United States 

Department of 

Agriculture

Animal and Plant 

Health Inspection 

Service

December 16, 2012

Version 9

Importation of Fresh Citrus Fruit, including Sweet 

Orange (Citrus sinensis (L.) Osbeck), Lemon (C. limon

(L.) Burm. f.), Mandarin (C. reticulata Blanco, C. 

clementina Hort. ex Tanaka, C. deliciosa Ten., C. unshiu

Marcow.), Citrus Hybrids, and the Citrus-Related Genus 

Fortunella (F. japonica (Thunb.) Swingle, F. margarita

(Lour.) Swingle), from Uruguay into the Continental 

United States 

A Qualitative, Pathway-Initiated Risk Assessment

Agency Contact:

Plant Epidemiology and Risk Analysis Laboratory

Center for Plant Health Science and Technology

United States Department of Agriculture

Animal and Plant Health Inspection Service

Plant Protection and Quarantine

Raleigh, NC 
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012 i

Executive Summary

The Plant Protection Division of the Dirección General de Servicios Agrícolas (DGSA), 

Ministerio de Ganadería, Agricultura y Pesca (MGAP) for Uruguay initially drafted a pest risk 

assessment to examine plant pest risks associated with importation of the following Citrus fruit 

from Uruguay into the continental United States: sweet oranges (Citrus sinensis (L.) Osbeck), 

lemons (C. limon (L.) Burm. f.), mandarins (C. reticulata Blanco, C. clementina Hort. ex 

Tanaka, C. deliciosa Ten., C. unshiu Marcow), Citrus hybrids, and the Citrus-related genus 

Fortunella (F. japonica (Thunb.) Swingle, F. margarita (Lour.) Swingle). The draft was 

reviewed and revised by the Plant Epidemiology and Risk Analysis Laboratory (PERAL) staff 

who examined the risk of commercially produced Citrus spp. and Fortunella spp. fruit from 

Uruguay. We assessed the risk in qualitative terms (high, medium, low). The details of the 

methodology and rating criteria used to analyze these pests are in the Guidelines for PathwayInitiated Pest Risk Assessment, Version 5.02 (PPQ, 2000). 

Quarantine pests of Citrus spp. and Fortunella spp. in Uruguay found to follow the pathway

include four arthropods and two plant pathogens:

Arthropods Anastrepha fraterculus (Wiedemann)

Ceratitis capitata (Wiedemann)

Cryptoblabes gnidiella Milliere 

Gymnandrosoma aurantianum (Lima) 

Fungi Elsinoё australis (Bitancourt & Jenks.) 

Bacteria Xanthomonas citri subsp. citri (ex. Hasse) 

In addition to the quarantine pests currently in Uruguay, quarantine pests of concern are present 

in citrus production areas in countries bordering Uruguay. Such quarantine pests include 

pathogens, such as Xylella fastidiosa Citrus Variegated Chlorosis strain (CVC), “Candidatus

Liberibacter” species, Citrus leprosis virus, Citrus Greening, and Zonate Chlorosis, and their 

associated vectors. In a previous revision of the PRA, Guignardia citricarpa Kiely was included 

as a quarantine pathogen likely to follow the pathway. However a pest risk assessment (PRA) 

conducted in 2010 concluded that fresh or dried citrus fruit is not epidemiologically significant 

as a pathway for the introduction of CBS because the combination of conditions required for 

disease transmission from harvested fruit are highly unlikely. We therefore consider that fruit 

which is commercially harvested and surface treated with fungicides prior to shipment is a 

negligible risk, so analysis of this pathogen was removed from the document.

We analyzed each quarantine pest likely to follow the pathway and rated its pest risk potential. 

The Pest Risk Potential is a summary of the ratings for the Consequences of Introduction and 

Likelihood of Introduction. We estimated the Consequences of Introduction by assessing the 

climate-host interaction, the host range, the dispersal potential, the economic impact, and the 

environmental impact: all are based on the biology of the pests. We estimated the Likelihood of 

Introduction by evaluating the proposed quantity imported annually in combination with the

pest’s survival potential. A given pest’s survival potential is the likelihood that the pest survives
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ii

standard production practices, post-harvest treatments, and shipment; avoids detection at the port 

of arrival; and is likely to be moved to a suitable habitat and come into contact with suitable host 

material. Rating of Likelihood of Introduction is followed by proposal of pest risk management 

strategies, designed to reduce the risk of introduction of a quarantine pest. 

Anastrepha fraterculus, Ceratitis capitata, Cryptoblabes gnidiella, and Gymnandrosoma 

aurantianum had High Pest Risk Potential; and Xanthomonas citri subsp. citri, and Elsinoё 

australis had Medium Pest Risk Potential.

We analyzed the quarantine pests based on international principles and internal guidelines 

described in the PPQ Guidelines for Pathway-Initiated Pest Risk Assessments, Version 5.02 

(PPQ, 2000). Pest biology studies are the basis for the Consequences of Introduction and 

Likelihood of Introduction sections. These analytical phases and specific criteria are then used to 

categorize pests; in this case the estimates resulted in several species receiving High risk ratings. 

Port-of-entry inspections, as a sole mitigative measure, are deemed insufficient to safeguard U.S. 

agriculture from pests; additional phytosanitary measures are necessary to reduce risks to 

acceptable levels.

Phytosanitary risk may be reduced using mitigation measures designed to eliminate, reduce, or 

prevent the presence of pests in shipments of commodities primarily in the country of origin. The 

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

The pest risks associated with the importation of fresh fruit of Citrus spp. from Uruguay were 

assessed, taking into account the standard industry practices (e.g., crop and pest management, 

routine processes in packinghouses), the Surveillance Program and Citrus Fruit Phytosanitary

Certification System, developed by DGSA (see Appendices), and several other risk mitigation 

measures for each pest. Possible options for mitigation of the pests identified are outlined in the 

document.
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Table of Contents 

1. Introduction............................................................................................................................... 1

1.1 Regulatory Authority .......................................................................................................... 2

1.2 Initiating Event / Proposed Action...................................................................................... 2

1.3 Citrus Pest Surveillance ...................................................................................................... 4

1.4 Citrus Fruit Phytosanitary Certification.............................................................................. 4

2. Risk Assessment ........................................................................................................................ 5

2.1 Assessment of Weediness Potential of Citrus spp. and Fortunella spp. ............................ 5

2.2 Pests intercepted on Citrus spp........................................................................................... 6

2.3 Pests Associated with Citrus spp. and hybrids and Fortunella spp. in Uruguay................ 7

2.4 Consequences of Introduction........................................................................................... 34

2.5 Likelihood of Introduction................................................................................................ 47

2.6 Pest Risk Potential ............................................................................................................ 61

3. Risk Management Options..................................................................................................... 62

3.1 Measures for Pest Risk Reduction .................................................................................... 62

3.2 Phytosanitary Options....................................................................................................... 63

3.3 Oversight........................................................................................................................... 69

3.4 Conclusions....................................................................................................................... 69

3.5 Contacts, Authors, Contributors, and Reviewers.............................................................. 71

4. References................................................................................................................................ 71

5. Appendices............................................................................................................................... 95

Appendix A. Citrus Pest Surveillance information provided by DGSA ................................ 95

Appendix B. Selected Plant Pest Interception Records.......................................................... 98

Appendix C. Citrus production, harvest, and post-harvest processes in Uruguay................ 108

Appendix D. Citrus Fruit Phytosanitary Certification .......................................................... 114

Appendix E. Life cycle of Xanthomonas citri subsp. citri, the pathogen causing citrus canker

............................................................................................................................................... 122
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1

1. Introduction

The Plant Protection Division of the Dirección General de Servicios Agrícolas (DGSA), 

Ministerio de Ganadería, Agricultura y Pesca (MGAP) for Uruguay initially drafted a pest risk 

assessment to examine plant pest risks associated with importation of Citrus and Fortunella fruit 

from Uruguay into the continental United States. The Plant Epidemiology and Risk Analysis 

Laboratory (PERAL) of the United States Department of Agriculture, Animal and Plant Health 

Inspection Service, Plant Protection and Quarantine, Center for Plant Health Science and 

Technology (USDA, APHIS, PPQ, CPHST) reviewed and revised this pest risk assessment to 

examine plant pest risks associated with the importation of the commercially produced fresh 

citrus fruit listed below from Uruguay into the continental United States: 

 Sweet oranges: Citrus sinensis (L.) Osbeck

 Lemons: C. limon (L.) Burm. f.

 Mandarins: C. reticulata Blanco, C. clementina Hort. ex Tanaka, C. deliciosa Ten., C. 

unshiu Marcow

 Citrus-related genus: Fortunella spp., Fortunella japonica (Thunb.) Swingle, F. 

margarita (Lour.) Swingle.

 Citrus hybrids: C. nobilis x C. deliciosa, C. clementina x C. tangerina, (C. paradisi x C. 

tangerina) x C. clementina, C. unshiu x C. sinensis, C. clementina x C. reticulata, C. 

clementina x (C. paradisi x C. tangerina), [C. clementina x (C. paradisi x C. tangerina)] 

x C. temple, C. paradisi x C. tangerina, C. reticulata x C. sinensis.

Commercially produced fresh citrus in Uruguay is grown, processed, and packed in accordance 

with DGSA Phytosanitary Standards, which support a production process that satisfies the 

requirements of the Quality Management Systems, Good Agricultural Practices, and Traceability

(Global G.A.P., 2008). In the packinghouse the fruit are subjected to cleaning and sanitizing 

processes, including a surface treatment of fungicides to produce quality fruit for the fresh fruit 

export market and to fulfill all the client’s requirements (DGSA, 2008; Díaz et al., 2001). The 

commodity includes short, clipped stems (~ 0.5 cm), and excludes fruit that is over-mature, offcolor for the Citrus species and variety, damaged, rotted, spotted, or misshapen. Fruit not 

commercially grown or packed are beyond the scope of this risk assessment.

Factors analyzed in the assessment include the biology, host range, distribution, entry potential, 

establishment potential, spread potential, and economic damage potential of the pests that may

be associated with shipments of fresh citrus fruits from Uruguay. The estimates of risk are 

expressed qualitatively (high, medium or low). Details of the risk assessment method may be 

found in Guidelines for Pathway-Initiated Pest Risk Assessment, Version 5.02 (PPQ, 2000).

The International Plant Protection Convention (IPPC) of the Food and Agriculture Organization 

(FAO) provides guidance for conducting pest risk analyses. The methods used to initiate and 

conduct this pest risk assessment are consistent with IPPC guidelines (IPPC, 2007a: ISPM # 11). 

Biological and phytosanitary terms conform to the IPPC Glossary of Phytosanitary Terms (IPPC, 

2007b: ISPM #5) and to the Definitions and Abbreviations (Introduction Section) in the 

International Standards for Phytosanitary Measures, Guidelines for Pest Risk Analysis for 

Quarantine Pests Including Analysis of Environmental Risks and Living Modified Organisms
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(IPPC, 2007a: ISPM #11). As used in this document, pest risk assessment is the determination of 

whether a pest is a quarantine pest and the evaluation of its introduction potential (IPPC, 2007a 

and 2007b: ISPM # 5 and 11). Pest risk management is the decision-making process of reducing 

the risk of introduction of a quarantine pest (IPPC, 2007a and 2007b: ISPM #5 and 11). Pest risk 

analysis is the process of evaluating biological or other scientific and economic evidence to 

determine whether a pest should be regulated and the strength of any phytosanitary measures 

taken against it. Pest risk analysis encompasses both risk assessment and risk management 

(IPPC, 2007a: ISPM #2). The Framework for Pest Risk Analysis (IPPC, 2007a: ISPM #2) 

describes three stages in pest risk analysis. This document satisfies the requirements of FAO 

Stages 1 and 2, initiation and risk assessment, and gives options for Stage 3 that will be met later

in the development of the risk management document.

1.1 Regulatory Authority

Title 7 of the Code of Federal Regulations 319, Part 56 (7 CFR § 319.56, 2008) provides 

regulatory authority for the importation of fruits and vegetables from foreign sources into the 

United States. Quarantine 19 (7 CFR §319.19, 2008, Citrus Canker and Other Citrus Diseases) 

prohibits the importation of citrus plants or plant parts except fruit into the United States. 

Quarantine 28 (7 CFR § 319.28, 2008, Citrus Fruit) prohibits the importation of citrus fruit from 

most countries where certain diseases occur, including Uruguay. Quarantine 28 further 

promulgates a general prohibition against the importation of citrus fruit from countries where 

citrus canker disease occurs. Importation of citrus fruit is generally prohibited except for 

particular citrus species and varieties grown, packed, and shipped under certain conditions from 

specific areas (e.g., Australia, Japan, Korea, Mexico, and Republic of South Africa) as stated in 

7CFR 319.28 and 56. These restrictions prevent the introduction of a number of citrus pests 

including, but not limited to, fruit flies in the genera Anastrepha and Ceratitis, citrus canker 

(Xanthomonas citri subsp. citri), and sweet orange scab (Elsinoë australis). Imported fruit is also 

subject to regulations that govern domestic interstate movement of regulated fruit from 

quarantined areas for citrus canker and sweet orange scab (7 CFR § 301.75-1 to 310.75-14. 2011; 

APHIS-USDA. 2010a).

1.2 Initiating Event / Proposed Action

In 1990, the government of Uruguay requested that the APHIS Administrator initiate the process 

to allow the export of citrus fruit from Uruguay into the Continental United States. APHIS 

identified Ceratitis capitata, Anastrepha fraterculus, Guignardia citricarpa, Elsinoё australis 

and Xanthomonas citri subsp. citri (Xcc), as quarantine pests. In 1995, APHIS developed the 

first draft of the Uruguayan proposal and required additional information. In November 1996, 

APHIS sent the first Technical Mission, and the DGSA proposed a systems approach for Xcc 

risk mitigation based on the Self Protecting Areas (SPAs). SPAs contain one or more canker free 

places of production or have a localized eradicated disease focus, in which symptoms have not 

been observed before harvest and all risk mitigation measures have been applied. The DGSA 

provided APHIS with survey results for G. citricarpa based on 1448 samples from all citrus 

areas to demonstrate the absence of this pathogen. Likewise the DGSA shared the results

obtained in determinations of citrus scab biotype, citrus scab control assays, and confirmed the 

absence of the pathogen in Uruguay at that time. The APHIS Technical Mission accepted the 
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Uruguayan proposal and decided to complete a qualitative PRA to define the phytosanitary

requirements within one year, after which APHIS could implement a possible operational pilot 

program. 

By 2000, the PRA had not been completed and APHIS sent a new Technical Mission to collect 

information needed for a quantitative pest risk assessment. The Mission reviewed the standards 

and protocols presented in 1996, and the DGSA presented the Citrus Fruit Phytosanitary

Certification System (CFPCS). The DGSA has had a legal framework since 1977 supporting the 

eradication campaign for Xcc and a risk mitigation system defined within the framework of the 

CFPCS. Xcc is the key pest for this system, which is based on risk mitigation and traceability

procedures. A Citrus Plant Production Program has been in place since 1998, which uses more 

restrictive measures for production and implements sanitation procedures for citrus materials 

entering the country. 

The DGSA implemented the National Surveillance System for Fruit Flies, including C. capitata 

and A. fraterculus. APHIS approved treatments for fruit flies are available. After this mission 

and up to 2002, the DGSA sent Dr. David Oryang (Tuskegee University) all the information 

required for a quantitative citrus canker PRA. For other pests of concern, G. citricarpa and E. 

australis, APHIS would develop a qualitative PRA. The PRA was put on hold from 2002 to 2005

in part because the DGSA and APHIS did not agree on the status of E. australis. In 2006, the 

Ministry of Livestock, Agriculture, and Fisheries (MGAP) of Uruguay asked for an update of the 

citrus PRA. 

The present risk assessment is for the importation of commercially grown and packed fresh 

Citrus, Citrus hybrids, and Fortunella fruit from Uruguay into the continental United States. 

Most commercial production in Uruguay occurs in the Northern and Southern areas of the 

country (Figure C1 in Appendix C). The Northern area includes the departments1of Salto, 

Paysandú, Río Negro, and Rivera. The Southern area includes the departments of San José, 

Canelones, Montevideo, Maldonado, and Colonia. The most recent National Citrus Census 

(CHNPC, 1996) reported that 85 percent of the total 20,862 hectares planted are located in the 

Northern area and 15 percent in the Southern area of the country. Prominent technological 

improvements implemented in Uruguay include the plant certification program, improvements in 

irrigation systems, continuous growth in productivity, changes to new varieties, modern cold 

storage facilities, and improvements in logistics. The citrus industry has developed an 

agroindustrial infrastructure of packing, cold storage, and ports that facilitates exports. The 

DGSA has a significant role in safeguarding citrus production through the support of 

phytosanitary surveillance, phytosanitary certification systems for export and its commitment in 

the opening of new markets. Great efforts are being made to produce high quality fruit within a 

responsible production process that satisfies the requirements of the Quality Management 

Systems, Good Agricultural Practices, and Traceability (Global G.A.P., 2008).

There are up to 14 packinghouses for citrus fruit processing in Uruguay: seven in the Northern 

area and the remainder in the Southern area. Five of them also have their own cold storage 

facilities and degreening chambers. Nueva Palmira Fruit Terminal, Frigofrut S.A, has ISO 

9000:2000 certification and operates under a bar coding system called Cooltrack. The 

 

1 Departments in Uruguay are equivalent of states or provinces.
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Montevideo port is used mainly to export fruit in containers. Commercial production areas and 

packinghouses approved for export in these provinces are defined by DGSA through a system of 

registration that is required in Uruguay for traceability (Appendices A, B, and C). 

This assessment is independent of previous risk assessment work. It draws from information 

compiled by DGSA and previous assessments as a baseline for pest listing, but it uses a different, 

more familiar methodology. The present pest risk assessment also incorporates important 

research, experience, and other evidence gained over the past thirteen years. The pest list has 

been substantially updated based on new information provided by DGSA or found by APHIS in 

the current literature. New information and experience have also contributed to a better 

understanding of the main pest risks associated with Citrus from Uruguay, including citrus 

canker, sweet orange scab, mites, fruit flies, and Lepidoptera pests– all pests of quarantine 

concern that are identified in this assessment.

1.3 Citrus Pest Surveillance

The DGSA continually surveys for quarantine pests of concern for importing countries through 

pre-harvest inspection of export fruit. These pre-harvest surveys are conducted on 100 percent of 

plants in all the places of production registered for export. Specific annual surveys are conducted 

in groves with fruit going to the domestic market. In the main citrus production area of Uruguay

(north), the DGSA has 50 trained inspectors and all the export companies have trained personnel 

who help with the pre-harvest inspection. All pests found during surveys and inspections that are 

not identifiable by personnel are sent to the DGSA lab for diagnosis. In addition, the DGSA has 

an agreement with the Agronomic Faculty and the National Research Institute, and their 

phytosanitary experts inform the DGSA about citrus survey and research conducted by these 

institutions.

See Appendix A for a detailed update on surveillance for some of the quarantine pests including

Xanthomonas citri subsp. citri, Guignardia citricarpa, Ceratitis capitata, and Anastrepha 

fraterculus.

1.4 Citrus Fruit Phytosanitary Certification

In 1998 the DGSA implemented the Citrus Fruit Phytosanitary Certification System (CFPCS) to 

comply with phytosanitary requirements of citrus fruit for export (summary in Appendix D). 

Accomplishments of this system follow:

 CFPCS has demonstrated that it can meet requirements for any export market. 

 The Uruguayan citrus industry has improved the traceability systems, adjusting them for 

phytosanitary regulation purposes.

 CFPCS allows the official and private sectors to clearly define their responsibilities in 

production and export. 
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2. Risk Assessment 

2.1 Assessment of Weediness Potential of Citrus spp. and Fortunella spp.

Citrus and Fortunella species do not have significant potential as weeds indicated in the 

scientific literature, so we concluded that Citrus and Fortunella species are not potential weeds

(Table 1). 

Table 1. Weediness potential of Citrus spp., Fortunella spp., and Citrus hybrids.

Plant Species: Sweet orange (Citrus sinensis (L.) Osbeck), lemons (C. limon (L.) Burm. f.), 

mandarins (C. reticulata Blanco, C. clementina Hort. ex Tanaka, C. deliciosa Ten., C. 

unshiu Marcow), the Citrus-related genus Fortunella (Fortunella japonica (Thunb.) 

Swingle, F. margarita (Lour.) Swingle), and Citrus hybrids.

Phase 1: Consider whether the species is new to or not widely prevalent in the United States 

(exclude plants grown under USDA permit in approved containment facilities).

Citrus limon, C. sinensis, C. reticulata, C. paradisi, C. clementina, C. unshiu, Citrus

hybrids, F. japonica and F. margarita are introduced and grown in the United States 

(USDA-NRCS, 2007b; USDA-ERS, 2007).

Phase 2: Weediness Potential. Is Citrus listed in:

No Geographical Atlas of World Weeds (Holm et al., 1979)

No Invasive Plant Species of the World: A Reference Guide to Environmental Weeds 

(Weber, 2003)

No World's Worst Weeds (Holm et al., 1977)

No World Weeds. Natural Histories and Distribution (Holm et al., 1977)

No Report of the Technical Committee to Evaluate Noxious Weeds; Exotic Weeds for 

Federal Noxious Weed Act (Gunn and Ritchie, 1982)

No Economically Important Foreign Weeds (Reed, 1977)

No Weed Science Society of America list (WSSA, 2007)

Yes Is there any literature reference indicating weed status (e.g., AGRICOLA, CAB, 

Biological Abstracts, AGRIS; Internet search")? 

Biondi and Pedrosa-Macedo, 2008 report that Citrus limon is invasive in Brazil.

No 7CFR § 360 (January 1, 2005; Skinner et al., 2008).

Yes Randall (2007) listed the status of the following species: C. limon: weed, naturalized, 

garden escape, environmental weed, cultivation escape, casual alien. C. reticulata: 

weed, naturalized, introduced. C. sinensis: weed, naturalized, introduced, 

environmental weed, casual alien. Citrus spp.: weed

Phase 3: Summary and Conclusions: There is no reason to consider Citrus species as potential 

weeds because various species, including C. sinensis, C. x paradisi, C. limon, C. 

reticulata, C. clementina, C. unshiu and Citrus hybrids are cultivated throughout the 

United States; furthermore, the scientific literature provides little indication of weed 

potential.
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2.2 Pests intercepted on Citrus spp. 

APHIS-PPQ maintains a database of all the interceptions of pests on commodities entering the 

United States (PestID, 2007), including permit cargo, general cargo, ship’s quarters, ship’s holds, 

passenger baggage, ship stores, mail, and other pathways. Between 1985 and 2007, 25,450 

interception records exist for Citrus fruit from South America (PestID, 2007), but only 160 of 

these records were from Uruguay (PestID, 2007), which increased to 174 records in 2008 

(PestID, 2008). Pest interception records on Citrus spp. from South America (1985-2007) are 

shown in Appendix B in Table B1, and from Uruguay (1985-2008) in Table B2. No interceptions 

were made of Fortunella spp. from South America.

2.2.1. Pests intercepted on Citrus spp. from Uruguay

Most of these interceptions were made from passenger baggage, and ship’s stores and quarters. 

The interception data shows three records from permit cargo, which must be in error, since 

Uruguay is not authorized to export citrus fruit to the United States.

Arthropods:

Aonidiella sp. (Homoptera: Diaspididae)

Lepidosaphes beckii (Homoptera: Diaspididae) 

Parlatoria sp. 

Parlatoria cinerea (Homoptera: Diaspididae) 

Parlatoria pergandii (Homoptera: Diaspididae) 

Parlatoria ziziphi (Homoptera: Diaspididae) 

Pseudococcus sp. 

Tarsonemus sp. 

Pathogens:

Colletotrichum sp.

Coniothyrium sp.

Diaporthe citri F. A. Wolf [Anamorph: Phomopsis citri H. S. Fawcett] (Ascomycetes: 

Diaporthales)

Elsinoё australis Bitanc. & Jenkins (Elsinoaceae) 

Elsinoё sp. (Elsinoceae)

Phoma sp.

Xanthomonas citri subsp. citri [reported as Xanthomonas axonopodis pv. citri (Hasse) Dye 

and Xanthomonas campestris pv. citri (Hasse) Dye] (Xanthomonadaceae)

2.2.2 Pests intercepted on Citrus from South America

Arthropods: 

We added the following to the pest list based on interceptions and evidence that they are Citrus

pests in Uruguay:

Aleurocanthus woglumi Ashby (Aleyrodidae)

Aleurothrixus floccosus Maskell (Aleyrodidae) 

Amyelois transitella (Walker) (Pyralidae) 

Aonidiella aurantii (Maskell) (Diaspididae)

Aspidiotus excisus Green (Diaspididae)
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Aspidiotus nerii Bouche (Diaspididae)

Aulacorthum solani (Kaltenbach) (Aphididae)

Brevipalpus obovatus Donnadieu (Tenuipalpidae)

Ceratitis capitata (Wiedemann) (Tephritidae)

Chysomphalus dictyospermi (Morgan) (Diaspididae)

Coccus hesperidium (L.) (Coccidae)

Dialeurodes citri (Ashmead) (Aleyrodidae)

Dialeurodes citrifolii (Morgan) (Aleyrodidae)

Diaphorina citri Kuwa Yama (Psyllidae)

Hemiberlesia rapax (Comstock) (Diaspididae) 

Lepidosaphes beckii (Newman) (Diaspididae)

Lepidosaphes gloverii (Packard) (Diaspididae)

Parlatoria ziziphi (Lucas) (Diaspididae)

Planococcus citri (Risso) (Pseudococcidae)

Planococcus minor (Maskell) (Pseudococcidae)

Pseudaonidia trilobitiformis (Green) (Diaspididae)

Pathogens:

Although numerous interceptions of pathogens occurred from South America, there were none 

added to the pest list based on this evidence. Most pathogens reported from South America had 

directly been reported from Uruguay on Citrus.

2.3 Pests Associated with Citrus spp. and hybrids and Fortunella spp. in Uruguay

2.3.1 Pest Categorization– Identification of Quarantine Pests

Our procedures are based on ISPM 11 (IPPC, 2007a). The first step in identifying quarantine 

pests is to present a comprehensive list of potential quarantine pests known to occur in the 

country or region from which the commodity is to be exported. The list includes all pests in the 

exporting country associated with the proposed export commodity. Because all pests on the list 

are associated with the plant species, they are considered to be “of potential economic 

importance” (IPPC, 2007a). The listed pests may or may not also occur in the United States.

Comprehensive pest lists are developed because of the dynamic nature of quarantine species (for 

example, species move into new territories, and, on the other hand, eradication programs change 

their distribution).

The definition of a quarantine pest has two primary components (IPPC, 2007b: ISPM #5). First, 

a pest must be “of potential economic importance” to be included in the comprehensive list of 

potential quarantine pests. An organism is considered to be of potential economic importance if 

evidence demonstrates that the organism is harmful and has an association with the plant species 

being assessed. Second, to be considered a quarantine pest, an organism must satisfy geographic 

and regulatory criteria; specifically, the pest must not yet be present in the area being assessed, or 

if present, it should be under official control (IPPC, 2007b).

The risk assessment documents the evidence used to determine how each organism satisfies the 

defining criteria for a quarantine pest. Pertinent geographic and regulatory information with 

respect to the exporting country and the United States is provided on the comprehensive pest list.
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If none of the listed pests satisfy the geographic and regulatory criteria for a quarantine pest, 

further assessment is not necessary. Below we comprehensively listed pests for Citrus spp.,

Citrus hybrids, and Fortunella spp. from Uruguay (Table 2). In the pest list we identified the 

presence or absence of these pests in the United States and the quarantine status of the pest with 

respect to the United States. If the pest has quarantine status we identify the generally affected 

plant part or parts, and whether or not the pest is likely to follow the pathway to enter the United 

States on commercially exported Citrus spp., Citrus hybrids, or Fortunella spp. For each piece of 

information, we include pertinent citations for distribution, host association, and biology of the 

pest for quarantine species.

2.3.2 Pest Categorization– Quarantine Pests Likely to Follow the Pathway

A pest is considered to follow the pathway if it is associated with the commodity and likely to 

survive with the commodity until entry into the United States. Quarantine pests identified as 

likely to be associated with the potential export commodity are subject to Steps 5-7 of the USDA 

Guidelines (PPQ, 2000). The biology and pest potential for these pests are documented as 

appropriate to inform the risk analysis; therefore, it is reasonable to assume that these quarantine 

pests:

 will be present in the exporting country;

 will be associated with the commodity at the time of harvest; and

 will remain with the commodity in a viable form during harvesting, packing, and 

shipping procedures.

Because all pests associated with the plant species are listed, there will be quarantine pests not 

expected to follow the pathway. For example:

 a pest may be only associated with plant parts other than commodity shipped, or

 a pest may not reasonably be expected to remain with the commodity during harvest and 

packing.

The status of the pests in the table assumes that the commodity will be produced using 

commercial practices and that post-harvest measures will include culling, cleaning (removing 

foreign matter, washing with brushing), and dipping with chemicals such as chlorine and/or other 

disinfectants, waxing, treatment with fungicides (imazalil and/or thiabendazole) and the 

exclusion of overripe fruit (7 CFR § 301.75-1 to 310.75-14, 2011; 7 CFR § 305.11, 2010;

APHIS-USDA, 2010b). If post-harvest processes are not followed, then status of the pests in the 

table may change, particularly the likelihood of the pest following the pathway. 

Pests not expected to follow the pathway are not considered. Supporting information must be 

documented on the pest list or in the text. The decision to not further analyze a particular pest 

only applies to the current assessment; a pest may pose a different level of risk for the same 

commodity from a different country, or for a different commodity (e.g., propagative cuttings) 

from the same host plant species. If any of the pests should be intercepted in commodity

shipments, quarantine action may be taken at the port-of-entry and additional risk analyses may

be conducted. Finally, the status of a pest may change (that is, global population dynamics result 

in changes in the distribution of pests) and the current document may need to be updated if 

significant changes occur in the future. A significant change would include the appearance of a 
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

9

new serious quarantine pest species in the exporting country or changes in the quarantine status 

of an existing pest if that organism becomes established in the United States and is deregulated.

We compiled the list by reviewing scientific literature and the PPQ database of pests intercepted 

on Citrus and Fortunella species and hybrids from South America (PestID, 2007), specifically

Uruguay (PestID, 2008). Of the pests intercepted on Citrus or Fortunella spp. from South 

America (Appendix B, Table B1) and from Uruguay specifically (Table B2), pests included in 

the list associated with citrus in Uruguay conformed to the following criteria:

o Organisms identified to species level found in Uruguay.

o Organisms identified to the genus level were included in the list only if reported on 

Citrus or Fortunella in Uruguay; if the genus is not known to occur in the United States 

the pest was analyzed further

o Intercepted pests identified to only the family level were not included because it is 

impossible to confirm pest identity.

The list of pests intercepted on Citrus spp. from South America was reviewed in consultation 

with DGSA Mycologist Luis Díaz and Entomologist Iris B. Scatoni, Faculty of Agronomy in

Uruguay (Scatoni, 2007). Pest interceptions from Citrus or Fortunella spp. from South America 

and Uruguay specifically are summarized from the extended table in Appendix B.

