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Table of contents :
Acknowledgments
Contents
Contributors
About the Editor
Part I: General Aspects of Fruit Fly Management
Chapter 1: Fruit Flies: A Threat to Fruit Production in the Americas
1.1 Introduction
1.2 Fruit Flies of Economic Importance in the Americas
References
Chapter 2: Fruit Fly (Tephritidae) Management in the Neotropical Region: History, State of the Art, and Perspectives
2.1 Introduction
2.2 Country-by-Country Assessment of Actions/Programs Devoted to Fruit Fly Management/Control in the Neotropics
2.2.1 Argentina
2.2.1.1 A Historical Overview
2.2.1.2 Current Status
2.2.1.3 Future Perspectives
2.2.2 Bolivia
2.2.3 Chile
2.2.4 Uruguay
2.2.5 Paraguay
2.2.6 Brazil
2.2.7 Peru
2.2.8 Colombia
2.2.8.1 Past and Present of Fruit Fly-Related Activities in Colombia
2.2.8.2 Fruit Fly Management in Colombia
2.2.9 Central America and the Caribbean
2.2.10 Mexico
2.3 Historical Account of the Seminal Role Played by the International Atomic Energy Agency (IAEA) in the Control/Management of Fruit Flies in the Neotropics
2.3.1 Research and Development
2.3.2 Technical Cooperation Programmes
2.3.3 South America
2.3.3.1 Argentina
2.3.3.2 Bolivia
2.3.3.3 Brazil
2.3.3.4 Chile
2.3.3.5 Peru
2.3.3.6 Ecuador
2.3.3.7 Suriname
2.3.4 Central America
2.3.4.1 Central American Regional Project
2.3.4.2 Honduras
2.3.4.3 Guatemala
2.3.5 Caribbean Region
2.3.5.1 Dominican Republic
2.3.6 Future Perspectives for IAEA Involvement in Fruit Fly Control in the Neotropics
2.4 Implementation of Environmentally Friendly Fruit Fly Management Schemes in the Neotropics
2.5 Climate Change/Global Warming and the Effect on Fruit Fly Distribution and Management
2.6 Conclusions
References
Chapter 3: Monitoring and Mass Trapping of Fruit Flies (Diptera: Tephritidae) in the Americas
3.1 Introduction
3.2 Fruit Fly Traps
3.2.1 Trap Visual Cues and Their Interactions
3.2.2 Commercial Traps
3.2.2.1 Wet Traps
3.2.2.2 Dry Traps
3.2.2.2.1 Sticky Traps
3.2.2.2.2 Dry Traps with Knockdown Insecticides
3.3 Fruit Fly Attractants
3.3.1 Food Attractants
3.3.1.1 Liquid Food Attractants
3.3.1.2 Dry Food Attractants
3.3.2 Sexual Attractants
3.3.2.1 Pheromones
3.3.2.2 Male Attractants
3.3.3 Host Attractants
3.4 Multiple Factors Affect Trap Captures
3.5 Placement and Distribution of Traps
3.6 The Main Traps and Attractants Used in the Americas
3.7 Mass Trapping: Specific Considerations
3.7.1 Trap–Attractant Combinations
3.7.2 Trap Density and Distribution
3.7.3 Trap Deployment and Timing of Use
3.8 Current Advances for Future Improved Monitoring Systems
3.8.1 Smart Traps
3.8.2 Advances in Semiochemistry
3.9 Conclusions and Future Research Needs
References
Chapter 4: Biological Control of Fruit Flies with Emphasis on Microbial Control
4.1 Introduction
4.2 Entomopathogenic Nematodes
4.3 Entomopathogenic Fungi
4.4 Entomopathogenic Bacteria
4.5 Parasitoids
4.6 Predators
4.7 Conclusions
References
Chapter 5: Phytosanitary Irradiation of Tephritid Fruit Flies
5.1 Introduction
5.2 Generic Treatments
5.3 Quarantine Irradiation Treatment Methodology
5.3.1 Dose–Response Tests
5.3.2 Large-Scale Confirmatory Testing
5.3.3 Poor Hosts
5.3.4 Artificial Versus Natural Infestation
5.3.5 Laboratory Versus Wild Strains of Test Insects
5.3.6 Dosimetry
5.3.7 Use of Probit 9 and Its Alternatives
5.3.8 Modified Atmospheres
5.3.9 Combination Treatments
5.4 Wider Adoption of Phytosanitary Irradiation
5.4.1 Country Approvals
5.4.2 Labeling
5.4.3 Consumer Perception
5.4.4 New Technology
5.5 Summary
References
Part II: Management of Fruit Flies in the Countries of the Americas
Chapter 6: Management of Tephritid Fruit Flies in Argentina
6.1 Introduction
6.2 Economically Important Tephritid Fruit Fly Species in Argentina
6.3 Background of the Earliest Methods of Monitoring and Control Pest Fruit Flies in Argentina
6.4 History and Status of the PROCEM
6.5 Strategies Implemented for Fruit Fly Integrated Management in Argentina
6.5.1 SIT
6.5.2 Mass Trapping
6.5.3 Biological Control
6.5.4 Chemical Control
6.5.5 Cultural Control
6.5.6 Domestic Quarantine Strategy
6.6 Challenges and Future Development
6.7 Concluding Remarks
References
Chapter 7: Augmentative Biological Control as a Workable Strategy Within an Area-Wide Integrated Fruit Fly Management Approach: Case Studies from Mexico and Argentina
7.1 Introduction
7.2 Augmentative Biological Control (ABC): An Eco-Friendly Strategy for Fruit Fly Suppression
7.3 Selection Criteria of Diachasmimorpha longicaudata for Fruit Fly ABC in Latin America
7.4 ABC in Mexican and Argentinean Fruit Fly Management Programs
7.5 Diachasmimorpha longicaudata Mass-Rearing Procedures in Mexico and Argentina
7.6 Parasitoid Packing and Release
7.7 Results of Diachasmimorpha longicaudata Augmentative Releases in Mexico and Argentina
7.8 Conclusions
References
Chapter 8: Preventive Control of Ceratitis capitata on Remote Islands in Belize
8.1 Introduction
8.2 Belize’s National Medfly Surveillance Programme
8.2.1 Quarantine System
8.2.2 Medfly Surveillance Programme
8.2.3 Medfly Eradication Action Plan
8.2.3.1 National Internal Quarantine
8.2.4 Export Certification Program
8.3 Historical Data
8.4 Declaration of Free Status
8.5 Recognition by Trading Partners
8.6 Surveillance in the Sapodilla Cayes
8.7 Preventative Control Plan
8.8 Strategies
8.9 Results
8.10 Conclusions
References
Chapter 9: Fruit Fly Management in Brazil: Current Status and Perspectives
9.1 Introduction
9.2 Economic Impact of Fruit Flies in Brazil
9.2.1 Economic Importance of Phytosanitary Requirements for the Fruit Sector
9.2.2 An Overview of Economic Studies for Fruit Flies in Brazil
9.3 Fruit Fly-Free Area
9.3.1 Location of the Free Area and Destination of the Production
9.3.2 Maintenance of the Free Area
9.3.3 Fruit Fly Species Present in the Free Area
9.3.4 Fruit Flies Hosts in the Free Area
9.4 The Case of Carambola Fruit Fly in the North Region
9.4.1 Carambola Fruit Fly Management
9.4.2 Detection and Monitoring
9.4.3 Control of Carambola Fruit Fly
9.4.4 Future Perspectives for the Management of the Carambola Fruit Fly
9.5 Chemical Control of Fruit Flies in Brazil
9.5.1 Fruit Fly Stages Targeted by the Insecticides
9.5.2 Chemical Control Tactics
9.5.3 Insecticide Compounds and Their Temporal Trends
9.5.4 Make-Decision System
9.5.5 Risks to Achieving the Desired Effectiveness
9.6 Biological Control
9.6.1 Parasitoids
9.6.2 Predators
9.6.3 Entomophatogens
9.7 Concluding Remarks
References
Chapter 10: The Management of Fruit Flies in Colombia: A Long Road to Travel
10.1 Introduction
10.2 Socioeconomic Aspects of Fruit Production in Colombia
10.3 Diversity, Biology, and Ecology of Fruit Flies in Colombia
10.4 Management of Fruit Flies in Colombia
10.4.1 Approaches Implemented by the Phytosanitary Authority
10.4.2 Establishment of Pest-Free Areas with a Low Prevalence of Fruit Flies
10.5 Studies on Quarantine Treatments
