Pest List for the Importation of Fresh Commercial Citrus Fruit: Grapefruit (Citrus × paradisi); Lime (C. aurantiifolia); Mandarin Orange, Tangerine, or Hybrids (C. reticulata); Sweet Orange (C. sinensis); and Tangelo (C. × tangelo) from Peru into the Continental United States

November 2, 2012

Version 1

Agency Contact:

Plant Epidemiology and Risk Analysis Laboratory Center for Plant Health Science and Technology

United States Department of Agriculture and Plant Health Inspection Service Plant Protection and Quarantine 1730 Varsity Drive, Suite 300 Raleigh, NC 27606

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Executive Summary

The Animal and Plant Health Inspection Service (APHIS) of the United States Department of Agriculture (USDA) prepared this pest list to examine plant pest risks associated with importing commercially produced fresh Citrus fruit for consumption from all areas of Peru into the continental United States. This request (SENASA-Peru, 2011) is for the following species: grapefruit (Citrus × paradisi Macfad.); lime (C. aurantiifolia [Christm.] Swingle); mandarin orange, tangerine, or hybrids (C. reticulata Blanco); sweet orange (C. sinensis [L.] Osbeck); and tangelo (Citrus × tangelo J.W. Ingram & H.E. Moore) (Rutaceae). An earlier risk assessment was developed for exports of citrus from five production regions, and market access was established (USDA, 2003).

Here, considering expansion of the export area from Peru to the entire country, we considered the pathway to include the following processes and conditions:  phytosanitary management of pests associated with Citrus in the grove;  packinghouse measures that include inspection primary grading to remove small, damaged, infected, or infested fruit; washing and brushing to clean fruit; spraying with wax containing fungicide, followed by air-drying; secondary grading to remove damaged or blemished fruit; sorting by size and packaging in new cardboard boxes; storage with safeguarding measures to prevent re-infestation under consistent conditions; and  final inspection and certification procedures, prior to approval to start cold treatment for fruit flies in transit. These processes (7 CFR § 319.56, 2012) have been successfully implemented for the five previously approved export areas.

Based on the scientific literature, port-of-entry pest interception data, and information from the government of Peru, we developed a list of all pests reported in Peru that infest or infect the Citrus species above. We identified the following five quarantine pests as likely to follow the commodity pathway of fresh citrus fruit from Peru that are candidates for risk mitigation. We analyzed all of these pests in the earlier risk assessment (USDA, 2003).

Type Pest Classification Pest Scientific Name Diptera: Tephritidae Anastrepha fraterculus Anastrepha obliqua Anastrepha serpentina Ceratitis capitata Lepidoptera: Tortricidae Ecdytolopha aurantiana

We found no evidence that the following damaging Citrus pests found in other countries in South America are in Peru: Bactrocera carambolae, ‘Candidatus Liberibacter asiaticus,’ Citrus leprosis virus, Diaphorina citri, Elsinoë australis, Guignardia citricarpa, Pseudococcus neomaritimus, Xanthomonas citri pv. citri, or Xylella fastidiosa subsp. pauca.

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Table of Contents

Executive Summary ...... ii 1. Introduction ...... 1 2. Pest Categorization ...... 1 2.1. Pests associated with Citrus species: C. × paradisi, C. aurantiifolia, C. reticulata, C. sinensis, and C. × tangelo ...... 1 2.2. Quarantine pests not considered for risk mitigation ...... 19 2.3. Quarantine pests likely to follow the pathway and candidates for risk mitigation ...... 20 3. Authors and Reviewers...... 21 4. Literature Cited ...... 21

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1. Introduction

This document accompanies a request for the United States Department of Agriculture (USDA)’s authorization to allow the importation of fresh fruit of the following Citrus species: grapefruit (C. × paradisi Macfad.), lime (C. aurantiifolia [Christm.] Swingle), mandarin orange or tangerine (C. reticulata Blanco), sweet orange (C. sinensis [L.] Osbeck), and tangelo (Citrus × tangelo J.W. Ingram & H.E. Moore) (Rutaceae) for consumption from the entire country of Peru into the continental United States. The movement of fruits and vegetables from foreign countries, such as Peru, into the United States is regulated (7 CFR § 319.56, 2012). Currently, the entry of fresh fruit of the above-listed Citrus species from Peru into the continental United States is authorized under 7 CFR §319.56 for only five production regions: Ica, Junin, Lambayeque, Lima, and Piura. The government of Peru seeks approval for entry of citrus from the entire country of Peru.

The movement of fresh Citrus fruit from Peru is a potential pathway for the introduction of unwanted plant pests into the continental United States. These risks were previously evaluated in a pathway-initiated plant pest risk assessment in 2003 (USDA, 2003). Since then, new pests may have been reported, pest statuses may have changed, and the expanded production area may have different pests than the previously evaluated five regions. Consequently, the USDA’s Animal and Plant Health Inspection Service (APHIS) Plant Protection and Quarantine (PPQ) prepared this document to examine the plant pest risks associated with the movement of this commodity into the continental United States from the expanded Citrus export area in Peru.

Based on the market access requesting expansion of the export area from Peru to the entire country, we considered the pathway to include the following processes and conditions (SENASA-Peru, 2011):  phytosanitary management of pests associated with Citrus in the grove;  packinghouse measures that include inspection; primary grading to remove small, damaged, infected, or infested fruit; washing and brushing to clean fruit; spraying with wax containing fungicide, followed by air-drying; secondary grading to remove damaged or blemished fruit; sorting by size and packaging in new cardboard boxes; storage with safeguarding measures to prevent re-infestation under consistent conditions; and  final inspection and certification procedures, prior to approval to start cold treatment for fruit flies in transit. These proposed processes have been successfully implemented for the five previously approved export areas in accordance with U.S. regulations (7 CFR § 319.56, 2012). By developing this pest list, we can determine if currently described requirements are adequate to provide phytosanitary security, or if other measures may be required.

2. Pest Categorization

2.1. Pests associated with Citrus species: C. × paradisi, C. aurantiifolia, C. reticulata, C. sinensis, and C. × tangelo

Below we list the pests associated with the following Citrus species: grapefruit (C. x paradisi), lime (C. aurantiifolia), mandarin orange or tangerine (C. reticulata), sweet orange (C. sinensis),

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and tangelo (Citrus x tangelo) (in any country) that occur in Peru (on any host) (Table 1). We identified the presence or absence of these pests in the continental United States, the quarantine status of the pests with respect to the continental United States, the generally affected plant part or parts, whether quarantine pests are likely to follow the pathway and enter the continental United States on commercial citrus fruit, and pertinent references. We developed this pest list based on the scientific literature, USDA port-of-entry pest interception data, and information provided by the government of Peru. Pests highlighted with a gray background are quarantine pests identified for potential risk mitigation, as we consider them reasonably likely to follow the pathway of commercial fruit shipments. We summarize those pests in a separate table (Table 2).

Please note that in the pest list (Table 1), we do not provide information on plant part association and whether the pest is likely to follow the pathway for non-quarantine pests. Even if non- quarantine pests are able to follow the pathway, phytosanitary measures against these pests would not be justified because they already occur in the continental United States. Therefore, for non-quarantine pests we indicate that information with N/A (not applicable).

