## The Importation of F resh Spinach [ Spinacia oleracea

Linnaeus ] from Colombia into the Continental United States

A Pathway

- Initiated Risk Assessment

December 200 7

United States Department of Agriculture

Animal and Plant H ealth Inspection Service Plant Protection and Quarantine Center of Plant Health Science and Technology Plant Epidemiology and Risk and Analysis Laboratory 1730 Varsity Drive , Suite 300 Raleigh, NC 27606Spinach from Colombia

Rev. 02 December 4, 2007 ii Executive Summary

The Republic of Colombia, Sout h America requested the authorization to export fresh s pinach ( Spinacia oleracea L.) in to the c ontinental United States. A list of s pinach pests in Colombia was prepared based on documentation submitted by the Agricultural and Rural Development Ministry

of Colombia , the Instituto Colombiano Agropec ario (ICA), and the USDA

- APHIS

- PPQ records on intercepted pests at ports of entry , scientific literature, and the opinions of experts in the field

of s pinach production.

This pest risk assessment identified the following quarantine pests in the pathway:

Copitarsia incommoda Walker (Lepidoptera: Noctuidae)

Diabrotica speciosa (Germar) (Coleoptera: Chrysomelidae)

Liriomyza huidobrensis Blanchard (Diptera: Agromyzidae)

For these species

, the ratings for the Consequences of Introduction, the Likelihood of Introduction, and the overall Pest Risk Potential were estimated to be High. Specific phytosanitary measures are strongly recommended for pests rated High. Risk mitigat ion options

are described in Appendix 2 at the end of the risk assessment.Spinach from Colombia

Rev. 02 December 4, 2007 iii Table of Contents

I. Introduction

................................ ................................ ................................ ............................. 1

II. Risk Assessment

................................ ................................ ................................ ...................... 1 2.1 Initiating Event: Proposed Action

................................ ................................ ......................... 2

2.2 Assessment of Weed Potential of Spinacia oleracea L.

................................ ....................... 2 2.3 Current Status, Decision History and Pest Interceptions

................................ ...................... 3 2.4 Pest Categorization

- Identification of Pests of Spinacia oleracea L. in Colombia

.............. 3 2.5 Quarantine Pests Likely to Follow the Pathway

................................ ................................ . 14 2.6 Consequences of Introduction

................................ ................................ ............................. 15 Copitarsia incommoda Walker

................................ ................................ .............................. 15 Diabrotica speciosa (Germar)

................................ ................................ ................................ 17 Liriomyza huidobrensis Blanchard

................................ ................................ ......................... 18

2.7 Likelihood of Introduction

................................ ................................ ................................ ... 20

2.8 Pest Risk Potential and Conclusion

................................ ................................ ..................... 23

III. Literature Cited

................................ ................................ ................................ ....................... 24 IV. Preparers and Reviewers

................................ ................................ ................................ ......... 30 Appendix 1. Port Information Network PIN (1985

- 2007) Interceptions on Spinacia oleracea

.. 31 Appendix 2. Mitigation of Quarantine Pests of Spinach from Colombia

................................ .... 35Spinach from Colombia

Rev.02 December 4, 2007 1 I. Introduction

This risk assessment was prepared by the Center for Phytosanitary Excellence (C EF) in Bogota, Colombia, the Plant Protection and Quarantine (PPQ), and the Animal and Plant Health Inspection Service (APHIS) of the United States Department of Agriculture (USDA). It was prepared in order to examine potential pest risks associated with t he importation of fresh s pinach ( Spinacia oleracea L.)

from Colombia into the continental United States . This pest risk assessment is called pathway

- initiated because it is based on the risks that may be associated with the importation of this commodity. T his risk assessment is qualitative ; risk is expressed in the descriptive terms of H igh, M edium, and L ow
, rather than probabilities or frequencies. The methodology and rating criteria are explained in Pathway

Initiated Pest Risk Assessments: Guidelines for Qualitative Assessments, Version 5.02 (USDA, 2000).

International plant protection organizations

, such as the North American Plant Protection Organization (NAPPO)

, the International Plant Protection Convention (IPPC) of the United Nations, and the Food

an d Agriculture Organization (FAO)

, provide guidance for conducting pest risk analyses. The methods used to initiate, conduct, and report this plant pest risk assessment are consistent with the guidelines provided by NAPPO and the IPPC. The use of biological and phytosanitary terms conforms to the Glossary of Phytosanitary Terms ISPM, No. 5 (IPPC, 200 7b ). The IPPC guidelines describe three stages of pest risk analysis: Stage 1 (initiation), Stage 2 (risk assessment), and Stage 3 (risk management) (IPPC, 2007a ). This document satisfies the requirements of IPPC Stages 1 and 2.

The plant Spinacia oleracea L. (Class: Dicotyledonae, Order: Caryophyllales, Family: Chenopodiaceae) is not known in a wild state. Spinach is believed to be native to the Middle East in t he general area of Iran, Afghanistan, and Turkmenistan (CAB International , 2006 ; Hochmuth et al. , 2003 ; and Perez, 1990 ). It is closely related to beets ( Beta vulgaris L ). While originiated in a warm climate, it is grown in temperate and cool tropical ar eas to prevent bolting (the rapid growth of the seed stalk) which makes the spinach unmarketable (CAB International , 2006 ).

Spinach is a dicotyledonous annual with a tap

- root that extends 15

- 25 cm into the soil ( Mills, 2001 ). The leaves are hairless, broad, and te nder. They may be wrinkled (Savoy), smooth (flat), or in

- between (Semi

- Savoy). Savoy types are primarily used for fresh market purposes, while smooth types are preferable for processing. Semi

- savoy typ es are grown for either market ( LeStrange et al., 200 4)

. The first growth stage is vegetative which is followed by a rosette stage. Spinach leaves are harvested during the rosette stage at 30

- 45 days ( Mills, 2001 ).

After harvest, the leaves should be stored at 0 C and 95

- 100% Rel. Hum.( Mills, 2001 ). Spinach can

last 10

- 1 4 days in storage before it becomes marketable( Mills, 2001 ). It is frequently packed in plastic bags to prevent injury. The average yield of spinach in Colombia for the year 2002 was 15 ton/ha and

the produc tion was 1,600 tons in 262 acre s (Ministerio de Agricultur a y Desarrollo Rural, 2003)

.

II. Risk Assessment

This pest risk assessment identif ies the initiating event, a weediness screening, and discussion of the decision history. The pests reported as attacking spinach in Colombia were identified and

characterized. The quarantine pests likely to follow the p athway were then analyzed. For this

assessment

, the first five Risk Elements considered are combined to form an assessment of the riskSpinach from Colombia

Rev.02 December 4, 2007 2 associated with the Consequences of Introduction. Six Sub

- Elements were evalu ated and combined to create a value that estimates the risk associated with the Likelihood of Introduction. Together, the Consequences of Introduction and the Likelihood of Introduction values form an evaluati on of the Pest

Risk Potential.

2.1 Initiating Event: Proposed Action

This commodity

- based, pathway

- initiated assessment is in response to a request made by the Instituto Colombiano Agropec ario (ICA) ( letter No. 04840 dated June 3 , 200 3 ) to the USDA for authorization to allow imports of spinach . In this case, the importation to all ports into the c ontinental United States of

fresh spinach , grown in Colombia, is not authorized and is a potential pathway for introduction of

exotic plant pests. Title 7 of the Code of Federal Regulations 319, Part 56 (7 CFR § 319.56) provides regulatory authority for the importation of fruits and vegetables from foreign sources into the United

States.

2.2 Assessment of Weed Potential of Spinacia oleracea L.

The results of the weed screening for spinach did not prompt a weed

- initiated risk assessment (Table 1).

T able 1. Assessment of Weed Potential of Spinacia oleracea L.

Commodity:

Scientific name and author: Spinacia oleracea L innaeus

. Plant family: Chenopodiaceae

Common name: Spinach (English)

, Espinaca (Spanish)

Phase 1: Spinach was introduced to the United States from another country. The species

, Spinacia

oleracea

, is widely prevalent in the United States

, as it is cultivated in 18 s tates (USDA and NRCS, 2002)

. Phase 2: Is the species listed in:

NO Geographical Atlas of World Weeds (Holm et al., 1991).

NO World’s Worst Weeds (Holm et al., 1991 a ).

NO Report of the Technical Committee to Evaluate Noxious Weeds; Exotic Weeds for the Federal Noxious Weed Act (APHIS

– USDA

, 2000).

NO Economically Important Foreign Weeds (Reed, 1977).

NO Composite List of Weeds ( WSSA. 2006 ).

NO AGRIS (AGRIS/CARIS, 2004) ; AGRICOLA ( NAL , 200 4 )

NO C rop Protection Compendium ( CAB International, 2006 )

.

Other literature and database search indicat ing weediness:

NO World Weeds: Natural H istories and D istributions (Holm et al., 1997).

NO World Economic Plants (Wiersema and León, 1999).

NO Florida's Invasive Species List, Florida Exotic Pest Plant Council (FLEPPC, 2001).

Phase 3:

A weed

- ini tiated risk assessment is not needed for S. oleracea because this plant does not
exhibit invasive behaviour according to literature searches.Spinach from Colombia

Rev.02 December 4, 2007 3 2.3 Current Stat us, Decision History and Pest Interceptions

Several countries have requested the ability to import spinach into the United States. Only France has ever been denied the entry into the U.S. for spinach , due to the presence of an exotic rust

. All enterable spinach is subject to inspection for pests and soil. Only Nigerian is restricted to any spec ific port (North Atlantic) in the continental U.S.

Table 2 . Prior Decisions the United States Has Made Regarding Requests to Import Spinacia oleracea

Year Country Decision Reasons / Conditions

1926 Cuba Approved No interceptions of pests on spinach fro m Cuba

1926 Mexico Approved N o pest interceptions related to spinach

1939 Netherlands Approved No record of injurious insects attacking spinach

1947 Bahamas Approved No record of any exotic spinach pests

1952 West Indies Approved No significant pest in terceptions on spinach

1967 Korea Approved No significant pest interceptions on spinach

1967 Japan Approved No significant pest interceptions on spinach

1972 France Denied The presence of an exotic rust ( Puccinia isiacae (Thuem))

1974 Nigeria Approved No significant pest interceptions or literature on Spinach Restricted to north Atlantic ports only1

1 981 Trinidad Approved No significant pests recorded

1999 Nicaragua Approved No significant pests recorded

Currently, s pinach is authorized to enter a ll U.S. ports from the following countries : B e lgi um , Belize, Bermuda, Costa Rica, Dominican Republic , El Salvador, Guatemala, Honduras, Japan

, Korea, Me xico,

Netherlands , Nicaragua, Panama and Surinam

. Nigeria imports are only authorized to enter through North Atlantic ports (USDA, 2002a).

P est species intercepted between 1985

- 2007 on spinach entering the U

. S

. a re listed in the Appendix 1

. .