10.6 Studies of the Host Condition of Fruit Flies
10.7 Legal Control Related to Fruit Flies in Colombia
10.8 Applied Technologies by Farmers
10.9 Final Considerations
References
Chapter 11: Current Fruit Fly Knowledge Status in Ecuador
11.1 Introduction
11.1.1 Field Sampling
11.1.2 Types of Sampling Carried Out
11.1.2.1 General Sampling
11.1.2.2 Targeted Sampling
11.1.2.3 Sample Handling in the Field
11.2 Sample Processing in the Laboratory
11.2.1 Sample Handling
11.2.2 Specimen Management
11.2.2.1 Adult Fly Management
11.2.3 Specimen Mounting and Fitting
11.2.3.1 Dry Mounting
11.3 Specimen Identification
11.4 Photographic Record
11.5 Fruit Fly Species and Their Hosts
11.5.1 Anastrepha distincta Greene
11.5.2 Anastrepha fraterculus (Wiedemann)
11.5.3 Anastrepha grandis (Macquart)
11.5.4 Anastrepha obliqua (Macquart)
11.5.5 Anastrepha serpentina (Wiedemann)
11.5.6 Anastrepha striata Schiner
11.5.7 Ceratitis capitata (Wiedemann)
11.6 Fruit Fly National Monitoring
11.6.1 Fruit Fly Surveillance
11.7 Plant Quarantine
11.8 Integrated Management
11.9 Analytical Capacity
11.10 Dissemination and Outreach and Training
11.11 Recorded Fruit Fly Natural Enemies in Ecuador
11.12 Regulatory Activities to Achieve the Export of Fruits in Ecuador
11.13 Final Considerations
References
Chapter 12: Fruit Flies Management in Haïti
12.1 Introduction
12.2 Fruits and Other Exported Products
12.3 MARNDR (DPV/PS) and FAMV Trials
12.4 Fruit Fly Detection and Control Program (Haiti-2007)
12.5 Host Plants
12.6 Fruit Fly Management Strategy
12.6.1 Sanitary Control
12.6.2 Preventive Control
12.6.3 Artisanal Trapping
12.6.3.1 The Corn Spine (Rachis) Method
12.6.3.2 The Plastic Bottle Traps
12.6.4 Capture Trap Augments (Mass Trapping)
12.7 Conclusions and Prospects for the Fight Against Fruit Flies
References
Chapter 13: Management of Economically Important Native and Exotic Fruit Fly (Tephritidae) Species in Mexico
13.1 Introduction
13.2 Fruit Fly Management History in Mexico
13.3 Trapping, Bait Stations, and Mass Trapping
13.4 Biological Control
13.5 Sterile Insect Technique (SIT)
13.5.1 Background of the MoscaMed Program
13.5.2 SIT Applied to Manage/Control Anastrepha ludens and A. obliqua
13.5.3 Mass Rearing
13.6 Area-Wide Management
13.6.1 Initial Conceptual Considerations
13.6.2 Requirements for AW-IPM
13.6.3 Fruit Fly AW-IPM
13.6.4 Perspectives
13.7 Low Prevalence or Fruit Fly-Free Areas
13.8 Other Promising Management Strategies
13.8.1 Experimental Testing of Host Marking Pheromones (HMPs)
13.8.2 Orchard Design Schemes
13.8.3 Biodiversity Conservation
13.9 Post-harvest Treatments
13.10 Recent Scientific Findings that Can Impact Fruit Fly Management in the Future
13.10.1 Anastrepha Microbiota (Including Fungi)
13.10.2 Population Genetics of Anastrepha
13.10.3 Various
13.11 Current Situation and Prospects
13.12 Conclusions
References
Chapter 14: Biological Control of Ceratitis capitata in the Mexico-Guatemala Border Region and Its Advantages in Opening Areas with Social Conflict
14.1 Introduction
14.2 The Social Issue
14.3 Integrated Pest Management of the Medfly in the Region
14.3.1 Basis of the Biological Control of Medfly Populations
14.4 Biological Control Against C. capitata in the Eradication Zone of Chiapas, Mexico
14.4.1 Characterization of the Work Zones
14.4.2 Determination of Field Parasitism
14.4.3 Obtained Parasitism in the Release Zones
14.5 Comments on Field Parasitism Results
14.5.1 Openness of Communities with a Social Conflict Against Pest Control Activities
References
Chapter 15: Parasitoid Species Associated with Fruit Flies of the Genus Anastrepha (Diptera, Tephritidae) in Panama
15.1 Introduction
15.2 Panamanian Study Sites
15.3 Sampling Protocol
15.4 Parasitoids Associated with Fruit Flies of the Genus Anastrepha in Panama
15.5 Percentage Native Parasitoidism
15.6 Biological Characteristics of Parasitoid Species
15.6.1 Doryctobracon areolatus Szépligeti
15.6.2 Doryctobracon zeteki (Muesebeck)
15.6.3 Doryctobracon crawfordi (Viereck)
15.6.4 Doryctobracon auripennis (Muesebeck)
15.6.5 Doryctobracpn trinidadensis Hoff
15.6.6 Opius bellus Gahan
15.6.7 Doryctobracon capsicola (Muesebeck)
15.6.8 Diachasmimorpha longicaudata Ashmead
15.6.9 Asobara anastrephae Muesebeck
15.6.10 Aganaspis pelleranoi (Brethés)
15.6.11 Dicerataspis sp.
15.6.12 Spilomicrus sp.
15.6.13 Trichopria sp.
15.7 Fruit Flies of the Genus Anastrepha Attack by Parasitoids
15.8 Concluding Remarks
References
Chapter 16: A Multifaceted Approach to Domestic Management of Invasive Fruit Flies in the United States
16.1 Introduction
16.2 Mediterranean Fruit Fly (Medfly, Ceratitis capitata)
16.2.1 Prevention of Infestations
16.2.2 Detection
16.2.3 Emergency Response
16.3 Mexican Fruit Fly (Mexfly, Anastrepha ludens)
16.3.1 Preventing and Eradicating Infestations
16.3.2 Detection
16.3.3 Emergency Response
16.4 Oriental Fruit Fly (OFF, Bactrocera dorsalis)
16.5 Other Exotic Fruit Flies
16.6 Integrated Approach for Managing Exotic Fruit Flies
16.7 Research and Development Needs
16.8 Conclusions
References
Chapter 17: Biological Control Introductions Against Invasive Tephritid Fruit Flies (Diptera: Tephritidae) in the US: Achievements, Opportunities, and Challenges
17.1 Introduction
17.2 Biological Control Introductions
17.2.1 Biological Control of Tephritid Pests in Hawaii
17.2.2 Biological Control of Caribbean Fruit Fly in Florida
17.2.3 Biological Control of Olive Fruit Fly in California
17.2.4 Biological Control of Native Rhagoletis
17.3 New Opportunities
17.4 Challenges
17.5 Future Direction
17.6 Summary
References
Chapter 18: Analysis of Historical Recapture Rates in the Anastrepha ludens (Loew), Mexican Fruit Fly (Diptera: Tephritidae) Program in Texas, USA
18.1 Introduction
18.2 History of Mexican Fruit Fly and the Citrus Industry in South Texas
18.3 Program Changes that Affect Sterile and Wild Mexfly Capture
18.4 Mexfly Sterile Release
18.5 Mexfly Trapping Program
18.6 Wild Mexfly Adult Capture and Larvae Detection
18.7 Closing Remarks
References
Chapter 19: Bases for Management of Fruit Flies (Diptera: Tephritidae) in Uruguay
19.1 Introduction
19.2 Fruit Flies
19.2.1 Ceratitis capitata and Anastrepha fraterculus
19.3 Parasitoids
19.4 Fruit Fly Fluctuation and Host Infestation in Commercial Orchards
19.5 Fruit Flies Management
19.6 Basis for Implementing an SIT Program in Uruguay
References
Chapter 20: What Will the Future of Fruit Fly Management in the Americas Look Like?
20.1 Introduction
20.2 Management of Fruit Flies and Sustainable Development
20.3 National and Interregional Program for Combating Fruit Flies
20.4 Area-Wide Integrated Pest Management (AWIPM)
20.5 Management of Fruit Flies in the Context of Agriculture 4.0
20.6 Equality, Diversity, and Inclusion
20.7 Final Considerations
References
Index
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Flávio Roberto Mello Garcia   Editor

