United States Importation of Fresh Avocado Fruit Department of Agriculture (Persea americana Miller) from

Animal and Plant Continental Ecuador into the Health Inspection Service Continental United States

July 18, 2017

Final A Qualitative, Pathway-Initiated Pest

Risk Assessment

Agency Contact:

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

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

Pest Risk Assessment for Avocado from Ecuador

Executive Summary

The Animal and Plant Health Inspection Service (APHIS) of the United States Department of Agriculture (USDA) prepared this risk assessment to examine plant pest risks associated with importing commercially produced fruit of avocado, Persea americana Miller (Lauraceae), for consumption from continental Ecuador into the continental United States, including Alaska. Based on the market access request submitted by Ecuador, we considered the pathway to include the following processes and conditions: fruit will be harvested by hand and washed with cool water, and damaged or ripe fruit will be culled. All processes and conditions considered during the risk assessment process become minimum conditions necessary for entry of avocado.

Based on the scientific literature, port-of-entry pest interception data, and information from the government of Ecuador, we developed a list of all potential pests with actionable regulatory status for the continental United States that are known to occur in continental Ecuador (on any host) and to be associated with avocado plant species (anywhere in the world). Of these, we found four organisms that have a reasonable likelihood of being associated with avocado following harvesting from the field and prior to any post-harvest processing, and thus may follow the pathway.

We analyzed the pest risk potential of these organisms and determined that the following met the threshold for unacceptable consequences of introduction and had non-negligible likelihoods of introduction. We therefore consider these pests to be candidates for risk management:

Pest type Taxonomy Scientific name Likelihood of Introduction overall rating Arthropod Diptera: Tephritidae Anastrepha fraterculus (Wiedemann) Medium Anastrepha serpentina (Wiedemann) Medium Anastrepha striata Schiner Medium Ceratitis capitata (Wiedemann) Medium

Detailed examination and choice of appropriate phytosanitary measures to mitigate pest risk are part of the pest risk management phase within APHIS and are not addressed in this document.

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Table of Contents

Executive Summary ...... i 1. Introduction ...... 1 1.1. Background ...... 1 1.2. Initiating event ...... 1 1.3. Determination of the necessity of a weed risk assessment for avocado ...... 1 1.4. Description of the pathway...... 2 2. Pest List and Pest Categorization ...... 3 2.1. Pests considered but not included on the pest list ...... 3 2.2. Pest list ...... 5 2.3. Pests selected for further analysis ...... 8 3. Assessing Pest Risk Potential ...... 8 3.1. Introduction ...... 8 3.2. Assessment results ...... 9 4. Summary and Conclusions of Risk Assessment ...... 21 5. Acknowledgements ...... 22 6. Literature Cited ...... 22 7. Appendix A. Pests with non-actionable regulatory status ...... 28

Final July 18, 2017 ii Pest Risk Assessment for avocado from Ecuador

1. Introduction

1.1. Background

This document was prepared by the Plant Epidemiology and Risk Analysis Laboratory of the Center for Plant Health Science and Technology, USDA Animal and Plant Health Inspection Service (APHIS), Plant Protection and Quarantine (PPQ), to evaluate the pest risk associated with the importation of commercially produced fresh fruit of avocado (Persea americana Miller) for consumption from Ecuador into the continental United States.

This is a qualitative risk assessment, meaning that the likelihood and consequences of pest introduction are expressed as qualitative ratings rather than in numerical terms. Methodology and rating criteria used are detailed in the Guidelines for Plant Pest Risk Assessment of Imported Fruit and Vegetable Commodities, Version 6.0 (PPQ, 2012). This methodology is consistent with guidelines provided by the International Plant Protection Convention (IPPC) in the International Standard for Phytosanitary Measures (ISPM) No. 11, “Pest Risk Analysis for Quarantine Pests, Including Analysis of Environmental Risks and Living Modified Organisms” (IPPC, 2013). The use of biological and phytosanitary terms is consistent with ISPM No. 5, “Glossary of Phytosanitary Terms” (IPPC, 2012).

As defined in ISPM No. 11, this document comprises Stage 1 (Initiation) and Stage 2 (Risk Assessment) of risk analysis. Stage 3 (Risk Management) will be covered in a separate document.

1.2. Initiating event

The importation of fruits and vegetables for consumption into the United States is regulated under Title 7 of the Code of Federal Regulations, Part 319.56 (7 CFR § 319.56, 2013). Currently, under this regulation, the entry of avocados from Ecuador into the continental United States is not authorized. This commodity risk assessment was initiated due to a request by Engineer Wilson Patricio Almeida Granja, Director of Sanidad Vegetal – Agrocalidad, of the Ecuadorian Ministry of Agriculture, Livestock, Aquaculture, and Fisheries to change the Federal Regulation to allow entry (Granja, 2013)

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

In some cases, an imported commodity could become invasive in the pest risk analysis (PRA) area. If warranted, the pest risk posed by avocado itself is evaluated in a weed risk assessment, conducted separately from avocado risk assessment.

Weed risk assessments are unnecessary for plant species that are widely established (native or naturalized) or cultivated in the continental United States, for commodities that are already enterable into the continental United States from other countries, or when the plant part(s) cannot easily propagate on its own or be propagated. We determined that a weed risk assessment is not needed for avocados because they are cultivated in the United States.

Final July 18, 2017 1 Pest Risk Assessment for avocado from Ecuador

1.4. Description of the pathway

A pathway is “any means that allows the entry or spread of a pest” (IPPC, 2012). In this risk assessment, the specific pathway of concern is the importation of fresh fruit of avocado (Persea americana Miller) for consumption from Ecuador into the continental United States; the movement of this commodity provides a potential pathway for the introduction and/or spread of plant pests.

The following description of this pathway focuses on the conditions that may affect plant pest risk, including morphological and physiological characteristics of avocado, as well processes that avocado will undergo from production in Ecuador through importation and distribution in the continental United States. These conditions provided the basis for creating the pest list and assessing the likelihood of introduction of the pests selected for further analysis; therefore, all components of the pathway, as they are described below, should be considered mandatory conditions for importation of avocado.

1.4.1. Description of avocado Fresh avocado fruit.

1.4.2. Production and harvest procedures in the exporting area Avocados in Ecuador are produced in the highlands of the provinces of Carchi, Imbabura, Pichincha, Cotopaxi, Tungurahua, Azuay, and Loja. The temperature is related to the altitude: between 1,500-3,000 meters the average temperatures range from 10 to 20 °C. The production is located in the Sub-humid Temperate region corresponding to the dry forest ecological formation Lower Montane (Sanidad Vegital, 2013). Ecuador can produce avocados year-round with peak production from February to March and harvest from August to September.

1.4.3. Post-harvest procedures in the exporting area Fruit are hand-harvested. Packing includes a preliminary wash with cool water and culling of damaged or overripe fruit.

1.4.4. Shipping and storage conditions Fruit are packed in wood or corrugated cardboard boxes, 45 x 30 cm in width, and ranging from 9.5–11 cm in height. Boxes hold between 13 and 15 fruit depending on fruit size. Fruit can be shipped by sea or air.

1.4.5. Summary of the pathway Figure 1 summarizes the pathway of concern: the importation of fresh fruit of avocados for consumption from Ecuador into the continental United States.

Final July 18, 2017 2 Pest Risk Assessment for avocado from Ecuador

Figure 1. Pathway diagram for imports of avocado from Ecuador into the continental United States.

2. Pest List and Pest Categorization

The pest list is a compilation of all plant pests with actionable regulatory status for the continental United States that are present in Ecuador (on any host) and associated with Persea americana (anywhere in the world). Species on the pest list with a reasonable likelihood of being present on avocado at the time of harvest could follow the pathway into the continental United States, and are therefore analyzed in more detail to determine their pest risk potential. Pests are considered to be of regulatory significance if they are actionable at U.S. ports-of-entry. Actionable pests include quarantine pests, regulated non-quarantine pests, pests under official control or considered for official control, and pests that require evaluation for regulatory action.

2.1. Pests considered but not included on the pest list

2.1.1. Pests with weak evidence for association with avocado or for presence in Ecuador Cercospora lingue Spegazzini is listed as associated with avocado in Wellman, 1977), but is not a recognized Cercospora fide (Chupp, 1953) and its status is unclear (Crous and Braun, 2003). Consequently, we did not list this pest in Table 1.

The orange worm, Ecdytolopha aurantiana Lima, is present in Ecuador but references indicate that it is not a host (Adamski and Brown, 2001; White, 1999).