2

. 4 Pest Categorization

- Identification of Pests of Spinacia oleracea L. in Colombia

Table 3 presents informatio n about the geographic distribution, host associations and regulatory data

for spinach from Colombia. The table includes (1) the presence of pests in Colombia relative to their presence in the United States, (2) the generally affected plant part or parts, (3) the quarantine status of the pest in the United States, (4) whether the pest is likely to follow the pathway into the United States

on spinach , and (5) pertinent citations for either the distributi on or the biology of the pest. Many organisms are not s ources of phytosanitary risk on spinach from Colombia because they do not satisfy the definition of a quarantine pest ( IPPC , 200 7a ). A quarantine pest is defined as, “ a pest of potential economic importance to the area endangered thereby and not yet presen t there, or present but not widely distributed and being officially controlled” ( IPPC, 2007 a ).Spinach from Colombia

Rev.02 December 4, 2007 4 Table 3 : Pests of Spinacia oleracea L. in Colombia

Pest Scientific Name

and Taxonomic

Classification Geographic

Distribution 1 Plant Part

Affected 2 Quaranti ne Pest Follow Pathway References

Arthropods Agromyzidae, species of (Diptera) CO L 5 Yes Yes AQAS

, 200 7

Agrotis ipsilon (Hufnagel) (Lepidoptera: Noctuidae) CO

, US L, S No Yes Arnett, 2000;

CAB International,

2006 ; Figueroa,
1977; Posada, 1989; Santiago, 2000 Agrotis spp. (Lepidoptera: Noctuidae) CO L, S , Sd Yes Yes Arnett, 2000; Figueroa,
1977; Sigueñas, 1995

Anasa sp. ( Hemiptera: Coreidae ) CO L Yes Yes Arnett, 2000; Brailovsky, 1985; Neartica, 1998; Posada,

1989 Anthomyiidae, species of 4

( Diptera ) CO L, R, S 5 Yes Yes AQAS

, 200 7

Aphididae, species of ( Homoptera ) CO L 5 Yes Yes AQAS

, 200 7

Aphis gossypii

Glover ( Homoptera: Aphididae ) CO, US Fl, L, S, Sh No No Arnett, 2000;

Bust illo and Sanchez, 1977; Figueroa,
1977; CAB International,

2006 ; Posada,

1989 Aphis sp. 4

( Homoptera: Aphididae ) CO Fl, L, S 5 Yes Yes Arnett, 2000

, AQAS

, 200 7 ; Santiago, 2000 Brachycerinae, species of 4
(Coleoptera: Curculionidae) CO L, S 5 Yes Yes AQAS

, 200 7

Bryobia praetiosa Koch (Acari: Tetranychidae) C O , US L No No Bolland et al

., 1998
Cercopidae, species of 4
(Homopt era) CO Fl, L, S 5 Yes Yes AQAS

, 200 7Spinach from Colombia

Rev.02 December 4, 2007 5 Table 3 : Pests of Spinacia oleracea L. in Colombia

Pest Scientific Name

and Taxonomic

Classification Geographic

Distribution 1 Plant Part

Affected 2 Quaranti ne Pest Follow Pathway References

Chrysodeixis includens (Walker) (Lepidoptera: Noctuidae) CO, US F, Fl , L No Yes CAB

International

, 200 6 ; Robinson et
al ., 2007 Chrysomelidae, species of 4
(Coleoptera) CO Fl, L, S 5 Yes Yes AQAS

, 200 7

Cicadellidae, species of 4
(Homoptera) CO F, Fl, L, S 5 Yes Yes AQAS

, 200 7

Coccidae, species of 4
(Homoptera) CO Fl, L, S 5 Yes Yes AQAS

, 200 7

Conotrachelus sp. 4
(Coleoptera: Curculionidae) CO Fl, L, S, Se 5 Yes Yes AQAS

, 200 7 ; Poole and Gentili, 1996 a ; Posada, 1989 Copitarsia sp. (Lepidoptera: Noctuidae) CO L Yes Yes AQAS

, 200 7

Copitarsia incommoda

Walker
[ Syn: Copitarsia consu eta (Walker) ] (Lepidoptera: Noctuidae) CO, MX L Yes Yes Bautista et al

., 2003 ; Rojas et
al ., 1993 ; Santiago, 2000

Coreidae, species of 4
(Hemiptera ) CO Fl, L, S 5 Yes Yes AQAS

, 200 7

Crambidae, species of 4
(Lepidoptera) CO Fl, L, S 5 Yes Yes AQAS

, 200 7

Curculionidae, species of 4
(Coleoptera) CO Fl, L, R, S 5 Yes Yes AQAS

, 200 7

Delia sp. (Diptera: Anthomyiidae) CO R, S Yes Yes Arnett, 2000;

Martínez et al

., 1999; Santiago, 2000
Delia platura (Meigen) (Diptera: Anthomyiidae) CO, US Fl, L, S, Sh No No CAB International,

2006 ; Mau and Kessing, 2004

Diabrotica sp. 4
(Coleoptera: Chrysomelidae) CO Fl, L, S 5 Yes Yes Arnett, 2000 ; AQAS

, 200 7,

Poole and Gentili, 1996 Diabrotica speciosa (Germar) (Coleoptera: Chrysomelidae) CO R, L, S, Fl

, F Yes Yes 4 CAB

International

, 200 6 ; Walsh,

2003Spinach from Colombia

Rev.02 December 4, 2007 6 Table 3 : Pests of Spinacia oleracea L. in Colombia

Pest Scientific Name

and Taxonomic

Classification Geographic

Distribution 1 Plant Part

Affected 2 Quaranti ne Pest Follow Pathway References

Diaprepes sp. 4
(Coleoptera: Curculionidae) CO Fl, L, S 5 Yes Yes AQAS

, 200 7 ; Poole and Gentili, 1996 Diaspididae, species of 4
(Homoptera) CO Fl, L, S 5 Yes Yes AQAS

, 200 7

Disonycha sp. 4
(Coleoptera: Chrysomelidae) CO Fl, L, S 5 Yes Yes AQAS

, 200 7 ; Poole and Gentili, 1996

Feltia spp. ( Lepidoptera: Noctuidae ) CO L, S, Sd Yes Yes Arnett, 2000; Sigueñas, 1995

Frankliniella sp. 4
(Thysanoptera: Thripidae) CO Fl, L, S 5 Yes Yes AQAS

, 200 7

Gelechiidae, spec ies of 4
(Lepidoptera) CO Fl, L, R 5 Yes Yes AQAS

, 200 7

Geom etridae, species of 4
(Lepidoptera) CO Fl, L, S 5 Yes Yes AQAS

, 200 7

Gracillariidae, species of 4
(Lepidoptera) CO Fl, L, S 5 Yes Yes AQAS

, 200 7

Gryllidae, species of 4
(Orthoptera) CO Fl, L, S, R 5 Yes Yes AQAS

, 200 7

Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) CO, US F, Fl, L, Sd No Yes CAB International,
2006;

Robinson et
al ., 200 4 Hellula phidilealis (Walker) (Lepidoptera: Crambidae) CO , US L, S No No 7 CAB International,

2006 ; Robinson et
al ., 2004 Hypothenemus sp. 4
(Coleoptera: Curculionidae) CO Fl, L, S 5 Yes Yes Atkinson and Peck, 1994; Figueroa, 1977; AQAS

, 200 7 Isonychus sp. 4
(Coleoptera: Scarabaeidae) CO Fl, L, S 5 Yes Yes AQAS

, 200 7

Leucinodes sp. 4
(Lepidoptera: Pyralidae) CO F 5 Yes No AQAS

, 200 7Spinach from Colombia

Rev.02 December 4, 2007 7 Table 3 : Pests of Spinacia oleracea L. in Colombia

Pest Scientific Name

and Taxonomic

Classification Geographic

Distribution 1 Plant Part

Affected 2 Quaranti ne Pest Follow Pathway References

Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae) CO, US L Yes 6 Yes Arnett, 2000;

CAB International,

2006 ; Figueroa, 1977; Posada,

1989 ; Sant iago, 2000; Sigueñas, 1995 Liriomyza sativae

Blanchard (Diptera: Agromyzidae) CO, US L No Yes CAB International,

2006 ; Figueroa,

1977 ; Posada,

1989 Liriomyza trifolii Burgess in Comstock (Diptera: Agromyzidae) CO, US L No Yes CAB International,

2006 ; Po sada,

1989

Listroderes sp. 4
(Coleoptera: Curculionidae) CO Fl, L, S 5 Yes Yes AQAS

, 200 7

Macrosiphum euphorbiae (Thomas) (Homoptera: Aphididae) CO , US L No Yes CAB International,

2006 ; Posada,

1989 Margarodidae, species of 4
(Homoptera) CO Fl, L, S 5 Yes Yes AQAS

, 200 7

Miridae, species of 4
(Hemiptera) CO Fl, L, S 5 Yes Yes AQAS

, 200 7

Myochrous sp. 4
(Coleoptera: Chrysomelidae) CO L 5 Yes Yes AQAS

, 200 7

Myzus persicae (Sulzer) (Homoptera: Aphididae) CO, US Fl, L, S, Sh No No Arnett, 2000 ; Bustillo and Sanchez, 1977;

CAB International,

2006 ; Figueroa, 1977; Posada,

1989 ; Santiago, 2000;Spinach from Colombia

Rev.02 December 4, 2007 8 Table 3 : Pests of Spinacia oleracea L. in Colombia

Pest Scientific Name

and Taxonomic

Classification Geographic

Distribution 1 Plant Part

Affected 2 Quaranti ne Pest Follow Pathway References

Noctuidae, species of (Lepidoptera) CO L Yes Yes AQAS

, 200 7

Nysius sp. 4
(Hemiptera: Lygaeidae) CO Fl, L, S, Se 5 Yes Yes Neartica, 1998 ; AQAS

, 200 7
Olethreutinae, species of 4
(Lepidoptera) CO Fl, L, S, Se 5 Yes Yes AQAS

, 200 7

Orthezia sp. 4
(Homoptera: Ortheziidae) CO L, S 5 Yes Yes Neartica, 1998 ; AQAS

, 200 7
Ortheziidae, species of 4
(Homoptera) CO L, S 5 Yes Yes AQAS

, 200 7

Pentatomidae, species of 4
(Hemiptera) CO Fl, L, S 5 Yes Yes AQAS

, 200 7

Peridroma saucia (Hübner) Lepidoptera: Noctuidae CO, US Fl, L , S, Sh No No Arnett, 2000;

CAB International,

2006 ; Poole and Gentili,

1996 c Pheidole sp. 4
(Hymenoptera: Formicidae) CO Fl, L, S 5 Yes Yes Poole and Gentili, 1996 b ; AQAS

, 200 7 Phlaeothripidae, species of

4
(Thysanoptera) CO Fl, L, S 5 Yes Yes AQAS

, 200 7

Pieridae, species of 4
(Lepidoptera) CO L 5 Yes Yes AQAS

, 200 7

Plutella xylostella Linnaeus (Lepidoptera: Yponomeutidae ) CO, US No No 7 CAB

International

, 2006;

Robinson et
al ., 20 07 Plusiinae, species of 4
(Lepidoptera) CO Fl, L, S 5 Yes Yes AQAS

