Pest Risk Assessment for Strawberries from Jordan

Importation of Fresh Strawberry, Fragaria spp., Fruitwith Flower Calyx and Short Stalkfrom Jordan into the Continental United States

A Pathway-Initiated Risk Assessment

March 8, 2010

Rev. 03

Agency Contact:

Center for Plant Health Science and Technology

Plant Epidemiology and Risk Analysis Laboratory

United States Department of Agriculture

Animal and Plant Health Inspection Service

Plant Protection and Quarantine

1730 Varsity Drive, Suite 300

Raleigh, NC27606

1

Rev. 03March 8, 2010

Pest Risk Assessment for Strawberries from Jordan

Executive Summary

The Kingdom of Jordan has requested approval for imports into the continental United States of fresh, field-grown strawberry fruit (Fragaria spp.) with calyces and short stalks. Because this commodity has not been imported from Jordan before, the United States Department of Agriculture (USDA), Animal and Plant Health Inspection Service (APHIS) conducted a pathway-initiated risk assessment to determine the risks associated with importing these strawberries. APHIS analysts prepared a list of pests in Jordan that are known to be associated with Fragaria spp., using standard sources, including documents submitted by Jordan, records of intercepted pests, and scientific literature. We determined which quarantine pests were likely to follow the pathway, and qualitatively analyzed them to determine the unmitigated risk each poses to the United States. We found the following six quarantine pests that could be introduced into the continental United States via this pathway:

Pest / Taxonomy
Cacoecimorpha pronubana Hübner / Lepidoptera: Tortricidae
Chrysodeixis chalcites (Esper) / Lepidoptera: Noctuidae
Eutetranychus orientalis (Klein) / Acari: Tetranychidae
Monilinia fructigena Honey / Leotiomycetes: Helotiales
Spodoptera littoralis (Boisduval) / Lepidoptera: Noctuidae
Thrips major Uzel / Thysanoptera: Thripidae

We rated all six pests with High Pest Risk Potential. We listed risk mitigation options for these pests. The choice of appropriate phytosanitary measures to mitigate pest risk is part of the pest risk management phase within APHIS and is not addressed in this document.

1

Rev. 03March 8, 2010

Pest Risk Assessment for Strawberries from Jordan

Table of Contents

Executive Summary

1. Introduction

1.1. Botany and Origin

1.2. Worldwide Production

1.3. Production in Jordan

2. Risk Assessment

2.1. Initiating Event: Proposed Action

2.2. Assessment of Weediness Potential of Fragaria spp.

2.3. Current Status, Decision History, and Pest Interceptions

2.4. Pest Categorization-Identification of Pests of Fragaria spp. in Jordan

2.5. Quarantine Pests Likely to Follow the Pathway

2.6. Consequences of Introduction

2.7. Likelihood of Introduction

2.8. Pest Risk Potential and Conclusion

3. Authors and Reviewers

4. Literature Cited

5. Appendices

Appendix A. Risk management options for importation of fresh strawberry (Fragaria spp.) from Jordan into the continental United States.

Appendix B. Countries with permitted entry of strawberries into the United States.

Appendix C. Decision sheets for Fragaria spp.

Appendix D. Pest interceptions on Fragaria sp., F. ananassa, F. chiloensis, and F. vesca entering the United States

1

Rev. 03March 8, 2010

Pest Risk Assessment for Strawberries from Jordan

1. Introduction

This risk assessment was prepared by analysts at the Center for Plant Health Science and Technology (CPHST) office in Colombia, Plant Protection and Quarantine (PPQ), Animal and Plant Health Inspection Service (APHIS), United States Department of Agriculture (USDA). We examined potential pest risks associated with the importation of fresh fruits of strawberry (Fragaria spp.) from the Kingdom of Jordan into the continental United States. Strawberry fruit from Jordan is intended to be exported with flower calyces and short stalks (EHKJ, 2004). Leaving the calyx on the fruit is important to decrease perishability (Strand, 1994; Mitcham and Mitchell, 2002).