Although Mycena citricolor (Berk. & M.A. Curtis) Sacc. has been reported in Ecuador (CABI, 2014), Mariau, 2001) and Wellman, 1977) report it infecting coffee beans, but not avocado fruit. M. citricolor is primarily a leaf spotting disease, and most references refer to it as a pest of coffee (Coffea spp.) (e.g., Mariau, 2001; CABI, 2014; Thurston, 1989; Wellman, 1977). Avocado is not listed as a major or even minor host by CABI (2014). Moreover, it has not been intercepted on avocado or other fruit from any country since at least 1985, the earliest APHIS computerized interception data available (PestID, 2014). Therefore, we did not include this pathogen in the pest list.

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Although CABI (2014) lists avocado as a host for Rhyncophorus palmarum (L.), we could locate no primary evidence to support that claim.

Stenoma catenifer was considered for inclusion on the pest list based on a paper by Landry et al. (2003), which mentioned a single interception of S. catenifer on an avocado reportedly coming from mainland Ecuador. A second reference, Eberling (1959), cites a note in the Proceedings of the Entomological Society of Washington (Busck, 1919). These two pieces of evidence were not considered strong, given that the National Phytosanitary Surveillance system of Ecuador has found no evidence of the pest on the mainland of Ecuador (Granja, 2014).

Rogg (2000) lists several potential pests of avocado in Ecuador, but specifically stated that that book is just a reference of pests that may be associated with each crop, and not an official list to be used to evaluate the presence or absence of a pest (Rogg, 2014). Therefore, we did not list any pests from that text that we could not otherwise corroborate.

2.1.2. Organisms with non-actionable regulatory status We found evidence of the organisms listed in the appendix being associated with avocado and being present in Ecuador; however, because these organisms have non-actionable regulatory status for the continental United States, we did not include them in Table 1 of this risk assessment. They are listed in Appendix A.

2.1.3. Organisms identified only to the genus level In commodity import risk assessments, the taxonomic unit for pests selected for evaluation beyond the pest categorization stage is usually the species (IPPC, 2013), as we focus assessments on organisms for which biological information is available. Therefore, generally, we do not assess risk for organisms identified only to the genus level, in particular if the genus in question is reported in the import area. Many genera contain several or more species, and we cannot know if the unidentified species occurs in the import area and, consequently, whether it has actionable regulatory status for the import area. On the other hand, if the genus in question is absent from the import area, any unidentified organisms in the genus can have actionable status; however, because such an organism has not been fully identified, we cannot properly analyze its likelihood and consequences of introduction.

In light of these issues, we usually do not include organisms identified only to the genus level in the main pest list. Instead, we address them separately in this sub-section. The information here can be used by risk managers to determine if measures beyond those intended to mitigate fully identified pests are warranted. Often, mitigation measures developed for identified pests will be effective against the pests for which we have little information, but only risk managers can make this judgement.

For this risk assessment, we identified the following organisms identified only to the genus level that are reported on avocados in Ecuador: Eotetranychus sp. (Acari: Tetranychidae), Lorrya sp., Tydeus sp. (Acari: Tydeidae), Corthylus sp. (Coleoptera: Scolytidae), Thamnophthorus sp. (Coleoptera: Scolytidae), Tetralicia sp. (Hemiptera: Aleyrodidae), Aphis sp. (Hemiptera: Aphididae), Pseudococcus sp. (Hemiptera: Pseudococcidae), Aetalion sp. (Hemiptera:

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Aetalionidae) (Yust, 1958). Of those genera, we determined that none were likely to be on the harvested commodity in Ecuador.

2.2. Pest list

In Table 1, we list the actionable pests associated with avocados that occur in Ecuador. The list comprises those actionable pests that occur in Ecuador on any host and are associated with avocados whether in Ecuador or elsewhere in the world. For each pest, we indicate 1) the part of the imported plant species with which the pest is generally associated and 2) whether the pest has a reasonable likelihood of being associated, in viable form, with avocado following harvesting from the field and prior to any post-harvest processing. We developed this pest list based on the scientific literature, port-of-entry pest interception data, and information provided by the government of Ecuador. Pests in shaded rows are pests identified for further evaluation, as we consider them reasonably likely to be associated with the harvested commodity; we summarize these pests in a separate table (Table 2).

Table 1. Actionable pests associated with Persea americana (in any country) and present in Ecuador (on any host). Pest name Evidence of Association Plant part(s) On harvested Remarks presence in with avocado association1 plant Ecuador part(s)?2 ACARI Tetranychidae Allonychus littoralis Baker and Baker and Leaf (Posada, No (McGregor) Pritchard, 1962 Pritchard, 1989) 1962 Oligonychus yothersi Yust, 1958 Yust, 1958 Leaf (Yust, No McGregor, 1958) Syn. Paratetranychus yothersi (McGregor) Tetranychus Yust, 1958 Yust, 1958 Leaf (Yust, No braziliensis 1958) (McGregor), Syn. Allonychus braziliensis (McGregor)

1 The plant part(s) listed are those for the plant species under analysis. If the information has been extrapolated, such as from plant part association on other plant species, we note that. 2 “Yes” indicates simply that the pest has a reasonable likelihood of being associated with the harvested commodity; the level of pest prevalence on the harvested commodity (low, medium, or high) is qualitatively assessed in Risk Element A1 as part of the Likelihood of Introduction assessment (section 3).

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Pest name Evidence of Association Plant part(s) On harvested Remarks presence in with avocado association1 plant Ecuador part(s)?2 DIPTERA Tephritidae Anastrepha Tigrero S., 2009 Some Fruit (Putruele, Yes Some varieties of fraterculus cultivars 1996) avocado, such as Hass (Wiedemann) (Putruele, are not hosts for A. 1996) fraterculus (Liquido et al., 2010). Although Tigrero (2009) did not list avocado as a host of A. fraterculus in Ecuador, some varieties were found to be hosts in Argentina (Putruele, 1996). Anastrepha Tigrero S., 2009 Bush, 1957 Fruit (Bush, Yes Avocado was not serpentina 1957) present in the annotated (Wiedemann) list of fruit fly hosts of Ecuador, but Bush (1957) found A. serpentina in Mexican avocados. One variety of avocado, Hass, is not a host for A. serpentina (Aluja et al., 2004). Anastrepha striata Tigrero S., 2009 Jirón et al., Fruit (Jirón et Yes Avocado was not Schiner 1988 al., 1988) present in the annotated list of fruit fly hosts of Ecuador, but Jirón et al., (1988) found A. striata in Costa Rican avocados. One avocado variety, Hass, is not a host for A. striata (Aluja et al., 2004). Ceratitis capitata Tigrero S., 2009 Putruele, Fruit (Putruele, Yes One avocado variety, (Wiedemann) 1996 1996) Hass, is not a host for C. capitata (Liquido et al., 2010). Although Tigrero (2009) did not list avocado as a host of Ceratitis capitata in Ecuador, some varieties were found to be hosts in Argentina (Putruele, 1996).

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Pest name Evidence of Association Plant part(s) On harvested Remarks presence in with avocado association1 plant Ecuador part(s)?2 Aleyrodidae Aleurocanthus Russell, 1962 Ebeling, 1959 Leaf (Ebeling, No woglumi Ashby 1959) Aleurodicus dispersus Russell, 1965 Kiyindou et Leaf No Russell al., 2002 (Kiyindou et al., 2002) Aleurodicus Martin and Evans, 2008 Leaf (Stocks No pulvinatus Watson, 1998 and Hodges, (Maskell) 2012) Empoasca sterensi Yust, 1958 Yust, 1958 Leaf (Yust, No (Young) 1958) Membracidae Metcalfiella Yust, 1958 Yust, 1958 Twig (Yust, No pubescens 1958) (Buckton), Syn. Hoplophora pubescens Buckton Pseudococcidae Pseudoparlatoria Yust, 1958 Yust, 1958 Leaf (Yust, No cristata (Lindiger) 1958) LEPIDOPTERA Pyralidae Stericta albifasciata Ebeling, 1959 Ebeling, 1959 Flower, leaf No Druce (Ebeling, 1959) FUNGI Rosellinia bunodes CABI, 2014 Ploetz et al., Root (Ploetz et No (Berk. & Br.) Sacc. 1994; Teliz, al., 1994; Black 2000; Wellman, Wellman, 1977) 1977 Rosellinia necatrix CABI, 2014 Ploetz et al., Root (Ploetz et No Prill. 1994; Teliz, al., 1994; Anamorph: 2000; Wellman, Dematophora Wellman, 1977) necatrix R. Hartig 1977 NEMATODES Radopholus similis CABI, 2014 CABI, 2014 Root (CABI, No Restricted distribution (Cobb) Thorne 2014) in the United States (CA, FL, TX) (CABI, 2014).

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2.3. Pests selected for further analysis

We identified four pests for further analysis (Table 2). All of these organisms are actionable pests for the continental United States and have a reasonable likelihood of being associated with avocado plant part(s) at the time of harvest and remaining with avocado, in viable form, throughout the harvesting process.