, 200 7

Pseudococcidae, species of

4
(Homoptera) CO Fl, L, S, Se 5 Yes Yes AQAS

, 200 7

Psyllidae, species of 4
(Homoptera) CO Fl, L, S 5 Yes Yes AQAS

, 200 7

Pyralidae, species of 4
(Lepidoptera) CO Fl, L, S, Se 5 Yes Yes Neartica, 1998 ; AQAS

, 200 7
Pyrausta sp. 4
(Lepidoptera: Pyralidae) CO L 5 Yes Yes AQAS

, 200 7Spinach from Colombia

Rev.02 December 4, 2007 9 Table 3 : Pests of Spinacia oleracea L. in Colombia

Pest Scientific Name

and Taxonomic

Classification Geographic

Distribution 1 Plant Part

Affected 2 Quaranti ne Pest Follow Pathway References

Rhinacloa sp. 4
(Hemiptera: Miridae) CO Fl, L, S 5 Yes Yes AQAS

, 200 7

Saissetia coffeae (Walker) (Hemiptera: Coccidae) CO, U.S N/A No N/A Ben

- Dov et al

., 2001
Spodoptera frugiperda

J.E. Smith (Lepidoptera: Noctuidae) CO, US Fl, L, S No Yes Arnett, 2000;

CAB International,

2006 ; Figueroa,
1977; Gallego

and V é lez,

1992 ; Posada,

1989 Spodoptera sp. 4
(Lepidoptera: Noctuidae) CO Fl, L, S 5 Yes Yes AQAS

, 200 7; Posada, 1989
Spoladea recurvalis (Fabricius) (Lepidoptera: Pyralidae) CO, US Fl, L, R, Sh No Yes CAB International,

2006 ; Perez,

2003 Sys tena sp. 4
(Coleoptera: Chrysomelidae) CO Fl, L, S 5 Yes Yes AQAS

, 200 7

Tetranychus sp. (Acari: Tetranichidae) CO L Yes Yes Posada, 1989; Santiago, 2000; Tetranychus cinnabarinus (Boisduval) (Acari: Tetranichidae) CO, US L No No CAB International,

2006 ; Mau and Kessing,

2004 ; Posada,

1989 Tetranychus ludeni Zahe r (Acari: Tetranichidae) CO, US L No No Bolland et al.,

1998 Tetranychus urticae Koch (Acari: Tetranichidae) CO, US L No No Bolland et al.,

1998
Tephritidae, species of 4
(Diptera) CO F 5 Yes No AQAS

, 200 7

Thripidae, species of 4
(Thysanoptera) CO Fl, L, S 5 Yes Yes AQAS

, 200 7

Trichoplusia ni (Hübner) (Lepidoptera: Noctuidae) CO, US L No Yes CAB International,

2006 ; Mau a nd Kessing, 2004Spinach from Colombia

Rev.02 December 4, 2007 10 Table 3 : Pests of Spinacia oleracea L. in Colombia

Pest Scientific Name

and Taxonomic

Classification Geographic

Distribution 1 Plant Part

Affected 2 Quaranti ne Pest Follow Pathway References

Bacteria Rhodococcus fascians (Tilford) Goodfellow ( Actinomycetales ) CO, US L, S No Yes CAB International,

2006 ; Euzéby,

2004 Fungi 3

Alternaria sp

. Ness (Mitosporic Fungi: Hyphomycetes) CO F, L Yes Yes Alfieri et al. 1994; Buriticá, 1999; Santiago, 2000

Cercospora sp (Mitosporic Fungi: Hyphomycetes) CO Fl, L, S 5 Yes Yes Caicedo and Ruiz, 1995;

Farr et al.,

1989 Cercospora beticola

Sacc ( Mitosporic Fungi: Hyphomycetes) CO, U

. S

. N/A No N/A Alfieri et al.
1994; CAB International,

20 06 ; Farr et al., 1989 Choanephora

cucurbitarum (Berk. & Ravenel) Thaxt. (Zyg omycetes: Mucorales) CO, U

. S

. N/A No N/A Alfieri et al.
1994; CAB International,

2006 ; Farr et al., 1989 Cladosporium sp. (Mitosporic Fungi: Hyphomycetes) CO L Yes Yes Alfieri e t al., 1994; Buriticá, 1999; Farr et al., 1989; Santiago, 2000 Cladosporium variabile ( Cooke) de Vries [Synonym: Heterosporum variabile

Cooke ] CO, U.S. N/A No N/A CAB International,

2006

Fusarium oxysproum Schlechtend.:Fr.f.sp. spinaciae Anamorph

, Gibberella sp. [ Sordariomycetes, Hypocreales], CO, U.S. N/A No N/A CAB International,

2006

Olpidium brassicae (Woronin) P.A. Dang. (Chytridiomycetes: Chytridiales) CO, U

. S

. N/A No N/A Farr et al.,
1989; CAB International,

2006 ;Spinach from Colombia

Rev.02 December 4, 2007 11 Table 3 : Pests of Spinacia oleracea L. in Colombia

Pest Scientific Name

and Taxonomic

Classification Geographic

Distribution 1 Plant Part

Affected 2 Quaranti ne Pest Follow Pathway References

Peronospora farinose f.sp spinacia Byford [Synonym: Pernospora effuse (Grave) Rabenh. [Oomycetes; Peronosporales] CO, U

. S

. N/A No N/A Buriticá, 1999;

Farr et al., 1989; Santiago,
2000; Sigueñas, 19 95

Peronospora sp. (Oomycetes: Peronosporales) CO L Yes Yes Alfieri et al.,
1994; Caicedo and Ruiz, 1995; Farr et al., 1989

Phoma sp. (Mitosporic Fungi: Coelomycetes) CO Fl, L, R, S 5 Yes Yes Alfieri et al. 1994; Caicedo and Ruiz, 1995; Farr et al., 198 9 Phoma spinaciae Bubak &Krieg Anamorph: Pleospora betae (Berl.) Nevodovsky
[ Dothideomycetes, Pleosporales] [Synonym:

Phoma betae A.B.Frank (Dothideomycetes, Pleosporales) CO , U.S. N/A No N/A Buritica, 1999
CAB International,

2006

Py thium sp

. (Mitosporic Fungi: Oomycetes) CO R, Sd Yes Yes Alfieri et al., 1994; Buriticá, 1999; Caicedo and Ruiz, 1995; Farr et al., 1989 Pythium aphanidermatum Edson (Fitz.) [ Oomycetes Peronsporales] CO, U.S. N/A No N/A CAB International,

2006

, Farr et

a l, 2006
Rhizoctonia solani Kuhn; Teleomorph:Thanatephorus cucmeris (A.B. Frank) Donk
[ Basidiomycetes, Corticiales] CO, U.S. N/A No N/A CAB

Int ernational,

2006Spinach from Colombia

Rev.02 December 4, 2007 12 Table 3 : Pests of Spinacia oleracea L. in Colombia

Pest Scientific Name

and Taxonomic

Classification Geographic

Distribution 1 Plant Part

Affected 2 Quaranti ne Pest Follow Pathway References

Sclerotinia sclerotiorum (Lib.) de Bary (Discomycetes: Helotiales) CO, U

. S

. N/A No N/A Alfieri et al.,
1994; Buriticá, 1999;

Farr et al.,

1989
Sclerotinia sp. (Discomycetes: Helotiales) CO L, S Yes Yes Alfieri et al.,
1994; Caicedo

and Ruiz, 1995; Farr et al., 1989

Molluscs

Dero c eras sp. ( L imacidae) CO L, S Yes Yes CAB International,

2006 ; Santiago, 2000; Helix aspersa 4

Muller [Syn: Cryptomphalus

aspersus 4

(Muller) ] ( Helicidae) CO, U

. S

. Fl, L, S 5 No Yes CAB International,

2006 ; AQA S,

2007

Milax gagatex (Draparnaud) (Milacidae) CO, U

. S

. L, S No Yes Fern á ndez,
1982; Santiago, 2000;
Veronicella sloanei (Cuvier) (Veronicellidae) CO 8 , U.S. 8 Yes No 8 Thome et al

., 1997

Nematodes Ditylenchus dipsaci (Kühn) Filip'ev CO, U

. S

. L, S, Bl N o Yes? CAB

International

, 200 6; Diekmann,

1997

Helicotylenchus dihystera (Cobb) Sher (Hoplolaimidae) CO, U

. S

. R No No Baujard. and Martiny. 1995;

CAB International,

2006 Phytoplasm aster yellows phytoplasma

group CO, U

. S

. N/A No N/A CAB International,

2006Spinach from Colombia

Rev.02 December 4, 2007 13 Table 3 : Pests of Spinacia oleracea L. in Colombia

Pest Scientific Name

and Taxonomic

Classification Geographic

Distribution 1 Plant Part

Affected 2 Quaranti ne Pest Follow Pathway References

Virus Beet western yellows

luteovirus

Luteoviridae U.S., CO ( Brunt et al.

, 1996 ) N/A No N/A Brunt et al.

, 1996

Cucu mber mosaic

cucumovirus

CMV (Bromoviridae) CO, U

. S

. N/A No N/A Alfieri et al., 1994; Brunt et
al. , 1996; CAB International,

2006

Potato T trichovirus ( Flexiviridae ) CO 9 L , Se, S, R Yes Yes Brunt et al.

, 1996

Potato U nepovirus ( Comoviridae ) PE 10 R, L, Se, S Yes Yes 11 Brunt et al.

, 1996

1 Geographic Distribution: CO = Colombia

, , US = United States.

2 Branch= B, Flower= Fl , Fruit= F, Leaf= L, Peduncle= P, Root= R, Seeds= Se, Seedling= Sd, Shoot= Sh, Stem= S,

Tuber= T , Bulb=Bl.

. 3 Biological hazards associated with organisms not identified to the species level are not assessed because often there are many species wi thin a genus, and we cannot know if the unidentified species occurs in the United States and, consequently, whether it meets the definition of a quarantine pest for the United States. This is not the case if the entire genus (or higher order taxonomic grou pin) is absent from the US in which case the quarantine classification would apply In this risk assessment, the above statement applies to the fungi Alternaria sp., Cercospora sp., Cladosproium sp.., Pernospora sp., Phoma sp., Pythium sp., and Sclerotinia sp. All eleven genera are known to occur in the United States (Farr et al ., 2006 ). The inability to specifically identify these specimens may indicate limits of current taxonomic knowledge, the life stage, o r the quality of the specimen submitted for i dentification. By necessity, pest risk assessments focus on organisms for which biological information is available. Lack of specific identification does not rule out the possibility that a high risk quarantine pest was intercepted. Conversely, the devel opment of detailed assessments for known pests that inhabit a variety of ecological niches, allow effective mitigation measures to eliminate the known organisms as well as similar but incompletely identified organisms that inhabit the same niche. If pests identified to higher taxa are intercepted in the future, then a reevaluation of their risk may occur.

4 This pest was intercepted or reported on spinach from other countries other than Colombia ; it was also intercepted on other

fresh products other than sp inach from Colombia ( AQAS, 2007 ).

5 A ffected p lant p art (s) correspond to the record in AQAS (2007) on other products from Colombia other than from spinach.

