices

beyond minimal handling during

harvest are known (see section 1.4:








Harris, 1992).




consignment



reduce the prevalence of A. striata

on the fruit (see section 1.4:

Description of pathway). Typical

shipping conditions for passion

fruit seem unlikely to affect the

pest population.



High N/A





endangered area

High MC Anastrepha striata feeds on

multiple genera in multiple plant

families (CABI, 2013; Weems and

Fasulo, 2012). Suitable hosts are

widely and regularly distributed


area.



area



area.



High N/A




High N/A




Assessment of the consequences of introduction of Anastrepha striata into the continental

United States (i.e., the PRA area)

Criteria Meets

criteria?

(Y/N)

Uncertainty

Ratinga




Direct Impacts



area

Yes MU Management strategies of the


accordingly (Miller et al., 2013), and

current management techniques in the

United States may not be sufficient

for A. striata. General control

practices for guava production in

Florida do not indicate specific fruit

fly control measures (Mossler and

Crane, 2012). While specific yield

losses attributable to infestations of A.

striata could not be found, it is

considered to be a pest species in

South America (Aguiar-Menezes et

al., 2002; CABI, 2013). For these

reasons, we estimate that there is

potential for significant damage to

occur in the endangered area, but with

moderate levels of uncertainty.


potential

Yes MU There do not appear to be any

biological factors that may reduce the

spread potential of A. striata in the

United States. As with other

Anastrepha species, the primary mode

of spread is likely through the

movement of infested fruit (Botha et

al., 2004; CABI, 2013).




Yes N/A

Trade Impacts


markets at risk

N/A N/A




requirements

N/A N/A



N/A N/A



Criteria Meets

criteria?

(Y/N)

Uncertainty

Ratinga




impacts

Conclusion



the PRA area?

Yes N/A


3.2.6. Ceratitis capitata

We determined the overall likelihood of introduction to be Medium. We present the results of

this assessment in the table below.

We determined that the establishment of Ceratitis capitata in the continental United States is

likely to cause unacceptable impacts. We present the results of this assessment in the table

below.

Determination of the portion of the continental United States endangered by Ceratitis

capitata

Climatic suitability Ceratitis capitata (Medfly) is widely distributed in the Mediterranean

region, South and Central America, west Asia, and Australia (CABI,

2013). Based on its current distribution, we estimate that Medfly could

establish in areas of the continental United States corresponding to Plant

Hardiness Zones 8-11 (Magarey et al., 2008).

Potential hosts at

risk in PRA Area

Medfly feeds on over 400 hosts (CABI, 2013), many of which are

common within Plant Hardiness Zones 8-11 in the United States.

Economically

important hosts at

riska

Economically important hosts widely present in the area of concern

include Capsicum annuum, Citrus spp., Ficus carica, Morus nigra,

Prunus domestica, and P. persica (CABI, 2013).

Pest potential on

economically

important hosts at

risk

Medfly is a serious pest on Citrus spp., Ficus carica, Mangifera indica,

and Prunus persica; damage to fruit crops may reach 100 percent (CABI,

2013). Medfly therefore could impact several of the economically

important hosts listed above.

Defined

Endangered Area

The area endangered by Medfly comprises Plant Hardiness Zones 8-11,

as this area is both climatically suitable and contains economically

important hosts. a As defined by ISPM No. 11, supplement 2, “economically” important hosts refers to both commercial and non-




Assessment of the likelihood of introduction of Ceratitis capitata into the endangered area

via the importation of passion fruit from Ecuador


Ratinga




Likelihood of Entry




rating for entry)

Low MU Even though C. capitata is widely

reported as a major pest of passion

fruit (e.g., Aguiar-Menezes et al.,

2002; CABI, 2013; Hill, 1983;

Liquido et al., 1991; Rogg, 2000),

multiple studies (e,.g. da Silva et

al., 2009; Pirovani et al., 2010;

Uramoto et al., 2004) researching

the species of fruit flies that

emerge from Passiflora fruit

collected in the field did not find C.

capitata. However, both male and

female adults emerged from fruit

collected from unsprayed P. alata

(Raga et al., 2011), indicating some

level of susceptibility within the

Passiflora genus. Eggs are laid

within fruit and larvae feed

internally during development

(Aguiar-Menezes et al., 2002). No

standard industry field practices

beyond minimal handling during

harvest are known (see section 1.4:





Low MC Fruit infested with fruit flies are



Harris, 1992).




consignment

Low MU No transport or storage conditions


reduce the prevalence of C.

capitata in the fruit (see section

1.4: Description of pathway).