Table 2. Pests selected for further analysis. Pest type Taxonomy Scientific name Arthropod Diptera: Tephritidae Anastrepha fraterculus Anastrepha serpentina Anastrepha striata Ceratitis capitata

3. Assessing Pest Risk Potential

3.1. Introduction

For each pest selected for further analysis, we estimate its overall pest risk potential. Risk is described by the likelihood of an adverse event, the magnitude of the consequences, and uncertainty. In this risk assessment, we first determine for each pest if there is an endangered area within the continental United States. The endangered area is defined as the portion of the import area where ecological factors favor the establishment of the pest and where the presence of the pest will result in economically important losses. Once an endangered area has been determined, the overall risk of each pest is then determined with two separate components: 1) the likelihood of its introduction into the endangered area on the imported commodity (i.e., the likelihood of an adverse event) and 2) the consequences of its introduction (i.e., the magnitude of the consequences). In general, we assess both of these components for each pest. If we determine that the risk of either component is negligible, however, assessing the other is not necessary, because the overall pest risk potential will be negligible regardless of the result of the second component. For example, if we determine that pest introduction is highly unlikely, we do not assess the consequences of it being introduced.

The likelihood and consequences of introduction are assessed using different approaches. For the consequences of introduction, we determine if the pest meets the threshold (Yes/No) of being likely to cause unacceptable losses. We base that determination on the physical damage the pest is likely to cause and/or the proportion of exports likely to be disrupted, rather than on an absolute value or amount of monetary loss.

The likelihood of introduction is based on the likelihoods of entry and establishment. We qualitatively assess risk using the ratings Negligible, Low, Medium, and High. The risk factors comprising the model for likelihood of introduction are interdependent and, therefore, the model is multiplicative rather than additive. Thus, if any one risk element is rated as Negligible, then

Final July 18, 2017 8 Pest Risk Assessment for avocado from Ecuador the overall likelihood will be Negligible. For the overall likelihood of introduction risk rating, we define the different categories as follows: High: Pest introduction is highly likely to occur. Medium: Pest introduction is possible, but for that to happen, the exact combination of required events needs to occur. Low: Pest introduction is unlikely to occur because one or more of the required events are unlikely to happen, or the full combination of required events is unlikely to align properly in time and space. Negligible: Pest introduction is highly unlikely to occur given the exact combination of events required for successful introduction.

3.2. Assessment results

3.2.1. Anastrepha fraterculus We determined the overall likelihood of introduction to be Medium and that the establishment of A. fraterculus in the continental United States is likely to cause unacceptable impacts. We present the results of this assessment in the table below.

Determination of the portion of the continental United States endangered by Anastrepha fraterculus Climatic suitability Anastrepha fraterculus occurs in South Texas, Belize, Colombia, Costa Rica, Ecuador, Panama, Paraguay, Peru, Trinidad and Tobago, Uruguay, Venezuela (Stone, 1942, Argentina (Oroño et al., 2005 Schliserman et al., 2010), Brazil (Sugayama et al., 1998), and Mexico (Baker, 1945). In terms of USDA Plant Hardiness Zones (Magarey et al., 2008), this distribution covers a temperature range corresponding to. Zones 8-11. Potential hosts at Anastrepha fraterculus feeds on multiple genera in multiple plant risk in PRA Area families, including Actinidiaceae (Actinidia), Anacardiaceae (Mangifera, Spondias), Annonaceae (Annona), Combretaceae (Terminalia), Ebenaceae (Diospyros), Juglandaceae (Juglans), Lauraceae (Persea), Moraceae (Ficus), Myrtaceae (Eugenia, Psidium, Syzygium), Oleaceae (Olea), Punicaceae (Punica), Rosaceae (Cydonia, Eriobotrya, Fragaria, Malus, Prunus, Pyrus, Rubus), Rutaceae (Citrus, Fortunella), Sapotaceae (Manilkara, Pouteria), Solanaceae (Solanum), and Vitaceae (Vitis) (CABI, 2014; White and Elson-Harris, 1992). Economically The A. fraterculus species complex may infest such important crops as important hosts at apple (Sugayama et al., 1998), peaches, plums, and grapefruits risk (Ovruski et al., 2003). Pest potential on The A. fraterculus species complex damages economically important economically plants (Weems, 2002). In Brazil it causes severe yield losses in apple due important hosts at to fruit malformation and fruit drop and significantly restricts fresh fruit riska exports to countries with quarantine barriers (Sugayama et al., 1996). Defined The area endangered by A. fraterculus comprises apple, peach, plum, Endangered Area and grapefruit crops in Plant Hardiness Zones 8-11. a As defined by ISPM No. 11, supplement 2, “economically” important hosts refers to both commercial and non- market (environmental) plants (IPPC, 2012).

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Assessment of the likelihood of introduction of Anastrepha fraterculus into the continental United States area via the importation of avocados from Ecuador Risk Element Risk Uncertainty Justification for rating and Rating Ratinga explanation of uncertainty (and other notes as necessary) Likelihood of Entry Risk Element A1: Pest Low MC Avocado was shown not to be a natural prevalence on the harvested host for A. fraterculus in Mexico commodity (= the baseline (Aluja et al., 1987) or in Ecuador rating for entry) (Tigrero S., 2009), and the results were the same in Argentina (Ovruski et al., 2003). Bush (1957) indicated that avocados are probably not a preferred host, but when high populations occur close to groves, fruit could be infested if primary hosts are not available. Risk Element A2: Likelihood Low MC During the first few weeks of avocado of surviving post-harvest damage by fruit flies, oviposition holes processing before shipment are small and inconspicuous, but later develop into a crack or a starshaped lesion (Du Toit et al., 1979). Only newly infested fruit would be hard to discover. Overall, we did not reduce the previsou risk rating. Risk Element A3: Likelihood Low MC Live Anastrepha species have been of surviving transport and intercepted at least 14 times at U.S. storage conditions of the ports-of-entry from a number of consignment countries (PestID, 2014), indicating that the genus is little affected by normal shipping conditions. The risk rating is not increased. Risk Element A: Overall risk Low N/A rating for likelihood of entry Likelihood of Establishment Risk Element B1: Likelihood High C Anastrepha fraterculus feeds on of coming into contact with multiple genera in multiple plant host material in the families (CABI, 2014; White and endangered area Elson-Harris, 1992). Suitable hosts are widely and regularly distributed throughout the entire endangered area. Risk Element B2: Likelihood High C More than 25 percent of the U.S. of arriving in the endangered population lives in the endangered area area.

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Risk Element Risk Uncertainty Justification for rating and Rating Ratinga explanation of uncertainty (and other notes as necessary) Risk Element B: Combined High N/A likelihood of establishment Overall Likelihood of Introduction Combined likelihoods of Medium N/A entry and establishment aC=Certain, MC=Moderately Certain, MU=Moderately Uncertain, U=Uncertain

Assessment of the consequences of introduction of Anastrepha fraterculus into the continental United States (i.e., the PRA area) Criteria Meets Uncertainty Justification for rating and criteria? Ratinga explanation of uncertainty (and (Yes/No) other notes as necessary) Direct Impacts Risk Element C1: Damage Yes MC Although widely reported as an potential in the endangered important pest of many hosts, high area levels of injury are not reported in the literature. Sugayama et al., (1996), for example, report A. fraterculus as a major pest of apple in Brazil, causing losses of up to 2 percent in untreated apple orchards. Lack of reported damage is likely the result of successful control programs. Damage potential in the United States is likely low, but would probably cause increased production costs, as demonstrated in Argentina (Guillen and Sanchez, 2007). Risk Element C2: Spread Yes C In mark-release-recapture experiments potential in Brazil, adults of A. fraterculus were captured up to 800 meters from their release point (Kovaleski et al., 1999). Anastrepha fraterculus also moves in trade via infested fruit (PestID, 2014). In addition, A. fraterculus can be transported as pupae in soil or in packaging or growing media accompanying plants (CABI, 2014). Risk Element C: Pest No N/A introduction is likely to cause unacceptable direct impacts Trade Impacts

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Criteria Meets Uncertainty Justification for rating and criteria? Ratinga explanation of uncertainty (and (Yes/No) other notes as necessary) Risk Element D1: Export Yes C Hosts of A. fraterculus include apples markets at risk (Sugayama et al., 1998), avocados, peaches, and citrus (Putruele, 1996), all of which are important U.S. crops for export. Risk Element D2: Likelihood Yes C Anastrepha fraterculus or Anastrepha of trading partners imposing sp. have been identified for trade additional phytosanitary restriction by Japan, the European requirements Union, and China (PExD, 2014) Risk Element D: Pest is likely Yes to cause significant trade impacts [Procedure 8-4] Conclusion Is the pest likely to cause Yes N/A unacceptable consequences in the PRA area? aC=Certain, MC=Moderately Certain, MU=Moderately Uncertain, U=Uncertain

3.2.2. Anastrepha serpentina We determined the overall likelihood of introduction of A. serpentina to be Medium, and that the establishment of A. serpentina in the continental United States is likely to cause unacceptable impacts. We present the results of this assessment in the table below.