Management of Fruit Flies in the Americas

Management of Fruit Flies in the Americas

Flávio Roberto Mello Garcia Editor

Management of Fruit Flies in the Americas

Editor Flávio Roberto Mello Garcia Departamento de Ecologia, Zoologia e Genética, Instituto de Biologia Universidade Federal de Pelotas Pelotas, RS, Brazil

ISBN 978-3-031-48607-4    ISBN 978-3-031-48608-1 (eBook) https://doi.org/10.1007/978-3-031-48608-1 © The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2024 This work is subject to copyright. All rights are solely and exclusively licensed by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Switzerland AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland Paper in this product is recyclable.

Acknowledgments

I would like to thank the Brazilian National Council for Scientific and Technological Development (CNPq) research productivity grant. I would like to thank the 68 contributors who made this book a reality.

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Contents

Part I General Aspects of Fruit Fly Management 1 Fruit  Flies: A Threat to Fruit Production in the Americas������������������    3 Flávio Roberto Mello Garcia 2 Fruit  Fly (Tephritidae) Management in the Neotropical Region: History, State of the Art, and Perspectives������������������������������   11 Martín Aluja, Sergio Marcelo Ovruski, Flávio Roberto Mello Garcia, Maribel Hurtado, and Walther Enkerlin 3 Monitoring  and Mass Trapping of Fruit Flies (Diptera: Tephritidae) in the Americas��������������������������������������������������   67 Rodrigo Lasa, Juan Rull, Lorena Suárez, Flávio Roberto Mello Garcia, Trevor Williams, and Francisco Díaz-Fleischer 4 Biological  Control of Fruit Flies with Emphasis on Microbial Control ������������������������������������������������������������������������������  127 Andressa Lima de Brida, Maguintontz C. Jean-Baptiste, Lorena Suárez, Sergio Marcelo Ovruski, Jorge Cancino, Oscar E. Liburd, and Flávio Roberto Mello Garcia 5 Phytosanitary  Irradiation of Tephritid Fruit Flies ������������������������������  143 Peter A. Follett Part II Management of Fruit Flies in the Countries of the Americas 6 Management  of Tephritid Fruit Flies in Argentina������������������������������  169 Lorena Suárez, María Josefina Buonocore-Biancheri, Albérico Fernando Murúa, Sergio Beltrachini, Luis Ernesto Kulichevsky, and Sergio Marcelo Ovruski

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7 Augmentative  Biological Control as a Workable Strategy Within an Area-­Wide Integrated Fruit Fly Management Approach: Case Studies from Mexico and Argentina��������������������������  197 Jorge Cancino, Lorena Suárez, Amanda Ayala, María Josefina Buonocore-Biancheri, Albérico Fernando Murúa, and Sergio Marcelo Ovruski 8 P  reventive Control of Ceratitis capitata on Remote Islands in Belize ����������������������������������������������������������������������������������������������������  221 Delilah Alice Cabb Ayala and Hernan Zetina 9 Fruit  Fly Management in Brazil: Current Status and Perspectives ��������������������������������������������������������������������������������������  235 Flávio Roberto Mello Garcia, Ricardo Adaime, Cristiane Ramos de Jesus, Adalton Raga, Elton Lucio Araujo, Sílvia Helena Galvão de Miranda, and Miguel de Souza Filho 10 The  Management of Fruit Flies in Colombia: A Long Road to Travel����������������������������������������������������������������������������  289 Nelson A. Canal and Emilio Arévalo-Peñaranda 11 Current  Fruit Fly Knowledge Status in Ecuador ��������������������������������  317 Juan Tigrero Salas, Myriam Arias de López, David Salas Mujica, Henry Troya Armijos, Julia Bolaños Pineda, and Ligia Romero Pardo 12 Fruit  Flies Management in Haïti������������������������������������������������������������  345 Daniel Jean-Pierre, Fractyl Mertilus, and Pierre Garry Augustin 13 Management  of Economically Important Native and Exotic Fruit Fly (Tephritidae) Species in Mexico��������������������������  355 Martín Aluja, Larissa Guillén, Carlos Pascacio-Villafán, Maritza Juárez-­Durán, Mario A. Miranda-Salcedo, and Pablo Liedo 14 B  iological Control of Ceratitis capitata in the Mexico-Guatemala Border Region and Its Advantages in Opening Areas with Social Conflict����������������������������������������������������������������������������������  407 Jorge Cancino, Guadalupe García-Coapio, Patricia López, Gabriela Juárez, Francisco S. Albores, Maritza Juárez, and Pablo Montoya 15 Parasitoid  Species Associated with Fruit Flies of the Genus Anastrepha (Diptera, Tephritidae) in Panama����������������  423 Enrique Medianero, Luis Alvarado-Gálvez, and Louise A. Rodríguez-Scott

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16 A  Multifaceted Approach to Domestic Management of Invasive Fruit Flies in the United States��������������������������������������������  445 Corinna S. Bazelet, Ashton Leo, Phillip Lowe, Richard Johnson, and Shaharra Usnick 17 Biological  Control Introductions Against Invasive Tephritid Fruit Flies (Diptera: Tephritidae) in the US: Achievements, Opportunities, and Challenges ��������������������������������������������������������������  461 Xingeng Wang, Mohsen M. Ramadan, and Kim A. Hoelmer 18 Analysis  of Historical Recapture Rates in the Anastrepha ludens (Loew), Mexican Fruit Fly (Diptera: Tephritidae) Program in Texas, USA ��������������������������������������������������������������������������  501 Hugh Conway, Jose Hinojosa, Tim Roland, and John Worley 19 Bases  for Management of Fruit Flies (Diptera: Tephritidae) in Uruguay������������������������������������������������������������������������������������������������  539 María Victoria Calvo, Felicia Duarte, Soledad Delgado, Flávio Roberto Mello Garcia, and Iris B. Scatoni 20 What  Will the Future of Fruit Fly Management in the Americas Look Like?��������������������������������������������������������������������  557 Flávio Roberto Mello Garcia Index������������������������������������������������������������������������������������������������������������������  567

Contributors

Ricardo Adaime  Embrapa Amapá, Macapá, AP, Brazil Francisco S. Albores  Programa Moscas de la Fruta SENASICA-SADER, Metapa de Domínguez, Chiapas, Mexico Martín Aluja  Red de Manejo Biorracional de Plagas y Vectores, Clúster Científico y Tecnológico BioMimic, Instituto de Ecología, A.C.  – INECOL, Xalapa, Veracruz, Mexico Luis  Alvarado-Gálvez  Dirección Nacional de Sanidad Vegetal, Ministerio de Desarrollo Agropecuario, Río Tapia-Tocumen, Ciudad de Panamá, Panama Elton  Lucio  Araujo  Universidade Federal Rural do Semi Árido, Mossoró, RN, Brazil Emilio Arévalo-Peñaranda  Consultant, Medellín, Antioquía, Colombia Henry Troya Armijos  AGROCALIDAD, Loja, Ecuador Pierre Garry Augustin  Ministère de l’Agriculture des Ressources Naturelles et du Développement Rural, Port-au-Prince, Haiti Amanda  Ayala  Programa Moscafrut SAGARPA-IICA, Metapa de Dominguez, Chiapas, Mexico Delilah Alice Cabb Ayala  Sanitary and Phytosanitary Enquiry Point, Belmopan City, Cayo District, Belize Corinna  S.  Bazelet  United States Department of Agriculture, Animal and Plant Health Inspection Service, Plant Protection and Quarantine (USDA APHIS PPQ), Raleigh, NC, USA Sergio Beltrachini  Dirección de Sanidad Vegetal, Animal y Alimentos (DSVAA), Gobierno de la provincia de San Juan, Rivadavia, San Juan, Argentina

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Contributors

María Josefina Buonocore-Biancheri  LIEMEN, División Control Biológico de Plagas, PROIMI Biotecnología, CCT CONICET NO, San Miguel de Tucumán, Tucumán, Argentina María Victoria Calvo  Universidad de la Republica, Montevideo, Uruguay Nelson A. Canal  Universidad del Tolima, Ibagué, Tolima, Colombia Jorge Cancino  Programa Operativo Moscas SADER-IICA, Metapa de Dominguez, Chiapas, Mexico Hugh  Conway  USDA- Animal and Plant Health Inspection Service, Edinburg, TX, USA Andressa Lima de Brida  CropSolutions, São Gabriel do Oeste, MS, Brazil Cristiane Ramos de Jesus  Embrapa Amapá, Macapá, AP, Brazil Soledad Delgado  Universidad de la Republica, Montevideo, Uruguay Myriam Arias de López  Sociedad Entomológica del Ecuador, Guayas, Ecuador Sílvia  Helena  Galvão  de Miranda  Universidade de São Paulo, Piracicaba, SP, Brazil Miguel de Souza Filho  Instituto Biológico, Campinas, SP, Brazil Francisco Díaz-Fleischer  INBIOTECA, Universidad Veracruzana, Xalapa, Veracruz, Mexico Felicia Duarte  Universidad de la Republica, Montevideo, Uruguay Walther Enkerlin  Insect Pest Control Section, Joint FAO/IAEA Division, Vienna, Austria Peter  A.  Follett  USDA-ARS, U.  S. Pacific Basin Agricultural Research Center, Hilo, HI, USA Guadalupe  García-Coapio  Programa Moscas de la Fruta SENASICA-SADER, Metapa de Domínguez, Chiapas, Mexico Flávio  Roberto  Mello Garcia  Departamento de Ecologia, Zoologia e Genética, Instituto de Biologia, Universidade Federal de Pelotas, Pelotas, RS, Brazil Larissa Guillén  Red de Manejo Biorracional de Plagas y Vectores, Clúster Científico y Tecnológico BioMimic, Instituto de Ecología, A.C. – INECOL, Xalapa, Veracruz, Mexico Jose  Hinojosa  USDA- Animal and Plant Health Inspection Service, Edinburg, TX, USA Kim  A.  Hoelmer  USDA-ARS Beneficial Insects Introduction Research Unit, Newark, DE, USA