Unless the genus or higher taxonomic group does not occur in the United States, organisms 

identified to the genus or higher taxonomic level, are not analyzed further, even though 

individual species within those taxonomic groups are potential pests that may or may not occur 

within the United States, The IPPC guidelines do not require risk assessment of pests identified 

only by genus name (IPPC, 2007a: ISPM # 11). By necessity, pest risk assessments focus on 

those organisms for which adequate biological and taxonomic information is available. Often, 

there are many species within a genus, and it is not reasonable to assume that the biology of all 

organisms within a genus is identical. Lack of species identification may indicate the limits of 

the current taxonomic knowledge, or inadequacy of the life stage or the quality of the specimen 

submitted for complete identification. The lack of identification at the species level does not rule 

out the possibility that a high risk quarantine pest was intercepted or that the intercepted pest was 

not a quarantine pest. By developing detailed assessments for known pests that inhabit a variety 

of niches on the parent commodity, for example, on the surface of, within the stem or fruit, on 

the flowers, etc., effective mitigation measures may be developed to eliminate the known pests, 

and any similar unknown ones that inhabit the same niches. Lack of biological information on 

any given insect or pathogen should not be equated with either a low or high risk. Organisms 

identified to the genus or higher taxonomic level, are not analyzed further, even though 

individual species within those taxonomic groups are potential pests that may or may not occur 

within the United States. Pests in this category were: Tarsonemus sp., Aonidiella sp., 

Colletotrichum sp. Cladosporium sp., and Phoma sp.
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

10

Table 2. Pests Associated with Citrus spp., Citrus hybrids, and Fortunella spp. in Uruguay. Scientific names in 

bold indicate when a synonym is the name reported from Uruguay. Pests shaded in gray are quarantine pests 

likely to follow the pathway and are analyzed below.

Pest Geographic 

Distribution 2

Host 

association

Quarantine PestFollows 

pathway 3

Plant Part 

Affected

ARTHROPODS

ACARI

Eriophydiae

Aceria sheldoni (Ewing),

Syn: Eriophyes 

sheldoni Ewing

UY (Bentancourt and 

Scatoni, 1999), US 

(CA, FL, HI) (Amrine 

and Stasny, 1994; 

CABI, 2012)

Amrine and 

Stasny, 1994; 

Bentancourt 

and Scatoni, 

1999; CABI, 

2012

No NA NA

Phyllocoptruta oleivora

(Ashmead)

UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (Anciso et 

al., 2002; CABI, 

2012)

Anciso et al., 

2002; 

Bentancourt 

and Scatoni, 

1999; CABI, 

2012

No NA NA

Tarsonemidae

Polyphagotarsonemus 

latus Banks

UY (Bentancourt and 

Scatoni, 1999; Bernal, 

1995), US (CABI, 

2012)

Bentancourt 

and Scatoni, 

1999; Bernal, 

1995; CABI, 

2012

No NA NA 

Tarsonemus sp. 4 UY (PestID, 2008) PestID, 2008 Yes Yes Fruit (PestID, 

2008)

Tenuipalpidae

Brevipalpus obovatus

Donnadieu

UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (Anciso et 

al., 2002; CABI, 

2012) 

Anciso et al., 

2002; 

Bentancourt 

and Scatoni, 

1999; CABI, 

2012

No NA NA

 

2 Abbreviations for Geographic Distribution: UY = Uruguay, US = United States: AL = Alabama, AZ = Arizona, CA = 

California, DC = District of Columbia, FL = Florida, GA= Georgia, HI= Hawaii, ID = Idaho, LA = Louisiana, MS = 

Mississippi, NC = North Carolina, OK = Oklahoma, SC = South Carolina, TX = Texas, VA = Virginia, VI = Virgin 

Islands.

3 NA means Not Applicable. For non-quarantine pests, we did not include pathway and plant part information. 

4 One interception of Tarsonemus sp. was associated with Citrus fruit considered to be of Uruguayan origin. PestID indicates 

that this was intercepted from permit cargo, but this must be in error since no permit cargo shipments are yet allowed from 

Uruguay. The citrus intercepted were likely not commercial export products, but were locally grown for consumption. The 

precise origin of intercepted items is uncertain since it may have originated in any country previously visited by the 

passenger.
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

11

Pest Geographic 

Distribution 2

Host 

association

Quarantine PestFollows 

pathway 3

Plant Part 

Affected

Brevipalpus phoenicis

Geijskes

UY (Bentancourt and 

Scatoni, 1999), US 

(DC, FL, TX, HI) 

(Anciso et al., 2002; 

CABI, 2012)

Anciso et al., 

2002; 

Bentancourt 

and Scatoni, 

1999; CABI, 

2012)

No NA NA

Tetranychidae

Bryobia rubrioculus 

(Scheuten)

UY (Bentancourt and 

Scatoni, 1999; Bolland 

et al., 1998), US 

(Bolland et al., 1998; 

Bolland et 

al., 1998

No NA NA

Eutetranychus banksi

Mc Gregor

UY (Bentancourt and 

Scatoni, 1999: Bolland 

et al., 1998), US (TX) 

(Anciso et al., 2002; 

Bolland et al., 1998)

Anciso et al., 

2002; 

Bentancourt 

and Scatoni, 

1999; 

Bolland et 

al., 1998

No NA NA

Panonychus ulmi Koch UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (CABI, 

2007; Bolland et al., 

1998)

CABI, 2012; 

Bolland et 

al., 1998

No NA NA

Tetranychus 

cinnabarinus

(Boisduval)

UY (Bentancourt and 

Scatoni, 1999; Bolland 

et al., 1998), US (CA, 

HI, TX) (CABI, 2012; 

Bolland et al., 1998)

Bentancourt 

and Scatoni, 

1999: 

Bolland et 

al., 1998; 

CABI, 2012

No NA NA

Tetranychus mexicanus 

(McGregor)

UY (Bentancourt and 

Scatoni, 1999; Bolland 

et al., 1998), US 

(Bolland et al., 1998)

Bentancourt 

and Scatoni, 

1999; 

Bolland et 

al., 1998; 

CABI, 2012

No NA NA

Tetranychus urticae 

Koch

UY (Bentancourt and 

Scatoni, 1999; Bolland 

et al., 1998), US 

(Bolland et al., 1998; 

CABI, 2012)

Bentancourt 

and Scatoni, 

1999; 

Bolland et 

al., 1998; 

CABI, 2012

No NA NA
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

12

Pest Geographic 

Distribution 2

Host 

association

Quarantine PestFollows 

pathway 3

Plant Part 

Affected

Coleoptera: Cerambycidae

Ancylocera cardinalis

(Dalman)

UY (Monné and 

Hovore, 2005; Duffy, 

1960) 

Bentancourt 

and Scatoni, 

1999; Duffy, 

1960

Yes No Twigs, 

branches, 

stems 

(Bentancourt 

and Scatoni, 

1999), items 

(Borror et al., 

1989)

Diploschema 

rotundicolle (Serville)

UY (Bentancourt & 

Scatoni, 1999; Monné, 

2005)

Bentancourt 

& Scatoni, 

1999

Yes No Twigs, 

branches, 

stems 

(Bentancourt 

and Scatoni, 

1999)

Rhopalophora collaris

(Germar)

UY (Monné and 

Hovore, 2002)

Duffy, 1960 Yes No Wood (Duffy, 

1960)

Stenodontes spinibarbis

(L.)

UY (SandovalClavería, 2005)Duffy, 1960 Yes No Wood (Duffy, 

1960)

Trachyderes striatus (F.) UY (Duffy, 1960; 

Rinderknecht, 2005)

Duffy, 1960 Yes No Wood (Duffy, 

1960)

Trachyderes thoracicus 

(Olivier) Syn:

Retrachyderes 

thoracicus (Ol.) 

UY (Bentancourt and 

Scatoni, 1999; 

Rinderknecht, 2005)

Bentancourt 

and Scatoni, 

1999; Duffy, 

1960

Yes No Wood (Duffy, 

1960), twigs, 

trunk 

(Bentancourt 

and Scatoni, 

1999)

Coleoptera: Chrysomelidae

Diabrotica significata 

Grahan

UY (Bentancourt and 

Scatoni, 1999)

Bentancourt 

and Scatoni, 

1999

Yes No 5Fruits, 

flowers, 

leaves, roots, 

stems, 

(Cabrera 

Walsh, 2003)

 

5 Adults of Diabrotica feed on leaves, fruit surfaces, and flowers. They are highly mobile, capable of flight, and are not 

expected to remain on fruit after harvest and packing (Cabrera Walsh, 2003). The larvae are pests on roots, especially 

maize (CABI, 2007). Thus, they are unlikely to follow the pathway. 
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

13

Pest Geographic 

Distribution 2

Host 

association

Quarantine PestFollows 

pathway 3

Plant Part 

Affected

Diabrotica speciosa

(Germar)

UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012

Bentancourt 

and Scatoni, 

1999; CABI, 

2012

Yes No 6Fruits, 

flowers, 

leaves, roots, 

stems, whole 

plants 

(Cabrera 

Walsh, 2003)

Coleoptera: Curculionidae

Naupactus 

xanthographus 

(Germar)

UY (Bentancourt and 

Scatoni, 1999)

CABI, 2012; 

Bentancourt 

and Scatoni, 

1999

Yes No 6Leaves, fruit, 

roots, shoots 

(Whitehead 

and Whittle, 

1985)

Pantomorus cervinus 

(Boheman)

UY (CABI, 2012; 

Wibmer and O'Brien, 

1986), US (CABI, 

2012) 

CABI, 2012 No NA NA

Rhynchophorus 

palmarum (Linnaeus)

UY (CABI, 2012) CABI, 2012 Yes No7Fruit (EPPO, 

2005a)

Coleoptera: Platypodidae

Megaplatypus mutatus 

(Chapuis) (syn:

Platypus mutatus 

(Chapuis), P. sulcatus

(Dejean))

UY (EPPO, 2004; 

Alfaro, 2007)

EPPO, 2004; 

Alfaro et al., 

2007

Yes No Wood (EPPO, 

2004)

Coleoptera: Scolytidae

Xyleborus volvulus

(Fabricius)

UY (CABI, 2012; 

PEET, 2009), US 

(CABI, 2012) 

CABI, 2012 No No Wood, stems, 

bark (CABI, 

2012)

Diptera: Tephritidae

Anastrepha fraterculus

Wiedemann

UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012; EPPO, 2008a ), 

US (TX) 8(CABI, 

2012; EPPO, 2008a)

Bentancourt 

and Scatoni, 

1999; CABI, 

2012

Yes Yes 9Fruit (CABI, 

2012)

 

6 Only adults feed on the fruit surface. Adults are highly mobile and are not expected to remain on the fruit through harvest.

7 Only Rhynchophorus palmarum adults feed on the surfaces of citrus fruit. These adult insects are large, conspicuous (black, 

4–5 cm in length, approx. 1.4 cm wide, weigh 1.6–2 g), and highly mobile (EPPO, 2005a), and therefore are highly 

unlikely to remain on fruit after harvest and commercial processing.

8 Weems (Weems, 2002) included south Texas in the distribution of A. fraterculus. However the USDA has informed EPPO 

that A. fraterculus does not occur in the United States. Pests Not Known to Occur No. 18 (INKTO/PINKTO, 2002) 

explains that the records in Texas are a distinct form of the species, with different host preferences and possibly 

morphology.
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

14

Pest Geographic 

Distribution 2

Host 

association

Quarantine PestFollows 

pathway 3

Plant Part 

Affected

Ceratitis capitata

(Wiedemann)

UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012) US (HI), CA, 

TX, and FL 

(eradicated) (CABI, 

2012; EPPO, 2005b

Bentancourt 

and Scatoni, 

1999; CABI, 

201211

Yes Yes Fruit (CABI, 

2012)

Hemiptera: Aleyrodidae

Aleurocanthus woglumi 

Ashby

UY (PestID, 2008; 

Evans, 2006), US (FL) 

(Nguyen et al., 2007) 

(HI, TX) (CABI, 

2012)

Nguyen et 

al., 2007

Yes No Leaves 

(CABI, 2012)

Aleurothrixus howardi 

(Quaintance) 

[=Aleurothrixus 

floccusus (Maskell)]

UY (Bentancourt and 

Scatoni, 1999), US 

(CA, FL, TX, HI) 

(CABI, 2012; 

Nearctica, 2007)

Bentancourt 

and Scatoni, 

1999; 

Timmer and 

Duncan, 

1999; CABI, 

2012

No NA NA

Dialeurodes citri

(Ashmead)

UY (Bentancourt and 

Scatoni, 1999, US 

(CABI, 2012; 

Nearctica, 2007)

Bentancourt 

and Scatoni, 

1999; CABI, 

2012; 

Timmer and 

Duncan, 

1999 

No NA NA

Dialeurodes citrifolii 

(Morgan)

UY (Bentancourt and 

Scatoni, 1999), US 

(CABI, 2012; 

Nearctica, 2007)

Bentancourt 

and Scatoni, 

1999; CABI, 

2012

No NA NA

Paraleyrodes citri 

Bondar

UY (Bentancourt and 

Scatoni, 1999), US 

(TX) (Anciso et al., 

2002)

Bentancourt 

and Scatoni, 

1999; Evans, 

2006

Yes No Leaves 

(Bentancourt 

and Scatoni, 

1999)

Hemiptera: Aphididae

Aphis fabae (Scopoli) UY, US (CABI, 2012) CABI, 2012 No NA NA

 

9 Citrus limon (not fully mature) are not considered hosts of A. fraterculus, however other Citrus species are hosts, thus for 

Citrus as a group, A. fraterculus is considered to follow the pathway.
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

15

Pest Geographic 

Distribution 2

Host 

association

Quarantine PestFollows 

pathway 3

Plant Part 

Affected

Aphis gossypii Glover UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (CABI, 

2012; Nearctica, 2007)

Anciso et al., 

2002; 

Bentancourt 

and Scatoni, 

1999; CABI, 

2012

No NA NA

Aphis spiraecola Patch UY (Bentancourt and 

Scatoni, 2002; CABI, 

2012), US (CABI, 

2012)

Anciso et al., 

2002; 

Bentancourt 

and Scatoni, 

2002; CABI, 

2012

No NA NA

Aulacorthum solani

Kaltenbach

UY (Bentancourt and 

Scatoni, 2002), US 

(Nearctica, 2007)

Bentancourt 

and Scatoni, 

2002; CABI, 

2012

No NA NA

Brachycaudus helichrysi

Kaltenbach

UY (Bentancourt and 

Scatoni, 1999), US 

(CA, ID) (CABI, 

2012; Nearctica, 2007)

CABI, 2012 No NA NA

Macrosiphum 

euphorbiae (Thomas) 

UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (CABI, 

2012; Nearctica, 2007) 

Bentancourt 

and Scatoni, 

1999; CABI, 

2012

No NA NA

Myzus persicae Sulzer UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012); US (CABI, 

2012; Nearctica, 2007 

)

Bentancourt 

and Scatoni, 

1999; CABI, 

2012

No NA NA

Rhopalosiphum maidis

(Fitch)

UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (Nearctica, 

2007; CABI, 2012)

CABI, 2012 No NA NA

Toxoptera aurantii

Boyer de Fonscolombe

UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (CABI, 

2012; Nearctica, 2007)

Bentancourt 

and Scatoni, 

1999; CABI, 

2012

No NA NA

Toxoptera citricidus 

(Kirkaldi)

UY (Bentancourt and 

Scatoni, 1999); US 

(FL, HI) (CABI, 2012; 

Nearctica, 2007)

CABI, 2012 Yes No Leaves, flower 

buds (CABI, 

2012)
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

16

Pest Geographic 

Distribution 2

Host 

association

Quarantine PestFollows 

pathway 3

Plant Part 

Affected

Hemiptera: Cicadellidae

Ceresa ustulata

Fairmaire 10

UY (Museo Virtual de 

la Biodiversidad, 

2008; de Andrade, 

2004)

de Coll et al., 

1998

Yes No Leaves, shoots 

(de Coll et al., 

1998)

Ciminius platensis 

(Berg)

UY (Remes-Lenicov 

et al., 1999)

RemesLenicov et 

al., 1999

Yes No Leaves 

(Ferreira et al., 

2003)

Frequenamia 

spiniventris 

Linnavuori & DeLong 

(Syn.: Bahita 

spiniventris 

Linnavuori)10

UY (Rocha Zanol, 

2003)

de Coll et al., 

1998; Beltrán 

et al., 2004

Yes No Leaves, shoots 

(Beltrán et al., 

2004; de Coll 

et al., 1998)

Hemiptera: Coccidae

Ceroplastes grandis 

Hempel

UY (Bentancourt and 

Scatoni, 1999)

Ben-Dov et 

al., 2007; 

Bentancourt 

and Scatoni, 

1999

Yes No Stems, twigs, 

leaves 

(Bentancourt 

and Scatoni, 

1999)

Ceroplastes rusci (L.) UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (FL) 

(CABI, 2012; BenDov et al., 2007; 

Miller and Miller, 

2003)

Ben-Dov et 

al., 2007; 

Bentancourt 

and Scatoni, 

1999; CABI, 

2012; Miller 

and Miller, 

2003 

Yes No Leaves,stems, 

branches 

(CABI, 2012)

Ceroplastes sinensis Del 

Guercio

UY (Bentancourt and 

Scatoni, 1999), US 

(CA, NC, VA) (Miller 

and Miller, 2003; 

Nearctica, 2007; 

Stimmel, 1998) 

Ben-Dov et 

al., 2007; 

Bentancourt 

and Scatoni, 

1999; Miller 

and Miller, 

2003; Qin et 

al., 1994; 

Stimmel, 

1998

Yes No Leaves, stems 

(Stimmel, 

1998) 

 

10 This species is a potential vector of CVC strains of Xylella fastidiosa (de Coll et al., 1998).
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

17

Pest Geographic 

Distribution 2

Host 

association

Quarantine PestFollows 

pathway 3

Plant Part 

Affected

Coccus hesperidum L. UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (CABI, 

2012; Miller and 

Miller, 2003; 

Nearctica, 2007)

Anciso et al., 

2002; 

Bentancourt 

and Scatoni, 

1999; CABI, 

2012

No NA NA

Coccus perlatus

(Cockerell) Syn: 

Parthenolecanium

perlatum (Cockerell)

UY (Bentancourt and 

Scatoni, 1999)

Ben-Dov et 

al., 2007; 

Bentancourt 

and Scatoni, 

1999

Yes No Leaves 

(Bentancourt 

and Scatoni, 

1999) 

Eulecanium perinflatum 

(Cockerell)

UY (Ben-Dov et al., 

2007; Bentancourt and 

Scatoni, 1999)

Ben-Dov et 

al., 2007; 

Bentancourt 

and Scatoni, 

1999

Yes No Branches 

(Bentancourt 

and Scatoni, 

1999)

Parthenolecanium 

persicae (Fabricius)

UY (CABI, 2012; 

Bentancourt and 

Scatoni, 1999), US 

(CABI, 2012; Miller 

and Miller, 2003; BenDov et al., 2007; 

Nearctica, 2007)

CABI, 2012; 

Ben-Dov et 

al., 2007

No NA NA

Saissetia coffeae

(Walker)

UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (Ben-Dov 

et al., 2007; CABI, 

2012; Miller and 

Miller, 2003; 

Nearctica, 2007) 

Ben-Dov et 

al., 2007; 

CABI, 2012

No NA NA

Saissetia oleae (Olivier) UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (Ben-Dov 

et al., 2007; CABI, 

2012; Miller and 

Miller, 2003; 

Nearctica, 2007)

Ben-Dov et 

al., 2007; 

Bentancourt 

and Scatoni, 

1999; CABI, 

2012

No NA NA

Hemiptera: Diaspididae

Abgrallaspis cyanophylli

(Signoret) 

[=Hemiberlesia 

cyanophylli]

UY (Watson, 2005), 

US (Ben-Dov et al., 

2007)

Watson, 

2005

No NA NA
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

18

Pest Geographic 

Distribution 2

Host 

association

Quarantine PestFollows 

pathway 3

Plant Part 

Affected

Aonidiella aurantii

(Maskell)

UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (CABI, 

2012; Miller, 2005; 

Nearctica, 2007)

Anciso et al., 

2002; 

Asplanato 

and García 

Marí, 2002; 

Bentancourt 

and Scatoni, 

1999; CABI, 

2012

No NA NA

Aonidiella sp.11 UY (PestID, 2008) PestID, 2008 Yes Yes Fruit (PestID, 

2008)

Aspidiotus nerii Bouché UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (CABI, 

2012; Miller, 2005; 

Nearctica, 2007)

Bentancourt 

and Scatoni, 

1999; CABI, 

2012

No NA NA

Chrysomphalus aonidum

(Linnaeus)

UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (CABI, 

2012; Miller, 2005; 

Nearctica, 2007)

Anciso et al., 

2002; CABI, 

2012; 

Bentancourt 

and Scatoni, 

1999 

No NA NA

Chrysomphalus 

dictyospermi (Morgan)

UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (CABI, 

2012; Miller, 

2005;Nearctica, 2007 

Bentancourt 

and Scatoni, 

1999; CABI, 

2012

No NA NA

Diaspidiotus perniciosus

(Comstock) [Syn: 

Quadraspidiotus 

perniciosus

(Comstock)] 

UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012; Ben-Dov et al., 

2007), US (Ben-Dov 

et al., 2007; CABI, 

2012)

Ben-Dov et 

al., 2007

No NA NA

Hemiberlesia rapax

(Comstock)

UY (Bentancourt and 

Scatoni, 1999; BenDov et al., 2007), US 

(Ben-Dov et al., 2007)

PestID, 

2012; BenDov et al., 

2007

No NA NA

 

11 Two interceptions of Aonidiella sp. were associated with citrus fruit considered to be of Uruguayan origin. The citrus 

intercepted were not commercial export products, but likely were locally grown for consumption. The precise origin of 

intercepted items is uncertain since it may have originated in any country previously visited by the passenger. 
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

19

Pest Geographic 

Distribution 2

Host 

association

Quarantine PestFollows 

pathway 3

Plant Part 

Affected

Lepidosaphes beckii 

(Newman)

UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012; PestID, 2008), 

US (CABI, 2012; 

Miller, 2005) 

Anciso et al., 

2002; 

Bentancourt 

and Scatoni, 

1999; CABI, 

2012

No NA NA

Lepidosaphes gloverii 

(Packard)

UY (Bentancourt and 

Scatoni, 1999), US 

(CABI, 2012; Miller, 

2005) 

CABI, 2012; 

Bentancourt 

and Scatoni,

1999

No NA NA

Lopholeucaspis 

cockerelli (Grandpré 

& Charmoy)

UY, US (Ben-Dov et 

al., 2007) 17

Ben-Dov et 

al., 2007

No NA NA

Parlatoria cinerea

Hadden

UY (PestID, 2012 12) Watson, 

2005

Yes Yes13 Stems, 

branches, 

leaves, fruit, 

roots (rarely) 

(Watson, 

2005)

Parlatoria pergandii 

Comstock

UY (PestID, 2012 14), 

US (CABI, 2012)

CABI, 2012 No NA NA

Parlatoria ziziphi

(Lucas)

UY (PestID, 2012 15), 

US (FL, HI, MS) 

(CABI, 2012)

CABI, 2012 Yes16 Yes Fruit, leaves, 

stems (CABI, 

2012)

Pseudaonidia 

trilobitiformis (Green)

UY, US (FL) (BenDov et al., 2007) 17Ben-Dov et 

al., 2007; 

CABI, 2012

Yes No Leaves 

(Watson, 

2005)

Pseudaulacaspis 

pentagona (Targioni 

Tozzetti)

UY (Bentancourt and 

Scatoni, 1999; BenDov et al., 2007), US 

(Ben-Dov et al., 2007)

Ben-Dov et 

al., 2007

No NA NA

 

12 Parlatoria cinerea was intercepted at U.S. ports of entry associated with citrus from 1985 to the present (PestID, 2012).

13 Parlatoria cinerea was not analyzed further due to the very low likelihood of establishment of armored scales (Zlotina and 

Hennessey, 2007).

14 Parlatoria pergandii was intercepted at U.S. ports of entry associated with citrus from 1985 to the present (PestID, 2012).

15 Parlatoria ziziphi was intercepted at U.S. ports of entry associated with citrus in baggage and ships’ stores 16 times from 

1985 to the present (PestID, 2012). Parlatoria ziziphi was not further analyzed because, although armored scales may 

enter on commercial fruit for consumption, they are not expected to become established (Miller, 1985; Zlotina and 

Hennessey, 2007).

16 This is a quarantine significant species with limited distribution in the United States and is being considered by APHIS for 

official control (NIS, 2006). However, we did not analyze it further due to the very low likelihood of establishment for 

armored scales (Zlotina and Hennessey, 2007).

17 According to personal communication (Scatoni, 2007), Uruguay reports that this pest is not present. They also dispute the 

reference given by Ben-Dov et al. (2007) as not specific enough to support its presence in Uruguay.
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

20

Pest Geographic 

Distribution 2

Host 

association

Quarantine PestFollows 

pathway 3

Plant Part 

Affected

Unaspis citri (Comstock) UY (Bentancourt and 

Scatoni, 1999), US 

(CABI, 2012; Miller, 

2005) 

Bentancourt 

and Scatoni, 

1999; CABI, 

2012

No NA NA

Hemiptera: Lecanodiaspididae

Lecanodiaspis dendrobii

(Douglas)

UY( Ben-Dov et al., 

2007) 17

Ben-Dov et 

al., 2007

Yes No Branches, 

trunk (Chiesa 

Molinari, 

1948)

Hemiptera: Margarodidae

Icerya purchasi Maskell UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (CABI, 

2012; Nearctica, 2007)

Anciso et al., 

2002; 

Bentancourt 

and Scatoni, 

1999; CABI, 

2012

No NA NA

Hemiptera: Pentatomidae

Edessa meditabunda

(Fabricius)

UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012) 

Bentancourt 

and Scatoni, 

1999; CABI, 

2012

Yes No 18 Flowers, 

leaves, stems, 

fruit, seeds 

(CABI, 2012)

Nezara viridula

(Linnaeus)

UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (CABI, 

2012; Nearctica, 2007)

Bentancourt 

and Scatoni, 

1999; CABI, 

2012

No NA NA

Hemiptera: Pseudococcidae

Dysmicoccus brevipes

(Cockerell)

UY (Ben-Dov et al., 

2007), US (Ben-Dov 

et al., 2007; CABI, 

2012)

Ben-Dov et 

al., 2007; 

CABI, 2012

No NA NA

Phenacoccus tucumanus

Granara de Willink

UY (Ben-Dov et al., 

2007)

Ben-Dov et 

al., 2007

Yes No Leaves (Culik 

et al., 2006)

Planococcus citri (Risso) UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (CABI, 

2012; Miller, 2005; 

Nearctica, 2007)

Anciso et al., 

2002; 

Bentancourt 

and Scatoni, 

1999; CABI, 

2012; 

Granara de 

Willink et 

al., 1997

No NA NA

 

18 This pest is not expected to survive post-harvest cleaning, chemical dip, and waxing.
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

21

Pest Geographic 

Distribution 2

Host 

association

Quarantine PestFollows 

pathway 3

Plant Part 

Affected

Planococcus minor

(Maskell)

UY (Bentancourt and 

Scatoni, 1999), US 

(CABI, 2012)

Bentancourt 

and Scatoni, 

1999; CABI, 

2012; 

Granara de 

Willink et 

al., 1997

No No 19 Fruit, flowers, 

leaves (Pena 

et al., 2002) 

Pseudococcus 

longispinus Targioni

UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (CABI, 

2012; Miller, 2005; 

Nearctica, 2007)

Bentancourt 

and Scatoni, 

1999; CABI, 

2012

No NA NA

Pseudococcus viburni

Signoret (Syn: 

Pseudococcus affinis

Maskell)

UY (Bentancourt and 

Scatoni, 1999), US 

(CABI, 2007; Miller, 

2005)

CABI, 2007; 

Granara de 

Willink et 

al., 1997

No NA NA

Hemiptera: Psyllidae

Diaphorina citri

Kumayama

UY (Bentancourt and 

Scatoni, 1999; CABI, 

2007), US (AL, AZ, 

CA, Fl, GA, HI, LA, 

MS, SC, TX)) (CABI, 

2012; Timmer and 

Duncan, 1999; 7CFR 

§ 319.19, 2012)

Anciso et al., 

2002; 

Bentancourt 

and Scatoni, 

1999; CABI, 

2012; 

Timmer and 

Duncan, 

1999

Yes No 20 Leaves , 

shoots, fruit 

(CABI, 2012)

Hymenoptera: Formicidae

Acromyrmex lundi 

(Guérin)

UY (Bernal, 1995; 

CABI, 2007)

Bernal, 1995; 

CABI, 2007

Yes No Leaves, whole 

saplings 

(Bernal, 1995) 

Atta sexdens Linnaeus UY, US (AZ) 

Bentancourt and 

Scatoni, 1999; CABI, 

2012;Weber, 1969)

CABI, 2012 Yes No 25 Leaves, whole 

plant (CABI, 

2012)

Linepithema humile

(Mayr) [=

Iridomyrmez humilis]

UY (Wild, 2004), US 

(CABI, 2012)

Haney et al., 

1987

No NA NA

 

19 Surface-feeding mites, mealy bugs, and thrips are not expected to survive post-harvest cleaning, chemical dip and waxing.

20 Surface feeders are not expected to remain associated with the commodity or the pathway through washing with soap, 

brushing, drying, waxing, and culling, which are part of standard commercial processing on the packing line.
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

22

Pest Geographic 

Distribution 2

Host 

association

Quarantine PestFollows 

pathway 3

Plant Part 

Affected

Solenopsis invicta 

(Buren)

UY (Folgarait et al., 

2008), US (CABI, 

2012)

CABI, 2012 Yes 21 No20 Fruit, leaves, 

roots, seeds, 

vegetative 

organs, whole 

plant (CABI, 

2012)

Lepidoptera: Gracillariidae

Phyllocnistis citrella

Stainton

UY (Buenahora, 1999; 

Bentancourt and 

Scatoni, 1999), US 

(Restricted 

distribution in AL, 

CA, FL, LA, TX) 

(CABI, 2012)

Anciso et al., 

2002; 

Bentancourt 

and Scatoni, 

1999; 

Buenahora, 

1999; CABI, 

2012

Yes No Leaves 

(CABI, 2012)

Lepidoptera: Noctuidae

Agrotis ipsilon 

(Hufnagel)

UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (CABI, 

2012; Nearctica, 2007) 

CABI, 2012 No NA NA

Helicoverpa zea 

(Boddie)

UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (CABI, 

2012; Nearctica, 2007) 

CABI, 2012 No NA NA

Peridroma saucia 

(Hubner)

UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (CABI, 

2012; Nearctica, 2007) 

CABI, 2012 No NA NA

Spodoptera eridania 

Stoll

UY (Bentancourt and 

Scatoni, 1999), US 

(CABI, 2012; 

Nearctica, 2007)

CABI, 2012 No NA NA

Spodoptera frugiperda J.

E. Smith

UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (CABI, 

2012; Nearctica, 2007) 

CABI, 2007 No NA NA

 

21 Solenopsis invicta is non-reportable if commodity destination is AL, AR, FL, GA, LA, MS, NC, SC, or TX, (PestID, 

2008). It is reportable if destined for states other than those listed.This pest on Citrus is highly unlikely to survive postharvest cleaning, chemical dip, and waxing, considering the type of damage caused on other hosts, such as apples and 

pears.
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

23

Pest Geographic 

Distribution 2

Host 

association

Quarantine PestFollows 

pathway 3

Plant Part 

Affected

Trichoplusia ni (Hubner) UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (CABI, 

2012; Nearctica, 2007) 

CABI, 2007 No NA NA

Lepidoptera: Papilionidae

Heraclides anchisiades 

capys (Hubner) Syn: 

Papilio anchisiades 

capys (Hubner)

UY (Bentancourt and 

Scatoni, 2006)

Bentancourt 

and Scatoni, 

2006; Opler 

et al., 2006

Yes No Leaves, stems 

(Young et al., 

1986)

Heraclides thoas 

brasiliensis 

(Rothschild & Jordan).

