UNIVERSIDADE ESTADUAL PAULISTA FACULDADE DE CIÊNCIAS AGRÁRIAS E VETERINÁRIAS CÂMPUS DE JABOTICABAL RESISTANT GENOTYPES, BIOLOGICAL CONTROL AND SELECTIVE PESTICIDES FOR THE INTEGRATED MANAGEMENT OF Tetranychus evansi (ACARI: TETRANYCHIDAE) ON TOMATO Patrice Jacob SAVI Agronomist Engineer Jaboticabal-SP 2022 UNIVERSIDADE ESTADUAL PAULISTA FACULDADE DE CIÊNCIAS AGRÁRIAS E VETERINÁRIAS CÂMPUS DE JABOTICABAL RESISTANT GENOTYPES, BIOLOGICAL CONTROL AND SELECTIVE PESTICIDES FOR THE INTEGRATED MANAGEMENT OF Tetranychus evansi (ACARI: TETRANYCHIDAE) ON TOMATO Patrice Jacob SAVI Advisor: Prof. Dr. Daniel Júnior de Andrade Co- Advisor: Prof. Dr. Gilberto José de Moraes 2022 Thesis presented to the Faculdade de Ciências Agrárias e Veterinárias-Unesp, Câmpus de Jaboticabal, as part of requirements to obtain the Doctorate degree in Agronomy (Agricultural Entomology) S267r Savi, Patrice Jacob Resistant genotypes, biological control and selective pesticides for the integrated management of Tetranychus evansi (Acari: Tetranychidae) on tomato / Patrice Jacob Savi. -- Jaboticabal, 2022 167 p. : il., tabs., fotos Tese (doutorado) - Universidade Estadual Paulista (Unesp), Faculdade de Ciências Agrárias e Veterinárias, Jaboticabal Orientador: Daniel Júnior de Andrade Coorientador: Gilberto José de Moraes 1. Tomato red spider mite. 2. Integrated Pest Management. 3. Resistant genotype. 4. Phytoseiidae. 5. Impact of pesticides on predator. I. Título. Sistema de geração automática de fichas catalográficas da Unesp. Biblioteca da Faculdade de Ciências Agrárias e Veterinárias, Jaboticabal. Dados fornecidos pelo autor(a). Essa ficha não pode ser modificada. UNIVERSIDADE ESTADUAL PAULISTA Câmpus de Jaboticabal RESISTANT GENOTYPES, BIOLOGICAL CONTROL AND SELECTIVE PESTICIDES FOR THE INTEGRATED MANAGEMENT OF Tetranychus evansi (ACARI: TETRANYCHIDAE) ON TOMATO TÍTULO DA TESE: CERTIFICADO DE APROVAÇÃO AUTOR: PATRICE JACOB SAVI ORIENTADOR: DANIEL JUNIOR DE ANDRADE COORIENTADOR: GILBERTO JOSÉ DE MORAES Aprovado como parte das exigências para obtenção do Título de Doutor em AGRONOMIA (ENTOMOLOGIA AGRÍCOLA), pela Comissão Examinadora: Prof. Dr. DANIEL JUNIOR DE ANDRADE (Participaçao Virtual) Departamento de Ciencias da Producao Agricola / FCAV UNESP Jaboticabal Prof. Dr. DANIEL CARRILLO (Participaçao Virtual) Departamento de Entomologia e Nematologia - UF/IFAS / Gainesville/Flórida Prof. Dr. RAPHAEL DE CAMPOS CASTILHO (Participaçao Virtual) Departamento de Entomologia e Acarologia / ESALQ/USP - Piracicaba/SP Prof. Dr. MARCELO COUTINHO PICANÇO (Participaçao Virtual) Universidade Federal de Viçosa-UFV / Viçosa/MG Pesquisador Dr. MÁRIO EIDI SATO (Participaçao Virtual) Instituto Biológico de Campinas / Campinas/SP Jaboticabal, 04 de março de 2022 Faculdade de Ciências Agrárias e Veterinárias - Câmpus de Jaboticabal - Via de Acesso Professor Paulo Donato Castellane, s/n, 14884900, Jaboticabal - São Paulo https://www.fcav.unesp.br/#!/pos-graduacao/programas-pg/agronomia-entomologia-agricola/CNPJ: 48.031.918/0012-87. ABOUT THE AUTHOR PATRICE JACOB SAVI was born in Ifangni (Republic of Benin) on March 17th, 1991. Son of Martin Savi and Beatrice Lokossou, he was an undergraduate in Agronomy at Université de Parakou (Republic of Benin), where he finished his degree in 2012. He did an undergraduate thesis under the supervision of Prof. Dr. Fabien C.C. Hountondji and worked with pest management approaches in vegetable crops at the Songhai center in Porto-Novo (Republic of Benin). After getting his degree, he got his first job as a Head Agriculturist at "Groupe Vision Plantain Hévea Cacao (GVPHeC)" in Ifangni (South of the Republic of Benin), mostly working with farmers on the control of the banana weevil, Cosmopolites sordidus (Coleoptera: Curculionidae), and farm maintenance. From there, he went for an internship of two- month at a non-governmental organization "FUDEL" in Ifangni (South Benin) specializing in vegetable crop production to gain more hands-on experience as a horticulturist. After completing this internship, he got a position as Head horticulturist for two years at Aganmandin Farm in charge of Formation, Research in Horticulture, and Animal Husbandry working with all aspects related to the maintenance, pest, and disease control strategies for vegetable crops. From 2014 to 2016, he was also a Professor at Benin Secondary School. In March 2016, he was awarded a scholarship by Conselho Nacional de Desenvolvimento Científico e Tecnológico- CNPq to join the Master Program in Agricultural Entomology Graduate Program (Agronomy) at São Paulo State University (UNESP) working under the supervision of Prof. Daniel Júnior de Andrade, and Gilberto José de Moraes. While in his Master's, he got an interest in selecting African tomato genotypes resistant to Tetranychus evansi (Acari: Tetranychidae). He was immediately accepted to continue as a Doctorate student, soon after the completion of his Master´s program, in early 2018 at the same University, under the supervision of the same advisors, and received a scholarship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-CAPES. e-mail: savipatricejacob@yahoo.fr mailto:savipatricejacob@yahoo.fr DEDICATION Every challenging work needs self-efforts as well as the guidance of elders especially those who were very close to our hearts. My humble effort I dedicate to my Parents: Béatrice and Martin Brothers: Simon, David, Élie, and Isaac Sisters: Agnès and Elisabeth Whose affection, love, encouragement and prayers of day and night make me able to get such success and honor. Along with all hardworking and respected Teachers A keep to growing, as a teacher is to keep company mainly with teachers who uplift you, whose presence inspire you, and whose dedication drives you Robert John Meehan ACKNOWLEDGMENTS First of all, to God Almighty for granting me this valuable opportunity of knowledge and intellectual aptitude to pursue my education life. To my beloved advisor Prof Dr. Daniel Júnior de Andrade, for being so generous with me, for opening his lab up to me, and for his feedback and advice in all aspects of this thesis. I honestly could not have asked for a better advisor and I am truly privileged to have had the opportunity to work under him. To my esteemed co-advisor Prof. Dr. Gilberto José de Moraes for all his constant support, professional orientation, and constructive comments over the years of my Ph.D. journey. I learned many things from him that reflected fruitfully in my academic career. To my precious undergraduate advisor Prof. Dr. Fabien C.C. Hountondji, for his excellent suggestions in drafting an article part of this thesis. To Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) - Finance Code 001 for giving me the scholarship during my PhD study. To Universidade Estadual Paulista “Júlio de Mesquita Filho”, School of Agricultural and Veterinarian Sciences of Jaboticabal (UNESP/FCAV), and the Department of Agricultural Sciences and Graduation Program in Agronomy (Agricultural Entomology), for the opportunity to perform my Ph.D. course. To the former and current Graduation Program in Agronomy (Agricultural Entomology) coordinators: Prof. Dr. Raphael de Campos Castilho, Prof. Dr. Guilherme Duarte Rossi, Prof. Dr. Ricardo Antonio Polanczyk for their assistance and contribution. To the professors of the Graduate Program in Agronomy (Agricultural Entomology), for the knowledge, which significantly contributed to my academic and personal formation. To Prof. Dr. Raphael de Campos Castilho and Prof. Dr. Arlindo Leal Boiça Junior, for their valuable participation and contribution during my Ph.D. qualifying examination. To Prof. Dr. Rogério Falleiros Carvalho, for his collaboration in conducting this work. To Prof. Dr. Tiago Gallina, Universidade Federal do Pampa, Uruguaiana campus, Rio Grande do Sul (Brazil), for valuable assistance in collection of Phytoseiulus longipes. To Prof. Dr. Wesley Augusto Conde Godoy and Dr. José Bruno Malaquias from the Insect Ecology Laboratory, Department of Entomology and Acarology, Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo (ESALQ/USP) for the assistance in the preparation of a video using the EthoVision XT software. To Institut National des Recherches Agricoles du Bénin (INRAB) for supplying the seeds of cultivated tomatoes used in this work. To Prof. Dr. André Luiz Lourenção of Instituto Agronômico (IAC) for supplying the seeds of South American tomato genotypes used in this work. To Wanderley Pintado Brasil for helping me with the soil sterilization every time this was necessary. To Ana Beatriz Piai Kapp, Bruno Rafael, Claudiane Martins da Rocha, Daiana Paixão Nogueira Silva, Gabriel, Monteiro, Hágabo Honorato, Maiara Alexandre, Jaqueline Della Vechia, Leilane Martins Lacerda, Matheus Cardoso de Castro, and Sidneia Terezinha Soares de Matos, undergraduate and graduate colleagues of Laboratory of Acarology, for their help and continuous companionship. To the employees of the Agricultural Production Sciences Department for their help throughout the great time I spent at UNESP/FCAV. To all who were not mentioned here but helped directly or indirectly the conduction of this work. Lastly and especially my gratitude goes to my wonderful family, my mom Béatrice, dad Martin, brothers Simon, David, Élie and Isaac, and sisters Agnès and Elisabeth for their patience when I was away from them over the past six years. Without their encouragement, support, and love, I would never have even thought to attempt this work, throughout my academic career. To all of you my muito obrigado!!! This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. i SUMMARY Page RESUMO................................................................................................................. vi ABSTRACT ........................................................................................................... viii LIST OF TABLES .................................................................................................... x LIST OF FIGURES ................................................................................................ xiv CHAPTER 1- General Considerations ................................................................. 1 Introduction ..................................................................................................... 1 2. Literature Review ........................................................................................ 5 2.1. Importance of tomato production ............................................................. 5 2.2. Mite pests in tomato production ............................................................... 6 2.3. Tetranychus evansi .................................................................................. 7 2.3.1. Geographical Distribution .................................................................... 7 2.3.2. Identification ........................................................................................ 7 2.3.3. Bioecological aspects .......................................................................... 8 2.3.4. Dispersion .......................................................................................... 10 2.3.5. Host Plants and Economic Importance .............................................. 10 2.3.6. Management of Tetranychus evansi .................................................. 11 2.3.6.1. Chemical control .......................................................................... 11 2.3.6.2. Host plant resistance control ....................................................... 13 2.3.6.3. Biological control ......................................................................... 15 2.3.6.3.1. Arthropod biocontrol agents .................................................. 16 2.3.6.3.2. Entomopathogenic fungi ....................................................... 17 2.3.6.4. Cultural practices ......................................................................... 