Contributors

xiii

Maribel  Hurtado  Organización Norteamericana de Protección a las Plantas  – NAPPO, Mexico City, Mexico Maguintontz C. Jean-Baptiste  Universidade Federal de Pelotas, Pelotas, RS, Brazil Daniel  Jean-Pierre  Ministère de l’Agriculture des Ressources Naturelles et du Développement Rural, Port-au-Prince, Haiti Richard  Johnson  USDA APHIS PPQ, Emergency, and Domestic Programs, Riverdale, MD, USA Maritza  Juárez-Durán  Programa Nacional de Moscas de la Fruta, DGSV, SENASICA, SADER, Metapa de Domínguez, Chiapas, México Gabriela Juárez  Programa Moscas de la Fruta SENASICA-SADER, Metapa de Domínguez, Chiapas, Mexico Luis  Ernesto  Kulichevsky  Dirección de Sanidad Vegetal, Animal y Alimentos (DSVAA), Gobierno de la provincia de San Juan, Rivadavia, San Juan, Argentina Rodrigo  Lasa  Red de Manejo Biorracional de Plagas y Vectores, Instituto de Ecología, Xalapa, Veracruz, Mexico Ashton  Leo  United States Department of Agriculture, Animal and Plant Health Inspection Service, Plant Protection and Quarantine (USDA APHIS PPQ), Raleigh, NC, USA Oscar E. Liburd  University of Florida, Gainesville, FL, USA Pablo Liedo  El Colegio de la Frontera Sur – ECOSUR, Tapachula, Chiapas, Mexico Patricia  López  Programa Moscas de la Fruta SENASICA-SADER, Metapa de Domínguez, Chiapas, Mexico Phillip Lowe  United States Department of Agriculture, Animal and Plant Health Inspection Service, Plant Protection and Quarantine (USDA APHIS PPQ), Raleigh, NC, USA Enrique Medianero  Universidad de Panamá, El Cangrejo, Panama Fractyl  Mertilus  Ministère de l’Agriculture des Ressources Naturelles et du Développement Rural, Port-au-Prince, Haiti Mario A. Miranda-Salcedo  Campo Experimental Valle de Apatzingán-CIRPAC-­ INIFAP, Antúnez, Michoacán, México Pablo  Montoya  Instituto de Biociencias, Universidad Autónoma de Chiapas, Tapachula, Chiapas, Mexico David  Salas  Mujica  Proyecto Nacional de Manejo de Mosca de la Fruta, Guayaquil, Ecuador

xiv

Contributors

Albérico  Fernando  Murúa  Dirección de Sanidad Vegetal, Animal y Alimentos (DSVAA), Gobierno de la provincia de San Juan, Rivadavia, San Juan, Argentina Sergio Marcelo Ovruski  LIEMEN, División Control Biológico de Plagas, PROIMI Biotecnología CONICET, San Miguel de Tucumán, Tucumán, Argentina Ligia  Romero  Pardo  Universidad de las Fuerzas Armadas ESPE, Sangolquí, Ecuador Carlos  Pascacio-Villafán  Red de Manejo Biorracional de Plagas y Vectores, Clúster Científico y Tecnológico BioMimic, Instituto de Ecología, A.C. – INECOL, Antúnez, Michoacán, Mexico Julia  Bolaños  Pineda  Estación Científica Charles Darwin, Santa Cruz, Galápagos, Ecuador Adalton Raga  Instituto Biológico, Campinas, SP, Brazil Mohsen  M.  Ramadan  State of Hawaii Department of Agriculture, Division of Plant Industry, Honolulu, HI, USA Louise A. Rodríguez-Scott  Universidad de Panamá, Panama City, Panama Tim  Roland  USDA- Animal and Plant Health Inspection Service (Retired), Edinburg, TX, USA Juan Rull  LIEMEN, División Control Biológico de Plagas, PROIMI Biotecnología, CONICET, San Miguel de Tucumán, Tucumán, Argentina Juan Tigrero Salas  Universidad de las Fuerzas Armadas ESPE, Sangolquí, Ecuador Iris B. Scatoni  Universidad de la Republica, Montevideo, Uruguay Lorena  Suárez  CONICET-Dirección de Sanidad Vegetal, Animal y Alimentos (DSVAA), San Juan, Argentina Shaharra Usnick  USDA APHIS PPQ, Fort Collins, CO, USA Xingeng  Wang  USDA-ARS Beneficial Insects Introduction Research Unit, Newark, DE, USA Trevor Williams  Red de Manejo Biorracional de Plagas y Vectores, Instituto de Ecología, Xalapa, Veracruz, Mexico John  Worley  USDA- Animal and Plant Health Inspection Service, Edinburg, TX, USA Hernan  Zetina  Quarantine Department, Belize Agricultural Health Authority, Belmopan City, Cayo District, Belize

About the Editor

Flávio Roberto Mello Garcia  He is a professor at Universidade Federal de Pelotas (UFPel), Brazil. He did a master’s degree and a Ph.D. in Zoology (Entomology) at the Pontifical Catholic University of Rio Grande do Sul (PUCRS), Brazil. He did post-doctoral training at the University of Florida (UF) and at the US Department of Agriculture (USDA). He is recepient of  Research Productivity Scholarship of CNPq (Brazilian National Council for Scientific and Technological Development). He is the author of more than 230 articles, 11 chapters, and 11 books. He advised postdoctoral, doctorate, master, and scientific initiation. He coordinated more than 34 research projects in Brazil, Africa, Uruguay, and the United States. Advised more than 100 undergraduate and graduate students  during his career. He was elected a full member of Sigma Xi for the quality of research in Entomology.

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Part I

General Aspects of Fruit Fly Management

Chapter 1

Fruit Flies: A Threat to Fruit Production in the Americas Flávio Roberto Mello Garcia

Abstract  This chapter briefly introduces the basics of fruit fly management in the Americas. A total of 21 species of fruit flies belonging to the genera Anastrepha Schiner, Bactrocera Macquart, Ceratitis MacLeay, and Rhagoletis Loew have economic importance. This chapter presents information about their host plants as well as the aspects of their biology, geographic distribution, and damage. Keywords  Ecology · Economic importance · Distribution · Tephritidae

1.1 Introduction The American continent consists of more than 50 countries divided into North, Central, and South America and the Caribbean and occupies an area of more than 40 million km2 (Worlddata 2023). The Americas have two ecozones: the Nearctics and the Neotropics. The Nearctic ecozone includes the entire territories of Canada and the United States of America and the central-northern regions of Mexico and has an extension of 22.9 million km2 (Anthropocene 2023). The vegetation comprises the tundra, taiga, temperate deciduous forests, temperate grasslands, and temperate deserts. Furthermore, along the Pacific coast, we find temperate rainforests to the north and Mediterranean ecosystems to the south, whereas mangroves are located along the coast of the Gulf of Mexico and the southern area of ​​the Atlantic coast (Anthropocene 2023). The Neotropical region comprises South America and Central America and reaches as far north as central Mexico (Morrone 2014), with diverse vegetation, dry deserts, and a humid rainforest (Burnham and Graha 1999). Most of Latin America (LA) is inside the Neotropical ecozone, leaving only a part of Mexico in the Nearctic. LA is the largest tropical fruit-exporting region in the F. R. Mello Garcia (*) Departamento de Ecologia, Zoologia e Genética, Instituto de Biologia, Universidade Federal de Pelotas, Pelotas, RS, Brazil e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2024 F. R. Mello Garcia (ed.), Management of Fruit Flies in the Americas, https://doi.org/10.1007/978-3-031-48608-1_1

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F. R. Mello Garcia

world and accounts for about 25% of the total worldwide production of fruits, with an annual production of about 54 million tons. This region generates an estimated total export value of around US $ 11 billion (FAO 2019). One of the biggest problems in fruit production is the attack of fruit flies. The females lay their eggs inside the fruits and, from these fruits, hatch larvae that feed on the endocarp; in addition, they allow the entry of microorganisms that cause fruit rot. Fruit flies can also cause damage to fruit exports from one country to another due to quarantine restrictions. The total amount of direct and indirect losses caused by fruit flies can exceed US$ 1 billion per year worldwide (Leonardo et al. 2019).

