Proceedings of the Work Group Meeting. Florence, Italy March 2009

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1 IOBC / WPRS Work Group Integrated Control of Plant-Feeding Mites OILB / SROP Groupe de Travail Lutte Intégrée Contre les Acariens Phytophages Proceedings of the Work Group Meeting at Florence, Italy 9 12 March 2009 Editors: Eric Palevsky, Phyllis G. Weintraub, Uri Gerson, Sauro Simoni IOBC wprs Bulletin Bulletin OILB srop Vol. 50, 2009

2 ii The content of the contributions is in the responsibility of the authors The IOBC/WPRS Bulletin is published by the International Organization for Biological and Integrated Control of Noxious Animals and Plants, West Palearctic Regional Section (IOBC/WPRS) Le Bulletin OILB/SROP est publié par l Organisation Internationale de Lutte Biologique et Intégrée contre les Animaux et les Plantes Nuisibles, section Regionale Ouest Paléarctique (OILB/SROP) Copyright: IOBC/WPRS 2009 The Publication Commission of the IOBC/WPRS: Horst Bathon Julius Kühn-Institute (JKI) Federal Research Center for Cultivated Plants Institute for Biological Control Heinrichstr. 243 D Darmstadt (Germany) Tel , Fax Luc Tirry University of Gent Laboratory of Agrozoology Department of Crop Protection Coupure Links 653 B-9000 Gent (Belgium) Tel , Fax Address General Secretariat: Dr. Philippe C. Nicot INRA Unité de Pathologie Végétale Domaine St Maurice - B.P. 94 F Montfavet Cedex (France) ISBN

3 The second meeting of the Working Group Integrated Control of Plant-Feeding Mites was supported (in alphabetical order) by: ARSIA - TOSCANA COOPERATIVA DI LEGNAIA BASF INTRACHEM BIO BEE KOPPERT BIOBEST SARIAF GOWAN BIOPLANET SOLDERA CERTIS SYNGENTA BIOLINE

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5 iii Preface This Bulletin contains the contributions to the second meeting of the IOBC/wprs Work Group Integrated Control of Plant-Feeding Mites held in Florence, Italy, 9-12 March, The meeting was hosted by the Agricultural Research Council - Research Center for Agrobiology and Pedology (CRA ABP), formerly Experimental Institute for Agricultural Zoology (ISZA), located in Florence, Italy. Mites are small arthropods that often get lost among their larger insect cousins. The aim of this Work Group is to bring together students, researchers and company representatives and focus on all aspects of integrated and biological control of plant feeding mites, in order to discuss approaches that can be taken to increase control efficacy. The meeting was attended by 62 participants from 12 countries, arriving from North America, Europe, and the Middle East. Over two days, 24 oral presentations and 6 posters were presented in six sessions covering: 1) Phytoseiid types in biological control; 2) Biological control of tetranychid, non-tetranychid and exotic acarine pests; 3) Chemical control; 4) Behavioral effects in biological control; 5) Management in vineyards; and 6) Host plant-mite interactions. We now look back on this successful meeting and would like to genuinely express our gratitude to all those who worked so hard to make this event an experience that the participants will not soon forget. The meeting was organized in-house by the dedicated faculty acarologists of CRA ABP, Marialivia Liguori playing a key role, along with their dynamic administrative and technical staff, Donatella Goggioli, Silvia Guidi, Giuseppino Sabbatini Peverieri and Franca Tarchi. We would like to acknowledge the scientific committee, composed of Phyllis Weintraub, Uri Gerson, Marisa Castagnoli and Roberto Nannelli for selecting the keynote speakers and preparing the meeting program. This teamwork paved the way to a wonderful meeting that we felt everyone thoroughly enjoyed both scientifically and socially. We would like to express our gratitude to the many sponsors who generously contributed to finance this meeting. Finally, we would like to thank the participants for their enthusiasm in preparing their contributions and for their collaboration in the success of the meeting. Sauro Simoni & Eric Palevsky Local Organizer & Convenor of the Work Group March 2009

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7 List of participants Einat Adar Haifa University and Newe-Ya'ar Research Center, Dept Entomology, ARO, PO Box 1021, Ramat Yishay 30095, ISRAEL Yves Arijs Biobest Belgium N.V., Ilse Velden 18, 2260 Westerlo, BELGIUM Massimo Benuzzi Intrachem bio Italia, Via Calcinaro 20085/7, Cesena (FC) ITALY Sylvia Blümel AGES, Institute of Plant Health, Spargelfeldstr. 191, 1226 Wien AUSTRIA Karel Bolckmans Koppert B.V., Veilingweg 17, 2651 BE Berkel en Rodenrijs THE NETHERLANDS Piero Braccini ARSIA Toscana, Servizi agroamb., vigilanza e controllo Via Pietrapiana 30, Firenze ITALY F. Javier Calvo Robles Koppert B.S. C/ Cobre, 22. Pol. Industrial Ciudad Del Transporte La Mojonera (Almería) SPAIN Marisa Castagnoli CRA-ABP, Research Center for Agrobiology and Pedology, Via Lanciola 12/a, Firenze ITALY Rosemary Collier The University of Warwick, Warwick HRI, Wellesbourne, Warwick CV35 9EF UNITED KINGDOM Lorenzo Corino CRA-UTV Via Casamassima 148, Turi (BA), ITALY Martha De Coss Universidad Autónoma de Chiapas, Facultad de Ciencias Agrícolas, Huehuetán, Chiapas. C.P MEXICO Carlo Duso University of Padua, Dept Environmental Agronomy and Crop Science, Agripolis, viale dell Università 16, Legnaro (PD), ITALY Stefano Foschi Bioplanet s.c.a., via Masiera prima 1195, Martorano di Cesena (FC) ITALY Elena Gagnarli University of Florence, Dept Biology "Leo Pardi", via Romana 17, Firenze ITALY v

8 vi Uri Gerson Hebrew University of Jerusalem, Fac. of Agriculture, Rehovot ISRAEL Donatella Goggioli CRA-ABP Research Center for Agrobiology and Pedology, via Lanciola 12/a, Firenze ITALY Richard GreatRex Syngenta Bioline, Telstar Nursery, Holland Road, Little Clacton, Essex, CO16 9QG UNITED KINGDOM Silvia Guidi CRA-ABP Research Center for Agrobiology and Pedology, via Lanciola 12/a, Firenze, ITALY Jorge Hernandez Biobest Sistemas, Spain. Bulevar de Vícar, 1267, Puebla de Vícar, Almería SPAIN Mónica Hurtado Ruiz Universitat Jaume I de Castelló, Campus del Riu Sec Castellón de la Plana. Castellón, SPAIN Ido Izhaki University of Haifa, Dept of Evolutionary and Environmental Biology, Haifa ISRAEL Kheradpir Neda Dept Entomology, Fac. Agriculture and Natural Resources, Sc. and Res. Branch, Islamic Azad University, Tehran, IRAN Markus Knapp Koppert Biological Systems, Veilingweg 14, Postbus 155, 2650 AD Berkel en Rodenrijs THE NETHERLANDS Izabela Lesna University of Amsterdam, Kruislaan 320, 1098 SM, Amsterdam THE NETHERLANDS Marialivia Liguori CRA-ABP Research Center for Agrobiology and Pedology, via Lanciola 12/a, Firenze ITALY Mauro Lorenzon University of Padua, Dept Environmental Agronomy and Crop Science, Agripolis, viale Università 16, Legnaro (PD) ITALY Alon Lotan Haifa University and Newe-Ya'ar Research Center, Dept. Entomology, ARO P.O. Box 1021, Ramat Yishay ISRAEL Anna Luczynski Koppert Biological Systems, B Ave Surrey BC V3S 0E3 CANADA Valeria Malagnini FEM IASMA, via E. Mach 1, San Michele all'adige (TN) ITALY Manuel Manduchi Bioplanet s.c.a., via Masiera prima 1195, Martorano di Cesena (FC), ITALY

9 vii Yonatan Maoz Hebrew Univ. and Newe-Ya'ar Research Center, Dept of Entomology, ARO, P.O. Box 1021, Ramat Yishay ISRAEL Maria Teresa Martinez Ferrer IRTA, Carretera De Balada Km 1, Amposta, Terragona SPAIN Jim McMurtry University of California, Riverside, CA USA Gerben Messelink Wageningen UR Greenhouse Horticulture, Violierenweg 1, 2665 MV Bleiswijk THE NETHERLANDS Roberto Nannelli CRA-ABP Research Center for Agrobiology and Pedology, via Lanciola 12/a, Firenze, ITALY Gabriel Otero-Colina Colegio de Postgraduados, Campus Montecillo, Km carretera Mexico-, Montecillo, Texcoco, Edo., MEXICO Hajar Pakyari Islamic Azad Univ., Fac. Agricultre and natural resources, Dept Entomology, Hessarak, Poonak Sq. Ashrafi Esfahani Highway. P.O. Box: , IRAN Eric Palevsky ARO - Dept of Entomology, Newe-Ya'ar Research Center, Ministry of Agriculture P.O. Box 1021, Ramat Yishay ISRAEL Peña Jorge E. University of Florida, Homestead, FL USA Matteo Perrone Cinque Terre National Park, via T. Signorini 118, Riomaggiore ITALY Alberto Pozzebon University of Padua, Dep Environmental Agronomy and Crop Science, Agripolis, viale Università 16, Legnaro (PD) ITALY Ernesto Ragusa University of Palermo, Facoltà di Agraria, Dept S.EN.FI.MI.ZO. viale delle Scienze 13, Palermo, ITALY Salvatore Ragusa University of Palermo, Facoltà di Agraria, Dept S.EN.FI.MI.ZO. viale delle Scienze 13, Palermo, ITALY Giuseppino Sabbatini Peverieri CRA-ABP Research Center for Agrobiology and Pedology, via Lanciola 12/a, Firenze, ITALY

10 viii Maurice W. Sabelis Inst. for Biodiversity and Ecosystem Dynamics (IBED), Kruislaan 320, 1098 SM, Amsterdam THE NETHERLANDS Francisco J. Sáenz-de-Cabezón Irigaray University of La Rioja, C/Madre de Dios 51, Logroño (La Rioja), SPAIN Peter Schausberger Univ. Natural Resources and Applied Life Sciences, Inst. of Plant Protection, Dept Applied Plant Sciences Plant Biotechnology, Peter Jordanstr.82, 1190 Vienna, AUSTRIA Sauro Simoni CRA-ABP Research Center for Agrobiology and Pedology, via Lanciola 12/a, Firenze, ITALY Menelaos Stavrinides University of California, Berkeley, 137 Mulford Hall, Berkeley, CA USA Shimon Steinberg BioBee Sde Eliyahu Ltd., Kibbutz Sde Eliyahu Beit Shean Valley ISRAEL Monica Soldera Az.Agr.Case Basse di Gianfranco Soldera, Loc. Case Basse, Montalcino (SI) ITALY Franca Tarchi CRA-ABP Research Center for Agrobiology and Pedology, via Lanciola 12/a, Firenze, ITALY Bryony Taylor CABI, Bakeham Lane, Egham, Surrey, TW20 9TY UNITED KINGDOM Paola Tirello Univ. of Padua, Dep. of Environmental Agronomy and Crop Science, Agripolis, viale Università 16, Legnaro (PD) ITALY Rocchina Tiso Servizio Fitosanitario Regione Emilia Romagna, Via di Saliceto 81, Bologna, ITALY Simone Tofani Società Cooperativa Agricola di Legnaia, via di Sollicciano 13, Firenze ITALY Haralabos Tsolakis University of Palermo, Fac. Agraria, Dept S.EN.FI.MI.ZO., viale delle Scienze 13, Palermo, ITALY Yvonne van Houten Koppert Biological Systems, Veilingweg 14, Postbus 155, 2650 AD Berkel en Rodenrijs THE NETHERLANDS

11 ix Andreas Walzer Univ. Natural Resources and Applied Life Sciences, Inst. of Plant Protection, Dept Applied Plant Sciences Plant Biotechnology, Peter Jordanstr.82, 1190 Vienna, AUSTRIA Phyllis Weintraub Agricultural Research Organization, Gilat Research Center, D. N. Negev 85280, ISRAEL Abbas Ali Zamani Razi University, Dept of Plant Protection, College of Agriculture, P.O. Box: , Kermanshah, IRAN Rostislav Zemek Institute of Entomology, Biology Centre AS CR, Branisovska 31, Ceske Budejovice CZECH REPUBLIC

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13 Contents Preface... iii List of Participants... v Subject Index... xv Eotetranychus carpini: biological control experiments in Tuscan vineyards (Italy) Marisa Castagnoli, Marialivia Liguori, Sauro Simoni, Giuseppino Sabbatini Peverieri, Donatella Goggioli, Silvia Guidi, Franca Tarchi Application of pollen for promotion of predatory mite populations in protected basil Einat Adar, Moshe Inbar, Eric Palevsky... 8 Integrated control of bulb-scale mite (Steneotarsonemus laticeps) in Narcissus Rosemary Collier, Gordon Hanks, Malcolm Millar... 9 Resistance in Carica papaya L. Cv. Maradol to the mite Eotetranychus lewisi (McGregor) induced by the herbivory of Estigmene acrea (Drury) Martha E. de Coss, Alexander E. Reyes, Mario E. Cabrera, Rodolfo Flores, Leopoldo Cruz Relationships between plant pathogenic fungi and mites in vineyards: implications for IPM Carlo Duso, Alberto Pozzebon, Paola Tirello, Mauro Lorenzon, Diego Fornasiero Comparative effectiveness of Phytoseiulus persimilis and P. longipes in the control of Tetranychus urticae on strawberries and roses Hans Hoogerbrugge, Yvonne van Houten, Markus Knapp, Karel Bolckmans Effect of physiochemical features of different species or cultivars of host plants on the foraging behavior of Scolothrips longicornis Neda Kheradpir, Mohammadreza Rezapanah, Karim Kamali and Yaghoub Fathipour Compatibility of Amblyseius swirskii with UV-absorbing nets Saioa Legarrea, Alberto Fereres, Phyllis G. Weintraub Notes on the phenology and the biology of Tydeus caudatus Dugès (Acari Tydeidae) Mauro Lorenzon, Alberto Pozzebon, Carlo Duso Biological control of the old world date mite, Oligonychus afrasiaticus, using indigenous predatory mites in the Southern Arava Valley of Israel Alon Lotan, Eric Palevsky, Ido Izhaki The spider mite Neotetranychus rubi (Träg.) a potential prey for the predatory mite Amblyseius andersoni (Chant) Valeria Malagnini, Alberto Grassi, Romano Maines, Gino Angeli, Claudio Ioriatti, Carlo Duso xi

14 xii Integrated pest management of Oligonychus perseae: developing action thresholds and the identification and conservation of natural enemies Yonattan Maoz, Eric Palevsky, Shira Gal, Miriam Zilberstein, Michael Noy, Yehonatan Izhar, Jonathan Abrahams Samuel Gan-Mor, Moshe Coll The two-spotted mite Tetranychus urticae Koch (Acari: Prostigmata) on citrus Clementine groves: seasonal trends and control strategies María Teresa Martínez-Ferrer, José Miguel Campos, José Miguel Fibla The Phytoseiidae in biological control: relevance of taxonomic classification and life style categorization James A. McMurtry Whitefly-induced plant defences in cucumber and their impact on biological control of spider mites Gerben J. Messelink, Arne Janssen Failure of methyl bromide fumigations to exterminate mites present on grapes exported to Mexico from Chile Gabriel Otero-Colina, Francisco Ramírez y Ramírez, Héctor Enrique Vega Ortiz Mutual interference of Scolothrips longicornis Priesner (Thysanoptera: Thripidae) with Tetranychus urticae Koch (Acari: Tetranychidae) Hajar Pakyari, Yaghoub Fathipour Predator-prey dynamics and strategies for control of the red palm mite (Raoiella indica) (Acari: Tenuipalpidae) in areas of invasion in the Neotropics Jorge E. Peña, Jose Carlos V. Rodrigues, Amy Roda, Daniel Carrillo and Lance S. Osborne The association between the red palm weevil Rhyncophorus ferrugineus (Olivier) and its phoretic mites: Centrouropoda almerodai Hiramatsu & Hirchmann and Uroobovella (Fuscuropoda) marginata (Koch) Ernesto Ragusa, Antonella Di Palma, Francesco Porcelli How homogeneous are Tetranychus urticae populations in citrus orchards? Preliminary isolation and characterization of polymorphic microsatellite markers for T. urticae (Acari: Prostigmata) Beatriz Sabater-Muñoz, Sara Pascual-Ruiz, Josep A. Jacas, Mónica A. Hurtado Spider mite control in California vineyards with conventional acaricides Francisco J. Sáenz-de-Cabezón Irigaray, Frank G. Zalom, Nicole Nicola Multiple predators, intraguild interactions and biological control of a single spider mite species Maurice W. Sabelis, Rachid Hanna, Alexis Onzo, Angelo Pallini, Ibrahim Cakmak and Arne Janssen Comparative repellent effects of different acaricide residues to predatory and spider mites. Is there a need for including behavior into standardized testing methods? Francisco J. Sáenz-de-Cabezón Irigaray, Frank G. Zalom Spatial refuge use by herbivorous mites poses major challenges for biological control Peter Schausberger Neoseiulus californicus and Beauveria bassiana: a proficuous coexistence? Sauro Simoni, Silvia Guidi, Franca Tarchi

15 Demographic testing reveals complex effects of pesticides on biological control of Pacific spider mite (Tetranychus pacificus) by the western predatory mite (Galendromus occidentalis) on grape plants Menelaos C. Stavrinides, Nicholas J. Mills Classical biological control of the red palm mite (Raoiella indica): area of origin and preliminary surveys Bryony Taylor Phytoseiid mites associated with forest trees in two Natura 2000 locations: S. Adriano woods (Sicily) and Fraktò virgin forest (Greece) Haralabos Tsolakis, Salvatore Ragusa Oviposition behavior of Phytoseiulus persimilis facing the risk of intraguild predation Andreas Walzer, Peter Schausberger Predator cues induce behavioral shifts in alternative prey: consequences forprey life history traits and its host plant Andreas Walzer, Peter Schausberger Novel application of pollen to augment the predator Amblyseius swirskii on greenhouse sweet pepper Phyllis Weintraub, Sophia Kleitman, Rafi Mori, Samuel Gan-Mor, Liana Ganot, Eric Palevsky Effect of host plant on the functional response of Orius albidipennis(hemiptera: Anthocoridae) to Tetranychus urticae (Acari: Tetranychidae) Abbas Ali Zamani, Shabnam Vafaei, Reza Vafaei, Shila Goldasteh, Katayoon Kheradmand Aceria carvi potential threat for caraway production in Europe? Rostislav Zemek, Erja Huusela-Veistola xiii

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17 Subject index Acaricides 9, 57, 61, 95, 82 Aceria carvi 131 Aceria guerreronis 99 Alternative prey 45, 83, 113 Amblydromalus manihoti 62, 83 Amblyseius andersoni 13, 53, 62, 107 Alternative food 13, 51, 83, 116 Amblyseius largoensis 69 Amblyseius swirskii 8, 41, 69 Areca catechu 103 Avocado 57 Basil 8 Behavior 35, 95, 107, 113, 125 Beauveria bassiana 101 Brevipalpus chilensis 64 Bulb-scale mite 9 Caraway 131 Cassava 62, 83 Centrouropoda almerodai 80 Chrysoperla carnea 59 Clementine 61, 81 Coconut 69, 99, 103 Colomerus vitis 14, 45 Conservation 51, 57 Conwentzia 59 Creontiades pallidus 59 Cucumber 29, 63, 65 Cydnoseius negevi 52 Date palm 51, 69, 80, 103 Dispersal 33, 41, 95, 119 DNA library 81 Eggplant 36 Enemy-free space 99 Eotetranychus carpini 1 Eotetranychus lewisi 11 Estigmene 11 Euseius finlandicus 23, 106 Euseius fustis 89 Euseius scutalis 8, 57 Forest Phytoseiidae 106 Frankliniella occidentalis 113, 119 Fumigation 64 Functional response 65, 125 Fungicides 13 Galendromus occidentalis 71, 95, 102 Grape vines 1, 13, 45, 64, 82, 102 Grape downy mildew 13, 45 Grape powdery mildew 13, 45 Host plant effects 11, 29, 29, 62, 64, 69, 95, 99, 103, 113, 125 Intraguild interactions 8, 83, 107 Induction of plant defenses 11, 63 Kampimodromus aberrans 1, 13, 106 xv

18 xvi Mutual interference 65 Microhabitat specialization 83 Narcissus 9 Neoseiulus californicus 1, 51, 61, 63, 83, 99, 101, 107, 113 Neoseiulus fallacis 95 Neoseiulus longilateratus 52 Neotetranychus rubi 53 Oil sprays 61 Oligonychus afrasiaticus 51 Oligonychus gossypii 87 Oligonychus perseae 57 Orius albidipennis 125 Ornamentals 29, 103 Oviposition behavior 107 Panonychus ulmi 14, 53 Papaya 11 Paraseiulus talbii 14 Pepper 36, 41, 113, 119 Pesticides 64, 95, 102, Phytoseiidae 13, 62 Phytoseiulus longipes 29 Phytoseiulus persimilis 29, 63, 69, 83, 95, 107 Pollen 8, 13, 45, 51, 54, 57, 62, 69, 88, 114, 119 Polyphagotarsonemus latus 41, 120 Powdery mildew 13 Quarantine pests 64 Raoiella indica 69, 103 Raspberry 53 Refuge 99 Release strategies 1 Repellency 95 Resistance induction 11 Rhyncophorus ferrugineus 80 Roses 29 Scolothrips longicornis 29, 65 Soybeans 126 Spatial refuge 99 Strawberry 29 Taxonomy 62 Tetranychus cinnabarinus 53, 85 Tetranychus evansi 29, 99 Tetranychus pacificus 32, 82, 102 Tetranychus urticae 20, 29, 36, 53, 63, 64, 65, 81, 83, 95, 101, 108, 114, 119, 125 Tomato 29, 36, 65, 99 Tydeus caudatus 14, 45 Trialeurodes vaporariorum 63 Typhlodromalus aripo 62, 83 Typhlodromus athiasae 52 Typhlodromus exhilaratus 1 Typhlodromus pyri 13, 62 Uroobovella marginata 80 UV-absorbing nets 41 Whiteflies 8, 41, 63, 119 Yield reduction 57, 61, 69