6 This pest is present in California , which is the only place of its existence within the continenta l United States ( CAB

International, 2006 ). P reliminary studies by Scheffer (Scheffer, 2000; Scheffer et al. , 2001; Scheffer, 2004) suggest that the

records on Liriomyza huidobrensis Blanchard with in the U

. S

. really refer to Liriomyza langei Frick (that is a cryptic species

within the Liriomyza huidobrensis ). T his pest is considered to be a quarantine pest because it is present in only one State o f

the continental United States (Reitz, 2004) and is being reviewed as part of official control plans

7 Hellula p hidilealis (Walker) listed in Robinson et al . (2007) as intercepted at a USA port on Spinacia oleracea . There are no

more records of association with this host. Known hosts include plants from the family Cruciferae

8 Restricted distribution : Colombia

- Is la de Providencia , United States: Massachusetts ( Thome et al ., 1997 ).

9 P otato T trichovirus has been detected in Peru and Bolivia and probably occurs throughout the Andes, including Colombia

( EPPO/OEPPO, 2007 ). The virus has a broad host range that includes many native Solanaceae ( Lizarraga et al. , 2000 ) speci es, native Chenopodaceae ( Brunt et al. , 1996 ) species and spinach ( Spinacea oleracea L.) ( Brunt et al. , 1996 ). The virus is transmitted by grafting, seed, and pollen. It is not transmitted by direc t contact between plants ( Brunt et al. , 1996 ). Although the precise nature of the infection in spinach is not known, the infection is systemic in other Chenopodiaceae which suggests that it could follow the pathway to the United States. Spinach leaves are washed prior to shi pment ( 2007 ) which removes pollen and attached seeds. Also, the shipments should be inspected to prevent contamination by seeds from other plants, whether weeds or volunteers, since they may carry the virus. These treatments should remove the potential forSpinach from Colombia

Rev.02 December 4, 2007 14 the virus to be vectored by a nematode or dispersed by seed, upon arri val in United States. Inspection at Points

- of

- Entry (POE) should verify that any seed, including non

- Federal Noxious Weeds species, is absent from the shipments. If these procedures are followed, the potential for the virus to disperse in United States i s minimal and no further analysis is required. However, if seeds or soils are found to be present in shipments of spinach, then there is a potential for dispersa l and the risk of this commodity entering the United States should be reevaluated.

10 The know n distribution of both Potato U virus includes the neighboring country of Peru. Based on the host range that

includes Solanum tuberosum and Chenopodium quinoa, there is a reasonable suspicion that both pathogens exist throughout the Andes, including Colo mbia ( EPPO/OEPPO, 2007 ) . In addition, spinach has not been cultivated on a large scale in the Andes. Thus, there may be o ther viruses with broad host ranges in the Solanaceae and Chenopodiaceae may be able to infect spinach when they are challenged by the virus for the first time. One potential spinach pathogen is Potato Ringsp ot nepovirus ( Brunt et al. , 1996 ).

11 Potato U nepovirus has been identified in the Andean reg ions of Peru a nd Bolivia ( Brunt et al. , 1996 ) and is likely to be present in the Andean region of Col ombia in both Solanaceae ( Jones, 1983 )and Chenopodiaceae ( Jones, 1983 ) species. The cultivation of spinach ( Spinacea oleracea L.) in the same areas as other hosts for the virus combined with sandy soi ls ( Castro, 2003

, Selvaradjou et al. , 2005

, Volveras et al. , 2007 ) that facilitate the vectoring of the virus by an unknown Longidorus sp. ( Jones, 1983 ) suggests that spinach in Colombia could be infected. Since the vi rus is systemic (i.e. found throughout the plant) in spinach ( Jones, 1983 ), it is likely to be present in the leaves that would be imported into the United States (thus, it follows the pathway). The virus is spread by the nematode vector, grafting, and seed but not direc t contact between plants ( Jones, 1983 ). Spinach leaves are washed prior to shi pment ( 2007 ) which removes nemato de laden soil and attached seeds. Also, the shipments should be inspected to prevent contamination by seeds from other plants, whether weeds or volunteers, since they may carry the virus. These treatments should remove the potential for the virus to be vectored by a nematode or dispersed by seed, upon arrival in United States. Inspection at Points

- of

- Entry (POE) should verify that any seed, including non

- Federal Noxious Weeds species, is absent from the shipments. If these procedures are followed, the potential for the virus to disperse in United States is minimal and no further analysis is required. However, if seeds or soils are found to be present in shipments of spinach, then there is a potential for dispersal and the risk of this commodity enteri ng the United States should be reevaluated.

2

. 5 Quarantine Pests Likely to Follow the Pathway

Quarantine pests that would reasonably be expected to follow the pathway, i.e. , be included in commercial shipments of spinach (Table 4), will be analyzed in de tail in this risk assessment [Steps 5

- 7 (USDA, 2000)].

Table 4 . Quarantine Pests Likely to Follow the Pathway and Selected for Further Analysis

Copitarsia incommoda Walker (Lepidoptera: Noctuidae)

Liriomyza huidobrensis Blanchard (Diptera: Agromyzidae)

Diabrotica speciosa (Germar) (Coleoptera: Chrysomelidae)

Other quarantine plant pests in this assessment that were not chosen for further scrutiny, may be potentially detrimental to the agricultural production systems of the United States . These pests were

not subjected to further analy sis because organisms identi fied only to the genus or less detailed taxonomic level are not analyzed further, even though individual species within those taxonomic groups are potential pests that may or may not occur with in the United States. The IPPC guidelines do not require risk assessment of pests identified only by genus name ( IPPC

, 2007a)

. By necessity, pest risk assessments focus on those organisms for which adequate biological and taxonomic information is

available . Often there are many species within a genus, and it is not reasonable to assume that the biology of all organisms within a genus is identical. The l ack of species identification may indicate the limits of current taxonomic knowledge

, the life stage or th e quality of the specimen submitted forSpinach from Colombia

Rev.02 December 4, 2007 15 identification. The lack of identification at the specific level does not rule out the possibility that either a high

- risk quarantine pest was intercepted or that the intercepted pest was not a quarantine pest.

Pest s for spinach that are likely to follow the pathway, but repo rted only at the genus or less detailed

taxonomic leve l that already occur in the United States are included in Table 3

, but not further analyzed

in this risk assessment , including arthropods: Ag romyzidae, spp., Agrotis spp., Anasa sp., Anthomyiidae, spp., Aphididae, spp., Aphis sp., Brachycerinae, spp., Cercopidae, spp., Chrysomelidae, spp., Cicadellidae, spp., Coccidae, spp., Conotrachelus sp., Coreidae, spp., Crambidae, spp., Curculionidae, spp

., Delia sp., Diabrotica sp., Diaprepes sp., Diaspididae, spp., Disonycha sp., Feltia

spp., Frankliniella sp., Gelechiidae, spp., Geometridae, spp., Gracillariidae, spp., Gryllidae, spp., Hypothenemus sp., Isonychus sp., Leucinodes sp., Listroderes sp., Ma rgarodidae, spp., Miridae, spp., Myochrous sp., Noctuidae, spp., Nysius sp., Olethreutinae, spp., Orthezia sp., Ortheziidae, spp., Pentatomidae, spp., Pheidole sp., Phlaeothripidae, spp., Pieridae, spp., Plusiinae, spp., Pseudococcidae, spp., Psyllidae, sp p., Pyralidae, spp., Pyrausta sp., Rhinacloa sp., Spodoptera sp., Systena sp., Tephritidae, spp., Tetranychus sp., Thripidae, spp. ; the fungi: Alternaria sp., Ascochyta sp., Cercospora

sp., Cladosporium sp., Colletotrichum sp., Fusarium sp., Peronospora sp
., Phoma sp.
, Pythium sp., Rhizoctonia sp., Sclerotinia sp. ; and the mollusk, Dero c eras sp.

The lack of biological information on any given organism should not be equated with low risk , since vague taxonomic identifications can hide the occurrence of know n or unknown quarantine pests . If the pests identified in this risk assessment at a genus, family, or order level are intercepted on spinach from Colombia in the future, their species specific determination should follow. Q uarantine action can be

taken wh ere appropriate and a re

- ev aluation of their risk may be necessary

. The analys e s of Copitarsia

incommoda and Diabrotica speciosa reasonably encompass the Copitarsia and Diabrotica species identified only to the genus level.

2

. 6 Consequences of Introduct ion

For each of the quarantine pests listed in Table 4 , the potential C onsequences of I ntroduction are rated using five Risk Elements: Climate

- Host Interaction, Host Range, Dispersal Potential, Economic Impact and Environmental Impact. For each Risk Elem ent, pests are assigned a rating of Low (1 point), Medium (2 points) or High (3 points). A Cumulative Risk Rating is then calculated by summing all Risk Element values. The values determined for the Consequences of Introduction for each pest are

summarize d in Table 5

.

Copitarsia incommoda Walker

Copitarsia consueta was found to be a taxonomically invalid name and designated a replacement name of

C. incommoda

. ( Angulo and Olivares, 2003 ; Gould et al ., 2000 ; Simmons and Pogue, 2004 ).

Risk Element #1: Cl imate

- Host Interaction Laboratory studies have indicated that C. incommoda is capable of completing its life

- cycle between 9

and 34 C (Gould et al , 2005)

. T he development time is longer at lower temperatures (9

- 14 C) and decreases with increasing temper ature until 34 C (Gould et al , 2005) . T he developmental time required for an egg to mature to an adult at 20.1 C is 41

- 50 days (Fl o res

- Per ez et al , 2004 Gould et al , 2005),

. Many states such as Iowa and Minnesota in zone 5 are capable of sustaining tha t temperature range or higher for sufficient time during the spring and summer months that an egg could develop into an adultSpinach from Colombia

Rev.02 December 4, 2007 16 ( USDA

- NA., 2003) . States in warmer climates w ould facilitate more rapid development

. In addition, C.

decolora , which is sometim es misclassified as C. incommmoda ( Simmons, R. B., and M. G. Pogue. 2004)

, requires only 38 days to develop from an egg to an adult at 23.9 C (Urra and Apalblaza, 2005) This time suggests a similar climatic range to C. incommod a

. Thus, C. incommo da w o ul d be capable of developing in at least four hardiness zones based during the s pring and summer growing months which

merits a Climate

- Host interaction rating of High (3).

Risk Element #2: Host Range Copitarsia incommoda has been reported feeding on differe nt species in several families : alfalfa, artichoke, asparagus, cabbage, cauliflower

, broccoli, coriander, cut flowers ( Limonium spp. and

Alstroemeria spp), garlic, jojoba, onion, potato, rapeseed, swiss chard, and spinach (Angulo and Olivares, 2003; Bautis ta, et al ., 2003 ). The risk rating for Host Range is High (3).

Risk Element #3: Dispersal Potential A study of C. decolora found that it could survive for a week on deteriorating asparagus (Gould and Maldaonado, 2006). Since C. incommoda is closely rela ted to and confused with C. decolora ( Simmons and Pogue, 2004)

, a reasonable inference would be that C. incommoda could do the same. This ability to survive in garbage or waste plant material could give it the opportunity to be transported by humans or to complete its life

- cycle in factorable environment such as a warehouse

. The ability to disperse with humans could facilitate long

- range transport. In the field

, C. incommoda completed development in 62 days on potato Copitarsia incommoda females are repor ted to lay 1,638 eggs per female on artificial diet;

in Colombia

, Copitarsia is reported to lay 550 eggs per female (Cardona, et al., 2002; Cardona, et al., 2003). The risk rating for Dispersal Potential is High (3).