18 2.3.7. Integrated pest management ............................................................. 19 ii 2.3.7.1. Combination of biological control and pest mites- resistant plants ................................................................................................................. 20 2.3.7.2. Combination of Biological control and chemical control .............. 21 2.4. References ............................................................................................. 22 CHAPTER 2- Bottom-up effects of breeding tomato genotypes on behavioral responses and performance of Tetranychus evansi population .................... 38 Abstract ................................................................................................................. 38 Introduction ................................................................................................... 39 Materials and Methods .................................................................................. 41 Selected tomato genotypes .......................................................................... 41 Quantification of types and trichome densities .............................................. 43 TRSM stock colony ....................................................................................... 43 Free-choice test ............................................................................................ 44 Effect of genotypes on TRSM walking ability ................................................ 46 Experimental procedure for evaluation of population performance ............... 46 Data analysis ................................................................................................ 47 Results .......................................................................................................... 49 Quantification of trichomes ........................................................................... 49 Settlement and oviposition ............................................................................ 51 Walking abilities ............................................................................................ 54 Duration of developmental stages, reproduction, and life table parameters . 55 Age - survival rate and fecundity of the specific stage .................................. 56 iii Cluster analysis ............................................................................................. 59 Discussion .................................................................................................... 61 ACKNOWLEDGMENTS ........................................................................................ 66 REFERENCES ...................................................................................................... 66 CHAPTER 3 - Effect of tomato genotypes with varying levels of susceptibility to Tetranychus evansi on performance and predation capacity of Phytoseiulus longipes................................................................................................................ 72 Abstract ................................................................................................................. 72 Introduction ................................................................................................... 73 Materials and Methods .................................................................................. 75 Studied genotypes ........................................................................................ 75 Tetranychus evansi stock colony .................................................................. 76 Phytoseiulus longipes stock colony ............................................................... 77 Experimental procedure ................................................................................ 77 Results .......................................................................................................... 80 Life stage durations, fecundity, sex ratio, and life table parameters.............. 80 Age- and stage-specific survival and fecundity rate ...................................... 82 Predation potential ........................................................................................ 84 Discussion .................................................................................................... 88 Acknowledgements ............................................................................................... 93 References ............................................................................................................ 93 iv CHAPTER 4 - Bioactivity of oxymatrine and azadirachtin against Tetranychus evansi (Acari: Tetranychidae) and their compatibility with the predator Phytoseiulus longipes (Acari: Phytoseiidae) on tomato.................................. 99 Abstract ................................................................................................................. 99 Introduction ................................................................................................. 100 Materials and Methods ................................................................................ 102 Mite rearing ................................................................................................. 102 Treatments .................................................................................................. 102 Experimental units for Tetranychus evansi ................................................. 104 Effect of recently applied treatments on Tetranychus evansi ...................... 104 Residual effect of biopesticides on Tetranychus evansi .............................. 105 Effect of recently applied treatments on Phytoseiulus longipes .................. 106 Data analysis .............................................................................................. 107 Results ........................................................................................................ 108 Discussion .................................................................................................. 115 Acknowledgments ............................................................................................... 119 References .......................................................................................................... 119 CHAPTER 5 - Risk assessment of ten commonly pesticides used in tomato cropping system on the predatory mite Phytoseiulus longipes (Acari: Phytoseiidae) ..................................................................................................... 125 Abstract ............................................................................................................... 125 Introduction ................................................................................................. 126 v 2. Materials and Methods ............................................................................ 129 2.1. Mites .................................................................................................... 129 2.2. Chemicals ............................................................................................ 130 2.3. Experimental units ............................................................................... 130 2.4. Topical exposure of Phytoseiulus longipes to the pesticides .............. 131 Eggs ............................................................................................................ 131 Adults .......................................................................................................... 132 2.5. Resiual effet and duration of the pesticides harmful to Phytoseiulus longipes ...................................................................................................... 133 2.6. Data analysis ....................................................................................... 135 3. Results .................................................................................................... 136 3.1. Topical exposure toxicity ...................................................................... 136 3.1.1. Lethal and sublethal effects on eggs ............................................... 136 3.1.2. Lethal and sublethal effects on adults ............................................. 141 3.2. Residual effects and duration of harmful activity of pesticides ............. 142 4. Discussion............................................................................................... 147 5. Conclusion .............................................................................................. 154 6. References.............................................................................................. 154 CHAPTER 6 – Final Regards ............................................................................ 165 vi GENÓTIPOS RESISTENTES, CONTROLE BIOLÓGICO E PESTICIDAS SELETIVOS PARA O MANEJO INTEGRADO DE Tetranychus evansi (ACARI: TETRANYCHIDAE) EM TOMATE RESUMO - O ácaro vermelho do tomateiro, Tetranychus evansi Baker & Pritchard (Acari: Tetranychidae), é uma praga invasora do tomateiro em vários países, com potencial de reduzir a produtividade em até 90% na África. Devido ao alto potencial biótico da praga, o manejo focado no uso de defensivos sintéticos muitas vezes não é eficiente ou insustentável ao longo do tempo, sendo necessária a sua integração com outros métodos de controle. Estudos anteriores encontraram em genótipos selvagens fonte expressiva de resistência (tricomas glandulares) que poderiam ser exploradas para aumentar o nível de resistência de variedades de interesse a esta praga. Além disso, Phytoseiulus longipes Evans (Phytoseiidae), encontrado na América do Sul, mostrou-se um promissor ácaro predador de T. evansi. No entanto, a integração deste ácaro predador em programas de MIP onde T. evansi é um problema sério requer conhecimento detalhado das interações com outras práticas de manejo. Dessa forma, objetivou-se com este trabalho estabelecer um sistema de manejo integrado para T. evansi com a aquisição de genótipos de tomateiro resistentes, biopesticides eficientes a T. evansi, um genótipo adequado que pudesse otimizar o desempenho do ácaro predador Phytoseiulus longipes Evans (Phytoseiidae) e com a definição de agrotóxicos seletivos comumente usado em tomateiro a esse predador. Os estudos foram conduzidos em condições de laboratório e semi-campo. As progênies F1, SPJ-10-2017 e SPJ-05-2018 obtidas cruzando o genótipo selvagem resistente [Solanum habrochaites, acesso PI 134417] com Solanum lycopersicum, cv TLCV15 [importante genótipo cultivado amplamente cultivado no Benin] herdaram significativos tricomas glandulares tipos I, IV e VI de seu pai resistente (PI 134417). As densidades de tricomas glandulares herdados pelos genótipos da progênie foram capazes de reduzir ou suprimir as infestações causadas por T. evansi. No entanto, o genótipo de progênie causou atrasos importantes no crescimento populacional e reduziu significativamente a sobrevivência e o potencial de predação de P. longipes. Os genótipos cultivados com maior número de tricomas não glandulares mostraram-se adequados para a implementação do programa IPM que visa otimizar o uso de P. longipes como agente de biocontrole. Os resultados demonstraram que o uso de biopesticidas à base de azadirachtin e oxymatrine apresentaram alta atividade contra T. evansi e pode ser uma importante alternativa para uso no manejo de T. evansi em substituição ou rotação com acaricidas sintéticos. Além disso, azadiractina mostrou- se mais segura ao ácaro predador tanto no controle biológico aumentativo quanto na conservação, enquanto a oximatrina mostrou-se adequada apenas para o controle biológico aumentativo se 10 dias for observado após aplicação. Os agrotóxicos comumente usados no sistema de cultivo do tomateiro como abamectina, propargite, imidacloprid e o fungo entomopatogênico Hirsutella thompsonii (Fischer) (Deuteromycetes) são mais compatíveis com o controle vii biológico