Typical shipping conditions for

passion fruit seem unlikely to

affect the pest population.



Low N/A




Ratinga








endangered area

High C Ceratitis capitata is a widely

polyphagous species (CABI,

2013). Suitable hosts are widely

and regularly distributed


area.



area


population lives within the

endangered area.



High N/A




Medium N/A


Assessment of the consequences of introduction of Ceratitis capitata into the continental

United States (i.e., the PRA area)

Criteria Meets

criteria?

(Y/N)

Uncertainty

Ratinga




Direct Impacts



area

Yes

C Ceratitis capitata is a serious pest

on numerous hosts, including

Citrus spp., Ficus carica, and

Prunus persica; damage to fruit

crops may reach 100 percent

(CABI, 2013). In the continental

United States, C. capitata is

considered a quarantine pest, and

eradication measures are

immediately activated when

populations are detected (PAS,

2013b).


potential

Yes C Ceratitis capitata has spread in the

Mediterranean area and Central

and South America (CABI, 2013),

and has repeatedly entered the

United States (PAS, 2013b).



Criteria Meets

criteria?

(Y/N)

Uncertainty

Ratinga







Yes

N/A

Trade Impacts


markets at risk

N/A N/A




requirements

N/A N/A



impacts

N/A N/A

Conclusion



the PRA area?

Yes N/A


4. Summary and Conclusions of Risk Assessment

Of the organisms associated with Passiflora spp. worldwide and reported in Ecuador, we

identified organisms that are actionable pests for the continental United States and have a

reasonable likelihood of being associated with the commodity following harvesting from the

field and prior to any post-harvest processing. We further evaluated these organisms for their

likelihood of introduction (i.e., entry plus establishment) and their potential consequences of

introduction. Pests that meet the threshold to likely cause unacceptable consequences of

introduction and receive an overall likelihood of introduction risk rating above Negligible are

candidates for risk management. The results of this risk assessment represent a baseline estimate

of the risks associated with the import commodity pathway as described in section 1.4.

Of the pests selected for further analysis, we determined that those identified in Table 4 are not

candidates for risk management, because no portion of the continental United States is likely to

be endangered by the pest. We summarize the results for each pest in Table 4.

All the other pests selected for further analysis are candidates for risk management, because they

meet the threshold to likely cause unacceptable consequences of introduction, and they received

an overall likelihood of introduction risk rating above Negligible. We summarize the results for

each pest in Table 5.

Detailed examination and choice of appropriate phytosanitary measures to mitigate pest risk are

part of the pest risk management phase within APHIS and are not addressed in this document.



Table 4. Summary for pests selected for further evaluation and determined not to be candidates

for risk management.

Pest Reason the pest is not a

candidate for risk management

Uncertainty statement

(optional)a

Anastrepha curitis No endangered area within the

PRA area.

Anastrepha dissimilis No endangered area within the

PRA area.

aThe uncertainty statement, if included, identifies the most important source(s) of uncertainty.

Table 5. Summary for pests selected for further evaluation and determined to be candidates for

risk management. All of these pests meet the threshold for unacceptable consequences of

introduction.

Pest Likelihood of Introduction

overall rating

Uncertainty statement

(optional)a

Anastrepha fraterculus High

Anastrepha pseudoparallela Medium

Anastrepha striata High

Ceratitis capitata Medium aThe uncertainty statement, if included, identifies the most important source(s) of uncertainty.

5. Acknowledgements

Authors Cynthia Landry, Ecologista

Reviewers Christina Devorshak, Entomologista

John Rogers, Plant Pathologista

a Plant Epidemiology and Risk Analysis Laboratory, USDA-APHIS-PPQ

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7. Appendix A. Pests with non-actionable regulatory status We found some evidence of the below listed organisms being associated with Passiflora spp. and

being present in the Ecuador; however, because these organisms have non-actionable regulatory

status for the continental United States, we did not list them in Table 2 of this risk assessment.

Below we list these organisms along with the references supporting their potential association

with Passiflora spp., their potential presence in Ecuador, their presence in the continental United

States (if applicable), and their regulatory status for the continental United States. For organisms

not present in the continental United States, we also provide justification for their non-actionable

status.

Organism Evidence and/or other notes

ARTHROPODS

Acari: Phytoseiidae

Typhlodromalus limonicus

(Garman & McGregor)

de Moraes et al., 1986. Genus is nonreportable (PestID,

2013).

Typhlodromalus peregrinus

(Muma)

de Moraes et al., 1986. Genus is nonreportable (PestID,

2013).