Risk Element #4: Economic Impact

The ability of Copitarsia to disperse or migrate has implications pertaining to its ability to become a serious pest in the U.S. Copitarsia directly damages crops by reducing the marketability of fruits and vegetables and indirectly by reducing overall yields. In South America, Copitarsia reduced marketability of certain vegetables by 24% and yields of grains by 80

- 90% and

, in Colombia alone, by 33% (Cardona et
al ., 2003). Copitarsia has the potential to affect the U.S. export markets as well. We assume that co untries

where Copitarsia is not established would reject commodities from the U.S. with Copitarsia larvae. The risk rating for Economic Impact is High (3).

Risk Element #5: Environmental Impact Once established, Copitarsia would have the potential to da mage the environment both directly, through feeding on native plants, and indirectly

, because of environmentally harsh methods used to control pest populations. Nearly 700 plants native to the U.S. are in the genera known to be attacked by Copitarsia larv ae. Seve ral of the native species at risk from Copitarsia are listed as threatened or endangered by the U.S. Fish and Wildlife Service : Allium munzii (CA), three species of Trifolium (CA, AR, IN, KY, WV, MO, OH), two species of Helianthus (NM, TX, NC, SC) (USFWS, 2007 ) . Indirect environmental damage could be caused by initiation of new biological or chemical control programs that may potentially affect non

- target organisms in the ecosystem (Cardona et al ., 2003 ). It is not known, however, if such new progra ms would be necessary since Copitarsia incommoda might be effectively controlled by the measures already in place against other pests on host commodities. The risk rating for Environmental Impact is Medium ( 2 ).Spinach from Colombia

Rev.02 December 4, 2007 17 Diabrotica s peciosa (Germar)

Risk Elemen t #1: Climate

- Host Interaction

D istribution o f Diabrotica speciosa is known in Central and South America. The pest is recorded in the north, from countries with the tropical climate (e.g. Costa Rica, Panama, Colombia, Brazil ) and in the south (Argentina) where climate is warm temperate to temperate. This distribution pattern corresponds to US plant hardiness zones 8

- 10 ( USDA

- NA., 2003 ). The risk rating is Medium (2).

Risk Element #2: Host Range Diabrotica speciosa is highly polyphagous as an adult, wit h more than 70 host species recorded ( CAB
International, 2006 ). The root

- feeding larva is also polyphagous, but its known host range is narrow er and includes maize, wheat, groundnut, soy beans and potato ( CAB International, 2006 ). Among major hosts are

Ara chis hypogaea Glycine max ( Fabaceae ), Capsicum spp.
, Solanum tuberosum (Solanaceae)

, Cucurbita

maxima and C. pepo ( Cucurbitaceae ), Triticum and Zea mays ( Poaceae ) ( CAB International, 2006 ). Other hosts of agricultural importance include plants from the f amilies Chenopodiaceae ( Beta vulgaris )

, Brassicaceae (cruciferous crops), Rutaceae ( Citrus spp.), Malvaceae ( Gossypium spp. ), Astraceae ( Helianthus annuus

, Lactuca sativa ), Rosaceae ( Prunus persica ) ( CAB International, 2006 ). Know n wild

hosts are Amaranthu s quitensis (Amaranthaceae) and Cynara cardunculus ( Cucurbitaceae ) ( CAB
International, 2006 ). The risk rating is High (3),

Risk Element #3: Dispersal Potential Diabrotica speciosa is a multivoltine, polyphagous species, which overwinters as an adult and is fairly tolerant to cold (EPPO, 2005)

. The species undergoes three larval instars

. Duration of the larval stage is

23

- 25 days ( including pre

- pupal period of 2

- 3 days ) ( CAB International, 2006 )

. T he pupal stage lasts 6 days, and is followed by a period of 3

- 5 days during which the recently moulted adults remain in the pupal case before eclosion . In laboratory conditions, mating has been observed between 4 and 6 days after emergence, and some females were observed mating again at day 35 ( CAB International , 2006 )

. Each female laid an average of 1164 eggs during her lifetime with p eak oviposition from days 16 to 56. The number of overlapping generations is conditioned to the climate, being continuous in tropical areas. In the Buenos Aires area in Argentina, observations indicate there are about three generations per

year ( CAB International, 2006 )

. D iabrotica speciosa can move locally by adult flight, and probably by movement of eggs, larvae or pupae in soil contaminating vehicles or farm machinery. Adults ar e active and are not likely to stay with the trade commodity. The risk rating is High (3)

.

Risk Element #4: Economic Impact Significant damage to agricultural crops is caused by both adults and larv a e which reduces the yield and the commodity value. Pesti cide s are often appli ed to control th is pest lead ing to the increased cost of production. Diabrotica speciosa is on EPPO A1 action list of pests (EPPO, 2005) and is absent from most of the worlds regions (e.g. Africa, Asia, Australia). Thus, i ntroduction of D. speciosa into the United States will cause loss of potential foreign and domestic markets. The risk rating is High.

Risk Element #5: Environmental Impact The following species are listed as Threatened or Endamgered in the Continental United States: Cucurbita okeechobeensis ssp. o keechobeensis (FL) , Helianthus paradoxus (NM, TX), H. schweinitzii (NC, SC)

, Prunus geniculata (FL), Amaranthus pumilus (DE, MD, NJ, NY, NC, SC, VI) (USFWS, 2007)

. Although some natural enemies of D. speciosa are known

, no biocontrol programs ha ve been implemented so far for this insect ( CAB International, 2006 ). Stimulation of new chemical controlSpinach from Colombia

Rev.02 December 4, 2007 18 programs, however, is likely upon i ntroduction of D. speciosa into the United States since soil and foliar pesticides are common ly used against this pest in the areas of its current establishment (EPPO, 2005)

. The hypogeal habitat of the larvae requires intensive and copious use of insecticides in order to

achieve control (CABI, 2006)

. Risk rating is High.

Liriomyza huidobrensis Blanchard

Risk Element #1: Climate

- Host Interaction

The hosts for Liriomyza huidobrensis belong to fifteen families ( CAB International, 2006 ; Braun and Shephard, 1997; DEFRA, 2001; EPPO 2003; Parrella, 1982; Posada, 1989; Saldarriaga et al. , 1987;

Stec k, 1999 ) and are present in plant hardiness zones 8

- 10 of the Contine n tal United States ( ARS,

1990 ). where the pest has the potential to establish a breeding colony

. Liriomyza huidobrensis is a pest

in tropical to warm temperate region s ; it has also been f ound at altitudes of up to 3000m (9,842,52ft.)

above sea level . The pest is able to survive a freez e of

- 18.7°C (

- 65.66°F) ( CAB International, 2006 ).

The behaviour of L. huidobrensis gives it a greater climatic range for survival ( CAB International,

2006 ). In some parts of Europe, it has the ability to become a major pest of a wide variety of ornamental or vegetable crops grown under glass ( CAB International, 2006 ). Chen and Kang (2004)

showed that i n China, winter temperatures b e low

- 4 o C and

- 6 o C we re limi ting establishment of breeding populations of L. huidobrensis

. The risk rating for Climate

- Host interaction is Medium (2).

Risk Element #2: Host Range
The primary hosts for Liriomyza huidobrensis are Abelmoschus esculentus, Allium cepa

, Allium

porrum , Al lium sativum

, Apium graveolens

, Capsicum frutescens

, Chrysanthemum x morifolium

, Cichorium sp., Cineraria sp., Cucurbita maxima, Cucurbita moschata, Cucurbita pepo, Cynara scolymus

, Daucus carota

, Delilia sp., Dendranthema sp., Dendranthema x grandiflorum

, Galinsoga

sp.
, Hordeum vulgare , the Inulae family, Lactuca sativa

, Matthiola incana, Parthenium argentatum,

Pastinaca sativa

, Phaseolus vulgaris

, Phaseolus vulgaris var. humilis

, Phlox sp., Piper nigrum

, Pisum

sativum

, Pisum sativum var. arvense , Pterocau lon sp., Taraxacum officinale , and Senecio vulgaris (Braun and Shephard, 1997; CAB International, 2006 ; DEFRA, 2001; EPPO 2003; Parrella, 1982; Posada, 1989; Saldarriaga et al. , 1987; Steck, 1999 ). The secondary hosts for L. huidobrensis are Amaranthus sp.
, Amaranthus retroflexus

, Aster sp.
, Beta vulgaris

, Beta vulgaris var. cicla

, Beta vulgaris var. saccharifera

, Calendula sp.
, Cannabis sativa subsp. sativa

, Capsicum annuum

, Citrullus

lanatus

, Cucumis sp., Cucumis melo , the Cruciferae family, Cucumis sativ us , Dahlia sp., Datura sp.
, Dianthus caryophyllus

, Gerbera sp.
, Gypsophila paniculata

, Lathyrus sp., Lathyrus odoratus

, Linum

sp.
, Linum usitatissimu m , Lisianthus russelianus

, Lycopersicon esculentum

, Medicago sp., Medicago

sativa

, Melilotus sp.
, Petunia sp.
, Primula polyanthus

, Raphanus sativus

, Solanum melongena

, Solanum tuberosum

, Solanum tuberosum ssp. andigena

, Spinacia oleracea

, Tagetes sp.
, Tropaeolum

sp.
, Tropaeolum majus, Valerianella locust

, Verbena sp.
, Vicia faba

, Viola sp., Zinnia sp., and Zin nia elegans . The wild hosts for L. huidobrensis are Oxalis sp.
, Bidens pilosa

, Emilia sonchifolia

, Galinsoga parviflora

, Portulaca oleracea

, Sonchus sp., and Sonchus oleraceus ( CAB International, 2006 ; Braun and Shephard, 1997; DEFRA , 2001; DEFRA, 2004; Pa rrella, 1982; Posada, 1989; Saldarriaga et al.

, 1987; Spencer, 1984; Steck, 1999 ). Liriomyza huidobrensis was found in consignments on Dendranthema morifolium

, Eryngium sp., and Gypsophila sp. (EPPO, 2003). In Guatemala, L.

huidobrensis attacks Cichorium i ntybus (MacVean and Pérez, 1996). Weeds

, such as Trianthema portulacastrum

, Stachys arvensis

, Chenopodium murale

, C. album, Datura stramonium

, Bidens pilosa

, Galinsoga parviflora

, Diplotaxis muralis

, Malva parviflora

, Ricinus communis , and Stellaria media

,Spinach from Colombia

Rev.02 December 4, 2007 19 are other hosts for L. huidobrensis (Mujica and Cisneros, 1996) . In Colombia, L. huidobrensis has been found on the following hosts: Allium cepa

, Alstroemeria sp., Amaranthus spinosus

, Beta vulgaris

, Beta vulgaris var. cicla, Beta vulgaris var. crassa , Br assica oleracea var. capitata

, Capsella bursa

- pastoris

, Capsicum sp., Chrysanthemum sp., Cucumis sativus

, Dendranthema grandiflora

, Galinsoga

caracasana , Galinsoga parviflora

, Gazania sp., Gypsophila elegans

, Hordeum vulgare

, Petunia sp.,
Pisum sativum

, Ph aseolus vulgaris

, Phaseolus vulgaris var. humilis, Portulaca oleracea , Sechium edule, Solanum tuberosum ssp. andigena

, Solanum melongena

, Spinacia oleracea and Vicia faba (Figueroa, 1977; Gallego and Vélez, 1992; Hincapie et al. , 1991; Posada, 1989; Santia go, 2000; Sigueñas, 1995; Spencer, 1984). Furthermore, the list of hosts increases as L. huidobrensis invades new countries ( Tømmerås e t al ., 2002). Liriomyza huidobrensis attacks multiple species among multiple plant families; consequently

, the risk ratin g for Host Range is High (3).