Table 1. Pests associated with relevant Citrus spp. that are also present in Peru. Scientific Name Reported on Distribution1 Quaran- Plant part(s) Follow Citrus spp. tine pest2 association3 pathway ARTHROPODS Acari: Eriophyidae

Phyllocoptruta oleivora CABI, 2012; PE (Alata Condor, No N/A N/A (Ashmead) Futch et al., 2011 1973), US (CABI, 2012) Acari: Tarsonemidae Polyphagotarsonemus latus CABI, 2012; PE, US (Vacante, No N/A N/A Banks Gerson, 1992 2010) Acari: Tenuipalpidae

Brevipalpus phoenicis Vacante, 2010 PE, US (Vacante, No N/A N/A (Geijskes) 2010) Acari: Tetranychidae

1 Geographic Distribution (specific states are listed only if distribution is limited): AL = Alabama, AR = Arkansas, AZ = Arizona, CA = California, DC = District of Columbia, FL = Florida, GA = Georgia, HI = Hawaii, IA = Iowa, LA = Louisiana, MD = Maryland, MS = Mississippi, TX = Texas, TH = Thailand, US = United States (widespread), VA = Virginia, WA = Washington (Individual U.S. states are listed only if the pest species is considered a quarantine pest for the United States.) 2 Brackets (“[ ]”) around the quarantine status designation indicate that the pest has a limited distribution in the continental United States and is either under official control or under consideration for official control. If no reference is listed, this was verified in PestID (2012). 3 Plant Parts: Br = Branch, F = Fruit, I = Inflorescence, GP = Growing point, L = Leaf, R = Root, S = Stem, Sd = Seed. For non-quarantine pests, we put N/A (= Not Applicable) in the columns for “Plant Part(s) Association” and “Follow Pathway.” See discussion above for more information.

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Scientific Name Reported on Distribution1 Quaran- Plant part(s) Follow Citrus spp. tine pest2 association3 pathway Eotetranychus lewisi Vacante, 2010 PE, US (Vacante, No N/A N/A (McGregor) 2010)

Oligonychus peruvianus Vacante, 2010 PE, US (Vacante, No N/A N/A (McGregor) 2010) Panonychus citri CABI, 2012; PE (Alata Condor, No N/A N/A (McGregor) Futch et al., 2011 1973), US (CABI, 2012) Tetranychus cinnabarinus CABI, 2012 PE, US (CABI, 2001; No N/A N/A (Boisduval) Ehler, 1974; Johnson et al., 1989; Mollet and Sevacherian, 1984) Tetranychus urticae Koch Vacante, 2010 PE, US (Vacante, No N/A N/A 2010) Coleoptera: Cerambycidae accentifer Escalante et al., PE (Escalante et al., Yes S (Escalante et No (Olivier) 1981 1981) al., 1981) Coleoptera: Chrysomelidae Diabrotica speciosa CABI, 2012; PE (CABI, 2012) Yes F, L, R No4 (Germar) Cabrera Walsh, (CABI, 2012) 2003 Coleoptera: Compsus sp. Alata Condor, PE (Alata Condor, Yes L, R (Alata No 1973; Arnett et al., 1973; Arnett et al., Condor, 1973; 2002; Borrer et al., 2002; Borrer et al., Arnett et al., 1989 1989 2002; Borrer et al., 1989) Macrostylus puberulus Alata Condor, PE (Alata Condor, Yes S (Alata No Boheman 1973; Garces, 1973; Garces, 1988; Condor, 1973; Syn.: Amphideritus 1988; Wibmer and Wibmer and O'Brien, Garces, 1988; puberulus O'Brien, 1986 1986) Wibmer and O'Brien, 1986) Pantomorus cervinus CABI, 2012 PE, US (Alata No N/A N/A (Boheman) Condor, 1973; CABI, [Syn.: P. godmani 2000) (Crotch)]

Rhynchophorus palmarum CABI, 2002; PE (CABI, 2002; Yes F, I, L, S No5 (Linnaeus) PestID, 2003 PestID, 2003), US (CABI, 2002; (CA, limited PestID, 2003) distribution) (Hoddle, 2011)

4 Because of its size, biology and mobility, this pest is highly unlikely to stay on the commodity through harvest and standard handling and processing.

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Scientific Name Reported on Distribution1 Quaran- Plant part(s) Follow Citrus spp. tine pest2 association3 pathway Coleoptera: Scarabaeidae Ancistrosoma klugi Curtis Alata Condor, PE (Alata Condor, Yes I, L, R (Alata No 1973; 1973; Blackwelder, Condor, 1973; Blackwelder, 1956; Dourojeanni, Blackwelder, 1956; 1992; Peña and 1956; Dourojeanni, Bennett, 1995) Dourojeanni, 1992; Peña and 1992; Peña Bennett, 1995 and Bennett, 1995) Gymnetosoma mathani Alata Condor, PE (Alata Condor, Yes F, I, L (Alata No7 (Pauill) 1973; Borrer et al., 1973; Borrer et al., Condor, 1973; 1989; White, 1983 1989; White, 1983) Borrer et al., 1989; White, 1983)6 Diptera: Lonchaeidae Neosilba pendula Bezzi Araújo and PE (Hofshi, 2003) Yes F (Araújo and No8 Zucchi, 2002 Zucchi, 2002) Diptera: Tephritidae Anastrepha fraterculus CABI, 2012; PE (Alata Condor, Yes F (CABI, Yes (Wiedemann) Ovruski et al., 1973; CABI, 2012; 2012) 2003 Steck, 1991) Anastrepha obliqua CABI, 2012 PE (CABI, 2012; Yes F (CABI, Yes Macquart Korytkowski and 2012; Ojeda, 1968) Korytkowski and Ojeda, 1968) Anastrepha serpentina CABI, 2012 PE (Alata Condor, Yes F (CABI, Yes (Wiedemann) 1973; CABI, 2012; 2012) Foote et al., 1993; Weems, 2012) Ceratitis capitata CABI, 2012 PE (Aguilar, 1982; Yes F (CABI, Yes (Wiedemann) Alata Condor, 1973; 2012) CABI, 2012)

5 Because of its size, biology, and mobility, this pest is highly unlikely to stay on the commodity through harvest and standard handling and processing. 6 Many scarabs feed on plant materials such as grasses, foliage, fruits, and flowers, and some are serious pests of various agricultural crops (Borrer et al., 1989). We assume that only the adults attack the fruit, as we found no evidence that scarab larvae feed on fruit (White, 1983). 7 Because of their size, biology, and mobility, adults of this pest are highly unlikely to stay on the commodity through harvest and standard handling and processing. 8 This species is a secondary pest that uses hosts previously damaged by primary invaders, particularly fruit flies (White and Elson-Harris, 1992). Culling damaged fruit and mitigating fruit flies is highly likely to remove these pests from the pathway.

