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      Assessing the Distribution of Exotic Egg Parasitoids of Halyomorpha halys in Europe with a Large-Scale Monitoring Program

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      1 , 2 , 1 , 3 , 4 , 5 , 6 , 6 , 5 , 7 , 8 , 9 , 10 , 9 , 11 , 12 , 13 , 9 , 6 , 14 , 12 , 15 , 16 , 2 , 15 , 17 , 18 , 15 , 11 , 19 , 12 , 2 , 20 , 7 , 21 , 12 , *
      Insects
      MDPI
      biological control, BMSB, exotic biological control agents, invasive species, natural enemies, Trissolcus japonicus, Trissolcus mitsukurii

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          Abstract

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          The management of invasive alien species is a very challenging task. For the brown marmorated stink bug ( Halyomorpha halys), classical biological control has been identified as the most suitable method to sustainably reduce its populations in the long-term. Among its natural enemies, two species were identified as the most promising candidates for biocontrol, Trissolcus japonicus and Trissolcus mitsukurii. Populations of these two species have recently been detected in Europe and to assess their distribution, a large-scale study was performed. Combining several monitoring methods, in four months (May–September 2019), a wide area covering northern Italy and parts of Switzerland was surveyed. The results showed that both species have spread into all types of habitats where H. halys is present and the parasitization of native species was rarely observed. Among native species, Anastatus bifasciatus was the predominant parasitoid of H. halys. This study supported the development of the first release program of Tr. japonicus in Europe.

          Abstract

          The brown marmorated stink bug Halyomorpha halys is an invasive agricultural pest with a worldwide distribution. Classical biological control has been identified as the most promising method to reduce the populations of H. halys. Adventive populations of two candidates for releases, Trissolcus japonicus and Trissolcus mitsukurii, have recently been detected in Europe. To assess their distribution and abundance, a large-scale survey was performed. From May to September 2019, a wide area covering northern Italy and parts of Switzerland was surveyed, highlighting the expanding distribution of both Tr. japonicus and Tr. mitsukurii. Within four years after their first detection in Europe, both species have rapidly spread into all types of habitats where H. halys is present, showing a wide distribution and continuous expansion. Both exotic Trissolcus showed high levels of parasitism rate towards H. halys, while parasitization of non-target species was a rare event. The generalist Anastatus bifasciatus was the predominant native parasitoid of H. halys, while the emergence of native scelionids from H. halys eggs was rarely observed. The presence of the hyperparasitoid Acroclisoides sinicus was also recorded. This study provided fundamental data that supported the development of the first inoculative release program of Tr. japonicus in Europe.

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          Biological control using invertebrates and microorganisms: plenty of new opportunities

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            Impact of the Invasive Brown Marmorated Stink Bug in North America and Europe: History, Biology, Ecology, and Management.

            The brown marmorated stink bug (BMSB), Halyomorpha halys (Stål), is an invasive pentatomid introduced from Asia into the United States, Canada, multiple European countries, and Chile. In 2010, BMSB populations in the mid-Atlantic United States reached outbreak levels and subsequent feeding severely damaged tree fruit as well as other crops. Significant nuisance issues from adults overwintering inside homes were common. BMSB is a highly polyphagous species with a strong dispersal capacity and high reproductive output, potentially enabling its spread and success in invaded regions. A greater understanding of BMSB biology and ecology and its natural enemies, the identification of the male-produced aggregation pheromone, and the recognition that BMSB disperses into crops from adjacent wooded habitats have led to the development of behavior-based integrated pest management (IPM) tactics. Much is still unknown about BMSB, and continued long-term collaborative studies are necessary to refine crop-specific IPM programs and enhance biological control across invaded landscapes.
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              Assessing risks of releasing exotic biological control agents of arthropod pests.