Risk Element #3: Dispersal Potential The plant parts liable to carry Liriomyza huidobrensis in trade or transport are leaves and seedlings ; transport pathways for long distance movement are conveyances (road and air transport ), travel l ers and baggage (land, sea and air) (CAB International

, 200 5 ). Dispersal over long distances is on plant material, cut flowers and soil. The pest may also be dispersed on equipment and containers that have not been properly cleaned (Tømmerås e t a l ., 2002).

The L. huidobrensis mating process takes place 24 hours after emergence ; a single mating is sufficient to fertilize all eggs left. In Peru, the mean number of eggs laid per female is 117 in winter, and 161 in spring (CAB International , 200 6 ). T he duration of its life

- cycle depends on temperature: egg stage (2.9 to 6 days)

, larval stage (6 to 13 days) , and pupal stage (7.4 to 21.1 days). The longevity of the females and males depends on temperatures and food availability: 3.5 to 32.6 days for fem ales and 2.1 to 15.1 days for males (Braun and Shepard, 1997). In Colombia, the duration of the life

- cycle of L.

huidobrensis reared on Allium cepa at 24oC (75.2oF) , with a relative humidity of 75% are the following: egg stage (1.5 days)

, larval stage (7 d ays) , and pupal stage (8.2 days). The longevity of the females in this case was 15 days (Hincapie et al. , 1991). Successful emergence to the adult stage is highly dependent on the host plant, ranging from 36% to 74% (Steck, 1999). The risk rating for Dispe rsal Potential is High (3).

Risk Element #4: Economic Impact Liriomyza leafminers impact crops by destroying young seedlings, causing reductions in crop yields, reducing the aesthetic value of ornamental plants, and causing some plant species to be quaran tined (Parrella, 198 2 ). Adult sting and larval mining of leaves reduce photosynthetic capacity, render leaves unmarketable, and provide an entrance for disease organisms (Mou and Ryder, 2003).

Liriomyza huidobrensis damage is caused by larvae mining into leaves and petioles. Severely infested leaves may fall, exposing plant stems to wind action. The presence of unsightly larval mines and adult punctures in the leaf palisade of ornamental plants can further reduce crop value. In young plants and seedlings, mining may cause considerable delay in plant development, leading to plant loss. Liriomyza

huidobrensis is a major quarantine pest and is officially listed in many areas of the world ( CAB International, 2006 ). The risk rating for Economic Impact for Liriom yza huidobrensis is High (3).Spinach from Colombia

Rev.02 December 4, 2007 20 Risk Element #5: Environmental Impact Liriomyza huidobrensis is reported on different plant species. Some of the genera of these species are included in plants listed as endangered and threatened in the Continental U.S.: Alli um, Amaranthus, Cucurbita, Eryngium, Phlox, Primula, Taraxacum, Senecio, and Verbena (USFWS, 2007 ) . These plants may be potential hosts

, although no specific data are reported in the literature to date.

Liriomyza huidobrensis has spread to other continent s where established populations are growing and more difficult to control. This is at least partly due to a shift in the susceptibility of this pest to insecticides (Steck, 1999). New control programs might be initiated if its introduction occurs. The risk rating on Environmental Impact for L. huidobrensis is High (3).

The Consequences of Introduction are summarized in the Table 5 *.

*Rating interpretation: Low: 5

- 8, Medium: 9

- 12, High: 13

- 15.

2

. 7 Likelihood of Introduction

These pests are rated for the Likelih ood of Introduction based on two separate components. First, an estimate is made concerning the amount of commodity likely to be imported (Sub

- Element #1). Then pest opportunity is estimated by using five biological features (Sub

- Elements #2

- 6) ( USDA

, 2000 ). These ratings and the value for the Likelihood of Introduction are summarized in Table 6

.

Risk Element #6: Pest Opportunity

Sub

- Element #1: Quantity of commodity imported annually The average production of spinach in Colombia in 2002 was 1,600 tons f or 106 hectares (Ministerio de Agricultura y Desarrollo Rural, 2003) . Spinach is mainly destined for local consumption. I nitially, i t is expected that only a portion of all produced spinach will be exported to the United States. Table 5 . Risk Rating for Consequences of Introduction

Pest Risk

Element

#1 Risk

Element

#2 Risk

Element

#3 Risk

Elemen t
#4 Risk

Element

#5 Cumulative

Risk Rating Climate/Host

Interaction Host Range Dispersal

Potential Economic Impact Environmen tal Impact

Copitarsia

incommoda High (3) High (3) High (3) High (3) Medium (2) High (1 4 )

Diabrotica speciosa Medium (2) High (3) High (3) High (3) High (3) High ( 14 )

Liriomyza

huidobrensis Medium (2) High (3) High (3) High (3) High (3) High (1 4 )Spinach from Colombia

Rev.02 December 4, 2007 21 If we consider, however, t hat all of the spinach will be exported to the United States and that a shipping container (40 cubic fee t) can transport an average of 20 tons of commodity

, the total number of containers

will be 80. Thus, th e quantity initially exported annually is Mediu m (2 points): 10

- 100 shipping containers (40 cubic foot) per year.

Sub

- Element #2: Survive post

- harvest treatment Once the spinach is harvested

, it is recommende d that it be store d at a relative humidity of 90% to 95%

and at a temperature between 0 oC to 5 oC (Saltveit, 2001). A t the beginning of the post

- harvest season
, the product is rated and washed . At this point

, the external feeders are removed from the leaf surface ; leav es with leafminers are rejected. Leaves that are affected by pests, diseases, an d other foreign

substances are discarded

.

Although Copitarsia incommoda and Liriomyza huidobrensis could be visually detected, the above

described post

- harvest procedure do es not ensure that these pests will be successfully removed from the commodity in e ach shipment , as records of interceptions indicate

. The risk associated with this

sub

- element for both pests is High (3). Only adults of Diabrotica speciosa feed on spinach leaves. This stage is mobile and is likely to be removed during washing process. T he visual detection of adults is easy , with the feeding period span ning from dawn until dusk ( CAB International, 2006 ). The risk rating is Medium (2) for D. speciosa

.

Sub

- Element #3: Survive shipment

Since species of Copitarsia , Diabrotica, and Liriomyz a were intercept ed at U.S. ports

- of

- entry multiple

times on different commodities including spinach ( AQAS

, 200 7 )

, this risk factor is rated High (3).

Sub

- Element #4: Not detected at the port of entry Colombia does not have a point

- of

- origin protocol for v egetable inspection. PPQ officers at ports

- of

- entry are instructed to inspect 2% of a given shipment arriving at a U.S. port. PPQ officers consider that more

than 10% of the viable larvae of Copitarsia that arrive at a port are not be detected by routine i nspections (Gould et al ., 2000)

. Consequently

, the risk rating for this sub

- element is High (3)

.

In the case of Liriomyza huidobrensis , the feeding punctures appear as white speckles between 0.13 and 0.15 mm in diameter. Oviposition punctures are smaller (0.05 mm) and are more uniformly round. The larva is primarily a leaf miner. Mines are usually white with dampened black and dried brown areas, and are usually associated with the midrib and lateral leaf veins. Mines are typically serpentine, tightly coile d and of irregular shape, increasing in width as larvae mature. Several larvae feeding on a single leaf may produce a secondary 'blotch' mine type and leaf wilt may occur ( CAB International, 2006 ). Since leaves attacked by Liriomyza huidobrensis can be vis ually detected, the risk associated with the inability to detect these pests is Medium (2).

T here are multiple interceptions of Diabrotica species at ports

- of

- entry

. Because only adults are expected to be with the spinach leaves , they are external feeder s and are eas il y detect ed ( CAB International, 2006 )

, we rate D. speciosa Medium (2) for this risk factor.

Sub

- Element #5: Imported or moved to area with environment suitable for survival The consumption and demand for spinach is not likely to be concent rated in cert ain areas of the United

States and associated with certain et h nic market demands. T he risk associated with this sub

- element willSpinach from Colombia

Rev.02 December 4, 2007 22 likely dependent on the proportion of the United States having suitable habitat ( i.e., climate and hosts) for

the quarantine pests

.

After Copitarsia larvae or eggs enter the U.S., they must undergo further rigors of shipment, and not all

final destinations will have climates suitable for survival. It is consider ed that some viable insects that

were not detected at a port

- of

- entry would be transported to this climati cally suitable habitat. The proportion of shipments arriving to areas with suitable environmental conditions will mainly depend on

the number of people living in those areas which is approximately 39% ( Ve nette and Gould

, 2006), Consequently, the risk rating for this sub

- element is High (3)

.

Leafminers represent a n important problem for spinach and other leafy commodities in vegetable growing regions

. Climatic requirements for establishment of L

. huidobr ensis indicate that a suitable habitat will comprise at least three plant hardiness zones which is more than 30% of the territory of the Continental

United States (Venette and Gould, 2006)

. The risk potential is High (3).

Diabrotica speciosa is widely di stributed through Central and South America

, from tropical climates to

warm temperate

, such as Argentina

. The pest is anticipated to be able to establish at least in three plants

hardiness zones , or more than 30% of the area of the Continental Un i ted State s (Venette and Gould, 2006

. The risk rating is High (3).

Sub

- Element #6: Come into contact with host material suitable for reproduction

N umerous hosts of Copitarsia incommod a , Diabrotica speciosa, and Liriomyza huidobrensis are present and highly cultivat ed in the continental United States . All three species possess natural mechanisms for successful dispersal toward potential host s; the rating for th is risk factor is High (3).

The likelihood of introduction is presented in Table 6 *

. .

Table 6 . Risk Rat ing for Likelihood of Introduction

Pest Sub

Element

#1 Sub

Element

#2 Sub

Element

#3 Sub

Element

#4 Sub

Element

#5 Sub

Element

#6 Cumulative

Risk

Rating Quantity Imported Annually Survive

Post

Harvest

Treatment Survive Shipment Not

Detected at

Port of Entry Moved to

Suitable

Habitat Contact

with Host

Material

Copitarsia

incommoda Medium ( 2 ) High (3) High (3) High (3) High (3) High (3) High (1 7 )

Diabrotica speciosa Medium (2) Medium (2) High (3) Medium (2) High (3) High (3) High (15)

Liriomyza

huidob rensis Medium (2) High (3) High (3) Medium (2) High (3) High (3) High (1 6 )

* Rating interpretation: Low: 6

- 9, Medium: 10

- 14, High: 15

- 18.Spinach from Colombia

Rev.02 December 4, 2007 23 2

. 8 Pest Risk Potential and Conclusion

The sum of the Cumulative Risk Rating for the Consequences of Introduction and the Cumulative Risk Rating for the Likelihood of Introduction of Liriomyza huidobrensis and Copitarsia incommoda

, shown

in Table 7

, clearly indicate that these species pose a High Pest Risk Potential (30 and 31 points

, respectively).