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Scientific Name Reported on Distribution1 Quaran- Plant part(s) Follow Citrus spp. tine pest2 association3 pathway Tetreuaresta punctipennata Alata Condor, PE (Alata Condor, Yes I (Alata No Hering 1973; Borge and 1973; Borge and Condor, 1973; Basedow, 1997; Basedow, 1997; Borge and Gordh and Gordh and Headrick, Basedow, Headrick, 2001 2001) 1997; Gordh and Headrick, 2001 Diptera: Muscidae Atherigona orientalis CABI, 2012 PE, US (CABI, 2012) No N/A N/A Schiner Diptera: Cecidomyiidae Prodiplosis longifila Gagné Pena et al., 1989 PE, US (FL) (Pena et [Yes] N/A N/A al., 1989) : Aleyrodidae Aleurocanthus woglumi EPPO/CABI, PE, US (FL, HI, TX) [Yes] L (Nguyen et No Ashby 1997a; Maes and (EPPO/CABI, 1997a) al., 2010) Mound, 1993 Aleurodicus sp cercana a A. Nunez, 2008 PE (Nunez, 2008) Yes L (Nunez, No cocois (Curtis) 2008) Aleurodicus coccolobae Nunez, 2008 PE (Nunez, 2008) Yes L (Nunez, No Quaintance and Baker 2008) Aleurodicus dispersus CABI, 2012 PE, US (Lambkin, No9 L (CABI, No Russell 1999) 2012) Aleurothrixus floccosus CABI, 2012 PE, US (CABI, 2012; No N/A N/A (Maskell) Kerns et al., 2001; Miklasiewicz and Walker, 1990) Aleurotrachelus sp. Nunez, 2008 PE (Nunez, 2008) Yes L (Nunez, No 2008) Dialeurodes citri (Ashmead) CABI, 2012 PE, US (CABI, 2012) No N/A N/A Paraleyrodes sp. Nunez, 2008 PE (Nunez, 2008) Yes L (Nunez, No 2008) Siphoninus phillyreae Nguyen et al., PE (Valencia et al., No10 N/A N/A (Haliday) 2010 2010); US (Nguyen et al., 2010) Hemiptera: Aphididae Aphis gossypii Glover CABI, 2012 PE, US (CABI, 2012) No N/A N/A Aphis spiraecola Patch CABI, 2012 PE, US (CABI, 2012) No N/A N/A Macrosiphum euphorbiae CABI, 2012 PE, US (CABI, 2012) No N/A N/A (Thomas) Myzus persicae Sulzer CABI, 2012 PE, US (CABI, 2012) No N/A N/A

9 Aleurodicus dispersus was listed previously as a quarantine pest (USDA, 2003). Currently, no action is required for this pest on commodities for consumption (PestID, 2012). 10 Status of this pest was recently changed to non-reportable/non-actionable (PestID, 2012).

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Scientific Name Reported on Distribution1 Quaran- Plant part(s) Follow Citrus spp. tine pest2 association3 pathway Rhopalosiphum maidis CABI, 2012 PE, US (CABI, 2012) No N/A N/A (Fitch) Toxoptera aurantii (Boyer CABI, 2012 PE, US (CABI, 2012) No N/A N/A de Fonscolombe) Toxoptera citricidus CABI, 2012 PE, US (FL, HI, PR) [Yes] L, S, I (CABI, No (Kirkaldy) (CABI, 2012) 2012) Syn: T. citricida Hemiptera: Asterolecaniidae Asterolecanium sp. Alata Condor, PE (Alata Condor, Yes L, S, F Yes 1973; Hamon, 1973) (Hamon, 1977; Hill, 1983 1977; Hill, 1983) Lecanodiaspis sp. Alata Condor, PE (Alata Condor, Yes S, B (Ben-Dov No 1973 1973) et al., 2012) Hemiptera: Coccidae Ceroplastes sp. Alata Condor, PE (Alata Condor, Yes L, S (Alata No 1973; CABI, 2012 1973) Condor, 1973; CABI, 2012) Ceroplastes cirripediformis CABI, 2000; PE, US (CABI, 2000; No N/A N/A (Comstock) Marin-Loayza and Marin-Loayza and Cisneros-Vera, Cisneros-Vera, 1995) 1995 Ceroplastes floridensis CABI, 2000 PE (Marin-Loayza No N/A N/A (Comstock) and Cisneros-Vera, 1995), US (CABI, 2000)

Coccus hesperidum L. Alata Condor, PE, US (Alata No N/A N/A 1973; CABI, Condor, 1973; CABI, 2000; Hamon, 2000; Hamon, 1984) 1984 Coccus viridis (Green) (Alata Condor, PE (Gomez de Picho, No11 N/A N/A 1973; CABI, 1991), US (Ben-Dov 2002; Dekle and et al., 2012) Fasulo, 2002)

Parthenolecanium corni Alata Condor, PE, US (Alata No N/A N/A (Bouché) (Syn: Lecanium 1973; CABI, 2002 Condor, 1973; CABI, corni Bouché) 2002) Protopulvinaria pyriformis Alata Condor, PE, US (Alata No N/A N/A (Ckll.) 1973; Ben-Dov et Condor, 1973; CABI, al., 2012; CABI, 2001;Ben-Dov et al., 2001 2012)

11 Coccus viridis was listed as a quarantine pest previously (USDA, 2003), but currently is non-reportable/non-actionable (PestID, 2012).

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Scientific Name Reported on Distribution1 Quaran- Plant part(s) Follow Citrus spp. tine pest2 association3 pathway Pulvinaria sp. (Tao, Wong Alata Condor, PE (Alata Condor, Yes L, S, F (Hill, Yes & Chang) 1973; Ben-Dov et 1973) 1983; Ben- al., 2012; CABI, Dov et al., 2002; Hill, 1983 2012; CABI, 2002) Saissetia coffeae (Walker) Alata Condor, PE, US (Alata No N/A N/A 1973; CABI, Condor, 1973; CABI, 2000; Hamon, 2001; Hamon, 1984) 1984 Saissetia oleae (Olivier) Alata Condor, PE, US (Alata No N/A N/A 1973; CABI, Condor, 1973; CABI, 2000; Hamon, 2001; Hamon, 1984 1984 Hemiptera: Diaspididae12 Aonidia sp. Alata Condor, PE (Alata Condor, Yes L (Ben-Dov et No 1973 1973) al., 2012)

Acutaspis albopicta Ben-Dov et al., PE, US (Ben-Dov et No N/A N/A (Cockerell) 2012 al., 2012) Aspidiotus destructor CABI, 2002 PE, US (CA, FL, HI) No N/A N/A Signoret (CABI, 2002) Aspidiotus nerii Bouché CABI, 2002 PE, US (CA, HI) No N/A N/A (CABI, 2002) Aulacaspis tubercularis CABI, 2002; PE (PestID, 2003) Yes L (Hodges and Yes12 Newstead PestID, 2003 Hamon, 2004); F (Daneel and Joubert, 2009) Chrysomphalus aonidum Alata Condor, PE, US (Alata No N/A N/A (L.) 1973; CABI, Condor, 1973; CABI, 2001; Nakahara, 2001; Nakahara, 1982 1982) Chrysomphalus Alata Condor, PE, US (Alata No N/A N/A dictyospermi (Morgan) 1973; CABI, Condor, 1973; CABI, 2001; Nakahara, 2001; Nakahara, 1982 1982) Diaspidiotus perniciosus CABI, 2000 PE, US (CABI, 2000) No N/A N/A (Comstock) Hemiberlesia lataniae Alata Condor, PE, US (Alata No N/A N/A (Signoret) 1973; CABI, Condor, 1973; CABI, 2000; Nakahara, 2000; Nakahara, 1982; Nunez, 2008 1982)

12 Although armored scales may enter on commercial fruit for consumption, they are highly unlikely to become established via this pathway. Please see discussion in section 2.2.2 for a detailed explanation.