Determination of the portion of the continental United States endangered by Anastrepha serpentina Climatic suitability Anastrepha serpentina has been reported from North America (the Rio Grande Valley of Texas in the United States, Mexico), Central America (Costa Rica, Guatemala, Panama), and South America (Argentina, Brazil, Colombia, Ecuador, Guyana, Peru, Suriname, Trinidad, and Venezuela) (CABI, 2014; Weems, 2001). USDA-APHIS maintains its status as a regulated pest and Texas has active programs for its control (APHIS, 2007). With regard to Plant Hardiness Zones (Magarey et al., 2008) we estimate that A. serpentina could establish in areas of the continental United States corresponding to.Zones 9-11. Potential hosts at Anastrepha serpentina has been reported from Annona glabra risk in PRA Area (Annonaceae), Citrus spp., C. sinensis (Rutaceae), Ficus sp. (Moraceae), Mangifera indica (Anacardiaceae), Manilkara zapota (Sapotaceae), Persea americana (Lauraceae), Cydonia oblonga, Malus domestica, Pouteria spp., Prunus spp. (Rosaceae), Pyrus communis, and Psidium guajava (Myrtaceae) (Weems, 2001).

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Economically Anastrepha serpentina is an important pest in the American tropics and important hosts at subtropics, especially of sapotaceous fruits (Shaw, 1947. It has also risk been reported to infest citrus (Weems, 2001), and the apparently secondary hosts (Shaw, 1947) of mango, apple, peach, and quince (Norrbom, 2003). Pest potential on The establishment of A. serpentina is likely to affect market access to economically the countries where this pest is of quarantine importance. The important hosts at establishment of A. serpentina in Florida could seriously affect tropical riska fruit production there (Weems, 2001). Defined The area endangered by Anastrepha serpentina comprises citrus, Endangered Area mango, apple, peach, and quince crops in Plant Hardiness Zones 9-11. a As defined by ISPM No. 11, supplement 2, “economically” important hosts refers to both commercial and non- market (environmental) plants (IPPC, 2012).

Assessment of the likelihood of introduction of Anastrepha serpentina into the endangered area via the importation of avocado fruit from Ecuador Risk Element Risk Rating Uncertainty Justification for rating and Ratinga explanation of uncertainty (and other notes as necessary) Likelihood of Entry Risk Element A1: Pest Low MU Avocado is not a natural host for A. prevalence on the harvested serpentina under field conditions commodity (= the baseline in Mexico (Aluja et al., 1987), and rating for entry) the ‘Hass’ variety, in particular, is not a host to Anastrepha species (Aluja et al., 2004). Risk Element A2: Likelihood Low C Fruit infested with fruit flies are of surviving post-harvest likely to escape detection during processing before shipment culling because they are internal feeders (White and Elson-Harris, 1992). We did not change the previous risk rating. Risk Element A3: Likelihood Low C U.S. ports-of-entry have of surviving transport and intercepted live Anastrepha species storage conditions of the at least 14 times on avocado consignment (PestID, 2014), indicating that the genus can survive standard shipping conditions. We did not change the previous risk rating. Risk Element A: Overall risk Low N/A rating for likelihood of entry Likelihood of Establishment Risk Element B1: Likelihood High MC Anastrepha serpentina has an of coming into contact with expansive host range (see above). Suitable hosts are widely and

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Risk Element Risk Rating Uncertainty Justification for rating and Ratinga explanation of uncertainty (and other notes as necessary) host material in the regularly distributed throughout the endangered area entire endangered area. Risk Element B2: Likelihood High MC More than 25 percent of the U.S. of arriving in the endangered population lives in the endangered area area. Risk Element B: Combined High N/A likelihood of establishment Overall Likelihood of Introduction Combined likelihoods of Medium N/A entry and establishment aC=Certain, MC=Moderately Certain, MU=Moderately Uncertain, U=Uncertain

Assessment of the consequences of introduction of Anastrepha serpentina into the continental United States (i.e., the PRA area) Criteria Meets Uncertainty Justification for rating and criteria? Ratinga explanation of uncertainty (and (Yes/No) other notes as necessary) Direct Impacts Risk Element C1: Damage No MU Anastrepha serpentina is an important potential in the endangered pest of sapote (Calocarpum spp.), area sapodilla (Manilkara zapota), Lucuma salicifolia, and other fruits in Mexico (Weems, 2001). Infestations have caused 80 percent losses in mamey sapote in Mexico (Ariza-Flores et al., 2009). None of those fruits, however, are economic crops in the United States. Mangan et al. (2011) indicated that A serpentina would be unlikely to persist in Texas citrus. Specific levels of damage to other host plants are not readily available in the literature. Risk Element C2: Spread N/A N/A potential Risk Element C: Pest No N/A introduction is likely to cause unacceptable direct impacts

Final July 18, 2017 14 Pest Risk Assessment for avocado from Ecuador

Criteria Meets Uncertainty Justification for rating and criteria? Ratinga explanation of uncertainty (and (Yes/No) other notes as necessary) Trade Impacts Risk Element D1: Export Yes Although citrus is a poor host for A. markets at risk serpentine, other countries may still regard the presence of the fruit fly as a problem for US citrus. More than 10 percent of the total value of citrus exports are sent to China and Japan (Global Trade Information Services, 2012) which are currently free of A. serpentina (Weems, 2001). Risk Element D2: Likelihood Yes Both China and Japan list Anastrepha of trading partners imposing spp. as harmful organisms (PExD, additional phytosanitary 2014), indicating that both countries requirements would likely impose additional phytosanitary requirements on U.S. citrus exports if A. serpentina became established in the United States. Risk Element D: Pest is likely Yes N/A to cause significant trade impacts Conclusion Is the pest likely to cause Yes N/A unacceptable consequences in the PRA area? aC=Certain, MC=Moderately Certain, MU=Moderately Uncertain, U=Uncertain

3.2.3. Anastrepha striata We determined the overall likelihood of introduction to be Medium, and that the establishment of Anastrepha striata in the continental United States is likely to cause unacceptable impacts. We present the results of this assessment in the table below.

Determination of the portion of the continental United States endangered by Anastrepha striata Climatic suitability Anastrepha striata is present in southern Mexico, in most of Central America, and through South America to Peru, Bolivia, and Brazil (CABI, 2014; Hernández-Ortiz, 1992; Weems and Fasulo, 2012). A comparison with the USDA Plant Hardiness Zones (Magarey et al., 2008) indicates that establishment may occur in Zones 9-13.

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Potential hosts at The primary host of A. striata is guava (Psidium guajava) (Hernández- risk in PRA Area Ortiz, 1992), though it may also infest fruits of lime (Citrus aurantifolia) and orange (C. sinensis) (Condor, 1973), Spondias purpurea, and other Psidium species (Zucchi and Moraes, 2008). All of those are found in Plant Hardiness Zones 9-13 (NRCS, 2013). Economically Guava and citrus are considered to be economically important hosts in important hosts at the United States (Mossler and Crane, 2012; NASS, 2011). riska Pest potential on Anastrepha striata is an important agricultural pest in guava, limes, and economically oranges (Aluja et al., 1987; Condor, 1973; Weems and Fasulo, 2012). important hosts at In general, A. striata does not appear to have primary economic risk importance (Weems and Fasulo, 2012), though significant damage may occur in dooryard plantings or other plants in the environment. Defined The endangered area encompasses areas where guava and citrus are Endangered Area grown in Plant Hardiness Zones 9-11. a As defined by ISPM No. 11, supplement 2, “economically” important hosts refers to both commercial and non- market (environmental) plants (IPPC, 2012).