Table 7 . Pest Ri sk Potential

Pest Consequences of

Introduction Cumulative Risk Rating Likelihood of

Introduction

Cumulative Risk Rating Pest Risk Potential

Copitarsia

incommoda High ( 1 4 ) High (1 7 ) High ( 3 1 )

Diabrotica speciosa High (1 4 ) High (15) High ( 29 )

Liriomyza

h uidobrensis High (1 4 ) High (1 6 ) High ( 3 0 )

Cumulative rating interpretation: Low: 5

- 18, Medium: 19

- 26, High: 27

- 33.

High risk rating of 29

- 30 is a baseline estimate of the risks associated with this importation, and reduction of risk occurs through the us e of mitigation measures. The guidelines state that a High Pest Risk Potential means that specific phytosanitary measures are strongly recommended, and that port

- of

entry inspection is not considered sufficient to provide phytosanitary security.

Copitar sia incommod a , Diabrotica speciosa, and Liriomyza huidobrensis can be detected during port

of

- entry visual inspections. This measure could be used in order to reduce the risk associated with the introduction of these pests but , only in combination with oth er measures. The Risk Mitigation Options Section is presented in the Appendix 2 , however, selection of the specific measures is a part of the risk management document and is not addressed here.Spinach from Colombia

Rev.02 December 4, 2007 24 III. Literature Cited

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- CMAVE on April 8th, 2004. Saldarriaga, A., Zenner De Polonia, I., Cardenas, R., Posada, L., and F. Garcia. 1987. Guía para el control de plagas. Manual d e asistencia técnica No.1 Cuarta edición. ICA. Saltveit, M.A. 2001. A summary of CA requirements and recommendations for vegetables. pp 71

- 94.Postharvest Horticulture Series No. 22A, University of California, Davis. Santiago, J. 2000. Diagnostico del Uso y Manejo de Plaguicidas en Tres Cultivos Horticolas en la Sabana de Bogotá y Propuesta de un Indice de Predicción de Residuos de Plaguicidas. Facultad de Agronomía. Universidad Nacional de Colombia. Bogota, Colombia. Scheffer, S. J. 2000. Molecular evidence of cryptic species within the Liriomyza huidobrensis (Diptera: Agromyzidae). Journa l of Economic Entomology. Volume: 93, Issue: 4, Pages: 1146

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Rev.02 December 4, 2007 29 Scheffer, S.J., Wijesekara, A., Visser, D. and R. H. Hallett. 2001. Polymerase Chain Reaction

restriction fragment

- length polymorphism method to distinguish Liriomyza huidobrensis from L. langei (Diptera: Agromyzidae) applied to three recent leafminer invasions. Horticultural Entomology. Journal of Economic Entomology 94(5): 1177

- 1182. <http://esa.edoc.com/

ec onomic/v94n5/v94n5p1177.pdf> Scheffer, S. J. 2004. Personal communication with Sonja J. Scheffer, Ph. D., Systematic Entomology Laboratory, USDA. Beltsville, on April 2nd, 2004. Selvaradjou, S.

- K., L. Montanarella, O. Spaargaren, and D. Dent. 2005. S oil Maps of Latin America and Caribbean Islands. European Digigtal Archive of Soil Maps. Sigueñas, S. 1995. El Cultivo de la Espinaca . Instituto Nacional de Investigación Agraria. Programa Nacional de Investigación en Hortalizas. Proyecto Sistema Nacional de De Investigación y Transferencia de Tecnología Agraria. Lima Perú. Simmons, R. B.

, and M. G. Pogue. 2004. Redescription of Two Often

- Confused Noctuid Pests, Copitarsia decolora and Copitarsia incommode (Lepidoptera: Noctuidae: Cuculliinae)

. Ann.

Entomol . Soc. Am. 97(6): 1159

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. Spencer, K.A. 1984. The Agromyzidae (Diptera) of Colombia, including a new species attacking potato in Bolivia. Department of Biological Sciences, University of Exeter, England. Revista Colombiana de Entomología. Vol. 10 Nos. 1

- 2, 1984. p. 3.33. Steck, G.J. 1999. Pea Leafminer, Liriomyza huidobrensis (Blanchard) (Insecta: Diptera: Agromyzidae).

EENY

- 111 (originally published as DPI Entomology Circular No. 378). Featured Creatures. Entomology and Nematology Department, Florida C ooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida. http://edis.ifas.ufl.edu/ pdffiles/IN/IN26800.pdf Thome, J.W., P.H. dos Santos, and L. Pedo tt (1997). Annotated list of Veronicellidae from the collections of the Academy of Natural Sciences of Philadelphia and the National Museum of Natural History, Smithsonian Institution, Washington, D.C., U.S.A. (Mollusca: Gastropoda: Soleolifera). Proc

. Bio

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. Wash .: 520

- 536. Tømmerås, B.A., Jelmert, A., Rafoss, T., Sundheim, L., Ødegaard F., and B. Økland. 2002. Report no. 15. Globalisation and Invasive Alien Species. Norwegian Institute for Nature Research (NINA). Norwegian Ministry of Foreign Affairs. <http://odin.dep.no/archive/ udvedlegg/01/04/glob1064.pdf> Tunçbilek, A. S., A. Ayvaz, F. Öztürk, and B. Kaplan. 2003. Gamma radiation sensitivity of larvae

and adults of the red flour beetle, Tribolium castaneum Herbst. Anzeiger fur Schadlingskunde/Jo urnal of Pest Science 76: 129

– 132. Urra, F. and J. Apablaza. 2005. Threshold temperature and thermal constant for the development of Copitarsia decolora (Lepdioptera: Noctuidae). Ciencia y Investigacion Agraaria. 32: 16

- 23. USDA and NRCS, 2002. The PLAN TS Database, Version 3.5 <http://plants.usda.gov> National Plant Data Center, Baton Rouge, LA 70874

- 4490 USA. USDA. 2000. Guidelines for pathway

- initiated pest risk assessments (version 5.02), USDA

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PPQ, MD. < www.aphis.usda.gov/ppq/pra/active >
USDA. 2002a. Online Manuals. Regulating the Importation of Fresh Fruits and Vegetables. Nonpropagative Manual. USDA, MRP, APHIS, PPQ. www.aphis.usda.gov/ppq/manuals

USDA

- NA. 2003. The 2003 US National Arbo retum "web version" of the USDA Plant Hardiness Zone Map. United States Department of Agriculture (USDA), National Arboretum (NA). Last accessed October 20, 2006, http://www.usna.usda.gov/Hardz one/ushzmap.html

. USDA. 2007. Electronic Code of Federal Regulations. Title 7: Agriculture. Part 330: F ederal P lant

P est R egulations ; G eneral ; P lant P ests ; S oil , S tone and Q uarry P roducts ; G arbage

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Rev.02 December 4, 2007 30 http://ecfr.gpoaccess.gov/cgi/t/text/textidx?c=ecfr&sid=64938ae67d906f1fc8ba68b478241a07 &rgn=div5&view=text&node=7:5.1.1.1.8&idno=7 (Accessed August 17, 2007)

. USEPA. 2006. Environmental Protection Agency: Irradiation for Postharvest and Quarantine Control. http://www.epa.gov/Ozone/mbr/casestudies/volume2/irad2.html (Accessed Augsut 17, 2007).

USFWS. 2007. USFWS Threatened and Endangered Species System (TESS)

. U.S. Fish and Wildlife

Service

. < http://ecos.fws.gov/tess_public/SpeciesReport.do?groups=Q&listingType=L&mapstatus=1 > Last accessed 09 Jul. 2007. Venette, R. C. and J. R. Gould. 2006. A pest risk assessment for Copitarsia spp., Insects associated with importation of commodities into the United States. Euphytica 148: 165

– 183. Volveras, B., E. Amezquita, and H. Tafur. 2007. Efecto del tiempo de uso en las condici ones fisicas del suelo andino en el departamento de Narino, Colombia. Acta Agronomia 56(1). Walsh, G. C. 2003. Host r ange and r eproductive t raits of Diabrotica speciosa (Germar) and Diabrotica

viridula (F.) (Coleoptera: Chrysomelidae), t wo s pecies of South American p est r ootworms, with

n otes on o ther Species of Diabroticina

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. Entomol

. 32(2) : 276

- 285. WSSA. 2006. Weed List. Weed Science Society of America (WSSA). Last accessed November 28, 2006, http://www.wssa.net/weednames/common.asp

. Wiersema, J. and Le ό n, B. 1999. World economic plants. CRC Press, Washington, D.C.

IV. Preparers and Reviewers

Preparer :

Luis Ernesto Forero , Agronomist, Risk Analyst Center for Phytosanitary Excellence, CEF

Pest Risk A ssessment Staff, Center for Phytosanitary Excellence, CEF :

Boris Orduz, Entomologist, Risk Analyst Elkin Florez, M. Sc. Phytosanitary Protection, Risk Analyst Guiovanni Zambrano, Risk Analyst Olivier Parfait, Biologist, Risk Analyst

Reviewers :

Hernan Arango

, M. Sc. Phytosanitary Protection, Risk Analyst Colombian Agricultural Institute (ICA), Risks Analysis Group Agricultural and Rural Development Ministry, Colombia Marina Zlotina, Entomologist, Risk Analyst John Rogers , Plant Pathologist, Ri sk Analyst

, USDA

- APHIS

- PPQ

- CPHST

- PERAL, R aleigh, NC

Acknowledgements

We are especially grateful for the ongoing support and technical expertise of the USDA

- APHIS

- PPQ

CPHST Unit, in particular, Heather Hartzog

, Kenneth R. Lakin, Leah Millar, and Marin a Zlotina

.Spinach from Colombia

Rev.02 December 4, 2007 31 Appendix 1. Port Information Network PIN (1985

- 2007) Interceptions on Spinacia oleracea

Pest Origin Location of Interception Number of Interceptions

Acarina, species of Japan Ships Stores 2

Agromyzidae, species of Argentina, Belgium, Brazil

, Colombia, Costa Rica, Dominican Republic, Ecuador, El Salvador, France, Guatemala, Hawaii, India, Italia, Japan, Jordan, Lebanon, Mexico, Netherlands, Peru , Spain,

St. Ki tts and Nevis, Syria,

Venezuela Baggage,

Permit Cargo, Ships

Stores 45

Anthomyiid ae, species of Mexico Permit Cargo 1

Aphididae, species of Belgium, Brazil, Colombia, Dominica, El Salvador, Greece, Jamaica, Japan, Korea, Mexico, Netherlands, Nigeria, Panama, Peoples  ́ Republi c of China , Spain,
Korea, West Germany Baggage,