aumentativo do que com a conservação se os prazos de segurança adequados forem respeitados antes da liberação. Os inseticidas piretróides (cipermetrina e deltametrina) e organofosforados (dimetoato, clorpirifós) não são compatíveis com o uso de P. longipes em programas de MIP. Esses resultados são importantes para o manejo sustentável dessa praga invasora e, ao mesmo tempo, fornecem diretrizes práticas que possibilitam uma melhor forma de uso de agrotóxicos em programas de MIP que visam conservar ou realizar liberações aumentativas do ácaro predador. Palavras-chave: ácaro vermelho do tomateiro, Manejo Integrado de Pragas, genótipo resistente, Phytoseiidae, potencial de predação, biopesticidas, impacto de agrotóxicos sobre predador viii RESISTANT GENOTYPES, BIOLOGICAL CONTROL AND SELECTIVE PESTICIDES FOR THE INTEGRATED MANAGEMENT OF TETRANYCHUS EVANSI (ACARI: TETRANYCHIDAE) ON TOMATO ABSTRACT - The tomato red spider mite, Tetranychus evansi Baker & Pritchard (Acari: Tetranychidae), is an invasive tomato pest in several countries, with the potential to reduce yield by up to 90% in Africa. Due to the high biotic potential of the pest, the management focused on the use of synthetic pesticides is often not efficient or unsustainable over time, requiring the integration with other control methods. Previous studies found in wild genotypes expressive source of resistance (glandular trichomes) that could be explored to increase resistance level of varieties of interest to this pest. Furthermore, Phytoseiulus longipes Evans (Phytoseiidae), found in South America proved to be a promising predatory mite of T. evansi. However, the incorporation of this predatory mite into IPM programs requires detailed knowledge of the interactions with other management practices. Within this context, the objective of the present study was to establish an integrated management system with the acquisition of tomato genotypes resistant to T. evansi, a suitable genotype that could optimize the performance of predatory mite P. longipes and with the definition of selective pesticides to this predator.The studies were conducted under laboratory and semi-field conditions. Our results indicated that the progenies F1, SPJ-10-2017 and SPJ-05-2018 obtained by crossing the wild-resistant genotype [Solanum habrochaites, Knapp e Spooner var glabratum access PI 134417] with Solanum lycopersicum L., cv. TLCV15 [cultivated genotype widely grown in Benin] have inherited significant glandular trichomes types I, IV and VI from their resistant parent (PI 134417). The densities of these glandular trichomes inherited by progeny genotypes were able to reduce supress the infestation caused by T. evansi. However, the bred progeny genotype SPJ-05-2018 caused important delays population growth and reduced significantly a survival, and the predation potential of P. longipes. The cultivated genotypes with many non-glandular trichomes proved to be more suitable for the implementation of IPM program that aim to optimize the use of P. longipes as biocontrol agent. The results showed that the use of azadirachtin- and oxymatrine based biopesticides had high activity against T. evansi and may be an important alternative in the management of the mite in replacement or rotation with synthetic acaricides. Azadirachtin proved to be the safest against the predatory mite toward both augmentative biological control and conservation whereas oxymatrine proved to be suitable only toward augmentative biological control 10 days after application. Other pesticides used in tomato cropping system such as abamectin, propargite, imidacloprid and the enthomopathogenic fungus Hirsutella thompsonii (Fischer) (Deuteromycetes) are more compatible with augmentative biological control than conservation if appropriate safety deadlines are respected before release. The insecticides belonging to pyrethroid (cypermethrin and deltamethrin) and organophosphate (dimethoate, chlorpyrifos) groups are not compatible with the use of P. longipes in IPM programs. These results are important to sustainably manage this invasive mite pest, and at the same time, provide ix practical guidelines to enable a better way of using pesticides in IPM programs that aim to conserve or increase the predatory mite P. longipes. Keywords: tomato red spider mite, Integrated Pest Management, resistant genotype, Phytoseiidae, predation potential, biopesticides, impact of pesticides on predator x LIST OF TABLES Page CHAPTER 2- Bottom-up effects of breeding tomato genotypes on behavioral responses and performance of Tetranychus evansi population……………... 38 Table 1. Mean for locomotion activities (± SE) of Tetranychus evansi within an observation period of 10 min, on leaflets of tomato parental (PI 134417 and TLCV15) and progeny (F1, SPJ-10-2017 and SPJ-05-2018) genotypes……. ...................................................................................................................... 54 Table 2. Duration (mean ± SE) of different life stages, pre-adult mortality, pre- oviposition period (APOP), total pre-oviposition (TPOP), longevity oviposition days, sex ratio, fecundity, and life table parameters (R0, r, λ, and T) of Tetranychus evansi on the parental (PI 134417 and TLCV15) and progeny (F1, SPJ-10-2017 and SPJ-05-2018) genotypes from interspecific crossing between PI 134417 and TLCV15. (Numbers in parentheses: n for the respective parameter). .................................................................................. 56 CHAPTER 3 - Effect of tomato genotypes with varying levels of susceptibility to Tetranychus evansi on performance and predation capacity of Phytoseiulus longipes................................................................................................................ 72 Table 1 Average duration (± SE), in days, and mortality rate (%) of Phytoseiulus longipes immature stages consuming Tetranychus evansi nymphal stages on three tomato genotypes (TLCV15, Tounvi and SPJ-05-2018)……………… . 81 Table 2. Duration (mean ± SE), in days, of the pre-oviposition period (APOP), total pre-oviposition (TPOP), longevity, oviposition (Od), sex ratio, total life xi span, fecundity, and life-table parameters of Phytoseiulus longipes consuming Tetranychus evansi nymphal stages on three tomato genotypes (TLCV15, Tounvi and SPJ-05-2018) ............................................................................. 82 Table 3. Averages (± SE) of total prey consumption for different life stages and consumption parameters of Phytoseiulus longipes consuming Tetranychus evansi nymphal stages reared on TLCV15, Tounvi, and SPJ-05-2018……… ...................................................................................................................... 88 CHAPTER 4 - Bioactivity of oxymatrine and azadirachtin against Tetranychus evansi (Acari: Tetranychidae) and their compatibility with the predator Phytoseiulus longipes (Acari: Phytoseiidae) on tomato……………………… . 99 Table 1. Description of biopesticides and standard control used in bioassays….. .............................................................................................. 103 Table 2. Ovicidal and larvicidal activities of commercial oxymatrine- and azadirachtin-based formulations (Azact and Azamax) on Tetranychus evansi 7 days after spraying. (n= 8 units per treatment)…………………………….. .. 109 Table 3. Mortality (%) of Tetranychus evansi larvae after increasing exposure time under different treatments (oxymatrine- and azadirachtin-based formulations Azact and Azamax; n= 8 units per treatment)………………. .. 109 Table 4. Mortality (%) of Tetranychus evansi protonymphs and deutonymphs after increasing exposure time under different treatments (Azact and Azamax are commercial azadirachtin-based formulations; n= 8 units per treatment)…… .................................................................................................................... 110 xii Table 5. Mortality (%) of Tetranychus evansi adult females after increasing exposure time under different treatments (oxymatrine- and azadirachtin-based formulations Azact and Azamax; n= 8 units per treatment)………………. .. 111 Table 6. Average number of eggs laid (± SE) per female of Tetranychus evansi (initial density of ten females per experimental unit) subjected to different treatments after increasing exposure time. ................................................. 112 Table 7. Lethal (adult mortality) and sublethal (fecundity and fertility) effects, reduction coefficient and IOBC/WPRS toxicity categories of Phytoseiulus longipes adults after 3days of exposure under different treatments (oxymatrine- as well as azadirachtin-based formulations Azact and Azamax)………….. 114 CHAPTER 5 - Risk assessment of ten commonly pesticides used in tomato cropping system on the predatory mite Phytoseiulus longipes (Acari: Phytoseiidae) ..................................................................................................... 124 Table 1. Means (±SE) duration (days) and survival (%) of immature stages of Phytoseiulus longipes when eggs were treated with pesticides…………….. .................................................................................................................... 137 Table 2. Lethal (corrected mortality of immature stage) and sublethal (total fecundity, fertility, and female and male longevities) effects, reduction coefficient and IOBC/WPRS toxicity categories of pesticides applied on eggs of Phytoseiulus longipes. ............................................................................ 140 Table 3. Mean (± SE) life-table parameters of Phytoseiulus longipes when eggs were treated with pesticides. ....................................................................... 141 xiii Table 4. Lethal (corrected adult mortality) and sublethal effects (total fecundity, fertility, and female and male longevities), reduction coefficient and IOBC class toxicity of pesticides applied on adult Phytoseiulus longipes……………… . 143 Table 5. Mean (±SE) of corrective mortality and reproductive parameters of adult Phytoseiulus longipes, reduction coefficient and IOBC class toxicity of pesticides applied after 72-h exposure to 4, 10, 20 and 31 DAA aged residues of pesticides under screen-house (26.7 ± 0.3o C, RH 59.05 ± 0.60%, light environment)…. .......................................................................................... 145 Table 6. Duration of the pesticides harmful to Phytoseiulus longipes…… .. 146 xiv LIST OF FIGURES Page CHAPTER 1- Geral Considerations ..................................................................... 1 Figure 1. Symptoms (a), ballooning (b) caused by Tetranychus evansi on tomato plants. Death of tomato plant caused by T. evansi (c) ........................................... 11 Figure 2. Female (a), nymphs (b) of Phytoseiulus longipes feeding on Tetranychus evansi eggs. (c) P. longipes female preying on T. evansi female. (d) Mating between male and female of P. longipes ............................................................................. 17 CHAPTER 2- Bottom-up effects of breeding tomato genotypes on behavioral responses and performance of Tetranychus evansi population .................... 38 Figure 1. Schematic representation of the experimental setups in different phases of this study. .......................................................................................................... 45 Figure 2. Average trichome densities (±SE) on the abaxial leaf surfaces of evaluated tomato genotypes of 35- day-old plants, for each trichome type and their combinations. ........................................................................................................ 50 Figure 3. Comparative box plot distribution of the numbers of adult females of Tetranychus evansi (a) or eggs laid by them (b) on leaflet discs of tomato plants, in a free-choice test under laboratory conditions, 24 and 48 h of mite release. ........ 