Syn: Papilio thoas 

brasiliensis Rothschild 

& Jordan

UY (Bentancourt and 

Scatoni, 2006)

Bentancourt 

and Scatoni, 

2006; Opler 

et al., 2006

Yes No Leaves 

(Jeppson, 

1989)

Papilio thoas 

thoantiades 

(Burmeister)

UY (Savela, 2008) Chiesa 

Molinari, 

1948

Yes No Leaves 

(Chiesa 

Molinari, 

1948)

Lepidoptera: Psychidae

Oiketicus platensis Berg UY (Bentancourt and 

Scatoni, 1999)

Bentancourt 

and Scatoni, 

1999

Yes No Leaves 

(Bentancourt 

and Scatoni, 

1999)

Lepidoptera: Pyralidae

Amyelois transitella 

(Walker)

UY(Bentancourt and 

Scatoni, 1999), US 

(CA) (CABI, 2007)

PestID, 

2008; CABI, 

2007

No NA NA

Cryptoblabes gnidiella 

Milliere

UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012)

Bentancourt 

and Scatoni, 

1999; 

Bentancourt 

and Scatoni, 

2006 22; 

CABI, 2012

Yes Yes 23 Fruit, leaves, 

stems (CABI, 

2012)

 

22 Although it is polyphagous, in Uruguay C. gnidiella was found on limited hosts, attacking grapes, and occasionally Citrus

(Bentancourt and Scatoni, 2006). It was never found during DGSA surveys in commercial citrus production areas.

23 Cryptoblabes gnidiella is an internal fruit feeder, which occasionally bores into citrus fruit causing fruit drop (CABI, 2007; 

SINAVIMO, 2005a). Moore (2003) noted that C. gnidiella will usually attack smaller lemons and does not finish the life 

cycle on fruit, it is unclear how C. gnidiella pupates in other Citrus sp.
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

24

Pest Geographic 

Distribution 2

Host 

association

Quarantine PestFollows 

pathway 3

Plant Part 

Affected

Lepidoptera: Tortricidae

Bonagota cranaodes

(Meyrick)

UY (Bentancourt and 

Scatoni, 1999)

Bentancourt 

and Scatoni, 

1999; 

Robinson et 

al., 2007

Yes No 24 Leaves, fruit 

(Bentancourt 

and Scatoni, 

1999)

Gymnandrosoma 

aurantianum (Lima)

[Syn. Ecdytolopha 

aurantiana, 

Ecdytolopha 

aurantiana]

UY (Bentancourt and 

Scatoni, 1999)

Bentancourt 

and Scatoni, 

1999; CABI, 

2012

Yes Yes 25 Fruit 

(SINAVIMO, 

2005b)

Thysanoptera: Thripidae

Frankliniella 

occidentalis

(Pergande)

UY (Bentancourt and 

Scatoni, 1999; CABI, 

2012), US (CABI, 

2012; Nearctica, 2007)

Bentancourt 

and Scatoni, 

1999; CABI, 

2012

No NA NA

Heliothrips 

haemorrhoidalis 

Bouché

UY (Bentancourt and 

Scatoni, 1999 CABI, 

2012), US (CABI, 

2012; Nearctica, 2007)

Bentancourt 

and Scatoni, 

1999; CABI, 

2012)

No NA NA

FUNGI

Athelia rolfsii (Curzi) Tu 

& Kinbr. [Syn. 

Corticium rolfsii; 

Anamorph Sclerotium 

rolfsii Sacc.]

[Basidiomycetes: 

Polyporales]

UY (DGSA, 2001a), 

US (CABI, 2012; Farr 

et al., 2008)

CABI, 2012; 

Farr et al., 

2008; 

Timmer et 

al., 2000

No NA NA

Alternaria citri Ellis and 

N. Pierce 

[Ascomycetes: 

Pleosporales]

UY(Koch de Brotos et 

al., 1981), US (Farr et 

al., 2008)

Farr et al., 

2008; Koch 

de Brotos et 

al., 1981

No NA NA

Alternaria alternata Fr. 

(Keissler) pv. citri

Solel [Ascomycetes: 

Pleosporales]

UY (Farr et al., 2008), 

US (CABI, 2012; Farr 

et al., 2008; Timmer et 

al., 1998)

Farr et al., 

2008; 

Timmer et 

al., 1998

No NA NA

 

24 This pest on Citrus is not expected to survive post-harvest cleaning, chemical dip, and waxing, considering the type of 

damage caused on other hosts, such as apples and pears.

25 Gymnandrosoma aurantianum was found in isolated fruits from domestic groves in Uruguay (Bentancourt and Scatoni, 

2006). In addition, although larvae develop inside fruit, damaged fruit often rot or drop prematurely limiting the number of 

infested fruit likely to be harvested from commercial citrus groves.
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

25

Pest Geographic 

Distribution 2

Host 

association

Quarantine PestFollows 

pathway 3

Plant Part 

Affected

Aspergillus níger Tiegh. 

[Ascomycetes: 

Eurotiales]

UY (DGSA, 2001b), 

US (Farr et al., 2008;

Timmer et al., 2000)

CABI, 2012; 

Timmer et 

al., 2000

No NA NA

Bionectria ochroleuca 

(Schwein) Schroers & 

Samuels [Syn. Nectria 

ochroleuca (Schwein) 

Berk.] Anamorph

Clonostachys rosea f. 

rosea (Link: Fr.) 

Schroers et al. 

[Ascomycetes: 

Hypocreales]

UY, US (Farr et al., 

2008)

Farr et al., 

2008

No NA NA

Botryosphaeria dothidea

(Moug.) Ces. & De 

Not [Syn. B. ribis) 

Grossenb. & Dugar); 

Anamorph

Fusicoccum aesculi 

Corda] [Ascomycetes: 

Dothideales]

UY (Farr et al., 2008), 

US (CABI, 2012; Farr 

et al., 2008)

Farr et al., 

2008; 

Timmer et 

al., 2000

No NA NA

Botryosphaeria ribis

Grossenb. & Duggar 

[Anamorph

Neofusicoccum ribis

(Slippers, Crous & M. 

J. Wingfield) Crous, 

Slippers & A. J. L. 

Phillips]

[Ascomycetes: 

Dothideales]

UY (Koch de Brotos 

et al., 1981), US (Farr 

et al., 2008)

Farr et al., 

2008

No NA NA

Botrytis cinerea Pers.: 

Fr. [Syn. Botryotinia 

fuckeliana (de Bary) 

Whetzel] 

[Ascomycetes: 

Helotiales]

UY (Farr et al., 2008), 

US (CABI, 2012; Farr 

et al., 2008)

CABI, 2012; 

Timmer et 

al., 2000

No NA NA

Capnodium sp. 26 UY (Koch de Brotos 

et al., 1981)

Koch de 

Brotos et al., 

1981

No NA NA

 

26 Organisms identified to the genus, or higher taxonomic level, are not analyzed further.
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

26

Pest Geographic 

Distribution 2

Host 

association

Quarantine PestFollows 

pathway 3

Plant Part 

Affected

Ceratocystis fimbriata

Ellis & Halst. 

[Ascomycetes: 

Microascales]

UY (Farr et al., 2008), 

US (CABI, 2012; Farr 

et al., 2008)

CABI, 2012 No NA NA

Colletotrichum sp. UY (PestID, 2008) PestID, 

2008; 

Yes Yes 27 Flowers, 

Fruits 

(Timmer et al., 

2000)

Cytosporina citriperda

Campan.

[Ascomycetes:

Incertae sedis]

UY (Koch de Brotos 

et al., 1981)

Koch de 

Brotos et al., 

1981

Yes Yes 28 Fruit (Koch de 

Brotos et al., 

1981)

Diaporthe citri F. A. 

Wolf [Anamorph: 

Phomopsis citri H. S. 

Fawcett] 

[Ascomycetes: 

Diaporthales]

UY (PestID, 2008),

US (Anciso et al., 

2002; CABI, 2012; 

Farr et al., 2008)

Anciso et al., 

2002; CABI, 

2012; 

DGSA, 

2004; Farr et 

al., 2008; 

Timmer et 

al., 2000

No NA NA

Elsinoë australis

(Bitancourt & Jenk.) 

[Anamorph: 

Sphaceloma australis

Bitancourt & Jenk.] 

[Ascomycetes: 

Myriangiales]

UY (Koch de Brotos et 

al., 1981; Palm, 2007, 

2008; PestID, 2008), 

US [TX, LA, MS, FL, 

AZ] (USDA APHIS, 

2010b; NAPPO, 2011)

Farr et al., 

2008; 

Timmer et 

al., 2000

Yes Yes Fruit (Timmer 

et al., 2000)

Elsinoё fawcettii Bitanc. 

& Jenkins [Anamorph: 

Spaceloma fawcetti 

var. fawcettii Jenkins] 

[Ascomycetes: 

Myriangiales]

UY (Díaz et al., 1992), 

US (CABI, 2012; Farr 

et al., 2008)

CABI, 2012; 

Díaz et al., 

1992; Farr et 

al., 2008; 

Timmer et 

al., 2000

No NA NA

Fusarium oxysporum

Schlechtendahl 

[Ascomycetes: 

Hypocreales]

UY (Farr et al., 2008), 

et al.,US (CABI, 

2012; Farr et al., 

2008)

CABI, 2012 No NA NA

 

27 Colletrichum spp. are noted by Timmer et al. (2000) as pathogens of citrus flowers. Infections result in young fruit drop, 

but C. accutatum attacks fruit and can follow the pathway. Therefore, the unidentified species of Colletotrichum has the 

potential to follow the pathway, but the level of uncertainty is high. 

28 Cytosporina citriperda was only reported once from Uruguay (Koch de Brotos et al., 1981), and the taxonomic status is not 

very clear. Therefore, this pest was not analyzed further.
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

27

Pest Geographic 

Distribution 2

Host 

association

Quarantine PestFollows 

pathway 3

Plant Part 

Affected

Fusarium solani

(Martius) Sacc. 

Ascomycetes

Hypocreales

UY (DGSA, 2004; 

DGSA, 2005), US 

(CABI, 2007; Farr et 

al., 2008)

CABI, 2007; 

Timmer et 

al., 2000; 

Farr et al., 

2008

No NA NA

Geotrichum citriaurantii (Ferraris) 

Butler Ascomycetes

UY (DGSA, 2005), 

US (Farr et al., 2007)

CABI, 2007; 

Timmer et 

al., 2000; 

Farr et al., 

2008

No NA NA

Glomerella acutata 

Guerber & J.C. Correll 

[Anamorph: 

Colletotrichum 

acutatum Simmonds 

ex Simmonds 

[Ascomycetes: 

Incertae sedis]

UY (CABI, 2012), US 

(CABI, 2012; Farr et 

al., 2008; Timmer et 

al., 2000)

DGSA, 

2004; Farr et 

al., 2008; 

Timmer et 

al., 2000

No NA NA

Glomerella cingulata 

(Stoneman) Spauld. & 

H. Schrenk 

[Anamorph: 

Colletotrichum 

gloeosporioides 

(Penz.) Sacc.] 

[Ascomycetes: 

Incertae sedis]

UY (Farr et al., 2008), 

US (Anciso et al., 

2002; CABI, 2012; 

Farr et al., 2008)

Anciso et al., 

2002; CABI, 

2012; 

DGSA, 

2004; Farr et 

al., 2008; 

Timmer et 

al., 2000

No NA NA

Guignardia citricarpa

Kiely [Anamorph: 

Phyllosticta citricarpa 

(McApline) Aa 

[Ascomycetes: 

Dothideales]

UY (DGSA, 2004; 

PestID, 2008), US 

[FL] (USDA APHIS, 

2010a; 2011)

CABI, 2007; 

DGSA, 

2004; 

Timmer et 

al., 2000 

Yes No29 Bud, Fruit, 

Flower, Stem, 

Leaves 

(Kotzé, 1981; 

Whiteside, 

1965)

 

29 APHIS has recently assessed the risk of fresh and dried fruit of Citrus spp. as a pathway for the introduction of G. 

citricarpa (Citrus Black Spot, or CBS) (USDA, 2010b). We concluded that fresh or dried citrus fruit is not epidemiologically 

significant as a pathway for the introduction of CBS because the combination of conditions required for disease transmission 

from harvested fruit are highly unlikely. We therefore consider that fruit which is commercially harvested and surface treated 

with fungicides prior to shipment is a negligible risk, so analysis of this pathogen was removed from the document.
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

28

Pest Geographic 

Distribution 2

Host 

association

Quarantine PestFollows 

pathway 3

Plant Part 

Affected

Lasiodiplodia 

theobromae (Pat.) 

Griffon & Maubl. Syn: 

Diplodia natalensis

Pole-Evans

Ascomycetes

UY (DGSA, 2003), 

US (CABI, 2012; Farr 

et al., 2008)

CABI, 2012; 

Timmer et 

al., 2000; 

Farr et al., 

2008

No NA NA

Limacinia citri (Briosi & 

Pass.) Sacc. [Syn. 

Capnodium citri

Mont.30 [Ascomycetes: 

Capnodiales]

UY (Koch de Brotos 

et al., 1981), US (as 

Capnodium citri Farr 

et al., 2008)

Farr et al., 

2008

No31 NA NA

Macrophomina 

phaseolina (Tassi) 

Goid [Syn: 

Macrophomina 

phaseoli (Maubl.) F. S. 

Ashby] [Ascomycetes: 

Incertae sedis]

UY (DGSA, 2001c; 

Koch de Brotos et al., 

1981), US (CABI, 

2012; Farr et al., 

2008)

CABI, 2012; 

Farr et al., 

2008 

No NA NA

Mycosphaerella citri

Whiteside [Anamorph: 

Stenella citri-grisea

(F.E. Fisher) Sivan.] 

[Ascomycetes: 

Mycosphaerellales]

UY (DGSA, 2003), 

US (FL, TX) (Anciso 

et al., 2002; CABI, 

2012; Farr et al., 

2008)

Anciso et al., 

2002; CABI, 

2012; 

Timmer et 

al., 2000

No NA NA

Penicillium digitatum 

(Pers.: Fr.) Sacc. 

[Ascomycetes: 

Eurotiales]

UY (Reyes et al., 

1993), US CABI, 

2012; Farr et al., 2008 

CABI, 2012; 

Farr et al., 

2008; Reyes 

et al., 1993; 

Timmer et 

al., 2000

No NA NA

Penicillium italicum

Wehmer 

[Ascomycetes: 

Eurotiales]

UY (Reyes et al., 

1993), US (CA, FL, 

HI) (CABI, 2012; Farr 

et al., 2008)

CABI, 2012; 

Reyes et al., 

1993; 

Timmer et 

al., 2000

No NA NA

 

30 Limacinia citri is a synonym of Capnodium citri according to the Catalogue of Life: 2007 Annual Checklist: Species 

Fungorum (GBIF, 2008), but are currently not listed as synonyms in the USDA Systematic Mycology and Microbiology 

Laboratory online database (Farr et al., 2008).

31 Limacinia citri and Capnodium citri may be synonyms, but the taxonomy of C. citri is not certain (Minnis, 2008); 

therefore, L. citri is not analyzed further.
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

29

Pest Geographic 

Distribution 2

Host 

association

Quarantine PestFollows 

pathway 3

Plant Part 

Affected

Penicillium ulaiense 

Hsieh, Su & Tzean 

[Ascomycetes: 

Eurotiales]

UY (Díaz and Sendra, 

1997), US (CA) 

(Holmes et al., 1994; 

Farr et al., 2008)

Díaz and 

Sendra, 

1997; 

Holmes et 

al., 1994; 

Timmer et 

al., 2000

No NA NA

Phoma sp. UY (PestID, 2008) PestID, 2008 Yes Yes32 Fruit (Timmer 

et al., 2000)

Phytophthora cactorum 

(Lebert & Cohn) J. 

Schröt. [Oomycetes: 

Pythiales]

UY (DGSA, 2002; 

CABI, 2012), US 

(CABI, 2012)

CABI, 2012; 

Farr et al., 

2008 

No NA NA

Phytophthora 

citrophthora (R. E. 

Sm. & E. H. Sm.) 

Leonian [Oomycetes: 

Pythiales]

UY (Koch de Brotos 

et al., 1981), US 

(CABI, 2012; Farr et 

al., 2008)

CABI, 2012; 

Timmer et 

al., 2000

No NA NA

Phytophthora nicotianae 

Breda de Haan [Syn. 

Phytophthora 

parasitica Dast.]

[Oomycetes: 

Pythiales]

UY (Koch de Brotos 

et al., 1981), US 

(CABI, 2012) 

CABI, 2012; 

Timmer et 

al., 2000

No NA NA

Rhizoctonia solani J. G. 

Khun [Teleomorph 

Thanatephorus 

cucumeris (A.B. 

Frank) Donk] 

[Basidiomycetes: 

Ceratobasidiales]

UY (DGSA, 2006; 

Koch de Brotos et al., 

1981), US (CABI, 

2012; Farr et al., 

2008)

CABI, 2012; 

Farr et al., 

2008; Koch 

de Brotos et 

al., 1981

No NA NA

Rosellinia necatrix Prill. 

[Teleomorph] 

[Ascomycetes: 

Xylariales]

UY (CABI, 2012; 

Koch de Brotos et al., 

1981), US (CABI, 

2012)

CABI, 2012; 

Koch de 

Brotos et al., 

1981

No NA NA

BACTERIA and PHYTOPLASMAS

Pseudomonas syringae 

pv. syringae van Hall 

UY, US ( CABI, 

2012)

Timmer et 

al., 2000

No NA NA

 

32 An unidentified species of Phoma was intercepted on fruit at the port of entry (PestID, 2008). 
Pest Risk Assessment for Citrus from Uruguay

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30

Pest Geographic 

Distribution 2

Host 

association

Quarantine PestFollows 

pathway 3

Plant Part 

Affected

Rhizobium radiobacter 

(Beijerinck & van 

Delden ) Young et al. 

[Syn: Agrobacterium 

tumefaciens (Smith & 

Tousend) Conn]

UY (CABI, 2012), US 

(Bradbury, 1986; 

CABI, 2012)

Timmer et 

al., 2000

No NA NA

Xanthomonas citri 

subsp. citri (ex Hasse ) 

Gabriel et al. 33 [Syn. 

X. axonopodis pv. citri

(Vauterin, et al.), X. 

campestris pv. citri

(Hasse) Dye; 

Pseudomonas citri

Hasse] (Citrus canker 

A )

UY (CABI, 2012; 

Koch de Brotos et al., 

1981; PestID, 2008), 

US (FL) (Bradbury, 

1986; CABI, 2012) 

Timmer et 

al., 2000

Yes 34 Yes Fruit, Leaves, 

Stem (CABI, 

2012; Timmer 

et al., 2000)

VIRUSES, VIROIDS, and VIRUS-LIKE PATHOGENS

Citrus cachexia viroid 

Pospiviroidae:

Hostuviroid

UY (Koch de Brotos 

et al., 1981), US 

(CABI, 2007) 

Timmer et 

al., 2000

No NA NA

Citrus exocortis viroid 

Pospiviroidae:

Pospiviroid

UY (Koch de Brotos 

et al., 1981), US () 

CABI, 2012

Timmer et 

al., 2000

No NA NA

Citrus psorosis virus

(CPsV) Ophiovirus

UY (Koch de Brotos 

et al., 1981), US 

(CABI, 2012; Alioto 

et al., 1999)

CABI, 2012; 

Timmer et 

al., 2000

No NA NA

Citrus tristeza virus 

Closteroviridae

UY (CABI, 2012; 

Koch de Brotos et al., 

1981), US (CABI, 

2012)

Anciso et al., 

2002; CABI, 

2012; 

Timmer et 

al., 2000

No NA NA

NEMATODES 

Tylenchulidae

Pratylenchus penetrans

(Cobb, 1917) Filipjev 

& Schuurmans 

Stekhoven

UY, US (CABI, 2012) CABI, 2012 No NA NA

 

33 This is the only Xanthomonas citri (Syn. X. axonopodis) strain currently reported in citrus in Uruguay. Information 

provided by DGSA to APHIS during technical missions 1996-2006.

34 Xanthomonas citri subsp. citri occurs in the United States (FL), but is under official control. 
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

31

Pest Geographic 

Distribution 2

Host 

association

Quarantine PestFollows 

pathway 3

Plant Part 

Affected

Tylenchulus 

semipenetrans Cobb

UY, US 35 (CABI, 

2012)

Anciso et al., 

2002; CABI, 

2012

No NA NA

Table 3. Pests of concern associated with Citrus spp., Citrus hybrids, and Fortunella spp. in citrus production 

regions adjacent to Uruguay, some with disputed previous reports in Uruguay. 

Pest Geographic 

Distribution

Host 

association

Quarantine PestFollows 

pathway 

Plant Part Affected

Xylella fastidiosa 

(Wells, et al.) 

Citrus variegated 

chlorosis strain 

[Syn.: Pecosita, 

declinamiento, 

fruta bolita]

UY (Bove and 

Ayres, 2007; 

Phillips, 2001)36

Timmer et 

al., 2000

Yes Yes Roots, Stems (CABI, 

2012), Fruit and Seed 

(Li et al., 2003)

‘Candidatus 

Liberibacter 

americanus’

BR1(Teixeira et 

al., 2005b)

Teixeira et 

al., 2005b

Yes Yes Vector, vascular tissues, 

including seed (CABI, 

2012; Tatineni et al., 

2008), Possible 

transmission by seed 37

(Graham et al., 2008; 

Hartung et al., 2008; 

Shatters, 2008; Zhou et 

al., 2008)

 

35 This pest was not detected during specific surveys of citrus areas and nurseries in Uruguay (DGSA 2000 – 2007 Nursery 

surveys).

36 These two papers note the presence of X. fastidiosa CVC strains in Uruguay, but neither report was further cited. The 

authors subsequently noted that the reports were not accurate (Bove and Ayres, 2008; Phillips, 2001). Although there are 

concerns about the pathogen since it occurs in neighboring countries, current monitoring and survey methods may not be 

sufficient for the detection of this pathogen because they do not include molecular methods. In addition, climate in 

Uruguay may suppress symptoms (Phillips, 2001). However, evidence is not available to confirm that X. fastidiosa CVC is 

in Uruguay and therefore the pathogen is not analyzed further.

37 This quarantine pest of concern is present in citrus production areas in countries bordering Uruguay, and vectors of this 

pathogen are present in Uruguay, thus additional monitoring measures may be needed to prevent spread of this pathogen. 

We found no evidence that the pathogen occurs in Uruguay, so it is not analyzed in this document. Multiple sources 

indicate that “Ca. Liberibacter” species are seed transmitted, as well as contradictory reports in the same proceedings that 

they are not (Graham et al., 2008; Hartung et al., 2008; Shatters, 2008; Zhou, et al., 2008). Due to this uncertainty and the 

seriousness of the consequences of introduction of “Ca. Liberibacter” species ,we indicated that the pathogen will follow 

the pathway with fruit, pending more conclusive evidence about seed transmission, although the pathway with fruit for 

consumption is not likely to result in the establishment of the pathogens.
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

32

Pest Geographic 

Distribution

Host 

association

Quarantine PestFollows 

pathway 

Plant Part Affected

‘Candidatus 

Liberibacter 

asiaticus’

BR (Lopes et al., 

2007; ColettaFilho et al., 2004; 

Teixeira et al. 

2005a), US 

(Manjunath et al., 

2008) (FL, GA, 

PR, USVI, SC, 

and LA, under 

official control)

(USDA, 2011)

Lopes et al., 

2007; 

ColettaFilho et al., 

2004; 

Teixeira et 

al. 2005a

Yes Yes Vector, vascular tissues, 

including seed (CABI, 

2012; Tatineni et al., 

2008), Possible 

transmission by seed38

(Graham et al., 2008; 

Hartung et al., 2008; 

Shatters, 2008; Zhou et 

al., 2008)

Citrus leprosis virus 

(CiLV-N) 

Rhabdovirus 

(unclassified) 

CiLV-C Cilevirus

proposed (LocaliFabris et al., 2006)

UY39 (Lovisolo, 

2001)

Timmer et 

al., 2000

Yes No40 Leaves, fruit, twigs 

(Lovisolo, 2001; 

Timmer et al., 2000)

Zonate Chlorosis 

Virus-like Disease

UY (Koch de 

Brotos et al., 

1981) 41

Frison and 

Taher, 2000; 

Koch de 

Brotos et al., 

1981; 

Timmer et 

al., 2000

Yes No 42 Fruit, leaves, twigs 

(Frison and Taher, 

2000)

 

38 This quarantine pest of concern is present in citrus production areas in countries bordering Uruguay, and vectors of this 

pathogen are present in Uruguay, thus additional monitoring measures may be needed to prevent spread of this pathogen.

We found no evidence that the pathogen occurs in Uruguay, so it is not analyzed in this document. Multiple sources 

indicate that “Ca. Liberibacter asiaticum” is seed transmitted, as well as contradictory reports in the same proceedings that 

it is not (Graham et al., 2008; Hartung et al., 2008; Shatters, 2008; Zhou, et al., 2008). Due to this uncertainty and the 

seriousness of the consequences of introduction of “Ca. Liberibacter” species, we indicated that the pathogen will follow 

the pathway with fruit, pending more conclusive evidence about seed transmission, although the pathway with fruit for 

consumption is not likely to result in the establishment of the pathogens.

39 Lovisolo (2001) cites old reports of Citrus leprosis virus in Uruguay. However, DGSA has conducted indirect surveys for 

this and other viruses, and has not detected this virus since an extensive freeze killed commercial citrus trees in 1967 

(DGSA, 2008). There is no report on the status of this virus in noncommercial plantings, the vectors are present, and the 

pathogen and vectors are present in neighboring countries (CABI, 2007). Fruit also has been suggested as a pathway 

(Lovisolo, 2001).

40 Citrus leprosis virus (CiLV) was once considered present in United States, but an extensive survey showed that it is absent

(Childers et al., 2003). CiLV is not seed transmitted, symptomatic fruit are likely to be culled at the packinghouse, and 

thus the fruit alone are not considered a pathway for pathogen dissemination. CiLV is vectored by mites in the genus 

Brevipalpus. Two Brevipalpus species, Brevipalpus obovatus and Brevipalpus phoenicis, are present in Uruguay where the 

disease also was once present. The pathogen CiLV and Brevipalpus vectors are present in the neighboring countries of 

Brazil and Argentina, however as the disease is not present in Uruguay we will not analyze mites. 

41 Zonate Chlorosis reports in Uruguay are old, 1941 and 1955 (Koch de Brotos et al., 1981).
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

33

 

42 Zonate Chlorosis has symptomology similar to Citrus Leprosis and is transmitted by Brevipalpus phoenicis (Frison and 

Taher, 2000; Timmer et al., 2000), but has not had the economic impact of CiLV (Timmer et al., 2000). This disease is 

graft transmissible with difficulty (Frison and Taher, 2000). Little information was available and no evidence was 

available to indicate whether or not fruit is a pathway.
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

34

Summary of quarantine pests likely to follow the pathway which were analyzed:

The pests listed below satisfy the defining criteria for a quarantine pest: “a pest of potential 

economic importance to the area endangered thereby, and not yet present there, or present but 

not widely distributed and being officially controlled” (IPPC, 2007b). These pests also satisfy

the defining criteria for following the pathway with the imported commodity: “any means that 

allows entry or spread of a pest (IPPC, 2007b).”

Arthropods

Anastrepha fraterculus (Wiedemann)

Ceratitis capitata (Wiedemann)

Cryptoblabes gnidiella (Millière)

Gymnandrosoma aurantianum (Lima)

Bacteria

Xanthomonas citri subsp. citri (ex Hasse 1915) Gabriel et al. 1989 [Syn. X. axonopodis pv. 

citri (Vauterin, et al.), X. campestris pv. citri (Hasse) Dye] (Citrus canker A)

Fungi

Elsinoë australis (Bitancourt & Jenk)

2.4 Consequences of Introduction

In this portion of the analysis we consider negative outcomes that may occur when the 

quarantine pests identified as following the pathway with Citrus spp., Citrus hybrids, and 

Fortunella spp. from Uruguay are introduced into the continental United States. Potential 

consequences of introduction are rated using five risk elements: climate-host interaction, host 

range, dispersal potential, economic impact, and environmental impact. These elements reflect 

the biology, host range, and climatic/geographic distribution of the pests. For each risk element,

pests are assigned a rating of Low (1 point), Medium (2 points) or High (3 points) based on the 

criteria as stated in the Guidelines for Pathway-Initiated Pest Risk Assessment, Version 5.02 

(PPQ, 2000). A Cumulative Risk Rating is then calculated by summing all risk element values. 

For each pest, the sum of the five risk elements produces a cumulative risk rating for the 

consequences of introduction. This cumulative rating is considered the biological indicator of the 

pest’s potential to cause economic and environmental impacts. We found a cumulative risk rating 

for the Consequences of Introduction for each pest (Table 4).

Anastrepha fraterculus Wiedemann (Diptera: Tephritidae) Risk ratings

Risk Element #1: Climate—Host Interaction

Anastrepha fraterculus ranges from the south of Texas to Argentina (Foote et 

al., 1993), including Uruguay, where it is widespread (CABI, 2007). These areas 

generally correspond to U.S. Plant Hardiness Zones 9 to 11 (PERAL, 2008). 

One or more of its potential hosts occurs in these zones (USDA-NRCS, 2007a). 

Anastrepha fraterculus can become established in at least 3 plant hardiness 

zones, so is rated High. 

High (3)
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35

Anastrepha fraterculus Wiedemann (Diptera: Tephritidae) Risk ratings

Risk Element #2: Host Range

Anastrepha fraterculus is very polyphagous. The preferred hosts are Myrtaceae, 

particularly the Psidium guajava, Eugenia and Syzygium (CABI, 2007). Annona 

cherimola, Citrus, Eugenia, Prunus, Psidium guajava, and Syzygium are major 

hosts (CABI, 2007). Other hosts include: Actinidia chinensis, Annona, Annona 

muricata, Annona squamosa, Averrhoa carambola, Citrus aurantium, Citrus 

limetta, Citrus maxima, Citrus reticulata, Citrus sinensis, Citrus x paradisi, 

Coffea arabica, Coffea liberica, Cydonia oblonga, Diospyros, Diospyros kaki, 

Eriobotrya japonica, Eugenia dombeyi, Eugenia uniflora, Feijoa sellowiana, 

Ficus carica, Fortunella japonica, Fragaria vesca, Inga edulis, Juglans 

neotropica, Juglans regia, Malus, Malus domestica, Mangifera indica, 

Manilkara zapota, Olea europaea subsp. europaea, Persea americana, Pouteria 

obovata, Prunus armeniaca, Prunus dulcis, Prunus persica, Psidium guineense, 

Psidium longipes, Punica granatum, Pyrus, Pyrus communis, Solanum 

quitoense, Spondias, Spondias dulcis, Spondias mombin, Spondias purpurea, 

Syzygium jambos, Syzygium malaccense, Terminalia catappa, Theobroma 

cacao, Vitis vinifera (CABI, 2007). Anastrepha fraterculus attacks multiple 

species among multiple plant families, so we rated it High. 