1.2 Fruit Flies of Economic Importance in the Americas There are 977 species of Tephritidae registered in the Americas, of which 73% occur in the Neotropical region (Hernandez-Ortiz et  al. 2010). Of these species, only 21 belonging to the genera Anastrepha Schiner, Bactrocera Macquart, Ceratitis MacLeay, and Rhagoletis Loew have economic importance (Table  1.1). Hawaii, which is a state in the United States of America, is not located in the Americas and presents fruit flies of great economic importance such as Bactrocera dorsalis (Hendel) (oriental fruit fly), Bactrocera latifrons (Hendel) (Solanum fruit fly), and Zeugodacus cucurbitae (Coquillett) (melon fruit fly); although Drosophila suzukii Matsumura (Diptera: Drosophilidae) causes many problems to fruit production in many countries of the Americas (Garcia et al. 2022), the management of this insect has already been addressed in another book by Springer Nature (Garcia 2020). Therefore, information about D. suzukii will not be addressed in this book. Most species of fruit flies of the genus Anastrepha occur in the Neotropical region, but some species can be found in the Nearctic region closest to the Neotropical region (Garcia 2009). Most species of fruit fly pests belong to the genus Anastrepha (11 species): Anastrepha curvicauda (Gerstaecker), Anastrepha fraterculus (Wied.), Anastrepha grandis (Macquart), Anastrepha ludens (Loew), Anastrepha obliqua (Macquart), Anastrepha serpentina (Wied.), Anastrepha sororcula Zucchi, Anastrepha striata Schiner, Anastrepha suspensa (Loew), Anastrepha pseudoparallela Loew, and Anastrepha zenildae Zucchi (Table 1.1). The second genus with the most fruit fly pests in the Americas is Rhagoletis with seven species: Rhagoletis cerasi Loew, Rhagoletis cingulata (Loew), Rhagoletis completa (Cresson), Rhagoletis fausta (Osten-Sacken), Rhagoletis indifferens Curran, Rhagoletis mendax Curran, and Rhagoletis pomonella Walsh. In the Americas, the genus Rhagoletis is distributed in both the Nearctic and Neotropical regions (Ramirez et al. 2008). Although there are records of some Neotropical species of Rhagoletis attacking Solanaceae in the Neotropical region, such as Rhagoletis blanchardi (Aczel) in Brazil (Fenili 1993), Rhagoletis nova (Schiner) and Rhagoletis tomatis Foote in Chile and Mexico (Salazar et al. 2002, Rull 2020), and Rhagoletis conversa (Brèthes) and Rhagoletis penela Foote in Chile (Salazar et al. 2002), their pest status

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1  Fruit Flies: A Threat to Fruit Production in the Americas

Table 1.1  List of species of fruit flies of importance in the Americas (North America, Central America, South America, US mainland), their common names, distribution, and host range Fruit fly pest Distribution (the Americas) Genus Anastrepha Schiner North America (Florida A. curvicauda Peninsula, southern (Gerstaecker), Texas, and Mexico), Central papaya fruit fly America, the Caribbean, and South America (Venezuela and Colombia) Neotropical region and the A. fraterculus United States of America (Wied.), South (southern Texas) American fruit fly

Host range

References

Monophagous Carica papaya

Mingoti et al. (2022)

Polyphagous

EPPO (2023a), Garcia et al. (2017, 2020), and Garcia (2023a, b) Machado Teixeira et al. (2022), and Garcia (2023a, b) EPPO (2023b) and Garcia et al. (2020) EPPO (2023c) and Garcia (2023a, b) CABI (2023a)

A. grandis (Macquart), South American cucurbit fruit fly

Argentina, Bolivia, Brazil, Colombia, Ecuador, Panama, Paraguay, Peru, and Venezuela

Oligophagous Cucurbitaceae

A. ludens (Loew), Mexican fruit fly

From northeastern Mexico south to Panama

Polyphagous

A. obliqua (Macquart), West Indian fruit fly A. serpentina (Wied.), sapodilla fruit fly

From Mexico and the West Indies Polyphagous to northern Argentina From Mexico to northern Argentina

A. sororcula Zucchi, Brazil, Colombia, Ecuador, and Paraguay South American guava fruit fly A. striata Schiner, guava fruit fly

Bolivia, Brazil, Colombia, Costa Rica, Ecuador, French Guiana, Guatemala, Guyana, Honduras, Mexico, Netherlands Antilles, Nicaragua, Panama, Paraguay, Peru, Suriname, Trinidad and Tobago, and Venezuela A. suspensa (Loew), Caribbean, southern and central Caribbean fruit fly Florida, and French Guiana A. pseudoparallela Brazil and Peru Loew, passion fruit fly

Sapotaceae occasionally attacks a variety of other hosts, including Citrus spp. Polyphagous

Polyphagous

Polyphagous Stenophagous, Passiflora spp.

Souza et al. (2021) and Garcia (2023a, b) EPPO (2023d)

Adaime et al. (2018) Alberti et al. (2009) and Salazar-­ Mendonza et al. (2020) (continued)

F. R. Mello Garcia

6 Table 1.1 (continued) Fruit fly pest Distribution (the Americas) A. zenildae Zucchi, Brazil Brazilian fruit fly Genus Bactrocera Macquart Brazil (Amapá, Pará, and B. carambolae Drew and Hancock, Roraima), French Guiana, carambola fruit fly Guyana, and Surinam The United States of America B. dorsalis (California and Florida) (Hendel), Oriental fruit fly B. oleae (Rossi), Mexico and the United States of olive fruit fly America (California) Genus Ceratitis MacLeay C. capitata (Wied.), Brazil (24 states), Colombia, Mediterranean fruit Costa Rica, Ecuador, El Salvador, Guatemala, Honduras, Nicaragua, fly Panama, Paraguay, Peru, the United States of America (California, Florida), Uruguay, and Venezuela Genus Rhagoletis Loew R. cerasi Loew, Canada (Ontario and Quebec) cherry fruit fly and the United States of America (New York state) From Michigan to New R. cingulata (Loew), cherry fruit Hampshire, southward to Florida, occurring over the entire middle fly and eastern region of the United States of America and also in southeastern and south-central Canada Southern, central, and western R. completa United States of America (Cresson), walnut husk fly R. fausta (Osten-­ The United States of America and Canada Sacken), black cherry fruit fly Western United States and R. indifferens southwestern Canada Curran, Western cherry fruit fly R. mendax Curran, Eastern North America (Canada blueberry fruit fly and the United States of America) R. pomonella Walsh, apple maggot

North America

Host range Polyphagous

References Garcia (2009)

Polyphagous

Polyphagous

EPPO (2023e) and Garcia (2009) USDA (2023)

Monophagous Olea europaea

Muller et al. (2019)

Polyphagous

EPPO (2023f)

Stenophagous, Prunus spp.

EPPO (2023g)

Stenophagous, Prunus spp.

Weems, Jr. (2021)

Stenophagous, Juglans spp. and Prunus spp. Stenophagous, Prunus spp.

CABI (2023b)

Stenophagous, Prunus spp.

Yee et al. (2013)

Stenophagous, Vaccinium spp. and Gaylussacia spp. Stenophagous, Crataegus spp. and Malus domestica

CABI (2023c)

EFSA (2020)

Yee et al. (2013)

1  Fruit Flies: A Threat to Fruit Production in the Americas

7

must be carefully evaluated on the basis of their population densities and economic damage in each region.. The genus Bactrocera is native to Asia and Europe and presents species with a high invasion capacity (Garcia 2009). This genus is represented by three invasive species in the Americas: Bactrocera carambolae Drew and Hancock, B. dorsalis (Hendel), and Bactrocera oleae (Rossi). The genus Ceratitis is native to the tropical areas of Africa (Garcia 2009), as only a single species has invaded the continent, that is, Ceratitis capitata (Wied.). Knowledge about the ecology and behavior of fruit flies is one of the pillars of their effective management (Garcia 2022). The tefritids, for example, can be divided into four groups according to their host range (Fletcher 1989): 1. The polyphagous species, for example, A. fraterculus, A. ludens, and C. capitata, are fruit flies that breed in a wide host range (several families). These species have many hosts of different plant families. They use exotic hosts, either native or non-native, although they may have a preference for some specific type of host. 2. The oligophagous species, for example, A. grandis, are fruit flies with the majority of their hosts boasting a single plant family; this is a species that has hosts of some genera of Cucurbitaceae in some South American countries (Machado Teixeira et al. 2022). 3. The stenophagous species, for example, many species of Rhagoletis (Table 1.1), breed in a smaller number of closely related hosts; this species has host plants of one or two genera, such as R. cerasi, R. fausta, R. completa, and R. mendax, as their hosts (Prunus spp.). 4. The monophagous species that are restricted to a single host, for example, A. curvicauda, has as host only papaya (Carica papaya) and B. oleae has only olive (Olea europaea). To suppress populations, an area-wide integrated pest management (AW-IPM) approach is required, ranging from monitoring to postharvest treatment. This book covers the main forms of fruit fly management in several countries of the Americas. Some countries in the Americas, such as Argentina, Brazil, Mexico, and the United States of America, have a long experience in the research and management of these pests, resulting in denser chapters. This book brings together 68 renowned researchers from the most important universities and research centers in the Americas. This book contains information about 18 countries: Argentina, Belize, Bolivia, Brazil, Chile, Colombia, Cuba, the Dominican Republic, Ecuador, Guatemala, Haiti, Honduras, Mexico, Panama, Peru, Suriname, Uruguay, and the United States of America. This book consists of two parts. The first part titled “General Aspects of Fruit Fly Management” addresses the general aspects of the management of fruit flies in the Neotropical region, monitoring and mass trapping of fruit flies, biological control, and phytosanitary irradiation. The second part, entitled “Management of Fruit Flies in the Countries of the Americas,” treats the way in which fruit fly management is carried out in each country in greater detail.