19 Integrated Control of Plant-Feeding Mites IOBC/wprs Bulletin Vol. 50, 2009 pp. 1-7 Eotetranychus carpini: biological control experiments in Tuscan vineyards (Italy) Marisa Castagnoli, Marialivia Liguori, Sauro Simoni, Giuseppino Sabbatini Peverieri, Donatella Goggioli, Silvia Guidi, Franca Tarchi CRA-ABP, Agricultural Research Council, Research Centre for Agrobiology and Pedology, via di Lanciola 12/a, Firenze, Italy Abstract: Infestations of Eotetranychus carpini (Oud.) have increased during recent years in organic as well as IPM vineyards in large, high quality wine producing areas of central Tuscany. We report a triennial experiment, attempting to re-establish a large population of phytoseiids in these vineyards, in order to achieve biological control of the tetranychid pest. Three generalist phytoseiids were compared: a commercialized strain of Neoseiulus californicus (McGregor), a laboratory strain of Typhlodromus exhilaratus Ragusa and a wild strain of Kampimodromus aberrans (Oud.). The phytoseiid species were released on selected vineyards at the highest level suggested in the literature and/or by the producer. Kampimodromus aberrans was introduced once per year, when the vines were still dormant ( specimens/tree); N. californicus and T. exhilaratus were repeatedly released with a density of specimens/plant, on an annual basis. Both released populations of T. exhilaratus and of N. californicus showed great difficulty in colonizing the vineyard. On the contrary, the release of K. aberrans during winter, on pruned branches from donor vineyards, was the most convenient strategy in controlling E. carpini in the Val d Orcia. A single high density release was sufficient to establish the species, which limited E. carpini outbreaks for two years after the release. Minimal releases of K. aberrans carried out in the third year of the experiment gave promising results. A longer time is needed to verify if minimal releases will allow the establishment of the phytoseiid sufficiently to achieve long-term tetranychid control. Key words: Kampimodromus aberrans, Typhlodromus exhilaratus, Neoseiulus californicus, release strategy Introduction In the Italian vineyard ecosystem mites hold an important role, mainly played by the herbivore (tetranychids) predators (phytoseiids) relationship. The best way to control tetranychids on vines is to achieve and maintain a good equilibrium between these two actors (Duso et al., 2007). In recent years, probably consequent upon more favourable climatic conditions and changes in vineyards management, infestations of Eotetranychus carpini (Oud.) have increased in organic as well as IPM vineyards of large, high quality wine producing areas of central Tuscany. In these vineyards phytoseiids were generally not present or present in extremely low numbers (personal observations). High E. carpini infestations induced premature drop of vine leaves, with a resultant decrease in the sugar content of grapes and in lignification of branches. The pest species is less known than other tetranychids inhabiting vine (Castagnoli et al., 1989), whereas the problems involved with its infestations are economically important and particularly difficult to be solved, especially in organic vineyards where synthetic pesticides cannot be used. 1

20 2 In this paper we report a triennial experience on re-establishing good populations of phytoseiids in some vineyards, in order to achieve biological control of E. carpini. Three different generalist phytoseiids were used: Neoseiulus californicus (McGregor), Typhlodromus exhilaratus Ragusa and Kampimodromus aberrans (Oud.). The first was chosen as the only commercialized species found in Mediterranean vineyards (Liguori & Castagnoli, 1989; Kreiter et al., 2000). Typhlodromus exhilaratus is the most common species in Tuscany vineyards (Castagnoli & Liguori, 1986) and successfully develops on the tetranychid (Castagnoli et al., 1989); K. aberrans, is found everywhere on vines in Italy, and has been shown to control tetranychids in North Italian vineyards (Duso, 1997). Materials and methods Vineyards location and characteristics The study was carried out in the vineyards of six farms located in Val d'orcia (South of Siena district, Central Tuscany), in an area of about 40 km 2 across Montalcino (43 3'N,11 29'E), Castiglione d'orcia (43 1'N,11 37'E) and Tavernelle (43 1'N,11 26'E). The territory, considered UNESCO's patrimony of humanity, is characterized by rolling hills and valleys covered by rich vegetation in which Mediterranean maquis is mixed with vineyards. The selected vineyards had about 5,500 plants per hectare, a surface ranging from 0.5 to 1ha and were 5-7 years old. They were mainly located on hills ( m a.s.l.), oriented towards east, south, south-west, and pruned according to the cord spur system and with organic or integrate pest management. In both cases no synthetic acaricides or insecticides were used; in organic vineyards sulphur, copper and Ampelomyces quisqualis Ces. (AQ10 coded product) were applied during the experiment to control diseases, whereas in the IPM vineyards fungicide pressure, including synthetic products, was higher. The vine variety was usually Sangiovese Grosso, the typical Brunello's variety, but the Petit Verdot variety was also grown, mainly in the surroundings of Castiglione d'orcia. Heavy infestation of E. carpini occurred everywhere and there was little or no presence of phytoseiids in the years before our experimentation. Phytoseiid origin, release and cost The laboratory strain of T. exhilaratus used for releases originated from a vineyard in the Chianti area (Tuscany) and was reared in the CRA-ABP laboratory with Quercus ilex L. pollen as food (Castagnoli & Liguori, 1994). Neoseiulus californicus specimens came from a commercial strain produced in Europe (Koppert strain). Kampimodromus aberrans was an over-wintering wild strain obtained from vineyards of the Veneto region (north-eastern Italy). The phytoseiid species were differently released in the selected vineyards. Kampimodromus aberrans was introduced only once a year, when the vines were still dormant, as a high number of over-wintering females can be transferred with pruned branches from donor vineyards. As the suggested release density for K. aberrans was about 90 specimens per plant (Duso et al., 1991), four density levels were considered: high ( specimens/tree), medium (60-90) low (30-60) and very low (<30). Neoseiulus californicus and T. exhilaratus, originating from commercial and laboratory rearings, and presumably requiring a longer period of adaptation to the outdoor conditions, were repeatedly released on the vines starting from blossom time until the end of July, every two-three weeks. The former phytoseiid was introduced at the density of specimens/plant on an annual basis, with each single introduction considerably higher than that suggested by the producer; as to T. exhilaratus, the total number of the released specimens on each vine plant varied from 130 to 180.

21 3 Table 1. Vineyards and treatments in a three year experiment in the Val d Orcia area. The farms are indicated with a capital letter, whereas vineyards are progressively numbered. In the Species release column the introduced species (NC = N. californicus, Koppert strain, KA = K. aberrans, TE = T. exhilaratus) are indicated and the different treatments in the same vineyard numbered. Release density is indicated as high (>90 specimens/tree), medium (60-90) low (30-60) and very low (<30). Farm-vineyard Variety Year Species release Release modality Release density A1 Organic Sangiovese NC 2. KA 3. NC+KA multiple single multiple+single no release high high high --- A1 Organic Sangiovese NC no release no release no release multiple high A2 Organic Sangiovese NC multiple no release high --- A1 Organic Sangiovese no release --- B3 Organic Sangiovese KA B3 Organic Sangiovese KA C4 IPM Sangiovese KA D5 Organic Petit Verdot TE D5 Organic Petit Verdot TE D6 Organic Petit Verdot KA single no release no release single single no release multiple no release multiple no release single no release D6 Organic Petit Verdot no release --- high very low very low high high high D7 Organic Petit Verdot KA single very low E8 IPM Sangiovese KA 2. KA 3. KA single single single no release very low low medium --- E9 IPM Sangiovese KA single very low F10 Organic Sangiovese KA single no release very low --- On account of the release modality, the species were ranked according to three levels of release cost, including an evaluation of availability and handling/rearing time before use: N. californicus, commercialized and easy to distribute, was classified at low cost; K. aberrans, which is easily transferred with branches in a single winter release, but which has to be found and the donor branches must be inspected, was considered at medium cost; and T. exhilaratus,

22 4 not commercially available and has to be reared in the laboratory, with prolonged handling time, was considered at high cost. Experiment timetable and sampling For three consecutive years, samples of vine leaves per treatment were taken every twothree weeks in the selected areas to check mite species and densities during the vegetative period of the vines, from the first days of May to the end of September. The experiment may be considered to be divided into two parts. In the first two years (2006 and 2007) we tested different predator species introduced in large numbers in order to evaluate their establishment on vine, suitability in terms of pest control and of cost. In the third year, the more suitable species was tested at different and lower densities of release. Table 1 summarizes vineyards and situations. Data analysis A General Linear Model was used during the first two years in order to evaluate the efficiency of the three phytoseiids, the E. carpini infestation during 2006/2007, the effects of variety (Sangiovese, Petit Verdot) and the effect of cost levels on the control success (ratio tetranychid/phytoseiid 5.5), and the establishment of released phytoseiid in the vineyards. This analysis was performed taking into account the presence of other phytoseiid species, and the control and recovery percentages of released species. Main effects indicated the significant variables, and the multiple bivariate correlations allowed us to evaluate the closeness of the relationship between species released and the considered variables. Third year. On the basis of the first two years' experience, the selected species of phytoseiid was released and further evaluated by focusing on a wider range of release densities. Both its presence and its density were analysed as responses to tetranychid infestation, vine variety, release and/or presence in the previous biannual samples, vineyard management (organic or IPM), sample time during the year and the three different release densities (Table 1). At each sampling date the foliar damage was evaluated by measuring the portion of leaf area damaged (Kondo, 2004) and correlated with the selected species presence and whether it was significantly dependent on the density of release. All statistical analyses (GLM, ANOVA and post hoc comparison, correlations) were performed by means of the statistical program SPSS (1999). Results and discussion Analysis with the GLM model, performed on the data of the first years with the aim of evaluating the three species on the basis of efficiency and minor release cost, provided highly significant results (P=0.000, n=890). No differences were found on regard to year (P=0.432) and vine variety (P=0.543). The density of E. carpini was the significant explicative variable (P=0.000) of the presence of the phytoseiids. By combining the cost levels with re-finding the released phytoseiid and the association with E. carpini, the best phytoseiid species was determined. Kampimodromus. aberrans was the most re-sampled species and the best both in term of persistence after release (P=0.000, Spearman s ρ correlation) and in association with E. carpini (P=0.001). This predator was collected in 83.9% of the first three samples following its release, whereas the frequency was 57.9% for T. exhilaratus and 18.7% for N. californicus. Furthermore, upon considering the total means of the tetranychid/phytoseiid ratios, being in 88.4% of the records, it was under the limit considered. Neoseiulus californicus had difficulties in remaining on the vine leaves (P=0.431), but its presence was better correlated with the presence of E. carpini (P=0.019) than T. exhilaratus (P=0.349). The

23 latter remained for longer periods on leaves (P=0.047), also in absence or scarce presence of target prey. The data of the third year confirmed the efficiency of K. aberrans: over the whole period it was collected in 87.2 % of the samples and, when associated with E. carpini, only in 11.3% of cases was the tetranychid/phytoseiid ratio higher than 5.5. This occurred in some summer samplings and remained low for a few weeks. The phytoseiid density was independent of the vine variety (P=0.308), but was dependent on sampling time (P=0.02), release density in 2008 (P=0.03), and was highly dependent (P=0.000) on vineyard management and release/presence of K. aberrans in previous years. On the whole, in organic vineyards, the numbers of K. aberrans sampled (2.94±3.07 specimens/leaf) was three times higher than on IPM vineyards (0.92±0.77/ leaf) (t-test, P<0.000). A similar ratio was seen by considering the areas where K. aberrans was already present in : 4.24±2.89/leaf were sampled where it occurred in the prior two years, 1.59±2.26 where the phytoseiid was collected for the first time. Only slightly significant differences were found in the density of phytoseiids after different releases. As a result the damage level of the leaves was, on the whole, low in the areas where K. aberrans was both released and already present. The frequency and intensity of damage observed were both strongly related to the presence of the phytoseiids (Spearman test, P<0.01). The number of undamaged leaves was higher than the damaged leaves (χ 2 test = 259.3, P<0.001) and release density affected the observed damage (χ 2 test = 23.2, P<0.001). The transfer of K. aberrans during winter on pruned branches from vineyards with high phytoseiid density to those without seems the most convenient strategy to control E. carpini in the Val d Orcia vineyards. This methodology was successfully used for a long time in North East Italy (Duso & Vettorazzo, 1999), where the species is more widespread in vineyards than in Tuscany and where it controls E. carpini, especially on all hairy varieties (Duso et al., 1991; Duso & Vettorazzo, 1999). However, the North East Italian viticulture is very different from that of Tuscany due to agronomic management, climatic condition, surrounding vegetation and vine varieties. A single high density release was sufficient to establish the predator that maintained and increased its ability to limit population outbreaks of E. carpini for two years after the release, even in a hairless variety like Sangiovese Grosso. In the future it would be possible to verify if minimal releases, as conducted in 2008, will allow an establishment of the phytoseiid in sufficient numbers to achieve long-term tetranychid control. These field results are in contrast with laboratory observations and, in some way, also with previous field records. Among the species considered K. aberrans has the lowest rate of increase on tetranychids (Kasap, 2005) and, although E. carpini is acceptable as food, attempts to rear the predator with this prey only were until now unsuccessful (personal observations). On the other hand, T. exhilaratus, is one of the most common phytoseiids in Tuscany, where it showed a strong association with E. carpini (Castagnoli et al., 1991). Furthermore, laboratory data indicated that with this prey as food the phytoseiid exhibits high reproductive parameters (Castagnoli et al., 1989). In the field, however, it lowered tetranychid populations only with very high released numbers (>2000 specimens/plant) (Liguori et al., 2007). Neoseiulus californicus, a species with a much higher rate of increase, when compared with the other phytoseiids (Castagnoli & Simoni, 2004), shows high reproductive parameters with E. carpini as prey (personal observations). This predator probably needs higher release densities in order to become established on vines. 5

24 6 Acknowledgement We thank Arsia (Regione Toscana), Biondi Santi Tenuta Il Greppo (Montalcino), Az. Case Basse Soldera (Tavernelle), Podere Forte (Castiglione d'orcia), Podere Sante Marie (Montalcino), Azienda Agricola San Polino (Montalcino), Stella di Campalto Az. Agricola San Giuseppe (Castelnuovo dell'abate) for their support and collaboration. References Castagnoli, M. & Liguori, M. 1986: Ulteriori indagini sull'acarofauna della vite in Toscana. Redia 69: Castagnoli, M. & Liguori, M. 1994: Utilizzazione di polline nell allevamento massale di Typhlodromus exhilaratus Ragusa e Amblyseius californicus (McGregor) (Acari: Phytoseiidae). In: MAF, Convegno "Lotta Biologica", ed. Viggiani, G., Acireale 1991, Ist. Pat. Veg., Roma: Castagnoli, M. & Simoni, S. 2004: Neoseiulus californicus (McGregor) (Acari: Phytoseiidae): survey of biological and behavioural traits of a versatile predator. Redia 86: Castagnoli, M., Amato, F. & Monagheddu, M. 1989: Osservazioni biologiche e parametri demografici di Eotetranychus carpini (Oud.) (Acarina: Tetranychidae) e del suo predatore Typhlodromus exhilaratus Ragusa (Acarina: Phytoseiidae) in condizioni di laboratorio. Redia 72(2): Castagnoli, M., Liguori, M., Amato, F. & Guidi, S. 1991: Dinamica spaziale e temporale di Eotetranychus carpini (Oud.) (Acarina: Tetranychidae) e dei fitoseidi suoi predatori sulla vite. In: Atti XVI Congresso Nazionale Entomologia, Martina Franca (Ta), settembre 1991: Duso, C. 1997: Distribution, biology and management of important phytophagous mites on temperate fruits in Italy. Redia 80, Appendice: Duso, C. & Vettorazzo, E. 1999: Mite population dynamic on different grape varieties with or without phytoseiids released (Acari: Phytoseiidae). Exp. Appl. Acarol 23: 741. Duso, C., Pasqualetto, C. & Camporese, P. 1991: Role of the predatory mites Amblyseius aberrans (Oud.), Typhlodromus pyri Scheuten and Amblyseius andersoni (Chant) (Acari: Phytoseiidae) in vineyards. II Minimum releases of A aberrans and T pyri to control spider mite populations (Acari, Tetranychidae). J. Appl. Entomol. 112: Duso, C., Angeli, G., Castagnoli, M., Facchin, P., Liguori, M., Malagnini, V. & Pozzebon, A. 2007: Pesticides and Phytoseiid mites: a synopsis of research carried out on grapes, apples and vegetable in northern and central Italy. In: Acarology XI. Proceeding of the International Congress, eds. Morales-Malcaras, J.B., Beham-pelletieer, V., Ueckermann, E., Perez, T.M. and Estrada-Venega, E.G., Badii M.: Kasap, I. 2005: Life-history traits of the predaceous mite Kampimodromus aberrans (Oudemans) (Acarina: Phytoseiidae) on four different types of food. Biol. Control 35: Kreiter, S., Tixier, M.-S., Auger, P., Muckensturm, N., Sentenac, G., Doublet, B. & Weber, M. 2000: Phytoseiid mites of vineyards in France (Acari:. Phytoseiidae). Acarologia 41: Kondo, A. 2004: Colonizing characteristics of two phytoseiid mites, Phytoseiulus persimilis Athias-Henriot and Neoseiulus womersleyi (Schicha) (Acari: Phytoseiidae) on greenhouse grapevine and effects of their release on the kanzawa spider mite, Tetranychus kanzawai Kishida (Acari: Tetranychidae). Appl. Entomol. Zool. 39:

25 Liguori, M. & Castagnoli, M : Association d'acariens sur la vigne en Toscane: répartition et fluctuation des populations sur les feuilles, les écorces et les herbs au pied des ceps. In: Influence of environmental factors on the control of grape pests, diseases and weeds, ed. Cavalloro, R., Proc. EC Experts Group Meeting, Thessaloniki, Greece, 6-8 October Balkema A A, Rotterdam/Brookfield: Liguori, M. Sabbatini Peverieri, G., Simoni, S. & Ferré, L. 2007: Biological control in vineyards by means of a laboratory phytoseiid strain: a small scale experiment in Tuscany (Italy). IOBC/wprs Bulletin 30(5): SPSS, Inc SPSS for Windows, v. 9.0 Chicago, Ill 7

26 Integrated Control of Plant-Feeding Mites IOBC/wprs Bulletin Vol. 50, 2009 p. 8 Application of pollen for promotion of predatory mite populations in protected basil Einat Adar 1,2, Moshe Inbar 1, Eric Palevsky 2 1 University of Haifa, Dept. of Evolutionary & Environmental Biology, Haifa, Israel 2 Dept. of Entomology, Agricultural Research Organization (ARO), Israel Abstract: It is well known that pollen is a natural supplemental food source for many acarine biological control agents (ABAs); it is also known that in some cases pollen applications may augment populations of predatory mites and thus increase their ability to control pests. Our goal is to develop the methodology for the creation of a standing army of predatory mites, which will protect basil from insect and acarine pests. We will study two omnivorous mites (Amblyseius swirskii and Euseius scutalis) in basil crops and assess the effects that supplemental pollen has on: A) Survival of the mites on the crop with or without pests; B) The ability of the mites to control pests such as broad mites, thrips and whiteflies; C) Intraguild interactions (between the omnivorous mites). We will work in three spatial scales. Under controlled conditions in potted plants in a walk-in growth chamber, in caged planters in screen houses under ambient conditions and in agricultural systems. We aim to determine the frequency and application rates of pollen in order to produce an efficient ABA based solution for basil cultivars. Preliminary results of a screen house study indicate that A. swirskii populations tend to increase when pollen is applied every fortnight. Key words: ABA, Amblyseius swirskii, basil, Euseius scutalis, pest control, pollen 8

27 Integrated Control of Plant-Feeding Mites IOBC/wprs Bulletin Vol. 50, 2009 p. 9 Integrated control of bulb-scale mite (Steneotarsonemus laticeps) in Narcissus Rosemary Collier 1, Gordon Hanks 1, Malcolm Millar 2 1 Warwick HRI, The University of Warwick, Wellesbourne, Warwick, CV35 9EF UK; 2 ADAS UK Ltd, Woodthorne, Wergs Road, Wolverhampton, WV6 8TQ UK Abstract: About 4,000 ha of Narcissus are field-grown in the UK, producing an annual saleable output of about 30,000t bulbs and 600m cut-flowers, of which perhaps 30% of bulbs and 40% of flowers are exported. Of three important pests that infest Narcissus from time to time, bulb-scale mite (Steneotarsonemus laticeps (Halbert)) has received least attention to date. While symptoms due to S. laticeps rarely cause concern in field-grown bulbs or in storage, temperatures in glasshouses, where Narcissus bulbs are forced for cut-flowers and grown as potplants, favour rapid pest multiplication, resulting in damaged, distorted leaves and stems. There are no approved acaricides to control S. laticeps in glasshouse Narcissus, or when bulbs are stored, and other than hot-water treatment, there is no non-chemical means of control. The aim of our project is to develop an integrated control strategy for S. laticeps based on an understanding of its biology and ecology. It is a collaborative project between the UK government and the horticultural industry and the project consortium includes a number of UK Narcissus growers. The project has several specific objectives. The first is to determine the relationship between the development of S. laticeps infestations and temperatures, in order to define the conditions that most favour mite development and reproduction, and to determine whether very low or very high temperatures cause mite mortality. A further objective is to discover how S. laticeps originates and spreads in field crops and in bulb storage and thereby determine how infestations move from crop to crop. Mites may move from bulb to bulb by themselves, either in the field or when harvested bulbs are stored, or they may be transported passively, for example, by winds or by other animals (e.g. insects such as the large narcissus fly (Merodon equestris)). We are examining a number of physical and chemical approaches to mite control and these include the use of acaricides and high- or low-temperature treatments. Although extreme temperatures may kill mites, it is important that the bulbs themselves are unaffected and that their quality is not impaired. We are also considering the options for biological control. We hope to provide Narcissus growers with an effective integrated strategy for control of S. laticeps that will have minimal impact on the environment. Acknowledgements We thank consortium members, including the Horticultural Development Company and the UK Department for Environment, Food and Rural Affairs, for supporting this project. 9

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29 Integrated Control of Plant-Feeding Mites IOBC/wprs Bulletin Vol. 50, 2009 pp Resistance in Carica papaya L. Cv. Maradol to the mite Eotetranychus lewisi (McGregor) induced by the herbivory of Estigmene acrea (Drury) Martha E. de Coss 1, Alexander E. Reyes 1, Mario E. Cabrera 1, Rodolfo Flores 1, Leopoldo Cruz 2 1 Universidad Autónoma de Chiapas, Facultad de Ciencias Agrícolas, C.P Huehuetán, Chiapas, México; 2 El Colegio de la Frontera Sur, C.P Tapachula, Chiapas, México Abstract: In this study, the herbivory of Estigmene acrea (Lepidoptera: Arctiidae) was used to demonstrate induction of resistance in papaya plants to Eotetranychus lewisi. The treatments consisted of (1) plants damaged by E. acrea larvae and infested with E. lewisi (CDL), (2) plants without damage of E. acrea larvae but infested with E. lewisi (SDL), and (3) healthy plants (control). The experiment included three phenological growth stages (1= 3 leaves, 2= 5 leaves, 3= 7 leaves) of papaya. The number of the different mite stages, the phenological variables, and the quantity of volatile compounds were recorded for each treatment. Phenological stage 1 showed a lesser number of mites in comparison to the other stages. Eotetranychus lewisi nymphs were the stage more affected by plant resistance. The leaf area, the stem diameter and the number of leaves were greater in the treatment CDL than in the control. The volatiles were sampled using dynamic headspace and solid phase microextraction techniques, and analyzed by gas chromatography-mass spectrometry. The volatiles identified were: 1,3, dichlorobenzene, alcohol-benzyl, 2-nonen-1-ol, benzyl isocyanate, benzyl nitrile, cyclodecanol, 2,3-dichloro anisole, benzyl isothiocyanate. Key words: induced-resistance, papaya, volatiles, Eotetranychus lewisi, Estigmene acraea, herbivory Introduction After Brazil, Mexico is the second papaya world producer, and the first exporter of this fruit worldwide (FAO, 2007). However, with few sound IPM tactics available, Mexican papaya farmers completely depend on agrochemicals for controlling pests affecting this crop. Previous studies in papaya have found that the release of benzyl isothiocyanate is induced by the herbivory of Estigmene acrea (Malavasi et al., 2004), possibly implying that this compound may play an important role in the plant's defenses against herbivores. The objective of our study was to determine whether the herbivory of E. acrea and the consequent release of allelochemicals could enhance the resistance of papaya plants to Eotetranychus lewisi. Material and methods Experimental conditions The rearing of the herbivores (E. acrea larvae and mites) and the bioassays were performed in climatic chambers at 28±1 C, 67.5±2.5% RH, with a photoperiod of 13:11 (L: D) h. There were three treatments, consisting of (1) plants damaged by E. acrea larvae and infested with mites (CDL), (2) plants without E. acrea larval damage but infested with E. lewisi (SDL), and 11