52 Figure 4. Comparative box plot distribution of the number of adult females of Tetranychus evansi (a) or eggs laid by them (b) on tomato plants genotypes, in a free-choice test under greenhouse conditions 24 h of mite release. ..................... 53 Figure 5. Variation of survival rates and fecundity of Tetranychus evansi on different genotypes along life stages; (a) age-stage specific survival rates (sxj); (b) age- xv specific survival rate (lx), age-specific fecundity (mx) and age-stage-specific fecundity (fxj). ........................................................................................................................ 58 Figure 6. Dendrogram of different tomato genotypes based on behavioral responses and performance of Tetranychus evansi, density, and type trichomes parameters. .............................................................................................................................. 59 Fig. 7 Principal components analysis ordination diagram of preference and population performance parameters of Tetranychus evansi, density and types trichomes parameters on the parental genotypes (PI 134417and TLCV15), and progeny genotypes (F1, SPJ-10-2017 and SPJ-05-2018) from interspecific crossing between PI 134417 and TLCV15. ......................................................................... 60 CHAPTER 3- Effect of tomato genotypes with varying levels of susceptibility to Tetranychus evansi on performance and predation capacity of Phytoseiulus longipes................................................................................................................ 72 Figure 1. Age-stage survival rate (sxj) of Phytoseiulus longipes consuming Tetranychus evansi nymphal stages reared on different tomato genotypes (Tounvi, TLCV15, and SP-05-2018). ................................................................................... 83 Figure 2. Age-specific survival rates (lx) and age-specific fecundity (mx) of Phytoseiulus longipes consuming Tetranychus evansi nymphal stages reared on different tomato genotypes (Tounvi, TLCV15, and SP-05-2018). .......................... 85 Figure 3. Predation rate to age x and /or stage j. a Age-specific consumption rate (kx) and age-specific net consumption rate (qx) of Phytoseiulus longipes fed Tetranychus evansi nymphal stages reared on different tomato genotypes (Tounvi, TLCV15, and SP-05-2018). b Age-stage predation rate (Cxj) derived from an age- xvi stage, two-sex life table for P. longipes fed Tetranychus evansi nymphal stages reared on three tomato genotypes (Tounvi, TLCV15, and SP-05-2018) ............... 87 CHAPTER 4 - Bioactivity of oxymatrine and azadirachtin against Tetranychus evansi (Acari: Tetranychidae) and their compatibility with the predator Phytoseiulus longipes (Acari: Phytoseiidae) on tomato.................................. 99 Figure 1. A- C. Mortality (%) of nymphs of Tetranychus evansi at 1, 3, 5, and 7 days after initiation of evaluation (DAIE) on leaflets taken from 1, 5, and 10 days tomato plants after application(DAA) in a screen-house [n= 8]. D. Cumulative mortality of nymphs of Tetranychus evansi at 7 days of exposure on leaflets taken respectively from 1, 5 and 10 days tomato plants after application(DAA) in a screen-house.[n= 8]. ........................................................................................................................ 113 CHAPTER 5 - Risk assessment of ten commonly pesticides used in tomato cropping system on the predatory mite Phytoseiulus longipes (Acari: Phytoseiidae) ..................................................................................................... 124 Figure1. Age-specific survival rates (lx), age-specific fecundity (mx) of Phytoseiulus longipes when eggs were treated with pesticides. The lines in red in different treatments indicate day of P. longipes adult emergence ..................................... 139 1 CHAPTER 1- General Considerations Introduction Tomato (Solanum lycopersicum L.) is one of the most widely cultivated and consumed vegetable crops worldwide (Kimura and Sinha, 2008; Sibomana et al., 2016). In sub-Saharan Africa, this crop is commonly planted by small-scale farmers and represents an important source of income (Arah et al., 2015; Sibomana et al., 2016). However, efforts of farmers to increase tomato production often face various problems in the field, such as interference from intruder organisms (pests and diseases) that substantially affect tomato production (Arah et al., 2015; Wakil et al., 2018; Abera et al., 2020). Among pests, the spider mites should be highlighted, as some species are key pests of this crop, requiring considerable investments in their control every year in an attempt to prevent yield losses (Brust and Gotoh, 2018). In this group, Tetranychus evansi Baker & Pritchard (Acari: Tetranychidae), also known as tomato red spider mite, has been considered as one of the most devastating pests for tomato and other solanaceous plants in the world, mainly in Africa (Navajas et al., 2013; Azandémè-Hounmalon et al., 2015; Savi et al., 2019a; Djossou et al., 2020). This mite is considered native to South America, probably from the northeastern part of Brazil, but over the past decades, it has gradually invaded and colonized several tropical and subtropical habitats worldwide (Navajas et al., 2013). Importantly, in most invaded regions, T. evansi is a recurrent pest responsible for massive crop losses and significant economic damages, especially to small-scale farmers (Ferragut et al., 2013; Azandémè-Hounmalon et al., 2015; Knegt et al., 2020). It is presently found in 44 countries in Africa, the Americas, Europe, and Asia (Migeon and Dorkeld, 2006-2019; Fan et al., 2021). The rapidly changing climate, which will result in higher average temperature and lower rainfall in large parts of the world, probably facilitates the ongoing expansion of T. evansi into new territories, thus putting progressively larger areas at risk (Meynard et al., 2013; Ximénez-Embún et al., 2016; Migeon and Dorkeld, 2006-2019). Tetranychus evansi pierces cell walls to extract their contents. This feeding activity causes chlorotic spots, reducing the 2 photosynthetic capacity and often leading to leaf fall (de Moraes and Flechtmann, 2008; Bensoussan et al., 2018). In the absence of effective management methods, mite-feeding activity can cause yield losses ranging from 56 to 100%, mostly in African countries (Sarr et al., 2002; Boubou et al., 2010; Azandémè-Hounmalon et al., 2015). In general, spraying acaricides or insecticides with acaricidal properties is the major management strategy for controlling T. evansi (Blair, 1989; Toroitich et al., 2014; Gotoh et al., 2011; Azandémè-Hounmalon et al., 2015; Bagaram, 2016). However, the rapid development and high reproductive capacity (Qureshi et al., 1969; de Moraes and Flechtmann, 2008) allow T. evansi to reach high population levels, leading producers to conduct several annual pesticide applications for its control (Savi et al., 2019a). Unfortunately, this excessive usage of pesticides usually becomes untenable in the long run because it leads inevitably to the development of resistance, negatively impacting the environment as well as human and livestock health, besides increasing crop production costs (Blair, 1989; Nyoni et al., 2011; Azandémè-Hounmalon et al., 2015). Therefore, the sustainable management of this invasive mite requires the development of ecologically friendly crop protection methods that suit the needs of small farmers. Within this context, the use of acaricides should be subordinated or integrated with other control methods, such as biological control and the use of resistant genotypes. The use of selective acaricides has also gained more credibility in the last decades (Hoy, 2011; Stenberg, 2017; Stout et al., 2018; Duso et al., 2020). In the search for such methods, the resistance of five cultivated tomatoes widely grown by smallholder farmers in western Africa (Kekefo, TOML4, Akikon, Tounvi, and TLCV15) and two wild relatives [Solanum habrochaites Knapp & Spooner (accessions PI 134417 and PI 134418) and Solanum pennellii Correll (accession LA-716)] have been evaluated in a previous study. Unfortunately, the tomato varieties grown in Africa and other commercial tomato cultivars have proved to be susceptible to T. evansi. In contrast, the wild tomato genotypes have been experimentally shown highly resistant to T. evansi (Savi et al., 2019a, b). This difference has been attributed to the presence of a greater number of glandular 3 trichomes and their toxic compounds (as acyl-sugars, methyl ketones, and terpenoids) on wild genotypes, but their absence of great reduction on cultivated tomatoes (Resende et al., 2008; Bleeker et al., 2012; Lucini et al., 2015). These structures proved to entangle or kill phytophagous arthropods through the sticky or toxic exudates that the trichomes produce (Kang et al., 2010; Zhang et al., 2020). They can also serve as repellent barriers to small herbivores, preventing them from feeding freely on the surface of a plant (Zhang et al., 2020). Hence, the introgression of glandular trichomes from wild tomato relatives to cultivated tomatoes, through interspecific crossings, could conceivably be one of the ways to increase the resistance degree of cultivars of interest against T. evansi and consequently adapted to sustainable production systems (Savi et al., 2019b). This could also help small- scale farmers who are not well resourced to purchase effective acaricides. That accounts for the first goal of this dissertation. Biological control using natural enemies is also a major component of any integrated pest management (IPM) program (Van Driesche et al., 2008; Almarinez et al., 2020). In the case of spider mites, predatory mites of the family Phytoseiidae are the most commonly studied and important group of natural enemies considered for their control (McMurtry et al., 2013). Species of this family have been commercialized to suppress pest mite populations (McMurtry et al., 2013). Their feeding preference for phytophagous mites, short life cycles, and feasible large- scale production make them good candidates for pest control (Abad-Moyano et al., 2009). The phytoseiid mite Phytoseiulus longipes Evans (Acari: Phytoseiidae) found naturally in association with T. evansi in the extreme south of Brazil and northern Argentina proved to be the only promising predator for red spider mite control (Furtado et al., 2007; Silva et al., 2010; Ferreiro et al., 2011). This predatory mite has the potential to control other Tetranychus species, given its adaptation to the type I-a lifestyle of McMurtry et al. (2013). However, the incorporation of predatory mites into IPM programs requires detailed knowledge and understanding of the interactions of these mites with other crop management practices (Fountain and Meed, 2015). The defensive traits that crops exhibit to protect themselves from damage caused by pests and disease can 4 also strongly influence the survival and efficacy of their predators. In the case of tomato, several studies have demonstrated that the performance of most phytoseiid mites tends to be lower compared to other crops (Koller et al., 2007; Sato et al., 2011; Davidson et al., 2016; Paspati et al., 2021). This fact has been attributed to the impact of tomato defenses mediated by the glandular trichomes and their exudates, increasing phytoseiid mortality or phytoseiid prey-searching efficacy if non-glandular and glandular trichomes are above a certain threshold (Castagnoli et al., 1999; Koller et al., 2007; Sato et al., 2011; Paspati et al., 2021). Tomato genotypes can vary highly in trichome density and such variation could influence differently the performance of phytoseiid mites. However, although tomato has been found to affect predatory mites more than other crops, studies about this subject are scarce. Thus, the effect of tomato genotypes with varying levels of susceptibility or resistance to T. evansi on P. longipes should