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Scientific Name Reported on Distribution1 Quaran- Plant part(s) Follow Citrus spp. tine pest2 association3 pathway Hemiberlesia palmae Nunez, 2008 PE (Nunez, 2008), No N/A N/A (Cockerell) US (Ben-Dov, et al., 2012) Lepidosaphes beckii Alata Condor, PE, US (Alata No N/A N/A (Newman) 1973; CABI, Condor, 1973; CABI, (Syn: Cornuaspis beckii) 2000; Nakahara, 2000; Nakahara, 1982 1982 Lepidosaphes gloverii Alata Condor, PE (Alata Condor, No N/A N/A (Packard) 1973; Gonzalez et 1973; Nuñez, 2008), (Syn: Insulaspis gloverii al., 2005; US (CABI, 2000; (Packard)) Nakahara, 1982 Nakahara, 1982; Ben- Dov et al., 2012) Mycetaspis personata Ben-Dov et al., PE, US (FL) (Ben- No N/A N/A (Comstock) 2012 Dov et al., 2012) Parlatoria cinerea Hadden Ben-Dov et al., PE, US (MD, DC) [Yes] F, L (Masten Yes12 in Doane & Hadden 2012; Kosztarab, (Ben-Dov et al., Milek et al., 1996; Ooi et al., 2002; Kosztarab, 2009; 2002 1996; Ooi et al., Neubauer, 2002) 1980) Parlatoria pergandii Alata Condor, PE, US (Alata No N/A N/A Comstock 1973; CABI, Condor, 1973; CABI, 2001; Kosztarab, 2001; Kosztarab, 1996 1996)

Pinnaspis aspidistrae Nunez, 2008 PE (Nunez, 2008), No N/A N/A (Signoret) US (Ben-Dov et al., 2012) Pinnaspis strachani Colley Alata Condor, PE, US (Alata No N/A N/A 1973; CABI, Condor, 1973; CABI, 2002; Ben-Dov et 2002; Ben-Dov et al., al., 2012 2002) Pseudaonidia trilobitiformis Kosztarab, 1996; PE (Kosztarab, 1996; Yes F, L, S Yes12 (Green) PestID, 2003 PestID, 2003) (Kosztarab, 1996; PestID, 2003) Pseudischnaspis acephala Ben-Dov et al., PE (Ben-Dov et al., Yes L (Ben-Dov et No Ferris 2012 2012) al., 2012) Selenaspidus articulatus Alata Condor, PE, US (FL) (Alata No N/A N/A (Morgan) 1973; CABI, Condor, 1973; CABI, 2000; Dekle, 2000; Ebeling, 1959) 1976; Ebeling, 1959

Hemiptera: Margarodidae

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Scientific Name Reported on Distribution1 Quaran- Plant part(s) Follow Citrus spp. tine pest2 association3 pathway Icerya purchasi Maskell Alata Condor, PE, US (Alata No N/A N/A 1973; CABI, 2000 Condor, 1973; CABI, 2000) Hemiptera: Ortheziidae Insignorthezia pseudinsignis Ben-Dov et al., PE, US (Ben-Dov et No N/A N/A (Morrison) 2012 al., 2012) Praelongorthezia citricola Beingolea, 1971b; PE (Beingolea, Yes L, S No (Beingolea) CABI, 2001; Ben- 1971b; CABI, 2001; (Beingolea, (Syn.: Orthezia citricola Dov et al., 2012 Ben-Dov et al., 2012) 1971b; CABI, Beingolea) 2001; Ben- Dov et al., 2002) Praelongorthezia olivicola Alata Condor, PE (Alata Condor, Yes L, S (Alata No Kozár 1973; CABI, 1973; CABI, 2001; Condor, 1973; (Syn.: Orthezia olivicola 2001; Peña and Peña and Bennett, CABI, 2001; Beingolea) Bennett, 1995; 1995; Ben-Dov et al., Peña and Ben-Dov et al., 2002) Bennett, 1995; 2012 Ben-Dov et al., 2002) Praelongorthezia praelonga Alata Condor, PE, US (VI, PR) Yes L, S (Alata No Douglas 1973; Ben-Dov et (Alata Condor, 1973; Condor, 1973; (Syn.: Orthezia praelonga al., 2012; CABI, CABI, 2001; Ben- CABI, 2001; Douglas) 2001; PestID, Dov et al., 2002; Ben-Dov et 2003 PestID, 2003) al., 2002; PestID, 2003) Hemiptera: Arvelius acutispinus Alata Condor, PE (Alata Condor, Yes L, S, I, F No13 Breddin 1973; Henry and 1973; Henry and (Alata Condor, Froeschner, 1988 Froeschner, 1988; 1973; Henry McPherson and and McPherson, 2000) Froeschner, 1988; McPherson and McPherson, 2000) Hemiptera: Pseudococcidae Dysmicoccus brevipes CABI, 2000 PE, US (CABI, 2000) No N/A N/A (Cockerell) Dysmicoccus neobrevipes Ben-Dov et al., PE (Ben-Dov et al., Yes L, S, I, F No14 Beardsley 2012 2012) (Kessing et al., 2007) Ferrisia virgata Cock CABI, 2000 PE, US (CABI, 2000) No N/A N/A

13 Because of its size, biology, and mobility, this pest is highly unlikely to stay on the commodity through harvest and standard handling and processing. 14 Mealybugs are conspicuous and highly unlikely to survive post-harvest grading and treatment.

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Scientific Name Reported on Distribution1 Quaran- Plant part(s) Follow Citrus spp. tine pest2 association3 pathway Nipaecoccus nipae CABI, 2002 PE, US (CABI, 2002) No N/A N/A (Maskell) Phenacoccus madeirensis CABI, 2002 PE, US (CABI, 2002) No N/A N/A Green Planococcus citri (Risso) Alata Condor, PE, US (Alata No N/A N/A 1973; Beingolea, Condor, 1973; 1971a; CABI, Beingolea, 1971a; 2000 CABI, 2000) Planococcus minor Ben-Dov et al., PE (CABI, 2002; No15 N/A N/A (Maskell) 2012; CABI, Ben-Dov et al., 2002; 2002; Ooi et al., PestID, 2003; Ben- 2002; PestID, Dov, 1994; Ooi et al., 2003 2002)

Pseudococcus longispinus CABI, 2002 PE, US (CABI, 2002) No N/A N/A Targioni Tozzetti Hemiptera: Pyrrhocoridae Euryophthalmus balteatus Alata Condor, PE (Alata Condor, Yes F (Alata No16 (Stal) 1973; UC IPM, 1973) Condor, 1973; 2008 UC IPM, 2008) Hymenoptera: Apidae Trigona hyalinata Alata Condor, PE (Alata Condor, Yes L, I, F (Alata No16 amazonensis Du. 1973; Hill, 1983; 1973; Hill, 1983; Condor, 1973; Myazaki et al., Myazaki et al., 1984) Hill, 1983; 1984 Myazaki et al., 1984) Trigona testacea cupira Alata Condor, PE (Alata Condor, Yes L, I, F (Alata No16 Smith 1973; Escalante et 1973; Freire and Condor, 1973; al., 1981; Hill, Gara, 1970; Hill, Freire and 1983; Escalante, 1983; Escalante, Gara, 1970; 1974 1974) Hill, 1983; Escalante, 1974) Trigona trinidadensis Alata Condor, PE (Alata Condor, Yes L, S, F (Alata No16 (Provancher) 1973; CABI, 1973; CABI, 2001; Condor, 1973; [Syn: Melipona 2001; Hill, 1983 Hill, 1983) CABI, 2001; trinidadensis] Hill, 1983) Hymenoptera: Formicidae Acromyrex hispidus Alata Condor, PE (Alata Condor, Yes whole plant, L No Santschi 1973 1973) (Alata Condor, 1973)

15 Planococcus minor was listed as a quarantine pest previously (USDA, 2003), but currently is non-reportable/non- actionable (PestID, 2012). 16 Because of its size, biology, and mobility, this pest is highly unlikely to stay on the commodity through harvest and standard handling and processing.