High (3)

Risk Element #3: Dispersal Potential

Anastrepha fraterculus has a high reproductive capacity; females deposit from 

200 to 400 eggs in host fruits (White and Elson-Harris, 1992). Long-distance 

dispersal has not been reported for adults of A. fraterculus. However, another 

Anastrepha sp., A. ludens, was trapped 135 km away from its origin (Fletcher, 

1989). In international trade, the major means of dispersal to previously uninfested areas is the transport of fruit containing eggs and live larvae. For most 

regions, the most important fruits liable to carry A. fraterculus are Annona, 

Citrus, Fortunella, Malus, mango, peach, and guava (CABI, 2007). The pest has 

both high reproductive potential and can disperse over long distances, so is rated 

High. 

High (3)

Risk Element #4: Economic Impact

Anastrepha fraterculus is the most economically important Anastrepha species 

in Brazil and other South American countries because of its broad host range 

(Foote et al., 1993). In Brazil, it causes severe yield losses in apple, is a major 

pest, and constrains fresh fruit exports to countries with quarantine barriers 

(Sugayama et al., 1996). Anastrepha fraterculus is a quarantine pest for several 

countries and regions including Europe (EPPO, 2008a); thus its introduction 

could result in a loss of foreign markets for American commodities such as 

citrus. Establishment of A. fraterculus in the United States would increase 

production costs in susceptible commodities (EPPO, 2008a). Anastrepha 

fraterculus lowers yield, increases cost of production, and can impact foreign or 

domestic markets, thus we rated it High.

High (3)

Risk Element #5: Environmental Impact

Because it is polyphagous, A. fraterculus can potentially impact numerous 

species listed as Threatened and Endangered (T&E) (50 CFR § 17, 2007). In 

places where it could become established in the continental United States (Zones 

Medium (2)
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36

Anastrepha fraterculus Wiedemann (Diptera: Tephritidae) Risk ratings

9-11), A. fraterculus could impact threatened or endangered species in the same 

genera as current hosts, although they do not directly injure their hosts, so 

impacts should be minimal. One example is Prunus geniculata in Florida 

(USFWS, 2007). If potential T&E plants are considered at the family level, then 

A. fraterculus could impact three additional taxa. Establishment of A. fraterculus

in the United States may require the use of additional control measures such as 

pesticide applications which may have environmental impacts (CABI, 2007). 

The pest is expected to have both direct and indirect impacts on T & E species 

and the environment, thus is rated Medium (2). 

Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) Risk ratings

Risk Element #1: Climate—Host Interaction

Ceratitis capitata is widely distributed in the Mediterranean, South and Central 

America, western Asia (CABI, 2012) and western Australia (Hassan, 1977). The 

area in which it survives has a Mediterranean climate, corresponding to citrus 

growing areas (Magarey et al., 2008). Based on this distribution and the 

geographic range predicted by Vera et al. (2002), we estimated that C. capitata

could establish in U.S. Plant Hardiness Zones 8-11. One or more of its potential 

hosts occur in these zones (USDA-NRCS, 2007a), so we rated C. capitata high.

High (3)

Risk Element #2: Host Range

Ceratitis capitata is recorded on hosts from numerous plant families, including 

Anacardiaceae, Arecaceae, Chrysobalanaceae, Cucurbitaceae, Ebenaceae, 

Lauraceae, Loganiaceae, Malpighiaceae, Meliaceae, Moraceae, Myrtaceae, 

Oleaceae, Podocarpaceae, Rosaceae, Rutaceae, Sapotaceae, Solanaceae and 

Sterculiaceae (CABI, 2012; Thomas et al., 2008; White and Elson-Harris, 

1992). Citrus species vary in their host status for C. capitata, for example, C. 

limon is not considered to be a fruit fly host under certain environmental 

conditions (Vaccaro and Bouvet, 2006; Spittler et al., 1984; Nguyen and Fraser, 

1989; Augier et al., 2008; Gastaminza et al., 2007; Willink et al., 2007). Other 

species of Citrus have not been shown to be non-hosts for C. capitata. The risk 

rating for this element is High.

High (3)

Risk Element #3: Dispersal Potential

Females may deposit up to 22 eggs per day, and as many as 300-800 eggs in a 

lifetime (Thomas et al., 2008; White and Elson-Harris, 1992). Eggs are inserted 

under the skin of host fruit as it begins to ripen (Thomas et al., 2008). There can 

be several overlapping generations each year (Hassan, 1977). There is evidence 

that C. capitata can fly at least 20 km during its two-month lifespan, and larvae 

can be transported over long distances in infested fruit (CABI, 2012). In 

addition, this species may disperse as pupae in soil, or in the growing medium 

accompanying plants (CABI, 2012). This species has a high biotic potential and 

capability for rapid dispersal. We rated it High for this element.

High (3)

Risk Element #4: Economic Impact

Ceratitis capitata is one of the world's most destructive and economically

High (3)
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37

Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) Risk ratings

important fruit pests, due to its wide distribution, ability to tolerate cooler 

climates, and wide host range (Thomas et al., 2008). In some Mediterranean 

countries, C. capitata infests approximately 100 percent of stone fruits (Weems, 

1981). In addition to substantial yield reductions, C. capitata lowers crop values 

by requiring control measures. In Central America, losses of 5 to 15 percent

have been recorded for coffee, as C. capitata infestations increase labor costs 

and reduce bean quality (Enkerlin et al., 1989). In addition to substantial yield 

reductions, C. capitata lowers crop values by requiring costly controls (Thomas 

et al., 2008). Eradication of C. capitata has occurred multiple times in the 

United States, and cost on average $10 million per introduction (USDA-APHISPPD, 2002. It is anticipated that if not eradicated, living with C. capitata could 

result in $1.5 billion in losses annually (USDA-APHIS-PPD, 2002). Ceratitis

capitata is of quarantine significance almost worldwide and countries without 

C. capitata use considerable resources to prevent its introduction. Ceratitis 

capitata is listed by EPPO as an A2 quarantine pest for Europe (Smith et al., 

1997).The introduction of C. capitata into the United States will lead to losses 

of foreign and domestic markets (CABI, 2012). The rating for this risk element 

is High.

Risk Element #5: Environmental Impact

Because C. capitata is a polyphagous pest, there are many closely related native 

Threatened and Endangered (T&E) species (USFWS, 2012) within the same 

host genera and families. The following T&E species are in the genera of known 

hosts of C. capitata: Eugenia haematocarpa, E. koolauensis, E. woodburyana, 

Flueggea neowawraea, Juglans jamaicensis, Opuntia treleasei, Prunus 

geniculata, Santalum freycinetianum var. lanaiense, Scaevola coriacea, 

Solanum drymophilum, S. incompletum, S. sandwicense, and Ziziphus celata

(USFWS, 2012). If potential hosts are considered at the family level, then there 

are an additional 174 T&E species (USFWS, 2012) that C. capitata may

negatively impact across the United States and its territories. However, not all of 

these may occur within the preferred climatic range for C. captitata, and the 

fruit fly does not directly injure the host plant, but affects only the fruit. Because 

of its potential to harm endangered taxa and economically important plants, 

conservation managers, farmers, and horticulturalists would likely need to use 

chemical and/or biological control programs to control populations of C. 

capitata (Weems, 2002). Its introduction and establishment in the United States 

would almost certainly trigger chemical or biological control programs. The 

rating for this risk element is Medium.

High (3)

Cryptoblabes gnidiella Milliere (Lepidoptera: Pyralidae) Risk ratings

Risk Element #1: Climate—Host Interaction

Cryptoblabes gnidiella is polyphagous, we therefore characterized its potential 

U.S. distribution based on climate (CABI, 2012). This moth does best in warm 

climates and cannot survive winters in cooler temperate areas (CABI, 2007). 

Cryptoblabes gnidiella is found in Europe (Austria, Cyprus, France, Greece, 

High (3)
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38

Cryptoblabes gnidiella Milliere (Lepidoptera: Pyralidae) Risk ratings

Italy, Malta, Portugal, and Spain), Asia (India, Israel, Lebanon, Pakistan, 

Thailand, and Turkey), Africa (Egypt, Liberia, Morocco, Nigeria, Sierra Leone, 

and South Africa), the Caribbean (Bermuda), North America (United States--

Hawaii), South America (Argentina, Uruguay), and Oceania (New Zealand) 

(CABI, 2012). We estimated the potential distribution of C. gnidiella using the 

degree-day model reported by Ringenberg et al. (2005). We simulated the 

degree-day model using the North Carolina State University APHIS Plant Pest 

Forecast System (Magarey et al., 2007) predictive modeling system. We 

considered areas where C. gnidiella could complete five generations as 

conducive for permanent establishment (Yehuda et al., 1991). We found that C. 

gnidiella could establish in U.S. Plant Hardiness Zones 6-11 (Figure 1) 

(Magarey et al., 2008). The risk rating for this element is High.

Risk Element #2: Host Range

Cryptoblabes gnidiella is polyphagous and attacks multiple plant species in 

multiple families (CABI, 2007). Examples of hosts C. gnidiella attacks include 

Allium sativum, Annona muricata, Citrus, Coffea, Ficus, Gossypium, Mangifera 

indica, Mespilus, Morus alba, Oryza sativa, Osmanthus, Philodendron, Persea 

americana, Phaseolus, Ricinus communis, Saccharum officinarum, Schinus 

terebinthifolius, Sorghum bicolor, Swietenia, Zea mays, and Vitis (CABI, 2007; 

CABI, 2012). The risk rating for this element is High.

High (3)

Risk Element #3: Dispersal Potential

The moth can have between three and nine generations per year and each female 

can lay an average of 105 eggs (Ringenberg et al., 2005; Wysoki et al., 1993). 

Cryptoblabes gnidiella adults can naturally disperse by flying (Ozturk and Ulusoy, 

2011; CABI, 2012). The risk rating is High.

High (3)

Risk Element #4: Economic Impact

Cryptoblabes gnidiella is a quarantine pest that is not distributed worldwide 

(CABI, 2012) and thus could cause a loss of markets if introduced into the 

United States. In citrus it is an internal feeder that punctures fruit and causes 

premature ripening, blotches, and early fruit drop (Silva and Mexia, 1999; 

PestID, 2012; CABI, 2012; Moore, 2003). This type of damage can cause 

substantial losses to citrus crops (Moore, 2003; Silva and Mexia, 1999). In 

grapes, C. gnidiella feeds on grape clusters which causes them to wilt and the 

consequent fall (Bisotto-de-Oliveira et al., 2007; Ringenberg et al., 2005). On 

fruit close to harvest, feeding causes the disruption of the berries, which results 

in leakage of juice which reduces the quality of wines or depreciates the fruits 

(Ringenberg et al., 2005). In addition, feeding increases the incidence of fungal 

and bacteria diseases that cause fruit rot (Bisotto-de-Oliveira et al., 2007; 

Ringenberg et al., 2005). Several countries actively control Cryptoblabes 

gnidiella populations (e.g. Turkey (Ozturk and Ulusoy, 2011) and Israel (Harari 

et al., 2007)). Control programs currently in place for other Lepidoptera pest are 

unlikely to be sufficient for managing this pest.The risk rating for this element is 

High.

High (3)

Risk Element #5: Environmental Impact

An endangered or threatened species that Cryptoblabes gnidiella could impact is 

High (3)
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39

Cryptoblabes gnidiella Milliere (Lepidoptera: Pyralidae) Risk ratings

Allium muznii (USFWS, 2012). Its introduction could also cause the 

implementation of chemical and/or biological control programs (CABI, 2012; 

Moore, 2003). The risk rating for this element is High.

Figure 1. Predicted U.S. distribution of C. gnidiella based on the ten-year frequency of 

occurrence of required degree days to complete five generations.

Gymnandrosoma aurantianum (Lima) (Lepidoptera: Tortricidae) Risk ratings

Risk Element #1: Climate—Host Interaction

Gymnandrosoma aurantianum is polyphagous (CABI, 2012) and we estimated 

its potential U.S. distribution using the degree-day model reported by Garcia 

(1998) as cited in Parr et al. (2004). We simulated the degree-day model using 

NAPPFAST (Magarey et al., 2007) predictive modeling system. We considered 

areas where G. aurantianum could complete seven generations as conducive for 

permanent establishment based on its biology in Brazil (Garcia, 1998 as cited in 

Parra et al., 2004). The resulting map indicated that G. aurantianum could 

establish in U.S. Plant Hardiness Zones 6-11 (Figure 2) (Magarey et al., 2008). 

The risk rating for this element is High.

High (3)

Risk Element #2: Host Range

Gymnandrosoma aurantianum’s main host is citrus, but it is polyphagous and 

attacks multiple plant species in multiple families (CABI, 2012). 

Gymnandrosoma aurantianum hosts include Pithecellobium dulce (Roxb.) 

Benth., Psidium guajava L., Punica granatum L., Eriobotrya japonica (Thunb.) 

Lindl., Prunus persica (L.) Batsch, and Sapindus saponaria L. (Gilligan and 

Epstein, 2012), which occur in the United States (NRCS, 2012). The risk rating 

for this element is High.

High (3)
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40

Gymnandrosoma aurantianum (Lima) (Lepidoptera: Tortricidae) Risk ratings

Risk Element #3: Dispersal Potential

Gymnandrosoma aurantianum is capable of flight and the larva is an internal 

fruit borer, indicating it could move in harvested fruits (Bento et al., 2001; Parra 

et al., 2004). The moth can have between seven to eight generations per year 

and each female can lay approximately 200 eggs (Garcia, 1998 as cited in Parra 

et al., 2004). The risk rating for this element is High.

High (3)

Risk Element #4: Economic Impact

Gymnandrosoma aurantianum is an internal feeder that punctures fruit (Parra et 

al., 2004). This type of damage can cause substantial losses to citrus crops due 

to fruit drop and rot, rendering fruit unsuitable for the fresh or processed 

markets (Parra et al., 2004). Gymnandrosoma aurantianum can attack fruit at 

the early, mid-, and late ripening stages and complete larval development within 

the host (Parra et al., 2004; Parra et al., 2001). In Brazil, yield losses of up to 50 

percent have been reported (Bento et al., 2001). In one major orchard in 

Trinidad, direct fruit loss reached up to 40 percent in the 1992-93 season 

(White, 1999). If G. aurantianum becomes established in the United States, 

growers would likely institute an Integrated Pest Management approach to 

controlling this pest, as is done in other countries (Parra et al., 2004). These 

measures would likely increase the cost of production. The risk rating for this 

element is High.

High (3)

Risk Element #5: Environmental Impact

None of the known hosts of Gymnandrosoma aurantianum or plants in the same 

genera are Threatened or Endangered plants in the United States. However, 

hosts of G. aurantianum belong to the Rutaceae, Sapindaceae, and Sterculiaceae 

families, members of which are listed as Threatened and Endangered plants 

(USFWS, 2012), although none have been confirmed as hosts. Also, the 

introduction of Gymnandrosoma aurantianum could cause the implementation 

of chemical and/or biological control programs (Molina and Parra, 2006; Parra 

et al., 2004; Scarpellini and Santos, 1997). Due to the potential for direct 

impacts on Threatened or Endangered plant species and the need for additional 

control programs, the risk rating for this element is High. 

High (3)
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41

Figure 2. Predicted U.S. distribution of Gymnandrosoma aurantianum based on the ten-year 

frequency of occurrence of required degree-days to complete seven generations.

Elsinoё australis (Bitancourt & Jenk.) (Sweet Orange Scab, SOS) Risk ratings

Risk Element #1: Climate–Host Interaction

Sweet orange scab (SOS), caused by E. australis, is largely confined to the 

humid citrus-producing areas in southern South America (Timmer et al., 2000): 

Argentina, Bolivia, Brazil, Paraguay (Sivanesan and Critchett, 1974) and 

recently confirmed in Uruguay (Palm, 2007; 2008). SOS was reported in 

Uruguay (Koch de Brotos et al., 1981) and as unpublished data by L. W. Timmer 

(Timmer et al., 1996b). It was intercepted on fruit from Uruquay (PestID, 2008), 

and recent testing has confirmed its presence (Palm, 2007, 2008) but not its 

distribution in Uruguay. Elsinoe australis has been reported in the United States

and is under official control, but it may become more widely established in 

warm, humid areas, such as the southeastern United States (Timmer et al., 2000), 

or in areas where fruit set coincides with relatively warm humid weather. Thayer 

et al. (2003) developed a NAPPFAST climate risk which predicted suitable 

climates for E. australis development are limited to the humid Southeast, 

primarily to the state of Florida. Thayer et al.’s prediction concurs with Timmer 

et al. (Timmer et al., 2000). In the United States citrus production areas

(Borchert, 2008) and favorable climatic conditions for SOS (Thayer et al., 2003; 

Timmer et al., 2000) occur in Plant Hardiness Zones 9-11 (Magarey, 2008). 

Therefore, we rated this element Medium.

Medium (2)

Risk Element #2: Host Range

Elsinoё australis primarily causes disease on the fruit of sweet oranges, such as 

navel orange (C. sinensis), and tangerines, such as mandarin (C. reticulata) 

(Timmer et al., 2000), but lemons (C. limon), satsumas (C. unshiu), limes (C. 

aurantifolia), oval kumquat (Fortunella margarita), Fortunella sp. and fruit of 

Medium (2)
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42

Elsinoё australis (Bitancourt & Jenk.) (Sweet Orange Scab, SOS) Risk ratings

many other citrus species can also be hosts (Farr et al., 2008; Timmer et al., 

1996b, Timmer et al., 2000). Thus, E. australis incites disease in two genera in 

the same family; therefore the rating for host range is Medium.

Risk Element #3: Dispersal Potential

Little is known about the biology, ecology, and epidemiology of E. australis and 

SOS. Bitancourt and Jenkins (1937) suggested four sources of primary inoculum:

the limited number of leaves with lesions; out of season, green, scabbed fruit;

scabbed fruit left from the past season; and twig infections. Elsinoe australis

requires moisture for both spore production and infection. Insects or windcarried water droplets containing spores may contribute to the spread of the 

pathogen (USDA-APHIS-PPQ, 2005). Young fruit are susceptible for only 6 to 8 

weeks after petal fall, but this time is sufficient for secondary infections to occur 

(Bitancourt and Jenkins, 1937). Natural dispersal over short distances occurs by

rain-splashing fungal spores between trees (Chung and Timmer, 2005). The 

estimated spread rate for E. fawcetti was no more than 100 to 300 meters per 

year in Florida groves (Whiteside, 1975). However, long distance dispersal 

occurs through the movement of fruit (Chung and Timmer, 2005). Therefore, the 

rating for dispersal is Medium.

Medium (2)

Risk Element #4: Economic Impact

Elsinoë australis is a fungal pathogen that causes fruit disfigurement and reduces 

fresh market value (Bitancourt and Jenkins, 1937; EPPO/CABI, 1997c); in 

addition, this pathogen may stunt young seedlings (EPPO/CABI, 1997c). The 

introduction of E. australis may not require the use of different chemicals since 

they are part of recommended citrus control programs (Timmer and Chung, 

2008). However, additional applications of chemicals may be required in the 

field or in post harvest treatments. Although the disease is not expected to be 

problem in California production areas (Thayer et al., 2003), the pathogen will 

be difficult to eradicate if established in Florida. The cost of permanent 

establishment of SOS in Florida is estimated to be high. “The cost of living with 

SOS would be primarily associated with increased expenditures for field control 

to reduce disease symptoms, post-harvest treatments, grove surveys, and the loss 

in export market of fresh citrus from all states. Thus, a rough estimate of the cost 

of a permanent establishment of SOS in Florida, including a loss in export 

revenue of $32 million per year, would be about $55 million annually (an 

amount which does not take into consideration the cost of post-harvest 

treatments)” (USDA-APHIS-PPD, 2002). Since E. australis may cause fruit to 

have a lower market value and control of the pathogen may increase costs of 

production, and foreign markets may be jeopardized, the risk rating is Medium.

Medium (2)

Risk Element #5: Environmental Impact

No threatened or endangered species of Citrus or Fortunella in the United States 

should be impacted by sweet orange scab (USFWS, 2012). The chemical control 

options for E. australis are copper products, which are commonly used by Citrus

pest management programs (Timmer and Chung, 2008; Timmer et al., 2000).

Since the chemicals are already recommended for control of E. fawcettii in some 

Low (1)
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43

Elsinoё australis (Bitancourt & Jenk.) (Sweet Orange Scab, SOS) Risk ratings

production regions of the United States, such as Florida the impacts may be 

minor. However, in other regions where E. fawcetti is not a problem (California), 

potential impact on the environment may occur with the increased use of 

pesticides (USDA-APHIS-PPD, 2002). Therefore, we rated its Environmental 

Impact Low.

Xanthomonas citri subsp. citri (Citrus Canker, Xcc) Risk ratings

Risk Element #1: Climate–Host Interaction

High relative humidity is conducive for reproduction and dispersal of 

Xanthomonas citri subsp. citri (Xcc) (Graham et al., 1992a; Serizawa et al., 

1959). Wind speeds greater than 8 m/sec. provide the necessary pressure for Xcc 

cells to penetrate the stomata, facilitating entry by the pathogen and thereby

increasing disease (Graham and Gottwald, 1991). Koizumi (1976) found the 

time needed for incubation decreased with increasing temperature, but no 

relationship was detected between the incubation period and the ten varieties 

tested. Koizumi (1976) also verified optimal temperatures for canker 

development under field conditions between 25 and 30 °C. The successful 

establishment of Xcc several times in the United States is indicative of favorable

climates (Graham et al., 2004; Civerolo, 1984; Smith et al., 1997). The disease 

was successfully eradicated in Florida by 1933 (Whiteside, 1988a) and 

nationwide by 1947 (Schubert and Sun, 2003). Citrus canker reappeared in 

Miami in 1995. Xcc is now widespread throughout citrus-producing areas in 

Florida and eradication is not possible. To date, Xcc has not spread outside of 

Florida to other U.S. citrus-producing areas. The main citrus-producing states 

are Florida, California, Arizona and Texas (USDA-NASS, 2008), but citrus is 

also cultivated in Louisiana and Arkansas (Cross, 2008). Borchert et al. (2007) 

developed a citrus canker spread model to identify areas where citrus canker 

could become established in the major citrus-producing regions of the United 

State; California and Arizona, though favorable conditions can occur, have a 

lower potential for establishment of Xcc than Florida.

The availability of both suitable host plants and suitable climatic conditions 

citrus canker could establish in three Plant Hardiness Zones (9-11), and our 

rating for Host-Climate Interaction is Medium.

Medium (2)

Risk Element #2: Host Range

Known natural hosts are members of the Rutaceae family, including species, 

hybrids and cultivars of Citrus spp., Poncirus trifoliata, Fortunella japonica, F. 

margarita, Severinia buxifolia, and Swinglea glutinosa. Two non-Rutaceous 

hosts, Lansium domesticum (Meliaceae) and Ageratum conyzoides (Asteraceae) 

have been reported, but this information was not confirmed (COSAVE, 2004; 

CABI, 2007). In addition, plants in several other plant families (Asteraceae, 

Convolvulaceae, Meliaceae, Poaceae, and Solanaceae) have been artificially 

infected with Xcc (CABI, 2012; Goto, 1970; Goto et al., 1975a; Goto et al., 

1978). The natural host range of citrus canker includes multiple species within 

Medium (2)
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Xanthomonas citri subsp. citri (Citrus Canker, Xcc) Risk ratings

one plant family so our rating was Medium. 

Risk Element #3: Dispersal Potential

Bacteria survive in lesions formed on aboveground parts of susceptible hosts, 

including fruit attached to the tree, leaves, twigs, stems, and the bark of the 

trunk (Leite Jr. and Mohan, 1990). Xcc can survive on non-citrus weed and 

grass hosts, although the epidemiological significance 43 is unclear (Stall et al., 

1980; Goto, 1970; Goto et al., 1975a; Goto et al., 1975b; 1978; Pereira et al., 

1976; 1978; Serizawa, 1981) Bacteria produced in leaf and twig lesions are 

epidemiologically significant for secondary infections (Pruvost et al., 2002); 

stem lesions can act as reservoirs of inoculum for longer periods than fruits and 

leaves (Leite Jr. and Mohan, 1990; Verniere et al., 2003). The number of Xcc 

bacteria present within active lesions decreases as the lesions age. Timmer et al.

(Timmer et al., 1991) demonstrated in vitro that young lesions (4-6 weeks old) 

exude ~104-106cfu44/ml in the first 48 hours of wetting, while older lesions (4-6 

months old) exude ~102-103cfu/ml in the same period. Bacteria may survive for 

a few weeks to several months on decomposing plant litter (fallen fruit, leaves, 

and limbs) on the soil surface (Civerolo, 1984; Gottwald et al., 2002a; Leite and 

Mohan, 1990; Graham et al., 1987; Schubert et al., 2001) or on plant material 

buried in the soil (Graham et al., 1987), but do not survive as well in the absence 

of host material (Graham et al., 1989; Leite Jr. and Mohan, 1984). Survival in 

decomposing leaves, both in and on the soil surface, is dependant on the 

moisture and temperature (Goto, 1992; Graham et al., 1987). This bacterium is a 

facultative saprotroph on citrus debris, Zoysia sp. rhizomes, and rice straw (Goto 

et al., 1978; Graham et al., 1987). Viable bacteria have been isolated from 

lesions on 5-7 year-old branches (Xun, unpublished data in: Schubert et al., 

2001). Asymptomatic citrus leaves still attached to the tree are believed to 

harbor citrus canker bacteria for several months. Late-season lesions are capable 

of sustaining bacteria from one season into the next season (Schubert et al., 

2001), and bacteria residing on plant material in the soil (as long as 2-4 years) 

has been shown to infect healthy trees (Goto, 1992;Goto, 1992; Goto et al., 

1975a; Pereira et al., 1976). Thus citrus canker bacteria can persist in areas 

where the disease is already established, providing inoculum for the spread of 

the pathogen (Graham et al., 1987) (Appendix E).

Citrus canker is readily dispersed by wind-driven rain in large quantities 

immediately after a rain event occurs (Bock et al., 2005). Pathogen spread has 

been recorded from 32 meters to several miles (Gottwald et al., 2002b; Stall et 

al., 1980; Gottwald and Graham, 2000; Gottwald et al., 1988). In Florida, 

pathogen spread was detected within 579 m (1900 ft) from the source 95 percent

of the time (Gottwald et al., 2002a; Compton and Fagan, 2000; Gottwald et al., 

2001; McElroy, 2000). Citrus canker spread from an initial 50 square miles to 

1,265 square miles area in the first five years following detection in Florida. The 

Medium (2)

 

43 The term “epidemiologically significant” refers to minimum conditions required for successful Xcc transmission. 

44 cfu refers to colony forming unit.
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45

Xanthomonas citri subsp. citri (Citrus Canker, Xcc) Risk ratings

epidemic centered on the Miami area (Gottwald et al., 2001). The spread 

possibly resulted from favorable environmental conditions that included storms 

with high winds and wind-driven rain on a regular basis, as well as limited 

management of the disease. For example, a thunderstorm in 1989 spread 

inoculum that resulted in the establishment of four new disease foci 230 to 810 

m from the infected source trees (Graham et al., 2004; Gottwald et al., 1992). 

Winds at speeds of 8 m/sec or greater aid in the penetration of bacteria through 

the stomatal pores or wounds (Timmer et al., 2000).

Long-distance spread of the pathogen can also occur via the movement of 

infected planting and propagating material, such as budwood, rootstock 

seedlings or budded trees from nurseries (Gottwald et al., 2002a; Smith et al., 

1997; Graham and Leite Jr., 2004). There is no confirmed record of seed 

transmission (Smith et al., 1997). Contaminated personnel, clothing, equipment, 

tools, field boxes, and other items associated with harvesting and post-harvest 

handling of fruit may also provide a means of long-distance dissemination, 

especially when trees are wet (Civerolo, 1984; Timmer et al., 2007). 

The movement of diseased fruit has often been considered a potential means of 

long-distance pathogen spread; however, there is no authenticated record of this 

being related to the epidemiology of the disease (Smith et al., 1997b), despite a 

long global history of commercial trade in citrus fruit. Likewise, infected culled 

fruit and processed fruit pulp have also been identified as possibly facilitating

long-distance pathogen spread. In recent research conducted by Gottwald et al. 

(2009), culled fruit and processed fruit pulp appear to be unlikely pathways for 

spread. Gottwald et al. (2009) examined several possible transmission scenarios 

to ascertain the potential of harvested fruit to transmit Xcc in the natural 

environment. In the first transmission scenario, symptomatic fruit that had 

undergone a typical packinghouse process were placed in cull piles with young 

susceptible trap trees surrounding them. The experiment was conducted in 

Florida and Argentina. In each experiment, treated symptomatic fruit (i.e. were 

put through the packinghouse process) were left in the field for several weeks 

under natural rain and wind conditions. None of the “trap” trees developed 

citrus canker. 

Gottwald et al. (2009) also tried to create a worst-case scenario by simulating 

spread with wind and rain events. In those experiments, severely infected fruit 

that were not put through the packinghouse process were either placed into 

elevated cull piles or suspended on vertical strings. Trap plants were placed 

around the infected fruit at distances of 0, 2, 5, and 10 m. An airboat fan was 

used to produce wind at various speeds (1, 10, and 25 m/sec), and garden 

sprayers were used to simulate rain. In all the treatments, only one plant became 

infected with Xcc. The infected tree developed a single lesion at a wound site 

(likely created by the wind treatment). The infection occurred on a plant that 

was 0 m away from the infected fruit cull pile, and was subjected to 25 m/sec 
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Xanthomonas citri subsp. citri (Citrus Canker, Xcc) Risk ratings

wind speed. The strength of this wind treatment is likely to only occur in strong 

storms, such as tropical storms. For contrast, a category 1 hurricane starts at 33 

m/s on the Saffir-Simpson scale (AOML, undated). Whereas the windspeeds 

used in the experiments were not equivalent to a hurricane, personal 

communications with the authors (December 2008) revealed that at the highest 

wind speed, the trap trees lost approximately 50 percent of their leaves. 

Gottwald et al. (2009) also examined the potential of Xcc bacteria to infect 

susceptible grapefruit plants when the fruit is forcefully broken and spread over 

the susceptible plants. This set of experiments used apparently healthy fruit from 

healthy trees, apparently healthy fruit from infected trees, and symptomatic 

fruit. Fruit were struck with a bat so that the flesh of the fruit would splatter over 

susceptible citrus plants. Three hundred total fruit (the juice, rind and fruit 

fragments) were splattered over 300 plants and none developed Xcc symptoms 

or had Xcc bacteria recovered from the surface of the plants. 

In the another transmission scenario, Gottwald et al. (2009) examined the 

potential for discarded infected citrus peel to infect susceptible citrus trees in 

nature. Fruit peels from severely infected 'Ruby Red' grapefruit were placed in 

fiberglass mesh and placed either under a susceptible grapefruit tree in the shade 

or near the tree exposed to the sun. The peels were sampled weekly for viable 

Xcc. No infections developed in bioassays from inoculations using Xcc-infected 

peels left in the field for more than eight days. Since peels were sampled on day

1 and at weekly intervals thereafter, viability was lost after more than 1 day and 

less than or equal to 8 days.

There is no record that either infected fruit with lesions or asymptomatic fruit 

are epidemiologically significant with respect to the initiation of new infections 

(Anonymous, 2005a; Anonymous, 2005b; Jetter et al., 2000; Canteros, 2004). 

Based on the above, citrus canker is rated Medium.