Assessment of the likelihood of introduction of Anastrepha striata into the endangered area via the importation of avocado fruit from Ecuador Risk Element Risk Rating Uncertainty Justification for rating and Ratinga explanation of uncertainty (and other notes as necessary) Likelihood of Entry Risk Element A1: Pest Low MC Avocado is not a natural host for A. prevalence on the harvested striata under field conditions in commodity (= the baseline Mexico (Aluja et al., 1987). rating for entry) Risk Element A2: Likelihood Low MC Fruit infested with fruit flies are of surviving post-harvest highly likely to escape detection processing before shipment during culling because they are internal feeders (White and Elson- Harris, 1992). We did not change the previous risk rating. Risk Element A3: Likelihood Low MU We found no evidence that of surviving transport and transport or storage conditions storage conditions of the reduced the prevalence of A. striata consignment on the fruit (see section 1.4). Typical shipping conditions for avocado (McGregor, 1987) seem unlikely to affect the pest population. We did not change the previous risk rating. Risk Element A: Overall risk Low N/A rating for likelihood of entry

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Risk Element Risk Rating Uncertainty Justification for rating and Ratinga explanation of uncertainty (and other notes as necessary) Likelihood of Establishment Risk Element B1: Likelihood High MC Anastrepha striata feeds on of coming into contact with multiple genera in multiple plant host material in the families (CABI, 2014; Weems and endangered area Fasulo, 2012). Suitable hosts are widely and regularly distributed throughout the entire endangered area. Risk Element B2: Likelihood High C More than 25 percent of the U.S. of arriving in the endangered population lives in the endangered area area. Risk Element B: Combined High N/A likelihood of establishment Overall Likelihood of Introduction Combined likelihoods of Medium N/A entry and establishment aC=Certain, MC=Moderately Certain, MU=Moderately Uncertain, U=Uncertain

Assessment of the consequences of introduction of Anastrepha striata into the continental United States (i.e., the PRA area) Criteria Meets Uncertainty Justification for rating and criteria? Ratinga explanation of uncertainty (and (Yes/No) other notes as necessary) Direct Impacts Risk Element C1: Damage Yes MU General control practices for guava potential in the endangered production in Florida do not area indicate specific fruit fly control measures (Mossler and Crane, 2012). While we found no specific information about yield losses attributable to infestations of A. striata, the fly is considered to be a pest in South America (Aguiar- Menezes et al., 2002). For those reasons, we estimate that there is potential for significant damage to occur in the endangered area, but with moderate levels of uncertainty. Risk Element C2: Spread Yes MU We found no evidence of any potential biological factors that might reduce

Final July 18, 2017 17 Pest Risk Assessment for avocado from Ecuador

Criteria Meets Uncertainty Justification for rating and criteria? Ratinga explanation of uncertainty (and (Yes/No) other notes as necessary) the spread potential of A. striata in the United States. As with other Anastrepha species, the primary modes of spread is likely through flight and the movement of infested fruit (Botha et al., 2004). Risk Element C: Pest Yes N/A introduction is likely to cause unacceptable direct impacts Trade Impacts Risk Element D1: Export N/A N/A markets at risk Risk Element D2: Likelihood N/A N/A of trading partners imposing additional phytosanitary requirements Risk Element D: Pest is likely N/A N/A to cause significant trade impacts Conclusion Is the pest likely to cause Yes N/A unacceptable consequences in the PRA area? aC=Certain, MC=Moderately Certain, MU=Moderately Uncertain, U=Uncertain

3.2.4. Ceratitis capitata We determined the overall likelihood of introduction of C. capitata (Medfly) to be High. We present the results of this assessment in the table below.

We determined that the establishment of Medfly in the continental United States is likely to cause unacceptable impacts. We present the results of this assessment in the table below.

Determination of the portion of the continental United States endangered by Ceratitis capitata Climatic suitability Medfly is widely distributed in the Mediterranean region, South and Central America, west Asia, and Australia (CABI, 2014). Based on its current distribution, we estimate that Medfly could establish in areas of the continental United States corresponding to Plant Hardiness Zones 8-11 (Magarey et al., 2008). Potential hosts at Medfly feeds on over 400 hosts (CABI, 2014), many of which are risk in PRA Area common within Plant Hardiness Zones 8-11 in the United States.

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Economically Economically important hosts widely present in the area of concern important hosts at include Capsicum annuum, Citrus spp., Ficus carica, Morus nigra, risk Prunus domestica, and P. persica (CABI, 2014; Mason, 1931). Pest potential on Medfly is a serious pest on Citrus spp., Ficus carica, Mangifera indica, economically and Prunus persica; damage to fruit crops may reach 100 percent important hosts at (CABI, 2014). Medfly therefore could impact several of the riska economically important hosts listed above. Defined The area endangered by Medfly comprises citrus, fig, mango, plums, Endangered Area peach, and other fruit crops in Plant Hardiness Zones 8-11. a As defined by ISPM No. 11, supplement 2, “economically” important hosts refers to both commercial and non- market (environmental) plants (IPPC, 2012).

Assessment of the likelihood of introduction of Ceratitis capitata into the endangered area via the importation of avocado fruit from Ecuador Risk Element Risk Uncertainty Justification for rating and Rating Ratinga explanation of uncertainty (and other notes as necessary) Likelihood of Entry Risk Element A1: Pest Low MC Ovruski et al. (2003) found no prevalence on the harvested infestation of avocado by C. capitata commodity (= the baseline in an extensive host survey. Avocado rating for entry) was shown to be a host of C. capitata in no-choice laboratory experiments by Oi and Ronald (1989) and Willard et al. (1930). Because avocado seems to be a secondary host, we rated it Low here. Risk Element A2: Likelihood Low C Internally feeding arthropods are of surviving post-harvest highly likely to survive minimal processing before shipment post-harvest treatment, such as washing and culling. Infested fruit are also highly likely to escape detection during culling (White and Elson-Harris, 1992). Risk Element A3: Likelihood Low MU U.S. ports-of-entry have intercepted of surviving transport and live C. capitata larvae in fruit over storage conditions of the 3,000 times from a number of consignment counties, with over 300 of these interceptions occurring in citrus fruit (PestID, 2014), indicating that C. capitata is little affected by standard shipping conditions. Based on this information, we did not change the previous risk rating.

Final July 18, 2017 19 Pest Risk Assessment for avocado from Ecuador

Risk Element Risk Uncertainty Justification for rating and Rating Ratinga explanation of uncertainty (and other notes as necessary) Risk Element A: Overall risk Low N/A rating for likelihood of entry Likelihood of Establishment Risk Element B1: Likelihood High C Ceratitis capitata has an expansive of coming into contact with host range (CABI, 2014). Suitable host material in the hosts are widely and regularly endangered area distributed throughout the entire endangered area. Risk Element B2: Likelihood High C More than 25 percent of the U.S. of arriving in the endangered population lives within the area endangered area. Risk Element B: Combined High N/A likelihood of establishment Overall Likelihood of Introduction Combined likelihoods of Medium N/A entry and establishment aC=Certain, MC=Moderately Certain, MU=Moderately Uncertain, U=Uncertain

Assessment of the consequences of introduction of Ceratitis capitata into the continental United States (i.e., the PRA area) Criteria Meets Uncertainty Justification for rating and criteria? Ratinga explanation of uncertainty (and (Yes/No) other notes as necessary) Direct Impacts Risk Element C1: Damage Yes C Ceratitis capitata is a serious pest on potential in the endangered numerous hosts including Citrus spp., area Ficus carica, and Prunus persica; damage to fruit crops may reach 100 percent (CABI, 2014). The introduction of the pest in the endangered area would likely guarantee implementation of eradication programs. Risk Element C2: Spread Yes C Ceratitis capitata has spread from potential likely origins in Africa to the Mediterranean and South America (Davies et al., 1999), and has repeatedly invaded the United States (Davies et al., 1999; Headrick and Goeden, 1996).

Final July 18, 2017 20 Pest Risk Assessment for avocado from Ecuador

Criteria Meets Uncertainty Justification for rating and criteria? Ratinga explanation of uncertainty (and (Yes/No) other notes as necessary) Risk Element C: Pest Yes introduction is likely to cause unacceptable direct impacts Trade Impacts Risk Element D1: Export N/A markets at risk Risk Element D2: Likelihood N/A of trading partners imposing additional phytosanitary requirements Risk Element D: Pest is likely N/A to cause significant trade impacts Conclusion Is the pest likely to cause Yes N/A unacceptable consequences in the PRA area? aC=Certain, MC=Moderately Certain, MU=Moderately Uncertain, U=Uncertain

4. Summary and Conclusions of Risk Assessment

Of the organisms associated with avocado worldwide and present in continental Ecuador, we identified organisms that are actionable pests for the continental United States and have a reasonable likelihood of being associated with avocado following harvesting from the field and prior to any post-harvest processing. If warranted, we further evaluated these organisms for their likelihood of introduction (i.e., entry plus establishment) and their potential consequences of introduction. Pests that are likely to cause unacceptable consequences of introduction with an overall likelihood of introduction risk rating above Negligible are candidates for risk management. These results represent a baseline estimate of the risks associated with the import commodity pathway as described in section 1.4. Fruit are to be harvested by hand and washed before packing. At the port of entry into the United States fruit will be inspected for pests and diseases.

All the pests selected for further analysis are candidates for risk management, because they are likely to cause unacceptable consequences of introduction, and they received a likelihood of introduction risk rating above Negligible. We summarize the results for each pest below (Table 3).

Detailed examination and choice of appropriate phytosanitary measures to mitigate pest risk are part of the pest risk management phase within APHIS and are not addressed in this document.