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Scientific Name Reported on Distribution1 Quaran- Plant part(s) Follow Citrus spp. tine pest2 association3 pathway Atta cephalotes L. Alata Condor, PE (Alata Condor, Yes L (Alata No 1973; Kliejunas et 1973) Condor, 1973; al., 2001 Kliejunas et al., 2001) Atta sexdens L. Alata Condor, PE (Alata Condor, Yes L (Alata No 1973; Escalante et 1973; Escalante et al., Condor, 1973; al., 1981; 1981; Kliejunas et al., Kliejunas et Kliejunas et al., 2001) al., 2001) 2001 Hymenoptera: Meliponidae Melipona sp. Escalante, 1974 PE (Escalante, 1974) Yes F (Escalante, No16 1974) Lepidoptera: Arctiidae Carales astur (Cramer) Jacobson, 1991; PE (Jacobson, 1991; Yes L No Jacobson, 2003; Anonymous, 2003; (Anonymous, Zhang, 1994 Zhang, 1994) 2003; Jacobson, 2003; Zhang, 1994) Lepidoptera: Gracillariidae Phyllocnistis citrella CABI, 2001; PE (Campos et al., [Yes] L (CABI, No Stainton Heppner and 2007), US (AL, FL, 2001; Campos Fasulo, 2010; LA, TX) (CABI, et al., 2007; Castillo C. and 2001; Heppner and Castillo C. and Cornejo H., 1995 Fasulo, 2010) Cornejo H., 1995; Heppner and Fasulo, 2010) Lepidoptera: Limacodidae Sibine sp. Alata Condor, PE (Alata Condor, Yes L (Alata No 1973 1973) Condor, 1973) Lepidoptera: Noctuidae Agrotis ipsilon Hufnagel CABI, 2012; PE (CABI, 2012; No N/A N/A Carbonell Torres, Carbonell Torres, 1999 1999), US (CABI, 2012) Helicoverpa zea (Boddie) CABI, 2002 PE, US (CABI, 2002) No N/A N/A Peridroma saucia (Hübner) CABI, 2012 PE, US (CABI, 2012) No N/A N/A Spodoptera eridania Stoll CABI, 2002 PE, US (CABI, 2002) No N/A N/A Spodoptera frugiperda J.E. CABI, 2002 PE, US (CABI, 2002) No N/A N/A Smith Lepidoptera: Oecophoridae

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Scientific Name Reported on Distribution1 Quaran- Plant part(s) Follow Citrus spp. tine pest2 association3 pathway Inga iacunata (Meyr.) Alata Condor, PE (Alata Condor, Yes L, F, S (Alata No17 1973; Borrer et al., 1973; Borrer et al., Condor, 1973; 1989; Borrer and 1989; Borrer and Borrer et al., White, 1970 White, 1970) 1989; Borrer and White, 1970) Lepidoptera: Papilionidae Papilio isidorus isidorus Alata Condor, PE (Alata Condor, Yes L (Alata No Doubleday 1973; Lewis, 2010 1973; Lewis, 2010) Condor, 1973; (Syn: Heraclides isidorus Lewis, 2010) isidorus Doubleday) Papilio paeon paeon Alata Condor, PE (Alata Condor, Yes L (Alata No (Boisduval) 1973; Lewis, 2010 1973; Lewis, 2010) Condor, 1973; (Syn: Heraclides paeon Lewis, 2010) paeon (Guilding) Lepidoptera: Psychidae Oiketicus kirbyi Guilding Alata Condor, PE (Alata Condor, Yes L (Alata No 1973; Gordh and 1973; Gordh and Condor, 1973; Headrick, 2001; Headrick, 2001; Gordh and Gravena and de Rhainds and Cabrera Headrick, Almeida, 1982; – La Rosa, 2010) 2001 Gravena Zhang, 1994 and de Almeida, 1982; Zhang, 1994) Lepidoptera: Tortricidae Argyrotaenia sphaleropa Aguilar, 1980; PE (Aguilar, 1980; Yes L, F, I No18 Meyrick Alata Condor, Alata Condor, 1973; (Aguilar, 1973; Ebeling, Ebeling, 1959; 1980; Alata 1959; Meneguim Meneguim and Condor, 1973; and Hohmann, Hohmann, 2007; Ebeling, 1959; 2007; Salazar Salazar Torres, 1999) Meneguim Torres, 1999 and Hohmann, 2007; Salazar Torres, 1999)

17 We found no specific biological information on I. iacunata. In general, though, caterpillars in this genus tie together mature or old leaves and line them with silk and frass, where they rest and develop (Diniz et al., 2007). The final instar completes the larval stage and pupates in a special envelope inside the leaf shelter. Therefore, Inga species are highly unlikely to be associated with fruit. 18 Argyrotaenia sphaleropa typically attacks citrus during fruit set, causing premature fruit drop, or causes noticeable damage to the fruit rind and does not feed inside fruit (Salazar Torres, 1999; Meneguim and Hohmann, 2007). It is, therefore, highly unlikely to be associated with fruit at harvest.

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Scientific Name Reported on Distribution1 Quaran- Plant part(s) Follow Citrus spp. tine pest2 association3 pathway Ecdytolopha aurantiana Adamski and PE (Escalante et al., Yes F (Adamski Yes (Lima) Brown, 2001; 1981) and Brown, (Syns.: E. torticornis, Bento et al., 2001 2001; Bento et Gymnandrosoma al., 2001; aurantianum) Escalante et al., 1981) : Microcentrum laurifolium L. Alata Condor, PE (Alata Condor, Yes F, L, I (Alata No 1973 1973) Condor, 1973; Griffiths, 195219) cancellata Alata Condor, PE (Alata Condor, Yes L (Alata No Serv. 1973; CABI, 2000 1973; CABI, 2000) Condor, 1973; CABI, 2000) Thysanoptera: Thripidae Frankliniella occidentalis CABI, 2012 PE, US (CABI, 2012) No N/A N/A (Pergande) Heliothrips haemorrhoidalis CABI, 2012 PE, US (CABI, 2012) No N/A N/A Bouché Microcephalothrips CABI, 2012 PE, US (CABI, 2012) No N/A N/A abdominalis (D.L. Crawford) Thrips tabaci Lindeman Tsuchiya, 2002; PE (SENASA-Peru, No N/A N/A Vassiliou, 2010 2011), US (Hodges and Hamon, 2004)

Criconemella sp. De Grisse CABI, 2000 PE (CABI, 2000) Yes R (CABI, No & Loof 2000; Norton et al., 1984)

Helicotylenchus dihystera CABI, 2001; PE, US (CABI, 2001; No N/A N/A (Cobb) Sher O'Bannon and Norton et al., 1984; Inserra, 1989 O'Bannon and Inserra, 1989)

19 Based on the feeding habits on Citrus trees of a related species of katydid, Microcentrum rhombifolium, katydids primarily feed on leaves, and only occasionally feed on the rind of Citrus fruit (Griffiths, 1952). In addition, these species are typically quite large and conspicuous, making them easy to remove from infested commodities. Thus, this pest seems highly unlikely to follow the pathway.