be investigated. Such knowledge will be fundamental in the choice of tomato genotypes to optimize the use of this phytoseiid mite as a biocontrol agent in the integrated management program of T. evansi. Accordingly, this was the second goal of this dissertation. In the development of Integrated Pest Management Programs, it is also important for farmers to have available pesticides minimally harmful to the natural enemies, or that the effect of these two control measures taken together is greater than the sum of their separate effect (Schmidt-Jeffris and Beers, 2020; Bilbo and Walgenbach, 2020). Several studies on non-target effects on key phytoseiid species have been conducted to address this need. However, knowledge of pesticides non- target effects on P. longipes is still scarce. Therefore, investigations should be conducted to determine which pesticides are most selective against this predatory mite in the tomato cropping system, as pest control practices adopted by most Western African tomato producers are dominated by the intensive use of pesticides, with no attention on their possible effect on natural enemies of T. evansi. Thus, this dissertation intends to establish an integrated management system for T. evansi, with the acquisition of tomato genotypes resistant to T. evansi, a suitable genotype that could optimize the performance of predatory mite P. longipes, and with the definition of pesticides with lower risk to this predator. The thesis is 5 organized as follows. Chapter 2 explores the bottom-up effects of progeny genotypes from interspecific crossings of wild and cultivated tomatoes on the behavioral responses and demographic parameters of T. evansi to increase resistance degree of a cultivar of interest in the Republic of Benin (West Africa) cropping system against T. evansi. Chapter 3 compares P. longipes population performance and predation capacity on tomato genotypes with different susceptibility levels to T. evansi, to identify the genotype, which should be included in the envisioned IPM program to optimize P. longipes as a biocontrol agent. Chapter 4 evaluates the effectiveness of two bio-acaricides (azadirachtin- and oxymatrine- based formulations), which are labeled as selective for bio-control agents for controlling T. evansi on tomato crop, explores also their synergistic effect with the predatory mite P. longipes to support effective integrated management of T. evansi. Chapter 5 assesses the short- and long-term effects of direct exposure as well as the persistence of residual activity of ten pesticides commonly used in the Western African tomato cropping system against P. longipes to screen those are suitable toward conservation and/ or preservation of this predatory mite in the field. Chapter 6 presents a summary of overall empirical findings, conclusion, and suggestions resulting from this thesis. 2. Literature Review 2.1. Importance of tomato production Tomato (S. lycopersicum L.) is one of the most popular horticultural commodities grown in practically every country of the world in outdoor fields, greenhouses, and screen houses (Adenuga et al., 2013). In 2019, world tomato production was estimated at more than 180.7 million tons produced on 5.3 million hectares generating $ 86.06 billion annually (FAO, 2019). Together, Asia and America account for 75% of the world’s total production. China is the world´s top tomato grower with 62.86 million tons, followed by India with 19 million tons (FAO, 2019). Turkey and USA are the other major tomato producing countries with an estimated above 10 million tons (FAO, 2019) 6 In Africa, the total tomato production for 2019 was estimated to be about 16.125 million tons with Egypt leading the continent with 6.7518 million tons. In the Western African countries, Nigeria recorded the highest production level, with 3.8 million tons produced from a total area of about 264,000 hectares, while the estimated tomato production in the Republic of Benin stood at 274.700 tons produced on 37.648 hectares giving an average of 7.2 tons per hectare (FAO, 2019). Tomato is an important component of the daily diet used as fresh or as processed products in preparation of different delicacies (Adenunga et al., 2013). This is because tomato is rich in vitamins, minerals, sugars, essential amino acids, iron, dietary fibers, and phosphorus (Arah et al., 2015). Moreover, it contains higher amounts of lycopene, a type of carotenoid with anti-oxidant properties (Arab and Steck, 2000) which is beneficial in reducing the incidence of some chronic diseases, like cancer and many other cardiovascular disorders (Miller et al., 2002; Arah et al., 2015). Tomato production can serve as a source of income for most rural and peri- urban producers in most developing countries (Çetin and Vadar, 2008), representing more than 51% of the total production of vegetable crops in the Republic of Benin (Sikirou et al., 2015). In that county, this crop is cultivated continuously throughout the year because apart from the most important rainy season that normally spans between April and July in the southern part of the country, and May to October in the northern part, there is a secondary rainy season between September and November, mainly in the south (Brassica, 2019). The crop is also grown in the so-called off- season period, between October to January in the north and between November to February in the south (Brasica, 2019). Despite the importance of the tomato crop, production is still insufficient to meet the national demand in most West African countries, requiring importation from neighboring countries. 2.2. Mite pests in tomato production Tomato production is severely constrained by diseases and several insect and mite pests (Wakil et al., 2018). The mites constitute a diverse group of the subclass Acari, of the class Arachnidae, belonging to the subphylum Chelicerata of 7 the phylum Arthropoda. Among the arachnids, Acari is the only group containing species adapted to feeding on plants (Jeppson et al., 1975). Plant feeding mites play an important role as agricultural pests of fruit, vegetable, forage, ornamental, and other crops (Hoy et al., 2011; Tehri, 2014). Among mite pests, Tetranychidae, also known as spider mites, standing out as the main group of plant-feeding mites, for the number of species and the number of host plants attacked by them around the world (Helle and Sabelis, 1985). About 1321 species belonging to over 70 genera are known to feed on 3917 plants (Migeon and Dorkeld, 2006-2021). The major spider mite species in tomato production include the two-spotted spider mite, Tetanychus urticae Koch (Acari: Tetranychidae) and red spider mite T. evansi (Moraes and Flechtmann, 2008; Brust and Gotoh, 2018). The broad mite Polyphagotarsonemus latus (Banks) (Acari: Tarsonemidae) and the tomato russet mite Aculops lycopersici (Massee) (Acari: Eriophyidae), are other pest mites of great importance in tomato production (Brust and Gotoh, 2018). 2.3. Tetranychus evansi 2.3.1. Geographical Distribution Tetranychus evansi was first recorded in northeastern Brazil under the name of Tetranychus marianae McGregor (Silva, 1954), but correct identification was described in 1960 from Mauritius (Baker and Pritchard, 1960). It was later found in several other countries, reaching more recently countries in Sub-Saharan Africa, Mediterranean area and Asia (Silva 1954; Navajas et al., 2013; Migeon and Dorkeld, 2006–2019). It has been reported from 45 countries worldwide. It has been considered that the climatic changes facilitated its invasion to new territories [see http://www.ensam.inra.fr/CBGP/spmweb/ (Migeon and Dorkeld, 2006-2021 Fan et al. 2021) for detailed coverage of its distribution]. 2.3.2. Identification 8 Tetranychus evansi belongs to the family Tetranychidae, of the superfamily Tetranychoidae, of the suborder Prostigmata, of the order Trombidiformes, of the subclass Acari, of the class Arachnida, of the subphylum Chelicerata of the phylum Arthropoda. The eggs of this species are typically round, with about 120 µm in diameter, pale orange soon after oviposition but rusty close to larval hatching. The larvae have three pairs of legs and are 150 µm in length, pale green or pink in color (Helle and Sabelis, 1985). The protonymph and the deutonymph have four pairs of legs and are respectively about 310 and 350 µm in length. Their color ranges from orange to brick red or dark red. As in other tetranychids, sexes are dimorphic, the males being rather triangular and the females broadly oval. Males are about half as long as females, the latter about 500 µm long. The color of females ranges from light orange to deep reddish-orange or brown with an indistinct dark blotch on each side of the body, whereas males are yellow-orange-colored, with pale legs. The shape of the structure on the palpal tarsus used for spinning silk and the shape of the male aedeagus (terminal part of a male copulatory organ) and the chaetotaxy of the legs are important characters to separate the adults from other Tetranychus species (Baker and Pritchard, 1960; de Moraes et al., 1987). Each empodium (structure between the two claws at the end of the tarsi) of the females ends in three pairs of filaments overlaid by a tiny mediodorsal spur. All four proximal tactile setae on female tarsus I are nearly in line with the proximal set of duplex setae. The aedeagus is upturned distally and the distal tip (head) is inverted shoe- shaped (Baker and Pritchard, 1960). 2.3.3. Bioecological aspects The life cycle of T. evansi includes the same developmental stages as all other tetranychid species (egg, larva, protonymph, deutonymph and adult male and female). There is always an inactive (quiescent) phase between each active stage, referred to as protochrysalis, deutochrysalis and teliochrysalis, respectively. The life cycle of T. evansi has been studied by several authors (de Moraes and McMurtry, 1987; Bonato, 1999, Gotoh et al., 2010; Murungi et al., 2010; Zriki et al., 2013; Savi https://link.springer.com/article/10.1007/s10493-019-00364-6#ref-CR16 https://link.springer.com/article/10.1007/s10493-019-00364-6#ref-CR6 https://link.springer.com/article/10.1007/s10493-019-00364-6#ref-CR21 https://link.springer.com/article/10.1007/s10493-019-00364-6#ref-CR32 9 et al., 2019b; Djossou et al., 2020). These authors observed that the population growth parameters of T. evansi such as developmental rate, survival, reproduction, and longevity vary in response to changes in temperature, relative humidity and host plant species. The development is favored by hot and dry conditions (minimum temperature 10°C; optimum temperature 34°C). Tetranychus evansi full life cycle ranges from 41.0 to 45.1days at 15°C to 5.5–6.5 days at 40°C, and 9.7–10.5 days at 25°C (de Moraes and McMurtry, 1987; Bonato, 1999, Gotoh et al., 2010; Murungi et al., 2010; Zriki et al., 2013; Savi et al., 2019b; Djossou et al., 2020). Males develop slightly more rapidly than females. Reproduction can be sexual or by arrhenotoky parthenogenesis (Sabelis, 1985). When the reproduction is sexual, the mites mate, the male inserting its aedeagus into the female to deposit sperm by bending the tip of its idiosoma up. Mating lasts 30–90 seconds, with an average of 75 seconds, occurring several times along the life of the female (Qureshi et al., 1969; Navajas et al., 2013). As in other tetranychids, a male will remain over a deutonymph waiting for adult emergence, mating occurring soon after that. Unfertilized females lay haploid eggs, which produce only males; fertilized females produces haploid and diploid eggs, with a predominance of males offspring early and late in the period of oviposition. The sex ratio of progeny produced by mated females is usually three diploid females to one haploid male (Qureshi et al.,1969; Moraes et al., 1987). Total fecundity also varies with environmental conditions, reaching up to 49.71-243 at 25 oC (Moraes and McMurtry,1987; Gotoh et al., 2010; Savi et al., 2019b). Tetranychus evansi prefers to live on the lower side of the leaves, but it can also occupy the upper side when the population is too high (de Moraes and Flechtmann, 2008; Navajas et al., 2013). The oviposition site seems to reduce the effect of high temperature, rainfall, and pesticide sprays, thus making control difficult (Helle and Sabelis, 1985). In addition, the habitat preference for the underside of leaves is difficult for the initial detection of mite infestation, thus providing an appropriate time for increasing its population (de Moraes and Flechtmann, 2008). In tropical and subtropical areas, they may remain active year-round (Navajas et al., 2013). The term spider mite highlights the ability of the tetranychid mites of the https://link.springer.com/article/10.1007/s10493-019-00364-6#ref-CR16 https://link.springer.com/article/10.1007/s10493-019-00364-6#ref-CR6 https://link.springer.com/article/10.1007/s10493-019-00364-6#ref-CR21 https://link.springer.com/article/10.1007/s10493-019-00364-6#ref-CR32 https://link.springer.com/article/10.1007/s10493-019-00364-6#ref-CR50 https://link.springer.com/article/10.1007/s10493-012-9590-5#ref-CR74 https://link.springer.com/article/10.1007/s10493-012-9590-5#ref-CR74 https://link.springer.com/article/10.1007/s10493-019-00364-6#ref-CR16 https://link.springer.com/article/10.1007/s10493-019-00364-6#ref-CR21 10 subfamily Tetranychinae to produce a variable amount of webbing (Helle and Sabelis, 1985). Tetranychus species produce profuse webbing, but T. evansi is aoutstanding in this regard (de Moraes and McMurtry, 1987). 