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Table 3. Summary for pests selected for further evaluation and determined to be candidates for risk management. All of these pests meet the threshold for unacceptable consequences of introduction. Pest Likelihood of Introduction Uncertainty statement overall rating (optional)a Anastrepha fraterculus Medium Anastrepha serpentina Medium Anastrepha striata Medium Ceratitis capitata Medium aThe uncertainty statement, if included, identifies the most important source(s) of uncertainty.

5. Acknowledgements

Authors Shawn Robertson, Entomologista Walter Gutiérrez, Plant Pathologista

Reviewers Christina Devorshak, Entomologista Kayimbi Tubajika, Plant Pathologista a Plant Epidemiology and Risk Analysis Laboratory, USDA-APHIS-PPQ

6. Literature Cited

7 CFR § 319.56. 2013. 7 CFR § 319. 2011. U.S. Code of Federal Regulations, Title 7, Part 319 (7 CFR § 319 – Foreign Quarantine Notices). 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. Aguiar-Menezes, E. L., E. B. Menezes, P. C. R. Cassino, and M. A. Soares. 2002. Passion Fruit. Pages 361-390 in J. E. Pena, J. L. Sharp, and M. Wysoki, (eds.). Tropical Fruit Pests and Pollinators: Biology, Economic Importance, Natural Enemies and Control. CABI Publishing, Wallingford, U.K. Aluja, M., F. Díaz-Fleischer, and J. Arredondo. 2004. Nonhost status of commercial Persea americana 'Hass' to Anastrepha ludens, Anastrepha obliqua, Anastrepha serpentina, and Anastrepha striata (Diptera: Tephritidae) in Mexico. Journal of Economic Entomology 97(2):293-309. Aluja, M., J. Guillen, M. Cabrera, H. Celedonio, P. Liedo, J. Hendrichs, and G. de la Rosa. 1987. Natural host plant survey of the economically important fruit flies (Diptera: Tephritidae) of Chiapas, Mexico. Florida Entomologist 70(3):329-330. APHIS. 2007. Fruit fly control programs. United States Department of Agriculture, Animal and Plant Health Inspection Service. http://www.aphis.usda.gov/plant_health/ea/fruitfly.shtml. (Archived at PERAL). Ariza-Flores, R., E. M. Yahia Kazuz, E. Vázquez-García, A. Barrios-Ayala, E. R. Garrido- Ramírez, A. C. Michel-Aceves, M. A. Otero-Sánchez, and I. Alia-Tejacal. 2009. Control

Final July 18, 2017 22 Pest Risk Assessment for avocado from Ecuador

de Anastrepha serpentina (Wiedemann) y Calidad de los Frutos de Zapote Mamey Pouteria sapota (Jacq) Moore & Stearn Tratados con Aire Caliente Forzado. Revista Chapingo. Serie horticultura 15(1):9-15. Baker, E. W. 1945. Studies on the Mexican fruitfly known as Anastrepha fraterculus. J. Econ. Entomol. 38(1):95-100. Baker, E. W., and A. E. Pritchard. 1962. Central American spider mites (Acarina: Tetranychidae) [Aranas Rojas de America Central (Acarina: Tetranychidae)]. Revista de la Sociedad Mexicana de Historia Natural XXIII:309-347. Ben-Dov, Y. 1993. A systematic catalogue of the soft scales insects of the world. Sandhill Crane Press, Inc., Gainesville, Florida. 536 pp. Botha, J., D. Hardie, and A. Reeves. 2004. Exotic threat to Western Australia - South American fruit flies not present in Western Australia: Anastrepha fraterculus and related species (No. 9/2004). in Factsheet. Government of Western Australia, Department of Agriculture. Busck, A. 1919. A microlepidopteron injurious to avocado. Proceedings of the Entomological Society of Washington 21:122-126. Bush, G. L. 1957. Some Notes on the Susceptibility of Avocados in Mexico to Attack by the Mexican Fruit Fly. Proceedings of the Rio Grande Valley Horticultural Society 11:75-78. CABI. 2014. Crop Protection Compendium, Commonwealth Agricultural Bureau International (CABI). Wallingford, UK. Last accessed February 11, 2014, http://www.cabi.org/cpc/. Chupp, C. 1953. Monograph of the fungus genus Cercospora. Published by the Author, Ithaca, New York, 667 pages. Condor, J. A. 1973. Cultivos Fruticolas. Pages 43-47, 50, 56 Manual: No. 38. Lista de insectos y otros animales daninos a la agricultura en el Peru. Ministerio de Agricultura, Direccion General de Investigacion Agraria, La Molina, Peru. Crous, P. W., and U. Braun. 2003. Mycosphaerella and its anamorphs: 1. Names published in Cercospora and Passalora. Centraalbureau voor Schimmelcultures, Utrecht, The Netherlands. 571 pp. Davies, N., F. X. Villablanca, and G. K. Roderick. 1999. Bioinvasions of the medfly Ceratitis capitata: source estimation using DNA sequences at multiple intron loci. Genetics 153(1):351-360. Du Toit, W., E. De Villiers, and A. Tuffin. 1979. The identification of causes of typical surface lesions on avocado fruit. South African Avocado Growers’ Association Research Report 3:52-53. Ebeling, W. 1959. Subtropical Fruit Pests. University of California. 1-436 pp. Evans, G. A. 2008. Whiteflies (Hemiptera: Aleyrodidae) of the World and Their Host Plants and Natural Enemies. USDA/Animal Plant Health Inspection Service (APHIS). Last accessed May 11, 2011, http://www.sel.barc.usda.gov:8080/1WF/World-Whitefly-Catalog.pdf Global Trade Information Services. 2012. Global Trade Atlas. Columbia, SC. Last accessed February 2013, http://www.gtis.com/gta Granja, W. P. A. 2013. Interest in exporting fresh avocado fruit (Persea americana) produced in Ecuador. Personal communication to J. Greifer on July 17, 2013, from Ing. Wilson Patricio Almeida Granja, Director Sanidad Vegital - Agrocalidad. Granja, W. P. A. 2014. Comments on the avocado pest risk assessment developed by the United States. Personal communication to A. K. Dowdy on December 31, 2014, from Guillen, D., and R. Sanchez. 2007. Expansion of the national fruit fly control programme in Argentina. Pages 653-660 in A. S. R. M. J. B. Vreysen, and J. Hendrichs, (ed.). Area

Final July 18, 2017 23 Pest Risk Assessment for avocado from Ecuador

wide control of insect pests: from research to field implementation. Springer, Dordrecht, Netherlands. Headrick, D. H., and R. D. Goeden. 1996. Issues Concerning the Eradication or Establishment and Biological Control of the Mediterranean Fruit Fly,< i> Ceratitis capitata(Wiedemann)(Diptera: Tephritidae), in California. Biological Control 6(3):412-421. Henry, T. J., and R. C. Froeschner. 1988. Catalog of the Heteroptera, or true bugs, of Canada and the continental United States. E.J. Brill, Leiden; Netherlands. xix + 958 pp. Hernández-Ortiz, V. 1992. El género Anastrepha en México. Taxonomia, distribución y sus plantas huéspedes. Instituto de Ecologfa, Xalapa, Mexico. Hernández, H. G., R. J. Naime, L. G. Corona, A. E. Martínez, A. S. Castro, E. E. Venegas, F. Durán de Anda, and A. R. Valle de la Paz. 2000. Plagas del aguacate. Pages 115-136 in D. Téliz, (ed.). El aguacate y su manejo integrado. Ediciones Munid-Prensa, Mexico City. IIE. 1995. Ceroplastes sinensis Del Guercio, Homoptera: Coccoidea, Coccidae, Chines wax scale, Series A: Map no. 412. International Institute of Entomology, London. IPPC. 2012. International Standards for Phytosanitary Measures, Publication No. 5 - Glossary of Phytosanitary Terms. Secretariat of the International Plant Protection Convention (IPPC), Food and Agriculture Organization of the United Nations, Rome, Italy. IPPC. 2013. International Standards for Phytosanitary Measures, Publication No. 11 - Pest risk analysis for quarantine pests including analysis of environmental risks and living modified organisms. Secretariat of the International Plant Protection Convention (IPPC), Food and Agriculture Organization of the United Nations, Rome, Italy. Jeppson, L. R., H. H. Keifer, and E. Baker, W. 1975. Mites Injurious to Economic Plants. University of California Press, Berkeley, Los Angeles, London. 614 pp. Jirón, L. F., J. Soto-Manitiu, and A. Norrbom. 1988. A preliminary list of the fruit flies of the genus Anastrepha (Diptera: Tephritidae) in Costa Rica. Florida Entomologist:130-137. Kiyindou, A., I. Adoumbaye, D. Mizere, and J. Moussa. 2002. Contribution to the Knowledge of the Ecology and Biology of Homopterous Pests of Fruit Trees and other Plants I.- Comparaison of Evolution of Population of Aleurodicus dispersus Russell (Hom.: Aleyrodidae) on Citrus and Avocado Trees in the Republic of the Congo. Tropicultura 20(3):135-139. Kovaleski, A., R. L. Sugayama, and A. Malavasi. 1999. Movement of Anastrepha fraterculus from native breeding sites into apple orchards in Southern Brazil. Entomologia Experimentalis et Applicata 91(3):457-463. Landry, B., and L. Roque-Albelo. 2003. Presence of Stenoma catenifer Walsingham (Lepidoptera, Elachistidae, Stenomatinae), the avocado seed moth, in the Galápagos. Noticias de Galápagos 62:15-16. Liquido, N. J., M. K. Hennessey, R. L. Griffin, J. F. Velapatiño, J. M. Layme, and L. B. Gonzales. 2010. Quarantine security for commodities: determining the non-host status of fruits regulated for Tephritid fruit flies. B. Sabater Muñoz, A. Urbaneja Garcia, and V. Navarro Llopis, (eds.). 8th International Symposium on Fruit Flies of Economic Importance, Valencia, Spain. MacGregor, R., and O. Gutierrez. 1983. Guia de insectos nocivos para la agricultura en Mexico. Editorial Alhambra Mexicana, S. A. 166 pp.