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Scientific Name Reported on Distribution1 Quaran- Plant part(s) Follow Citrus spp. tine pest2 association3 pathway Helicotylenchus multicinctus CABI, 2001; PE, US (CABI, 2001; No N/A N/A (Cobb) Golden Norton et al., Norton et al., 1984; 1984; O'Bannon O'Bannon and and Inserra, 1989 Inserra, 1989) Hemicriconemoides CABI, 2001; PE (CABI, 2001; Yes20 R (CABI, No mangiferae Siddiqi MacGowan, 1984 MacGowan, 1984; 2001; Norton et al., 1984) MacGowan, 1984; Norton et al., 1984) Meloidogyne exigua Goeldi CABI, 2001 PE (CABI, 2001) Yes R (CABI, No 2001) Pratylenchus brachyurus CABI, 2001 PE, US (CABI, 2001; No N/A N/A (Godfrey) Filipjev & Norton et al., 1984) Schuurmans Stekhoven Radopholus similis (Cobb) CABI, 2001; PE, US (FL, HI, PR) [Yes] R (CABI, No Thorne Timmer et al., (CABI, 2001; 2001; Timmer 2000 Timmer et al., 2000) et al., 2000) Rotylenchulus reniformis CABI, 2001 PE, US (CABI, 2001; No N/A N/A Linford & Oliveira Norton et al., 1984) Scutellonema brachyurus CABI, 2001; PE, US (CABI, 2001; No N/A N/A Steiner, Andrássy O'Bannon and O'Bannon and Inserra, 1989 Inserra, 1989) Trichodorus sp. CABI, 2001; PE (CABI, 2001; Yes R (CABI, No Norton et al., 1984 Norton et al., 1984) 2001; Norton et al., 1984) Tylenchulus semipenetrans CABI, 2001; PE (Koc, 1997), US No N/A N/A Cobb Herrera et al., (CABI, 2001; Herrera 1980; Koc, 1997 et al., 1980) Xiphinema brasiliense Alkemade and PE, US (FL) [Yes] R (Alkemade No Lordello Loof, 1990; (Alkemade and Loof, and Loof, Lamberti et al., 1990; Lamberti et al., 1990; 1987; Norton et 1987; Norton et al., Lamberti et al., 1984) 1984) al., 1987; Norton et al., 1984) Xiphinema brevicolle Alkemade and PE, US (CA) [Yes] R (Alkemade No Lordello & Da Costa Loof, 1990 (Alkemade and Loof, and Loof, 1990; Norton et al., 1990; Norton 1984) et al., 1984) Xiphinema californicum Alkemade and PE, US (Alkemade No N/A N/A Lamberti and Bleve- Loof, 1990; and Loof, 1990; Zacheo Norton et al., 1984 Norton et al., 1984) Xiphinema floridae Lamberti et al., PE, US (Lamberti et No N/A N/A Lamberti and Bleve- 1987 al., 1987; Norton et Zacheo al., 1984)

20 No action required except when destined to Hawaii, Puerto Rico, and the U.S. Virgin Islands (PestID, 2012).

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Scientific Name Reported on Distribution1 Quaran- Plant part(s) Follow Citrus spp. tine pest2 association3 pathway Xiphinema index Thorne & CABI, 2001; PE, US (CABI, 2001; No N/A N/A Allen Lehman, 1981 Lehman, 1981; Norton et al., 1984) Xiphinema paritaliae Loof Lamberti et al., PE (Lamberti et al., Yes R (Lamberti et No & Sharma 1987 1987) al., 1987) Xiphinema peruvianum n.sp. Lamberti and PE (Lamberti and Yes R (Lamberti No (Syn.: X. americanum Bleve-Zacheo, Bleve-Zacheo, 1979; and Bleve- Cobb sensu lato) 1979; Lamberti et Lamberti et al., 1987) Zacheo, 1979; al., 1987 Lamberti et al., 1987) Xiphinema setariae Luc Alkemade and PE, US (Alkemade No N/A N/A Loof, 1990 and Loof, 1990; Norton et al., 1984) Xiphinema vulgare Tarjan Lamberti et al., PE, US (Lamberti et No N/A N/A 1987; Tarjan, 1964 al., 1987; Tarjan, 1964) FUNGI AND CHROMISTANS Alternaria alternata (Fr.: Farr and Rossman, PE (Farr and No21 N/A N/A Fr.) Keissl. 2012; Marín et al., Rossman, 2012; 2006 Marín et al., 2006), US (Farr and Rossman, 2012) Alternaria brassicae (Berk.) CABI, 2001 PE, US (CABI, 2001; No N/A N/A Sacc. Farr and Rossman, 2012) Alternaria citri Ellis and N. Farr and Rossman, PE (Koc, 1997; No N/A N/A Pierce 2012; Koc, 1997 SENASA-Peru, 2011), US (Farr and Rossman, 2012) Athelia rolfsii (Curzi) Tu & Farr and Rossman, PE, US (Farr and No N/A N/A Kimbr 2012 Rossman, 2012) (Syn.: Corticium rolfsii Curzi) (Anamorph: Sclerotium rolfsii Sacc.) Botryosphaeria parva Cunnington et al., PE (Javier-Alva et al., No N/A N/A Pennycook & Samuels 2007; Adesemoye 2009), US (Urbez- (Anamorph: and Eskalen, 2011 Torres and Gubler, Neofusicoccum parvum 2009; Adesemoye (Pennycook & Samuels) and Eskalen, 2011) Crous, Slippers & A. J. L. Phillips)

21 Marín et al. (2006) report a damaging tangerine-pathotype of Alternaria alternata in Peru, which may be a unique strain of this pathogen. Currently, however, we cannot regulate this pathogen strain, because we cannot distinguish it from native strains of A. alternata in the United States.

Ver. 1 (Original) November 2, 2012 15

Scientific Name Reported on Distribution1 Quaran- Plant part(s) Follow Citrus spp. tine pest2 association3 pathway Botryotinia fuckeliana (de Fullerton et al., PE (Koc, 1997), US No N/A N/A Bary) Whetzel 1999; Farr and (Farr and Rossman, Anamorph: Botrytis cinerea Rossman, 2012 2012) Ceratocystis fimbriata Ellis Castrillón A. and PE (CABI, 2012) , No N/A N/A & Halst. Urrea J., 2000; US (Farr and CABI, 2001; Farr Rossman, 2012) and Rossman, 2012 Colletotrichum Farr and Rossman, PE (Farr and No N/A N/A gloeosporioides (Penz.) 2012; Agostini et Rossman, 2012; Penz. & Sacc. al., 1992 Lenne and Burdon, (Teleomorph: Glomerella 1990), US (Farr and cingulata (Stonem.) Rossman, 2012) Spauld. & Schrenk) Corticium koleroga (Cooke) CABI, 2012; Farr PE, US (CABI, 2012; No N/A N/A Höhnel and Rossman, Farr and Rossman, Syn.: Pellicularia 2012; Timmer et 2012) koleroga Cooke al., 2000 Corticium salmonicolor CABI, 2000; PE, US (CABI, 2000; No N/A N/A Berk. & Broome Timmer et al., Timmer et al., 2000) Syn.: Erythricium 2000 salmonicolor Berk. & Broome) Burdsall Elsinoë fawcettii Bitanc. & CABI, 2000; PE, US (CABI, 2000; No N/A N/A Jenkins Sivanesan and Sivanesan and Critchett, 1974 Critchett, 1974) Haematonectria Koc, 1997 PE (Koc, 1997), US No N/A N/A haematococca (Berk. & (Farr and Rossman, Broome) Samuels & 2012) Rossman (Anamorph: Fusarium solani (Mart.) Sacc.) Lasiodiplodia theobromae Farr and Rossman, PE (Farr and No N/A N/A (Pat.) Griffon & Maubl. 2012; Koc, 1997 Rossman, 2012; Koc, (Syn.: Botryodiplodia 1997), US (Farr and theobromae Pat.) Rossman, 2012) (Teleomorph: Botryosphaeria rhodina (Berk. & M.A. Curtis) Arx) Macrophomina phaseolina CABI, 2012; Farr PE (CABI, 2012; No N/A N/A (Tassi) Goid and Rossman, Torres, 2002), US 2012 (CABI, 2001; Farr and Rossman, 2012) Penicillium digitatum (Pers.: Farr and Rossman, PE (Farr and No N/A N/A Fr.) Sacc. 2012; Koc, 1997 Rossman, 2012; Koc, 1997)