2.3.4. Dispersion When the plant is damaged, resulting in an unsuitable food supply, mites tend to disperse (Kennedy and Smitley, 1985; Pralavorio et al., 1989; Kungu et al., 2020), usually aggregating on the uppermost parts of the plants (Kungu et al., 2020). Spider mites may disperse individually by walking from one plant to another, or aerially by positioning their bodies in such a way as to catch the wind (de Moraes and Flechtmann, 2008; Santos et al., 2020). Under extreme conditions (overcrowding coinciding with food depletion), individuals gather at the plant apex to form a ball made by mites and silk threads (Gerson, 1985; Kungu et al., 2020). This phenomenon is called ballooning. Once formed, the balls are not firmly attached to the apex of the plant. In the field, the wind or a passing animal would be sufficient for dispersing individuals in that ball (Kennedy and Smitley, 1985; de Moraes and Flechtmann, 2008, Hoy et al., 2011). 2.3.5. Host Plants and Economic Importance Just like every spider mite, T. evansi is cell content-feeders, piercing plant parenchyma cells with their stylets, sucking up the contents, and leaving behind empty cells that are visible as white feeding scars (Bensoussan et al., 2016). Damage first appears as stipples that later result in a silvery or yellowish appearance to the leaves, thereby inducing enormous yield losses and even plant death (Savi et al., 2019b; Djossou et al., 2020). Tetranychus evansi feeds preferentially on solanaceous plants including cultivated crops such as S. lycopersicum, tobacco (Nicotiana tabacum L.), potato (Solanum tuberosum L.), and eggplant (Solanum melongena L.) (Navajas et al., 2013; Migeon and Dorkeld, 2006-2019). Although it has also been reported associated with 136 host plants of 36 other families (Migeon and Dorkeld, 2006–2021), high population levels have only been encountered a few https://onlinelibrary.wiley.com/doi/full/10.1002/ece3.6204#ece36204-bib-0013 11 times on the Cucurbitaceae and Fabaceae (Navajas et al., 2013; Migeon and Dorkeld, 2006-2021). In Brazil, the red spider mite is not a serious pest, probably for being this its native habitat. However, this pest mite causes severe losses sometimes reaching 100% on cultivated tomatoes (Figure 1) in invaded areas mostly in African countries due to favorable climate conditions (Saunyama and Knapp, 2003; Azandémè-Hounmalon et al., 2015). It also disrupts the community composition of T. urticae and other indigenous spider mite species becoming the dominant species in invaded areas mostly in African countries (Ferragut et al., 2013; Azandémè-Hounmalon et al., 2015). Figure 1. Symptoms (a), ballooning (b) caused by Tetranychus evansi on tomato plants. Death of tomato plant caused by T. evansi (c) 2.3.6. Management of Tetranychus evansi 2.3.6.1. Chemical control Historically, chemical control is the major adopted practice in the management of T. evansi, as the discovery of other control strategies such as natural (a) (b) (c) https://link.springer.com/article/10.1007/s10493-008-9229-8#ref-CR42 https://link.springer.com/article/10.1007/s10493-019-00364-6#ref-CR39 https://link.springer.com/article/10.1007/s10493-019-00364-6#ref-CR3 12 enemies and plant resistance has been slow (Blair, 1989; Toroitich et al., 2014; Azandémè-Hounmalon et al., 2015; Bagaram, 2016). The older synthetic pesticides have a long history of use against T. evansi. For this reason, it is not surprising to find high resistance ratios of this mite to these pesticides. Early researches on effective pesticides for controlling red spider mite in Zimbabwe were conducted in the 1990s with 57 pesticides from a range of chemical groups under laboratory conditions (Blair, 1989). In that study, T. evansi was found to be tolerant to some organophosphates, such as thiophosphate. However, chemicals such as binapacryl, cyhexatin, and dicofol, evaluated in that study are no longer used in some countries because of their toxicity to humans and the environment. Similarly, the survey conducted by Azandémè-Hounmalon et al. (2015) in the Republic of Benin revealed that older broad-spectrum insecticides such as organophosphates and pyrethroids used singly or in tandem by farmers in vegetable fields have not proved to be effective for controlling T. evansi. In Kenya, Toriotich et al. (2014) also indicated that the organophospate dimethoate should not be recommended in the management of T. evansi, but instead, suggesting that specific acaricides, such as propargite and abamectin, could produce high reductions in populations of T. evansi when applied with adequate application methods. Toroitich (2006) evaluated the effect of bifenthrin, lambda-cyhalothrin, dimethoate and profenofos + cypermethrin against T. evansi in the laboratory, but only bifenthrin and profenofos + cypermethrin proved to be effective. Gotoh et al. (2011) examined the efficacy of acaricides recently developed in the management of T. evansi strains from Brazil, France, Kenya, Spain, Canary Island, Taiwan and Japan (Kagoshima, Osaka, and Tokyo). From 11 tested acaricides, bifenazate, cyenopyrafen, milbemectin, spirodiclofen and tebufenpyrad proved to be highly toxic to this mite. The authors suggested that these new products could be incorporated into acaricide rotations taking into consideration their modes of action. Four strains used by Nyoni et al. (2011) were collected from Malawi and France. The LC50 values of four chemicals to adult females were variable. Only abamectin was considered to be effective to all four strains tested (Nyoni et al., 2011). For bifenthrin, the LC50 values exceeded the recommended concentration in 13 all four strains tested, and the LC50 values of two Malawian strains (1858–3560mg/L) were 20 to 39-fold higher than those of the two French strains (92.0–134.6mg/L). For chlorpyriphos and fenpyroximate, LC50 values were similar among the four strains (Nyoni et al., 2011). Some plant-based products such as neem (from Azadirachta indica A. Jussie) have been evaluated in the management of spider mites, including T. evansi. Soto et al. (2010) determined mortality of T. evansi females on tomato above 95% with Natuneem Agrícola® (Natural Rural, Araraquara, São Paulo, Brazil) and Organic Neem® (Dalquim Indústria e Comércio Ltda, Itajai, Santa Catarina, Brazil) (39.1 and 30.4 mg a.i. L-1). In contrast, Santos et al. (2017) observed lower efficacy (5-15% mortality) of still other azadirachtin formulations (Organic® and Pironim®, Agroterra Insumos Agrotecnologia, São José do Rio Preto, São Paulo, Brazil) at concentrations of 2, 4, 6, 8, and 10% against T. evansi females. The use of acaricide-treated nets, as traps to control phytophagous mites has been evaluated (Pralavorio et al., 1989; Martin et al., 2010). This technique has been used for controlling the broad mite, Polyphagotarsonemus latus (Banks), given its preference to the top leaves of plants, but it was hypothesized that it could also be used for the control of T. evansi, as this mite collectively migrates upwards towards the plant apex due to population pressure (Azandémè-Hounmalon et al. 2014; Kungu et al., 2020). While preventing the presence of acaricide residues on the plant and the environmental contamination, this technique would also lower mite population by preventing inter-plant dispersal by walking or aerially (Kungu et al., 2020). 2.3.6.2. Host plant resistance control The concerns about the development of resistance of T. evansi to synthetic acaricides, the limited availability and high costs of effective acaricides, and worker safety issues have motivated the identification of novel, appropriate replacements for plant protection with fewer adverse impacts (Savi et al., 2019a, b). The cultivation of arthropod-resistant plants has been proposed as one of the main alternatives to 14 broad-spectrum acaricide use in pest control. The economic advantages that arthropod-resistant cultivars offer are genetically incorporated arthropod control for the cost of the seed alone (Smith, 2005). Antixenosis (non-preference), antibiosis, and tolerance have been reported to be the three resistance categories through which plants defend themselves against attacks by herbivores, including pest mites (Maluf et al., 2010; Lucini et al., 2015; Savi et al., 2019b). Antixenosis refers to characteristics of the plant that prevent or reduce colonization by the pest. In other words, antixenosis cause adverse effects on mite behavior (turning the prospective host plant unattractive for feeding and reproduction). Antibiosis refers to characteristics of the plant that negatively affect its life cycle (development, reproduction, and survivorship of the pest), considered to be the most important category for mite management (Maluf et al., 2010; Lucini et al., 2015; Savi et al., 2019a,b). Tolerance refers to characteristics of the plant that enable them to withstand or recover from herbivore damage (Smith, 2005). In the case of T. evansi, researchers have focused mainly on the two former resistance categories. Results obtained by these researchers showed that cultivated tomato (S. lycopersicum) genotypes are usually susceptible to T. evansi (Silva et al., 1992; Resende et al., 2008; Murungi et al., 2009; Onyambus et al., 2012; Musa et al., 2016; Savi et al., 2019; Djossou et al., 2020). Most plant resistance traits in relation to spider mites have been found in accessions of wild tomato relatives, particularly S. habrochaites Knapp and Spooner, S. pennellii Correll, S. cheesmaniae (L. Riley) Fosberg, and S. galapagense S. C. Darwin and Peralta (Silva et al., 1992; Resende et al., 2008; Murungi, et al., 2009; Onyambus et al., 2011; Lucini et al., 2015, Rakha et al., 2017; Savi et al., 2019a,b). Leaf trichomes and the compounds produced by them have been considered to be the most important factor associated with the resistance mechanism of tomato genotypes (Simmons and Gurr, 2005; Rezende et al. 2008; Maluf et al., 2010; Rakha et al., 2017). Seven types of trichomes have been identified on tomato plants, grouped as glandular (types I, IV, VI, and VII) and non-glandular (types II, III, and V) (Luckwill, 1943; Simmons and Gurr, 2005). The glands of type I, IV, and VI on tomato 15 leaves play key anti-herbivory roles via chemical secretions (Kang et al., 2010; Zhang et al., 2020). They can also serve as repellent barriers to small herbivores and