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References Adaime R., Jesus CR. Lima, AL et al. (2018) Anastrepha suspensa (Loew) (Diptera: Tephritidae). In: Fidelis EG, Lohmann, TR et  al (Eds). Priorização de pragas quarentenárias ausentes no Brasil. Brasília: Embrapa, p. 123–136 Alberti S, Garcia FRM, Bogus GM (2009) Moscas-das-frutas (Diptera: Tephritidae) em pomares de pessegueiro e maracujazeiro no município de em Iraceminha, Santa Catarina. Ciên Rural 39:1565–1568. https://doi.org/10.1590/S0103-­84782009005000077 Anthropocene (2023). https://antropocene.it/en/2023/02/01/neartic/ Burnham RJ, Alan Graham A (1999) The history of neotropical vegetation: new developments and status. Ann Missouri Bot Gard 86(2):546–589. https://doi.org/10.2307/2666185 CABI (2023a) Anastrepha serpentina. https://www.cabidigitallibrary.org/doi/10.1079/ cabicompendium.5665 CABI (2023b) Rhagoletis completa. abidigitallibrary.org/doi/10.1079/cabicompendium.4705 3#:~:text=fragmentary%20morphological%20data.-,Distribution,Seljak%20and%20 Zezlina%2C%201999) CABI (2023c) Rhagoletis mendax. https://www.cabidigitallibrary.org/doi/10.1079/ cabicompendium.47057 EFSA European Food Safety Authority (2020) Pest survey card on Rhagoletis fausta 20p. https:// doi.org/10.2903/sp.efsa.2020.EN-­1917 EPPO (2023a) Anastrepha faterculus. https://gd.eppo.int/taxon/ANSTFR EPPO (2023b) Bactrocera carambolae. https://gd.eppo.int/taxon/BCTRCB/distribution EPPO (2023c) Anastrepha ludens. https://gd.eppo.int/taxon/ANSTLU/distribution EPPO (2023d) Ceratitis capitata. https://gd.eppo.int/taxon/CERTCA/distribution EPPO (2023e) Anastrepha obliqua https://gd.eppo.int/taxon/ANSTOB EPPO (2023f) Anastrepha striata. https://gd.eppo.int/taxon/ANSTST EPPO (2023g) Rhagoletis cerasi. https://gd.eppo.int/taxon/RHAGCE FAO 2019 Available on http://www.fao.org/brasil/noticias/detail-­events/pt/c/1193684/. Accessed 22 Jun 2020 Fenili R (1993) Ocorrência de Rhagoletis blanchardi (Aczél) (Diptera: Tephritidae) em tomateiro. An Soc Entomol Brasil 22:415–416 Fletcher BS (1989) Life history strategies of tephritid fruit flies. In: World Crop Pests. Vol.3B: Fruit Flies: Their Biology, Natural Enemies and Control. Amsterdam: Elsevier, p. 195–208 Garcia FRM (2009) Fruit fly: biological and ecological aspects. In: Bandeira RR (ed) Current trends in fruit flies control on perennial crops and research prospects. Kerala: Transworld Research Network, pp 1–35 Garcia FRM (2020) Drosophila suzukii management, 1st edn. Springer International Publishing, New York, p 287p. https://doi.org/10.1007/978-­3-­030-­62692-­1 Garcia FRM (2022) Studies of Fruit Flies and their Behaviors, 1st edn. Nova Publisher, New York, p 223p. https://doi.org/10.52305/ZCQJ2829 Garcia FRM, Ovruski SM, Suárez L et al (2020) Biological control of tephritid fruit flies in the Americas and Hawaii: A review of the use of parasitoids and predators. Insects 11:662. https:// doi.org/10.3390/insects11100662 Garcia FRM (2023a) Moscas-das-frutas, suas plantas hospedeiras e parasitoides no Estado do Paraná. In: Zucchi RA, Malavasi A, Adaime et  al (eds) Moscas-das-frutas no Brasil: Conhecimento básico e Aplicado, vol 2. FEALQ, Piracicaba, pp 241–247 Garcia FRM (2023b) Moscas-das-frutas, suas plantas hospedeiras e parasioides no Estado de Santa Catarina. In: Zucchi RA, Malavasi A, Adaime et al (eds) Moscas-das-frutas no Brasil: Conhecimento básico e Aplicado, vol 2. FEALQ, Piracicaba, pp 345–355 Garcia FRM, Brida AL, Martins LN et  al (2017) Biological control of fruit flies of the genus Anastrepha (Diptera: Tephritidae): Current status and perspectives. In: Davenport L (ed) Biological control: methods, applications and challenges, 1st edn. Nova Science Publishers, Hauppauge, pp 29–71

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Garcia FRM, Lasa R, Funes C et al (2022). Drosophila suzukii Management in Latin America: Current status and perspectives. J Econ Entomol 115, p. 1008–1023 https://doi.org/10.1093/ jee/toac052 Hernández-Ortiz V, Guillén-Aguilar J, Ópez L (2010) Taxonomía e Identificación de Moscas de la Fruta de Importancia Económica en América In Montoya P, Toledo P, Hernández E (eds.), Moscas de la Fruta: Fundamentos y Procedimientos para su Manejo, 2010. S y G editores, México, D.F. pp. 49–80 Leonardo MM, Faria FA (2019) Um Sistema de Reconhecimento de Espécies de Moscas-das-­ Frutas. Rev Eletron Iniciação Científ Comp 17(2):1–10. https://seer.ufrgs.br/reic/article/ view/93500 Machado Teixeira C, Peter Kruger A, Garcia FRM et  al (2022) Global potential distribution of Anastrepha grandis (Diptera, Tephritidae) under climate change scenarios. Crop Prot 151(105836):2. https://doi.org/10.1016/j.cropro.2021.105836 Mingoti R, Young MCP, Jacomo BO et al (2022) Territorial zoning of Brazilian areas favorable to Anastrepha curvicauda (Diptera: Tephritidae) in papaya crop. Res J Agric Sci 2(3):2. https:// doi.org/10.22533/at.ed.973232218048 Morrone JJ (2014) Biogeographical regionalization of the Neotropical region. Zootaxa 3782(1):1–110. https://doi.org/10.11646/zootaxa.3782.1.1 Muller FA, Dias NP, Gottschalk MS et al (2019) Potential distribution of Bactrocera oleae and the parasitoids Fopius arisanus and Psyttalia concolor, aiming at classical biological control. Biol Control 132:144–151. https://doi.org/10.1016/j.biocontrol.2019.02.014 Ramírez CC, Salazar M, Palma RE et al (2008) Phylogeographical analysis of Neotropical Rhagoletis (Diptera: Tephritidae): Did the Andes uplift contribute to current morphological differences? Neotrop Entomol 37(6):651–661. https://doi.org/10.1590/s1519-566x2008000600005 Rull J (2020) Distribución y Relevancia del género Rhagoletis en México. In: Toledo J, Hernández E (eds) Moscas de la Fruta: Fundamentos y Procedimientos para su Manejo; Montoya P. S y G Editores, México, pp 165–184 Salazar M, Theoduloz C, Vega A et al (2002) PCR-RFLP identification of endemic Chilean species of Rhagoletis (Diptera: Tephritidae) attacking Solanaceae. Bull Entomol 92(4):337-41. Bull Entomol 92(4):337–341. https://doi.org/10.1079/BER2002168 Salazar-Mendoza P, Ninahuamán-Calderón A Fernández CG et  al (2020). First record of Anastrepha pseudoparallela Loew (Diptera: Tephritidae) infesting passion flowers in Peru. Rev Peru Biol 27(2): 229–232. https://doi.org/10.15381/rpb.v27i2.17878 Souza AV, Miranda EA, Passos JF et al (2021) Predicting the invasion risk by Anastrepha sororcula (Diptera: Tephritidae) in distinct geographic regions. Neotrop Entomol 50(6):989–998. https://doi.org/10.1007/s13744-­021-­00907-­w USDA (2023) Fruit flies. https://www.aphis.usda.gov/aphis/ourfocus/planthealth/ plant-­pest-­and-­disease-­programs/pests-­and-­diseases/fruit-­flies/fruit-­flies-­home Weems Jr HV (2021). Cherry fruit fly, Rhagoletis cingulata (Loew) (Insecta: Diptera: Tephritidae). UF Extnsion. https://edis.ifas.ufl.edu/publication/IN360 Worlddata (2023) Americas. https://www.worlddata.info/america/index.php Yee WL, Hernández-Ortiz V, Rull J et al (2013) ST 04: Status of Rhagoletis (Diptera: Tephritidae) Pests in the NAPPO Countries. NAPPO Science and Technology Documents, p 27p