30 12 (3) healthy plants (controls). Two third-instar larvae of E. acrea were placed on the plants' apical leaves for two hours; the larvae were then removed and five females and one male of E. lewisi placed on the plants. The papayas were sampled during three phenological growth stages (3, 5, and 7 true leaves), until they were 9-wk old. The number of the different mite stages, the plant growth stages, and the quantity of volatiles compounds were recorded for each treatment. There were twelve replicates per treatment, comprising a total of 108 plants used in the experiment. The volatiles of the experimental papaya plants during the phenological stage 1 (i.e,. plants with 3 true leaves) were sampled using dynamic headpace and solid phase microextraction techniques, and analyzed by gas chromatography (Varian model CP-3800) coupled mass spectrometry (Saturn 2200) using a DB-5MS column (30 m x 0.25 mm i.d., film thickness of 0.5 µm). The oven temperatures were programmed from 50 C at 15 C per minute -1 to 280 C. The compounds were identified using the NIST version 2.0. Data were analyzed by a two-way analysis of variance of repeated measures using the plant growth stages (3, 5 and 7 true leaves) and treatment (CDL, SDL) as factors while the untreated control was used for comparing the phenological variables. Results and discussion The phenological stage of 3 true leaves showed significant differences in the mite population, in comparison to the populations in plant phenological stages of 5 and 7 true leaves. The interaction was significant for nymphs, plant phenological stages, presence of herbivores (CDL and SDL), and dates. The vegetative growth of the plants damaged by E. acrea followed by mite infestation was less than the growth of healthy plants (controls). The volatile compounds released by the papaya plants were identified as 1,3, dichlorobenzene, alcoholbenzyl, 2-nonen-1-ol, benzyl isocyanate, benzyl nitrile, cyclodecanol, 2,3-dichloro anisole, benzyl isothiocyanate. In this study, an induction of resistance of papaya plants to mite nymphs was shown to occur during the first half of the experiment, within the physiological stage of 3 true leaves. Of the compounds identified, benzyl isothiocyanate increased highly in the plants damaged by E. acrea. Further studies are needed to clarify the effect of early herbivory on the production of allelochemicals and their effect on other herbivores. Acknowledgements We thank Julio Rojas for comments on an earlier draft of the manuscript and Armando Virgen for advice on rearing E. acrea. This work was supported by El Consejo de Ciencia y Tecnologia de Chiapas (FOMIX-CHIS-2005-C03). References FAO, FAOSTAT: Food and Agriculture Organization of the United Nations. Malavasi, A., Uramoto, K. & do Nascimento, A. 2004: Latex exudates of papaya as fruit fly oviposition deterrence factor. 5 th Meeting of the Working Group on Fruits Flies of the Western Hemisfere. Ft. Lauderdale, Florida, USA. May (Abstract).

31 Integrated Control of Plant-Feeding Mites IOBC/wprs Bulletin Vol. 50, 2009 pp Relationships between plant pathogenic fungi and mites in vineyards: implications for IPM Carlo Duso, Alberto Pozzebon, Paola Tirello, Mauro Lorenzon, Diego Fornasiero Department of Environmental Agronomy and Crop Science, University of Padua, Agripolis, Legnaro, Padova, Italy Abstract: In this paper we summarize the results of studies aimed at investigating the relationships between fungal diseases and mites occurring in European vineyards. Most of the data originated from observations carried out in commercial and experimental vineyards in north-eastern Italy. Grapevine downy mildew, Plasmopara viticola, and grape powdery mildew, Uncinula necator, are the most significant grape diseases in several viticultural areas in Europe and throughout the world. The spread of downy mildew in European vineyards may increase the abundance of some species of Phytoseiidae and Tydeidae. Amblyseius andersoni responded clearly to the spread of downy mildew symptoms, an effect also observed, but at lower magnitudes, for Typhlodromus pyri and Kampimodromus aberrans. The beneficial effect of downy mildew on the survival, development and reproduction of phytoseiids and tydeids has a clear impact on their population dynamics. Downy mildew effects varied among phytoseiids, being more relevant for A. andersoni than for T. pyri. These interactions may have implications for IPM because T. pyri is more effective than A. andersoni in controlling phytophagous mites in vineyards. The role of powdery mildew as a food source for A. andersoni and T. pyri was less pronounced than that of downy mildew. The capacity of generalist predatory mites to persist in perennial ecosystems contributes to the successful biological control of phytophagous mites. In vineyards, the persistence of generalist predators in the absence of prey may be improved by their feeding on various food sources. Pollen is probably the most important food source in spring and early summer, whereas mildews increase in importance in late summer. Predatory mite persistence is largely affected by pesticide use. The results of our studies showed that downy mildew availability mediates the effects of fungicides on predatory mites because it represents an alternative food for them. Moreover, downy mildew can enhance the recovery of predatory mite populations after pesticide applications. Key words: Phytoseiidae, Tetranychidae, Tydeidae, grape, Plasmopara viticola, Uncinula necator, biological control Introduction The interactions of arthropods with plant pathogenic fungi in European vineyards have some implications for Integrated Pest Management (IPM). A number of pests increase the spread of fungal diseases, which then require additional fungicide applications. Grape berry moths that feed on bunches can increase the phytopathogenic potential of Botrytis bunch rot (Botrytis cinerea Persoon). Grape phylloxera infesting roots is associated with various forms of damage including those caused by soil-borne pathogens (e.g. Fusarium spp.). The activity of Bostrichidae (Coleoptera) is suspected to favour the spread of wood diseases. Mealybugs and coccids damaging to grapes produce a large amount of honeydew that serves as a substrate for sooty mould fungi, such as Cladosporium herbarum (Pers. ex Fr.) Link. Little is known about the potential role of arthropods in reducing the impact of fungal diseases on grapes. The grape downy mildew, Plasmopara viticola (Berk. & Curtis ex de 13

32 14 Bary) Berlese & De Toni, and the grape powdery mildew, Uncinula necator (Schwein) Burrill, are the most significant grape diseases in several viticultural areas in Europe and throughout the world. Interactions between mildews and insects have been poorly investigated. A number of predators belonging to the Diptera (e.g. Cecidomyiidae) and Thysanoptera (e.g. Haplothrips spp.) are attracted by mildew foliar symptoms but the nature of these relationships requires to be studied (Duso, unpubl. data). More information is available regarding interactions between mildews and mites. Relationships between powdery mildew and Tydeidae have been investigated in North America (English-Loeb et al., 1999; 2005). Orthotydeus lambi (Baker) effectively suppressed the development of powdery mildew on the wild riverbank grape, Vitis riparia Michx. Moreover, English-Loeb et al. (2007) demonstrated the potential of tydeid mites in successfully controlling powdery mildew in IPM vineyards. The activity of tydeids in reducing fungal incidence was mostly seen on leaves, and lowering the potential of fungal inoculum on leaves reduced its incidence on fruits (Melidossian et al., 2005). The magnitude of powdery mildew suppression by O. lambi varied among grape genotypes. Leaf architecture traits appeared to have an important role in mediating interactions among grapevines, fungal pathogen and mycophagous mites (Norton et al., 2000; English-Loeb et al., 2005). The spread of downy mildew in European vineyards can increase the abundance of some species of the Phytoseiidae (Duso et al., 2003), and the Tydeidae (Duso et al., 2005a). As these mites may have a role in controlling phytophagous mites, interest in their relationships with plant pathogenic fungi has rapidly increased. In this paper we summarize the results of studies aimed at investigating the relationships between fungal diseases and mites occurring in European vineyards. Most of the data originated from observations carried out in commercial and experimental vineyards in north-eastern Italy. Laboratory studies were conducted to ascertain the effect of downy mildew on the development and reproduction of a number of mite species. A limited number of studies involved powdery mildew in order to investigate its role as an alternative food for generalist phytoseiids. The role of mildews in altering the effects of pesticides on mite communities has been reported. Potential implications of mite-fungi relationships for IPM are discussed. Initial evidence of a relationship between downy mildew spread and seasonal mite abundance Preliminary observations were conducted in a commercial vineyard located in north-eastern Italy (Veneto region). In this vineyard the phytoseiids Amblyseius andersoni (Chant) and Typhlodromus pyri Scheuten were frequently observed, and were more common than Kampimodromus aberrans (Oudemans) and Paraseiulus talbii (Athias-Henriot). Tydeus caudatus Dugès was dominant among tydeids. The pest mites Panonychus ulmi (Koch) and Colomerus vitis (Pagenstecher) were seldom detected. This vineyard consisted of different cultivars but the data obtained from the Prosecco and Cabernet Franc cultivars were the most interesting. Observations were conducted there from 1999 to 2003 (Duso et al., 2003; 2005a; 2005b). Leaf samples were removed every 14 days and examined to assess downy mildew incidence (percentage of leaves and average leaf surface with symptoms) and mite densities. Most pesticides used were selective to phytoseiids. When observations started, T. pyri was dominant over A. andersoni and K. aberrans (Figure 1). In September, A. andersoni became more abundant than the remaining species, concurrent with the spread of downy mildew symptoms on leaves. The same trend was observed in 2000 and 2002, when the incidence of downy mildew was relatively high (Figure 1). In contrast, A. andersoni remained at lower levels when downy mildew infections were moderate to low (2001 and 2003). In the late summer of three out of five seasons, populations

33 15 of A. andersoni were significantly higher (p< 0.01) on leaves with downy mildew symptoms than on leaves without symptoms. Regarding T. pyri, similar differences (p< 0.01) were reported on a few dates in 2000 and The densities of A. andersoni were positively correlated with the extent of symptoms, whereas this correlation was lower for T. pyri. The spread of downy mildew symptoms in certain seasons also affected tydeid populations, with some variations between the cultivars considered. Tydeus caudatus reached relatively high densities in 1999 and 2000 whereas lower numbers were detected in 2003, when downy mildew incidence was negligible (Figure 1). In the seasons characterised by a high downy mildew incidence, P. talbii also increased in numbers, confirming its preference for tydeids (Camporese and Duso, 1995). Populations of T. caudatus were significantly higher (p< 0.01) on leaves with symptoms than on leaves without downy mildew during various dates in 1999, 2000 and Regarding P. talbii, this trend was seen in a few samplings in Densities of T. caudatus were often positively correlated with the extent of downy mildew symptoms, but a similar relationship was seldom found for P. talbii. Further evidence of downy mildew effects on A. andersoni and T. caudatus A field experiment was conducted to confirm the effect of downy mildew on A. andersoni and T. caudatus populations in vineyards (Duso et al., 2003; 2005a). In a randomized block trial, a number of plots were treated with the fungicide folpet (known to be selective to phytoseiids) to avoid the spread of downy mildew symptoms onto leaves. Additional vine plots were left untreated with fungicides as controls. Leaf samples were examined during the season to assess the incidence of downy mildew symptoms and of mite densities. Severe downy mildew infections were detected in early summer of the experimental growing season (Figure 2) with significant differences (p< 0.01) between the control and folpet plots. Amblyseius andersoni was dominant among phytoseiids and T. caudatus among tydeids. Their densities increased in the control plots, corresponding to downy mildew spread (Figure 2), with significant differences (p<0.01) when compared to the folpet plots. Panonychus ulmi was also detected at lower densities (p<0.01) in the control plots. Downy mildew can affect T. pyri and K. aberrans populations A similar experiment was conducted in a vineyard colonized by T. pyri and K. aberrans (Duso et al., 2003; 2005b). It consisted of a randomized block trial in which untreated plots, or plots treated with copper fungicides (considered selective to phytoseiids), were monitored during a growing season. In the controls downy mildew showed dramatic effects from late spring onwards (Figure 3). The extent of symptoms was much lower (p< 0.01) in fungicide treated plots. Typhlodromus pyri and K. aberrans numbers increased in June (Figure 3), the numbers of the former being higher (p< 0.01) in the controls than in the fungicide treated plots. The seasonal abundance of K. aberrans showed a similar pattern. Grape downy mildew and Tydeus californicus Tydeus californicus is another common tydeid species in south-european vineyards (Castagnoli, 1989; Liguori et al., 2002). It was largely dominant amongst the Tydeidae in another experimental vineyard. During a growing season, its abundance was monitored in plots treated with folpet and in untreated plots. The proportion of leaves with downy mildew symptoms exceeded 70% in June in the control, being much lower in folpet plots (p< 0.01). In the controls T. californicus densities increased in early summer following the spread of downy mildew symptoms and the tydeids were more abundant in the controls than in folpet plots (p< 0.01) (Pozzebon et al., unpubl. data).

34 Figure 1. Mite population dynamics and grape downy mildew foliar symptoms observed in a commercial vineyard during growing seasons 16

35 Figure 2. Mite population dynamics and grape downy mildew foliar symptoms observed in an experimental vineyard. Vine plots were treated with the selective fungicide folpet or left untreated (controls). 17

36 Figure 3. Mite population dynamics and grape downy mildew foliar symptoms observed in an experimental vineyard. Vine plots were treated with copper fungicides, selective to predatory mites, or left untreated (controls). 18

37 19 Detection of downy mildew GPI in mites and its consumption Isoelectrofocusing (IEF) analyses were conducted on single individual mites to detect the presence of downy mildew glucose-phosphate isomerase (GPI) in species potentially interacting with downy mildew. In preliminary experiments a number of A. andersoni or T. pyri females were collected from leaves with downy mildew symptoms and surface-sterilized in a sodium hypochlorite solution before performing IEF analyses. In additional experiments these analyses were also performed with P. ulmi, T. caudatus and P. talbii. IEF analyses showed a stain corresponding to that of downy mildew, in addition to the intrinsic phytoseiid stains, in most A. andersoni (97.5%) and of T. pyri (87.5%) females collected from symptomatic leaves. No specific stains for P. ulmi were detected in these analyses (Duso et al., 2003). A high proportion (82%) of T. caudatus females collected from infected leaves proved to be IEF positive. The percentage of P. talbii females collected in similar situations that were IEF positive reached 37% (Duso et al., 2005a). More recent investigations conducted with K. aberrans and T. californicus females showed a significant number of both species, collected from symptomatic leaves, to be IEF positive (Duso et al., unpubl. data). Experiments on downy mildew consumption were initially conducted with A. andersoni and T. pyri. Their females were reared with pollen and then confined onto leaves showing downy mildew symptoms for 1, 4, or 11 h. The same number of mites was confined on leaves without symptoms for the same periods. The incidence of A. andersoni and T. pyri females IEF positive increased in correspondence with the longest time periods (40/40 and 38/40 after 11 h). No downy mildew stains were detected in predatory mites confined on leaves without symptoms, nor in P. ulmi females placed on symptomatic leaves (Duso et al., 2003). Additional experiments conducted with T. caudatus females, using the same procedures, indicated that the proportion of IEF positive T. caudatus females increased over time (Duso et al., 2005a). Regarding P. talbii, its females fed on tydeids (collected from elders) confined on symptomatic grape leaves with no prey, but none were IEF positive. In another experiment the percentage of positive P. talbii females reached 75% when they were fed with T. caudatus that had originated from symptomatic grape leaves. A significant proportion (70%) of the P. talbii females fed on T. caudatus, which had been reared on pollen and then transferred onto symptomatic leaves was positive (Duso et al., 2005a). The effect of downy mildew and powdery mildew on phytoseiid development and reproduction Laboratory studies were conducted to determine if downy mildew can be considered an alternative food for A. andersoni and T. pyri (sensu Overmeer, 1985). Mite eggs were isolated on grape leaf discs with downy mildew sporangia, with pollen or without any food. Each egg was monitored throughout its development to adult. One male and one female were later placed on single discs, and fed on the same food sources, to assess oviposition. Life history parameters calculated for predatory mites reared on downy mildew infected leaves were compared with those of mites fed on pollen (Pozzebon and Duso, 2008). Typhlodromus pyri females reared on downy mildew-infected discs had longer developmental times and a lower fecundity than those reared on discs with pollen. Food sources thus had significant effects on life-table parameters: T. pyri females fed on pollen had higher r m, R 0 and λ values, but lower D t and T than those reared on downy mildew. Regarding A. andersoni, the food source affected neither development nor longevity, but females reared on pollen had a higher fecundity than those reared on downy mildew. Rearing A. andersoni on pollen resulted in higher r m, R 0, λ, and lower D t values than when reared on downy mildew, whereas mean generation time was not influenced by the food source.

38 20 In another experiment mite eggs were confined on grape leaf discs and powdery mildew mycelium, pollen and motile stages of Tetranychus urticae Koch were offered as food sources. Grape leaf discs without any food source were the controls. A longer developmental time for A. andersoni and T. pyri females was observed when they fed on the fungus, when compared to those feeding on T. urticae or on pollen. No differences were observed between T. urticae and pollen as food. Predatory mites did not reproduce when reared on powdery mildew (Pozzebon et al., 2009). The effect of downy mildew on tydeid development and reproduction Laboratory experiments were conducted to determine the effects of downy mildew on the development and reproduction of T. caudatus and of T. californicus (Lorenzon, 2007). Mites were reared on grape leaf discs with downy mildew sporangia, on leaf discs provided with pollen of Papaver rhoeas L. or on leaf discs without any food. Tydeids did not develop on the latter discs. The time needed to develop from larva to larva was similar when offered downy mildew or P. rhoeas pollen, nor was fecundity influenced by these foods. Downy mildew and pollen thus seem to have a similar impact on the demographic parameters of these tydeids. Downy mildew mediates the effects of pesticides on phytoseiids Pesticide side-effects on phytoseiids can be evaluated in the laboratory or in the field. In the EC regulatory processes the latter test procedures are necessary when a pesticide proves to be toxic in laboratory trials (Blümel et al., 2000). Field test procedures can be applied to a large number of natural enemies and are more realistic than laboratory procedures, providing information useful for delineating the ecotoxicological profile of a pesticide. The effect of a certain pesticide on predatory mites is expressed by the reduction in population size in treated plots as compared to control plots, represented (in the present case) by untreated vines. However, when fungicides are evaluated, vines not treated with these compounds may be infected by plant pathogenic fungi that are under control in treated vines. Since a number of predatory mites develop and reproduce on downy mildew, differences between the control and the treated plots can be affected by downy mildew levels. In other words, downy mildew availability could mediate the impact of pesticides on predatory mites. The results of field experiments conducted on this topic are summarized herewith. Amblyseius andersoni and T. pyri densities on untreated (control) and fungicide (copper hydroxide and Bordeaux mixture) treated plots were compared for two growing seasons. Fungicide effects were evaluated by considering two different periods: a) the fungicide application period plus one month following IOBC procedures (Blümel et al., 2000); b) the subsequent growing season period. During the fungicide evaluation period of the first year, phytoseiid densities fluctuated at similar levels among treatments. In contrast, in the second period, A. andersoni numbers were significantly higher (p<0.01) in the controls than in Bordeaux mixture plots. Higher T. pyri densities were observed in the controls when compared to the two fungicide treated plots (p< 0.05). Downy mildew foliar symptoms were not detected in the first evaluation period, but were more common (p<0.01) in the controls than in Bordeaux mixture plots in the second period. One year later, T. pyri was largely dominant among phytoseiids. During the first evaluation period, its densities were higher (p<0.05) in the controls than in fungicide treatments. An insecticide treatment applied in late July dramatically reduced the predatory mite densities. No differences were observed in the second period. Higher levels of downy mildew foliar symptoms were recorded in the controls than in the fungicide treated plots in both evaluation periods (for all comparisons: p<0.05).