prevent them from feeding freely on the surface of a plant due to the high viscosity of allelochemical secretions (Simmons and Gurr, 2005; Zhang et al., 2020). Non-glandular trichomes may act as physical barriers, hampering micro-arthropods movement on the leaf surface when large and present in high densities (Baur et al., 1991; Aragão et al., 2000; Simmons and Gurr, 2005). Leaves of cultivated tomatoes tend to have copious non-glandular whereas leaves of wild tomato accessions have usually abundant glandular trichomes (types I, IV, and VI) (Zhang et al., 2020). Three main chemical classes that have been identified in association with glandular trichomes are methyl-ketones (notably 2- tridecanone; Gonlçalves et al., 1998), sesquiterpenes (notably zingiberene; De Azevedo et al., 2003; Bleeker et al., 2012), and acyl sugars (Resende et al., 2008; Lucini et al., 2015). The former two are abundant in the wild tomato S. habrochaites and found in high concentrations in the glandular trichomes of types IV and VI, whereas the latter is present in high concentrations in type IV glandular trichomes of S. pennellii, S. cheesmaniae, and S. galapagense (Rahka et al., 2017). The high defensive traits mediated by glandular trichomes and toxic compounds found on wild tomato relatives have been used to increase the level of resistance against mite pests, including T. evansi, in several cultivated tomatoes, through interspecific crosses (Rezende et al. 2008; Lucini et al., 2015; Maciel et al., 2018). The resistance level revealed by most of these interspecific hybrids was demonstrated to be generally comparable to that of wild tomato relatives (Resende et al. 2008; Alba et al., 2008; Lucini et al., 2015; Maciel et al., 2018; de Oliveira et al., 2018; AL-Bayati, 2019). This can constitute an important avenue to be further explored in an attempt to mitigate the use of synthetic pesticides. 2.3.6.3. Biological control Biological control can be considered a powerful tool and one of the most important measures of pest control, providing environmentally safe and sustainable plant protection (Van Driesche et al., 2008; Almarinez et al., 2020). Arthropod 16 biocontrol agents and microbial pathogens have been successfully used in agricultural systems for many years (Van Driesche et al., 2008; Wang et al., 2014). 2.3.6.3.1. Arthropod biocontrol agents Predatory mites of the family Phytoseiidae are important biocontrol agents of a variety of crop pests and their presence can negate the need for application of other control methods (McMurty et al., 2013; Fountain and Medd, 2015). The most common targets of predatory mite treatments are pest mites of the families Tetranychidae, Tarsonemidae, and Eriophyiidae (Gerson and Weintraub 2007; McMurty et al., 2013). However, predatory mites are also associated with the suppression of other small arthropod populations, including thrips (Thysanoptera: Thripidae) and whiteflies (Hemiptera: Aleyrodidae) (McMurty et al., 2013). According to Demite et al. (2021), Phytoseiidae contained 2,522 described valid species, distributed in 91 genera and three subfamilies, Amblyseiinae, Phytoseiinae, and Typhlodrominae. Among the phytoseiids, Phytoseiulus persimilis Athias-Henriot and Neoseiulus californicus McGregor (Acari: Phytoseiidae) are some of the species that have been most extensively used for the protection of many crops against tetranychid pests worldwide (McMurty et al., 2013). These species proved to be particularly effective for controlling T. urticae (Gerson et al., 2003). However, attempts to control T. evansi using those phytoseiids have been unsuccessful (de Moraes and McMurtry, 1986; Escudero and Ferragut, 2005, Koller et al., 2007). The authors have observed that none of the tested predators could feed and grow properly on T. evansi. Moraes and McMurtry (1986) suggested that T. evansi contained a depressant, which hampered phytoseiids from consuming their eggs. The fact that T. evansi has become a serious threat to Solanaceae crops in Africa and Europe, expanding its invasion in the 2000s (Migeon et al., 2009; Migeon and Dorkeld, 2019) has given new impetus to the search for effective natural enemies of this mite. Over that prospection, South America, mostly Brazil and Argentine were prioritized for being close to the region of origin of that pest (Rosa et https://link.springer.com/article/10.1007/s12600-015-0485-y#ref-CR13 https://onlinelibrary.wiley.com/doi/full/10.1111/j.1570-7458.2007.00625.x?casa_token=H5Z_gz96kpAAAAAA%3AeJLigymApwBRZC-Jr_2LStCL9csZePaeBNfctUra4-FEELpkqD42f6Ljh5_33sYvPr9-eICw4ZlBtow#b25 17 al., 2005; Fiaboe et al., 2007a,b; Furtado et al., 2006, 2007; Navajas et al., 2013). Predaceous mites and insect species most frequently found in association with T. evansi in these prospections were the following: Phytoseiidae: Euseius concordis (Chant) (Acari: Phytoseiidae), N. californicus, Phytoseiulus fragariae Denmark & Schicha (Acari: Phytoseiidae) and P. longipes; Insecta, Coccinellidae: the ladybird beetle Stethorus tridens Gordon(Coleoptera: Coccinelidae) (Rosa et al., 2005; Furtado et al., 2006, 2007a, b; Fiaboe et al. 2007a,b; Brito et al. 2008; da Silva et al., 2008). Upon further evaluation, only the predatory mite P. longipes (Figure 2) has been shown to be more promising for T. evansi control (Furtado et al., 2007). Figure 2. Female (a), nymphs (b) of Phytoseiulus longipes feeding on Tetranychus evansi eggs. (c) P. longipes female preying on T. evansi female. (d) Mating between male and female of P. longipes (Photos: Savi, P.J. & de Matos, S.T.S.) 2.3.6.3.2. Entomopathogenic fungi (a) (c) (b) (d) 18 Entomopathogenic fungi are also known to cause epizootics in populations of mites (der van Geest et al., 2000). In the case of T. evansi, Neozygites floridana (Weiser and Muma) Remaudiére and Keller (Entomophthorales: Neozygitaceae)] a pathogen of several spider mites species, has been observed associated with T. evansi (Humber et al., 1981). Isolates of Metarhizium anisopliae (Metschnikoff) Sorokin (Hypocreales: Clavicipitaceae) and Beauveria bassiana (Balsamo) (Hypocreales: Cordycipitaceae) have been tested against T. evansi and shown to be highly virulent, suggesting a potential for their use in the management of this pest (Wekesa et al. 2005; Bugeme et al., 2008; Maniania et al., 2008). The fungus N. floridana extensively found in Brazil infecting T. evansi has shown to be compatible with the phytoseiid mite P. longipes (Wekesa et al., 2007). However, Maniania et al.(2016) reported that there was no benefit in combining M. anisopliae and P. longipes for the control of T. evansi in tomato. Omukoko et al. (2020) reported under screen-house conditions that B. bassiana could colonize and persist on tomato varieties for 6 weeks and reduce adult T. evansi populations. 2.3.6.4. Cultural practices Cultural control is a key first step in preventing initial infestations and the spread of T. evansi. Plants should be routinely examined for any evidence of infestation and all infested materials should be disposed of carefully (Wakil et al., 2018). Some weeds are better at sustaining mite pests than others and these weeds, such as plantains, black nightshade, or solanaceous weeds should be targeted (Brust and Gotoh, 2018). Once harvest is complete, crop residues should be destroyed thus removing a breeding ground for the mites. Pruning back the affected plants and removing infested leaves will reduce pest numbers (Brust and Gotoh, 2018). Saunyama and Knapp (2003) pointed out that the pruning and trellising of tomato plants make the chemical control more effective and allow getting in better red spider mite management offering a positive effect on yields and quality of tomato fruits in Zimbabwe. Cantore et al. (2016) reported that tomato plants have high 19 sensitivity to water deficit. Therefore, water shortage caused by drought periods can lead to hydric stress, which can result in outbreaks of spider mites and considerable yield reduction (Cantore et al., 2016; Ximénez-Embún et al., 2016, 2018). For this reason, demand in the management of water application of tomato crops in dry regions or dry seasons should be stricter. Sprinkler irrigation has been used as an important practice to reduce the mite populations through mechanical actions that dislodge the mite, disrupting its life cycle (Chandler et al., 1979; Opit et al., 2001; Atakan et al., 2021 Alizade et al. (2016) reported that spider mites feeding on plants grown with low nitrogen inputs had reduced survival rates and delayed development. Thus, proper N content in fertilization input could avoid T. evansi population increase (Alizade et al., 2016; Brust and Gotoh, 2018). Although cultural practices have shown noticeable impact on mite population, these practices should be subordinated to other control strategies for more effective pest control. 2.3.7. Integrated pest management Integrated pest management (IPM) is critical for effective and economically viable use (Duso et al., 2020). This approach involves the integration of multiple control tactics (cultural, biological, pesticide selective, and host plant resistance) to favor long-term stability of a cropping system, minimizing the disadvantages (mainly causing risk to human and environment) of chemical control programs (Kogan, 1998; Jonsson et al., 2008; Fathipour and Sedaratian, 2013). In such an approach, three types of interactions can occur between different control measures, namely additive, synergistic and antagonistic (Fathipour and Sedaratian, 2013). In additive interaction, the combined effect of two control measures is equal to the sum of the effect of the two measures applied separately (Fathipour and Sedaratian, 2013). In synergistic interaction, the resulting effect is greater than the sum of the separate effects. Finally, in antagonistic interaction the resulting effect is lower than the sum of the effects of measures applied independently of each other (Fathipour and Sedaratian, 2013). For this reason, it is essential to understand the compatibility 20 between different control tactics intended to be integrated for the control of a target pest in any crop, to optimize IPM planning. 2.3.7.1. Combination of biological control and pest mites- resistant plants The defensive traits that help plants to protect themselves from damage caused by pests can vary qualitatively and quantitatively. Such variation may also affect positively or negatively other organisms, as predatory mites. Some studies have suggested gains in the concurrent use of resistant plants and phytoseiid mites in optimization of IPM (Bottrell et al., 1998; Khanamani et al., 2014; 2015; Fathipour et al., 2019). Fathipour et al. (2019) studied three cucumbers cultivars for their effects on the life table, and predation parameters of the phytoseiid P. persimilis. Their results suggested that the resistant cultivar supported more P. persimilis than other cultivars. Khanamani et al. (2015) found that a eggplant cultivar resistant to T. urticae concurs for better performance of the phytoseiid mite Typhlodromus bagdasarjani Wainstein & Arutunjan than susceptible cultivars. However, several cases of negative effects between resistance traits and biological agents have been also mentioned in the literature (Heinz and Zalom, 1996; Drukker et al., 1997; Koller et al., 2007; Sato et al., 2011; Bottega et al., 2017; Han et al., 2019; Paspati et al., 2021). This seems to be the case with tomato crops in relation to the performance of some phytoseiid mites when compared to other crops. The defensive traits found in tomato crops and mediated by trichomes and toxic compounds are usually more deleterious to natural enemies than in other crops. For instance, the survival of the generalist predatory mite Amblyseius swirskii Athias- Henriot juveniles on tomato leaves was not different from that on sweet pepper, but adult survival was significantly lower on whole tomato plants (Paspati et al. 2021). Amblyseius swirskii walked slower on plant species with increasing trichome density and on tomato leaves, their walking speed was lower when compared to rose plants (Buitenhous et al., 2014). Amblydromalus limonicus Garman & McGregor preyed fewer Bactericera cockerelli (Sulc) (Hemiptera: Triozidae) psyllid nymphs per day on tomato than on sweet pepper, but the mite survival was similar on the leaves of both 21 plants (Davidson et al., 2016). The developmental time and sex ratio of N. californicus on T. urticae were similar on tomato and strawberry, but immature survival rate and oviposition were lower on tomatoes (Castagnoli et al., 1999). The oviposition rate of N. californicus was negatively affected on tomato leaves, both directly and indirectly through the prey T. evansi, when compared to bean leaves (Koller et al., 2007). Walking activity, predation, and oviposition rates of Phytoseiulus macropilis Banks and P. longipes fed with T. uticae were reduced on tomato leaves, when compared to strawberry (Sato et al., 2011). Although tomato crops have been shown in several studies to affect predatory mites, including P. longipes, more than other crops, studies that compare the performance of phytoseiid among different tomato genotypes are still scarce. Such knowledge is essential to choose the tomato genotype that may optimize the use of determined phytoseiid mites as a bio-control agents in IPM implementation. 