Acari: Tarsonemidae

Polyphagotarsonemus latus

(Banks)

Aguiar-Menezes et al., 2002; Rogg, 2000. Nonreportable

(PestID, 2013).

Acari: Tenuipalpidae

Brevipalpus phoenicis (Geijskes) Hill, 2008; Maes, 2004; Rogg, 2000. Nonreportable

(PestID, 2013).

Acari: Tetranychidae

Mononychellus tanajoa (Bondar) CABI, 2013; De Moraes et al., 1995

Oligonychus coffeae (Nietner) Bolland et al., 1998. Nonreportable (PestID, 2013).

Tetranychus marianae McGregor Denmark, 1970; Hill, 2008; Maes, 2004; Rogg, 2000

Tetranychus mexicanus

(McGregor)

Aguiar-Menezes et al., 2002; García, 2011; Gil, 1998.

Nonreportable (PestID, 2013).

Tetranychus urticae Koch Aguiar-Menezes et al., 2002; Bolland et al., 1998; MAG-

IICA, 2001. Nonreportable (PestID, 2013).

Tetranychus yusti McGregor Bolland et al., 1998. Nonreportable (PestID, 2013).

Coleoptera: Anthribidae

Araecerus fasciculatus (De Geer) Aguiar-Menezes et al., 2002; CABI, 2013; Rogg, 2000.

Nonreportable (PestID, 2013).


Hypothenemus crudiae (Panzer) Maes, 2004. Nonreportable (PestID, 2013).

Pantomorus cervinus Boheman Rogg, 2000. Nonreportable (PestID, 2013).

Coleoptera: Scarabaeidae

Cyclocephala melanocephala

Fabricius

Aguiar-Menezes et al., 2002; Bauernfeind, 2001; Rogg,

2000

Diptera: Agromyzidae

Liriomyza sativae Blanchard Maes, 2004; Rogg, 2000. Nonreportable (PestID, 2013).





Lonchaea sp. Rogg, 2000. Genus is nonreportable (PestID, 2013).

Diptera: Otitidae

Notogramma cimiciforme Loew Uchôa-Fernandes et al., 2002. Nonreportable (PestID,

2013).

Hemiptera: Aleyrodidae

Bemisia tabaci (Gennadius) Maes, 2004; Rogg, 2000. Nonreportable (PestID, 2013).

Trialeurodes vaprariorum

(Westwood)

Mound and Halsey, 1978

Hemiptera: Aphididae

Aphis gossypii Glover Aguiar-Menezes et al., 2002; Blackman and Eastop, 2000;

CABI, 2013; Hill, 2008; Rogg, 2000

Aphis spiraecola Patch CABI, 2013

Aulacorthum solani Kaltenbach Blackman and Eastop, 2000; Rogg, 2000. Nonreportable

(PestID, 2013).

Brachycaudus helichrysi

Kaltenbach

Blackman and Eastop, 2000; Rogg, 2000. Nonreportable

(PestID, 2013).

Macrosiphum euphorbiae

Thomas

Aguiar-Menezes et al., 2002; Blackman and Eastop, 2000;

CABI, 2013; Hill, 2008

Myzus persicae Sulzer Aguiar-Menezes et al., 2002; Blackman and Eastop, 2000;

CABI, 2013

Toxoptera aurantii Boyer de

Fonscolombe

Blackman and Eastop, 2000; CABI, 2013; Rogg, 2000

Hemiptera: Asterolecaniidae

Russellaspis pustulans pustulans

(Cockerell)

Ben-Dov et al., 2013

Hemiptera: Coccidae

Ceroplastes cirripediformis

Comstock

García, 2011; Martorell, 1976. Nonreportable (PestID,

2013).

Coccus hesperidum Linnaeus Aguiar-Menezes et al., 2002; CABI, 2013; Hill, 2008

Parasaissetia nigra (Nietner) Ben-Dov et al., 2013; CABI, 2013

Saissetia coffeae (Walker) CABI, 2013; Maes, 2004

Hemiptera: Coreidae

Dallacoris pictus (Drury) (=

Phthia picta (Drury))

Maes, 2004; Rogg, 2000

Leptoglossus gonagra Fabricius Aguiar-Menezes et al., 2002; Froeschner, 1981; Maes,

2004. Nonreportable (PestID, 2013).

Leptoglossus zonatus (Dallas) Froeschner, 1981; MAG, 1986; Rogg, 2000. Nonreportable

(PestID, 2013).

Hemiptera: Diaspididae Non-actionable status for Diaspididae on commodities for

consumption (NIS, 2008).