39 21 In the first year, copper hydroxide and Bordeaux mixture did not appear to be detrimental to predatory mites, confirming literature data for copper based fungicides (Ivancich Gambaro, 1973; Duso et al., 1983). However, one year later these fungicides were associated with lower predatory mite numbers when compared to the controls. These differences are probably associated with the differences in downy mildew incidence. Moreover, downy mildew favoured the re-colonization of phytoseiids during late summer of the first season. Fungicides, downy mildew and biological control of tetranychids Interactions between downy mildew and mites were studied in an additional experimental vineyard during a growing season characterized by high downy mildew incidence. Previous observations had shown that A. andersoni dominated over T. pyri; P. ulmi and T. californicus were also seen. Mite seasonal dynamics were compared amongst plots treated with different fungicides (folpet, copper hydroxide or mancozeb) and untreated plots. Among the fungicides considered, folpet and copper hydroxide are selective to phytoseiids whereas the effects of mancozeb depend on the predatory mite strains and on their history of exposure to pesticides (Duso et al., 1983; Angeli and Ioriatti, 1994; Pozzebon et al., 2002; Auger et al., 2004a; 2004b). Experimental procedures and data analyses were similar to those reported above. Predatory mite population densities during the first assessment period (fungicide application plus one month) were higher in the controls than in the fungicide treated plots, with similar levels among fungicides. Similar trends were observed for the incidence of downy mildew symptoms. Tetranychid numbers fluctuated at similar levels among treatments. In the subsequent assessment period, severe defoliation affected the control vines. No differences were therefore seen among treatments, neither for predatory mites nor for downy mildew incidence. During the same period P. ulmi reached higher levels (p< 0.05) in the fungicide treated plots than in the controls. Discussion Plant pathogens can alter the growth of spider mite populations, sometimes favouring the latter (Karban et al., 1987). It has been suggested that plant pathogenic fungi could: a) reduce plant defences making the leaf nutrients more accessible to the mites, and/or b) represent a source of food for spider mites (Belczewski and Harmsen, 2000). We did not observe any direct effect of downy mildew on P. ulmi, the most common tetranychid mite in European vineyards. Isoelectrofocusing analyses failed to reveal downy mildew stains in P. ulmi females removed from infected leaves, whereas such stains were detected in phytoseiid and tydeid individuals collected in similar conditions. Nevertheless, in some trials P. ulmi populations reached lower levels in plots with high downy mildew symptoms as compared to those with low downy mildew incidence. This effect was most likely due to an increased phytoseiid population density favoured by downy mildew. Mycophagy is a well-known characteristic of the Tydeidae (Krantz and Lindquist, 1979; Mendel and Gerson, 1982; Knop and Hoy, 1983; Hessein and Perring, 1986; English-Loeb et al., 1999) but the impact of fungi on tydeid demographic parameters has seldom been investigated (e.g. McCoy et al., 1969). Tydeids occurring in European vineyards were positively affected by downy mildew. Tydeus caudatus and T. californicus developed and reproduced when reared on leaves with downy mildew, whose mycelia represent a food source that is comparable to pollen but remains available for a longer time. The seasonal abundance of tydeid populations is often characterised by an increase in late summer when downy mildew incidence is moderate to high. The population increase of tydeids in vineyards

40 22 with a high incidence of downy mildew favours the predatory P. talbii. This species, which is specialized on tydeids, occasionally feeds on tetranychids and on eriophyids (Camporese and Duso, 1995). The colonization of vineyards by P. talbii has therefore no significant implications for the control of phytophagous mites. Tydeids occurring in European vineyards prey on eriophyid mites (Schruft, 1972; Duso and de Lillo, 1996; Niemczyk, 2002). Tydeus caudatus was observed to overwinter in association with colonies of C. vitis (Camporese and Duso, 1995) and the predation of T. caudatus upon C. vitis has recently been studied (Lorenzon et al., unpublished data). The impact of tydeids on eriophyids populations requires an in-depth study in order to evaluate the potential role of downy mildew in enhancing tydeid numbers in late season and consequent overwintering populations. A higher density of overwintered tydeids at the sprouting period could alleviate problems caused by eriophyids at this phase of the growing season. Tydeids control powdery mildew on wild and cultivated grapes in North America, opening new perspectives for biological control (English-Loeb et al., 1999; Norton et al., 2000). To our knowledge, similar studies have not yet been conducted in Europe, despite the potential implications of this phenomenon for southern viticultural regions. As the downy mildew cycle comprises an endophytic phase, the impact of tydeids on this pathogen would be less relevant than their impact on powdery mildew. Some authors demonstrated a role of plant pathogenic fungi for phytoseiid survival and development (Chant, 1959; Daftari, 1979; Zemek and Prenerova, 1997), whereas development and reproduction on fungi has less frequently been reported (Kropczynska- Linkiewicz, 1971; Bakker and Klein, 1992; Bakker, 1993). McMurtry and Croft (1997) in their review stated that no close associations are known to exist between generalist phytoseiids and fungi. In our studies, A. andersoni clearly responded to the spread of downy mildew symptoms. This effect was observed with a lower magnitude for T. pyri and for K. aberrans. Downy mildew consumption was shown first by using IEF, then by rearing predatory mites only on downy mildew-infected leaves. The effect of downy mildew on the survival, development and reproduction of predatory mites can partly explain its impact on phytoseiid populations. Laboratory data suggest that the intrinsic rates of increase of A. andersoni and T. pyri reared on downy mildew are lower than those calculated for predators fed on P. ulmi (Dicke et al., 1990; Pozzebon and Duso, 2008). Downy mildew effects varied among phytoseiids, being most relevant for A. andersoni. This predator occurs in north-eastern Italian vineyards in significant numbers during spring and late summer, and downy mildew is probably a major factor affecting this trend. Its numbers increase in late summer when infections spread, persist in autumn on infected leaves and then overwinter on these vines. Grape cultivars characterized by smooth lower leaf surfaces are frequently dominated by A. andersoni, and downy mildew is an additional factor in strengthening the status of this species. Downy mildew can exert similar effects on T. pyri, which requires pubescent leaves if it is to persist and build up significant populations (Camporese and Duso, 1996). In the commercial vineyards considered herein, the leaf morphology of cultivars, whose lower leaf surfaces are moderately to very pubescent, and the incidence of downy mildew, allows A. andersoni and T. pyri to coexist. Their different population growth patterns on downy mildew (Pozzebon and Duso, 2008), combined with interspecific predation (Croft and Croft, 1996; Croft et al., 1996; Zhang and Croft, 1995) can explain the competitive displacement of T. pyri by A. andersoni in this vineyard. However, in seasons characterised by negligible downy mildew incidence, A. andersoni densities declined whereas those of T. pyri persisted better. These interactions affect IPM, because T. pyri is more effective than A. andersoni in controlling phytophagous mites in vineyards (Duso, 1989;

41 23 Girolami et al., 1992; Duso and Vettorazzo, 1999). It should be stressed that the importance of A. andersoni in vineyards is due more to the spread of pesticide resistant strains (e.g. Ioriatti and Baillod, 1985; Duso et al., 1992) than to effective biocontrol exerted by this species. On the other hand, among generalist phytoseiids, only A. andersoni [and to a lesser extent Euseius finlandicus (Oudemans)] seems to be able to build up significant populations on grape cultivars characterised by smooth lower leaf surfaces. The impact of powdery mildew on phytoseiids has less often been investigated. We found that A. andersoni and T. pyri completed their development on leaf discs infected by powdery mildew, but failed to oviposit (Pozzebon et al., 2009). The real importance of powdery mildew for generalist predatory mites under field conditions requires ad hoc studies. Alternative foods, such as pollen or certain fungi, could reduce short-term predator pressure on prey (Wei and Walde, 1997; Zemek, 2005). Our data suggest that downy mildew does not distract predatory mites from controlling tetranychid populations, but additional studies are needed to clarify this important topic. It was reported that predators should prefer to forage on a more profitable food and switch to a less profitable food when the former is scarce (Murdoch, 1969; van Baalen et al., 2001). If the intrinsic rate of increase r m is considered to be a measure of nutritional value (Dicke et al., 1990), generalist predatory mites should switch to mildews at low prey densities, with clear implications for their persistence in vineyards. The capacity of generalists to persist in perennial ecosystems contributes to the successful biological control of phytophagous mites (Walde et al., 1992; Strong et al., 1997; Nyrop et al., 1998; Lester et al., 2005). In vineyards, the persistence of generalist predators in the absence of prey could be improved by feeding on various food sources. Pollen is probably the most important source during spring and early summer, but its availability declines in mid and late summer (Eichhorn and Hoos, 1990; Wiedner and Boller, 1990; Engel and Onhesorge, 1994; Duso et al., 1997). Downy mildew and powdery mildew are controlled by fungicides from vine sprouting to mid-summer. The economic importance of these pathogens declines in late summer, and they could therefore be managed with positive implications for tetranychid control in the short-term. Large numbers of phytoseiids may overwinter on infected vines and colonize the new vegetation in the following spring, with positive implications for the control of herbivorous mites and insects (e.g. thrips). Predatory mite persistence is largely affected by pesticide use. In European vineyards, the impact of fungicides on predatory mite populations is much stronger than that of insecticides. Most fungicides are applied to control mildews. The results of our studies show that downy mildew availability mediates the effects of fungicides on predatory mites, because it represents an alternative food for them. Moreover, downy mildew can enhance the recovery of predatory mites after pesticides are applied. Indirect effects, mediated by alternative food availability, should be considered when evaluating the side-effects of pesticides on predatory mites. Acknowledgements The authors wish to thank M. Borgo and D. Bellotto (CRA, Conegliano, Italy), E. Marchesini (Agrea, Verona, Italy), F. Bertoldi (University of Padua), for their support and assistance. This work has been supported mainly by grants of the University of Padua (ex-60%). References Angeli, G. & Ioriatti, C. 1994: Susceptibility of two strains of Amblyseius andersoni Chant (Acari: Phytoseiidae) to dithiocarbamate fungicides. Exp. Appl. Acarol. 16:

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47 Integrated Control of Plant-Feeding Mites IOBC/wprs Bulletin Vol. 50, 2009 pp Comparative effectiveness of Phytoseiulus persimilis and P. longipes in the control of Tetranychus urticae on strawberries and roses Hans Hoogerbrugge, Yvonne van Houten, Markus Knapp, Karel Bolckmans Koppert Biological Systems, Veilingweg 14, Postbus 155, 2650 AD Berkel en Rodenrijs, The Netherlands Abstract: The effectiveness of Phytoseiulus persimilis and Phytoseiulus longipes in the control of Tetranychus urticae on roses and strawberries was compared in small cage trials. Release of both predatory mite species led to a significant reduction of the spider mite population. The number of cumulative spider mite days was not significantly different between the two phytoseiid species. However, the population development during the experiment indicated that P. persimilis was able to control T. urticae slightly faster than P. longipes. Key words: Phytoseiulus longipes, Phytoseiulus persimilis, Tetranychus urticae, roses, strawberries Introduction The two-spotted spider mite, Tetranychus urticae Koch, is a key pest of strawberries and roses. The specialist spider mite predator Phytoseiulus persimilis Athias-Henriot has been used for the biological control of T. urticae on these crops for many years, however results are not always satisfactory. Phytoseiulus longipes Evans is closely related to P. persimilis and is also a specialized predator of web-producing tetranychid mites (Badii & McMurtry, 1983). Greenhouse strawberries and roses are grown in relatively dry environments. One major advantage of P. longipes, compared to P. persimilis, is that it is less susceptible to low relative humidities (Badii & McMurtry, 1984). In this study we compared the performance of two recently collected strains of P. longipes with P. persimilis against T. urticae on roses and strawberries in small cage experiments. The strain used on roses was collected in Chile and performed well with T. urticae as prey in laboratory experiments (Ferrero et al., 2008a). The strain used for the strawberry trial was collected in Argentina and has been shown to be a potentially effective predator of T. urticae and of Tetranychus evansi Baker & Pritchard on tomatoes in laboratory experiments (Ferrero et al., 2008b). Both strains of P. longipes are well adapted to low humidity conditions, as the critical relative humidity at which 50% of their eggs do not hatch (RH 50) at 25 C is around 45-50% (unpublished results). The RH 50 for the commercial Koppert strain of P. persimilis is 65%. Material and methods Mites The strain of P. longipes from Chile used on roses was reared on T. urticae on tomato leaves. The P. longipes strain from Argentina used in strawberry was reared on T. urticae on cucumber leaves. The P. persimilis were taken from the commercial product (SPIDEX, Koppert Biological Systems, The Netherlands). The spider mites used were obtained from a culture kept on beans at Koppert. 29

48 30 Strawberry experiment The experiment was carried out in 12 small cages (1.5 x 1 x 2 m) in an experimental greenhouse in June and July Two pots, each with 3 strawberry plants (var. Elsanta), were placed in each cage. No synthetic pesticides were applied before or during the experiment. The cages were randomly assigned to 3 treatments, P. persimilis, P. longipes or untreated control. On 26 th June, the plants were infested with 0.15 g T. urticae mixed with 12 g sawdust and equally spread over the plants. One week later, 10 female predatory mites per pot were released in the P. persimilis and P. longipes cages. A mite count on 7 leaflets per cage on the day before the predatory mite release showed that the spider mite population was similar in all cages. Mite density was afterwards assessed by randomly picking 15 leaflets per cage at weekly intervals until 31 st July and counting spider mites (motile stages) and predatory mites (all stages) in the laboratory under a stereo-microscope. The mean temperature in the cages was 22.8 C ( ); the mean relative humidity 66.8% ( ). Rose experiment The experiment was carried out in 4 small cages (2.5 x 1 x 2 m) in an experimental greenhouse between January and March Three rose plants (var. Illios) were placed in each cage on 23 rd January. The plants had been cut back completely in December 2007 and were placed in small containers with water and soap as a barrier to prevent contamination, and did not touch each other nor the screen of the cage. No synthetic pesticides were applied during the experiment. Each cage contained one replicate of each treatment, i.e. P. longipes, P. persimilis and an untreated control (4 replicates per treatment). The mean temperature in the cages was 20.9 C ( ); the mean relative humidity was 66.8% ( ). The plants were infested with 0.1 g T. urticae mixed with sawdust on 25 th January and again one week later. On 6 th February, 10 female predatory mites were released on the plants assigned to the P. longipes and P. persimilis treatments. In each cage the predatory mites were released on the 2 outer plants while the central plant served as the untreated control. Fifteen leaflets were randomly collected from each rose plant just before the predatory mite release (day 1) and on day 9, 17, 24, 31 and 37 after predatory mite release, and the spider mites (motile stages) and phytoseiid mites (all stages) were counted under a stereomicroscope in the laboratory. Statistics Cumulative mite days (CMD) were calculated according to: xi + xi + 1 * t t 2 where x i is the number of mites at sampling date i, x i+1 is the number of mites at sampling date i+1 and t is the number of days between the sampling dates (Park & Lee, 2005) and analysed by Kruskal-Wallis test using Minitab. Mean separation was performed with a Mann-Whitney test. Results and discussion Strawberries The T. urticae populations in the controls reached a maximum of 117 motile stages per leaflet 3 weeks after predatory mite release. Both predatory mite species kept the population below 24 mites per leaflet throughout the experiment and almost complete control was achieved at the end of the experiment (Figure 1).

49 31 T. urticae (motile stages)/leaflet weeks after predatory mite release 10 Untreated control P. persimilis P. longipes Phytoseiulus sp. (all stages)/leaflet weeks after predatory mite release Untreated control P. persimilis P. longipes Figure 1. Development of the spider mite (A) and predatory mite (B) populations in strawberries The number of cumulative spider mite days was significantly higher in the controls than in the two treatments with predatory mites (Table 1). The P. persimilis density increased very quickly after the release to a maximum of 6.3 mites per leaflet 2 weeks after release and thereafter declined, probably due to lack of prey. Phytoseiulus longipes reached its maximum density 3 weeks after the releases and its population declined rapidly thereafter (Figure 1). There was no significant difference in the number of cumulative phytoseiid mite days in both treatments (Table 1). Roses The T. urticae population increased much more rapidly in the untreated control than in the treatments with predatory mites. With P. persimilis, almost complete control was achieved. As in the strawberry experiment, the P. persimilis population increased faster than the P. longipes population and the spider mite population was lower on the P. persimilis plants than on the P. longipes plants at the end of the trial (Figure 2).

50 T. urticae (motile stages)/leaflet Days after predatory mite release Untreated control P. persimilis P. longipes Phytoseiulus sp. (all stages)/leaflet Days after predatory mite release Untreated control P. persimilis P. longipes Figure 2. Development of the spider mite (A) and predatory mite (B) populations on roses. This was also expressed in the number of cumulative spider mite days; however there was no significant difference between the two predatory mite treatments (Table 1). There was a slight contamination with predatory mites at the end of the experiments in both cases but this did not influence the results. In both experiments, P. persimilis performed better than P. longipes. Although differences in cumulative spider mite days were not significant, the spider mite density was lower in the P. persimilis plants than in the P. longipes plants at the last examinations, especially in roses. This was probably caused by the more rapid increase of the P. persimilis population after the release. The biology of these two predatory mites is very similar under standard laboratory conditions. Badii & McMurtry (1984) reported a slightly higher intrinsic rate of increase of P. persimilis (0.374) compared to P. longipes (0.366) at 25 C and 80 ± 7% relative humidity and with Tetranychus pacificus McGregor as prey, whereas Takahashi & Chant (1994) reported, to the contrary, that at 26 C and 80 ± 10% relative humidity, with the same prey, these values were P. persimilis: 0.428; P. longipes: The differences in performance on plants may therefore be caused by other mechanisms, for instance differences in dispersal ability. In these cage experiments, P. longipes had no advantage over P. persimilis in spider mite control on strawberries and roses. However, the experiments were carried out in winter and early

51 33 spring (roses), or early summer (strawberries) in the Netherlands. The low RH 50 of P. longipes and its good performance at temperatures above 30 C (Badii & McMurtry, 1984) indicate that it will probably perform better than P. persimilis under hot and dry conditions. This should be tested in experiments in areas with a hotter and drier climate. Furthermore, greenhouse experiments under production conditions need to be conducted before final conclusions can be made. Table 1. Mean cumulative mite days (CMD) ± standard error in the predatory mite treatments and controls Cumulative mite days (CMD) ± s.e. Strawberries Roses Treatments Control P. persimilis P. longipes T. urticae ± 24.0 a* ± 16.3 b ± 44.2 b Phytoseiulus sp. 3.8 ± 0.5 a 43.9 ± 7.7 b 31.2 ± 1.1 b T. urticae ± 19.0 a ± 28.5 b ± 58.8 b Phytoseiulus sp. 0.7± 0.5 a ± 34.7 b 43.5 ± 4.4 b * Values within rows followed by the same letters are not significantly different (Mann-Whitney test, P<0.05) References Badii, R.D. & McMurtry J.A. 1983: Effect of different foods on development, reproduction and survival of Phytoseiulus longipes (Acarina: Phytoseiidae). Entomophaga 28: Badii, R.D. & McMurtry J.A. 1984: Life history and life table parameters for Phytoseiulus longipes with comparative studies on P. persimilis and Typhlodromus occidentalis (Acari: Phytoseiidae). Acarologia 25: Ferrero, M., Kreiter, S. & Tixier, M.S. 2008a: Ability of Phytoseiulus longipes to control spider mite pests on tomato. In: Integrative Acarology. Proceedings of the 6 th European Congress, eds. Bertrand, Kreiter, McCoy, Migeon, Navajas, Tixier and Vial. European Association of Acarologists: Ferrero, M., Atuahiva, M., Saeed, M., Tixier, M.S. & Kreiter, S. 2008b: Éfficacité d un acarien pédateur, Phytoseiulus longipes Evans, pour le contrôle biologique en serres de l acarien rouge de la tomate, Tetranychus evansi Baker & Pritchard. In: AFPP 8ème Conférence Internationale Sur les Ravageurs en Agriculture, Montpellier, 22 et 23 Octobre 2008: Park, Y.L. & Lee, J.H. 2005: Impact of two-spotted spider mite (Acari: Tetranychidae) on growth and productivity of glasshouse cucumbers. J. Econ. Entomol. 98: Takahashi, F. & Chant, D.A. 1994: Adaptive strategies in the genus Phytoseiulus Evans. (Acari: Phytoseiidae). II. Survivorship and reproduction. Int. J. Acarol. 20:

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53 Integrated Control of Plant-Feeding Mites IOBC/wprs Bulletin Vol. 50, 2009 pp Effect of physiochemical features of different species or cultivars of host plants on the foraging behavior of Scolothrips longicornis Neda Kheradpir 1, Mohammadreza Rezapanah 2, Karim Kamali 1 and Yaghoub Fathipour 3 1 Dept. Entomology, Fac. Agriculture and Natural Resources, Islamic Azad University, Science and Research Branch, P.O. Box: , Tehran, Iran; 2 Dept. Biological Control Research, Plant Protection Research Institute of Iran, P.O. Box: , Tehran, Iran; 3 Dept. Entomology, Fac. Agriculture, Tarbiat Modares University, P.O. Box: Tehran, Iran. Abstract: There is increasing evidence that host plant features can be used as reliable indicators for the location behavior of natural enemies. The predaceous thrips Scolothrips longicornis Priesner was used in two release and recapture tests on different host plants, infested by spider mites and clean, and on various cultivars of cucumber, in order to identify its ability to discriminate host plants according to their features under greenhouse condition. The response of the predaceous thrips toward different plants was highly significant and the infested cucumber attracted the most predators; on the other hand, the responses of S. longicornis were similar towards eight tested cultivars of cucumber. It was concluded that the predator locates spider mite colonies by host plant signals and has the ability to recognize different host plant species, a finding that should be considered in IPM programs against spider mites when using this predaceous thrips. Key words: Scolothrips longicornis, preference, host plant, tetranychids Introduction Foraging behavior of biocontrol agents has a major effect on the occurrence and strength of direct or indirect interactions among members of a food web (Janssen et al., 1998; Janssen et al., 1999). Host plants play an important role in the natural enemies` performance, as the interactions between host plant and natural enemies are a key factor in pest management (Bottrell et al., 1998). Since the 1980's, new discoveries have revealed that plants infested by spider mites emit volatile info-chemicals that attract their natural enemies (Dicke & Sabelis, 1988). This phenomenon has been studied for two decades and a wealth of knowledge has been collected on several plant-herbivore-predator systems (Vet & Dicke, 1992; Shimoda et al., 1997). Predators identify herbivore species on the same plant (De Moraes et al., 1998; Dicke, 1999) and are also attracted to herbivore products such as feces in weaker tendency (Vet & Dicke, 1992). In previous studies on plant-carnivore interactions mediated by herbivore induced plant volatiles, the interactions were mainly demonstrated under laboratory condition using olfactometers or wind tunnels, focusing only on chemical features (Drukker et al., 2000; Sengonca & Kranz, 2001; Lou & Cheng, 2003). Beyond the effect of herbivore induced plant volatiles (HIPVs), the physical structure of the host plants can also affect the predators final decision to locate the prey. Some studies came to the same conclusion in different host plant-herbivore-predator combinations (Evans, 1976; Eigenbrode et al., 1996; Agrawal, 1997; Clark & Messina, 1998; Roda et al, 2001; Chang & Eigenbrode, 2004; Lundgren & Fenlon, 2006) 35

54 36 The two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae) is a widespread agricultural pest that often causes severe damage to various crops (Gerlach & Sengonca, 1985). There are many effective natural enemies, mostly predators, which can suppress spider mites` populations under laboratory and field conditions and often co-occur in the same field (Shimoda & Ashihara, 1996; Takahashi et al., 2001). All species in the genus Scolothrips (Thysanoptera: Thripidae) appear to be specialized predators of spider mites (Gilstrap, 1995). Scolothrips longicornis Priesner is a native predator in Iran, occurring on many crops, such as cucumber, bean, tomato and sugar cane. Several studies have focused on the attraction of predatory mites to host plant-induced volatiles, but there are only few available papers about the attraction of the predatory thrips Scolothrips takahshii Priesner towards bean volatiles induced by the two-spotted spider mite (Shimoda & Takabayashi, 2001; Takahashi et al., 2001). In contrast, nothing is known about the responses of the predatory thrips S. longicornis towards plant structures, such as leaf shape and size (Kheradpir et al., unpublished data) nor about the chemical features of different species or the cultivars of one crop species. In this study, we investigated the tritrophic interactions between different host plants, such as cucumber, tomato, eggplant and sweet pepper, the two-spotted spider mite and the predatory thrips S. longicornis under greenhouse conditions. We first studied the behavior of S. longicornis when locating spider mites on different host plants and then compared the ability of the predator to find its prey as affected by the features of various cultivars of the host, Cucumis sativus. Material and methods Prey rearing The two-spotted spider mite was reared on bean plants in a climate-controlled room (26±1 ºC, RH=65±5% and 16L:8D) at the Biological Control Research Department of the Institute of Plant Protection Research (IPPR). Spider mites of the third generation were used for predatory thrips culture and also for other treatments. Predator culture The culture of S. longicornis was established from specimens obtained off greenhouse cucumber in IPPR and kept in the same climate room on cow pea plants infested by spider mites. Experimental plants Four species of greenhouse vegetables, cucumber var. Sultan, tomato var. Cantander, eggplant var. Valencia and sweet pepper var. local were planted in small pots in the same climate room. Plants at the age of 4-5 leaves were used for the experiment. Half the pots of each plant species were infested by mites and the rest left intact. Each plant was covered by a box that contained a transparent part with a window fixed with the plant size (60 90 mm). Cucumber cultivars such as Sultan, Sina, Fadia, Super Royal, Negin, GM, Dominos, Super Myra cross were also grown for the second preference test. Release and recapture experiments In a greenhouse compartment, eight potted experimental plants of cucumber, tomato, eggplant and sweet pepper were placed inside a tray filled with soil, thus they occupied the eight corners of an octagon with a diameter of 90 cm. Pots were put into the soil with the rim just below the soil surface. Soil was added to the pots so that the levels inside and outside the pots