This pest risk assessment is pathway-initiated because it is based on the risks that may be associated with the importation of this commodity, and is qualitative in that risk is expressed in descriptive terms (High, Medium, and Low) rather than as probabilities or frequencies. The methodology and rating criteria are explained in “Guidelines for Pathway-Initiated Pest Risk Assessments, Version 5.02”(PPQ, 2000).

International plant protection organizations such as the North American Plant Protection Organization (NAPPO) and the International Plant Protection Convention (IPPC) of the United Nations Food and Agriculture Organization (FAO) provide guidance for conducting pest risk analyses. The methods used in this plant pest risk assessment are consistent with this guidance and are in accordance with the Framework for Pest Risk Analysis (IPPC, 2007: ISPM #2). Biological and phytosanitary terms used in this document are in accordance with those in the Glossary of Phytosanitary Terms (IPPC, 2007: ISPM #5). The guidelines describe three stages of pest risk analysis: Stage 1 (initiation), Stage 2 (risk assessment), and Stage 3 (risk management). A pest risk assessment is a component of an overall pest risk analysis; this document satisfies the requirements of Stages 1 and 2.

1.1. Botany and Origin

Fragaria species belong to the Rosaceae family. The genus Fragaria contains fifteen strawberry species that are distributed throughout the northern temperate regions of the world and one species that extends into South America. Fragaria virginiana and F. chiloensis are native to the Americas (CABI, 2007). There are five species of Fragaria native to or found in the United States (F. x ananassa, F. bringhurstii, F. chiloensis, F. vesca and F. virginiana). Within these five species there are 13 subspecies that are native or naturalized in the continental United States (NCRS, 2008).Northeast Asia contains the largest number of species.

The hybrid F. ananassa Duchesne was obtained in Europe in the mid-18th century from the crossing of F. virginiana Duchesne and F. chiloensis (L). This hybrid was rapidly cultivated by growers around the world because it was superior in many ways to the wild species that were the source of strawberry fruit (CABI, 2007). Other native species are still harvested from the wild, but these rarely appear in markets because of their small size and poor shelf life. Indigenous peoples of Chile selected and cultivated large-fruited clones of F. chiloensis that are still grown in that region (CABI, 2007). Also, color variants of F. vesca are grown for ornamental purposes, but only rarely for fruit. Today, wild species are mainly of interest for specific genes that they can contribute to the octoploid F. x ananassa (CABI, 2007).

1.2. Worldwide Production

North America is the largest producer of strawberries (Perez and Pollack, 2007). Strawberry production in California and Florida in 2007 was forecast to be 10,432,625 metric tons (2.3 billion pounds). California produced 88 percent of the U.S. crop in 2007, while Florida was second with about 10 percent (Perez and Pollack, 2007).

Although fresh strawberry imports are a relatively small portion of what is consumed in the United States, this volume has increased over the last five years (Perez and Pollack, 2007). In 2006, fresh strawberry imports were a record 69,581 metric tons, 25 percent greater than the previous year (Perez and Pollack, 2007). For 2007, 157.7 million pounds (71,519 metric pounds) were imported (Pollack and Perez, 2008). Almost all of those strawberries came from Mexico, but other suppliers included Argentina, China, Chile, Canada, Ecuador, New Zealand, Peru, and Poland (Perez and Pollack, 2007; Pollack and Perez, 2008).

1.3. Production in Jordan

In Jordan, strawberries are produced in 500 m2 (0.124 acre) plastic tunnels (Abu-El Samen, 2008). No open field plantations are used, but multi-span plastic tunnels are employed on a few farms. All strawberry production uses drip irrigation. The major varieties produced are Anar, Splinder, Camarosa, Ventana, Alpion, and C-scape.Transplants are produced in tissueculture from California and Europe, or by local producers in Jordan. The tunnels are re-planted each year. Commercial cultivars produce individual fruits weighing as much as 30-50 g, although 10-20 g is typical (CABI, 2007).

The cultivated area for strawberries in Jordan was 41.4 ha (102.3 acres) in 2006 and 60 ha (148.3 acres) in 2007 (Abu-El Samen, 2008). Total production was 828 tons in 2006 and 1,200 tons in 2007. In 2007, 700 tons were produced in the Jordan Valley and 500 tons in the highlands (Abu-El Samen, 2008).Exports of strawberries from Jordan to the European Union and Jordan’s neighboring countries—Israel, Iraq, Egypt, Saudi Arabia, and Syria—have increased rapidly in recent years (DOS, 2006; Magnani et al., 2004).