              More than 5000 introductions of about 2000 species of exotic arthropod agents for control of arthropod pests in 196 countries or islands during the past 120 years rarely have resulted in negative environmental effects. Yet, risks of environmental effects caused by releases of exotics are of growing concern. Twenty countries have implemented regulations for release of biological control agents. Soon, the International Standard for Phytosanitary Measures (ISPM3) will become the standard for all biological control introductions worldwide, but this standard does not provide methods by which to assess environmental risks. This review summarizes documented nontarget effects and discusses the development and application of comprehensive and quick-scan environmental risk assessment methods.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                Insects
                Insects
                insects
                Insects
                MDPI
                2075-4450
                01 April 2021
                April 2021
                : 12
                : 4
                : 316
                Affiliations
                [1 ]Centro Ricerca e Innovazione, Fondazione Edmund Mach (FEM), via Mach 1, 38098 S. Michele all’Adige, TN, Italy; livia.zapponi@ 123456fmach.it (L.Z.); gianfranco.anfora@ 123456unitn.it (G.A.)
                [2 ]Dipartimento di Scienze Agrarie, Forestali e Alimentari, University di Torino (UniTO), Largo Paolo Braccini 2, 10095 Grugliasco, TO, Italy; francesco.trt@ 123456gmail.com (F.T.); silvia.moraglio@ 123456unito.it (S.T.M.); luciana.tavella@ 123456unito.it (L.T.)
                [3 ]Centro Agricoltura Alimenti Ambiente (C3A), Università di Trento, Via Mach 1, 38098 S. Michele all’Adige, TN, Italy
                [4 ]Fondazione per la Ricerca l’Innovazione e lo Sviluppo Tecnologico dell’Agricoltura Piemontese (AGRION), Via Falicetto 24, 12100 Manta, CN, Italy; s.bardella@ 123456agrion.it
                [5 ]Servizio Fitosanitario Emilia-Romagna, via Andrea da Formigine 3, 40128 Bologna, Italy; massimo.bariselli@ 123456regione.emilia-romagna.it (M.B.); alda.butturini@ 123456regione.emilia-romagna.it (A.B.)
                [6 ]Servizio Fitosanitario Friuli Venezia Giulia (ERSA), via Sabbatini 5, 33050 Pozzuolo del Friuli, UD, Italy; luca.benvenuto@ 123456ersa.fvg.it (L.B.); iris.bernardinelli@ 123456ersa.fvg.it (I.B.); giorgio.malossini@ 123456ersa.fvg.it (G.M.)
                [7 ]Consorzio Fitosanitario di Modena, via Santi 14, Direzionale Cialdini 1, 41123 Modena, Italy; stefano.caruso@ 123456regione.emilia-romagna.it (S.C.); giacvac@ 123456gmail.com (G.V.)
                [8 ]Consorzio Fitosanitario di Piacenza, via Cristoforo Colombo 35, 29122 Piacenza, Italy; ruggero.colla@ 123456regione.emilia-romagna.it
                [9 ]Dipartimento di Scienze della Vita, Università di Modena e Reggio Emilia (UniMORE), Via G. Amendola 2, 42122 Reggio Emilia, Italy; elecosti@ 123456unimore.it (E.C.); emanuele.dibella@ 123456unimore.it (E.D.B.); lara.maistrello@ 123456unimore.it (L.M.)
                [10 ]Servizio Fitosanitario Lombardia (ERSAF), via Pola 12, 20124 Milano, Italy; paolo_culatti@ 123456regione.lombardia.it
                [11 ]Centro di Sperimentazione Laimburg, Laimburg 6, 39051 Pfatten/Vadena, BZ, Italy; Martina.Falagiarda@ 123456laimburg.it (M.F.); Silvia.Schmidt@ 123456laimburg.it (S.S.)
                [12 ]CREA, Research Centre for Plant Protection and Certification, via di Lanciola 12a, 50125 Firenze, Italy; lucrezia.giovannini@ 123456crea.gov.it (L.G.); leonardo.marianelli@ 123456crea.gov.it (L.M.); piofederico.roversi@ 123456crea.gov.it (P.F.R.)
                [13 ]CABI, Rue des Grillons 1, 2800 Delemont, Switzerland; t.haye@ 123456cabi.org
                [14 ]Dipartimento delle Finanze e dell’Economia, Servizio Fitosanitario Cantonale, Sezione dell’Agricoltura, Viale S. Franscini 17, 6500 Bellinzona, Switzerland; cristina.marazzi@ 123456ti.ch
                [15 ]Department of Agronomy Food Natural Resources Animals and Environment, Università degli Studi di Padova (UniPD), Viale dell’Università 16, 35020 Legnaro, PD, Italy; alberto.mele@ 123456studenti.unipd.it (A.M.); alberto.pozzebon@ 123456unipd.it (A.P.); davide.scaccini@ 123456phd.unipd.it (D.S.)
                [16 ]Condifesa Lombardia Nord-Est, Servizio Tecnico, via Malta 12, 25124 Brescia, BS, Italy; lorenza.michelon@ 123456alice.it
                [17 ]ASTRA, Astra Innovazione e Sviluppo srl, via Tebano 45, 48018 Faenza, RA, Italy; michele.preti@ 123456astrainnovazione.it
                [18 ]Fondazione Fojanini, via Valeriana 32, 23100 Sondrio, SO, Italy; msalvetti@ 123456fondazionefojanini.it
                [19 ]Strickhof, Fachstelle Obst, Riedhofstrasse 62, 8408 Winterthur, Switzerland; david.szalatnay@ 123456strickhof.ch
                [20 ]CRPV, Centro Ricerche Produzioni Vegetali, via dell’Arrigoni 120, 47522 Cesena, FC, Italy; mgtommasini@ 123456crpv.it
                [21 ]Department of Agricultural, Food, Environmental and Animal Sciences, Università di Udine (UniUD), Via delle Scienze 206, 33100 Udine, UD, Italy; pietro.zandigiacomo@ 123456uniud.it
                Author notes
                Author information
                https://orcid.org/0000-0003-4033-9001
                https://orcid.org/0000-0002-0071-3292
                https://orcid.org/0000-0003-2545-1409
                https://orcid.org/0000-0001-5459-5706
                https://orcid.org/0000-0002-2996-8993
                https://orcid.org/0000-0002-4132-5245
                https://orcid.org/0000-0003-1594-6133
                https://orcid.org/0000-0001-9922-5071
                https://orcid.org/0000-0002-2445-7211
                https://orcid.org/0000-0002-6944-5142
                https://orcid.org/0000-0002-6850-7911
                https://orcid.org/0000-0002-8098-8367
                https://orcid.org/0000-0002-3711-1017
                Article
                insects-12-00316
                10.3390/insects12040316
                8067160
                33915993
                5f35f17a-b1ab-475e-a847-e9c44f4893fe
                © 2021 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( https://creativecommons.org/licenses/by/4.0/).

                History
                : 19 February 2021
                : 27 March 2021
                Categories
                Article

                biological control,bmsb,exotic biological control agents,invasive species,natural enemies,trissolcus japonicus,trissolcus mitsukurii

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