Aonidiella aurantii (Maskell) Aguiar-Menezes et al., 2002; CABI, 2013; Hill, 2008;

Rogg, 2000

Aspidiotus destructor Signoret Ben-Dov et al., 2013; CABI, 2013




Chrysomphalus dictyospermi

(Morgan)

CABI, 2013

Hemiberlesia lataniae (Signoret) Ben-Dov et al., 2013; CABI, 2013; Maes, 2004; Williams

and Watson, 1988

Hemiberlesia palmae (Cockerell) Ben-Dov et al., 2013; Williams and Watson, 1988

Howardia biclavis (Comstock) Ben-Dov et al., 2013; Martorell, 1976

Lepidosaphes beckii (Newman) Ben-Dov et al., 2013; Maes, 2004

Lopholeucaspis cockerelli

(Grandpré & Charmoy)

Ben-Dov et al., 2013

Parlatoria proteus (Curtis) Ben-Dov et al., 2013

Pinnaspis strachani (Cooley) Ben-Dov et al., 2013; Maes, 2004

Pseudaonidia trilobitiformis

(Green)

Ben-Dov et al., 2013; Hill, 1983; Hill, 2008; Rogg, 2000;

Williams and Watson, 1988

Pseudaulacaspis pentagona

(Targioni)

Rogg, 2000; Williams and Watson, 1988

Pseudischnaspis bowreyi

(Cockerell)

Ben-Dov et al., 2013; Maes, 2004

Pseudoparlatoria ostreata

Cockerell

Ben-Dov et al., 2013; Martorell, 1976

Selenaspidus articulatus

(Morgan)

Aguiar-Menezes et al., 2002; Ben-Dov et al., 2013; CABI,

2013

Hemiptera: Monophlebidae

Icerya purchasi Maskell Ben-Dov et al., 2013

Hemiptera: Pentatomidae

Nezara viridula (Linnaeus) CABI, 2013; Hill, 2008. Nonreportable (PestID, 2013).

Hemiptera: Pseudococcidae

Dysmicoccus brevipes

(Cockerell)

Ben-Dov, 1994; Halbert, 2003. Nonreportable (PestID,

2013).

Dysmicoccus grassii (Leonardi)

(= D. alazon Williams)

Ben-Dov et al., 2013; Ben-Dov, 1994; Williams and

Granara de Willink, 1992. Nonreportable (PestID, 2013).

Planococcus citri (Risso) Aguiar-Menezes et al., 2002; Ben-Dov, 1994; Ben-Dov et

al., 2013; Hill, 2008. Nonreportable (PestID, 2013).

Planococcus minor (Maskell) (=

P. pacificus Cox)

Aguiar-Menezes et al., 2002; CABI, 2013; Cox, 1989

Pseudococcus viburni (Signoret)

(= P. affinis (Maskell))

Ben-Dov et al., 2013; Ben-Dov, 1994. Nonreportable

(PestID, 2013).


Agrotis ipsilon (Hufnagel) García, 2011; MAG, 1986. Nonreportable (PestID, 2013).

Peridroma saucia (Hübner) Aguiar-Menezes et al., 2002; CABI, 2013; Gallego and

Velez, 1992


Agraulis vanillae (Linnaeus) Aguiar-Menezes et al., 2002; Friesen et al., 2008; Gilbert,

1969; Rogg, 2000. Nonreportable (PestID, 2013).




Dione juno Cramer Aguiar-Menezes et al., 2002; Dominguez-Gil and

McPheron, 1992; Friesen et al., 2008; MAG, 1986; MAG-

IICA, 2001; Rogg, 2000

Dione moneta Hübner Gilbert, 1969; Pemberton, 1989; Willmott and Hall, 2013

Dryadula phaetusa Linnaeus Opler et al., 2013; Willmott and Hall, 2013

Dryas iulia Fabricius Opler et al., 2013; Willmott and Hall, 2013; Young, 1978

Heliconius charithonia Linnaeus Opler et al., 2013; Willmott and Hall, 2013

Thysanoptera: Thripidae

Chaetanaphothrips orchidii

(Moulton)

CABI, 2013

Heliothrips haemorrhoidalis

Bouché

CABI, 2013; Hill, 2008

BACTERIA

Ralstonia solanacearum (Smith)

Yabuuchi et al.