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Magarey, R. D., D. M. Borchert, and J. W. Schlegel. 2008. Global Plant Hardiness Zones for Phytosanitary Risk Analysis. Scientia Agricola (Piracicaba-Brazil) 65:54-59. Mangan, R. L., D. B. Thomas, and A. M. Tarshis Moreno. 2011. Host Status of Grapefruit and Valencia Oranges for Anastrepha serpentina and Anastrepha ludens (Diptera: Tephritidae). Journal of Economic Entomology 104(2):388-397. Manicom, B. Q. 2001. Diseases of avocado. Pages 214-230 in E. A. de Villiers, (ed.). Cultivation of avocado. Institute for tropical and subtropical crops, Nelspruit, South Africa. Mariau, D. 2001. Diseases of Tropical Tree Crops. Enfield, NH, USA: Science Publishers, Inc. and CIRAD, France. . Martin, J., and G. Watson. 1998. Aleurodicus pulvinatus (Maskell)(Homoptera: Aleyrodidae), and its emergence as a pest of coconut in the Caribbean. Journal of Natural History 32(1):85-98. Mason, A. 1931. The Economic Importance of the Mediterranean Fruit Fly to Hawaiian Horticulture. proc. Haw. Ent. Soc. 8(1):163-178. McCarthy, A. 2006. Chines wax scale taking a liking to avocados. Agricultural Memo 33(3):6. McGregor, B. M. 1987. Tropical Products Transport Handbook. Agriculture Handbook No. 668. Pages 148 in U. S. D. o. Agriculture, ed. United States Department of Agriculture, Washington, D.C. Miller, D. R., and J. A. Davidson. 1998. A new species of armored scale (Hemiptera: Coccoidea: Diaspididae) previously confused with Hemiberlesia diffinis (Newstead). Proceedings of the Entomological Society of Washington 100(2):193-201. Mossler, M. A., and J. Crane. 2012. Florida Crop/Pest Management Profile: Guava and Wax Jambu. (CIR 1415). University of Florida, Institute of Food and Agricultural Sciences, Florida Cooperative Extension Service, Horticultural Sciences Department. 5 pp. Nakahara, S. 1982. Checklist of the Armoured Scales (Homoptera: Diaspididae) of the Conterminous United States. United States Department of Agriculture, Animal and Plant Health Inspection Service, Plant Protection and Quarantine, Riverdale, Maryland. NASS. 2011. Commercial Citrus Inventory: Preliminary Report. United States Department of Agriculture, National Agricultural Statistics Service (NASS). 6 pp. Norrbom, A. L. 2003. Anastrepha serpentina (Wiedemann). The Diptera Site: Information about the World's flies, Systematic Entomology Laboratory. Last accessed 2012, http://www.sel.barc.usda.gov/diptera/diptera.htm. NRCS. 2013. The PLANTS Database. United States Department of Agriculture, Natural Resources Conservation Service (NRCS), The National Plant Data Center. http://plants.usda.gov. (Archived at PERAL). Oi, D. H., and F. L. Ronald. 1989. Relationship of fruit ripeness to infestation in'Sharwil'avocados by the Mediterranean fruit fly and the Oriental fruit fly (Diptera: Tephritidae). Journal of Economic Entomology 82(2):556-560. Oroño, L. E., S. M. Ovruski, A. L. Norrbom, P. Schliserman, C. Colin, and C. B. Martin. 2005. Two new native host plant records for Anastrepha fraterculus (Diptera: Tephritidae) in Argentina. Florida Entomologist 88(2):228-232. Ovruski, S., P. Schliserman, and M. Aluja. 2003. Native and introduced host plants of Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae) in Northwestern Argentina. Journal of Economic Entomology 96(4):1108-1118.

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PestID. 2014. Pest Identification Database (PestID). United States Department of Agriculture, Animal and Plant Health Inspection Service, Plant Protection and Quarantine. https://mokcs14.aphis.usda.gov/aqas/login.jsp (Archived at PERAL). PExD. 2014. Phytosanitary Export Database (PExD). United States Department of Agriculture, Animal and Plant Health Inspection Service, Phytosanitary Certificate Issuance & Tracking System (PCIT). Last accessed 2012, https://pcit.aphis.usda.gov/PExD/faces/ReportHarmOrgs.jsp. Ploetz, R. C., G.A.Zentmyer, W. T. Nishijima, K. G. Rohrbach, and H. D. Ohr. 1994. Compendium of Tropical Fruit Diseases. APS Press, St. Paul, Minnesota. Posada, L. 1989. Lista de insectos dañinos y otras plagas en Colombia. Instituto Colombiano Agropecuario, División de disciplinas agricolas, Seción de Entomología. PPQ. 2012. Guidelines for Plant Pest Risk Assessment of Imported Fruit and Vegetable Commodities, Version 6.0. United States Department of Agriculture, Animal and Plant Health Inspection Service, Plant Protection and Quarantine (PPQ), Raleigh, NC. Putruele, M. T. G. 1996. Hosts for Ceratitis capitata and Anastrepha fraterculus in the Northeastern Province of Entre Ríos, Argentina. Pages 343-345 in B. A. McPheron and G. J. Steck, (eds.). Fruit fly pests: a world assessment of their biology and management. St. Lucie Press, Delray Beach, FL. Rogg, H. W. 2000. Manual de entomología agrícola de Ecuador. DocuTech, Quito. 694 pp. Rogg, H. W. 2014. Draft Pest Risk Assessment Available for Review and Comment: Passion Fruit from Ecuador. Personal communication to APHIS on 4 August 2014, from Helmut W. Rogg, IPPM Program Manager, Oregon Department of Agriculture. Russell, L. M. 1962. The citrus blackfly. FAO Plant Protection Bulletin 10(2):36-38. Russell, L. M. 1965. A new species of Aleurodicus Douglas and two close relatives (Homoptera: Aleyrodidae). Florida Entomologist:47-55. Sanidad Vegital. 2013. Information submitted to APHIS by the Ecuadorian Sanidad Vegital - Agrocalidad in support of a market access request for Ecuadorian avocados. Sanidad Vegital - Agrocalidad, Quito, Ecuador. Schliserman, P., S. M. Ovruski, O. R. De Coll, and R. Wharton. 2010. Diversity and abundance of hymenopterous parasitoids associated with Anastrepha fraterculus (Diptera: Tephritidae) in native and exotic host plants in Misiones, Northeastern Argentina. Florida Entomologist 93(2):175-182. Shaw, J. 1947. Hosts and distribution of Anastrepha serpentina in northeastern Mexico. Journal of Economic Entomology 40(1):34-40. Stocks, I. C., and G. Hodges. 2012. The Rugose Spiraling Whitefly, Aleurodicus rugioperculatus Martin, a New Exotic Whitefly in South Florida (Hemiptera: Aleyrodidae). Pest Alerts. Stone, A. 1942. Fruitflies of the genus Anastrepha. United States Department of Agriculture, Miscellaneous Publication No. 439, Washington, DC. Sugayama, R. L., A. Kovaleski, P. Liedo, and A. Malavasi. 1998. Colonization of a new fruit crop by Anastrepha fraterculus (Diptera: Tephritidae) in Brazil: a demographic analysis. Environmental Entomology 27(3):642-648. Sugayama, R. L., A. Malavasi, I. Nora, and E. S. Branco. 1996. Ovipositional responses to apple in a caged tree by Anastrepha fraterculus in southern Brazil. Pages 67-69 in B. A. McPheron and G. J. Steck, (eds.). Fruit fly pests: a world assessment of their biology and management. St. Lucie Press, Delray Beach, Florida.