55 37 were equal. Half of the plants (one of each species) were infested by spider mites. Forty eight hours before the experiments infested green bean leaves were placed on the leaves of the experimental plants, in order that at the time of experiment, each plant held mites per leaf. The experiment was run in ten replicates with different sets of plants (intact and infested). About 120 pupae of the predatory thrips were isolated individually four days before the experiment and transferred to a glass cage with a leaf disk of squash in wet cotton. Green bean leaves infested by spider mites were provided for the newly emerged predatory female thrips. Eight hours before the experiments, 110 female adult thrips of the isolated culture were transferred to a large Petri dish without any food, and released together from the dish in the middle of the plant octagon. Starting three hours after releasing, plants were checked for the presence of S. longicornis. The same design was used for eight infected cultivars of cucumber; the numbers of trapped predators were recorded and the data of both tests were subjected to an ANOVA test under complete randomized block design and the means were compared by the Duncan method with SPSS 14.0 software. Results and discussion In the first test, which consisted of four host plants (cucumber, tomato, eggplant and sweet pepper) in two situations, infested and clean, 95.2% of all predators released were recovered on eight infected and intact plants (so we had 4.8% no-choice); 33.6% were observed on clean and 62.6% were found on the four infected plants. The difference among the number of trapped predaceous thrips on four infested and intact plants was highly significant. Among the clean plants, the highest number of thrips was attracted and counted on cucumber plants (F= 7.95, p>0.001; 11±1.60 thrips; Table. 1) and there was no significant difference among the numbers of S. longicornis on the other three clean plants (eggplant= 8.7±1.03, tomato= 7.3±1.32 and sweet pepper= 6.6±1.04). The mean number of thrips counted on infested plants showed significant difference (F= 34.83, p>0.001). The highest number of S. longicornis were on cucumber (25.10±1.41 thrips) and the least on infected sweet pepper (9.7±1.5). The mean number of thrips counted on different plant species had some overlap and only on infested cucumber were the values significantly different from the rest of the species. Table 1- The mean number of predaceous thrips collected on the experimental plants (± SE mean). Plant species Cucumber Tomato Eggplant Sweet pepper Infected 25.1±1.4 a 15.3±3.1 b 11.5±2.2 c 9.7±1.5 c Intact 11±1.60 a 7.3±1.32 b 8.7±1.03 b 6.6±1.04 b Cucumber cultivars Number of thrips (n.s.) Sultan Sina Fadia GM Super Royal Negin Dominos Super Myra cross The results of the first release recapture test of the predator show that cucumber was the most attractive host plant, especially when infested by spider mites. For this reason the eight cucumber cultivars with the highest plantation area in Iranian greenhouse were used for the second test, in order to measure the ability of the predator to distinguish among different cultivars of the same species. Of the predators released in the second test, 96.8% were

56 38 recollected on eight infested cucumber cultivars (3.2% no-choice) and the difference among the mean number of predators on each cultivars was insignificant (F=0.46, p>0.001). The predator's ability to discriminate among different cultivars of host plants indicates the ability of host plants to produce different features which can be distinguished by predators. These features can be divided into two main groups, chemical (Herbivore-Induced Plant Volatiles) and physical features (plant architecture, color, trichomes and so on). The findings in the first test, that the predator distinguished between infested and clean plants of the same species suggested that the chemical cues related to spider mite infestation were the most effective factor affecting predator behavior. However, in the second test with different cucumber cultivars, the predator did not chose any cultivar as the most attractive for providing mites. As the physical features of cucumber cultivars were similar, it may be concluded that the volatiles produced due to spider mite infestation were similar in quality and quantity among the tested cultivars. The release-recapture test demonstrated that S. longicornis females are attracted to volatiles from host plants infested by T. urticae mites. These volatiles probably originate from leaves infested by spider mite, because the predator did not effectively respond to volatiles from clean host plants. These results indicate that the volatiles attracting the predators are induced by spider-mite damage, not by the host plant itself. Many studies relating to host plants infested by spider mites have shown the same response of the predators through olfactometers or release-recapture tests. Most authors studied the responses of the predacious mite, Phytoseiulus persimilis, toward plants infested by spider mites (Dicke et al., 1993, Agrawal et al., 2000, Venzon et al., 2002, Shimoda et al., 2005, Moayeri et al., 2006). The predatory mites were attracted to the infested leaves themselves but not to the spider mites or to artificially damaged leaves. Other researchers have observed the response of other species of Scolothrips toward host plants. Shimoda et al. (2002) showed that S. takahashii significantly preferred host plants (green beans) infested by spider mites over clean plants. The results of this study revealed that S. longicornis can discriminate among different host plants and that host plant infestation by spider mites attracted the predaceous thrips more than clean plants. Various cultivars of greenhouse cucumber did not have different features which could affect the prey-location behavior of the predator. More studies are needed in order to conduct similar experiments with other natural enemies, to provide biological control of higher quality. References Agrawal, A.A. 1997: Do leaf domatia mediate a plant-mite mutualism? An experimental test of the effects on predators and herbivores. Ecol. Entomol. 122: Agrawal, A.A., Karban, R. & Colfer, R.G. 2000: How leaf domatia and induced plant resistance affect herbivores, natural enemies and plant performance. Oikos 89: Bottrell, D.G., Barbosa, P. & Gould, F. 1998: Manipulating natural enemies by plant variety selection and modification: A realistic strategy? Ann. Rev. Entomol. 43: Chang, G.C. & Eigenbrode, S.D. 2004: Delineating the effects of a plant trait on interactions among associated insects. Oecologia. 139: Clark, T.L. & Messina, F.J. 1998: Foraging behavior of lacewing larvae (Neur.: Chrysopidae) on plants with divergent architecture. J. Ins. Behav De Moraes, C.M., Lewis, W.J., Pare, P.W., Alborn, H.T. & Tumlinson, J.H. 1998: Herbivore infested plants selectively attract parasitoids. Nature 393: Dicke, M. 1999: Are herbivore-induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods? Ent. Exp. Appl. 91:

57 Dicke, M. & Sabelis, M.W. 1988: How plants obtain predatory mites as bodyguards. Netherlands J. Zool. 38(2-4): Dicke, M., Van Baarlen, P., Wessels, R. & Dijkman, H. 1993: Herbivory induces systemic production of plant volatiles that attract predators of the herbivore: extraction of endogenous elicitor. J. Chem. Ecol. 19(3): Drukker, B., Bruin, J. & Sabelis, M.W. 2000: Anthocorid predators learn to associate herbivore-induced plant volatiles with presence or absence of prey. Physiol. Entomol. 25: Eigenbrode, S.D., Castagnola, T., Roux, M.B. & Steljes, L. 1996: Mobility of three generalist predators is greater on cabbage with glossy leaf wax than on cabbage with a wax bloom. Ent. Exp. Appl. 81: Evans, H.F. 1976: The searching behaviour of Anthocoris confusus (Reuter) in relation to prey density and plant surface topography. Ecol. Entomol. 1: Gerlach, S. & Sengonca, C. 1985: Comparative studies on the effectiveness of the predatory mite, Phytoseiulus persimilis and the predatory thrips Scolothrips longicornis. Zeitschrift f. Planzenkrankh. Pflanzenschutz 92: Gilstrap, F.E. 1995: Six-spotted thrips: A gift from nature that controls spider mites. In: Thrips Biology and Management. ed: Parker, B.L.: Janssen, A., Pallini, A., Venzon, M. & Sabelis, M.W. 1998: Behaviour and indirect interactions in food webs of plant-inhabiting arthropods. Exp. Appl. Acar. 22: Janssen, A., Pallini, A., Venzon, M. & Sabelis, M.W. 1999: Absence of odour-mediated avoidance of heretospecific competitors by the predatory mite Phytoseiulus persimilis. Ent. Exp. Appl. 92: Lou, Y.G. & Cheng, J.A. 2003: Role of rice volatiles in the foraging behaviour of the predator Cyrtorhinus livipennis for the rice brown planthoper Nilaparvata lugens. BioControl 48: Lundgren, J.G. & Fergen, J.K. 2006: The oviposition behavior of the predator Orius insidiosus: acceptability and preference for different plants. Biocontrol 51: Moayeri, H.R.S., Ashouri, A., Brodsgaard, H. & Enkegaard, A. 2006: Odour-mediated response of a predatory mired bug and its prey, the two-spotted spider mite. Exp. Appl. Acar. 40: Roda, A., Nyrop, J., English-Loeb, G. & Dicke, M. 2001: Leaf pubescence and two-spotted spidre mite webbing influence phytoseiid behavior and population density. Oecologia. 129: Sengonca, C. & Kranz, J. 2001: A modified four armed olfactometer for determining olfactory reactions of beneficial arthropods. J. Pest Sci. 74: Shimoda, T. & Ashihara, W. 1996: Seasonal population trends of spider mites and their insect predator Oligota kashmirica benefica Naomi (Coleoptera: Staphylinidae) in Satsuma mandarin groves and in Japanese cedar windbreaks around the orchards. Proc. Assoc. Plant Prot. Kyushu 42: Shimoda, T., Ozawa, R., Arimura, G., Takabayashi, J. & Nishioka, T. 2002: Olfactory response of two specialist insect predators of spider mite toward plant volatiles from lima bean leaves induced by jasmonic acid and/or methyl salicylate. Appl. Entomol. Zool. 37(4): Shimoda, T., Ozawa, R., Sano, K., Yano, E. & Takabayashi, J. 2005: The involvement of volatile infochemicals from spider mites and from food-plants in prey location of the generalist predatory mite Neoseiulus californicus. J. Chem. Ecol. 31(9): Shimoda, T. & Takabayashi, J. 2001: Migration of specialist insect predators to exploit patchily distributed spider mites. Pop. Ecol. 43:

58 40 Takahashi, H., Takafuji, A., Takabayashi, J., Yano, S. & Shimoda, T. 2001: Seasonal occurance of specialist and generalist insect predators of spider mites and their response to volatiles from spider-mite-infested plants in Japanese pear orchards. Exp. Appl. Acar. 25: Venzon, M., Janssen, A., & Sabelis, M.W. 2002: Prey preference and reproductive success of the generalist predator Orius laevigatus. Oikos 97: Vet, L.E.M. & Dicke, M. 1992: Ecology of infochemical use by natural enemies in a tritrophic context. Ann. Rev. Entomol. 37:

59 Integrated Control of Plant-Feeding Mites IOBC/wprs Bulletin Vol. 50, 2009 pp Compatibility of Amblyseius swirskii with UV-absorbing nets Saioa Legarrea 1, Alberto Fereres 1, Phyllis G. Weintraub 2 1 Centro de Ciencias Medioambientales-CSIC, C/Serrano 115 dpdo, Madrid, Spain. 2 Agricultural Research Organization (ARO), Gilat Research Center, DN Negev, 85280, Israel Abstract: Releases of Amblyseius swirskii effectively control the population of the broad mite Polyphagotarsonemus latus (Banks) in sweet pepper crops. In the context of an IPM strategy in protected crops, the release of natural enemies joins other tactics like the use of UV-photoselective covers. However, the effect of these materials on predators still remains unknown. In this study, a choice experiment was designed to test whether UV-absorbing covers negatively affected the mite dispersal behaviour. Over fifty eight percent of the mites were found in the plant placed under the UVabsorbing net showing the compatibility of both IPM tools. Key words: Phytoseiidae, UV-absorbing net, choice-test behaviour Introduction Amblyseius swirskii (Athias-Henriot) has been commercialized and is one of the most often released predatory mites in protected crops in the Mediterranean basin (Gerson and Weintraub, 2007). It is a phytoseiid mite that can feed on whiteflies, thrips and demonstrates a type II functional response to the tarsonemid mite P. latus (Tal et al., 2007). The integrated pest management (IPM) of horticultural protected crops in the tropical and subtropical area includes various biological, cultural and chemical tactics that should be applied in harmony. Among them, the use of UV-absorbing nets and inundative releases of predators are important tools leading to successful pest control in sweet pepper (Weintraub, 2007). Greenhouse covers that filter light in the UV range ( nm) have an exclusion effect in some pests because the insect orientation ability is modified. In fact, until 2007, 16 UV-blocking plastic films have been proven efficient against the main pest species tested, reducing the number of captures in traps placed inside the greenhouses (Diaz & Fereres, 2007). However, the effect of UV-absorbing screens on predatory mites has not yet been studied. Phytoseiids, the best known group of predatory mites, are characterized by the lack of eyes as all the mites belonging to the Order Mesostigmata (Gerson et al., 2003). However, behavioural studies have shown that several species have a negative phototrophic response to light (Weintraub et al., 2007). This study aims to clarify the effect that UV-absorbing nets produce on the dispersal behaviour of the predatory mite A. swirskii. Material and methods A choice cage was designed to test the preference of A. swirskii for either an environment that receives the full light spectrum or without the UV- light radiation. Two wooden cages (50 x 50 x 50 cm) were joined by a narrow black plastic cylinder (16 cm diameter). One cage was covered with an UV-absorbing net (BioNet Transparent - Meteor Agricultural Nets, Ltd, 41

60 42 Israel - which transmits 35% of UV radiation) while the other cage was covered with a non- UV absorbing net (Antivirus Net - Meteor - transmitting 60% of UV radiation), both materials having a density of 20 x10 threads per cm (50 mesh). For each experiment, one pepper plant variety Miko (7-9 leaves and cm high) was placed in each cage. The plants were joined by a cardboard platform (15 x 3 cm) attached to each stem with a metal wire. One pepper leaf from each plant was held to the platform with a clip; apices being separated by 5 cm. One square centimetre was delimited in the middle of the platform as the mite release area (Figure 1). The A. swirskii used in this experiment were provided by BioBee Biological Systems (Sde Eliyahu, Israel) and kept for the experimental time in a rearing colony with free access to water and corn pollen. b a c d Figure 1. Schematic drawing of pepper plants with cardboard bridge (a) release area, (b) cardboard platform, (c) clip, (d) metal wire. In each trial, hundreds of mites were released in the central area of the platform. In order to record the movement of the mites, the aerial parts of the pepper plants were washed in alcohol 80% two hours later, The mites were counted under a stereoscopic microscope, and the proportion of mites under each cover was calculated. The cages were placed in direct sunlight and adjusted so that neither cage cast a shade on the other. A total of nine trials were conducted during the days th November at the Gilat Agricultural Center, Israel. To avoid influence from the west or east position of the cage, the designed structure was turned round in each trial. Differences between treatments were determined using a Chi square test (SPSS, 2006). Results and discussion A significantly (χ 2 =21.444, p <0.001) higher proportion of mites (58%) were found on plants under the BioNet Transparent net than under the AntiVirus net (Figure 2). In these trials, A. swirskii showed a slight preference towards the environment provided by the greater UV-absorbing net. Even though the statistical differences found may not constitute biologically significant differences, we have shown that the predatory mite A. swirskii does not avoid the environment created under the UV-absorbing net tested. This result suggests that both strategies, UV-absorbing materials and releases of predatory mites, can be implemented successfully together in an IPM program.

61 BioNet Transparent 60 Antivirus Net Net type Figure 2. Percentage (Mean ± SD) of Amblyseius swirskii found on the plant placed under each net type two hours after the release. n=9. References Percentage of mites Diaz, B.M, & Fereres, A. 2007: Ultraviolet-blocking materials as a physical barrier to control insect pests and plant pathogens in protected crops. Pest Tech. 1: Gerson, U., Smiley R. L. & Ochoa R. 2003: Mites (Acari) for pest control. Oxford: Blackwell Science Ltd.: 539 pp. Gerson, U. & Weintraub, P.G. 2007: Review: Mites for the control of pests in protected cultivation. Pest Manag. Sci. 63: SPSS, 2006: SPSS statistical package, version Chicago, SPSS Inc. Tal, C., Coll, M. & Weintraub, P.G. 2007: Biological control of Polyphagotarsonemus latus by the predaceous mite Amblyseius swirskii. IOBC/wprs Bull. 30(5): Weintraub, P.G. 2007: Review: Integrated control of pests in tropical and subtropical sweet pepper production. Pest Manag. Sci. 63: Weintraub, P.G., Kleitman S., Alchanatis, V. & Palevsky, E. 2007: Factors affecting the distribution of a predatory mite on greenhouse sweet pepper. Exp. Appl. Acarol. 42:

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63 Integrated Control of Plant-Feeding Mites IOBC/wprs Bulletin Vol. 50, 2009 pp Notes on the phenology and the biology of Tydeus caudatus Dugès (Acari, Tydeidae) Mauro Lorenzon, Alberto Pozzebon, Carlo Duso Department of Environmental Agronomy and Crop Science, University of Padua, Agripolis, Viale dell Università 16, Legnaro, Padova, Italy. Abstract: Knowledge on the biology and ecology of the Tydeoidea is limited. Regarding feeding habits, tydeids appear as an unspecialized group. of the families Tydeidae and Iolinidae are frequently observed in vineyards associated with eriophyid Members mites, and feeding on pollen or fungi has also been reported. Tydeus caudatus Dugès is one of the most common tydeid species occurring in Italian vineyards. Tydeus caudatus populations can persist and increase in vineyards when eriophyid levels are low, suggesting that its diet includes non-prey food sources. In this paper, the suitability of pollen and grape downy mildew as food sources for T. caudatus has been explored. Some findings on the phenology of T. caudatus in vineyards are also reported. Key words: Tydeus caudatus, grape, downy mildew, pollen, life history parameters, phenology Introduction Tydeid mites (Acari: Tydeoidea) are widely distributed around the world and reach significant population densities in certain perennial agro-ecosystems, such as citrus and grapevine (Krantz, 1978; Garcia Mari et al., 1986; Vacante & Tropea Garzia, 1987; Corino & Duverney, 1989; Castagnoli, 1989). Tydeids are considered an unspecialized group as regards their feeding habits, probably because knowledge on their biology and ecology is limited (Baker & Wharton, 1952). Phytophagy has been reported for some species (Karg, 1992; Badii et al., 2001) but feeding on pollen (Flaherty & Hoy, 1971; Liguori et al., 2002), fungi (Sinha, 1962; McCoy et al., 1969), honeydew and sooty moulds (Mendel & Gerson, 1982) is more common. Some tydeids can prey upon small arthropods such as eriophyoid mites and are considered important biocontrol agents (Laing & Knop, 1983; Hessein & Perring, 1986; Perring & McMurtry, 1996; Abou-Awad et al., 1999). Finally, tydeids have been considered an alternative prey for phytoseiid mites in vineyards and fruit orchards (Flaherty & Hoy, 1971; Calis et al., 1988). Among the Tydeoidea, some members belonging to the families Tydeidae and Iolinidae frequently occur in vineyards where they exert a role as predators of eriophyoid mites (Schruft, 1972; Duso & de Lillo, 1996). Orthotydeus lambi (Baker) is considered an important control agent of grape powdery mildew in North America (English-Loeb et al., 1998; Norton et al., 2000). Tydeus caudatus Dugès is one of the most common tydeid species occurring in Italian vineyards (Castagnoli, 1989), but little is known about its biology and ecology. Camporese & Duso (1995) reported T. caudatus in association with Colomerus vitis (Pagenstecher) during winter, and suggested that it is a predator of this mite pest. In that study, T. caudatus was the preferred prey for the predatory mite Paraseiulus talbii (Athias- Henriot). A positive relationship between T. caudatus and the grape downy mildew Plasmopara viticola (Berk. and Curtis ex de Bary) Berlese and De Toni has been shown in 45

64 46 north-italian vineyards (Duso et al., 2005). In the same study, the consumption of downy mildew by T. caudatus was shown using isoelectrofocusing. Observations carried out in northern Italian vineyards showed that T. caudatus populations reach higher densities in spring and late summer. Factors affecting this trend and major events in the phenology of T. caudatus have recently been investigated. Preliminary results of this research are reported herein. Materials and methods Field studies The phenology of T. caudatus was investigated in a vineyard located in the Veneto region (north-eastern Italy), where high population densities had been observed in previous studies. Observations were carried out during a growing season by sampling 2-year old branches from winter to spring, and leaves from spring to fall. Branches or leaf samples were transported into the laboratory and immediately examined under a dissecting microscope to assess mite diversity and abundance. Mites were mounted on slides in Hoyer s medium and examined under a phase contrast microscope for species and development stage identification. Laboratory studies In the laboratory we compared the developmental times and life history parameters of T. caudatus individuals reared on leaf discs with poppy (Papaver rhoeas) pollen or grape downy mildew mycelium as food sources. Additional mites were reared on leaf discs without food as a control. The mites used in the experiments originated from the above-mentioned vineyard and were reared in the laboratory (23 ± 2 C, 70% ± 5 R.H.) at the Department of Environmental Agronomy and Crop Science, University of Padua, Legnaro (PD). Single tydeid larvae were transferred to each experimental unit and monitored throughout their development to adults. A total of 30 larvae per treatment was used. The experimental units were placed in climate-controlled chambers held at 23 ± 2 C, 70 75% RH with a 16L: 8D regime. During the development from larva to adult we made two observations per day (every 12h) to assess survival and the duration of each developmental stage. Leaf discs were replenished every two days. Mites were gently transferred from old to new discs using a fine paint brush. Once the adult stage was reached, one male and one female obtained using the same food source were placed on a disc together. Their survival and offspring were recorded every 24 hours. The offspring obtained in the first 72 h was monitored until development was complete in order to assess sex-ratio and estimate life-table parameters (Maia et al., 2000). Data analysis The effects of different food sources on tydeid development and fecundity were analyzed with ANOVA using the GLM procedure of SAS (SAS Institute, 1999). We evaluated the food source effect on the duration (h) of each development stage and fecundity applying a Tukey- Kramer test (α = 0.05). Life table parameters were estimated and compared using a SAS based procedure and by applying a Jackknife method developed by Maia et al. (2000). Results and discussion Tydeids overwintered under the bark of 2-year old branches, sometimes in crevices at the insertion of one-year old branches on 2-year old branches. In February, most of the overwintering tydeids were tritonymphs. The first adults were recorded in late March. Reproduction started in April and the first larvae were recorded soon afterwards. At