CABI, 2013; Fischer and Rezende, 2008; Manicom et al.,

2003

Rhizobium radiobacter

(Beijerinck & van Delden)

Young et al. (= Agrobacterium

tumefaciens (Smith &

Townsend) Conn)

CABI, 2013; Manicom et al., 2003; Rogg, 2000

FUNGI AND CHROMISTANS

Alternaria alternata (Fr. : Fr.)

Keissl.

Farr and Rossman, 2013; Joy and Sherin, 2012; Manicom

et al., 2003; Pacin et al., 2002. Nonreportable (PestID,

2013).

Alternaria brassicae (Berk.)

Sacc. (= A. macrospora (Sacc.)

Sawada)

Farr and Rossman, 2013; Manicom et al., 2003; Rogg,

2000. Nonreportable (PestID, 2013).

Aspergillus niger Tiegh. Farr and Rossman, 2013; Peregrine and Ahmad, 1982;

Rogg, 2000

Botryotinia fuckeliana (de Bary)

Whetzel (=Botrytis cinerea Pers.

: Fr.)

Farr and Rossman, 2013; Rogg, 2000; Wellman, 1977

Cephaleuros virescens Künze Farr and Rossman, 2013; Guiry and Guiry, 2013

Cladosporium herbarum Farr and Rossman, 2013; Manicom et al., 2003; Rogg,

2000

Cladosporium oxysporum Berk.

& M.A. Curtis

Farr and Rossman, 2013; Fischer and Rezende, 2008; Joy

and Sherin, 2012; Manicom et al., 2003

Colletotrichum acutatum J.H.

Simmonds

CABI, 2013; Farr and Rossman, 2013

Colletotrichum truncatum

(Schwein.) Andrus & W.D.

Moore

Farr and Rossman, 2013

Erysiphe polygoni DC. Farr and Rossman, 2013; Rogg, 2000

Fusarium lateritium Nees : Fr. Farr and Rossman, 2013




Fusarium moniliforme J. Sheld. Farr and Rossman, 2013; Peregrine and Ahmad, 1982;

Rogg, 2000

Fusarium oxysporum f. sp.

passiflorae W.L. Gordon

Rogg, 2000; Rooney-Latham et al., 2011

Fusarium oxysporum Schltdl. :

Fr.

Farr and Rossman, 2013; Joy and Sherin, 2012; Wellman,

1977

Fusarium solani (Mart.) Sacc. Farr and Rossman, 2013; Fischer and Rezende, 2008; Joy

and Sherin, 2012

Gibberella baccata (Wallr.)

Sacc.


Glomerella cingulata (Stoneman)

Spauld. & H. Schrenk

Anamorph: Colletotrichum

gloeosporioides (Penz.) Penz. &

Sacc.

Farr and Rossman, 2013; Fischer and Rezende, 2008; Joy

and Sherin, 2012; Pacin et al., 2002; Rogg, 2000

Haematonectria haematococca

(Berk. & Broome) Samuels &

Rossman (= Nectria

haematococca Berk. & Broome)

Farr and Rossman, 2013; Fischer and Rezende, 2008;

García, 2011; Joy and Sherin, 2012; Lozano et al., 2007

Lasiodiplodia theobromae (Pat.)

Griffiths & Maubl.

CABI, 2013; Fischer and Rezende, 2008; Peregrine and

Ahmad, 1982

Phytophthora cinnamomi Rands CABI, 2013; Joy and Sherin, 2012; MAG-IICA, 2001;

Rogg, 2000

Rhizoctonia solani J.G. Kühn Farr and Rossman, 2013; Fischer and Rezende, 2008

Septoria passiflorae Syd. Farr and Rossman, 2013; Fischer and Rezende, 2008; Joy

and Sherin, 2012; Wellman, 1977

Seuratia millardetii (Racib.)

Meeker

Farr and Rossman, 2013; Gillis and Glawe, 2008

Thanatephorus cucumeris (A.B.

Frank) Donk


Trichoderma hamatum Rifai Farr and Rossman, 2013

NEMATODES

Meloidogyne arenaria (Neal)

Chitwood

CABI, 2013; Fischer and Rezende, 2008; Manicom et al.,

2003

Meloidogyne incognita (Kofoid

& White) Chitwood

CABI, 2013; Fischer and Rezende, 2008; MAG-IICA,

2001; Manicom et al., 2003

Meloidogyne javanica (Treub)

Chitwood

CABI, 2013; Fischer and Rezende, 2008; Joy and Sherin,

2012; Manicom et al., 2003

VIRUS

Cucumber mosaic virus CABI, 2013; Fischer and Rezende, 2008

Soybean mosaic virus Benscher et al., 1996; CABI, 2013; MAG, 1986

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