Risk Element #4: Economic Impact

Citrus canker is mainly a leaf-spotting and rind-blemishing disease, but when 

conditions are highly favorable for infection, it causes defoliation, death of 

terminal branches and premature fruit drop in susceptible hosts (Timmer et al., 

2000). The internal quality of the infected tree-ripened fruit is not affected; 

however, such fruit have reduced marketability as fresh fruit. In general,

grapefruits, limes and Poncirus trifoliata are highly susceptible; sour orange, 

lemon and sweet orange are moderately susceptible. Mandarins are moderately 

resistant, but some mandarins and hybrid mandarins, such as Fremont, Kara, and 

Umatilla are highly susceptible to citrus canker (Leite Jr., 2000). Defoliation and 

fruit drop are more severe on very susceptible varieties, under highly favorable 

conditions for disease development, and without adequate phytosanitary

management (Timmer et al., 2000). Although there is a loss in commercial 

quality due to rind-blemishes and fruit drop, the most important economic loss 

results from quarantine restrictions imposed on the international trade of citrus 

High (3)
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Xanthomonas citri subsp. citri (Citrus Canker, Xcc) Risk ratings

fruit. Thus, the rating for Economic Impact is High.

Risk Element #5: Environmental Impact

There are no related threatened and endangered species within the same host 

genera infected by Xcc (USFWS, 2012). The introduction of citrus canker in a 

new area may require specific control programs that may negatively impact nontarget pests and the environment. Prophylactic sprays of copper oxychloride or

other copper-containing compounds are commonly used to provide protection 

against initial infection in canker-endemic areas during growth flushes and fruit

development (2-6 cm diameter) (Graham et al., 2004; Stall et al., 1980; Leite, 

1990; Muraro et al., 2001; Das, 2003; Kuhara, 1978; Koizumi, 1977b; MedinaUrrutia and Stapleton, 1985; Timmer, 1988). Additional copper fungicide sprays 

are often necessary to avoid symptoms in infected areas because the initial spray

wears off (Gottwald et al., 2002a; Stall et al., 1980; Leite and Mohan, 1990). 

Five to six copper sprays during the susceptible rainy season in Brazil decreased 

disease incidence 90 percent in moderately susceptible cultivars (Leite Jr. et al., 

1987). This pesticide is commonly used within citrus pest management 

programs for other diseases; however, in some environments, like Florida, 

additional copper sprays may be needed. Therefore, the rating for 

Environmental Impact is Medium.

Medium (2)

Table 4. Risk Ratings for Consequences of Introduction

Pest ClimateHost 

Interaction

Host 

Range

Dispersal 

Potential

Economic 

Impact

Environmental 

Impact

Cumulative 

risk rating a

Anastrepha fraterculus High (3) High (3) High (3) High (3) Med (2) High (14)

Ceratitis capitata High (3) High (3) High (3) High (3) High (3) High (15)

Cryptoblabes gnidiella High (3) High (3) High (3) High (3) High (3) High (15)

Elsinoё australis Med (2) Med (2) Med (2) Med (2) Low (1) Medium (9)

Gymnandrosoma 

aurantianum

High (3) High (3) High (3) High (3) High (3) High (15)

Xanthomonas citri subsp. 

citri

Med (2) Med (2) Med (2) High (3) Med (2) Medium (11)

Low is 5-8 points; Medium is 9-12 points; and High is 13-15 points

2.5 Likelihood of Introduction

In this portion of the assessment we consider two separate components. First, we estimate the 

amount of commodity likely to be imported (which is the same for all quarantine pests 

considered). Second, we consider five biological features (i.e., sub-elements) concerning the pest 

and its interactions with the commodity. The likelihood of a pest being introduced and 

establishing a reproductive population is dependent on six independent criteria: 1) quantity of the 

commodity imported, 2) ability of the pest to survive standard production practices and postharvest treatment, 3) ability of the pest to survive shipment, 4) probability that pests will not be 
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

48

detected at the port-of-entry, 5) likelihood that it will be moved to a suitable habitat, and 6) 

probability that it will come into contact with suitable host material (PPQ, 2000). For consistency

of approach with other PRA’s for similar commodities, we have altered sub-element 2 from our 

standard guidelines to account for prevalence of pests and ability of production practices to 

reduce prevalence of some infested or infected fruit that are exported.

The resulting risk ratings are specific to each pest. For each pest, the sum of the sub-elements 

produces a cumulative risk rating for likelihood of introduction. The cumulative risk rating for 

introduction is considered to be an indicator of the likelihood that a particular pest would be 

introduced. These ratings and the value for the Likelihood of Introduction are summarized below 

(Table 5).

2.5.1. Quantity Imported Annually

The likelihood that an exotic pest will be introduced depends on the amount of potentially

infested commodity imported. For qualitative pest risk assessments, the amount of commodity

imported is estimated in units of standard 40-foot-long shipping containers. Standard 40-foot 

shipping containers have a capacity of slightly over 210 tons. Uruguayan exporters estimate a 

total of 39,000 tons will be exported per year for the different varieties (Appendix C). This is 

>100 containers per year, therefore the Quantity Imported Annually is rated High for all pests.

2.5.2 Survives standard production practices and post-harvest treatment

The second sub-element is the likelihood of a pest or pathogen surviving the packing process and 

post-harvest treatment. It also attempts to account for expected prevalence of each pest under 

standard production practices which are outlined in Appendices C and D. We assumed that 

infestation is likely if fruit originates in areas where the pest/disease occurs, but the magnitude of 

the hazard at this stage will depend in large part on the proportion of infested/infected fruit and 

the nature of the infestation/contamination. The incidence of infested/infected fruit will depend 

primarily on the species of Citrus or Fortunella, variety, environmental conditions, field 

management, and harvesting practices. The location of the pest in or on fruit will directly impact 

its abililty to survive any post-harvest treatments. 

Post-harvest treatment refers to any manipulation, handling, or specific phytosanitary treatment 

to which the commodity is subjected. The citrus fruit packing process includes washing with 

disinfectant, culling, mechanical brushing, chemical treatments, drying, and waxing (see 

Appendix C). This process removes organic matter and other contaminants (such as soil), and 

some pests and pathogens from the fruit surface. Harvested fruit is transported to the 

packinghouse where it is subjected to manual and/or optical scanner culling. Citrus fruit is 

washed when it enters the packinghouse as a normal part of any packing process. This washing 

usually includes mechanical brushing, detergent, and disinfectant with chlorine and/or sodium 

orthophenylphenate (SOPP). The fruit may also be chemically treated (Thiabendazole (TBZ), 

Imazalil) to control fungal and bacterial growth. Finally, the fruit is dried and waxed. We 

evaluated ability to survive the listed post-harvest measures, as well as determining impacts of 

standard production and harvest practices. 

Anastrepha fraterculus and Ceratitis capitata. Several methods exist for controlling fruit fly 

populations in the field which include bait sprays, sterile insect technique (SIT), and male 
Pest Risk Assessment for Citrus from Uruguay

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49

annihilation (CABI, 2012). Appendix A outlines Uruguay’s fruit fly surveillance program, and 

provides monthly data on fruit fly populations from 2003 to 2006, and data showing populations 

associated with different species and varieties of Citrus grown in Uruguay. 

Harvest and export of Citrus fruits in Uruguay stretches from late February through December, 

although the volume and type of fruit shipped varies during this time period (Appendix C). The 

earliest harvest and export begins with mandarins in late February to March. The highest levels 

of harvest and export, which includes lemons, most orange varieties (except Valencia), many 

mandarin varieties, and grapefruits, occur during June, July, and August. The majority of harvest 

and exports finish at the end of September. The exceptions to the harvest and export calendar are 

Valencia oranges, whose harvest stretches from July to December. January and February are the 

two months in which little or no Citrus spp. are harvested or shipped. Typically, post-harvest 

measures remove overripe or damaged fruit which are more likely to be infested (Willink et al., 

2007). Due to the number of Citrus species and varieties produced by Uruguay, it seems difficult 

to avoid times of the year when A. fraterculus and C. capitata populations are present (Appendix 

A). For example, numbers of C. capitata trapped were highest in the Southern production region 

from December to March, which overlaps with harvest periods for some mandarin varieties and 

Valencia oranges, but may diminish the risk associated with certain other Citrus species and 

cultivars. In the Northern production region, C. capitata were lower than the Southern region, 

but numbers peaked between December and March, and sometimes extended into May when 

larger amounts of fruit are harvested and shipped. Anastrepha fraterculus numbers were 

relatively low for both production regions and varied in months in which they peaked, but the 

pest is still a concern for fruit exported. Selective harvesting methods, such as harvesting green 

fruit and eliminating damaged and overripe fruit, accompanied with monitoring may reduce 

prevalence of fruit flies in the harvested fruit for export. 

Generally, internally feeding arthropods are expected to survive minimal post-harvest treatment. 

Because Anastrepha fraterculus and Ceratitis capitata are internal feeders, they are expected to 

survive post-harvest processing in host fruits, such as washing and culling, especially if the 

infestation of the fruit does not result in obvious damage. Fruit fly-infested fruit may have a high 

probability of escaping detection during culling, since fruit fly-infested fruit may go 

unrecognized (White and Elson-Harris, 1992). Anastrepha fraterculus and Ceratitis capitata are 

rated High (3) for the likelihood that they will survive post harvest treatment and standard 

production practices.

Cryptoblabes gnidiella. Cryptoblabes gnidiella is an internal fruit feeder reported to occasionally 

bore into citrus fruit and cause fruit drop (CABI, 2007; SINAVIMO, 2005a). Newly enclosed 

larva will move directly into the fruit, typically dwelling within the peel or flavedo (Moore, 

2003). Cryptoblabes gnidiella is an internal feeder and Moore (2003) noted that C. gnidiella will 

usually attack smaller lemons and does not finish the life cycle on fruit. Silva and Mexia, 1999 

report C. gnidiella early instars feed primarily on honeydew associated with aphids or 

mealybugs, and only later instars can pierce the fruit unless it is already previously damaged by

other pests. Symptoms may include premature coloring followed by fruit drop, which can lead to 

yield losses in the grove (Silva and Mexia, 1999). Cryptoblabes gnidiella feeding injury consists 

of fruit piercing and gallery formation at fruit exocarp and endocarp. Gummy exudates may be 

apparent and fruits may turn yellow and dropped prematurely. It is unclear how C. gnidiella
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50

impacts or survives in other Citrus fruits. Larvae bore into other fresh fruits such as avocados, 

and reportedly overwinter in fruit (Swirski et al., 1995). However, it has characteristics that 

probably make it less likely than the fruit flies to survive the post-harvest culling phase. Any 

visible symptoms of infestation by C. gnidiella should decrease the chance of infested fruit being 

selected during post-harvest processing for export. Based on this evidence, we theorize that only

fruit infested at early stages and at low levels of infestation would go undetected and survive the 

post-harvest treatments and standard production practices. The risk rating for this sub-element is 

Medium.

Gymnandrosoma aurantianum. The tortricid G. aurantianum (Syn: Ecdytolopha aurantiana) is 

also an internal feeder (White, 1999; Adamski, 2001), which protects it from most post-harvest 

treatments (e.g., chlorine dip, brushing) (Parra et al., 2004; Parra et al., 2001). However, it has 

characteristics that probably make it less likely than the fruit flies to survive the post-harvest 

culling phase. Fruit attacked by G. aurantianum gradually develop a necrotic area around the 

entrance hole caused by the larva in the rind of the fruit, and then the fruit either drops 

prematurely or develops a bright orange color distinct from healthy fruit (White and Tuck, 1993). 

These symptoms caused by infestation by G. aurantianum should decrease the chance of infested 

fruit being selected during post-harvest processing for export. Based on this evidence, we 

theorize that only fruit in early stages of infestation would go undetected and survive the postharvest treatments and standard production practices. The risk rating for this sub-element is 

Medium.

Elsinoё australis. Elsinoё australis infects fruit when new shoots emerge and “petal-fall” starts; 

tissue susceptibility decreases as fruit mature. Lesion development on leaves is rare but can 

occur (Bitancourt and Jenkins, 1937). For six to eight weeks after petal fall, fruits are susceptible 

to E. australis (Timmer et al., 2000). 

Production practices such as barrier zones around export groves reduce inoculum spread from 

one grove to another. Chemical sprays during new spring growth and flowering further protect 

the young fruit from infection (Timmer et al., 2000; Whiteside, 1975): copper oxychloride sprays 

protect the young leaves and fruit by preventing germination of E. fawcetti spores and 

subsequent infection (Timmer et al., 2007; Chung and Timmer, 2005). Spray programs used to 

control E. fawcettii are anticipated to be effective for controlling E. australis in heavily infected 

groves (Timmer et al., 2007). Two fungicide sprays are often applied in infected regions 

(Bushong and Timmer, 2000). Copper fungicides may be used to control citrus scab, but may not 

be as effective in heavily infected groves (Diaz et al., 1996).

Harvested fruit is visually inspected for disease symptoms, both in the grove and in the 

packinghouse (DGSA, 2008). Fruit infected in the early stages of their development grow 

misshapen and are subject to premature fall (EPPO/CABI, 1997b). Lesions on young fruit are 

round to irregular, 2 to 6 mm in diameter. They begin as slightly raised and pink to light brown 

scab pustules and later become warty, cracked, and yellowish-brown to dark gray in color 

(Bitancourt and Jenkins, 1937; Timmer et al., 2000). Since these symptoms are distinctive and 

easily detected by visual inspection, culling procedures used to remove symptomatic Xcc fruit 

(Ploper et al., 2004) should be effective in removing E. australis symptomatic fruit 
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51

Routine packinghouse treatments to control E. australis include chlorine dips, warm water baths, 

chemical tank dips (1000 μg ml-1guazatine, 503 μg ml-1 imazalil sulphate, 500 μg ml-1 2,4-D 

sodium salt) or combinations of these treatments (Korf et al., 2001), and should reduce the 

viability of fungal spores present on the fruit. The fungicide imazalil is active against a large 

number of fungi imperfecti and some ascomycetes (IPCS, 1977) and is often incorporated into 

the waxing process. Packinghouse treatments reduced the viability of Elsinoë spp. in highly 

infected fruit (60 percent of its surface covered by scab lesions) during DGSA trials (Díaz et al., 

2001; Habtemariam et al., 2001). 

The rating for survives standard production practices and post-harvest treatment is Medium.

Xanthomonas citri subsp. citri (Xcc). Resistance of fruit to infection by citrus canker is 

correlated with its stage of maturity. Small fruit (<20mm) are not susceptible to infection as the 

stomata are not fully open at this stage. Above this size susceptibility is inversely related to fruit 

age. The younger the fruit, the less resistant it is to citrus canker (Graham et al., 1992b). 

Persistence of the citrus canker pathogen in lesions varies based on the plant part infected 

(Schubert et al., 2001). Fruit and leaves removed from trees sustain bacterial populations in 

lesions for 1-2 months in the presence of saprophytic microorganisms (Schubert et al., 2001). 

Timmer et al. (1991) inoculated grapefruit and Swingle citrumelo leaves with Xanthomonas 

campestris in the field, and then collected the leaves at 14, 21, and 49 days after inoculation to 

assess bacteria concentrations within the active lesions. Fourteen-day-old lesions produced 

significantly more bacteria than 49-day-old lesions. Young leaves (4-6 weeks old) and mature 

leaves (4-6 months old) naturally infected with Xanthomonas c. pv. citri were removed from the 

infected tree and assessed in the lab. Bacterial populations within the lesions were closely 

correlated with lesion age. Young leaves exuded ~106 cells/ml, while older lesions exuded ~103

cells/ml. After a 48-hour period, all samples exuded fewer than 102cells/ml (Timmer et al., 

1991). Fruit and leaves removed from trees sustain bacterial populations in lesions for 1-2 

months in the presence of saprophytic microorganisms (Schubert et al., 2001). Diseased leaves 

removed from trees and placed on the soil surface harbor bacteria populations for 90 to 120 days, 

with no detectable bacteria after 120 days (Graham et al., 1987). Xcc populations within the 

lesions of infected fruit decline after harvest (Koizumi, 1972). 

Epiphytic populations of Xcc on citrus tissue drop 3-5 orders of magnitude in 24 hours during 

experimental testing (Timmer et al., 1996b). Timmer et al. (1996) detected epiphytic populations 

of Xcc on asymptomatic plants, but these populations did not correlate with subsequent symptom 

development and did not survive very long on either hosts or non-hosts. No bacteria could be 

recovered form asymptomatic fruit that had been removed from trees, treated with a bacterial 

suspension of 106cfu/ml, and incubated at room temperature for 5 days (Belasque Jr. and 

Rodriguez Neto, 2000). The survival of epiphytic Xcc populations on asymptomatic fruit under 

natural conditions would be expected to be further reduced due to harsher environmental 

conditions. 

Harvested fruit is transported to the packinghouse, where it is subjected to one or more visual 

inspections. Field culling is highly effective in removing symptomatic and blemished or injured 

fruit prior to arrival at the packinghouse. Visual and/or mechanical inspection at the 

packinghouse further reduce the possibility that symptomatic, injured, or blemished fruit, as well 
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52

as misshapen, off-color, damaged, and otherwise low quality fruit, will be packed. Current 

programs in Argentina have demonstrated that culling of symptomatic citrus canker fruit is 

highly effective in packinghouse operations. For example, trays of fruit known to contain either 1

percent or 3 percent of symptomatic fruit were visually inspected at three stages throughout the 

packing process, resulting in extremely low (near 0) numbers of symptomatic, injured or 

blemished fruit reaching the packing bench, and zero symptomatic fruit packed in boxes (Ploper

et al., 2004).

Commercially packed citrus fruit is washed when it enters the packinghouse. This washing 

usually includes mechanical brushing and detergent (at least), which will remove organic and 

other contaminants (such as soil) (Schubert et al., 1999). Brushing increases the exposure of Xcc 

to detergents or other toxins (Brown and Schubert, 1987). New research by Gottwald et al. 

(2009) observed that exposing apparently healthy fruit from infected citrus trees to a prewash 

with SOPP detergent followed by a wash with chlorine (Cl) reduced the survival of surface Xcc. 

Although the observations by Gottwald et al. (2009) were not conclusive given the variability in 

the experiments, prewashing the fruit with sodium ortho-phenylphanate (SOPP) detergent may

be effective because it lowers the surface tension, which allows the Cl better access to bacteria 

and prevents the Cl from binding to debris or other surface contaminants. The drying process 

(i.e., hot air at 58 °C for 2.5 minutes), further reduces epiphytic Xcc populations (Schubert et al., 

1999). 

When the washing process includes a disinfectant, such as 200 ppm chlorine or sodium 

orthophenylphenate (SOPP) or both, the closely related species Xanthomonas campestris pv. 

vesicatoria populations are significantly reduced to epidemiologically insignificant or 

undetectable levels (Brown and Schubert, 1987; Graham and Gottwald, 1991). The packinghouse 

wash with disinfectants can practically remove all epiphytic Xcc from fruits without symptoms 

(Canteros, 2004, (undated); Canteros et al., 2000). The use of 200 ppm Cl for two minutes 

reduces natural bacterial populations on citrus fruits from 77-99 percent (Stapleton, 1986). The 

estimated reduction in bacterial populations on the surface of citrus fruits brushed, washed, and 

disinfected with Cl or SOPP is between 3 and 7 orders of magnitude. In contrast research by 

Gottwald et al. (2009) treating the fruit with only Cl for 45 s did not significantly reduce surface 

bacteria populations. The differing results could be attributed to differing bacteria loads on the 

fruit entering treatment or differences in exposure time of the treatments. The amount of bacteria 

on the fruit can be affected by several factors, such as field control measures, the time of year 

that the fruit was harvested (differences in field bacteria load), and the amount of time the fruit 

were held before treatment. The results also may differ because the treatments were not identical. 

Gottwald et al. (2009) treated fruits in chlorine for 45 s with and without pre-wash. Canteros et 

al. (2000) treated fruit in chlorine for 2 min with pre-wash.

According to research by Verdier et al. (undated) indicated that average bacterial populations on 

artificially infested fruits were 1.7x10

3

cfu/ml and 39.4 cfu/ml on naturally infested 

asymptomatic fruit prior to post-harvest treatment in Uruguay. After treatment, bacterial 

populations were tested by plating on artificial growing medium and were reduced to 8 cfu/ml on

artificially infested fruit and 0.06 cfu/ml for naturally infested fruit. No growth or disease 

developed on tests using susceptible leaf tissue. Bacterial populations used for artificial 
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53

inoculation of fruit are at extremely high levels typically never found in natural conditions (~43 

times higher than naturally infected fruit) (Verdier et al., undated). 

Such levels of bacterial presence as used in these experiments are considered “high” because 

those levels are consistent with every tree in a grove being infected (as all fruit in the 

experiments are inoculated or exposed to Xcc). That very high level of disease incidence is not 

likely to be found in any commercial grove anywhere because the grove would not be productive 

and the fruit would not be marketable. Studies performed in Argentina on the effectiveness of 

sodium hypochlorite on mature symptomless fruit artificially inoculated with Xcc showed that 

sodium hypochlorite levels as low as 8 ppm were effective in eliminating epiphytic or surface 

bacteria from fruit (Canteros, undated). If a small epiphytic population of Xcc did survive the 

post-harvest treatment it would not survive on the surface of the fruit for long (Goto, 1969; 

Timmer et al., 1991; USDA and FDACS, 2000). Epiphytic bacteria do not multiply in water, on 

leaf surfaces, or on dry leaves (Timmer et al., 1991; Timmer et al., 1996b).

Disinfection protocols are not 100 percent effective. Golmohammadi et al. (2007) report that a 

low level of Xcc may survive post harvest treatments and shipment in fruit lesions. The pathogen 

was recover from 11 of 16 fruit samples: 16 of 130 tested lesions yielded viable Xcc by isolation, 

and some samples were only positive by PCR protocols (Golmohammadi et al., 2007).

Golmohammadi et al. (2007) found molecular methods to be the more efficient in detecting Xcc, 

suggesting it was because the treatments used prior to shipment did indeed reduce the Xcc

population.

Healthy fruit can be obtained in Xcc endemic areas. There is a high likelihood that symptomatic 

fruit that are harvested are likely to be culled out in the packinghouse. Any symptomatic fruit 

that are not culled would be subjected to brushing, washing with disinfectant, and waxing,that is 

likely to greatly reduce the number and viability of bacteria within lesions and eliminated 

epiphytic bacteria. Therefore, it is likely that very low levels of Xcc survive standard production 

practices and post harvest treatments inside lesions. Therefore, the rating for this sub-element is 

Low.

2.5.3 Survives shipment

The third sub-element is concerned with the survival of pests and pathogens during shipment. 

Pest survival depends on several factors, including duration of shipment and ambient conditions. 

Transport of citrus fruit from Uruguay to the United States takes 14 to 20 days under 

refrigeration at temperatures of 4 °C– 8 oC, depending on the Citrus species.

Anastrepha fraterculus and Ceratitis capitata. Low temperatures lengthen the duration of larval 

instars of both species (CABI, 2007), but under normal shipment temperatures, larvae are 

expected to survive. APHIS-approved cold treatments for A. fraterculus and C. capitata require

temperatures lower than 2 oC for a duration between 15 and 17 days (USDA, 2008a, T107-a-1)). 

The current USDA approved cold treatment schedule (T107-a-1) for Ceratitis capitata and 

species of Anastrepha (other than A. ludens) in grapefruit, mandarins, oranges, and tangerines 

(including clementines) requires either 34° F (1.11° C) or below for 15 days, or 35° F (1.67° C) 

or below for 17 days (USDA-APHIS-PPQ, 2008a, 2008b, T107-a-1). Standard shipping 

procedures will not lower the temperature to these levels so at least some of the larvae and eggs 
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54

of C. capitata and Anastrepha species would survive. The fruit itself should provide larvae and 

eggs some protection against. Both Anastrepha sp. and C. capitata have been intercepted by PPQ 

at ports of entry with citrus fruit in cargo (PestID, 2012), which demonstrates that at least a small 

percentage of these fruit flies have the ability to survive the transport conditions of citrus. 

Shipping temperatures will vary based on Citrus species shipped. The rating for this element is 

High for Anastrepha fraterculus and Ceratitis capitata.

Cryptoblables gnidiella. There were 457 interceptions of C. gnidiella, 51 reported on Citrus spp. 

and one on Fortunella sp., although most were intercepted from fruit in baggage, ships stores and 

in general cargo. In permit cargo Cryptoblabes gnidiella has only been intercepted 11 times in 

permit cargo shipments, with four of those interceptions occurring in fruit. One of the 

interceptions was on citrus leaves (PestID, 2012). It is unclear what effect proposed shipping 

temperatures will have on C. gnidiella. Therefore, the risk rating for this sub-element is High.

Gymnandrosoma aurantianum. There are several factors that may aid survival of G.

aurantianum during shipment. Gymnandrosoma aurantianum is an internal feeder, which can 

remain viable in green and ripe fruits, and completes larval development within the host (Parra et 

al., 2004; Parra et al., 2001). We concluded it could survive shipment in harvested fruits. The 

risk rating for this sub-element is High.

Elsinoё australis. This pathogen survives in scab pustules on fruits remaining on the tree 

providing inoculum for the next season (Bitancourt and Jenkins, 1937; CABI, 2012), and may

also survive on twigs and in leaf lesions (Bitancourt and Jenkins, 1937; Timmer et al., 2000). 

Whiteside (1988b) demonstrated that the viability of E. fawcetti mycelium in scabs decreases 

significantly after nine months. Elsinoë australis may present little additional threat to sweet 

orange unless it is able to survive in scab pustules on fruit rind longer than E. fawcettii does 

(Whiteside, 1988b). Since E. australis survives both overwinter conditions and survives crossAtlantic, the rating is High.

Xanthomonas citri subsp. citri. Xcc cells that may survive the packing process on the surface of 

citrus fruit are unlikely to survive the shipping process. Epiphytic populations of X. citri subsp. 

citri only survive for a limited amount of time, 8-72 hours in sun and shade (Goto, 1962; Goto, 

1969). No variation of survival has been detected for epiphytic Xcc bacteria on varying plant or 

inorganic material. Gottwald examined epiphytic bacteria survival on metal, wood, plastic, cloth, 

leather, and grass; he did not detect Xcc on any surface tested after 72 hours (USDA and 

FDACS, 2000). In one study, leaves inoculated with culture grown bacteria displayed a 

significant population decline (3-5 orders of magnitude) in the first 24 hours following 

inoculation, but bacteria persisted in low numbers (<104cfu/leaf) for up to 5 days (Timmer et al., 

1996b). In a laboratory study inoculating unwounded leaves via air pressure, bacteria 

concentrations of less than 104cells per ml were unable to cause infection (Gottwald and 

Graham, 1992). Wounded leaves are more susceptible to infection and may only require a 

minimum of 102cells per ml (Goto et al., 1978). Epiphytic bacteria do not multiply in water on 

leaf surfaces or on dry leaves (Timmer et al., 1991; Timmer et al., 1996b). There is, therefore, a 

very limited window of time when an epiphytic population will pose an epidemiological threat. 
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Temperatures during shipping and storage influence Xcc inoculum survival. Recommended 

shipping and storage temperatures and times for citrus vary from and from two to twelve weeks 

(one to six months for lemons) (Cantwell, 2002). Only grapefruit are stored at the highest 

temperatures (10 to 15°C). In host plant tissues, Xcc infection and subsequent multiplication 

only occurs at temperatures above 14oC and below 38oC (Koizumi, 1976). Dalla Pria et al.

(2006) reported 20°C temperatures, interfere in the infection process, reducing disease incidence. 

Bacterial populations in existing lesions decreased from 107to between 102and 104cells when 

the average maximum temperature was below 20°C and average minimum temperature was 

below 10°C (Koizumi, 1977b). 

Xanthomonas is unable to grow at 4-5 oC (Swings et al., 1993) and epiphytic Xcc populations on 

asymptomatic leaves and fruits have previously been shown to decline substantially in 3 to 5 

days under suitable conditions for bacterial multiplication (Belasque Jr. and Rodriguez Neto, 

2000; Timmer et al., 1996a). Storage conditions can vary from 0°C to 15°C, with the cooler 

temperatures used for sweet orange (0-9°C), kumquat (4°C), and tangerines (4-7°C), and warmer 

temperatures used for grapefruit (10-15°C) (Cantwell, 2002). Therefore, the few Xcc bacteria 

that survive the post-harvest treatment may not survive storage temperatures during the transport 

period (14-18 days) for sweet orange, kumquat, and tangerine fruit stored at the lower 

temperatures but may for grapefruit and other citrus stored above 5°C. The post-harvest 

treatment described effectively eliminated more than 99.5 percent of the Xcc population from 

naturally and artificially infested fruit in these tests. Fruit-to-fruit post-harvest spread of bacteria 

has not been documented. Xcc latent populations do not produce symptoms in harvested fruit 

(Civerolo, 1997). The multiplication of Xcc bacteria associated with lesions is closely related to 

lesion expansion. Xcc multiplies abundantly during lesion expansion but decreases noticeable as 

lesion expansion ceases (Koizumi and Kuhara, 1982). In addition, with the exception of the early 

stages of lesion development, the cells in the center of lesions disintegrate during lesion 

expansion, and during the late stages of lesion expansion, bacterial multiplication becomes 

inhibited at the edges of the lesion as well (Koizumi, 1977a). Bacteria survive in the margin of 

the lesions in citrus leaves and fruit, until they fall off or are removed from the tree (Graham et 

al., 2004). Xcc bacteria do not increase in number on fruit once the fruit is removed from the 

tree; rather, populations decline within the lesions of infected fruit following harvest (Civerolo, 

1981; Koizumi, 1972). 

Several experiments by Gottwald et al. (2009) suggested that the viability of bacteria on fruit and 

in lesions drops off once fruit is harvested, but their observations were inconsistent. In a 2007 

study using naturally infected ‘Ruby Red’ grapefruit, Gottwald et al. (2009) concluded that 

viable Xcc populations generally declined with time when the fruit was stored at 5 to 8°C. 

However, in those experiments, general bacterial population data were variable and although 

bioassay plants formed no lesions when inoculated with washates from fruit stored for 21 days, 

there was no statistical difference among the pretreatment controls and the 21 day results. In a 

related experiment using the lemon cultivar ‘Lisbon’, a statistically significant reduction in both 

total bacterial populations and lesion formation in bioassays after infected fruit was stored for 7 

days at 5 to 8°C (Gottwald et al., 2009). Importantly, in all of the experimental scenarios, no 

harvested mature fruit ever developed new Xcc lesions.
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Golmohammadi et al. (2007) were able to detect viable Xcc on symptomatic fresh citrus fruit in 

11 of 15 shipments from Argentina and Uruguay to Spain. Shipments from which Xcc-infected 

citrus fruit were sampled were certified to have been treated with bactericides [chlorine or 

sodium orthophenylphenate (SOPP)]. These results indicate disinfection protocols are not 100 

percent effective. Some samples were only positive by PCR protocols. The authors concluded 

this was probably due to the disinfection treatments, which would reduce bacterial populations, 

and may induce the non-cultivable state in the analyzed lesions. They further suggested that the 

bacterial cells in the lesions could be stressed after the fruit treatments (washing, disinfection, 

chemical treatments, transport, and storage at low temperatures for variable periods of time). 

Pathogenicity tests were successfully conducted by artificial inoculations, but the 

epidemiological significance of these results was not evaluated. The rating is Low for this risk 

element.

2.5.4 Not detected at the port-of-entry

The likelihood that a pest will not be detected at a port-of-entry is dependent on several factors 

including pest size, mobility, and degree of concealment. 