65 47 sprouting, all the developmental stages were seen on leaves. The populations peaked from late May to mid-june and in September. In late October most of the population was represented by tritonymphs. In this vineyard, the phenology of T. caudatus scarcely appeared to be affected by phytoseiids or other predators. Tydeus caudatus females and males completed their development on leaf discs with poppy pollen or downy mildew mycelium. Larvae died before molting when placed on leaf discs without food. Developmental times (from larva to adult) of T. caudatus females lasted hours, and hours for males. Food sources had no effect on developmental times. Reproduction was observed on both food sources. Life table parameters were similar when pollen or downy mildew were offered as food. Moreover, a demographic parameter analysis indicated that both food sources were suitable for the increase and persistence of T. caudatus populations. Phytophagy on apple leaves was reported for T. caudatus (Karg, 1992) but in our experiments tydeids did not develop on grape leaf discs. Our studies confirmed the importance of pollen as a food source for tydeids (Flaherty & Hoy, 1971; Hessein & Perring, 1988; Liguori et al., 2002). Downy mildew allowed the development and reproduction of T. caudatus, partly explaining the positive relationships between tydeids and the plantpathogenic fungus which had emerged in previous investigations (Duso et al., 2005). Tydeid seasonal abundance appears to reflect typical trends in pollen and downy mildew availability. The first tydeid peak corresponded with a phase of typical pollen abundance (Eichhorn & Hoos, 1990; Engel & Ohnesorge, 1994; Duso et al., 1997), while the second followed a period of extensive downy mildew availability. The latter is known to affect phytoseiid mite abundance positively during fall and winter, with potential consequences for biological control (Duso et al., 2003; 2005; Pozzebon & Duso, 2008). Overwintering T. caudatus nymphs have been found associated with colonies of C. vitis (Camporese & Duso, 1995). Since downy mildew positively affects T. caudatus abundance in late season, this phenomenon may be important for the control of eriophyids by tydeids. The present study sheds light on the biology and ecological traits of T. caudatus. Its role in vineyards appears to have been underestimated and further studies should be undertaken in order to clarify this aspect. References Abou-Awad, B.A., El-Sawaf, B.M. & Kader, A.A.A. 1999: Life history and life table of Pronematus ubiquitus (McGregor) as a predator of eriophyoid mites in Egypt (Acari: Tydeidae). Acarologia 40: Badii, M.H., Flores, A.E., Ponce, G., Landeros, J. & Quiroz, H. 2001: Does the Lorryia formosa Cooreman (Acari: Prostigmata: Tydeidae) population visit or reside on citrus foliage? Acarology: Proceeding of the 10 th International Congress: Baker, E.W. & Wharton, G.W. 1952: An Introduction to Acarology. Mc Millan Co., N.Y. 465 pp. Calis, J.N.M., Overmeer, W.P.J. & van der Geest, L.P.S. 1988: Tydeids as alternative prey for phytoseiid mites in apple orchards. Med. Fac. Landbouw. Rijksuniv. Gent 53: Camporese, P. & Duso, C. 1995: Life history and life table parameters of the predatory mite Typhlodromus talbii. Entomol. Exp. Appl. 77: Castagnoli, M. 1989: Recent advances in knowledge of the mite fauna in the biocenoses of grapevine in Italy. In: Influence of environmental factors on the control of grape pests, diseases and weeds, ed. Cavalloro:

66 48 Corino, L. & Duverney, C. 1989: Distribuzione geografica delle differenti specie di Fitoseidi (Acarina: Phytoseiidae) e Tideidi (Acarina: Tydeidae) nei vigneti della Valle d'aosta. Riv. Vitic. Enol. Conegliano. 42: Duso, C. & de Lillo, E. 1996: Grape. In: Eriophyoid Mites. Their Biology, Natural Enemies and Control, World Crop Pests, eds. Lindquist, E.E., Sabelis. M.W. and Bruin, J.: Elsevier, Amsterdam. Duso, C., Malagnini, V. & Paganelli, A. 1997: Indagini preliminari sui rapporti tra polline e Kampimodromus aberrans (Oudemans) (Acari: Phytoseiidae). Allionia 35: Duso, C., Pozzebon, A., Capuzzo, C., Bisol, P.M. & Otto, S. 2003: Grape downy mildew spread and mite seasonal abundance in vineyards: evidence for the predatory mites Amblyseius andersoni and Typhlodromus pyri. Biol. Control. 27: Duso, C., Pozzebon, A., Capuzzo, C., Malagnini, V. & Otto, S. 2005: Grape downy mildew spread and mite seasonal abundance in vineyards: effects on Tydeus caudatus and its predators. Biol. Control. 32: Eichhorn, K.W. & Hoos, D. 1990: Investigations in population dynamics of Typhlodromus pyri in vineyards of Palatina, F.R. Germany. IOBC/wprs Bull. 13 (7): Engel, R. & Ohnesorge, B. 1994: Die Rolle von Ersatznahrung und Mikroklima im System Typhlodromus pyri Scheuten (Acari, Phytoseidae) Panonychus ulmi Koch (Acari, Tetranychidae) auf Weinreben. II. Freilandversuche. J. Appl. Entomol. 118: English-Loeb, G., Norton, A.P., Gadoury, D.M., Seem, R.C. & Wilcox, W.F. 1998: Control of powdery mildew in wild and cultivated grapes by a tydeid mite. Biol. Control. 14: Flaherty, D.L. & Hoy, M.A. 1971: Biological control of Pacific mites and Willamette mites in San Joaquin Valley vineyards. Part III. Role of tydeid mites. Res. Pop. Ecol. 13: Garcia Mari, F., Ferragut, F., Marzal, C., Costa Comelles, J. & Laborda, R. 1986: Acaros que viven en las hojas de los citricos españoles. Prod. Prot. Veg. 1: Hessein, N.A. & Perring, T.M. 1986: Feeding habits of the Tydeidae with evidence of Homeopronematus anconai (Acari: Tydeidae) predation on Aculops lycopersici (Acari: Eriophyidae). Int. J. Acarol. 12: Karg, W. 1992: The importance of so-called indifferent mite species for the equilibrium between spider mites and their antagonists. Acta Phytopathol. Entomol. Hungarica 27: Krantz, G.W. 1978: A Manual of Acarology. Oregon State University Book Stores, Inc., Corvallis, Oregon. Laing, J.E. & Knop, N.F. 1983: Potential use of predaceous mites other than Phytoseiidae for biological control of orchard pests. In: Hoy, M.A., Cunningham, G.L., Knutson, L., eds. Biological Control of Pests by Mites, Agricultural Experiment Station, Division of Agriculture and Natural Resources, University of California Special Publication 3304: Liguori, M., Simoni, S. & Castagnoli, M. 2002: Aspects of life history of Tydeus californicus (Banks) (Acari Tydeidae). Redia 85: Maia, A.H.N., Luiz, A.J.B. & Campanhola, C. 2000: Statistical inference on associated fertility life table parameters using jackknife technique: computational aspect. J. Econ. Entomol. 93: McCoy, C.W., Selhime, A.G. & Kanavel, R.F. 1969: The feeding behaviour and biology of Parapronematus acaciae (Acarina: Tydeidae). Fla. Entomol. 52: Mendel, Z. & Gerson, U. 1982: Is the mite Lorryia formosa Cooreman (Prostigmata: Tydeidae) a sanitizing agent in citrus groves? Acta Oecol. 3:

67 Norton, A.P., English-Loeb, G., Gadoury, D. & Seem, R.C. 2000: Mycophagous mites and foliar pathogens: leaf domatia mediate tritrophic interactions in grapes. Ecology 81: Perring, T.M. & McMurtry, J.A. 1996: Other predatory arthropods. In: Eriophyoid Mites. Their Biology, Natural Enemies and Control, World Crop Pests, eds. Lindquist, E.. Sabelis, M.W. and Bruin, J: Pozzebon, A. & Duso, C. 2008: Grape downy mildew Plasmopara viticola, an alternative food for generalist predatory mites occurring in vineyards. Biol. Control. 45: SAS Institute Inc. 1999: SAS/STAT User's Guide, Version 8. SAS Institute Inc, Cary, NC. Schruft, G. 1972: Das Vorkommen von Milben aus der Familie Tydeidae (Acari) an Reben. VI. Beitrag über Untersuchungen zur Faunistik und Biologie der Milben (Acari) an Kulturreben (Vitis sp.). Z. ang. Entomol. 71: Sinha, R.N. 1962: A note of associations of some mites with seedborne fungi from the prairie provinces. Proc. Entomol. Soc. Manitoba. 18: Vacante, V. & Tropea Garzia, G. 1987: Grape mites in Sicily. Contribution I. In: Integrated pest control in viticulture, Cavalloro ed.:

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69 Integrated Control of Plant-Feeding Mites IOBC/wprs Bulletin Vol. 50, 2009 pp Biological control of the old world date mite, Oligonychus afrasiaticus, using indigenous predatory mites in the Southern Arava Valley of Israel Alon Lotan 1,2, Eric Palevsky 2, Ido Izhaki 1 1 Department of Evolutionary & Environmental Biology, University of Haifa, Israel. 2 Department of Entomology, Newe-Ya ar Research Center, Agricultural Research Organization (ARO), Ministry of Agriculture, Israel. Abstract: The old world date mite, Oligonychus afrasiaticus (McGregor), is a severe pest of date palms, Phoenix dactilifera L., in arid regions throughout the Middle East and North Africa (Carpenter and Elmer, 1978). Depending on the variety, infestation period and mite density, damage to the fruit cuticle can range from minimal to overall surface scarring and, in worse cases, cracking as well. In Israel this pest was first observed during the 1980's on ground cover vegetation in date palm orchards of the Southern Arava Valley (SAV) (Gerson et al., 1983). During the 1990's it became a severe pest, causing substantial damage and economic loss (Palevsky et al., 2003). The current control strategy is based on prophylactic applications of acaricides that were evaluated and introduced several years ago, following control failures with sulfur (Palevsky et al., 2004). Clearly, chemical control can only be considered to be a short term solution, as acaricide resistance in spider mites may develop rapidly (Cranham and Helle, 1985). In fact, this year (2008), despite the regular applications of acaricides, outbreaks and damage were observed in numerous plots. Together, resistance development, the awareness of the deleterious effects of pesticides on the environment, legal restrictions on using them and the lack of new pesticides are the key factors that are motivating date palm growers to seek new integrated pest management (IPM) strategies. Whereas phytoseiids have been successfully integrated in pest control programs in temperate and relatively humid ecosystems, their application in hot arid environments has encountered difficulties (Walzer et al., 2007). For instance, in southern Tunisia augmentative releases of the European mass reared Neoseiulus californicus McGregor in date palm gardens did not provide satisfactory control of O. afrasiaticus (Othman et al., 2001). These extreme arid conditions favor spider mite population development (Hazan et al., 1974) and suppress the populations of many phytoseiids (Bakker et al., 1993). Thus we hypothesized that indigenous phytoseiids, adapted to the extreme climatic conditions of the arid date palm growing areas, could provide better control of this pest. In a three-years study conducted in the SAV, nine generalist phytoseiid species were identified in date palm gardens, most having been collected on Bermuda grass from the orchard floor (Palevsky, personal communication). Oligonychus afrasiaticus colonizes the green fruit as individual mated females and within 2-4 weeks their populations increase by several orders of magnitude. Generalist predators may restrain spider mite pests with such explosive nature provided they are present in sufficient numbers before pest arrival. Conservation techniques such as the provision of pollen can allow for generalist predator establishment and subsequent suppression of pest populations (Van Rijn and Sabelis, 1999; Nomikou et al., 2002). To test the hypothesis that conservation as a sole technique could enhance biological control of O. afrasiaticus, bunches were dusted weekly with date and maize pollen throughout the ripening season (May-July). Despite ample pollen and spider mite prey, phytoseiid populations remained almost undetected and pest populations were equally high on the treated and control bunches. We concluded that pollen applications, as a stand-alone treatment, failed to conserve indigenous phytoseiids on date palm bunches and that predator augmentation may be necessary for the successful control of the pest. 51

70 52 To evaluate the suitability of predators for augmentative releases, phytoseiids were collected from weeds in date palm orchards of the Dead Sea and Arava valleys and their surroundings. To evaluate their ability to inhabit bunches in the SAV, we examined the establishment of three phytoseiid species on isolated bunches with and without pollen provision. Six weeks post-release population levels of Typhlodromus athiasae Porath and Swirski were higher than those of Cydnoseius negevi (Swirski and Amitai) and Neoseiulus longilaterus (Athias-Henriot), with and without pollen. In addition, pollen considerably improved the establishment of T. athiasae and C. negevi. Taking these encouraging results one step forward, we evaluated the ability of T. athiasae to control the pest mite on a semi-commercial scale. Releasing four thousand predatory mites per tree, together with pollen applications, demonstrated not only that this predatory mite can reduce O. afrasiaticus population, but may also mitigate fruit damage. However, damage was still above the acceptable level. Further research will focus on the evaluation of additional species and strains as well as alternative foods to enhance the biological control of O. afrasiaticus. Key words: Date palms, spider mites, Phytoseiidae, pollen, alternate food References Bakker, F.M., Klein, M.E., Mesa, N.C. & Braun, A.R. 1993: Saturation deficit tolerance spectra of phytophagous mites and their phytoseiid predators on cassava. Experimental and Applied Acarology 17: Carpenter, J.B. & Elmer, H.S. 1978: Pests and diseases of the date palm. Agriculture Handbook. Science and Education Administration, Department of Agriculture, USA. Cranham, J.E. & Helle, W. 1985: Pesticide resistance in Tetranychidae. In: Spider Mites, Their Biology, Natural Enemies and Control. Vol 1B, eds. Helle, W. & Sabelis, M.W.: Elsevier, Amsterdam: Gerson, U., Venezian, A. & Blumberg, D. 1983: Phytophagous mites on date palms in Israel. Fruits 38: Hazan, A., Gerson, U. & Tahori, A.S. 1974: Spider mite webbing. I. The production of webbing under various environmental conditions. Acarologia 16: Nomikou, M., Janssen, A., Schraag, R. & Sabelis, M.W. 2002: Phytoseiid predators suppress populations of Bemisia tabaci on cucumber plants with alternative food. Experimental and Applied Acarology 27: Othman, K., Rhouma, A., Belhadj, R., Alimi, E., Fallah, H., Kreiter, P., Lenfant, C. & Brun, J. 2001: Lutte biologique contre un acarien ravageur des dattes: essai d'utilisation de Neoseiulus californicus contre Oligonychus afrasiaticus dans les palmeraies du Djerid (Sud Tunisien). Phytoma 540: Palevsky, E., Ucko, O., Peles, S., Yablonski, S., & Gerson, U. 2003: Species of Oligonychus infesting date palm cultivars in the Southern Arava Valley of Israel. Phytoparasitica 31: Palevsky, E., Ucko, O., Peles, S., Yablonski, S. and Gerson, U. 2004: Evaluation of control measures for Oligonychus afrasiaticus infesting date palm cultivars in the Southern Arava Valley of Israel. Crop Protection 23: Van-Rijn, P.C.J. & Sabelis, M.W. 1999: Pollen improves thrips control with predatory mites. IOBC/wprs Bull. 22 (1): Walzer, A., Castagnoli, M., Simoni, S., Liguori, M., Palevsky, E. & Schausberger, P. 2007: Intraspecific variation in humidity susceptibility of the predatory mite Neoseiulus californicus: Survival, development and reproduction. Biological Control 41:

71 Integrated Control of Plant-Feeding Mites IOBC/wprs Bulletin Vol. 50, 2009 pp The spider mite Neotetranychus rubi (Träg.) a potential prey for the predatory mite Amblyseius andersoni (Chant) Valeria Malagnini, Alberto Grassi 1, Romano Maines 1, Gino Angeli 1, Claudio Ioriatti 1, Carlo Duso 2 1 FEM-IASMA Research Centre, Plant Protection Department, via E. Mach, San Michele all Adige (TN) Italy; 2 University of Padua, Department of Environmental Agronomy and Crop Science, Viale dell Università, Legnaro (PD) - Italy Abstract: The spider mite Neotetranychus rubi is a phytophagous mite common on raspberries in north-eastern Europe. Recently it has been detected in northeastern Italy on commercial raspberries. The predatory mite Amblyseius andersoni can keep N. rubi populations at low levels during spring but not during summer when A. andersoni seems to prefer the two-spotted spider mite Tetranychus urticae. The aim of this study was to evaluate the role of N. rubi as a prey for A. andersoni as compared to T. urticae. Key words: Phytoseiidae, Tetranychidae, biological control, raspberry. Introduction Neotetranychus rubi (Träg.) is a phytophagous mite belonging to the family Tetranychidae. It is a pest of raspberries in northeastern Europe, particularly wild raspberry (Rubus idaeus L.) (Skorupska, 1975). Populations of the raspberry spider mite in protected and commercial raspberry crops increased at the end of the 1980s (Michalska & Kropczyńska, 2002). In 2005, this spider mite was first reported on commercial raspberry in the Trentino region (northeastern Italy), where raspberry is one of the most economically important soft fruits (Grassi, 2007). Adult female N. rubi overwinter in bark crevices at the base of canes and on old dead leaves in the soil. Females can be found on the vegetation from April onward. During this period, natural populations of predatory mites belonging to the Phytoseiidae can keep raspberry spider mite populations at low levels (Grassi, 2007). Later, raspberry leaves are also colonized by the two-spotted spider mite Tetranychus urticae Koch, which usually causes more damage than N. rubi. Amblyseius andersoni (Chant) is the main component of phytoseiid communities associated with commercial raspberry crops in Trentino. Amblyseius andersoni seemed to prefer T. urticae to N. rubi. When A. andersoni was common during summer, T. urticae population densities reached low levels, whereas those of N. rubi increased (Grassi, 2007). Laboratory studies conducted with Phytoseiulus persimilis Athias- Henriot and different prey organisms [T. urticae, T. cinnabarinus Boisduval, Panonychus ulmi (Koch) and N. rubi] showed that the predatory mite exhibited lower fecundity when N. rubi or P. ulmi were present instead of T. urticae or T. cinnabarinus (Petrova, 1972). The aim of this study was to evaluate the role of N. rubi as prey for A. andersoni, as compared to T. urticae. The development and reproduction of A. andersoni were studied in the laboratory by offering T. urticae and N. rubi to the predator. In an additional treatment, the predators were fed Papaver rhoeas L. pollen, which has previously been shown to be a suitable source of food for A. andersoni (Tsolakis & Ragusa, 1994; Pozzebon & Duso, 2008). 53

72 54 Materials and methods Amblyseius andersoni was collected in cultivated raspberry in the Trentino region (near Pergine). To study its survival, development and oviposition when raised on diets of T. urticae and N. rubi, ovipositing female A. andersoni were collected from raspberry leaves and reared in arenas similar to those described by Overmeer (1981). Papaver rhoeas pollen was provided as food for the predator. Additional arenas were divided into three sections and each section was considered to be an experimental unit. A fine-tipped paint brush was used to place one egg of the predator into each unit. Food was also provided in each unit, and there were three different dietary treatments: females of T. urticae, of N. rubi and P. rhoeas pollen. For each treatment, 20 eggs were assayed. Spider mites (about 10 females) and pollen ( mg) were provided daily. Observations were made three times per day (approximately every eight hours) until juveniles reached adulthood. Trials were carried out under controlled conditions (26 ± 1 C, 70 ± 5% R.H. and a 16L: 8D regime). A male was added to deutonymph females for mating. The percentage of surviving females and the number of eggs/ female were recorded daily. Statistical analysis The effects of the three different diets on the development and reproduction of A. andersoni were analyzed with one-way ANOVA using KyPlot version 2.0. Means were separated applying Tukey s test (α = 0.05). Only individuals that reached adulthood were included in this analysis. Data sets concerning the development of females and males were analyzed separately. Results and discussion The two spider mites and the P. rhoeas pollen were all suitable food for A. andersoni, capable of supporting normal development. The durations of the juvenile stages of phytoseiids reared on the different types of food were calculated and compared. Amblyseius andersoni females developed more quickly when fed P. rhoeas pollen than when fed N. rubi and T. urticae. Additional differences emerged between N. rubi and T. urticae; phytoseiids developed quickly when fed the former. The duration of the pre-oviposition period was not affected by the different diets. Predators reared on T. urticae had higher percentages of female survival and fecundity than those reared on N. rubi. Predators fed pollen showed an intermediate level of fecundity. The different diets did not affect the development of A. andersoni males. Amblyseius andersoni developed quicker when given P. rhoeas pollen than when fed spider mites, confirming data presented by Tsolakis & Ragusa (1994) for T. urticae. Duso and Camporese (1991) reported similar a pattern when they compared the development of A. andersoni fed Mesembryanthemum criniflorum pollen and A. andersoni offered grape spider mites. The finding that the juveniles of A. andersoni fed P. rhoeas developed quicker than reported by Pozzebon and Duso (2008) for predatory mites provided with the same diets probably reflects the different temperatures used in the two experiments (25 C vs. 23 C). This preliminary study shows that N. rubi is a suitable prey for A. andersoni, capable of supporting development and reproduction. Amblyseius andersoni developed quicker when fed N. rubi than when fed T. urticae, but laid more eggs when given the latter. Differences in oviposition between N. rubi and T. urticae are consistent with data reported by Petrova (1972) for P. persimilis. Additional studies are needed to understand the value of N. rubi as prey for A. andersoni and to evaluate the predator s response to large prey populations. The preference

73 55 of A. andersoni for T. urticae, suggested by field studies (Grassi, 2007), must also be demonstrated in ad hoc experiments. References Duso, C. & Camporese, P. 1991: Developmental times and oviposition rates of predatory mites Typhlodromus pyri and Amblyseius andersoni (Acari: Phytoseiidae) reared on different kinds of foods. Exp. Appl. Acarol. 13: Grassi, A. 2007: Ragnetto del lampone (Neotetranychus rubi). In: La coltivazione dei piccoli frutti in Trentino (San Michele all Adige (TN) di Claudio Agnolin: Michalska, K. & Kropczyńska, D. 2002: Fauna roztoczy w uprawach malin chronionych i niechronionych. Prog. Plant Prot. / Post. Ochr. Roślin 42: Overmeer, W.P.J. 1981: Notes on breeding phytoseiid mites from orchards (Acarina: Phytoseiidae) in the laboratory. Meded. Fac. Landbouwwet. Rijksuniv. Gent. 46: Petrova, V.I. 1972: The effect of the feeding and temperature factors on ovo- and spermatogenesis in the predacious mite Phytoseiulus. In: The Pathology of Insects and Mites. Patalogiya nasekomykh I kleshchei: Pozzebon, A. & Duso, C. 2008: Grape downy mildew Plasmopara viticola, an alternative food for generalist predatory mites occurring in vineyards. Biol. Cont. 45: Skorupska, A. 1975: Obserwacje nad morfologią i biologią przędziorka malinowca Neotetranychus rubi (Träg), Acarina, Tetranychidae. Prace Nauk. Inst. Ochr. Roślin 17(1): Tsolakis, H. & Ragusa, S. 1994: Biological and life table parameters of Amblyseius andersoni (Chant) (Parasitiformes, Phytoseiidae) on different kinds of food substances. Phytophaga 5:

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75 Integrated Control of Plant-Feeding Mites IOBC/wprs Bulletin Vol. 50, 2009 pp Integrated pest management of Oligonychus perseae: Developing action thresholds and the identification and conservation of natural enemies Yonattan Maoz 1, Eric Palevsky 1, Shira Gal 1, Miriam Zilberstein 2, Michael Noy 2, Yehonatan Izhar 3, Jonathan Abrahams 4 Samuel Gan-Mor 5 and Moshe Coll 6 1 Agricultural Research Organization (ARO), Newe-Ya ar Research Center, Ramat Yishay, 30095, Israel, 2 Bio-Fly, Kibbutz Sdeh Eliyahu, Beit Shean Valley, 10810, Israel; 3 Western Galilee R&D, MP Oshrat, 25212, Israel; 4 Soil Conservation and Drainage Unit, Upper Galilee Ministry of Agriculture, Sefad, Israel; 5 Institute of Agricultural Engineering, ARO, P.O. Box 6 Bet Dagan, Israel; 6 Department of Entomology, The Hebrew University of Jerusalem, POB 12, Rehovot 76100, Israel. Abstract: Since its entry in 2001, the persea mite, Oligonychus perseae, has become a primary pest of avocado in Israel. Field trials over three consecutive growing seasons were conducted to develop an action threshold for the pest. To identify its indigenous predators and to evaluate methods for their conservation, we monitored populations in orchards and performed trials in three spatial scales: in Petri dishes, on seedlings and in the field. We found that mite populations caused significant foliar damage. Mean tri-annual yield was reduced by 20% when mite populations were high ( 250 mites/leaf) in comparison to yields attained when plots were sprayed at a threshold of mites per leaf. Euseius scutalis was by far the most abundant predatory mite species in Israeli avocado orchards. Laboratory experiments in Petri dishes and on seedlings showed that it significantly reduced adult persea mite populations. In the seedling experiment and in the field we also found that conservation of this predator through the provisioning of supplemental food (i.e. maize pollen) substantially increased E. scutalis populations and enhanced persea mite control. In addition to E. scutalis, we found four generalist insect predators that fed upon and ripped open the nests of persea mite. The high proportion of torn nests found in the field suggests that these predators are important contributors to the control of the persea mite. Key words: Oligonychus perseae, Euseius scutalis, avocado, foliage damage, yield, pollen, biological control Introduction The persea mite, Oligonychus perseae (Acari: Tetranychidae) Tuttle, Baker & Abatiello, is a pest of Avocado (Aponte and McMurtry, 1997a), originating from Central America (Tuttle et al., 1976). It was first discovered in Israel in the autumn of 2001 in several avocado plots located in the Western Galilee and has since spread to most growing areas. Several studies have dealt with different aspects of this pest: biology (Aponte and McMurtry, 1997b), biological control (Hoddle et al., 1999; 2000; Kerguelen and Hoddle, 1999a), cultivar susceptibility (Kerguelen and Hoddle, 2000) and damage (Kerguelen and Hoddle, 1999a; 1999b). Following the pest s entry to Israel we anticipated that chemical control would be necessary in IPM programs to prevent damage as a short-term solution but that the long term solution would depend on the integration of natural enemies. Accordingly, we invested our 57

76 58 efforts in these two approaches. To develop an action threshold for the chemical control of the pest we conducted field trials over three consecutive seasons. To identify its indigenous predators and to evaluate conservation methods we monitored populations in the orchard and conducted trials in three spacial scales: in Petri dishes, on seedlings and in the field. Below we review the results of these studies. Developing action thresholds As no damage thresholds have been developed for this pest, some Israeli growers will apply up to four acaricide applications per year, a practice that can have negative effects in the long run on the control of the persea mite (Rabbinge, 1985; Penman and Chapman, 1988; McMurtry et al., 1970). Other growers will not spray at all, often leading to extensive foliar damage which may cause partial or total defoliation of the trees (Bender, 1993; Faber, 1997). In the intent of reducing pesticide use on the one hand, and preventing damage to fruit quality and yield on the other, we attempted to develop an action threshold. We created different pest levels on trees (Haas CV) by applying acaricides (spirodiclofen and abamectin) at 50, 100, 250 mites/leaf and a non-sprayed control, evaluating the leaf damage and yields during the years Based on cumulative mite days (CMD), the plots sprayed at 50 and 100 mites/leaf were similar and differed from the two higher levels, the latter pair also being similar. Mite population levels significantly affected leaf damage and mean tri-annual yields ( ). A positive correlation was found upon comparing persea mite CMD s with leaf damage, whereas, a negative correlation was obtained when comparing CMD s with fruit yield. At the higher mite population levels mean yield was reduced by 20% in comparison to the mean yield attained when plots were sprayed at a threshold of mites per leaf. Conservation of the indigenous predatory mite Euseius scutalis While field monitoring for persea mite we observed phytoseiid mites feeding on various life stages of O. perseae within torn nests and outside nests. To identify the indigenous predatory mite fauna on avocado, a survey was conducted in the different avocado growing regions of Israel. The survey revealed that Euseius scutalis (Athias-Henriot) was by far the most dominant species in Israeli avocado orchards (Maoz et al., 2007). Subsequently we conducted laboratory studies to evaluate the predation efficacy of this indigenous species. Laboratory leaf disc trials indicated that although E. scutalis cannot enter intact nests of the persea mite and is unable to tear them, it reduced adult persea mite populations significantly. Because species of the genus Euseius are pollen feeders (McMurtry and Croft, 1997) we explored the possibility of conserving E. scutalis on avocado seedlings (Hass CV) in a walk-in growth chamber and on trees in the field by provisioning maize pollen as a food supplement. The seedling experiment began by applying a surplus of pollen on one leaf to the seedlings of both treatments (control and pollen-provision). Once E. scutalis populations established (after a fortnight) the pollen was removed from the control and all seedlings were infested with persea mite. For the remainder of the experiment we continued to provision pollen to half the seedlings twice a week. The field experiment was conducted in an organic orchard.,maize pollen was fortnightly applied with a prototype electrostatic pollen applicator (Gan-Mor et al., 2003) on trees that were previously sprayed with a fine mist of water, while the negative controls were sprayed with water only. The provision of pollen on seedlings significantly enhanced persea mite control and substantially increased E. scutalis populations. Without pollen E. scutalis left the plants and

77 59 O. perseae populations increased. In the field trial there was a non-significant trend of lower pests and higher predator populations on the trees that received pollen applications. Identification of nest tearing insects and their effect on persea mite Field monitoring of the persea mite revealed a large proportion of torn nests, implying the possible involvement of additional predators in pest predation (as E. scutalis are unable to tear the nest). To identify these predators, insects were collected from avocado trees using a beating tray. Individuals were placed on newly infested leaf discs and monitored for several days. We observed nest tearing and predation by green lace wing Chrysoperla carnea, dusty wing Conwentzia sp., the omnivorous bug Creontiades pallidus and predatory thrips (unidentified). To determine the impact of these nest-tearing predators on the field populations of persea mite, these insect generalist predators were monitored as well as the proportions of abandoned intact nests, ripped nests with and without mites, in two avocado orchards (without chemical treatments) through the summer and autumn of Based on our laboratory observations, we interpreted: 1) the abandoned intact nests as nests that were not attacked by predators, and that the persea mite developed fully; 2) ripped nests with no live mites as nests that were attacked (motiles and eggs either eaten or fled) and 3) ripped nests that still contained live mites as nests that a predator frequented but did not consume all prey, creating an opportunity for intra-guild facilitation (i.e., providing opportunity for other predators to prey on the now exposed mites). Throughout the seasons monitored, in both orchards, the proportion of torn nets with or without mites was between 30%-70%. We also found that the relation between the presence of the nest tearing predators and the amount of torn occupied nests on leaves (nests that a predator recently ripped) was significantly positive. These two results combined suggest that nest tearing predators are playing a role in persea mite control. Conclusion To the best of our knowledge our study is the first to demonstrate a significant effect of O. perseae CMDs on yield reduction. This result has a number of implications. The first being that O. perseae is an economic pest that must be dealt with. Second, an action threshold of mites/leaf can be adopted, at least as a starting point; future refining of this action threshold can be expected. Third, the foliar damage threshold found in this study can be used to assess the degree of success of integrated control programs, such as conservation and augmentation of mite predators. The results of the pollen provision experiments on seedlings and trees signify the importance of pollen for persea mite biocontrol. Extending the period of pollen availability by the establishment of cover crops that would release wind-borne pollen could be a viable way of keeping E. scutalis populations high, thereby preventing or reducing persea mite outbreaks. In this work we developed tools to improve the IPM of the persea mite, and, have laid the foundations for the continuation of research focusing on conservation of acarine and insect indigenous natural enemies in the avocado orchards. Acknowledgements We are indebted to the avocado growers that participated and assisted in the field trials. We would like to acknowledge the Chief Scientist of the Israeli Ministry of Agriculture and the Plant Production and Marketing Board of Israel for their financial support.

78 60 References Aponte, O. & McMurtry, J.A. 1997a: Damage on Hass avocado leaves, webbing and nesting behavior of Oligonychus perseae (Acari: Tetranychidae). Exp. Appl. Acarol. 21: Aponte, O. & McMurtry, J.A. 1997b: Biology, life table and mating behavior of Oligonychus perseae (Acari: Tetranychidae). Int. J. Acarol. 23: Bender, G.S. 1993: A new mite problem in avocados. The Avocado Yearbook. Cal. Avocado Soc. 77: Faber, B. 1997: The Persea mite story. Citrograph. 82: Gan-Mor, S., Bechar, A., Ronen, B., Eisikowitch, D. & Vaknin, Y. 2003: Electrostatic pollen applicator development and tests for almond, kiwi, date and pistachio an overview. App. Eng. Agric. 19: Hoddle, M.S., Aponte, O., Kerguelen, V. & Heraty, J. 1999: Biological control of Oligonychus perseae (Acari: Tetranychidae) on avocado: I. Evaluating release timings, recovery and efficacy of six commercially available phytoseiids. Int. J. Acarol. 25: Hoddle, M.S., Robinson, L. & Virzi, J. 2000: Biological control of Oligonychus perseae (Acari: Tetranychidae) on avocado: III. Evaluating the efficacy of varying release rates and release frequency of Neoseiulus californicus (Acari: Phytoseiidae). Int. J. Acarol. 26: Kerguelen, V. & Hoddle, M.S. 1999a: Biological control of Oligonychus perseae (Acari: Tetranychidae) on avocado: II. Evaluating the efficacy of Galendromus helveolus and Neoseiulus californicus (Acari: Phytoseiidae). Int. J. Acarol. 25: Kerguelen, V. & Hoddle M.S. 1999b: Measuring mite [Oligonychus perseae] feeding damage on avocado leaves with automated image analysis software. Fla. Entomol. 82: Kerguelen, V. & Hoddle, M.S. 2000: Comparison of the susceptibility of several cultivars of avocado to the persea mite, Oligonychus perseae (Acari: Tetranychidae). Sci. Hort. 84: Maoz, Y., Gal, S., Argov, Y., Berkeley, M., Zilberstein, M., Noy, M., Izhar, Y., Abrahams, J., Coll, M. & Palevsky, E. 2007: Biological control of the newly introduced persea mite with indigenous and exotic predators. IOBC/wprs Bulletin. 30(5): McMurtry, J.A. & Croft, B.A. 1997: Life-styles of phytoseiid mites and their roles in biological control. Annu. Rev. Entomol. 42: McMurtry, J.A., Huffaker, C.B. & Van de Vrie, M. 1970: Ecology of tetranychid mites and their natural enemies: a review. I. Tetranychid enemies: their biological characters and the impact of spray practices. Hilgardia 40: Penman, D.R. & Chapman, R.B. 1988: Pesticide-induced mite outbreaks: pyrethroids and spider mites. Exp. Appl. Acarol. 4: Rabbinge, R. 1985: Aspects of damage assessment. In: Spider Mites: Their Biology, Natural Enemies and Control, Vol. 1B, eds. Helle and Sabelis. Elsevier, Amsterdam: Tuttle, D.M., Baker, E.W. & Abbatiello, M.J. 1976: Spider mites of Mexico (Acari: Tetranychidae). Int. J. Acarol. 31:

79 Integrated Control of Plant-Feeding Mites IOBC/wprs Bulletin Vol. 50, 2009 p. 61 The two-spotted mite Tetranychus urticae Koch (Acari: Prostigmata) on citrus clementine groves: seasonal trends and control strategies María Teresa Martínez-Ferrer, José Miguel Campos, José Miguel Fibla. IRTA Amposta. Carretera de Balada, Km Amposta (Tarragona), Spain Abstract: Tetranychus urticae is a major pest of clementines (Citrus reticulata Blanco) in Spanish groves. Citrus is one of the most important economic crops in Spain, growing on 300,000 ha, producing around 6 million t per year, half of them being exported for fresh market. These mites infest fruits and leaves, feeding on them. On leaves, profuse webbing hinders the movement of generalist biological control agents and interferes with chemical control. As a result of their attack, leaves acquire characteristic chlorotic spots and often drop from the tree prematurely. Besides yield reduction, even light infestations on fruits can result in scarring, thus decreasing quality and the commercial value of fruits. The use of pesticides, and especially acaricides, has been reduced in agriculture, thus it is necessary to look for alternatives to chemical control for T. urticae on citrus. This study was conducted in a commercial clementine grove located at Vinaroz (Castellón). The development of T. urticae populations from June to November were monitored on leaves and on fruits. In addition, control strategies were evaluated in a block randomized design, where mineral oil sprays and Neoseiulus californicus releases were compared with an acaricide conventional treatment and nontreated control plots. In the commercial grove the number of symptomatic leaves on the trees increased over the duration of the experiment, ranging from 28 per m 2 at the beginning, to a maximum of 100 per m 2. Populations of T. urticae increased throughout the study period, reaching high values at the end of August, exceeding the established treatment threshold. Phytoseiid populations declined dramatically in July, when temperatures went up, coinciding with peak densities of T. urticae, and did not return to initial levels until mid-september, without providing effective control of the pest. Two mineral oil sprays significantly reduced the number of symptomatic leaves in comparison to the controls during seven weeks, and also significantly diminished T. urticae population densities. Releases of N. californicus did not reduce the numbers of symptomatic leaves, but reduced T. urticae numbers. Neoseiulus californicus did not persist in the crop, possibly due to high temperatures coupled with low humidity. We intend to continue to evaluate the use of mineral oils, N. californicus releases and the two methods combined as alternatives to conventional acaricides for the control of this pest on citrus. Key words: citrus, Tetranychidae, mineral oil sprays, biological control 61

80 Integrated Control of Plant-Feeding Mites IOBC/wprs Bulletin Vol. 50, 2009 p. 62 The Phytoseiidae in biological control: relevance of taxonomic classification and life style categorization James A. McMurtry P.O. Box 4487, Sunriver, OR 97707, USA; Emeritus, University of California Abstract: Early phytoseiid mites colonizing the plant habitat probably were generalized types with omnivorous food habits. Various life styles and body plans evolved, some adapted to exploiting certain foods, others to cope with specific plant characteristics. Marked specialization for utilizing as prey spider mites producing copious webbing probably evolved independently in at least 4 of the 16 tribes (taxonomic revision of Chant & McMurtry 2007) across 2 of the 3 subfamilies. The Phytoseiulus species are the most specialized predators (Type I) of Tetranychus spp. The Galendromus spp. and some Neoseiulus prefer spider mites (Type II) but also utilize other prey. All species closely associated with spider mites producing copious webbing (Types I and II) seem to have long dorsal (j-j) and some lateral (z and s-s) setae. Hypotheses are discussed regarding the function of these long setae. Are ALL species with long j-j setae closely associated with spider mites spinning dense webbing? This is probably true of some genera or species groups, but not enough is known about others with long setae. Also discussed is whether specialization has been documented for other types of mite prey, such as tetranychids that produce only a small amount of webbing, tenuipalpids, eriophyoids and tarsonemids. Species with generalist feeding habits (Type III) seem to be predominant in most tribes. There exists a wide range of body plans, some of which seem more closely related to the plant habitat than to food source. Examples are preferences for hairy leaves (Phytoseius and Paraphytoseius, in different subfamilies), preferences for grasses or palms (Neoseiulus paspalivorus group), associations with eriophyoid galls (Neoseiulus desertus group (could this be a prey preference?), and preference for certain plant growth stages (Typhlodromalus aripo on apical growth and Amblydromalus manihoti on mature growth of cassava). Some fairly limited host plant ranges are known for Paragignathus (Neoseiulini) and Eharius (Kampimodromini) where no prey have been identified. Smooth species (i.e., those with mostly minute setae on the dorsal surface) are often associated with smooth foliage and have a high activity level. Ambyseius species fall into this category. Some genera considered in Type III, in which species valuable for biological control have been documented include Typhlodromus (e.g. pyri), Neoseiulus (cucumeris, barkeri), Kampimodromus (aberrans), Amblyseius (andersoni), Amblydromalus (aripo), Typhlodromalus (manihoti), and Scapulaseius (newsami). Two genera in the tribe Euseiini evolved unique characteristics (short, stubby chelicerae and wide deutosternum), presumably for utilizing pollen as a food source (Type IV). Population increases are sometimes related to airborne pollen fallout on the foliage. Iphiseius degenerans and some Euseius species have been documented as suppressing pest mite populations. Biological control programs continue to stimulate advances in systematics of the Phytoseiidae. Key words: Phytoseiidae, phytoseiid classification, biological control of phytophagous mites 62

81 Integrated Control of Plant-Feeding Mites IOBC/wprs Bulletin Vol. 50, 2009 p. 63 Whitefly-induced plant defences in cucumber and their impact on biological control of spider mites Gerben J. Messelink 1, Arne Janssen 2 1 Wageningen UR Greenhouse Horticulture, PO Box 20, 2265 ZG Bleiswijk, The Netherlands 2 IBED, Section Population Biology, University of Amsterdam, PO Box 94084, 1090 GB Amsterdam, The Netherlands Abstract: Whiteflies are known to induce plant responses, which have physical and chemical effects on herbivores and their natural enemies. Possibly because of the importance of whiteflies as pest species, research has mainly focused on the impact of these responses on whiteflies (herbivoreinduced direct defence). The indirect defences through herbivore-induced plant volatiles that promote the activity of natural enemies of whiteflies have also been studied widely. The impact on other (nonwhitefly) herbivores has been relatively overlooked. We studied plant-mediated effects of the greenhouse whitefly Trialeurodes vaporariorum (Westwood) on the spider mite Tetranychus urticae (Koch) infesting cucumber. We observed a reduction in spider mite population growth of up to 30% on whitefly-infested plants. The two pest species were spatially separated on the plants, so the effects were indirect and thus plant-mediated. The consequences of these plant responses for biological control of spider mites were substantial: both the phytoseiid predators Phytoseiulus persimilis (Athias- Henriot) and Neoseiulus californicus (McGregor) reduced spider mites to low levels much quicker on whitefly-treated plants than on control plants. Inhibition of spider mite development did not occur on cucumber plants treated with the cabbage whitefly Aleyrodes proletella (Linnaeus). The adults of this species easily survive and oviposit on cucumber plants, but crawlers were observed to die shortly after egg hatching. We therefore suggest that the indirect plant responses to whiteflies are caused by feeding of the nymphs but not by feeding of adults. Plant responses to whiteflies are supposed to be specific by inducing specific genes that transcribe pathogenesis-related proteins (Walling, 2000). The exact mechanism in our study is not clear yet, but might be comparable. To our knowledge, this study is the first to report whitefly-induced plant responses on spider mites. Reciprocal effects were observed in cotton, where an early infection with Tetranychus turkestani (Ugarov & Nikolskii) reduced the population level of whiteflies later on in the season (Agrawal et al., 2000). Future research will focus on possible applications for pest control as well as on the elucidation of the underlying mechanisms. Key words: induced resistance, cucumber, Tetranychus urticae, Trialeurodes vaporariorum References Agrawal, A.A., Karban, R. & Colfer, R.G. 2000: How leaf domatia and induced plant resistance affect herbivores, natural enemies and plant performance. Oikos 89: Walling, L.L. 2000: The myriad plant responses to herbivores. Journal of Plant Growth Regulation 19:

82 Integrated Control of Plant-Feeding Mites IOBC/wprs Bulletin Vol. 50, 2009 p. 64 Failure of methyl bromide fumigations to exterminate mites present on grapes exported to Mexico from Chile Gabriel Otero-Colina 1, Francisco Ramírez y Ramírez 2, Héctor Enrique Vega Ortiz 2 1 Colegio de Postgraduados Campus Montecillo, km Carretera Mexico-Texcoco. Montecillo, Mex., Dirección General de Sanidad Vegetal, Guillermo Pérez Valenzuela No. 127, Coyoacán, México, D.F Abstract: Brevipalpus chilensis is an important pest of grapes, whose current distribution is restricted to Chile and Argentina. To prevent its introduction into Mexico, grapes to be imported from Chile must be fumigated with methyl bromide. Inspectors in the ports of entry detected living mites on grapes from Chile, probably B. chilensis, as well as apparently viable eggs, some even in the process of hatching. A study was therefore conducted to identify mites present on grapes imported by Mexico from Chile, and to determine if living mites were present on grapes, whether mobile forms or eggs. A first lot of grapes imported from Chile on January 2007 had been fumigated with 64 g/m 3 methyl bromide for 2 h; a second lot, imported from Chile on March 2007, had been fumigated with methyl bromide for 2.5 h. Samples from both lots were inspected to detect associated mites. Representatives of visually different mites were mounted and identified. In addition, mite eggs were observed on grapes and their peduncles: 67 from the first lot and 380 from the second lot. Mite eggs with a portion of the substrate they were found on were incubated on fresh grape leaves placed upside down on observation arenas, to determine if viable eggs were present. Incubation conditions were: 25 C, 50-60% R.H., photoperiod 14L: 10D h, and a minimum incubation time of 21 days. Every 3-4 days grape leaves were replaced by fresh ones. All grape leaves used during the study were previously checked under a stereomicroscope to eliminate all arthropods. In the first lot of grapes, B. chilensis and Tetranychus sp. were identified, whereas in the second lot, Oligonychus vitis, Tetranychus urticae, B. chilensis, Neotarsonemoides sp., unidentified eriophyid mites and Tyrophagus sp. were identified; all specimens from both lots were found dead. Both O. vitis and B. chilensis are not present in Mexico, so they constitute a hazard of being introduced into the country together with infested grapes. Fumigation with methyl bromide was targeted against B. chilensis; however, O. vitis is equally important and should be added to the list of quarantine species. Eggs of O. vitis and B. chilensis were identified by their close association with their adults and because some contained easily recognizable embryos. They clearly differed from each other in shape and size, and as no sample contained both O. vitis and B. chilensis, the risk of misidentification was low. After incubation of 67 eggs from the first lot of Chilean grapes, three specimens of Bryobia sp. and nine specimens of Ereynetes amplectorus hatched. One Bryobia sp. and nine specimens of E. amplectorus reached adulthood. After incubation of 380 eggs from the second lot, two specimens of O. vitis and one specimen of a Tydeus sp. And an E. amplectorus hatched. They remained alive until adulthood but did not oviposite. Hatching was estimated at 18% for the first lot and 0.8% for the second, suggesting that a higher fumigation time increases efficacy. However, the study shows that fumigation with methyl bromide does not result in total annihilation of mites and that surviving mites are able to feed and grow; eggs seemed the most resistant stage. 64