Permit Cargo , Ships

Stores 36

Aphis sp. Dominica General Cargo 1

Artipus sp. Jamaica General Cargo 1

Ascochyta sp. United Kingdom General Cargo 1

Athalia sp. Japan Baggage 1

Auchenorrhyncha, species of Dominica Permit Cargo

, Ships

Stores 7

Brachycerinae, spec ies of Dominica Baggage 1 Cercopidae, species of Mexico Permit Cargo 1 Cercospora sp. Asia (c ountry) Baggage 1 Charidotella trisignata (Boh.) Guayana Baggage 1

Chrysomelidae, species of Dominica, Mexico Ships Stores, Permit Cargo 2

Cicadellidae, species of Dominica, Mexico Baggage, Permit Cargo 5

Coccidae, species of India, St. Lucia Baggage 2

Colletotrichum sp. Vietnam Baggage 1

Conotrachelus sp. Mexico Ships Stores 1

Copitarsia sp. Colombia, Mexico Permit Cargo, Ships

Stores 16Spinach from Colombia

Rev.02 December 4, 2007 32 Pest Origin Location of Interception Number of Interceptions

Coreidae, s pecies of Jamaica Baggage 1 Crambidae, species of Dominica Baggage 1 Cryptomphalus aspersus Mexico Ships Stores 1 Curculionidae, species of Mexico Baggage 1

Delia sp. United Kingdom Ships Stores 1

Diabrotica s p. Mexico Permit Cargo 1

Diabrotica

un decimpunctata,

Diabrotica

duodecimnotata Harold Mexico Permit Cargo 7

Diaphania sp. Nigeria, Trinidad and Tobago Baggage 3 Diaprepes sp. St. Kitts and Nevis Baggage 1 Diaspididae, species of Dominica Baggage 1 Diptera, species of Korea, United King dom Ships Stores 2

Discula sp. Dominica Permit Cargo 1

Disonycha sp. Mexico Permit Cargo, Baggage 2

Empoasca sp. Mexico Baggage, Permit Cargo 3

Frankliniella sp. Unknown Ships Stores 1

Gelechiidae, species of Dominica, Ghana, Nigeria Baggage,

Per mit Cargo 14

Geometridae, species of Japan, Lebanon Baggage, Permit Cargo 2

Gracillariidae, species of Dominica General Cargo 1

Gryllidae, species of Dominica Permit Cargo 1 Hypera sp. Jordan Baggage 1 Hypothenemus sp. Jamaica Baggage 1 Isonychus sp. Venezuela Ships Stores 1 Lachnopus sp. Dominican Republic Permit Cargo 1

Lepidoptera, species of Dominica, Guyana, Nigeria, St.

Croix Baggage,

General Cargo, Permit Cargo 8

Leptinotarsa sp. Jordan Baggage 1

Leucinodes sp. Nigeria Baggage 1

Listrod eres sp. Japan, Mexico Baggage 2 Lobometopon metallicum Mexico Permit Cargo 1 Lygaeoidea, species of Mexico Ships Stores 1 Lygocoris sp. Belgium Ships Stores 1 Margarodidae, species of Nigeria Baggage 1Spinach from Colombia

Rev.02 December 4, 2007 33 Pest Origin Location of Interception Number of Interceptions

Miridae, species of Domi ni ca, Haiti, Mexico Ba ggage, General Cargo, Permit Cargo 8

Myochrous sp. Haiti Baggage 1

Noctuidae, species of Antigua and Barbuda , Belgium, Colombia, Dominica, Ecuador, Guatemala, Haiti, Jamaica, Japan, Korea, Mexico, Panama, Puerto Rico, Republic of China, Spain, St.

Chr istopher, St. Kitts and N evis

, Venezuela Baggage,

General Cargo,

Permit Cargo, Quarters, Ships Stores 58

Nysius sp. Mexico, Nigeria Baggage, Permit Cargo 5

Olethreutinae, species of Dominica, Venezuela, Permit Cargo, Ships

Stores 2

Orthezia sp. Domin ica Permit Cargo 1 Ortheziidae, species of Dominica Baggage 1 Oxycarenus pallens India Baggage 1 Pachybrachis sp. Mexico Permit Cargo 1 Pegomya sp. Mexico Quarters 1

Pentatomidae, species of Haiti, Dominica, Dominican Republic Baggage,

Permit Car go 4

Phaedon sp. Republic of China Permit Cargo 1

Pheidole sp. Nigeria Baggage 1 Phlaeothripidae, species

of Jordan Baggage 1

Phoma sp. Netherlands Permit Cargo 1

Pier idae, species of St. Kitts and N evis Baggage 1

Planococcus minor Dominica Genera l Cargo, Permit Cargo 2

Plusiinae, species of Nigeria Baggage 1

Pseudococcidae, species

of Antigua and Barbuda, Dominica, Nigeria, St. Kitts and Nevis, St.

Thomas Baggage, Permit Cargo 8

Psyllidae, species of El Salvador Baggage 1

Pyralidae, species of Dominica, Guyana Baggage, Permit Cargo 3

Pyrausta sp. Antigua and Barbuda, Dominica,

Mexico Baggage,

General Cargo, 9Spinach from Colombia

Rev.02 December 4, 2007 34 Pest Origin Location of Interception Number of Interceptions

Permit Cargo

Pyraustinae, species of Antigua and Barbuda, Dominica, Dominican Republic, Haiti, Jamaica, Mexico, Nigeria, Peru,

Vene zuela Baggage,

Permit Cargo, Ships

Stores 22

Rhinacloa sp. Dominica Permit Cargo 1

Sitona crinita Ecuador Ships Stores 1

Spodoptera sp. Haiti, Japan, Mexico, Republic of China, Yugoslavia Baggage,

General Cargo,

Permit Cargo, Quarters 7

Steiarrhinus sp. Dominica Permit Cargo 2

Systena sp. Mexico General Cargo 1

T ephritidae, species of Jordan Baggage 1

Thripidae, species of Mexico, Nigeria Baggage, Quarters 3

Tortricinae, species of Dominica Baggage, Permit Cargo 3

Toxoptera citricida Antigua a nd Barbuda Baggage 1

Veronicella sp. Dominica General Cargo 1Spinach from Colombia

Rev.02 December 4, 2007 35 Appendix 2. Mitigation of Quarantine Pests of Spinach from Colombia

A risk assessment for Spinach, Spinacea oleracea L., exported from Colombia to the coterminous

United Stat es determined that three quarantine pests would reasonably be expected to follow the pathway. They are: Copitarsia incommoda Walker (Lepidoptera: Noctuidae), Liriomyza huidobrensis Blanchard (Diptera: Agromyzidae), and Diabrotica speciosa (Germar) (Coleo ptera: Chrysomelidae). The stage of C. incommoda associated with spinach would most likely be larvae; L. huidobrensis larvae are leaf miners and would remain in the leaves; and Diabrotica speciosa adults only would likely be

associated with the host. Dia brotica speciosa eggs, larvae, and pupae are associated with roots and soil which are not permitted into U. S. ports of entry, and only adult D. speciosa use spinach as a host ( USDA, 2007; Walsh, 2003).

Mitigations for these pests may include inspection at the point of origin, systems approach production and harvesting, and radiation. Liriomyza huidobrensis spends most of its lifecycle in larval form, mining leaves especially along the midrib, and so are readily detectable via visual inspection (GPO,

200 6a). Pupae of L. huidobrensis are found in the soil and so would not be imported, and adults are active and not likely to remain with the host (GPO, 2006b; USDA, 2007). Visual inspection may be required as a condition of movement, and the exporting count ry’s National Plant Protection Organization (NPPO) is responsible for export certification, inspection, and issuance of phytosanitary certificates stating that such inspection was done (GPO, 2005a; GPO, 2006c). The phytosanitary certificate must be signed by an official of the NPPO and bear the declaration “the shipment has been inspected and found free of the pests listed in the export requirements; and all damaged produce was removed from the shipment prior to export” (GPO, 2006a; GPO, 2006c; GPO, 2007). The shipping box must be labeled with the identity of the production site (GPO, 2006a).

The main potential pathway for D. speciosa is soil (EPPO, 2005). Soil and underground parts of Colombian spinach are prohibited and are unlikely to be moved; and sp inach is not a larval host for D. speciosa (Walsh, 2003; USDA, 2007). A similar rootworm, D. virgifera , was likely carried from the United States to Europe via aircraft and a similar pathway could conceivably operate for D. speciosa

, but D. speciosa does not have a history of international movement and the active adults would likely not remain on the host during inspection of the commodity (Hostetler, 2002; EPPO, 2005; USDA, 2007).

A second mitigation would be production, packing, and shipping under a sys tems approach. The Plant Protection Act of 2000 [7 USC §§ 319.37

- 8] defines a systems approach as a defined set of phytosanitary procedures, at least two of which have independent effects mitigating pest risk. The Food and Agricultural Organization stand ards define systems approach as the integration of different pest risk management measures, at least two of which act independently and cumulatively achieve the desired level of phytosanitary protection (FAO, 2002). A suitable systems approach for commodi ty production consists of: 1) all production sites approved and registered with the exporting country’s NPPO; 2) production sites visited, inspected, and certified by officials of the exporting country’s NPPO; 3) the NPPO and APHIS agree that pest risk mit igation has been achieved; 4) inspections for visible damage are conducted regularly, and if a pest outbreak occurs, exports of the commodity are immediately cancelled until pest risk mitigation has again been achieved; 5) commodity is packed with

pest

- pro of screening that remains intact until arrival at a U. S. port of entry; and 7) commodity is accompanied by a phytosanitary certificate (PC) issued by the exporting country’s NPPO stating:Spinach from Colombia

Rev.02 December 4, 2007 36 “grown in an approved production site; the shipment has been inspec ted; and shipment has been found free of the pests listed on the PC” (GPO, 2005b).

Third, the commodity may be irradiated to sterilize or kill pests that remain following inspection. Irradiation is used as a pest mitigation tool in over 40 countries (U SEPA, 2006). The unit of absorbed dose is the gray (Gy) where 1 gray is equivalent to 1 Joule per kilogram (USEPA, 2006). Life stages of Lepidoptera that are successfully treated by irradiation are eggs and larvae, and of Coleoptera adults;

and a dose of 400 gray is approved to treat all insect pests (Hallman, 1998; Loaharanu, 1998; GPO, 2006d). Leafy vegetables’ tolerance to irradiation of a dose of 1,000 Gy has been determined to be Low, so additional testing to determine the specific tolerance of spin ach may be necessary (USEPA, 2006). Studies of other Lepidoptera, e. g. : Grapholita molesta ; and Coleoptera, e. g .: Conotrachelus nenuphar

, Cryptorhynchus mangiferae

, Tribolium castaneum , and Trogoderma granarium ; have

demonstrated effectiveness of lower doses of iradiation ranging from 80 to 300 Gy (Hallman, 1998; Tunçbilek et al., 2003; Hallman, 2005; El

- Nozahy et al ., 2007).

Therefore, inspection has been determined to remove Liriomyza huidobrensis leafminers, processing of the spinach leaves will remo ve the active adults of Diabrotica speciosa , and radiation will sterilize or kill any Copitarsia incommoda larvae that remain following inspection.