Anastrepha fraterculus and Ceratitis capitata. In general, internal pests of fruit are likely to 

escape detection. Eggs and larvae of the fruit flies (Ceratitis capitata, Anastrepha fraterculus) 

are borne internally and are quite small (CABI, 2012). Therefore, they would be difficult to 

detect, depending on the age of infestation. Fruit fly-infested fruit can go unrecognized (White 

and Elson-Harris, 1992) even if fruit are dissected. Fruit can show signs of oviposition punctures; 

however, these are often difficult to detect in early stages of infestation (CABI, 2012). Gould 

(1995) examined inspectors’ ability to detect Anastrepha suspensa infesting a variety of fruit and 

found inspectors unable to detect infested grapefruit in most cases, indicating species and variety 

differences in appearance of infested fruit. Consequently this risk element is rated as High.

Cryptoblabes gnidiella and Gymnandrosoma aurantianum. Depending on how recently fruit 

are infested and the extent of infestation, internal feeders may have a high probability of 

escaping detection at a port-of-entry, unless fruit is cut open. Entrance holes of C. gnidiella and 

G. aurantianum on the outside of fruit might be detected by visual inspection, so fruit infested by 

these Lepidoptera are probably easier to detect than fruit infested by fruit flies. For this reason 

we rated this element as Medium. 

Elsinoë australis. The fungus produces distinctive lesions on infected fruit and has been detected 

at the port multiple times, both from Uruguay and other South American countries (Appendix C, 

Tables C1 and C2). Therefore, the rating for “Not Detected at the Port of Entry” is Low.

Xanthomonas citri subsp. citri (Citrus Canker or Xcc). The bacterium produces distinctive 

lesions on infected fruit and has been detected at the port multiple times, both from Uruguay and 

other South American countries (Appendix C, Tables C1 and C2). Therefore, the rating for “Not 

Detected at the Port of Entry” is Low. 

2.5.5 Imported or moved subsequently to an area with an environment suitable for survival

This sub-element considers the geographic location of likely markets and the proportion of the 

commodity that is likely to move to a location suitable for pest survival. Even if an infested 
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commodity enters the country, not all final destinations will have suitable climatic conditions for 

pest survival.

In risk element 1 Climate-Host Interaction, we determined areas in the United States with both 

suitable host plants and suitable climate, where pests have potential for establishment. Fruit that 

arrives in the United States does not arrive in a single state. Rather, the fruit is distributed 

according to market demands through commercial distribution areas. The distribution channels 

and the fact that all fruit is destined for consumption reduce the number of fruit which arrive in 

the potential suitable areas. 

Demographics and the distribution of markets in the United States are strong indicators of the 

ultimate destination of fruit. The distribution of the U.S. population according to the 2000 U.S. 

Census (Figure 3) describes the likely patterns of fruit destined for human consumption (U.S. 

Census Bureau, 2001). Comparing the suitable U.S. Plant Hardiness Zone Map (Magarey et al., 

2008) determined in risk element 1 and the U.S. census map (Figure 3) for each arthropod pest is 

a useful tool in estimating the risk of imported fruit being moved to a suitable habitat. 

Anastrepha fraterculus and Ceratitis capitata. Citrus fruit potentially contaminated with fruit 

flies will be moved to areas suitable for the survival of these pests. Based on the predicted 

distribution of imported citrus fruit in the United States described above and the areas with 

suitable conditions for these pests, the risk associated with this sub-element is estimated to be 

Medium.

Cryptoblabes gnidiella and Gymnandrosoma aurantianum. Both C. gnidiella and G. 

aurantianum can probably survive in Plant Hardiness Zones 6-11. States within these zones 

contain more than 89 percent of the U.S. population (US Census Bureau, 2005), and a significant 

percentage of citrus imports likely would be shipped there. Risk associated with the likelihood 

that these pests will be moved to suitable habitat in the United States is estimated to be High.

Elsinoё australis. Climate mapping showed that E. australis was likely to become established 

only in the Southeast United States and principally in the state of Florida (Thayer et al., 2003) , 

and in 2011, the pathogen had been confirmed and quarantined in five U.S. states: Louisiana, 

Mississippi, Texas, Florida, and Arizona (APHIS-USDA, 2011). With citrus shipped 

proportionally to the populations across the United States (Figure 3), the likelihood that E. 

australis infected fruit will be shipped to a suitable habitat is limited. Therefore the risk rating 

for this element is Medium.

Xanthomonas citri subsp. citri. Three of the four most populous states in the United States, 

Florida, Texas, and California, are in the southern tier of the United States (Figure 3) where the 

climate most closely resembles the native climates for Xcc. With the assumption that citrus is 

distributed across the United States in proportion to the human population an even smaller 

portion of fruit will be distributed to areas with climates suitable for Xcc disease development.

Still there are regions with suitable climates, and therefore, the rating for this risk element is 

Medium.
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Figure 3. U.S. population density, by state, 2000 U.S. Census (U.S. Census Bureau, 2001).

2.5.6 Come into contact with host material suitable for reproduction

The sixth sub-element examines the risk that imported infested fruit will encounter a suitable 

host within the suitable habitat, and a viable reproductive unit of the insect pest or plant pathogen 

associated with the fruit is able to complete its life cycle. Furthermore, for disease development 

to occur, the host must be at a stage that is susceptible to the pathogen, with proper 

environmental conditions. In determining the risk ratings for this element, we considered the 

complete host range of the pest species. This process depends on two factors, the pest’s potential 

for dispersal, and the presence of host material in the region.

Anastrepha fraterculus and Ceratitis capitata. Upon arrival at the port-of-entry, these pests 

could be in various developmental stages inside the fruit, according to their biology and 

temperature required for their development. Thus it is unlikely that all specimens that could be 

present in the fruit could complete their life cycles. Since both fruit fly species are polyphagous 

and adults highly mobile, hosts should be available throughout its potential area of 

establishment. Ceratitis capitata, for instance, has become established sporadically in the 

continental United States (CABI, 2012; Foote et al., 1993). However, C. capitata has not become 

permanently established and is subject to official control when detected. These species have a 

high probability of contacting host material suitable for reproduction, as demonstrated by the fact 

that C. capitata has already done so during past transient outbreaks. The probability that these 

pests will encounter suitable host material is considered High for Anastrepha fraterculus and 

Ceratitis capitata.

Cryptoblabes gnidiella and Gymnandrosoma aurantianum. Cryptoblabes gnidiella and G. 

aurantianum are both polyphagous and attack multiple plant species in multiple families (CABI, 

2012). Also, the adults fly, which increases the likelihood of locating a host and mating (Bento et 

al., 2001; Parra et al., 2004). Consequently, both insects are likely to encounter hosts and become 

established in areas with suitable climates. As evidence of this, C. gnidiella was recently 

introduced into South Africa and has become a pest of lemons (Moore, 2003). For gravid 
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females of either species to come into contact with hosts the following would have to happen: 1) 

multiple infested fruit must be discarded together 2) a male and female emerge, find each other, 

and mate and 3) female flies to a suitable host. The risk rating for this sub-element is Medium.

Elsinoё australis. The suitable climate for E. australis development is limited to Florida (Thayer 

et al., 2003) and other humid southeast citrus production areas. Infection only occurs when there 

is new shoot growth (Timmer et al., 2000). Lesion development on leaves is rare but can occur 

(Bitancourt and Jenkins, 1937). Fruit are only susceptible to E. australis infection for 6-8 weeks 

following petal fall and become less susceptible as they mature (Timmer et al., 2000). According 

to Whiteside (1988b) even if E. australis is more virulent than E. fawcettii on sweet orange fruit, 

it may not create a problem on sweet orange cultivars in Florida unless there is leaf infection.

The pathogen will survive if existing scab pustules retain the infectious conidia (EPPO/CABI, 

1997b). Conidia form abundantly on wet scabs (CABI, 2012). Germination of conidia and 

infection do not require rainfall, but a minimum wet period, via dew, fog, or other high moisture 

conditions of 2.5-3.5 hours, is necessary for conidial infection (CABI, 2012; EPPO/CABI, 

1997b). When these favorable conditions are present, infection and further conidial production 

can occur within 4-6 hours (Whiteside, 1975). Elsinoë australis might present little additional 

threat to sweet orange unless it is able to survive in scab pustules on fruit longer than E. fawcettii

does (Whiteside, 1988b).

Fruit are a known pathway for spreading Elsinoë spp. (EPPO/CABI, 1997b). The closely related 

species E. fawcettii was already established in Florida, and E. australis performs well at both the 

same and higher temperatures than E. fawcettii in laboratory tests (Bitancourt and Jenkins, 1937).

APHIS has recently assessed “ The significance of Citrus spp. fruit as a pathway for the 

introduction or spread of Elsinoë australis, the organism that causes Sweet orange scab disease 

(SOS). We concluded that symptomatic fresh fruit that is commercially packed is not 

epidemiologically significant as a pathway if washed with a surface disinfestant and treated with 

fungicides during packing (PERAL, 2010b). The implementation of a disease management 

program reduces the incidence of SOS infected fruit in the field. Commercial packinghouse 

procedures that include culling, washing with a surface disinfectant, and surface treatment with a 

fungicide-wax destroy fruiting bodies on symptomatic fruit and inhibit further sporulation 

(APHIS-USDA 2010b ; PERAL, 2010b). The potential for establishment is further reduced by 

the unique set of conditions that must be met for infection to occur during the 1.5 hours that any 

spores which may be produced will survive (PERAL, 2010b). Therefore, it is likely that E. 

australis will encounter suitable host and climatic conditions for disease development, as we 

have already seen in five U.S. states, and the rating for this subelement is Low.

Xanthomonas citri subsp. citri (Citrus Canker or Xcc). The development of disease requires 

the presence of the pathogen in an infective stage, the host with susceptible tissues, and favorable 

environmental conditions. It is unlikely that viable bacteria from an infected fruit would 

encounter a suitable host under the conditions required for disease development for several 

reasons. First, the fifteen proven hosts of Xcc are exclusively in the Rutaceae family (CABI, 

2012; Smith et al., 1997; Gottwald et al., 1993; Pereira et al., 1976), particularly Citrus spp.
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Second, the host would need to be in a susceptible state for infection to occur. The majority of 

leaf infection occurs during enlargement (Civerolo, 1984) with the majority of infection 

occurring within the first six weeks (Gottwald and Graham, 2000). Fruit are susceptible to 

infection 90-120 days beginning with petal fall. Fruit can be exposed to several infection cycles 

(Civerolo, 1984; Gottwald et al., 2002a; Gottwald and Graham, 2000). Fruit 2-6 cm in diameter 

are highly susceptible to infection; however, susceptibility reduces as fruit develops (Civerolo, 

1984; Graham et al., 1992a; Graham and Leite Jr., 2004; Verniere et al., 2003). Mature, 

unwounded fruit are not susceptible to infection (Civerolo, 1984; Gottwald and Graham, 2000). 

Mature fruit and leaves are relatively immune to citrus canker because a waxy cuticle builds up 

on maturing fruit and leaves causing the stomata and other natural openings to become plugged 

and less susceptible to pathogen penetration (Albrigo, 1976; Gottwald and Graham, 2000; 

Graham et al., 1992b; NPB, 2002). Therefore, as long as fruit are not wounded during harvest, 

post harvest treatments and packing, susceptible tissue is unlikely to be available. Hosts, 

however, may be available in the unlikely scenario that infected fruit is discarded near hosts in 

residential or commercial plantings.

Third, weather conditions must be appropriate for infection, which often includes dispersal of 

Xcc. Infection is likely when high moisture and wind conditions occur in conjunction with the 

presence of sufficient inoculum and susceptible hosts. The infiltration of bacteria into stomata on 

unwounded fruit or leaves is aided by wind-driven rain, in which wind speeds are in excess of 

eight meters/second; these wind speeds generate sufficient impact force to drive inoculum 

infested water into the stomata (Gottwald et al., 2002a; Graham et al., 2004). Gottwald et al. 

(2009) examined several possible transmission scenarios to ascertain the potential of harvested 

fruit to transmit Xcc in the natural environment. In the first transmission scenario, symptomatic 

fruit that had undergone a typical packinghouse process were placed in cull piles with young 

susceptible trap trees surrounding them. The experiment was conducted in Florida and 

Argentina. In each experiment, treated symptomatic fruit (i.e. were put through the packinghouse 

process) were left in the field for several weeks under natural rain and wind conditions. None of 

the “trap” trees developed citrus canker. 

Gottwald et al. (2009) also tried to create a worst-case scenario by simulating spread with wind 

and rain events. In those experiments, severely infected fruit that were not put through the 

packinghouse process were either placed into elevated cull piles or suspended on vertical strings. 

Trap plants were placed around the infected fruit at distances of 0, 2, 5, and 10 m. An airboat fan 

was used to produce wind at various speeds (1, 10, and 25 m/sec), and garden sprayers were used 

to simulate rain. In all the treatments, only one plant became infected with Xcc. The infected tree 

developed a single lesion at a wound site (likely created by the wind treatment). The infection 

occurred on a plant that was 0 m away from the infected fruit cull pile, and was subjected to 25 

m/sec wind speed. The strength of this wind treatment is likely to only occur in strong storms, 

such as tropical storms. For contrast, a category 1 hurricane starts at 33 m/s on the SaffirSimpson scale (AOML, undated). Whereas the windspeeds used in the experiments were not 

equivalent to a hurricane, personal communications with the authors (December 2008) revealed 

that at the highest wind speed, the trap trees lost approximately 50% of their leaves. During an 

experiment by Shiotani et al. (2009), a typhoon with winds as high as 50 m/sec struck the 

experimental Xcc experimental site. At the time of the storm, fruit artificially contaminated with 
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a traceable strain of Xcc were hung in the field. Shiotani et al. (2009) were unable to recover the 

specific strain of Xcc from any of the fruit harvested after the storm.

Smith et al. (1997) found no authenticated record for diseased fruit playing a role in the 

epidemiology of citrus canker disease). Neither infected fruit with lesions or asymptomatic fruit 

are epidemiologically significant with respect to the initiation of new infections (Anonymous, 

2005a, 2005b; Canteros, 2004; Jetter et al., 2000; USDA, 2007a), although a recent report did 

find 1 of 16 plants became infected when infected fruit were used to as an inoculum source under 

artificially produced conditions of high wind with moisture (Gottwald et al., 2009). Since post 

harvest and packinghouse treatments reduce both the risk would be expected to be much lower. 

Consequently, the risk associated with this sub-element is estimated to be Low.

Table 5. Risk Rating for Likelihood of Introduction. 

Pest Risk elements Cumulative 

Risk Ratinga

Quantity 

Imported

Survive 

Standard 

Production 

and PostHarvest

Survive 

Shipment

Not 

Detected

Moved to 

Suitable 

Area

Contact 

Host 

Material

Anastrepha fraterculus High (3) High (3) High (3) High (3) Med (2) High (3) High (17)

Ceratitis capitata High (3) High (3) High (3) High (3) Med (2) High (3) High (17)

Cryptoblabes gnidiella High (3) Med (2) High (3) Med (2) High (3) Med (2) High (15)

Elsinoё australis High (3) Med (2) High (3) Low (1) Med (2) Low (1) Medium (12)

Gymnandrosoma 

aurantianum

High (3) Med (2) High (3) Med (2) High (3) Med (2) High (15)

Xanthomonas citri 

subsp. citri

High (3) Low (1) Low (1) Low (1) Med (2) Low (1) Low (9)

a

Low is 6-9 points; Medium is 10-14 points; and High is 15-18 points

2.6 Pest Risk Potential

Pest risk potential is an estimate of the risk associated with importation in the absence of 

mitigation. The overall risk potential of a pest is the summation of the Consequences of 

Introduction and Likelihood of Introduction values for that pest. According to the Guidelines for 

Pathway-Initiated Pest Risk Assessments, Version 5.02 (PPQ, 2000), port-of-entry inspection 

provides sufficient phytosanitary security for pests assigned low pest risk potentials, while 

specific phytosanitary measures may be necessary for pests assigned medium pest risk potentials 

and are strongly recommended for pests assigned high pest risk potentials.

Anastrepha fraterculus, Ceratitis capitata, Cryptoblabes gnidiella, and Gymnandrosoma 

aurantianum had High risk ratings for Consequences of Introduction and Likelihood of 

Introduction, resulting in a high pest risk potential. Elsinoё australis and Xanthomonas citri

subsp. citri had ratings resulting in a medium pest risk potential for each (Table 6). 
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Table 6. Pest Risk Potentials

Pest Cumulative Risk Ratings Pest Risk Potential a

Consequences 

of Introduction

Likelihood of 

Introduction

Anastrepha fraterculus High (14) High (17) High (31)

Ceratitis capitata High (15) High (17) High (32)

Cryptoblabes gnidiella High (15) High (15) High (30)

Elsinoё australis Medium (9) Medium (12) Medium (21)

Gymnandrosoma aurantianum High (15) High (15) High (30)

Xanthomonas citri subsp. citri Medium (11) Low (9) Medium (20)

a

Low is 11-18 points; Medium is 19-26 points; and High is 27-33 points

3. Risk Management Options

3.1 Measures for Pest Risk Reduction

The appropriate level of protection for an importing country can be achieved by the application

of a single phytosanitary measure, such as inspection or a quarantine treatment, or a combination 

of measures. The combination of specific phytosanitary measures that provides overlapping or 

redundant safeguards is distinctly different from the use of a single risk mitigation technique. 

Such combinations vary in complexity; however, all require the integration of two or more 

measures that act independently of each other, the cumulative effect achieving the desired level 

of phytosanitary protection (i.e., a systems approach; ISPM No. 14: IPPC, 2007a). Specific 

mitigations may be selected from a range of pre-harvest and post-harvest options, and may

include other safeguarding measures. Measures may be added or the strength of measures 

increased to compensate for uncertainty. At a minimum, for a measure to be considered for use 

in a systems approach, it must be: 1) clearly defined; 2) efficacious; 3) officially required 

(mandated); and 4) subject to monitoring and control by the responsible national plant protection 

organization (IPPC, 2007a). Systems approaches to risk mitigation have been specified in recent 

work plans for the importation of commodities, such as citrus from Chile (Fernandez, 2004) and 

avocado from Mexico (USDA, 2005).

A systems approach to mitigating risks involved with Citrus spp., Citrus hybrids, and Fortunella 

spp. including: sweet oranges (Citrus sinensis (L.) Osb.), lemons (C. limon (L.) Burm.), 

mandarins (C. reticulata Blanco, C. clementina Hort. ex Tan., C. deliciosa Ten., C. unshiu

(Mak.) Marc.), Citrus hybrids, and Citrus-related genus (Fortunella japonica Thunb., F. 

margarita (Lour.) Swing.) from Uruguay might combine a variety of measures. These measures 

may include: 1) certification of pest free areas, pest free places of production, or areas of low 

pest prevalence for certain quarantine pests, such as fruit flies; 2) programs (e.g., mechanical, 

chemical, cultural) to control pests within orchards; 3) preclearance oversight by USDA-APHIS 

officials; 4) packinghouse procedures (e.g., washing with detergent, chemical dips, brushing, 
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culling and inspection of fruit) to eliminate external pests; 5) quarantine treatments to disinfest 

fruit of internal and external pests; 6) consignments inspected and certified by Uruguay’s DGSA 

and APHIS, PPQ to be free of quarantine pests; 7) fruit traceable to state of origin, packing 

facility, grower, and orchard; 8) consignments subject to sampling and inspection after arrival in 

the United States; and 9) limits on distribution and transit within the United States.

We identified the following six quarantine pests that could be introduced with fresh 

commercially produced Citrus, Citrus hybrids, or Fortunella fruit imported from Uruguay: 

Anastrepha fraterculus (South American fruit fly), Ceratitis capitata- Mediterranean fruit fly 

(Medfly), Cryptoblabes gnidiella (honeydew moth), Elsinoë australis (causal agent of sweet 

orange scab disease (SOS)), Gymnandrosoma aurantianum- citrus borer, and Xanthomonas citri 

subsp. citri (causal agent of citrus canker disease (Xcc)). Since quarantine plant pests are likely 

to be present, a risk management strategy is required to mitigate the phytosanitary risks posed by 

these pests. Below we outline options available to mitigate risk of introduction of these 

quarantine pests. 

For the quarantine pathogens Elsinoë australis and Xanthomonas citri subsp. citri, a baseline of 

packinghouse processes and treatments which meet current domestic regulations for these 

pathogens will be required for imported fruit to reduce risk of introduction of these pathogens (7 

CFR § 301.75-1 to 310.75-14,2011; 7 CFR § 305.11, 2010; APHIS-USDA, 2010b ). 

3.2 Phytosanitary Options

This section describes risk mitigation options with discussion of efficacy, if known, and 

application.

3.2.1 Pest-free areas

As a sole mitigative measure, the establishment of pest-free areas or pest-free places of 

production may be completely effective in satisfying an importing country’s appropriate level of 

phytosanitary protection (ISPM # 4, 10, 29; IPPC, 2007a). This option has proven to be 

successful in practice, eliminating the need for post-harvest commodity treatments to achieve 

probit-9-level security (e.g., TDOA, 2003). Establishment and maintenance of pest-free areas or 

production sites should comply with international standards (e.g., ISPM Nos. 4, 10, 29: IPPC, 

2007a; NAPPO, 2004). 

Anastrepha fraterculus and Ceratitis capitata: For example, in surveys for fruit flies, such as 

Anastrepha spp., for which parapheromones are not available, minimal trap density in zones of 

high risk (areas having high probability of fly establishment or introduction) should be five traps 

per km2 (NAPPO, 1998), traps (e.g., McPhail) to be baited with protein hydrolysate (IAEA, 

2003; NAPPO, 2004). To confirm area freedom from A. fraterculus and C. capitata, which are 

currently being monitored in Uruguay (Fruit Fly Surveillance program), surveillance and 

identification would be needed to monitor fruit flies in the area.

The sex pheromone of Gymnandrosoma aurantianum has been discovered, and the active 

ingredients isolated, synthesized, and field-tested (Leal et al., 2001). The resulting 

parapheromone has been developed into a commercial product in Brazil under the trade name 

Ferocitrus Furão®(http://www.ferocitrusfurao.com.br/controlar.htm), which includes the 
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compound in tablet form and a trap (Parra et al., 2004). This pheromone could be used for 

trapping to monitor G. aurantianum populations.

There are various methods available for survey of the remaining arthropods and pathogens,

Cryptoblabes gnidiella, Elsinoë australis, and Xanthomonas citri subsp. citri to establish pest 

free areas. 

3.2.2 Areas of low pest prevalence

According to the IPPC, an area of low pest prevalence may comprise all of a country, part of a 

country, or all or parts of several countries, in which a particular pest species occurs at low 

population densities and which is or are subject to effective surveillance and control or 

eradication measures (ISPM No. 5: IPPC, 2007b). Procedures for the establishment and 

maintenance of areas of low pest prevalence should comply with international standards (e.g., 

NAPPO, 2003; ISPM No. 29: IPPC, 2007a). For example, elements of an operational plan for 

establishment and maintenance of such areas might include a geographic description to delimit 

the area; specification of an upper limit to pest densities; means to document and verify all 

necessary procedures and maintain records; specification of phytosanitary procedures (e.g., 

survey, pest control); and movement controls to prevent pest entry or re-entry into the area. The 

international standards recommend that the exporting country consult with the importing country

in the early stages of implementation to ensure that importing country requirements are met. In 

particular, target or threshold population densities defining an area of low pest prevalence should 

be established in consultation with the importing country.

3.2.3 Control program

Cultural, chemical, or mechanical means (e.g., grove sanitation, pruning of dead and diseased 

branches, pre-harvest application of pesticides, fruit bagging) may be used to eliminate pests 

from groves or prevent fruit infestation. Sanitation and pesticide applications, as essential 

components of best management practices, are mainstays of commercial fruit production (e.g., 

Kirk et al., 2001). For fruit flies, in particular, sterile insect release and other controls may be 

employed as prophylactic measures or in response to pest detection, following guidelines in 

USDA (2003a).

Simple physical barriers, such as paper or plastic bags, may be highly effective in protecting fruit 

from pests. For example, fruit bagging combined with protein bait sprays reduced fruit fly

(Bactrocera and Dacus spp.) infestations in unspecified fruit by up to 98 percent (Sar et al., 

2001). Depending on the timing of the operation (early or late in fruit development), bagging 

reduced infestations of the fruit-boring caterpillar, Deudorix livia (Klug) (Lycaenidae), by 84-98 

percent in pomegranate, Punica granatum (Hussein et al., 1994). In pineapple guava, Feijoa

sellowiana, effective control of Anastrepha fraterculus was achieved if bagging was commenced 

when fruit reached an average diameter of 22 mm (Hickel and Ducroquet, 1994). 

Experimentation is needed to determine the timing of Citrus fruit bagging that will provide 

optimal control of pests in Uruguay. However, despite its high degree of efficacy in preventing 

attack by some insect pests, bagging may increase fruit infestation by others, such as mealybugs 

(Shevale and Khaire, 1998).
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Products frequently used in citrus groves, such as abamectin, chlorpyrifos, and oil sprays, target 

citrus leafminer and rust mites and may be applied before the harvest season. Insecticide 

programs in the grove would also impact Lepidopteran pests, C. gnidiella and G. aurantianum. 

Elsinoë australis: Integrated pest management practices in the grove can also be used to control 

the fungal pathogen, E. australis. These practices may include grove sanitation measures, 

chemical spray programs, barrier zones, or other practices to reduce incidence and severity of 

disease. Spray programs used to control Elsinoë fawcetti, a fungus related to E. australis, would 

also be expected to be effective in controlling sweet orange scab (SOS) caused by E. australis

(EPPO/CABI, 1997b). Products such as thiophanate methyl, azoxytrobin, trifloxystrobin, 

pyraclostrobin, ferbam, and copper fungicides are used to control E. fawcetti and citrus scab 

disease (Garran, 2006; Chung and Timmer, 2005). Barrier zones around export groves help to 

reduce the spread of pathogens from one grove to another (Palacios, 2005). 

Xanthomonas citri subsp. citri: Well-timed field treatments significantly reduce the incidence of 

citrus canker, the level of inoculum, and the number of symptomatic fruit in the field.

Combinations of prophylactic sprays and cultural control practices, such as windbreaks and 

pruning diseased shoots, further reduce disease incidence (Das, 2003; Leite Jr., 2000; Leite and 

Mohan, 1990).

3.2.4 Phytosanitary certification inspections and monitoring

If pest-free areas are established, fruit of Citrus spp., Citrus hybrids, and Fortunella spp. should 

be sampled and inspected periodically during the growing season and after harvest for both 

quality control and phytosanitary precautionary measures. Production areas also should be 

subject to scheduled audits and periodic, unannounced inspections by certified inspectors from 

PPQ and Uruguay’s DGSA. These inspections should insure that production areas meet 

stipulated requirements for the issuance of a phytosanitary certificates required for each 

consignment. This measure is useful for detecting pests present during the growing season that 

may be more difficult to detect post-harvest. Detection methods need to be combined with other 

measures to ensure the absence of pests of concern. Fruit should be sampled and inspected 

periodically during the growing season and after harvest. These measures are useful for detecting 

pests present in the field that may be more difficult to detect post-harvest, but it must be 

combined with other measures to ensure the absence of pests of concern. Statistical procedures 

are available to verify, to a specified confidence level, the pest-free status of an area, given 

negative survey or trapping results (e.g., Venette et al., 2002; Barclay and Hargrove, 2005).

3.2.5 Post-harvest safeguards and packinghouse procedures

Covering containers of harvested fruit with tarpaulins or other covers and moving them to the 

packinghouse in a fruit fly-proof conveyance in a timely manner can prevent infestation (USDA, 

2005). Practices in the grove such as selective harvesting, in which harvesters select only fruit 

visually free of disease symptoms and blemishes, can reduce levels of infested or infected 

harvested fruit (USDA-APHIS-PPQ, 2007). In the packinghouse, fruit may undergo sanitizing, 

washing, mechanical brushing, rinsing, waxing, treatment with fungicides, and drying, as well as 

visual inspection or other treatment to remove external pests and to cull damaged or symptomatic 

fruit. Inspection for internal pests can remove or reduce the risk of introduction of certain pests.

Phytosanitary treatment of fruits to comply with domestic quarantine regulations will be required

(7 CFR § 301.75-1 to 310.75-14, 2011; 7 CFR § 305.11, 2010; APHIS-USDA, 2010b). For 
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citrus canker fruit treatment must include one of the following in accordance with federal 

regulations: (a) fruit must be thoroughly wetted for at least 2 minutes with a solution containing 

200 parts per million sodium hypochlorite; (b) thoroughly wetted with a solution containing 

sodium o-phenyl phenate (SOPP) at a concentration of 1.86 to 2.0 percent of the total solution, 

for 45 seconds if the solution has sufficient soap or detergent to cause a visible foaming action or 

for 1 minute if the solution does not contain sufficient soap to cause a visible foaming action; or 

(c) must be thoroughly wetted for at least 1 minute with a solution containing 85 parts per 

million peroxyacetic acid (7 CFR § 305.11, 2010 ). 

Cryptoblabes gnidiella: Fruit attacked by C. gnidiella, if showing visible symptoms, could be 

removed during the packing inspection process. Cryptoblabes gnidiella feeds in its early stages 

on honeydew on the fruit surface excreted by aphids or mealybugs (Silva and Mexia, 1999) and 

standard commercial processing (washing with detergent-brushing-rinsing-drying-waxingdrying) on the packing line may remove larvae that have not bored into fruit. Later instars 

usually burrow into the fruit and exterior damage and signs on the fruit may allow visual 

inspection to be effective. Inspection in the packinghouse in Uruguay, following by port-of-entry

inspections (for external and internal pests) will reduce numbers of infested fruit that enter the 

United States. 

Gymandrosoma aurantianum: Since females deposit one egg externally on the fruit (Parra et al., 

2004), and larvae, upon hatching, bore into the rind of the fruit (White, 1999), eggs and newly

hatched larvae on the surface of the fruit (prior to larvae boring into the fruit) could be removed 

during standard commercial processing (washing with detergent-brushing-rinsing-dryingwaxing-drying) on the packing line. Removing obviously damaged fruits during the packing line 

inspection or post-packing inspection will also reduce numbers of infested fruit.

Elsinoë australis: Culling procedures used commercially to remove diseased and blemished fruit 

on the packinghouse line in Uruguay can be effective in also removing sweet orange scab (SOS) 

symptomatic fruit by visual inspection. The incubation period (from spore infection to symptoms 

expression) could be up to fourteen days and fruit is only susceptible to infection for up to eight 

weeks after petal fall. As a result, any fruit that is infected will express symptoms during the first 

10 weeks of development. Since all citrus requires more than 3 months for fruit to develop and 

mature, infected fruit will show symptoms well before they are harvested (USDA, 2010) If 

mature fruit that does not show scab symptoms at harvest is not infected and therefore has no 

possibility to be a source of inoculums for the spread of SOS.. 

Xanthomonas citri subsp. citri: Packinghouse processes that cull out fruit with citrus canker 

lesions can reduce numbers of infected fruit packaged. Packinghouse requirements in Uruguay

for cleaning fruit which include mechanical brushing, detergent, sanitizing agents or 

disinfectants, followed by drying, cumulatively reduce levels of Xcc present on the exterior of 

the fruit (Schubert et al., 1999; Brown and Schubert, 1987). Disinfectants for use in the washing 

process, such as sodium hypochlorite, SOPP (sodium orthophenylphenate), peroxyacetic acid 

(PAA) or combinations of products are currently approved by USDA for Xcc decontamination of 

fresh citrus fruit moved interstate from areas quarantined for Xcc within the United States. 

Various studies demonstrated the effectiveness of these disinfectants in reducing numbers of Xcc 
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cells or similar bacteria to low or undetectable levels (Brown and Schubert, 1987; Canteros et al., 

2000; Gottwald et al., 2009; Obata et al., 1969; Parra, 2007; Rybak and Canteros, 2001).