Integrated pest management (IPM) practices are used in strawberry production in Jordan in collaboration with GTZ (German Agency for Technical Cooperation)-Germany IPM projects. Primary treatments include predators and parasites of insect pests and restricted pesticide applications. The commonly used pesticides are Floromite (for management of red spider mites), Proclaim (for insect pest management), Boscalid (fungal diseases), and Bellis (Boscalid combined with pyraclostrobin) (fungal diseases) (Abu-El Samen, 2008; Sallato et al., 2007).

Soil fumigation with chemicals (e.g. MB and Dazomet) is practiced by farmers specially in the establishing of a new farm or site in addition to soil solarization (Katbeh Bader, 2010).
2. Risk Assessment

2.1. Initiating Event: Proposed Action

We conducted this commoditybased, pathwayinitiated risk assessment in response to a request made by the Kingdom of Jordan (EHKJ, 2004) to the USDA to authorize the importation of fresh strawberry fruit (with flower calyx and short stalk) grown in Jordan (in the Jordan valley and highlands) into the continental United States. The importation is a potential pathway for the introduction of plant pests. USDA has regulatory authority for the importation of fruits and vegetables from foreign sources into the United States (7 CFR § 319, 2007).

2.2. Assessment of Weediness Potential of Fragaria spp.

The results of the weediness screening for Fragaria spp.did not prompt a weedinitiated risk assessment (Table 1).

Table 1. Assessment of weediness potential of Fragaria spp.