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Scientific Name Reported on Distribution1 Quaran- Plant part(s) Follow Citrus spp. tine pest2 association3 pathway Penicillium italicum Koc, 1997 PE (Koc, 1997), US No N/A N/A Wehmer (Farr and Rossman, 2012) Phytophthora cactorum CABI, 2001; Farr PE, US (CABI, 2001; No N/A N/A (Lebert & Cohn) Schröter and Rossman, Farr and Rossman, 2012; Thomidis et 2012) al., 2005 Phytophthora capsici CABI, 2001; Farr PE, US (CABI, 2001; No N/A N/A Leonian and Rossman, Farr and Rossman, 2012; Horst, 2001 2012; Horst, 2001) Phytophthora citrophthora Bowman et al., PE (Farr and No N/A N/A (R.H. Sm. & E. Sm.) 2007; CABI, Rossman, 2012; Koc, Leonian 2001; Farr and 1997), US (CABI, Rossman, 2012; 2001; Farr and Koc, 1997 Rossman, 2012) Phytophthora nicotianae Bowman et al., PE (Koc, 1997), US No N/A N/A Breda de Haan 2007; CABI, (CABI, 2001; Farr (Syn.: P. parasitica 2001; Farr and and Rossman, 2012) Dastur) Rossman, 2012 Phytophthora palmivora (E. Bowman et al., PE, US (CABI, 2001; No N/A N/A J. Butler) E. J. Butler 2007; CABI, Farr and Rossman, 2001; Farr and 2012; Timmer et al., Rossman, 2012; 2000) Timmer et al., 2000 Phytophthora spp. Koc, 1997 PE (Koc, 1997) Yes Seedlings, F Yes (Koc, 1997) Rosellinia bunodes (Berk. & CABI, 2002; Farr PE, US (PR, VI) Yes R (CABI, No Broome) Sacc. and Rossman, (CABI, 2002; Farr 2002; Farr and 2012; Koc, 1997; and Rossman, 2012; Rossman, Timmer et al., Timmer et al., 2000) 2012; Timmer 2000 et al., 2000) Sclerotinia sclerotiorum CABI, 2001; Farr PE (Torres, 2002; No N/A N/A (Lib.) de Bary and Rossman, Farr and Rossman, 2012; Timmer et 2012), US (CABI, al., 2000 2001; Farr and Rossman, 2012; Timmer et al., 2000) Septoria sp. Alvarez-Bernaola PE22 (Alvarez- Yes F (Alvarez- Yes et al., 2007 Bernaola et al., 2007) Bernaola et al., 2007)

22 Alvarez-Bernaola et al. (2007) reported what appears to be a unique species of Septoria that infects fruit of Citrus limetta in Peru. Extensive host range testing of other Citrus species has not been reported to date, so we do not know if the host range is limited to C. limetta. It appears distinct from Septoria citri (on C. limon from Spain) and S. citricola (on C. sinensis in Italy), but it is not clear if it has been described and named as a new species to date (Alvarez-Bernaola et al.,

Ver. 1 (Original) November 2, 2012 17

Scientific Name Reported on Distribution1 Quaran- Plant part(s) Follow Citrus spp. tine pest2 association3 pathway Sphaeropsis tumefaciens Abbott, 1931; Farr PE (Abbott, 1931), No N/A N/A Hedges and Rossman, US (Farr and 2012; Timmer et Rossman, 2012) al., 2000 Thanatephorus cucumeris Farr and Rossman, PE, US (CABI, 2001; No N/A N/A (Frank) Donk 2012; Timmer et Farr and Rossman, (Anamorph: Rhizoctonia al., 2000 2012) solani J.G. Kühn BACTERIA AND PHYTOPLASMAS Rhizobium radiobacter Bradbury, 1986; PE, US (Bradbury, No N/A N/A (Beij. & v. Deld.) Pribram CABI, 2001 1986; CABI, 2001)

VIRUSES AND VIROIDS Citrus exocortis viroid CABI, 2012 PE (CABI, 2012; No N/A N/A (CEVd) Murcia et al., 2010), US (CABI, 2012) Citrus psorosis virus (CPsV) Timmer et al., PE (Bazan de Segura, No N/A N/A 2000 1972; Koc, 1997), US (Timmer et al., 2000) Citrus tristeza virus (CTV) Saponari and PE (Koc, 1997), US No N/A N/A Yokomi, 2010; (Roistacher and CABI, 2000; Moreno, 1991; Roistacher and Saponari and Moreno, 1991 Yokomi, 2010; CABI, 2000) Citrus vein enation virus Bazan de Segura, PE, US (Bazan de No N/A N/A (CVEC) 1972; Timmer et Segura, 1972; al., 2000 Timmer et al., 2000) Citrus dwarfing viroid Murcia et al., 2010 PE (Murcia et al., No N/A N/A (Syn.: Citrus viroid III 2010), US (Brlansky (CVd-III)) and Timmer, 2012; Kunta et al., 2007) Hop stunt viroid (HSVd) Murcia et al., 2010 PE (Murcia et al., No N/A N/A (Citrus cachexia) 2010), US (Brlansky and Timmer, 2012; Kunta et al., 2007; Timmer et al., 2000) ALGAE Cephaleuros virescens Koc, 1997 PE (Koc, 1997), US No N/A N/A Künze (CABI, 2012) MOLLUSKS

2007). Citrus limetta is not proposed for export from Peru, so if this Septoria species infects only C. limetta, then it would not move on other exported Citrus species.

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Scientific Name Reported on Distribution1 Quaran- Plant part(s) Follow Citrus spp. tine pest2 association3 pathway Helix aspersa Muller CABI, 2001; PE, US (CABI, 2001; Yes23 Bark, wood, No24 (Mollusca: Helicidae) Dekle and Fasulo, Dekle and Fasulo, R, F, L, S, Sd, 2002 2002) I (CABI, 2001; Dekle and Fasulo, 2002)

2.2. Quarantine pests not considered for risk mitigation

Quarantine pests not listed above could be detrimental to agriculture or ecosystems in the continental United States, but they are not candidates for risk mitigation for a variety of reasons. For example, they may be mainly associated with plant parts other than the commodity; they may be associated with the commodity, but would not reasonably remain with the commodity through standard harvest and post- harvest processing; they may have been intercepted as biological contaminants of these commodities during U.S. agricultural port-of-entry inspection, but would not likely be present in commercial shipments; or the organism may have been identified (in the literature or in USDA’s interception data) only to the genus level, and the genus in question occurs in the continental United States.