Chapter 2

Fruit Fly (Tephritidae) Management in the Neotropical Region: History, State of the Art, and Perspectives Martín Aluja, Sergio Marcelo Ovruski, Flávio Roberto Mello Garcia, Maribel Hurtado, and Walther Enkerlin Abstract  We first examine the most active countries in terms of research and highlight the critical role that international organizations have been playing in aiding fruit fly control/management efforts in the Neotropics. We then briefly review highlights on the history and current situation of fruit management in the Neotropical region moving from south to north, including the introduction of exotic species such as Ceratitis capitata and Bactrocera carambolae. A special section of this chapter is dedicated to the seminal role played by the International Atomic Energy Agency (IAEA) in helping countries in the Neotropics manage fruit flies. In doing so, we have touched upon the recent advances made in implementing area-wide management and establishing low-prevalence and pest-free areas (PFAs) using the sterile insect technique and biological control. We finish by briefly reviewing the advances in the implementation of environmentally friendly schemes such as the experimental application/testing of the incompatible insect technique (IIT), host marking pheromones (HMPs), mycoinsecticides/pathogens, magnetite nanoparticles, saliM. Aluja (*) Red de Manejo Biorracional de Plagas y Vectores, Clúster Científico y Tecnológico BioMimic, Instituto de Ecología, A.C. – INECOL, Xalapa, Veracruz, Mexico e-mail: [email protected] S. M. Ovruski LIEMEN, División Control Biológico de Plagas, PROIMI Biotecnología, CCT CONICET NOA Sur, San Miguel de Tucumán, Argentina e-mail: [email protected] F. R. Mello Garcia Departamento de Ecologia, Zoologia e Genética, Instituto de Biologia, Universidade Federal de Pelotas, Pelotas, RS, Brazil e-mail: [email protected] M. Hurtado North American Plant Protection Organization, NAPPO, Raleigh, NC, USA W. Enkerlin Insect Pest Control Section, Joint FAO/IAEA Division, Vienna, Austria e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2024 F. R. Mello Garcia (ed.), Management of Fruit Flies in the Americas, https://doi.org/10.1007/978-3-031-48608-1_2

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cylic acid, chitosan coatings, breeding for fruit resistance to attacks by fruit flies, fruit bagging, and orchard design, touching upon the threat represented by global climate change, particularly mass deforestation, and global warming, as the range of certain pestiferous species such as Anastrepha ludens, Anastrepha grandis, and C. capitata could considerably expand. Keywords  Neotropics · Tephritidae · Area-wide management · Sterile insect technique · Biological control · Anastrepha · Ceratitis · Bactrocera

2.1 Introduction The history of fruit fly (Diptera: Tephritidae) research/management in the Neotropics is rich and varied and has been reviewed, among others, by Aluja (1999). The basis of our knowledge on fruit flies stems from the pioneering work by taxonomists/ systematists, who, many times, not only described species but also shared insightful information on their biology. Among the most influential (measured by the number of species identified), M. Aczél, M. Bezzi, F.L. Blanc, E.E. Blanchard, J. Brethes, D.W. Coquillet, R.H. Foote, C.T. Greene, K.J. Hayward, F.G. Hendel, A.M Lima da Costa, H. Loew, J.P.M. Macquart, G.C. Steyskal, and C.R.W. Wiedemann stand out. More recently, A.L.  Norrbom (USA), R.A.  Zucchi (Brazil), D.  Frías (Chile), C. Korytkowski (Panama†), K. Uramoto (Brazil), G.J. Steck (USA), V. Hernández-­ Ortíz (Mexico), N.A.  Canal (Colombia), and P.A.  Rodríguez-Clavijo (Colombia) have greatly contributed not only to the taxonomy/systematics of fruit flies in the Neotropics but also to the knowledge of their natural history and biology (Carroll et al. 2002). The important role of taxonomists has recently been highlighted by the publication of Norrbom et al.’s study (2018a), in which the former genus Toxotrypana Gerstaecker (1860) is now part of Anastrepha Schiner (1868), given the precedence of the latter genus. As a result, the former Toxotrypana curvicauda Gerstaecker, a notorious pest of papayas, has been renamed as Anastrepha curvicauda (Gerstaecker) (Norrbom et al. 2018b). Based on publication records, a few countries have been standing out as leaders in both research activities and control/management programs in more recent times: from south to north, these are Argentina (Ovruski et al. 2003, 2010; Fernandes et al. 2012; Oroño et al. 2013; Cladera et al. 2014; Vera et al. 2014; Schliserman et al. 2014a; Segura et  al. 2018), Brazil (Malavasi and Zucchi 2000; Adaime da Silva et al. 2011; Deus et al. 2016; García and Ricalde 2013; Garcia et al. 2020; Magalhães et  al. 2022; Machado-Teixeira et  al. 2022), and Mexico (Aluja and Liedo 1986; Montoya et al. 2000; Piñero et al. 2003; Porras and Lecuona 2008; Aluja and Rull 2009; Toledo et  al. 2017; Díaz-Fleischer et  al. 2009, 2017, 2019; Cancino et  al. 2019; Birke et al. 2019; Liedo et al. 2021; Pérez-Staples et al. 2021; Aluja et al. 2014a, 2021, 2023; Rull et  al. 2018; Pascacio-Villafán et  al. 2022; Guillén et  al.

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2022a, b). Additional efforts, albeit at a much smaller scale, come from Chile (Harris and Olalquiaga 1991; Frías et al. 1986, 1992; Lobos 1996), Peru (Herrera and Viñas 1977; Korytkowski 2001), Ecuador (Tigrero 1998; Tigrero and Salas 2007; Tigrero and Vitaluña 2010; Meza-Aguilar et al. 2022), Venezuela (Briceño 1975; Boscán de Martínez et al. 1980; Caraballo 1981, 1985; Katiyar et al. 2000), Colombia (Peña and Bellotti 1977; Olarte 1980; Núñez-Bueno 1981; Norrbom et al. 2005; Canal 2010; Aluja et al. 2019; Amat et al. 2022), Panama (van der Linde et al. 2006; Medianero et al. 2006; Norrbom and Korytkowski 2008; Medianero and Alvarado-­Gálvez 2016), Costa Rica (Picado 1920; Jirón and Soto-Manatiú 1987; Jirón and Hedström 1988, 1991; Soto-Manatiú et  al. 1987; Hedstroem 1991; Camargo et al. 1996), and Guatemala (Eskafi and Cunningham 1987; Sivinski et al. 2000; López et al. 2003; Puche et al. 2005; Rendón et al. 2004; Flores et al. 2016; Lira and Midgarden 2021; Cotoc-Roldán et al. 2021). Finally, isolated efforts come from Uruguay (Calvo et al. 2019; Duarte et al. 2020, 2021), Bolivia (Conde-Blanco et  al. 2018), Suriname (Van Sauers-Muller 1991, 2005), Nicaragua (Borge and Basedow (1997); Saldaña-Reyes et  al. 2019; Martínez and Castillo  2020; Juárez et al. 2021), El Salvador (Delmi et al. 1996), and a few of the Caribbean Islands such as the Dominican Republic (Serra et  al. 2011; Torres-Quezada et  al. 2021; Zavala et al. 2021), Puerto Rico (Sein 1933; Segarra 1988; Jenkins and Goenaga 2007, 2008; Jenkins et  al. 2013), and Cuba (Vázquez et  al. 2008; Borges-Soto et al. 2019). Only those aspects related to control and management will be reviewed in this chapter, and we will do so by considering the countries where the most action has occurred in the Neotropics. As this book contains chapters dedicated to specific countries, we were careful not to unnecessarily repeat information here. For reviews on fruit fly biology, ecology, and behavior, we refer the reader to the following books: Aluja and Norrbom (2000) and, more recently, Garcia (2022). We also refer the reader to various broad reviews in which a wealth of information can be found that we do not repeat here. The following stand out: Aluja (1994), Purcell (1998), Aluja and Mangan (2008), Ovruski et al. (2000), Badii et al. (2015), De Meyer et al. (2015), Enkerlin et al. (2015, 2017), Garcia et al. (2020), Pérez-Staples et al. (2021), Scolari et  al. (2021), Rendón and Enkerlin (2021), and Dias et  al. (2018, 2022). Several recent books will also come in handy as general references: Clarke (2019), Pérez-Staples et al. (2019), Dyck et al. (2021), and Hendrichs et al. (2021a, b). Finally, we highlight the seminal role that international organizations have been playing in aiding fruit fly control/management efforts in the Neotropics. The following stand out: International Atomic Energy Agency (IAEA), the Food and Agriculture Organization (FAO), El Instituto Internacional de Cooperación para la Agricultura (IICA), and El Organismo Internacional Regional de Sanidad Agropecuaria (OIRSA). These organizations often offer expert advice to many countries in the Neotropics, many times financing cooperative applied research, action programs, or mass-rearing/sterilization facility construction. They also finance or directly publish many manuals, booklets/leaflets, and guidelines/action plans supporting both technical staff and fruit growers. For example, in recent years, the FAO/IAEA or the FAO/IAEA/OIRSA or the IAEA/OIRSA have published the following taxonomic