Commodityscientific name:Fragaria × ananassa Duchesne ex Rozier [Rosaceae]
Common name: Strawberry
The Fragaria genus has 15 species, but only Fragaria × ananassa contributes significantly to commercial production. It is the hybrid of two species: F. virginiana Duchesne from eastern North America and F. chiloensis (L.) Duchesne from North and South America, which is still grown in Chile (CABI, 2007). Fruits of wild native species are still harvested, but these rarely appear in markets because of their small size and short shelf-life (CABI, 2007). Other species, such as F. vesca, are mainly cultivated for ornamental purposes (CABI, 2007). Today, wild species are mainly of interest for specific genes that they can contribute to the octoploid F. x ananassa (CABI, 2007).
Synonyms:Fragaria × ananassa var. cuneifolia (Nutt. ex Howell) Staudt (= F. × ananassa nothosubsp. cuneifolia)
F. chiloensis var. ananassa (Duchesne ex Rozier) Ser.
F. cuneifolia Nutt. ex Howell (= F. × ananassa nothosubsp. cuneifolia)
F. × magna auct.
Potentilla × ananassa (Duchesne ex Rozier) Mabb. (NGRP, 2008)
Phase 1:
Fragaria spp.L. are reported in all states of the continental United States (NRCS, 2008). The hybrid Fragaria x ananassais reported in the following states: Alaska, Connecticut, Illinois, Massachusetts, Maine, Missouri, North Carolina, New Hampshire, New York, Oregon, Pennsylvania, Rhode Island, and Washington (NRCS, 2008).
Phase 2:
The species is listed in:
YESGeographical Atlas of World Weeds (Holm et al., 1991a) as: F. indica (for Mauritius), F. vesca,and F. virginiana (both for the United States).
NOWorld’s Worst Weeds (Holmet al., 1991b).
NOWorld Weeds: Natural Histories and Distribution (Holmet al., 1997).
YESWeed Science Society of America (WSSA, 2007) as Fragaria virginiana.
NOFederal Noxious Weed List (PPQ, 2006).
NOEconomically Important Foreign Weeds (Reed, 1977).
NOIdentification of disseminules listed in the Federal Noxious Weed Act (Gunn and Ritchie, 1988).
NOGlobal Invasive Species Database (ISSG, 2008).
YESA Global Compendium of Weeds (Randall, 2003) as:
F. x ananassa: Naturalized, cultivation, escape, and casual alien. Cultivated medicinal and culinary uses.
F. chiloensis: Cultivated, medicinal and culinary uses.
F. chiloensis ssp. lucida: Naturalized.
F. indica: Weed. Cultivated medicinal and culinary uses.
F. moschata: Cultivation escape. Cultivated, medicinal and culinary uses.
F. muricata: Naturalized.
Fragaria spp.: Weed. Medicinal and culinary uses.
F. vesca: Weed, Naturalized. Cultivated, medicinal and culinary uses.
F. vesca ssp. americana: Weed.
F. virginiana: Weed. Cultivated, medicinal and culinary uses.
F. viridus: Weed.
NOInvasive Species of the World (Weber, 2003).
YESAlien Plant Invaders of Natural Areas (Swearingen, 2008) as: F. vesca ssp. vesca (NJ, invasive), F. chiloensis (HI, invasive).
NONoxious weeds in the United States and Canada (Rice, 2008).
NOState Regulated Noxious Weeds (APHIS, 2007).
Other: Scientific literature, Internet sources, etc.:
NOAGRICOLA (NAL, 2008), CAB (CABI, 2007), AGRIS (FAO, 2008).
NOFlorida's Invasive Species List, Florida Exotic Pest Plant Council (FLEPPC, 2007).
YES Pacific Island Ecosystems at Risk (USFWS, 2008a), as Fragaria vesca.
NONoxious weed list for Australian states and territories (Australian Weeds Committee, 2007).
Phase 3:
Fragaria sp. and Fragaria x ananassaare widely prevalent in the continental United States and the answer to four of the above questions is yes. In this case, we need to provide additional comments on our findings (PPQ, 2000):
  • Fragaria vesca andF. virginiana are listed as weeds of unknown importance in the United States (Holm et al., 1991a), while Fragaria indica, Fragaria spp., F. vesca, F. vesca ssp. americana, F. virginiana, and F. viridus are also considered weeds(Randall, 2003)
  • F. vesca ssp. vesca is invasive in NJ, and F. chiloensis is invasive in HI (Swearingen, 2008)
  • F. vesca is “present on Pacific islands” (USFWS, 2008a)
Conclusion: We proceeded with the pest risk assessment for the following reasons: 1) Cropped strawberries are economically important (Wiersema and Leon, 1999); 2) cultivated and wild strawberries (Fragaria spp.) grow in 49 states without being under official control; and 3) Fragaria spp., as strawberry fruit, are currently permitted entry into the United States from 88 countries (PPQ, 2008a).

2.3. Current Status, Decision History, and Pest Interceptions

2.3.1. Current status

Strawberries are authorized to enter into the United States through all U.S. ports-of-entry from 88 countries (see Appendix B). Over the past few decades, no pest risk assessment has been conducted for the importation of strawberries into the United States.

2.3.2. Decision history

From 1924 to 1994, the importation of strawberries into the United States was denied from the following countries: Australia, French Guiana, Ghana, Guyana, Korea, Peru, the Philippines, and Zimbabwe. The principal risks detected in decision sheets were 1) Halotydeus destructor, 2) mites, 3) Dacus sp., and 4) Bactrocera sp. (CPHST, 2008).

Decisions without clear dates are as follows: Argentina (authorized entry via Miami), Belgium, Cuba, Ecuador, England, Europe, France, French Guiana, Haiti, Italy, Jamaica, Japan, Mexico, the Netherlands, New Zealand, Peru (rejected at South Pacific ports), Scotland, Switzerland (decision unknown), Chile (approved), and the Philippines (denied) (CPHST, 2008). For further details see Appendix C.

2.3.3. Pest interceptions

From 1984 to 2008, many different pests were intercepted on F. x ananassa, F. chiloensis, Fragaria sp.,and F. vesca at U.S. ports-of-entry (see Appendix D) (PestID, 2009).

2.4. Pest Categorization-Identification of Pests of Fragaria spp. in Jordan

2.4.1. Pest list

Below we present information on pests associated with Fragaria spp. (in any country) that occur in Jordan and neighboring countries (Table 2). The data includes (1) the presence or absence of these pests in the continental United States and pertinent citations for that distribution, (2) pertinent citations supporting the association of the pest with Fragaria spp., (3) the association of the pest with plant parts and pertinent citations showing that association, (4) the quarantine status of the pest in the continental United States, and (5) whether the pest is likely to follow the pathway into the United States on strawberry.