2.2.1. Pests not identified to species Generally, based on standards by the International Plant Protection Convention (IPPC, 2009), we do not consider risk mitigation measures for organisms identified only to the genus level if the genus in question is reported in the continental United States. Often there are many species within a genus, and we cannot know if the unidentified species occurs in the continental United States and, consequently, whether it meets the definition of a quarantine pest for the continental United States. In this risk assessment, the above statement applies to the arthropods Compsus, Aleurotrachelus, Aonidia, Paraleyrodes, Asterolecanium, Lecanodiaspis, Ceroplastes, Pulvinaria, Melipona, and Sibine and to the pathogens Criconemella, Septoria, and Trichodorus. These genera occur in the continental United States (CABI, 2012; Farr and Rossman, 2012; Ben-Dov et al., 2012; O’Brien and Peña, 2012; Hodges and Hamon, 2004; Bibbs and Frank, 2012). Lack of specific identification may indicate the limits of current taxonomic knowledge, or the life stage or quality of the specimen submitted for identification. 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 development of detailed assessments for known pests that inhabit a variety of ecological niches, such as internal fruit feeders or foliage pests, allows effective mitigation measures to eliminate the known organisms as well as similar but incompletely identified organisms that inhabit the same niche. If pests identified to higher taxa are intercepted in the future, we may reevaluate their risk.

2.2.2. Armored scales We did not further analyze the armored scales (Hemiptera: ) identified in this risk assessment as quarantine pests likely to follow the pathway, Aulacaspis tubercularis, Parlatoria

23 Listed as actionable pest for Alabama and Florida only (PestID, 2012). 24 Because of its size, biology, and/or mobility, this pest is highly unlikely to stay on the commodity through harvest and standard handling and processing.

Ver. 1 (Original) November 2, 2012 19

cinerea, and Pseudaonidia trilobitiformis, because armored scales are highly unlikely to become established via this pathway due to their very limited ability to disperse to new host plants (Miller et al., 1985; PERAL, 2007). Only a certain immature form of armored scales, the crawler, can self-disperse. Crawlers are highly unlikely to successfully disperse by walking from their natal host since they are not capable of rapid movement over bare soil or rough surfaces. They typically disperse by being blown from plant to plant in the wind. Additionally, their dispersal period is limited to approximately 24 hours, after which they start feeding, become firmly anchored to the host tissue, and lose their legs. Adult females have no wings or legs. Dispersal from fruit discarded into the environment is highly unlikely because of low wind speeds at ground level and low survival rate of crawlers on the ground or on decaying fruit or fruit peels.

2.2.3. Doubtful host association Anastrepha distincta. Anastrepha distincta Greene [Diptera: Tephritidae] is reported in Peru (CABI, 2002; Norrbom and Kim, 1988; Couturier et al., 1993) and on Citrus spp. (CABI, 2002; Norrbom and Kim, 1988; Uchoa-Fernandes et al., 2003). Despite that, Norrbom and Kim, 1988) list only lab and questionable reports of A. distincta on citrus. Consequently, we think that this fruit fly species is unlikely to be associated with commercial citrus for export. Anastrepha grandis and A. minensis. Anastrepha grandis Macquart (CABI, 2002; Korytkowski and Ojeda, 1968; Norrbom and Kim, 1988; Stone, 1942), and A. minensis Lima (synonym = A. extensa Stone) [Diptera: Tephritidae] (Korytkowski and Ojeda, 1968; Norrbom and Kim, 1988; Stone, 1942) are both reported to be in Peru. For both pests, Citrus spp., however, are either doubtful hosts (Norrbom and Kim, 1988; Ooi et al., 2002) or are not included in the reported host range (White and Elson-Harris, 1992). Therefore, we did not list them above.

Anastrepha striata. Anastrepha striata Schin. is reported in Peru (Alata Condor, 1973; CABI, 2012), but is typically restricted to fruit of the genus Psidium (guavas) and is considered stenophagous (Aluja et al. 2000a; Aluja et al. 2004). The primary records of A. striata on citrus are questionable, and, therefore, this fruit fly is unlikely to attack citrus (Norrbom, 2003). Based on that evidence, we did not list the pest above.

Mycena citricolor. Mycena citricolor (Berk. & Curtis) Sacc. [Fungi and Chromistans] has been reported in Peru (CABI, 2002; Farr and Rossman, 2012; Mariau, 2001; Thurston, 1973), and is actionable except when destined to Puerto Rico or the U.S. Virgin Islands, where it is already established (PestID, 2012). It has only been reported to infect coffee fruit (Trujillo et al., 1995) and has not been associated with Citrus fruit infection to date.

2.3. Quarantine pests likely to follow the pathway and candidates for risk mitigation

We identified quarantine pests that are likely to follow the commodity pathway and that are candidates for further mitigation below (Table 2).

As noted in the Introduction, Peru proposes to include the following processes and conditions prior to approval to start cold treatment for fruit flies in transit:  phytosanitary management of pests associated with Citrus in the grove;  packinghouse measures that include inspection; primary grading to remove small, damaged, infected, or infested fruit; washing and brushing to clean fruit; spraying with wax containing

Ver. 1 (Original) November 2, 2012 20

fungicide, followed by air-drying; secondary grading to remove damaged or blemished fruit; sorting by size and packaging in new cardboard boxes; storage with safeguarding measures to prevent reinfestation under consistent conditions; and  final inspection and certification procedures, These processes (7 CFR § 319.56, 2012) have been successfully implemented for the five previously approved export areas.

Table 2. Quarantine pests likely to follow the pathway with fresh fruit of Citrus spp. from all parts of Peru and under consideration for further mitigation. Pest Classification Pest Scientific Name Diptera: Tephritidae Anastrepha fraterculus Anastrepha obliqua Anastrepha serpentina Ceratitis capitata Lepidoptera: Tortricidae Ecdytolopha aurantiana 3. Authors and Reviewers

Author: Lisa M. Ferguson, Risk Analyst/Plant Pathologista

Reviewers: Robert G. Ahern, Risk Analyst/Entomologista Betsy Randall-Schadel, Risk Analyst/Plant Pathologista a Plant Epidemiology and Risk Analysis Laboratory, USDA-APHIS-PPQ

4. Literature Cited

7 CFR § 319.56. 2012. U.S. Code of Federal Regulations, Title 7, Part 319 (7 CFR § 319.56 - Foreign Quarantine Notices), Subpart 56 (7 CFR § 319.56 - Fruits and Vegetables). Abbott, E. V. 1931. Enfermedades de las plantas en el Peru. Boletin De La Direccion De Agricultura y Ganaderia 1(1):54-58. Adamski, D., and J. W. Brown. 2001. Systematic revision of the Ecdytolopha group of genera (Lepidoptera: Tortricidae: Grapholitini) in the New World. Entomologica Scandinavica Supplement (58):1-86. Adesemoye, A. O., and A. Eskalen. 2011. First report of Spencermartinsia viticola, Neofusicoccum australe, and N. parvum causing branch canker of citrus in California. Plant Disease 95(770). Agostini, J. P., L. W. Timmer, and D. J. Mitchell. 1992. Morphological and pathological characteristics of strains of Colletotrichum gloeosporioides from Citrus. 82 (1377-1382). Aguilar, F. P. G. 1980. Apuntes sobre el control biologico y el control integrado de las plagas agricolas en el Peru. [Notes on biological control and integrated control of agricultural pests in Peru.]. Revista Peruana de Entomologia [Peruvian Magazine of Entomology] 23(1):83-110. Aguilar, F. P. G. 1982. El control biologico y el control integrado de las plagas agricolas en el Peru. [The biological control and the integrated control of agricultural pests in Peru.] Zoologia neotropical. Actas del VIII Congreso Latinoamericano de Zoologia. [Proceedings of the VIII Latin American Congress of Zoology.] 1982:293-296. Alata Condor, J. 1973. Lista de insectos y otros animales daninos a la agricultura en el Peru. Manual No. 38 [List of and other pests in agriculture in Peru. Manual No. 38]. Pages 43-47, 50, 56 Lista de insectos y

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