3.2.6. Quarantine treatments

There are several quarantine treatment schedules for citrus fruit specified in the APHIS, PPQ 

Treatment Manual (PPQ, 2008c). These treatment protocols employ heat (e.g. forced air, vapor, 

or hot water: T103-a-1, T103-b-1, T106a, T102-a) cold (e.g. T107-a-1, T107-b-1, T107-c, T107-

k), irradiation (T101-i-1-1) and methyl bromide fumigation (e.g. T101-w-1-2, T101-n-2-1, T101-

j-2-1, T101-j-2), and have been tested and found to be effective in disinfesting citrus fruit of 

pests, with a strong focus on control of fruit flies (Anastrepha and Ceratitis spp.) and external 

pests and may be suitable for citrus fruit from Uruguay. 

Hot-water treatment usually entails dipping fruit in water baths heated to temperatures between 

43° and 49°C, and may provide effective control of arthropod pests and plant pathogens (Fallik, 

2004). For example, immersion of Persian lime, Citrus latifolia, for 20 minutes in water at 49°C 

eliminated infestations of mealybugs, Coleoptera, Hymenoptera, Lepidoptera, Thysanoptera, and 

mites on the fruit surface and within the calyx with no loss of fruit quality (Gould and McGuire, 

2000). Hallman (1998) obtained 100 percent mortality in larvae and adults of Conotrachelus 

nenuphar (Herbst) immersed for 40 minutes in water baths heated to 46°C (a similar protocol 

might prove successful in disinfesting citrus fruit if pests are susceptible to similar high 

temperatures). Results of studies of apricot, Prunus armeniaca, indicated that immersion of fruit 

in water at 46°C for about 10 minutes produced 99 percent mortality in external infestations of 

the tydeid mite, Orthotydeus californicus (Koch) (Jones and Waddell, 1996). Immersion of 

guava for 30 minutes in water heated to 50° C eliminated Pestalotiopsis versicolor (Speg.) 

Steyaert infection while preserving storage quality of the fruit (Madhukar and Reddy, 1990), so 

there may be some potential for use to treat other plant pathogenic fungi. Hot-water treatment 

thus is a risk mitigation option, provided that the appropriate research demonstrates its efficacy

in eliminating infestations of the Anastrepha spp., Ceratitis capitata, and other internal and 

external pests of Citrus fruit in Uruguay.

Cold treatment of Citrus is another option for controlling C. capitata and Anastrepha spp. that 

may infest fruit from Uruguay. 

APHIS has approved irradiation with a minimum generic absorbed pest dose of 150 Gy as a 

treatment for all tephritid fruit flies in fruit, a minimum dose of 400 Gy for all other insects, 

except Lepidoptera pupae and adults (PPQ, 2008d). Therefore, irradiation would be an effective 

pest quarantine treatment for all the insect pests of concern, except for the pupae and adults of G. 

aurantianum, and Cryptoblabes gnidiella.

Treatment of commodities with ionizing radiation, employing x-rays, gamma rays (from 60Co or 

137Cs), or electron beams (beta rays), has been shown to be an effective means of controlling 

pests to achieve quarantine security (Hallman, 2000; Fields and White, 2002). For example, 

based on results of experiments on several species in various hosts, a generic dose of 150 Gy has 

been proposed for the control of pestiferous fruit flies, including Anastrepha spp. (Bustos et al., 

2004; Follett and Armstrong, 2004). At least one study showed that a dose of 400 Gy was 

sufficient to control G. aurantianum in citrus (Faria et al., 1998), but efficacy for both 
Pest Risk Assessment for Citrus from Uruguay

Ver. 9 December 16, 2012

68

Lepidopteran pests (pupae and adults) must be demonstrated. External pests, such as scales, were 

controlled effectively at a dose of 250 Gy (Hara et al., 2002). Hallman (2003) found that a target 

dose as low as 80 Gy (maximal absorbed dose: 92 Gy) was sufficient to prevent development 

and reproduction of Conotrachelus nenuphar in apple, Malus pumila; a comparable dose might 

provide effective control of C. dimidiatus and C. psidii if their biologies are similar. Minimal 

absorbed doses (preventing normal pest development or reproduction) ranging from 50-100 and 

200-350 Gy provided effective control of Aleyrodidae and tetranychid mites, respectively (ISPM 

#18; IPPC, 2007a). Specifically, doses of 100-300 Gy, administered to eggs and adults, resulted 

in sterility in Oligonychus biharensis (Majumder et al., 1996). 

Methyl bromide (CH3Br) fumigation is effective in killing eggs and larvae of internal Diptera 

and Lepidoptera, as well as some scale insects and mites, infesting fresh fruit (Bond, 1984), and 

thus is an option for disinfesting guava of these pests. In one study, for example, methyl bromide 

produced 100 percent mortality in A. suspensa at all dosages tested (16, 32, and 48 g/m3at 24° 

and 30°C); by the ninth day of storage under ideal conditions (10°C at 85-90 percent R.H.), 

fumigated guava fruit had suffered no loss of market quality (Witherell, 1983). Further research 

is needed to determine the efficacy of fumigation for the control of the Anastrepha spp. and other 

quarantine-significant Citrus fruit pests in Uruguay.

The probit-9-level security afforded by a quarantine treatment may be overwhelmed by a large 

volume of infested fruit (Powell, 2003). For this reason, adoption of a particular quarantine 

treatment should be in conjunction with efforts to maintain pest populations in production zones 

below specified densities (e.g., 0.01 fruit fly trap-1day-1; DeHaven, 2005), as would satisfy

requirements for the establishment of areas of low pest prevalence (ISPM #22; IPPC, 2007a).

3.2.7. Point-of-entry sampling and inspection

Upon arrival in the United States, consignments should be inspected, with particular attention 

given to paperwork and seals on vehicles, to ascertain that the chain of custody has remained 

intact. A random sample of fruit from each consignment should be inspected to detect a pest

infestation rate of 10 percent or greater (Page 4-3; PPQ, 2008a).

Gymandrosoma aurantianum: Fruit attacked by the citrus borer can develop lesions (CABI, 

2007) and a necrotic area in the rind around the larval entrance hole; the fruit either drops 

prematurely or the fruit becomes discolored and easily distinguishable from that of the healthy

fruit (White and Tuck, 1993). Frass around the entrance hole is also very likely to be present (as 

occurs for codling moth; Metcalf and Metcalf, 1993). Because of the nature of the damage and 

the biology of the pest, detection through inspection should be effective. Inspection for this 

lepidopteran, G. aurantianum, is currently required by APHIS for citrus from Peru (part 41: 7 

CFR § 319.56, 2008). To certify inspections and fruit freedom from the citrus borer, a 

phytosanitary certificate can be issued by the country’s NPPO. 

3.2.8 Limits on distribution and transit within the United States

Under § 412(a) of the Plant Protection Act (U.S., 2000), the Secretary of Agriculture may

prohibit or restrict the movement in interstate commerce of any plant or plant product if the 

Secretary determines that the prohibition or restriction is necessary to prevent the dissemination 

of a plant pest within the United States. The actions the Secretary may take under this paragraph 

include limiting the importation or distribution of a plant or plant product to certain States. 
Pest Risk Assessment for Citrus from Uruguay

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69

Limiting distribution of citrus fruit imported or moved from areas where citrus diseases are 

present prevents the introduction of the diseases into those States that have the highest likelihood 

for introduction of the diseases, due to the density of citrus plantings in those States. Outside of 

commercial citrus-producing States, conditions under which citrus diseases could be introduced 

or established are far less likely to prevail.

Limiting imports of Citrus to certain time periods can also be an effective way to reduce risk of 

pest introduction, for example shipping Citrus fruit from Uruguay when the fruit fly populations 

are lowest would reduce risk of entry of A. fraterculus and C. capitata. 

3.3 Oversight

3.3.1 Pre-shipment programs

Inspection, treatment, or other mitigation measures performed in the orchard and packinghouse

should be under the direct supervision of qualified APHIS and DGSA personnel, and in 

accordance with specified phytosanitary procedures. Such programs require monitoring all 

aspects of the application of any required phytosanitary measures and also aim to identify

shortcomings or opportunities for program modifications (ISPM # 14; IPPC, 2007a). Provision 

should be made for the formal recognition of approved areas, sites, or producers, as well as the 

specification of conditions for revoking approvals or refusing certification for export to the 

United States.

3.3.2 Shipments traceable to place of origin in Uruguay

A requirement that Citrus spp., Citrus hybrids, and Fortunella spp. be packed in containers with 

identification labels indicating the specific place of origin is necessary to ensure traceability to 

each production site.

3.4 Conclusions

The number and diversity of pests potentially infesting Citrus imports make it unlikely that a 

single mitigation measure will be adequate to reduce risk of their introduction into the United 

States. For this reason, a combination of measures in a systems approach, including orchard 

monitoring and management programs to achieve and maintain area pest freedom or low pest 

prevalence, packinghouse inspection and treatments, quarantine treatments, and maintenance of 

consignment security and traceability in transit, is most feasible. Options for risk mitigation are 

summarized in Table 7.

This document does not purport to establish specific work plans or to evaluate the quality of a 

specific program or systems approach. It identifies risks and provides information regarding 

known mitigation measures. The specification and implementation of measures, as would be 

present in an operational work plan, is beyond the scope of this document.
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70

Table 7. Summary of risk mitigation options for Citrus spp., Citrus hybrids, and Fortunella spp.

from Uruguay.

Measure(s) Pests Efficacy

Pest-free areas or places of 

production

All Satisfies requirements for 

appropriate level of 

protection

Areas of low pest prevalence All Typically would require 

additional measures.

Control program All Research required to 

demonstrate efficacy

Phytosanitary certification 

inspections and monitoring

Monitoring could work effectively 

for all pests, although tools and 

techniques would need to be 

validated

Some pests would be likely

to escape detection in 

phytosanitary inspections, 

such as internal pests or 

pathogens with a latent 

phase. 

Post-harvest safeguards and 

Packinghouse procedures

Fruit cleaning: Xanthomonas citri

subsp. citri (Xcc), when washing, 

sanitizing, drying etc. are done in a 

prescribed required program that 

shows effective removal of pests

(7 CFR § 305.11. 2010)

Fruit waxing/fungicide treatment:

Elsinoe australis (APHIS-USDA,, 

2010b)

Culling/inspection: obvious 

symptomatic fruit for Xcc, Elsinoe

australis, Lepidopteran boring (C. 

gnidiella, G. aurantianum).

Obvious symptomatic or 

damaged fruit can be 

removed, but internal pests 

or latent pathogens would be 

difficult to detect and 

remove.

Quarantine treatments

Hot-water treatment 

combined with low pest 

prevalence

Anastrepha fraterculus, Ceratitis 

capitata

APHIS-recognized 

quarantine treatment

Cold treatment with low pest 

prevalence

Anastrepha fraterculus, Ceratitis 

capitata

APHIS-recognized 

quarantine treatment

Irradiation combined with 

low pest prevalence

All insect pests (except pupae and 

adults of Gymnandrosoma 

aurantianum)

APHIS-recognized 

quarantine treatment

All other pests Potential probit-9; research 

required to demonstrate 

efficacy

Methyl bromide fumigation 

combined with low pest 

Anastrepha spp., C. capitata, APHIS-recognized 

quarantine treatment
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71

Measure(s) Pests Efficacy

prevalence

Point-of-entry sampling and 

inspection

Fruit flies (internal sampling), X. 

citri subsp. citri, and E. australis

(if symptomatic)

Some pests would be likely

to escape detection in 

phytosanitary inspections, 

such as internal pests (fruit 

flies, Lepidoptera), 

pathogens with a latent 

phase (E. australis,), or 

organisms which are too tiny

to see 

3.5 Contacts, Authors, Contributors, and Reviewers

APHIS Contact

Robert Griffin

APHIS Authors/Reviewers and Contributors

Betsy L. Randall-Schadel, Risk Analyst/Plant Pathologist

Lisa M. Ferguson, Risk Analyst/Plant Pathologist

Walter Gutierrez, Risk Analyst/Plant Pathologist

Shawn Robertson, Risk Analyst/Entomologist

Gary L. Cave, Senior Risk Analyst/Entomologist

Tony Koop, Risk Analyst/Botanist

DGSA Authors/Contributors

María Inés Ares, Director of Plant Protection Division, MGAP/DGSA

Beatriz Melcho, Sub Director of Plant Protection Division, MGAP/DGSA

Elina Zefferino, Citrus Health Department, MGAP/DGSA

Enrique Verdier, Bacteriologist, MGAP/DGSA

Luis Díaz, Plant Pathologist, MGAP/DGSA

Isabel Frioni, Entomologist, MGAP/DGSA

Iris B. Scatoni, Entomologist, Faculty of Agronomy

Carlos Bentancourt, Entomologist, Faculty of Agronomy

Gabriela Asplanato, Entomologist, Faculty of Agronomy

Roberto Bernal, Plant Pathologist, National Research Institute (INIA)

Jose Buenahora, Entomologist, National Research Institute (INIA)

Gonzalo Arocena, Citrus Exporters Chamber

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5. Appendices

Appendix A. Citrus Pest Surveillance information provided by DGSA

Citrus Canker: From 1977-2002, the DGSA had a Citrus Canker Prevention and Eradication 

Campaign. In 1997, the introduction of Phyllocnistis citrella (leaf miner) and especially 

favorable climatic conditions (El Niño phenomenon) led to an increase in the incidence of the 

disease. This climate change in combination with the arrival of the leaf miner changed the 

distribution pattern of citrus canker. Due to leaf miner injury, the clustered distribution that was 

common in previous years changed to aggregated and random distribution patterns.During the 

eradication campaign, the DGSA destroyed 505,085 plants (9 percent of existing plants on nearly 

1,300 hectares). Citrus canker A (or Asiatic citrus canker, X. citri subsp. citri) was detected in 

Salto (1979), Paysandú (1981), Rivera (1995), and Río Negro (1997) in the North, and in San 

Jose in the South (2002). Citrus canker B (originally from South America, X. axonopodis pv. 

aurantifolii), which causes canker on lemon, Mexican lime, sour orange, and pummelo, was 

eradicated in 1985; between 1977 and 1985, 2,970 infected plants were detected and 12,804 were 

eradicated.

In the North, disease incidence (plants and fruit) varies by the place of production and the 

cultivars grown. In the South, the prevalence is 9 percent and the incidence 1 percent; therefore, 

there are citrus-canker-free places of production. Prevalence means the number of places of 

production where the disease is present over the total places of production, including domestic 

groves. Disease incidence was calculated by dividing the number of affected plants by the total 

number of plants in the area (Zadoks and Schein, 1979).

Citrus Black Spot: In 1996, the DGSA made the first national survey for G. citricarpa: all 

citrus production areas were included and 1,448 samples were tested by incubating 

asymptomatic fruit at 27–29 o C under high humidity for 13-17 days to stimulate development of 

citrus black spot (CBS) symptoms/signs. If symptoms or signs appeared, specific lab protocols were 

followed to complete pathogen identification (MGAP-DGSA, 2000). No G. citricarpa was 

detected in this survey. In 1999, within the Citrus Fruit Phytosanitary Certification System for 

export (CFPCS), the DGSA established the Black Spot Surveillance program and inspected 

places of production and packinghouses.

Since this time, the DGSA has provided training activities at different levels for official 

personnel, technicians, workers at citrus companies, and growers. In 2000, the second national 

survey (690 samples) was conducted with induction testing, and again G. citricarpa was not 

detected.

In 2001, the EPPO Reporting Service (109, 2001 No. 9) published an interception from the 

Netherlands, but the DGSA did not receive notification from either the European Commission or 

an individual European country. The information from the exporters indicated that no lot was 

refused for this disease. For that reason the DGSA suspects that it was a mistake from EPPO and 

sent a letter informing EPPO of the error. However, in 2004, the disease was detected in groves 

of Valencia orange during regular surveys on places of production for the domestic market.

The DGSA continues to find G. citricarpa in crops for the domestic market in Valencia orange 

in the North and lemon in the South. It has also been detected in lemon with a prevalence of 3.9
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percent (6 out of 154 groves were found to have G. citricarpa) in the places of production 

registered in the CFPCS for export fruit.

The prevalence in the North is 5.3 percent (5/95), and 1.7 percent (1/59) in the South. The grove 

in the south is in Soriano Department, outside the main Southern citrus production area. The 

prevalence in the lemon production blocks is 16.4 percent (12/73) in the North and 9.4 percent

(3/32) in the South.

Low prevalence in the groves for export fruit is due to the application of preventive measures, 

such as use of healthy propagative material, windbreaks in all production fields, field treatments 

for fungal diseases and citrus canker, and management of the fruit (total harvest). The DGSA’s 

actions include continued surveillance in the export system, epidemiological studies, and 

application of chemical control measures. In addition, surveillance specific for this disease will 

be conducted next year (induction test) to determine the prevalence of the disease in all citrus 

areas.

Fruit flies: The fruit flies present in Uruguay are the Mediterranean fruit fly (Ceratitis capitata) 

and the South American fruit fly (Anastrepha fraterculus). Their presence in Argentina and 

Uruguay was first reported in the early 20th century. In Uruguay, they were declared as 

agricultural pests in 1937, and there are bibliographic references related to their study and 

control programs from that time up to the present. In the last decades an important effort was 

made in Uruguay to conduct studies to obtain updated information about the species present in 

the country, their host ranges, and to evaluate integrated management control measures and 

eradication programs.

The DGSA implemented the National Surveillance System for Fruit Flies in 2001. The objective 

was to establish an official monitoring network to collect and preserve permanent and reliable 

data about the fruit fly species present in the country, their hosts, and the characteristics of pest 

population. The information obtained from the National Surveillance System for Fruit Flies is 

useful for: 

 Identifying population fluctuations of the fruit flies present in the country.

 Determining and analyzing general and regional variations in the pest populations 

throughout the year, interactions with climatic conditions, and phenology of the different 

citrus species and varieties. This information and analysis assists in making pest 

management decisions as well as evaluating which of the export varieties are of higher 

risk.

 Obtaining updated and historical information to support negotiations in international 

trade. 

 Detecting, in an appropriate manner, the presence of exotic pests in the country.

The population fluctuations of C. capitata and A. fraterculus from 2003 to 2006 in the main 

citrus area are illustrated in the following figures (Figures 4 and 5). It appears that the earliest 

harvest and export begins with mandarins in late February to March. The highest levels of 

harvest and export, which includes lemons, most orange varieties (except Valencia), many 

mandarin varieties, and grapefruits, occur during June, July, and August, when fruit fly 

populations are not typically at their peak. The majority of harvest and exports finish at the end 
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of September. The exceptions to the harvest and export calendar are Valencia oranges, whose 

harvest stretches from July to December. January and February are the two months in which little 

or no Citrus spp. are harvested or shipped. Harvesting and shipping when fruit fly populations 

are lowest will minimize the risk of introduction of these fruit flies into importing countries. 

From February 2004 to October 2006, the DGSA conducted a special survey to gather scientific 

information to identify which Citrus species or varieties are hosts of Anastrepha fraterculus. The 

fruit was sampled from the field, based on information provided by the Surveillance System, 

when the number of Flies per Trap per Day (FTD) for Anastrepha was greater than Ceratitis

FTD and from the packinghouse from damaged fruit. All the larvae were identified by the DGSA 

laboratory.

Six-hundred and fifteen samples were collected from groves with different species and varieties: 

 518 samples were negative for Tephritidae.

 Ceratitis capitata was detected in 49 samples.

 Anastrepha fraterculus was detected in 48 samples.

 As of 2006, the results of 28 samples are pending.

Anastrepha fraterculus was confirmed on varieties of pink and white grapefruits (43 samples), 

T. Ortanique (tangor = C. reticulata Blanco x C. sinensis) (3 samples) and Valencia oranges (2 

samples).

During 2005–2006, 26 samples (fruits/larvae) from the packinghouses were sent to the 

laboratory. Eight samples contained C. capitata, 11 samples had A. fraterculus, and 7 samples 

were negative. The samples in which A. fraterculus was confirmed were pink and white 

grapefruits (6 samples) and T. Ortanique (5 samples).

Based on the above-mentioned survey, A. fraterculus and C. capitata were not detected in lemon, 

although as shown in Figure 5 there are populations of both fruit flies in the Southern part of the 

country. As mentioned in 1.2.2, 15 percent of the Citrus production area is located in the 

Southern part of the country, where mainly lemon is planted (70 percent).
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Appendix B. Selected Plant Pest Interception Records

Table B1. Pests Intercepted On Citrus spp. from South America (1985 - 2007) (PestID, 2007). 

*Non-Rep* indicates that the pest was non reportable. Interceptions that occurred less than 5 

times since 1985 are considered relatively rare, and may reflect anomalies in the data or errors in 

identification.

Scientific Name (taxonomic affiliation) Interceptions (no.)

Acremonium sp. (Hyphomycetes) 1

Acutalis sp. (Membracidae) 1

Acutaspis rhizophorae (Cockerell) (Diaspididae) 4

Acutaspis sp. (Diaspididae) 2

Aelia acuminata (Linnaeus) (Pentatomidae) 1

Aeolus nigromaculatus Drapiez (Elateridae) 1

Agallia sp. (Cicadellidae) 1

Agromyzidae, Species of 2

Aleurocanthus woglumi Ashby (Aleyrodidae) 3

Aleurodothrips fasciapennis (Franklin) (Phlaeothripidae) *Non-Rep* 2

Aleurodothrips sp. (Phlaeothripidae) *Non-Rep* 1

Aleurolobus marlatti (Quaintance) (Aleyrodidae) 1

Aleurothrixus floccosus Maskell (Aleyrodidae) *Non-Rep* 4

Aleurothrixus sp. (Aleyrodidae) 2

Aleurotrachelus sp. (Aleyrodidae) 1

Aleyrodes sp. (Aleyrodidae) 1

Aleyrodidae, Species of 7

Alleculinae, Species of (Tenebrionidae) *Non-Rep* 1

Alternaria sp. (Hyphomycetes) *Non-Rep* 2

Amyelois transitella (Walker) (Pyralidae) *Non-Rep* 1

Anastrepha sp. (Tephritidae) 37

Anaxipha sp. (Gryllidae) 1

Anomala sp. (Scarabaeidae) 1

Aonidiella aurantii (Maskell) (Diaspididae) *Non-Rep* 32

Aonidiella citrina (Coquillett) (Diaspididae) *Non-Rep* 1

Aonidiella comperei Mckenzie (Diaspididae) 2

Aonidiella inornata Mckenzie (Diaspididae) 3

Aonidiella SP. (Diaspididae) 7

Aphididae, Species of 4

Arctiidae, Species of 1

Ascochyta citri Penz. (Coelomycetes) 2

Ascochyta sp. (Coelomycetes) 1

Aseminae, Species of (Cerambycidae) *Non-Rep* 1

Aspidiotus excisus Green (Diaspididae) *Non-Rep* 1

Aspidiotus nerii Bouche (Diaspididae) *Non-Rep* 1

Aulacaspis tubercularis Newstead (Diaspididae) 12

Aulacorthum solani (Kaltenbach) (Aphididae) *Non-Rep* 1

Aureobasidium sp. (Hyphomycetes) 1

Baridinae, Species of (Curculionidae) 1

Blapstinus sp. (Tenebrionidae) 6

Brevipalpus chilensis Baker (Tenuipalpidae) 6
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Scientific Name (taxonomic affiliation) Interceptions (no.)

Brevipalpus obovatus Donnadieu (Tenuipalpidae) *Non-Rep* 2

Brevipalpus sp. (Tenuipalpidae) 3

Camarosporium sp. (Coelomycetes) 1

Camponotus sp. (Formicidae) *Non-Rep* 1

Carabidae, Species of *Non-Rep* 1

Cecidomyiidae, Species of 1

Cephaleuros virescens Kunze (Trentepohliaceae) *Non-Rep* 1

Ceraspis sp. (Scarabaeidae) 1

Ceratitis capitata (Wiedemann) (Tephritidae) 16

Ceratitis sp. (Tephritidae) 1

Cercospora sp. (Hyphomycetes) 2

Charidotella sp. (Chrysomelidae) 1

Chrysomelidae, Species of 1

Chrysomphalus aonidium (Linnaeus) (Diaspididae) *Non-Rep* 6

Chrysomphalus dictyospermi (Morgan) (Diaspididae) *Non-Rep* 1

Chrysomphalus pinnulifer (Maskell) (Diaspididae) 2

Chrysomphalus sp. (Diaspididae) 3

Cicadellidae, Species of 2

Cladosporium citri Mass. (Hyphomycetes) *Non-Rep* 1

Cladosporium sp. (Hyphomycetes) 34

Coccidae, Species of 12

Coccostroma sp. 2

Coccus hesperidium (Linnaeus) (Coccidae) *Non-Rep* 1

Coccus viridis (Green) (Coccidae) 7

Coleoptera, Species of 1

Colletotrichum acutatum J.H. Simmonds (Coelomycetes) *Non-Rep* 4

Colletotrichum gloeosporioides (Penz) Penz & Sacc. (Coelomycetes) *NonRep*46

Colletotrichum sp. (Coelomycetes) 16

Coniothyrium sp. (Coelomycetes) 1

Conoderus sp. (Elateridae) 1

Conoderus varians (Steinheil) (Elateridae) 3

Contarinia sp. (Cecidomyiidae) 1

Copitarsia sp. (Noctuidae) 1

Corylophidae, Species of *Non-Rep* 1

Cryptoblabes gnidiella (Milliere) (Pyralidae) 1

Cryptophlebia sp. (Tortricidae) 1

Dead organism *Non-Rep* 7

Diabrotica sp. (Chrysomelidae) 1

Dialeurodes citri (Ashmead) (Aleyrodidae) *Non-Rep* 1

Dialeurodes citrifolii (Morgan) (Aleyrodidae) *Non-Rep* 1

Dialeurodes sp. (Aleyrodidae) 1

Diaphorina citri Kuwa Yama (Psyllidae) 1

Diaporthe arctii (Lasch) Nits. 1

Diaporthe citri Wolf (Valsaceae) *Non-Rep* 34

Diaspididae, Species of 141

Didymella sp. (Pleosporaceae) 1
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Scientific Name (taxonomic affiliation) Interceptions (no.)

Didymosphaeria sp. (Didymosphaeriaceae) 1

Digitaria insularis (Linnaeus) Fedde (Poaceae) *Non-Rep* 1

Diplodia sp. (Coelomycetes) 3

Diptera, Species of 4

Dorylaimidae, Species of *Non-Rep* 1

Dothiorella sp. (Coelomycetes) 1

Drosophilidae, Species of *Non-Rep* 1

Dynastinae, Species of (Scarabaeidae) 1

Dysmicoccus sp. (Pseudococcidae) 2

Ecdytolopha sp. (Tortricidae) 3

Echidnodes sp. 1

Echoma sp. (Chrysomelidae) 1

Elsinoe annonae Bitanc. & Jenkins (Elsinoaceae) 1

Elsinoe australis Bitanc. & Jenkins (Elsinoaceae) 9879

Elsinoe fawcetti Bitanc. & Jenkins (Elsinoaceae) *Non-Rep* 20

Elsinoe sp. (Elsinoaceae) 46

Epermeniidae, Species of 1

Epicoccum sp. *Non-Rep* 1

Eucalandra sp. (Dryophthoridae) 1

Euplatypus parallelus (Fabricius) (Platypodidae) *Non-Rep* 1

Fiorinia sp. (Diaspididae) 1

Fiorinia theae Green (Diaspididae) *Non-Rep* 1

Frankliniella sp. (Thripidae) 2

Fusarium sp. (Hyphomycetes) 6

Fusicoccum sp. (Coelomycetes) 2

Gelechiidae, Species of 3

Geometridae, Species of 1

Geotrichum sp. *Non-Rep* 1

Gnomoniella sp. 1

Gracillariidae, Species of 1

Gryllus sp. (Gryllidae) 1

Guignardia citricarpa Kiely (Botryosphaeriaceae) 1107

Guignardia sp. (Botryosphaeriaceae) 1

Gymnandrosoma sp. (Tortricidae) 1

Helicellidae, Species of 1

Helicotylenchus pseudorobustus Steiner (Golden) (Hoplolaimidae) *NonRep*1

Helicotylenchus sp. (Hoplolaimidae) 1

Hemiberlesia lataniae (Signoret) (Diaspididae) *Non-Rep* 3

Hemiberlesia rapax (Comstock) (Diaspididae) *Non-Rep* 1

Hemiberlesia sp. (Diaspididae) 1

Hesperiidae, Species of 1

Heteroptera, Species of 2

Homoptera, Species of 1

Hypothenemus sp. (Scolytidae) 1

Icerya sp. (Margarodidae) 1

Injury sp. *Non-Rep* 25
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Scientific Name (taxonomic affiliation) Interceptions (no.)

Insecta, Species of 1

Karnyothrips sp. (Phlaeothripidae) *Non-Rep* 2

Lepidoptera, Species of 1

Lepidosaphes beckii (Newman) (Diaspididae) *Non-Rep* 35

Lepidosaphes bladhiae Takahashi (Diaspididae) 1

Lepidosaphes gloverii (Packard) (Diaspididae) *Non-Rep* 7

Lepidosaphes sp. (Diaspididae) 2

Lepidosaphes tapleyi Williams (Diaspididae) 1

Lepidosaphes tokionis (Kuwana) (Diaspididae) 1

Leprosis, sp. *Non-Rep* 1

Leptodothiorella sp. 1

Leptosphaeria sp. (Leptosphaeriaceae) 1

Lestodiplosis sp. (Cecidomyiidae) *Non-Rep* 3

Lonchaeidae, Species of 2

Margarodidae, Species of 2

Melanaspis sp. (Diaspididae) 2

Meloidogyne sp. (Meloidogynidae) 1

Membracidae, Species of 1

Metamasius dimidiatipennis (Jekel) (Dryophthoridae) 1

Microsphaeropsis sp. (Coelomycetes) 3

Miogryllus convolutus (Johansson) (Gryllidae) 1

Miyagia pseudosphaeria (Mont.) Jørst. (Pucciniaceae) 1

Monomorium destructor (Jerdon) (Formicidae) *Non-Rep* 1

Morganella longispina (Morgan) (Diaspididae) *Non-Rep* 1

Murraya sp. (Rutaceae) *Non-Rep* 2

Mycetaspis personata (Comstock) (Diaspididae) *Non-Rep* 8

Mycetaspis sp. (Diaspididae) 2

Mycosphaerella sp. (Mycosphaerellaceae) 2

Nasonovia ribisnigri (Mosley) (Aphididae) *Non-Rep* 1

Nasonovia sp. (Aphididae) 1

No identifiable insecta found *Non-Rep* 6

No identifiable pathogen found *Non-Rep* 16

No pathogen found *Non-Rep* 2

No specimen found *Non-Rep* 2

Noctuidae, Species of 2

Oecophoridae, Species of 1

Olethreutinae, Species of (Tortricidae) 3

Oryza sp. Red rice (Poaceae) 1

Paragryllus temulentus Saussure (Gryllidae) 1

Paraleyrodes sp. (Aleyrodidae) 1

Parasaissetia nigra (Nietner) (Coccidae) *Non-Rep* 2

Paratettix sp. (Tetrigidae) 2

Parisoschoenus sp. (Curculionidae) 2

Parlatoria cinerea Hadden (Diaspididae) 3544

Parlatoria citri Mckenzie (Diaspididae) 2

Parlatoria crypta Mckenzie (Diaspididae) 2

Parlatoria pergandii Comstock (Diaspididae) *Non-Rep* 10
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Scientific Name (taxonomic affiliation) Interceptions (no.)