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or photographic guides on fly identification, fruit sampling guidelines, or action plans: FAO/IAEA (2016, 2017, 2018), Enkerlin et al. (2019), IAEA/OIRSA (2019), Guillén-Aguilar (2020), and Piper et al. (2021) (plus many others). The Inter-American Coordinating Group in Plant Protection (GICSV, Spanish acronym) was founded in 1998 to encourage the adoption of appropriate pest management measures and to promote coordinated actions to prevent the introduction and spread of pests in plants, plant products, and other regulated commodities. The GICSV is coordinated by El Instituto Interamericano de Cooperación para la Agricultura (IICA), which serves as the technical secretariat, and by the Regional Plant Protection Organizations, or RPPOs, of the Americas, which are the following: • The North American Plant Protection Organization (NAPPO) that is the Regional Plant Protection Organization for the North American region (Canada, the United States, and Mexico). • El Organismo Internacional Regional de Sanidad Agropecuaria (OIRSA) that includes the Agriculture and Livestock Ministries and Secretariats of its nine member countries: Mexico, Belize, Guatemala, El Salvador, Honduras, Nicaragua, Costa Rica, Panama, and the Dominican Republic. • Comité de Sanidad Vegetal del Cono Sur (COSAVE) that includes the governments of Argentina, Bolivia, Brazil, Chile, Paraguay, Peru, and Uruguay. • Comunidad Andina (CAN) that includes the governments of Bolivia, Colombia, Ecuador, and Peru. • The Caribbean Agricultural Health and Food Safety Agency (CAHFSA) that includes the governments of Antigua and Barbuda, Bahamas, Barbados, Belize, Dominica, Grenada, Guyana, Haiti, Jamaica, Montserrat, Suriname, St. Lucia, St. Kitts and Nevis, St. Vincent and the Grenadines, and Trinidad and Tobago. The GICSV has set up working groups for several economically important pests in the region. Each working group is composed of experts from various RPPO countries. The Fruit Fly Working Group (FFWG) was created in response to the significant relevance of pestiferous tephritids in the region and internationally. Several projects have been developed or are planned by this working group for the period 2021–2023 following its work plan, for example, a survey of the surveillance and management programs implemented in each of the GICSV member countries. The following variables will be recorded in the study: the species of economically important fruit flies present in each country, human resources and installed capacity available for the development of programs, declarations of free and low-prevalence areas, and available diagnostic technologies. The results of this survey will be used to identify the strengths and weaknesses of the different countries and regions as well as the areas in need of support. They will also be used to lead technical cooperation measures based on the needs and development opportunities for the regions. Additionally, the FFWG has invested a considerable amount of time in creating a digital library for the continuous exchange of relevant information related to the surveillance, control, and eradication of fruit flies, such as manuals, scientific papers, guides, protocols, and regulations. The following website can be visited for further information on the GICSV or the initiatives launched by the various working

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groups and its members: http://apps.iica.int/GICSV/programas/SanidadVegetal/ default.aspx.

2.2 Country-by-Country Assessment of Actions/Programs Devoted to Fruit Fly Management/Control in the Neotropics In what follows, we will review management/control actions/programs in selected countries (i.e., Argentina, Uruguay, Bolivia, Paraguay, Chile, Peru, Brazil, Ecuador, Colombia, Suriname, and Mexico), trying, as mentioned before, not to duplicate the information provided in the entire chapters on some of these countries. Given the magnitude of the impact it has had over the years, we devote a special section to activities led by the IAEA, which include the countries mentioned above plus several others in Central America and the Caribbean. We highlight the fact that when the South American fruit fly, Anastrepha fraterculus (Wiedemann), is mentioned, the readers should be aware that this species actually represents a species complex, with specimens exhibiting clear genetic differences depending on the region they come from (Ludeña et al. 2010; Hernández-Ortíz et al. 2012, 2015; Sutton et al. 2015; Vaníčková et al. 2015; Logan and McKenna et al. 2019; Selivon et al. 2022), and that, in some cases (e.g., Mexico), the naming of a new species is long overdue (Aluja et al. 2003; Hernández-Ortíz et al. 2004). We also address the issue of the impact of global change/global warming on fruit fly distribution and management. We conclude this chapter by cursorily reviewing notable recent research and methodological advances that will likely guide future control/management approaches.

2.2.1 Argentina 2.2.1.1 A Historical Overview Tephritid fruit fly control in Argentina was traditionally based on combining chemical and cultural control practices at the orchard level. Malathion plus a food attractant, such as corn, soybean protein, or sugarcane molasses, commonly known as bait sprays, and cultural practices, such as the removal of the infested fruit, were, for a long time, the only methods used (Turica et al. 1971; Aruani et al. 1996). However, high levels of damaged fruit recorded annually in the different fruit-growing areas of the country led to the implementation of fruit fly control, applying an area-wide, integrated management perspective. The Argentinian National Fruit Fly Control and Eradication Programme (locally known as PROCEM), which belongs to the National Service of Agri-Food Health and Quality, Argentina (SENASA, Spanish acronym), was established in 1994 with the aim of integrating local management/ control actions against fruit fly pests on a regional level. This regional division has

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enabled the application of specific control/eradication strategies with an area-wide integrated fruit fly management (AW-IFFM) perspective, adapted to specific ecological features of one or two target fruit fly species (Guillén and Sánchez 2007; Vreysen et  al. 2007). Thus, the country was divided into different fruit-growing regions based on their geographical and ecological conditions, type of soil, isolation of cropped areas, and occurrence of one or both tephritid species of economic importance in Argentina, that is, Ceratitis capitata (Wiedemann) and A. fraterculus. 2.2.1.2 Current Status The exotic C. capitata has spread throughout Argentina, covering latitudes from 22° to 56°S. Thus, in the cold and dry southern (Patagonia) and central-western (Cuyo) fruit-producing regions, the only economically important tephritid species is C. capitata. Area-wide management actions against this species, based on the integrated use of the sterile insect technique (SIT), selective toxic bait spraying, cultural control methods, and stringent quarantine systems, have achieved the phytosanitary status of fruit fly-free areas in the Andean–Patagonian valleys and in both the central and southern fruit-producing highland valleys of the Mendoza province (Cuyo region). The fruit-growing highland Calingasta Valley of the San Juan province (Cuyo region) has reached the phytosanitary status of medfly low-prevalence area. In contrast, the remaining fruit-growing valleys of San Juan are managed with a medfly suppression program (Ramirez 2017). In addition to the abovementioned control tactics, biological control by means of Diachasmimorpha longicaudata (Ashmead) (Braconidae)-augmentative releases has been recently incorporated as a complementary action by the San Juan Fruit Fly Control and Eradication program (Sánchez et al. 2016; Suárez et al. 2019). Anastrepha fraterculus, native to the Neotropics, is mainly confined to the warm and humid northwestern (NOA, Spanish acronym) and northeastern (NEA, Spanish acronym) fruit-producing regions, covering latitudes from 22° to 34°S.  In both northern Argentinian regions, where subtropical environmental conditions prevail, and citrus crops are predominant, A. fraterculus and C. capitata populations coexist in rainforest and cropped areas (Ovruski et al. 2003; Segura et al. 2006). Although A. fraterculus is a widespread cryptic species complex in the Neotropics (Hernández-­ Ortíz et  al. 2012), molecular evidence and mating compatibility tests have suggested that only one morphotype is distributed throughout Argentina (Gómez-Cendra et al. 2016). Interestingly, A. fraterculus has already colonized the western highland valley region of northwestern Argentina, locally known as the Tafí and Calchaquí Valleys (Ovruski et al. 2010; Funes et al. 2017). This region covers the highlands between 1800 and 2100 meters above sea level (MASL) in the provinces of Tucumán, Catamarca, and Salta. It is characterized by valleys surrounded by extensive semiarid plains and high arid mountains devoid of native fruit fly host plants but with the presence of commercially grown fruits such as peaches, apricots, figs, and apples found in artificially irrigated oases. The climate varies from cool, dry, occasionally frosty winters and hot summers with scarce rainfall (with a mean

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temperature of around 16 °C and annual rainfall 29,956 tested individuals) for others, but in all cases, testing provided a predetermined level

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of statistical confidence in the efficacy of the treatment. These studies, and other studies with smaller numbers of insects, were used to set the 150 Gy generic dose for tephritid fruit flies (Follett and Armstrong 2004). For several species, lower doses have been approved, including Mediterranean fruit fly, oriental fruit fly, and several Anastrepha species (Table 5.2).

5.3.8 Modified Atmospheres Modified atmosphere packaging (MAP) and controlled atmosphere (CA) storage creating a low-oxygen environment are used to preserve the quality of fruits and vegetables (Yahia 2006). Low oxygen is known to be radioprotective in insects and other organisms. This raises the question of whether MAP or CA may reduce the efficacy of phytosanitary irradiation treatments. IPPC regulations prohibit the application of phytosanitary irradiation for fruits and vegetables under modified atmospheres; the USDA APHIS has placed minimal limits on the level of O2 created by MAP for produce treated by phytosanitary irradiation. Many studies examining the effect of low oxygen and MAP on radiation tolerance have used tephritid fruit flies as model organisms. Low oxygen has been demonstrated to provide radiation protection at sublethal doses for various biological parameters such as adult emergence, flight ability, mating success, and fertility (Lopez-Martinez and Hahn 2012). The radioprotective effects appear to depend on the radiation dose and oxygen level, with measurable effects occurring at sublethal radiation doses and very low-oxygen concentrations. To date, no studies have shown that irradiation of fruit flies at approved phytosanitary doses under modified atmospheres results in treatment failure, that is, allows successful reproduction (Follett and Neven 2020). For apple maggot, Rhagoletis pomonella (Walsh), irradiation of third instars at 50 Gy in apples under low oxygen (