2.3.7.2. Combination of Biological control and chemical control Despite being effective in pest control, biological control is often not a stand- alone solution, requiring its incorporation into a larger pest management context, that frequently includes the application of chemical pesticides (Foutain and Medd, 2015; Bilbo and Walgenbach, 2020). For example, Bilbo and Walgenbach (2020) reported in staked tomatoes that the separate use of P. persimilis or the acaricide acramite labeled as selective did not reduce T. urticae pressure below the control, but the combination of both provided the most effective treatment in that regard. Given that the management of non-target pests in the tomato cropping systems is dominated by the use of synthetic pesticides, which can range from broad-spectrum to selective (Nyoni et al., 2001; Gotoh et al., 2010; Azandémè- Houmalon et al., 2015), the combination of predatory mites with chemical control requires an in-depth knowledge of potential risks to the predatory mites. Thus, risk assessment should take into account both acute toxicity and sublethal effects on biological (immature-stage development, fecundity, fertility, longevity, and sex ratio) and behavioral (predation rate, mobility, orientation, and feeding activity) parameters 22 of the biological-control agents (Desneux et al., 2007; Guedes et al., 2016; Zanardi et al., 2017; Duso et al., 2020). Additionally, pesticides can act through multiple routes of exposure (direct or residual contact, food ingestion), and this should be considered in these studies. Applications of these concepts are essential to recognize among the pesticides used in agroecosystems those which could be safely combined with the predatory mite, allowing its conservation. Several studies also reported that the compatibility of phytoseiid mites with chemical control could substantially vary between phytoseiid species and depending upon pesticide group (Fountain and Medd, 2015; Bergeron and Schmidt-Jeffris, 2020). For instance, bifenazate, labeled as selective for predatory mites, is minimally harmful to P. persimilis but can cause significant mortality of Neoseiulus fallacis (Garman) (Acari: Phytoseiidae), N. californicus and Amblydromella caudiglans (Schuster) (Schmidt-Jeffris and Beers, 2015, Schmidt-Jeffris et al., 2015, Bergeron and Schmidt-Jeffris, 2020). Similarly, hexythiazox, which is labeled as broad- spectrum acaricide proved to be more tolerated by N. californicus than by P. persimilis to the tested pesticides (Alzoubi and Çobanoglu, 2008). Chlorpyrifos, another broad-spectrum product showed no negative effect on the specialist phytoseiid Galendromus occidentalis Nesbitt, but lowered the population of the generalist phytoseiids Amblyseius andersoni Chant, Galendromus flumenis (Chant), Metaseiulus citri (Garman and McGregor), M. pomi (Parrott et al.), Typhlodromus caudiglans Schuster and T. pyri Scheuten] (Prischmann et al., 2005). 2.4. References Abad-Moyano R, Pina T, Ferragut F, Urbaneja A (2009) Comparative life-history traits of three phytoseiid mites associated with Tetranychus urticae (Acari: Tetranychidae) colonies in clementine orchards in eastern Spain: implications for biological control. Experimental and Applied Acarology 47:121–132. Abera G, Ibrahim AM, Forsido SF, Kuyu CG (2020) Assessment on post-harvest losses of tomato (Lycopersicon esculentem Mill.) in selected districts of East Shewa Zone of Ethiopia using a commodity system analysis methodology. Heliyon 23 6:e03749. Adenuga AH, Muhammad-Lawal A, Rotimi OA, Adenuga AH, Muhammad-Lawal A, Rotimi OA (2013) Economics and technical efficiency of dry season tomato production in selected areas in Kwara state, Nigeria. AgEcon Search 5:11-19 Alba JM, Montserrat M, Fernández-Muñoz R (2009) Resistance to the two-spotted spider mite (Tetranychus urticae) by acylsucroses of wild tomato (Solanum pimpinellifolium) trichomes studied in a recombinant inbred line population. Experimental and Applied Acarology 47:35–47. AL-Bayati AS (2019) Breeding for Tomato Resistance to Spider Mite Tetranychus urticae Koch (Acari: Tetranychidae). University of Kentucky Libraries Alizade M, Hosseini M, Modarres awal M, Goldani M, Hosseini A (2016) Effects of nitrogen fertilization on population growth of two-spotted spider mite. Systematic & Applied Acarology 21:947-956. Almarinez BJM, Barrion AT, Navasero MV, Navasero MM, Cayabyab BF, Carandang JSR, Legaspi JC, Watanabe K, Amalin DM (2020) Biological control: a major component of the pest management program for the invasive coconut scale insect, Aspidiotus rigidus Reyne, in the Philippines. Insects 11:745. Alzoubi S, Cobanoglu S (2008) Toxicity of some pesticides against Tetranychus urticae and its predatory mites under laboratory conditions. American-Eurasian Journal of Agricultural and Environmental 3: 30-37. Arab L, Steck S (2000) Lycopene and cardiovascular disease. The American Journal of Clinical Nutrition 71:1691S-1695S. Arah IK, Kumah EK, Anku EK, Amaglo H (2015) An overview of post-harvest losses in tomato production in Africa: causes and possible prevention strategies. Journal of Biology, Agriculture and Healthcare 5: 78–88. Atakan E, Sarıdaş MA, Pehlivan S, Achiri TD, Çeliktopuz E, Kapur B (2021) Influence of irrigation regimes on yield, pomological parameters and population development of Tetranychus cinnabarinus Boisd. (Acari: Tetranychidae) in 24 strawberry. Systematic & Applied Acarology 26: 1241-1253. Azandémè-Hounmalon GY, Fellous S, Kreiter S, Fiaboe KKM, Subramanian S, Kungu M, Martin T (2014) Dispersal behavior of Tetranychus evansi and T. urticae on tomato at several spatial scales and densities: implications for integrated pest management. PLoS ONE 9:e95071. Azandémè-Hounmalon GY, Affognon HD, Komlan FA, Tamò M, Fiaboe KKM, Kreiter S, Martin T (2015) Farmers’ control practices against the invasive red spider mite, Tetranychus evansi Baker & Pritchard in Benin. Crop Protection 76:53–58. Bagarama F (2016) Why is the red spider mite (Tetranychus evansi) a threat to dry season tomato growing in Tabora, Tanzania. Huria: Journal of the Open University of Tanzania 22: 1-10. Baker EW, Pritchard AE (1960) The tetranychoid mites of Africa. Hilgardia 29:455– 574. Bensoussan N, Zhurov V, Yamakawa S, O’Neil CH, Suzuki T, Grbić M, Grbić V (2018) The digestive system of the two-spotted spider mite, Tetranychus urticae Koch, in the context of the mite-plant interaction. Frontiers in Plant Science 9:1206. Bergeron PE, Schmidt‐Jeffris RA (2020) Not all predators are equal: miticide non‐ target effects and differential selectivity. Pest Management Science 76:2170– 2179. Bilbo TR, Walgenbach JF (2020) Compatibility of Bifenazate and Phytoseiulus persimilis for management of twospotted spider mites in North Carolina staked tomatoes. Journal of Economic Entomology 113:2096–2103. Blair BW (1989) Laboratory screening of acaricides against Tetranychus evansi Baker & Pritchard. Crop Protection 8:212–216. Bleeker PM, Mirabella R, Diergaarde PJ, VanDoorn A, Tissier A, Kant MR, Prins M, de Vos M, Haring MA, Schuurink RC (2012) Improved herbivore resistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative. Proceedings of the National Academy of Sciences 109:20124–20129. 25 Bonato O (1999) The effect of temperature on life history parameters of Tetranychus evansi (Acari: Tetranychidae). Experimental & Applied Acarology 23:11–19. Bottega DB, Souza BHS de, Rodrigues NEL, Eduardo WI, Barbosa JC, Boiça Júnior AL (2017) Resistant and susceptible tomato genotypes have direct and indirect effects on Podisus nigrispinus preying on Tuta absoluta larvae. Biological Control 106:27–34. Bottrell DG, Barbosa P, Gould F (1998) Manipulating natural enemies by plant variety selection and modification: a realistic strategy? Annual Review of Entomology 43:347–367. Boubou A, Migeon A, Roderick GK, Navajas M (2011) Recent emergence and worldwide spread of the red tomato spider mite, Tetranychus evansi: genetic variation and multiple cryptic invasions: Recent emergence and multiple cryptic invasions of Tetranychus evansi. Biological Invasions 13:81–92. Brassica (2019) Tomatoes in Benin. In: World Vegetable Center. https://avrdc.org/tomatoes-in-benin/. Accessed 28 Dec 2021 Britto EPJ, Gondim MGC, Torres JB, Fiaboe KKM, Moraes GJ, Knapp M (2009) Predation and reproductive output of the ladybird beetle Stethorus tridens preying on tomato red spider mite Tetranychus evansi. BioControl 54:363–368. Brust GE, Gotoh T (2018) Mites. In: Sustainable Management of Arthropod Pests of Tomato. Elsevier, pp 111–130 Bugeme DM, Maniania NK, Knapp M, Boga HI (2009) Effect of temperature on virulence of Beauveria bassiana and Metarhizium anisopliae isolates to Tetranychus evansi. In: Bruin J, van der Geest LPS (eds) Diseases of Mites and Ticks. Springer Netherlands, Dordrecht, pp 275–285 Buitenhuis R, Shipp L, Scott-Dupree C, Brommit A, Lee W (2014) Host plant effects on the behaviour and performance of Amblyseius swirskii (Acari: Phytoseiidae). Experimental & Applied Acarology 62:171–180. 26 Cantore V, Lechkar O, Karabulut E, Sellami MH, Albrizio R, Boari F, Stellacci AM, Todorovic M (2016) Combined effect of deficit irrigation and strobilurin application on yield, fruit quality and water use efficiency of “cherry” tomato (Solanum lycopersicum L.). Agricultural Water Management 167:53–61. Castagnoli M, Liguori M, Simoni S (1999) Effect of two different host plants on biological features of Neoseiulus californicus (Mcgregor). International Journal of Acarology 25:145–150. Çetin B, Vardar A (2008) An economic analysis of energy requirements and input costs for tomato production in Turkey. Renewable Energy 33:428–433. Chandler LD, Archer TL, Ward CR, Lyle WM (1979) Influences of irrigation practices on spider mite densities on field corn. Environmental Entomology 8:196–201. da Silva CAD, Lourenção AL, Moraes GJ de (1992) Resistência de tomateiros ao ácaro vermelho Tetranychus evansi Baker & Pritchard (Acari: Tetranychidae). Anais da Sociedade Entomológica do Brasil 21:147–156. da Silva FR, de Moraes GJ, Knapp M (2008) Distribution of Tetranychus evansi and its predator Phytoseiulus longipes (Acari: Tetranychidae, Phytoseiidae) in southern Brazil. Experimental & Applied Acarology 45:137–145. Davidson MM, Nielsen M-C, Butler RC, Silberbauer RB (2016) Prey consumption and survival of the predatory mite, Amblydromalus limonicus , on different prey and host plants. Biocontrol Science and Technology 26:722–726. de Azevedo SM, Ventura Faria M, Maluf WR, Barneche de Oliveira AC, de Freitas JA (2003) Zingiberene-media