Parlatoria sp. (Diaspididae) 28

Parlatoria vandae Mckenzie (Diaspididae) *Non-Rep* 1

Parlatoria ziziphi (Lucas) (Diaspididae) 8654

Pentatomidae, Species of 3

Pentatomoidea, Species of 1

Pestalotiopsis sp. (Coelomycetes) 4

Pheidole sp. (Formicidae) 2

Phenacoccus sp. (Pseudococcidae) 2

Phlaeothripidae, Species of 9

Phoma sp. (Coelomycetes) 16

Phomopsis citri Fawc. (Coelomycetes) *Non-Rep* 1

Phomopsis sp. (Coelomycetes) 6

Phthia picta (Drury) (Coreidae) *Non-Rep* 1

Phyllosticta citricarpa (Mcalpine) Aa (Coelomycetes) 94

Phyllostictina hypoglossi (Mont.) Petr. & Syd. 1

Pinnaspis aspidistrae (Signoret) (Diaspididae) *Non-Rep* 5

Pinnaspis strachani (Cooley) (Diaspididae) *Non-Rep* 7

Planococcus citri (Risso) (Pseudococcidae) *Non-Rep* 4

Planococcus minor (Maskell) (Pseudococcidae) 4

Planococcus sp. (Pseudococcidae) 15

Pleospora sp. (Pleosporaceae) 1

Plutellidae, Species of 1

Protopulvinaria longivalvata Green (Coccidae) 2

Pseudaonidia trilobitiformis (Green) (Diaspididae) 512

Pseudaulacaspis cockerelli (Cooley) (Diaspididae) *Non-Rep* 1

Pseudaulacaspis sp. (Diaspididae) 28

Pseudococcidae, Species of 89

Pseudococcus cryptus Hempel (Pseudococcidae) 1

Pseudococcus landoi (Balachowsky) (Pseudococcidae) 1

Pseudococcus sp. (Pseudococcidae) 6

Pseudoparlatoria sp. (Diaspididae) 1

Pseudorobillarda sp. 1

Psyllidae, Species of 1

Psyllobora sp. (Coccinellidae) *Non-Rep* 1

Pterophoridae, Species of 1

Puccinia sp. (Pucciniaceae) 1

Pyralidae, Species of 2

Pyralinae, Species of (Pyralidae) 1

Pyraustinae, Species of (Crambidae) 1

Rhyparochromidae, Species of 1

Rhyparochromus quadratus (Fabricius) (Rhyparochromidae) 1

Saissetia neglecta Delotto (Coccidae) *Non-Rep* 1

Sancassania sp. (Acaridae) *Non-Rep* 1

Saprophyte sp. *Non-Rep* 2

Scirtidae, Species of *Non-Rep* 1

Scythridinae, Species of (Coleophoridae) 1

Secondary fungi *Non-Rep* 1
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Scientific Name (taxonomic affiliation) Interceptions (no.)

Selenaspidus articulatus (Morgan) (Diaspididae) *Non-Rep* 5

Selenaspidus sp. (Diaspididae) 1

Septoria sp. (Coelomycetes) 11

Silvanidae, Species of *Non-Rep* 1

Sinoxylon anale Lesne (Bostrichidae) *Non-Rep* 1

Sphaceloma fawcettii Bitanc. & Jenkins var. scabiosa (Mcalp. & Tryon) 1

Sphaceloma punicae Bitanc. & Jenkins (Coelomycetes) 1

Stemphylium sp. (Hyphomycetes) 1

Strabala sp. (Chrysomelidae) 1

Syngenaspis parlatoriae Sulc (Diaspididae) 1

Tarsonemus sp. (Tarsonemidae) 26

Tenebroides sp. (Trogossitidae) *Non-Rep* 1

Tephritidae, Species of 3

Tetraleurodes sp. (Aleyrodidae) 1

Tetranychidae, Species of 1

Tetranychus sp. (Tetranychidae) 2

Thripidae, Species of 3

Tortricidae, Species of 4

Tortricinae, Species of (Tortricidae) 1

Trioza anceps Tuthill (Psyllidae) 1

Tydeidae, Species of *Non-Rep* 1

Unaspis citri (Comstock) (Diaspididae) *Non-Rep* 9

Unaspis yanonensis (Kuwana) (Diaspididae) 1

Vinsonia stellifera (Westwood) (Coccidae) 3

Xanthomonas axonopodis pv. citri (Hasse) Dye (Xanthomonadaceae) 90

Xanthomonas campestris (Pam.) Dows. (Xanthomonadaceae) *Non-Rep* 23

Xanthomonas campestris pv. citri (Hasse) Dye (Xanthomonadaceae) 374

Xanthomonas sp. (Cancrosis B) 1

Xanthomonas sp. (Xanthomonadaceae) 6

Grand Total 25450
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Table B2. Pests intercepted on Citrus spp. arriving from Uruguay (1985 – 2008) (PestID, 

2008).

Host Host Part Where Intercepted Pest Records

Citrus limon Fruit Stores Aonidiella aurantii 1

Citrus limon Fruit Stores Aonidiella orientalis 1

Citrus reticulata Not reported Quarters Aonidiella Sp. 1

Citrus sinensis Fruit Stores Aonidiella Sp. 1

Citrus aurantiifolia Fruit Stores Chrysomphalus aonidum 1

Citrus sinensis Fruit Baggage Colletotrichum Sp. 1

Citrus sinensis Fruit Stores Coniothyrium Sp. 1

Citrus reticulata Fruit Quarters Diaporthe citri 1

Citrus sinensis Stores Diaporthe citri 1

Citrus sp. Fruit Permit cargo Diaporthe citri 1

Citrus sinensis Fruit Quarters Diaspididae 1

Citrus aurantiifolia Fruit Stores Elsinoe australis 1

Citrus limon Fruit Baggage Elsinoe australis 1

Citrus limon Fruit Stores Elsinoe australis 1

Citrus limon Fruit Stores Elsinoe australis 1

Citrus limon Fruit Stores Elsinoe australis 1

Citrus nobilis Fruit Stores Elsinoe australis 1

Citrus reticulata Fruit Quarters Elsinoe australis 1

Citrus reticulata Fruit Stores Elsinoe australis 1

Citrus reticulata Fruit Stores Elsinoe australis 1

Citrus reticulata Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis) 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1
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Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Baggage Elsinoe australis 1

Citrus sinensis Fruit Baggage Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Miscellaneous Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Quarters Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Miscellaneous Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Baggage Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Baggage Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Quarters Elsinoe australis 1
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Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Not reported Stores Elsinoe australis 1

Citrus sinensis Not reported Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Quarters Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Quarters Elsinoe australis 1

Citrus sinensis Not reported Stores Elsinoe australis 1

Citrus sinensis Not reported Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Baggage Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe australis 1

Citrus sp. Fruit Baggage Elsinoe australis 1

Citrus sp. Fruit Baggage Elsinoe australis 1

Citrus sp. Fruit Baggage Elsinoe australis 1

Citrus sp. Fruit Baggage Elsinoe australis 1

Citrus sinensis Fruit Stores Elsinoe Sp. 1

Citrus sp. Fruit Mail Elsinoe Sp. 1

Citrus aurantium Fruit Stores Guignardia citricarpa 1

Citrus limon Fruit Stores Guignardia citricarpa 1

Citrus reticulata Not reported Quarters Guignardia citricarpa 1

Citrus reticulata Fruit Holds Guignardia citricarpa 1

Citrus sinensis Fruit Stores Guignardia citricarpa 1

Citrus sinensis Fruit Stores Guignardia citricarpa 1

Citrus sinensis Fruit Stores Guignardia citricarpa 1

Citrus sinensis Fruit Stores Guignardia citricarpa 1

Citrus sinensis Fruit Stores Guignardia citricarpa 1

Citrus sinensis Fruit Stores Guignardia citricarpa 1

Citrus sp. General Cargo Homoptera 1

Citrus limon Fruit Baggage Injury Sp. *Non-Rep* 1

Citrus sinensis Not reported Stores Injury Sp. *Non-Rep* 1

Citrus sinensis Fruit Baggage Lepidosaphes beckii 1
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Citrus paradisi Fruit Stores Parlatoria cinerea 1

Citrus reticulata Stores Parlatoria cinerea 1

Citrus sinensis Fruit Baggage Parlatoria cinerea 1

Citrus sp. Fruit Baggage Parlatoria cinerea 1

Citrus sp. Fruit Stores Parlatoria cinerea 1

Citrus reticulata Not reported Stores Parlatoria pergandii 1

Citrus sp. Not reported Baggage Parlatoria pergandii 1

Citrus reticulata Not reported Stores Parlatoria Sp. 1

Citrus aurantiifolia Baggage Parlatoria ziziphi 1

Citrus aurantiifolia Fruit Stores Parlatoria ziziphi 1

Citrus aurantiifolia Fruit Stores Parlatoria ziziphi 1

Citrus aurantiifolia Fruit Stores Parlatoria ziziphi 1

Citrus aurantiifolia Fruit Stores Parlatoria ziziphi 1

Citrus aurantiifolia Fruit Stores Parlatoria ziziphi 1

Citrus limon Fruit Stores Parlatoria ziziphi 1

Citrus limon Fruit Stores Parlatoria ziziphi 1

Citrus paradisi Fruit Baggage Parlatoria ziziphi 1

Citrus paradisi Fruit Stores Parlatoria ziziphi 1

Citrus sinensis Fruit Stores Parlatoria ziziphi 1

Citrus sinensis Not reported Stores Parlatoria ziziphi 1

Citrus sinensis Not reported Quarters Parlatoria ziziphi 1

Citrus sinensis Fruit Baggage Parlatoria ziziphi 1

Citrus sinensis Fruit Stores Parlatoria ziziphi 1

Citrus sp. Fruit Baggage Parlatoria ziziphi 1

Citrus limon Fruit Stores Phoma Sp. 1

Citrus limon Fruit Stores Phoma Sp. 1

Citrus sinensis Fruit Stores Pseudococcus Sp. 1

Citrus sinensis Fruit Baggage Pseudococcus Sp. 1

Citrus sinensis Fruit Permit cargo Tarsonemus Sp. 1

Citrus limon Fruit Baggage Xanthomonas axonopodis pv. Citri 1

Citrus sinensis Fruit Stores Xanthomonas axonopodis pv. Citri 1

Citrus aurantiifolia Fruit Baggage Xanthomonas campestris (pam.) 1

Citrus aurantiifolia Dried fruit Stores Xanthomonas campestris pv. Citri 1

Citrus limon Fruit Stores Xanthomonas campestris pv. Citri 1

Citrus limon Fruit Stores Xanthomonas campestris pv. Citri 1

Citrus paradisi Fruit Stores Xanthomonas campestris pv. Citri 1

Citrus sinensis Fruit Stores Xanthomonas campestris pv. Citri 1

Citrus sp. Leaf Baggage Xanthomonas campestris pv. Citri 1

Citrus sp. Fruit Permit cargo Xanthomonas campestris pv. Citri 1

Total 174
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Appendix C. Citrus production, harvest, and post-harvest processes in Uruguay

The citrus sector in Uruguay 

Uruguay’s citrus industry developed significantly during the 1970 ́s, 1980 ́s and 1990 ́s. Key

factors for this increase included a climate conducive for citrus development, fruit with 

external and internal quality suitable for the European market, and the competitive

advantages of the counter season production. Both the state and private industry provided 

additional key factors that facilitated this growth. Growers increased productivity and 

provided innovations, introducing new technologies which increased the production areas and 

provided citrus varieties with higher market value. The State fulfilled a very important roll by

giving support to the incipient export sector, declaring the sector of national interest and 

creating the Citrus Commission. During the last decade growers have made additional 

changes to improve efficiency, diminish production and handling costs, and improve 

logistics, commercial channels and marketing.

Uruguay specializes in the production of high quality fresh fruit for the international market, 

particularly to the Northern Hemisphere during its off-season. Citrus has become one of the 

main agricultural export products, after rice and dairy products. The citrus industry is 

characterized today by 20,862 hectares, 6.36 million plants and around 300 thousand metric 

tons of production. There are 479 growers distributed thoughout the country. More than 75

percent of the citrus production occurs on orchards of 10 or more hectares. Between 1981 and 

1999, the citrus industry increased 23 percent in hectares, 180 percent in production and 330

percent in exports of fresh fruits. At the moment Uruguay is supplying 30 markets with a 

wide range of varieties of oranges, mandarins, lemons and grapefruits. A vertical and 

horizontal integration of companies has characterized the last decade. Prominent 

technological improvements include: the plant certification program, the irrigation systems 

that cover 25 percent of the total production area and 37 percent of the effective hectares, the 

continuous growth in productivity, the changes to new varieties, the modern cold storage 

facilities, and the improvement of the logistical process. Nationally the per hectare net 

productivity for adult plants is 19 tons, for an average density of 413 plants/hectare. 

According to the Census information, plantations in full production, obtain yields of 35 and 

40 tons/hectare in mandarins; 40 to 45 tons in oranges and 45 to 60 tons/hectare in lemons 

and grapefruits, for densities of approximately 500 plants/hectare. The sector employs 0.7 

people/hectare, or around 15,000 people for permanent and seasonal labor.

The structure of the industry. 

The most recent National Citrus Census (CHNPC, 1996) reported that 85 percent of the 

20,862 planted total hectares are located in the Northern Area and 15 percent in the Southern 

Area of the country (Fig. C1). The Northern Area includes the Departments of Salto, 

Paysandú, Río Negro and Rivera. The Southern Area includes the Departments of San José, 

Canelones, Montevideo, Maldonado and Colonia. The varietal composition, harvest time and 

the export period are detailed in Table C1.

According to the census, oranges and mandarins each represent 43 percent, lemons 11

percent, and grapefruits 3 percent of the plants in production. In metric tons, oranges 

represent 52 percent, mandarins 30 percent, lemons 14 percent and grapefruits 4 percent. 

Valencias constitute the main variety of oranges (66 percent), followed by the Navel group 

(27 percent). Satsuma occupies the first place in the mandarins (30 percent), then the 
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Ellendale (22 percent), followed by Clementina and Nova (20 percent), Common mandarin 

for domestic consumption (11 percent) and then Murcott, Ortanique and others. The 

developed lemon variety called “Four Seasons”, is similar to Lisbon. The largest proportion 

of grapefruit belongs to the red and pink varieties (60 percent) and followed by white 

seedless. 

There are 9 to 14 packinghouses for citrus fruit processing, 7 in the Northern Area and the 

rest in the Southern Area. Five of them also have their own cold storage facilities and 

degreening chambers. With the cold storage capacity in the port of Nueva Palmira and other 

service companies, the national total capacity reaches 22,000 pallets.

Nueva Palmira Fruit Terminal, Frigofrut S.A, has a total capacity of 5,300 pallets in cold 

storage and 2000 pallets in sheds. It also has precooling Californian tunnels, with a capacity

of 1000 pallets per day. The company has obtained the certification of ISO 9000:2000 and it 

operates under a bar coding system called Cooltrack. Montevideo port is used mainly to 

export fruit in containers.

Figure C1. Citrus production zones in Uruguay. The Northern Area is indicated in red and 

the Southern Area in green.
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Table C1. Harvest and export calendar for citrus production in Uruguay. Lemon varieties are 

noted in green, orange in red, mandarins in orange and grapefruit in yellow

Citrus production and destination. 

Total production has grown from 272 thousand tons in the year 1996 to 358 in the year 1988, 

but from 1999 until 2006, total production fluctuates near an average of 277,000 tons, with 

important annual variations (Table C2). Annual domestic consumption is estimated between 

24 and 27 kg per capita, depending on the exports of fresh fruit. 

Agroindustry began to grow during the decade of the 1980 ́s, as an alternative for the 

growing production of non-exportable quality produce. The volumes that are processed 

annually fluctuate according to production levels and amount of the exports in fresh fruit. 

Concentrated juices, essential oils, and pectin are the main processed products for the 

international market. There are four industrial plants, three of which produce concentrated 

juices and essential oils and one which produces natural juices.

The production by species is shown in Table C3.

The export harvest begins in March with Satsuma mandarins and goes through mid- October 

with Valencia oranges for the European Union and into November for Eastern Europe. 

Within the region, and depending on supplies of citrus fruit in Argentina and Brazil, exports 

can continue until December. 

The most important traditional market for Uruguay is the European Union, and in recent 

years, the EU participation has been between the 79 and 85 percent in average for all species. 

Table C4 shows exports of citrus fruit by destination.

J F M A M J J A S O N D

LEMON

 NAVEL

 SALUSTIANA

 CADENERA

 VALENCIA

 SATSUMA

 CLEMENULES

 CLEMENVILLA

 CLEMENTINA

 ORLANDO

 MINEOLA

 ELLENDALE

 URUNIQUE

 SALTEÑITA

 MURCOTT

GRAPEFRUIT WHITE

GRAPEFRUIT RED

High Low
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Table C2. Production And Market Distribution Of Uruguayan Citrus (1970 To 2006)

Sector Production and Destination In 000 Tons

Year 1971 1981 1991 2001 2002 2003 2004 2005 2006

Production 73.9 116.7 226.5 342.5 235.5 248.7 242.2 326.0 277.0

Export 13.4 28.0 78.1 98.0 86.8 117.9 129.4 158.5 136.0

Export ( Percent) 18.1 24.0 34.5 28.6 36.9 47.4 53.5 48.6 49.1

Processing N.S. N.S. 67.4 87.4 62.9 32.0 44.0 64.5 47.0

Domestic And Losses 60.5 88.7 81.9 157.1 85.7 98.7 68.6 103.2 94.0

Table C3. Citrus production in Uruguay by species (1970 to 2006)

Type 1970 1980 1991 1996 2001 2002 2003 2004 2005 2006

Lemons 5.5 13.8 42.2 36.5 46.4 38.5 36.7 33.5 46.0 43.0

Mandarins 35.9 36.7 52.5 82.1 97.0 74.5 74.7 77.3 94.4 88.0

Oranges 42.1 61.6 121.4 141.2 189.0 115.8 131.6 124.1 176.5 138.0

Grapefruit 2.5 9.0 10.4 11.6 10.1 6.7 5.7 7.3 9.1 8.0

Total 86.0 121.1 226.5 271.4 342.5 235.5 248.7 242.2 326.0 277.0

Table C4. Geographic distribution of fresh citrus fruit from Uruguay (2002 to 2006).

Region Fruit Exports (percent)

2002 2003 2004 2005 2006

European Union 82.35 81.32 85.07 79.60 82.10 

Russia And E. Europe 7.14 11.25 8.41 13.42 11.7

Mercosur (Argentina, Brazil, Paraguay) 3.07 2.21 2.11 2.90 1.66

Others American Countries 3.82 2.01 2.34 1.77 2.07

Arab Countries And Africa 0.58 0.97 0.21 0.59 1.23

Far East 3.04 2.25 1.86 1.73 1.28

Citrus industry, actual situation and perspectives.

Uruguay has demonstrated over the last four decades characteristics that make it ideal for the 

citrus production. Among these are natural resources, climate and appropriate soils which 

allow high fruit quality production. Distance to main ports and access to national and 

international routes is not restrictive. The citrus industry has developed an agroindustrial 

infrastructure of packing, cold storage, and ports that facilitates exports. The structure of the 

industry clearly shows that the scale economies have become very important for the 

achievement of success. The role of the Ministry (DGSA) in safeguarding production through 

the support of phytosanitary surveillance, phytosanitary certification system for export and its 

commitment in the opening of new markets has been of particular significance. One of the 

most dramatic outstanding aspects in Uruguayan agriculture was the change in the trade 

structure at the world level. The Uruguayan citrus industry has made a great effort to adapt to 

this change. Today we see substantial changes in the trade channels and in the relationship 

with client-importers. The companies have prioritized the requirements of the market to 

promote growth in new areas. The new scenario implies the necessity to open new markets 

and development of the current ones. The relationship between the Euro and the US dollar 

has had negative effects on the profitability of the companies. Growing competition of citrus 

and other fruit suppliers and related products are forcing the companies to improve efficiency
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along the whole supply chain. In spite of this, great efforts are being made to produce high 

quality fruit within a responsible production process that satisfies the requirements of the 

Quality Management Systems, Good Agricultural Practices and Traceability (EUREPGAP).

Current Citrus Fruit Export Process

Citrus fruit for export is cultivated under a specific crop management system in the case of 

citrus canker, because this pest has been regulated under an eradication program since 1976. 

Citrus canker has been the key pest for Uruguayan citrus exports, being of quarantine concern 

of its main importing countries. Some preventive measures are routine for citrus growers such 

as: 

Selection of varieties - There are cultivars that have demonstrated significantly less 

susceptibility to disease both in foliage and fruit, allowing a better phytosanitary conditions in 

the crop. 

Measures in affected trees - Pruning, defoliation or tree removal, and removal of fruit with 

symptoms, applicable to the pest situation in an area, reduces the available inoculum. 

Preventive crop chemical treatments – Application of Cooper products protects the new 

flushes of growth and fruits from pest infection.

Integrated management of Citrus leaf miner - Chemical and biological control lower the 

number of its lesions, and reduce entry points for the bacteria through these lesions.

Cultural measures - Windbreaks, pruning, irrigation, appropriate fertilization to avoid a 

large number of flushes, inter row management, disinfection measures (grove entrance, 

personnel, tools, equipments, etc) reduce favorable conditions for infection development. 

A specific harvest date is used by export growers to ensure the quality of export fruit. The 

start of harvest is determined using a Maturity Index and the fruit is selected according to 

several criteria including: color (especially early varieties that need degreening); absence of 

lesions and other blemishes; absence of visible signs of pests; and size.

In the packinghouse the fruit are subjected to cleaning and sanitizing processes (washing, 

disinfection with chlorine and sodium orthophenyl phenate (SOPP), culling, brushing, 

waxing) to produce quality fruit for the fresh fruit export market and to fulfill all the client’s 

requirements. In Uruguay the citrus packinghouse vary in size and scale, and not all have pregrading machine. Figure C2 shows the general steps applied to citrus fruit, including pregrading.
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Figure C2: Process flow of citrus fruit in the Uruguayan packinghouse (DGSA, 2007)

Start

1.Weigh

5. Wash, disinfect, apply

chemical treatment, cull, dry

and wax. (Processing line -

Packaging)

3. Wash, cull and grade 

fruit. (Pre-Grading)

2. Disinfect 

fruit

6. Store fruit 

(Cool chambers)

4. Degreen fruit

End
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Appendix D. Citrus Fruit Phytosanitary Certification

MINISTERIO DE GANADERIA, AGRICULTURA Y PESCA

DIRECCION GENERAL DE SERVICIOS AGRICOLAS

DIVISION PROTECCION AGRICOLA

CITRUS FRUIT PHYTOSANITARY CERTIFICATION SYSTEM

(Summary 2007)

1. - INTRODUCTION

This System establishes the requirements needed to issue Phytosanitary Certificates for Citrus 

Fruit consignments according to the requirements of the NPPO’s from the importing 

countries.

Phytosanitary requirements are based on the knowledge of the specified pest situation of an 

area, Place of Prodution or Block of Production from which fruit originates. Thus 

consignments need proper identification of the area of origin. This kind of Phytosanitary

Certification System ensures the traceability of export consignments.

All operators involved at all stages from production to export (Places of production, 

packinghouses, storage facilities and exporters) are registered in the Citrus Fruit 

Phytosanitary Certification System (CFPCS) and need to fulfill DGSA requirements to obtain 

the phytosanitary certification for consignments to be exported.

2. - GENERAL REQUIREMENTS

2.1 REGISTRATION OF OPERATORS

The different operators through all stages from production to export (Places of Production, 

Packinghouses, Fruit Storage Facilities and Exporters) will apply to DGSA, at least a month 

before their first operation destined to intended markets. The registration will be renewed 

annually. Application implies compliance with the responsibilities derived from the 

fulfillment of terms and conditions of CFPCS. General conditions for registration of 

operators are included in the corresponding registration forms. For example for places of 

production these conditions include to specify their location using geographical position 

system, varieties planted, number of plants/variety, etc.

2.2 CERTIFICATION OF PHYTOSANITARY REQUIREMENTS IN THE PLACES 

OF PRODUCTION REGISTERED IN THE CFPCS

INSPECTION 

Phytosanitary inspection in the field is made pre-harvest on 100 percent of the trees to 

determine the occurence of citrus canker and black spot diseases. If disease occurence is 

verified, then its incidence is determined.
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Types of Inspection. The following types of inspection of Places of Production will be 

applied:

Official: Inspections are made by official inspection teams (DGSA). 

Officially recognized: Inspections are made by personnel of the owner of the Place of 

Production, under the supervision of a Responsible Technician and under Official Audit. The 

Responsible Technician must be registered with the DGSA.

Audit: Officially Recognized Inspections are subject to audits by official inspection teams.

DGSA has 55 inspectors in the north and 15 in the south for official field Inspection and 

audits.

2.3 AUTHORIZATION OF OPERATORS 

Operators registered in the CFPCS will be authorized after the corresponding verifications. 

Their status will be continuously updated in the Computer System of CFPCS and will be sent 

to all Packinghouses, Fruit Storage Facilities and points of export.

Operator’s authorization will be annual and it can expire at any time due to non-compliance 

with the CFPCS conditions accepted at registration or due to inspection or audit results.

2.4 TRACEABILITY (See Diagram)

Acceptance of the terms of the CFPCS at the moment of registration requires all registered 

operators maintain fruit identification through all stages from production to export and 

provide the traceability of export consignments back to the Places of Production.

2.4.1 At Places of Production Level

The grower of the Place of Production, the Responsible Technician and/or the person 

responsible for the documentation (non-price invoice) accompanying fruit during transport to 

the packing house have the responsibility to fulfill the DGSA requirements, specifically:

a) Be sure before harvest, based on the information consigned in the CFPCS, that the Place 

of Production is authorized to send fruit to the Packinghouse.

b) Identify all harvest bins with code number of each Place of Production or Block. 

c) Consign the required information in the no price invoice that must accompany the fruit.

2.4.2 At Packinghouse Level

Packinghouses must fulfill DGSA requirements, specifically:

a) Verify that the information from the CFPCS is correct and that code numbers on the bins 

correspond to Places of Production authorized in the CFPCS to process to the established 

destination.

b) Enter into the Computer System the information of all no price invoices as the 
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corresponding consignment enters for processing.

c) Do not process consignments from Places of Production not authorized by the CFPCS, or 

whose invoices are not properly completed or which do not have the code number, when 

they are processing.

d) Consign on all export pallets the code numbers of Place/s and Block/s of Production, 

which indicates the origin of the fruit.

e) Allow the DGSA inspectors full access at any time to all facilities of the Packinghouse, 

and keep available and updated all the backup documentation of the fruit processing 

within CFPCS, entry registers, intermediate destination (degreening, culling, cool) and 

fruit delivery.

f) Apply the required phytosanitary treatments for the pests of concern.

g) Confirm the citrus fruit consignments only with pallets or bins with code numbers 

authorized in the CFPCS, including on the no price invoice the code numbers, species, 

and the quantity of units that correspond to each.

2.4.3 At Fruit Storage Facilities Level

The Fruit Storage Facilities have the responsibility specifically to:

a) Verify that no price invoices only come from Packinghouses authorized by the CFPCS to 

process citrus fruit for the established destination.

b) Enter into the Computer System the information of all no price invoices at arrival of fruit.

c) Allow full access of the DGSA inspectors at any time to all Fruit Storage Facilities, and 

keep available and updated in its Computer system entry and fruit delivery registers, as 

well as all backup information.

d) Keep individualized DGSA lots authorized for some market separated from other lots not 

authorized for these destinations.

e) Conform the citrus fruit consignments, only with pallets or bins with code numbers 

authorized by the CFPCS, indicating in the no price invoice the code numbers, the 

species, and the quantity of units (pallets) that correspond to each.

2.4.4 At Exporter level

Exporters have the responsibility to fulfill the procedures that lead in the issue of the 

Phytosanitary Certificate by DGSA (Name and address of importer, number of pallets, codes 

of places of production, etc.).

3. - CERTIFICATION AT PACKINGHOUSE LEVEL

3.1 Inspection

Routine inspections will be made by DGSA personnel to verify the phytosanitary condition 

of export fruit and to verify the post harvest treatments required by the export markets.

Detection of quarantine pests for the specific market in lots from Places of Production 

authorized will result in automatic non-authorization.
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3.2 Verification of export lots identification

Inspectors will verify the fulfillment of the procedures established in item 2 about 

traceability.

3.3 Conformity to Certification of export lots

When containers proceed directly to the port of expot, inspectors will issue a certificate of 

conformity for each export lot stating lot details and fulfillment of export market 

requirements.

4. - PHYTOSANITARY CERTIFICATE ISSUE

Phytosanitary Certificates accompanying consignments to the importing country will be 

issued by DGSA authorized personnel in the point of export. To issue the Phytosanitary

Certificate, the information of the no price invoice, information supplied by the CFPCS and 

the certificate of conformity is verified. 

5. AUDIT OF THE SYSTEM 

To continually improve CFPCS, DGSA will establish audit procedures to the registered 

operators, in order to follow the different stages of the CFPCS.
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TRACEABILITY SCHEME

PROCEDURES INVOLVED IN THE CFPCS 

Production

Processing

Concentration Export

Register 

Operators

Authorization of 

Operators

Audit

Control
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OPERATOR REGISTRATION

Submission of required 

information

Evaluation of supplied 

information

Location

Description Technician 

Responsible

Responsible of 

non-price 

invoice

Standard 

met

Inclusion in the CFPCS 

Register

YES

NO

Enter the information 

to the System

Registration 

Process

Registered 

Operator

Description of 

the Traceability 

System 

(processing, 

packing, cool 

chamber)
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AUTHORIZATION OF PLACES OF PRODUCTION

Officially recognized 

inspections Audit 

Process

Authorization 

Process

Report of 

Phytosanitary

Situation 

Official

Inspections

Report of 

Phytosanitary

Situation 

Presentation of 

Application

Authorization 

Request

Authorized 

Operator

Verification of 

Information

Communications

Points of 

Export

Packinghouses 

Storage 

facilities
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PLACE OF PRODUCTION

STORAGE FACILITY

PACKINGHOUSE

Harvest and Bin 

filling Transport

Bin Identification

Reception of No 

Price Invoice

Control of System 

Authorization Control of Bins 

Identification

Grading

Degreening

Processing Line

Packing Conformation of 

Pallets

Place of 

Production 

No Price 

Invoice

Internal 

No Price 

Invoice

Internal No

Price 

Invoice

Packinghouse

No Price 

Invoice

Reception of

No price Invoice

Verification of 

System

Authorization

Control of Pallet 

Identification

Internal

No price 

invoice

Conformation of 

Pallets

(Chamber)

Control of System 

Authorisation at Export 

Point

Transport

Transport

Storage no 

price Invoice

EXPORT POINT

Pallets 

Conformation

(Chamber)
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Appendix E. Life cycle of Xanthomonas citri subsp. citri, the pathogen causing citrus canker

.

Bacteria wind and rain 

dispersed small distances 

within trees or to 

neighboring trees; 

bacterial multiplication 

occurs from 14-36oC with 

optimum temperature of 

25-30oC

harvest

Immature fruit 3-6 cm diameter 

are highly susceptible

Leaf infection rarely 

occurs after 85% 

expansion. Mature fruit 

gain some immunity.

Warm (20-30 C), 

wet weather favors 

bacterial growth 

and spread

Leaves, twigs and fruit are highly susceptible for the first 6 weeks. Infection 

can occur with 14-21 days after shoots begin to develop. Critical period for 

rind infection occurs between petal fall and 90 days thereafter.

New plant growth initiated

winter