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Teliz, D. 2000. El Aguacate: y su manejo integrado. Mundi-Prensa, Mexico City, Mexico. 219 pp. Thurston, H. D. 1989. Tropical Plant Diseases 2nd Edition. St. Paul, MN: The American Phytophathological Society. 200p. Tigrero S., J. O. 2009. Lista anotada de hospederos de moscas de la fruta presentes en Ecuador. Boletín Técnico 8, Serie Zoológica 4-5:107-116. Waite, G. K., and R. M. Barrera. 2002. Insect and mite pests. Pages 339-362 Avocado: botany, production and uses, the. CABI Publishing, Wallingford, UK. Watson, G. W. 2014. Arthropod of Economic Importance: Diaspididae. NLBIF is the Dutch national node of the Global Biodiversity Information Facility (GBIF). (Archived at PERAL). Weems, H. V. 2002. South American Fruit fly, Anastrepha fraterculus (Wiedemann) (Insecta: Diptera: Tephritidae). University of Florida, Institute of Food and Agricultural Sciences, Gainsville, Florida. Last accessed 07/19/2007, http://creatures.ifas.ufl.edu/fruit/tropical/south_american_fruit_fly.htm. Weems, H. V., and T. R. Fasulo. 2012. Featured Creatures: guava fruit fly, Anastrepha striata Schiner (Insecta: Diptera: Tephritidae) University of Florida. http://entnemdept.ufl.edu/creatures/fruit/tropical/a_striata.htm. (Archived at PERAL). Weems, H. V. J. 2001. Sapote fruit fly, serpentine fruit fly. University of Florida Institute of Food and Agricultural Sciences; Florida Department of Agriculture and Consumer Services, Gainsville, Florida. Last accessed 26 June, 2006, http://creatures.ifas.ufl.edu/fruit/tropical/sapote_fruit_fly.htm. Wellman, F. L. 1977. Dictionary of Tropical American Crops and their Diseases. The Scarecrow Press, Metuchen, New Jersey and London, United Kingdom. 495 pp. White, G. L. 1999. Sapindus saponaria L. (Sapindaceae), a new host of Ecdytolopha aurantianum (Lima) (Lepidoptera: Tortricidae: Olethreutinae). International Journal of Pest Management 45(4):287-291. White, I. M., and M. M. Elson-Harris. 1992. Fruit flies of economic significance: Their identification and bionomics. CAB International and the Australian Center for International Agricultural Research (ACIAR), Wallingford, UK. 601 pp. Willard, H., A. Mason, and D. Fullaway. 1930. Susceptibility of Avocados of the Guatemala Race to Attack by the Mediterranean Fruit Fly in Hawaii. Hawaiian Forester and Agriculturist 26(4):171-176. Wood, S. L. 1992. A Catalog of Scolytidae and Platypodidae (Coleoptera), Part 2: Taxonomic Index, Volume A. Brigham Young University, Provo, Utah. 833 pp. Wood, S. L., and D. E. Bright. 1992. A Catalog of Scolytidae and Platypodidae (Coleoptera), Part 2: Taxonomic Index (Vol. B). Brigham Young University, Provo, Utah. 1-1553 pp. Yust, H. R. 1958. Insect identifications made in Ecuador and key to collection. Servicio cooperativo interamericano de agricultura, Quito, Ecuador. 85 pp. Zucchi, R. A., and R. C. Moraes. 2008. Fruit Flies (Dipera: Tephritidae) in Brazil: Anastrepha species their host plants and parasitoids. http://www.lea.esalq.usp.br/anastrepha/edita_ssp_i.php. (Archived at PERAL).

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

We found some evidence of the below listed organisms being associated with avocado and being present in Ecuador. Because these organisms have non-actionable regulatory status for the continental United States, however, we did not list them in Table 1 of this risk assessment, and we did not evaluate the strength of the evidence for their association with avocado or their presence in Ecuador. Because we did not evaluate the strength of the evidence, we consider the following pests to have only “potential” association with avocado and presence in Ecuador.

Below we list these organisms along with the references supporting their potential association with avocados, their potential presence in Ecuador, their presence in the continental United States (if applicable), and their regulatory status for the continental United States. For organisms not present in the continental United States, we also provide justification for their non-actionable status.

Organism Evidence and/or other notes Aetalion picta (God.) Yust, 1958, non-rep (PestID, 2014) Aleurothrixus floccosus (Maskell) Evans, 2008, non-rep (PestID, 2014) Aonidiella orientalis (Newstead) CABI, 2014 (FL) CABI, 2014 Araptus schwarzi (Blackman) Wood, 1992, non-rep (PestID, 2014) Aspidiotus destructor Signoret Ebeling, 1959, non-rep (PestID, 2014) Atherigona orientalis Schiner Ebeling, 1959, US (CABI, 2014) Bemisia tabaci (Gennadius) US (CABI, 2014), non-rep (PestID, 2014) Ceroplastes sinensis Del Guercio McCarthy, 2006, US (IIE, 1995) Chrysodeixis includens CABI, 2014, US (CABI, 2014) Chrysomphalus dictyospermi (Morgan) Hernández et al., 2000, US (CABI, 2014) Coccus longulus (Douglas) Ben-Dov, 1993, US (Ben-Dov, 1993) Dysdercus bimaculatus Stal = D. obliquus Ebeling, 1959, US (Henry and Froeschner, (Herrich-Schaeffer) 1988) Dysmicoccus brevipes (Cockerell) Hernández et al., 2000, US (CABI, 2014) Ferrisia virgata (Cockerell) Ebeling, 1959, US (CABI, 2014) Heliothrips haemorrhoidalis (Bouché) Hernández et al., 2000; Waite and Barrera, 2002, US (CABI, 2014) Helix aspersum (Müller) CABI, 2014, non-rep (PestID, 2014) Hemiberlesia diffinis (Newstead) Miller and Davidson, 1998; Hernández et al., 2000 All Diaspidid scales have non-actionable status on commodities for consumption (PestID, 2014) Hemiberlesia lataniae (Signoret) Hernández et al., 2000, US (CABI, 2014) Hemiberlesia palmae (Cockerell) Ebeling, 1959 Hemiberlesia rapax (Comstock) Hernández et al., 2000, US (CABI, 2014) Largus succinctus (L.) (= L. cinctus Herrich- Ebeling, 1959, non-rep (PestID, 2014) Schaeffer) Lorryia formosa Cooreman Jeppson et al., 1975, non-rep (PestID, 2014)

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Organism Evidence and/or other notes Myzus persicae (Sulzer) CABI, 2014, US (CABI, 2014) Nezara viridula (L.) Ebeling, 1959, US (CABI, 2014) Nipaecoccus nipae (Maskell) Ebeling, 1959; Hernández et al., 2000, US (CABI, 2014) Oligonychus peruvianus (McGregor) CABI, 2014, (CA, TX) (CABI, 2014) Pagiocerus frontalis (Fabricius) Ebeling, 1959, non-rep (PestID, 2014) Parasaissetia nigra (Nietner) CABI, 2014, US (CABI, 2014) Peridroma saucia (Hubner) CABI, 2014, US (CABI, 2014) Planococcus citri (Risso) Hernández et al., 2000, US (CABI, 2014) Planococcus minor (Maskell) Non-rep (PestID, 2014) Polyphagotarsonemus latus (Banks) Waite and Barrera, 2002, US (CABI, 2014) Protopulvinaria pyriformis (Cockerell) Manicom, 2001; Waite and Barrera, 2002, Pseudaonidia trilobitiformis (Green) Watson, 2014, US (Nakahara, 1982) Saissetia coffeae (Walker) MacGregor and Gutierrez, 1983, US (CABI, 2014) Saissetia oleae Olivier Hernández et al., 2000, US (CABI, 2014) Selenaspidus articulatus (Morgan) Ebeling, 1959, (CA) CABI, 2014 Selenothrips rubrocinctus (Giard) Waite and Barrera, 2002, (FL) (CABI, 2014) Solenopsis geminata (Fabricius) Ebeling, 1959, non-rep (PestID, 2014) Spodoptera eridania (Cramer) CABI, 2014, US (CABI, 2014) Toxoptera aurantii (Fonscolombe) Ebeling, 1959, non-rep (PestID, 2014) Trialeurodes vaporariorum (Westwood) Ebeling, 1959, non-rep (PestID, 2014) Xyleborinus saxesenii (Ratzeburg) CABI, 2014, US (Wood and Bright, 1992) Xyleborus ferrugineus (Fabricius) CABI, 2014, US (CABI, 2014) Xyleborus volvulus (Fabricius) CABI, 2014, (FL) CABI, 2014

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