1

Rev. 03March 8, 2010

Pest Risk Assessment for Strawberries from Jordan

Table 2. Pests reported on Fragaria spp. and present in Jordan and neighboring countries.

Pest / Geographic distribution[1] / Reported on Fragaria spp. / Plant part affected[2] / Quaran-tine pest / Follow pathway
ARTHROPODS
ARACHNIDA
Acari: Tarsonemidae
Phytonemus pallidus (Banks) / JO (EHKJ, 2004); US (CABI, 2007) / EHKJ, 2004; INRA, 2008 / N/A / No / N/A
Acari: Tenuipalpidae
Brevipalpus obovatus Donnadieu / JO (PestID, 2009); US (CABI, 2007) / MAG, 2008 / N/A / No / N/A
Acari: Tetranychidae
Bryobia praetiosa Koch / JO (PestID, 2009); US (Migeon and Dorkeld, 2007) / Migeon and Dorkeld, 2007 / N/A / No / N/A
Eutetranychus orientalis (Klein) / JO (CABI, 2007; EPPO and CABI, 1997; Migeon and Dorkeld, 2007) / Migeon and Dorkeld, 2007 / F (Poole, 1999); L (CABI, 2007; NAPPO, 2001) / Yes / Yes
Tetranychus cinnabarinus (Boisduval)
Syn: Tetranychus telarius (L.) / JO (CABI, 2007; Kasem and Yakob, 1985); US (CABI, 2007) / CABI, 2007 / N/A / No / N/A
Tetranychus urticae Koch / JO (CABI, 2007; EHKJ, 2004; Migeon and Dorkeld, 2007); US (CABI, 2007) / CABI, 2007; EHKJ, 2004; Migeon and Dorkeld, 2007 / N/A / No / N/A
INSECTA
Coleoptera: Chrysomelidae
Altica (Haltica) oleracea(L.) / JO (Furth, 1980) / Furth, 1980 / L (Cranshaw, 2006) / Yes / No[3]
Coleoptera: Curculionidae
Hypera postica (Gyllenhal)
Syn: Phytonomus variabilis Herbst. / JO (AQIS, 2008; EPPO, 1999); US (CABI, 2007) / CABI, 2007 / N/A / No / N/A
Coleoptera: Scarabaeidae
Polyphylla fullo (Linnaeus) / JO (EHKJ, 2004); US (MA) (Herrmann et al., 2006) / EHKJ, 2004 / R (INRA, 2008) / Yes / No
Melolontha melolontha Linnaeus / JO (AQIS, 2008) / CABI, 2007; Graham, 2008; INRA, 2008; Plant Health Australia, 2005 / F (CABI, 2007); L, R (Graham, 2008; INRA, 2008) / Yes / No[4]
Diptera: Tephritidae
Ceratitis capitata (Wiedemann) / JO (AQIS, 2008; EPPO, 1999; PestID, 2009) / Liquido et al., 1991; Thomas et al., 2005 / F[5] (CABI, 2007) / Yes / No[6]
Hemiptera: Aphididae
Aphis gossypii Glover / JO (AQIS, 2008; CABI, 2007); US (CABI, 2007) / EHKJ, 2004; Strand, 1994 / N/A / No / N/A
Aulacorthum solani Kaltenbach / JO; US (CABI, 2007) / CABI, 2007 / N/A / No / N/A
Brachycaudus helichrysi Kaltenbach / JO (AQIS, 2008; EPPO, 1999); US (CABI, 2007) / CABI, 2007 / N/A / No / N/A
Macrosiphum euphorbiae (Thomas) / JO (CABI, 2007); US (CABI, 2007; Strand, 1994) / CABI, 2007; Strand, 1994 / N/A / No / N/A
Macrosiphum rosae (Linnaeus) / IS (PestID, 2009; CABI, 2007); EG; US (CABI, 2007) / CABI, 2007 / N/A / No / N/A