83 Integrated Control of Plant-Feeding Mites IOBC/wprs Bulletin Vol. 50, 2009 pp Mutual interference of Scolothrips longicornis Priesner (Thysanoptera: Thripidae) on Tetranychus urticae Koch (Acari: Tetranychidae) Hajar Pakyari 1, Yaghoub Fathipour 2 1 Department of Plant Protection, Islamic Azad University, Takestan Branch, Iran, - Member of Young Researchers Club of Takestan Branch-Iran; 2 Department of Entomology, Faculty of Agriculture, Tarbiat Modares University, P.O. Box ; Tehran, Iran, Abstract: The mutual interference of the predatory thrips Scolothrips longicornis Priesner on the twospotted spider mite, Tetranychus urticae Koch was studied in 24 h time period at 26 ±1 C, 60 ±5% RH and a photoperiod of 16:8 L:D h. Nicholson's model and linear regression were used to determine per capita searching efficiency and interference coefficient, respectively. The per capita searching efficiency decreased significantly from to as the predator densities increased from one to sixteen. Therefore, different densities of the predator (intraspecific competition) could affect the efficacy of Scolothrips longicornis. Key words: two-spotted spider mite, predatory thrips, Scolothrips longicornis, Tetranychus urticae Introduction Spider mites (Acari: Tetranychidae) are widespread agricultural pests, which often cause severe damage to various crops (Gerlach & Sengonca, 1985). The use of fertilizers and chemicals seems to enhance their intrinsic powers of increase (Van de Vrie et al., 1972). Biological control is an alternative to their chemical control. Predatory thrips (Thysanoptera) are among the natural enemies of spider mites. All species of the genus Scolothrips appear to be specialized predators of spider mites (Priesner, 1950). Scolothrips longicornis Priesner is a native beneficial thrips in Iran. It is common in bean, cucumber and tomato fields and is considered to be an important predator of numerous spider mite species (Pakyari et al., 2008). The phenomenon of mutual interference was initially modelled by Hassell and Varely (1969), who found an inverse relationship between a predator's searching efficiency and and its density. Understanding the mutual interference of predators is necessary for the success of biological control programs, as it assists with mass rearing efforts and can facilitate the explanation of observed outcomes in the field (Fathipour et al., 2006). Therefore, in this study we determined the mutual interference (intraspecific competition) of Scolothrips longicornis on Tetranychus urticae under laboratory conditions. Material and methods Mite and thrips colony The colony of T. urticae was initiated using individuals collected from cucumber fields of Varamin (Tehran province). The mites were maintained on detached cucumber leaves placed upside down on a layer of wet cotton inside Petri dishes (150 mm in diameter). The lids of the Petri dishes had a 30 mm diameter hole covered with fine nylon mesh to allow ventilation. 65

84 66 The dishes were kept in a growth chamber at 26±1 C, 60±10% RH and a photoperiod of 16L: 8D h. A laboratory colony of S. longicornis was initiated with adults collected from the same cucumber fields, placed on leaves infested with an ample number of spider mites. Each leaf was placed in a Petri dish (180 mm in diameter) and maintained in another growth chamber set at the above-mentioned conditions. Adult thrips were transferred to newly infested cucumber leaves every 2 days. After a rearing period of 2 and 3 months for thrips and spider mites, respectively, the experiments were initiated. Test arena Bean leaf discs without major veins (30 mm in diameter) were cut and used as the test arena. Each disc was placed upside down on a layer of wet cotton inside Petri dishes. The lids of the Petri dishes had a hole covered with fine nylon mesh to allow ventilation. Experimental design Three hundred and twenty eggs of T. urticae were placed in each Petri dish. Different densities of one, two, four, eight and sixteen 1-day-old S. longicornis were added on each leaf and the number of eggs eaten was determined after 24 h. Experiments were carried out in the laboratory (conditions as above) and replicated ten times. The per capita searching efficiency (a) of the predator at different predator densities was calculated according to the following equation (Nicholson 1933): a = (1/PT) ln (N t/(n t-n a )) where N t is total number of available preys (=320), N a is the total number of prey eaten, P is the number of predators and T is the duration of the experiment. Searching efficiency was fitted against the predator density on a logarithmic scale. The points were fitted to a linear regression by the least square method, according to the inductive model provided by Hassell and Varley (1969) as follows: Log a = log Q - m log P where a is the searching efficiency of the predator, Q is the quest constant, and m includes only the component of interference due to behavioural interactions between predators (Free et al., 1977). Results and discussion The per capita predation rate decreased significantly from to with increasing predator densities from one to sixteen, with 320 prey eggs (F= 43.76; df = 4,45; P<0.01). Therefore, the per capita searching efficiency decreased significantly from to when increasing predator densities from one to sixteen (F= 22.76; df = 4,45; P<0.01) (Table 1). The linear regression between the natural logarithm of per capita searching efficiency and the natural logarithm of predator density in this analysis is demonstrated in the equation: Log a = Log p (R 2 = 0.92) where the interference coefficient (slope of the regression line) is m= The regression line is shown in Figure 1 using the natural logarithmic scale on both axes. The negative value of the regression slope indicates an inverse relationship between predator density and its per capita searching efficiency.

85 67 Table 1. Per capita predation rate and per capita searching efficiency (mean±se) of Scolothrips longicornis on Tetranychus urticae (values followed by different letters within columns are significantly different, P<0.01). Predator densities Per capita predation 12.50±0.563 a 9.95±0.329 b 9.225±0.304 bc 8.452±0.145 c 6.502±0.103 d Per capita searching efficiency (a) ±1.869 a ±1.056 b ±1.139 bc ±6.197 bc ±4.744 c Log per capita searching effeciency Log predator density y = x R 2 = Fig. 1. Regression line describing the mutual interference of Scolothrips longicornis. A similar result was reported in a study on the mutual interference of the predatory mite Phytoseiulus persimilis (Acari: Phytoseiidae) where the predation rate on T. urticae decreased per capita with increasing predator densities (Nachmann, 2006). Van den Meiracker et al. (1999) reported that the per capita predation rate of Orious insidiosus was low, even when numbers of the western flower thrips as prey were high. With the increasing number of predatory thrips, greater numbers of prey were predated. Therefore, in order to predate a greater number of spider mites, more spider mite predators are required. However, a doubling in the number of predators employed for spider mite predation did not result in doubling the number of prey eaten, owing to mutual interference. The reason that S. longicornis consumed fewer spider mites at their higher densities may be attributed to mutual interference between the predator individuals. This is probably due to a closed experimental arena with limited predation time and a high probability of mutual interference. Although laboratory data do not adequately explain these interactions in the field, other factors in field conditions like interspecific competition with other predators, spatial complexity, and weather may adversely influence the effectiveness of natural enemies (Gintonga et al., 2002).

86 68 Finally, by understanding these interactions, we will be able to develop suitable strategies for the biological control of T. urticae using predators in both greenhouse and field conditions. References Fathipour, Y., Hosseini, A., Talebi, A.A. & Moharramipour, S. 2006: Functional response and mutual interference of Diaeretiella rapae (Hymenoptera: Aphidiidae) on Brevicoryne brassicae (Homoptera: Aphididae). Ent. Fennica 17: Free, C.A., Beddington, J.R. & Lawton, J.H. 1977: On the inadequacy of simple models of mutual interference for parasitism and predation. J. Anim. Ecol. 46: Gerlach, S. & Sengonca, C. 1985: Comparative studies on the effectiveness of the predatory mite, Phytoseiulus persimilis and the predatory thrips Scolothrips longicornis. Zeitschrift f. Pflanzenkrankheiten Pflanzenschutz 92: Gitonga, L.M., Overholt, W.A., Lohr, B., Magambo, J.K. & Mucke, J.M Functional response of Orius albidipenis (Hemiptera: Anthocoridae) to Megalurothrips sjostedti (Thysanoptera: Thripidae). Biol. Control 24: 1-6. Hassell, M.P. & Varley, G.C. 1969: New inductive population model for insect parasites and its bearing on biological control. Nature 223: Nachman, G The effects of prey patchiness, predator aggregation, and mutual interference on the functional response of Phytoseiulus persimilis feeding on Tetranychus urticae (Acari: Phytoseiidae, Tetranychidae). Exp. Appl. Acar.38: Nicholson, A.J. 1933: The balance of animal populations. J. Anim. Ecol. 2: Pakyari, H., Fathipour, Y., Rezapanah, M. & Kamali, K Prey-stage preference in Scolothrips longicornis Priesner (Thysanoptera: Thripidae) on Tetranychus urticae Koch (Acari: Tetranychidae). IOBC/wprs Bulletin 32: Priesner, H. 1950: Studies on the genus Scolothrips. Bull. Soc. Roy. d Entomol. Egypte 34: Van de Vrie, M., McMurtry, J.A. & Huffaker, C.B. 1972: Ecology of tetranychid mite and their natural enemies. A review. III. Biology, ecology and pest status, and host plant relations of tetranychids. Hilgardia 41: Van den Meiracker, R.A.F. & Sabelis, M.W. 1999: Do functional responses of predatory arthropods reach a plateau? A case study of Orius insidiosus with western flower thrips as prey. Ent. Exp. Applicata 90:

87 Integrated Control of Plant-Feeding Mites IOBC/wprs Bulletin Vol. 50, 2009 pp Predator-prey dynamics and strategies for control of the red palm mite (Raoiella indica) (Acari: Tenuipalpidae) in areas of invasion in the Neotropics Jorge E. Peña 1, Jose Carlos V. Rodrigues 2, Amy Roda 3, Daniel Carrillo 1 and Lance S. Osborne 4 1 University of Florida, Tropical REC, Homestead, FL 33031, USA; 2 University of Puerto Rico, 1193 Calle Guayacan, San Juan Puerto Rico; 3 USDA, APHIS, Plant Protection & Quarantine, Miami, FL 33158, USA; 4 University of Florida, Mid-Florida- REC, Apoka, FL., 32703, USA Abstract: The red Palm mite, Raoiella indica (Acari: Tenuipalpidae) invaded the new world around 2004 and is now reported from the Caribbean islands, Florida, USA and northern South America (Venezuela). Surveys to determine generalist fauna prior to its arrival during the end of 2007 in Florida, reported the predators Amblyseius largoensis, Stethorus utilis, Chrysoperla spp., Aleurodothrips fasciapennis and Bdella distincta in association with diaspidids, aleyorids and tetranychids. Predator density increase was not observed until 6 months after the arrival of R. indica in Florida. Studies on predator composition after the initial detection in 2006 of R. indica in Trinidad and Tobago, indicated that the predaceous mite, A. largoensis increased its densities as the red palm mite grew and spread to new locations. Other reported predators were A. fasciapennis, Bdella spp., Cheletomimus sp., and species of the families Cecidomyiidae and Chrysopidae. Amblyseius largoensis, while preying on the red palm mite in Puerto Rico, has not substantially reduced the high numbers of R. indica. Studies to find exotic and more effective predators of the red palm mite should be intensified. Key words: coconuts, red palm mite, phytoseiid mites, biological control Introduction The red palm mite (RPM), Raoiella indica Hirst, (Acari: Tenuipalpidae), also known as the coconut mite (Somchoudhury & Sarkar, 1987), coconut red mite (Jalaluddin & Mohanasundaran, 1990), red date palm mite (Elwan, 2000), leaflet false spider mite (FAO, 2005), frond crimson mite, scarlet mite (Gassouma, 2005) is an important pest of coconuts, date palm, other palm species (PROSEA, 2006), and bananas, beans, and durian in different parts of the world. Previous to its arrival in the New World, the mite was found in India, Philippines, Mauritius, Reunion, Malaysia, Israel and Egypt. Raoiella indica was found in Martinique and St. Lucia in During 2005, RPM was found in Dominica and during 2006 on the islands of Trinidad, Guadeloupe and Saint Martin (Kane et al., 2005; Etienne & Fletchmann, 2006), and in Puerto Rico (Rodrigues et al., 2007). The mite was discovered in Florida during December 2007 (Peña et al., 2008). Damages to coconut, ornamental palms and bananas are extensive. It is considered that the pest has serious consequences for the coconut, ornamental palm and banana industries of the Caribbean islands. Damage to coconuts results in a 70% yield reduction and possibly job losses, which lead to a major socio-economic problem for some of the islands (Mr. Philippe Agostini, President Trinidad and Tobago Coconut Growers Assoc., Pers. Comm). In Florida, cost of regulatory actions, such as precautionary sprays before shipping R. indica hosts to other states, will represent an 69

88 70 additional production cost of more than half a million dollars to palm nursery producers per year. Raoiella indica is found on the underside of the leaves of the host plant in very large numbers. On coconuts, attacked leaves display on the upperside uneven dark patches that correspond with the area where the mites are located, this is followed by necrosis of the patches; when seen from a distance, the fronds become yellowish to bronze-orange, followed by necrosis. Heavy mite infestations result in the death of young plants. Management programs for this mite in areas where it is present, as well as preventative programs for areas where it has not yet arrived, are urgently needed. Past chemical control tactics against R. indica were proven inefficacious and costly in India and Egypt, but they are considered necessary for regulatory purposes in infested palm exporting areas (Florida & Puerto Rico). Biological control is one of the most important alternatives to conventional pesticide use in pest management. Classical biological control, or the introduction of natural enemies from the areas of origin for R. indica has been initiated under the auspices of APHIS, PPQ (Marjorie Hoy, pers. comm.), resulting in the quarantine screening of one classical biocontrol candidate. Prior to release of any exotic predator, it is necessary to put greater emphasis on other areas of biological control, such as natural enemy conservation and augmentation. The objectives of this study were 1) to determine the density of predators and herbivorous micro-arthropods associated with palms and bananas in Florida before the arrival of R. indica and record the response of the current beneficial fauna to the invading mite in Trinidad, Puerto Rico and Florida. Materials and methods Generalist fauna prior invasion by the red palm mite in Florida A survey for natural predators infesting palms and bananas was carried out in South Florida, where most of the palm, Musa, gingers and heliconid production is concentrated. Monthly surveys were conducted in Miami-Dade and Monroe counties in the landscape on coconut palms and on bananas from the end of 2005 until Twenty pinnae per frond were collected per palm species while 20 sections (ea. ~ 60 cm 2 ) were removed from a banana leaf. Samples were taken to the laboratory, where densities of microarthropods, i.e., tetranychids, tenuipalpids, diaspidids, phytoseiids, bdellids and others were recorded, labeled and mounted and sent for identification by specialists. Predator composition in Trinidad and Tobago. A study was conducted at the St. Andrews Estate coconut plantation,-cedros, Trinidad, to determine the distribution of R. indica and predators in the canopy of a coconut tree. Fronds were collected from the upper (leaf 3), mid (leaf 9) and lower (leaf 13) canopy from 5 trees and 9 pinna from each frond representing the top, middle and base were sampled. All motile RPM and predators were counted under a steromicroscope. A predator was determined by having observed it to feed on R. indica. Predator abundance in Puerto Rico Samples were taken monthly in 8 different sites around Puerto Rico by collecting 10 leaflets, 3 replicates per site, and washing them in 80% ethanol. Ethanol wash samples were then inspected in the laboratory under a stereomicroscope to record presence and abundance of red palm mites and potential predators.

89 71 Naturally occurring generalist predators currently preying on R. indica in Florida Eight coconut palms were selected in two areas in West Palm Beach ( N W) and Broward ( N W). Once each month, since the time of the discovery of the R. indica invasion on December 2007, a single pinna was collected from each of two fronds per palm, totaling 16 samples per site. Each pinna was placed in a plastic bag, sealed and placed in a refrigerated cooler, and frozen before evaluation. Each sample was examined under the microscope, and number of red palm mite, tetranychids, diaspidid scales, whiteflies, mealybugs and different predaceous arthropods (Phytoseiidae, Neuroptera, Thripidae, Coccinellidae) was recorded. Preliminary tests to determine the efficacy of commercial predators that show potential for control of R. indica Several commercially produced predators will be tested for efficacy to feed, survive and reproduce on R. indica (i.e., Amblyseius swirskii, Phytoseiulus persimilis, Neoseiulus longipes, N. californicus, Galendromus occidentalis). The predator Amblyseius swirskii was selected for a preliminary trial under laboratory conditions. The arena consisted of a 5 cm petri dish placed inside of a 12 cm petri dish. Water was added to the larger petri dish to prevent predator or prey escape from the arena. A 4 cm 2 section of a coconut frond that held a known number of different stages of R. indica was added. Then, presumably mated 1 to 2 day old single females were individually placed inside of the arena. The number of eggs, nymphs and adults consumed daily was calculated and new food sources added daily. Results and discussion Generalist fauna prior to invasion by the red palm mite in Florida The scale, Aonidiella orientalis (Newstead) (Heteroptera: Diaspididae), the whitefly, Aleurocanthus woglumi Ashby (Heteroptera: Aleyrodidae) and the spider mites, Tetranychus spp., Tetranychus gloveri Banks (Acari: Tetranychidae), were the most common microarthropods inhabiting coconuts, while Tetranychus sp., and Brevipalpus spp., were the most common inhabiting bananas from 2006 to 2008 in areas before the arrival of RPM (Figures 1 and 2). On coconuts, the predators, Amblyseius largoensis (Muma) (Acari: Phytoseiidae), Stethorus utilis (Horn) and Chrysoperla spp., (Neuroptera: Chrysopidae) were the most common predators followed by Bdella distincta (Barker and Bullock) (Acari: Bdellidae) and Aleurodothrips fasciapennis (Franklin) (Thysanoptera: Phlaeothripidae). On bananas, the predators Amblyseius spp., and Stethorus utilis were recorded (Figures 3 and 4). Amblyseius largoensis was the only phytoseiid on coconuts, while the identification of the Amblyseius sp. found in bananas is pending. Amblyseius largoensis is a generalist feeding not only on mites, but also on pollen (Yue & Tsai, 1996). A study conducted in Brazil to determine the survival of A. largoensis on Aceria guerreronis (Acari: Eryophidae), a pest of coconuts and on other food sources (pollen and honey), determined that a mixed diet of A. guerreronis, or T. urticae + pollen and + honey increased the predator's fertility parameters (Galvao et al., 2008). Although A. largoensis is one of two predators found earlier in The Philippines in association with Rarosiella cocosae Rimando (= Raoiella indica) (Gallego et al., 2002), its efficacy has not been determined yet. Amblyseius. largoensis was also found in association with Aceria guerreronis (Acari: Eryophidae) on coconuts fruits, but no clear prey preference has yet been determined for this species on that plant (Reis et al., 2008). The predaceous thrips, A. fasciapennis, was previously reported feeding on eggs of diaspidid scales such as Chrysomphalum aonidum and Aspidiotus nerii and on eggs of the pyralid moth, Corcyra cephalonica (Watson et al., 2004; Beshear & Nakahara, 1975).

90 72 Stethorus utilis is cited as a common predator of tetranychid mites (Chazeau, 1985). In general, because of the high densities of both diaspidids and aleroydids present on coconuts, the prey preference for the native predators needs further study under Florida conditions. Figure 1. Dynamics of herbivorous micro-arthropods inhabiting coconuts prior to establishment of R. indica in south Florida (Miami-Dade). Figure 2. Dynamics of natural enemies inhabiting coconuts prior to establishment of R. indica in south Florida (Miami-Dade).

91 73 Figure 3. Dynamics of herbivorous micro-arthropods inhabiting bananas prior ot establishment of R. indica in south Florida (Miami-Dade) Figure 4. Dynamics of natural enemies inhbiting bananas prior to establishment of R. indica in south Florida (Miami-Dade).

92 74 Predator composition in Trinidad and Tobago Raoiella indica rapidly spread throughout Trinidad after its initial detection in May Since September 2006, changes in RPM and predatory mite populations were monitored at the St. Andrews coconut estate, Cedros, Trinidad. Red palm mite populations increased dramatically, doubling at each sampling period. More mites were initially found in the lower canopy, but as the quality of these fronds decreased, red palm mite populations shifted to upper portions of the canopy. Interestingly A. largoensis increased in numbers as the RPM population grew and it followed the pest to new locations in the coconut canopy. However, the increase in A. largoensis numbers did not cause a corresponding decrease in R. indica numbers. The other predators seen feeding on red palm, Aleurodothrips fasciapennis, Bdella sp., Cheletomimus sp (Acari: Cheyletidae), Ceciodmyiidae and Chrysopidae (Figure 5), did not increase in numbers nor did they follow RPM movement to other locations in the canopy. The predators not identified to species are likely new species. A B C Figure 5: Predators observed preying upon R. indica included Aleurodothrips fasciapennis (A) pictured feeding on a R. indica larvae, Cheletomimus sp. (B) pictured feeding on a R. indica adult female, and a possible ceciodmyiid larvae (C) pictured feeding on a R. indica egg. Predator abundance in Puerto Rico Raoiella indica was first reported from eastern Puerto Rico in late October, 2006 (Rodrigues et al., 2007) and has since spread through the island. Both R. indica and natural enemy populations have been monitored. Four months after the first report in Puerto Rico the pest was observed around Ponce (central south part of the island) about 50km from the original detection sites. Later, in December 2007, RPM populations were seen on the extreme west side of Puerto Rico. Phytoseiids mites, crisopids and predatory thrips species were observed in association with R. indica populations (Figure 6). Samples from adult coconut palms (10 leaflets, 3 replicates per site) were washed in 200mL of 80% ethanol, which was then inspected in the laboratory under a stereomicroscope for the presence of red palm mites and potential phytoseiid mite predators. Mite specimens were slide mounted for species confirmation. Amblyseius largoensis was the most common potential predator observed associated with RPM in the palm samples. Variations of the pest populations among different localities and over time were observed (Figure 7). Comparing the different sites, one saw that the arrival of RPM was followed by an increase in phytoseiid mites (data not shown). Correlation between populations of phytoseiid mites and the occurrence of red palm mite on coconut were statistically significant.

93 75 Despite the increase of Amblyseius after the reported arrival of R. indica, the predator has not substantially reduced the high numbers of RPM. In order to control the pest's outbreaks and minimize the its damages, work to find exotic natural enemies should be intensified. In addition, we developed a PCR-based method to identify the phytoseiid mites feeding on RPM. This method could be applied to identify R. indica predators in samples taken directly from the field. Figure 6. Predator species observed in Puerto Rico associated with Raoiella indica. Left: Amblyseius largoensis; observe the coloration inside, the mite's digestive tract after it has fed on a red palm mite. Right: a chrysopid larva observed feeding on R. indica. Naturally occurring generalist predators currently preying on R. indica in Florida The relationships between phytoseiid predators, i.e., A. largoensis and the potential new prey were erratic. For instance, while an increase in predator density was observed following an increase in the prey during January-February, and May -June, 2008, numbers of predators were still consistently low, compared to the number of prey present Site - Humacao Numbe of 1500 RPM 15 Number of Phyt Oct-07 Nov-07 Dec-07 Jan-08 Feb-08 Mar-08 Apr-08 May-08 Jun-08 Jul-08 Aug-08 0 Figure 7. Population dynamics of Raoiella indica and Amblyseius largoensis in coconut palms, Humacao, Puerto Rico. Average of number of mites per 10 leaflets, three repetitions.

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