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      New opportunities for the integration of microorganisms into biological pest control systems in greenhouse crops

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          Abstract

          Biological pest control with mass-produced arthropod natural enemies is well developed in greenhouse crops and has often resulted in the evolution of complex ecosystems with persistent populations of multiple arthropod natural enemy species. However, there are cases where arthropod natural enemies are either not effective enough, not available, or their use is rather costly. For these reasons, biological control based on microorganisms, also referred to as ‘microbials’, represents a complementary strategy for further development. Although commercially available microbials have been around for quite some time, research on and the applied use of combinations of arthropod natural enemies and microbials have remained relatively under explored. Here, we review current uses of entomopathogenic fungi, bacteria and viruses, and their possible direct and indirect effects on arthropod natural enemies in European greenhouses. We discuss how microbials might be combined with arthropod natural enemies in the light of new methodologies and technologies such as conservation biological control, greenhouse climate management, and formulation and delivery. Furthermore, we explore the possibilities of using other microorganisms for biological control, such as endophytes, and the need to understand the effect of insect-associated microorganisms, or symbionts, on the success of biological control. Finally, we suggest future research directions to optimize the combined use of microbials and arthropod natural enemies in greenhouse production.

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          Most cited references143

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          Wolbachia: master manipulators of invertebrate biology.

          Wolbachia are common intracellular bacteria that are found in arthropods and nematodes. These alphaproteobacteria endosymbionts are transmitted vertically through host eggs and alter host biology in diverse ways, including the induction of reproductive manipulations, such as feminization, parthenogenesis, male killing and sperm-egg incompatibility. They can also move horizontally across species boundaries, resulting in a widespread and global distribution in diverse invertebrate hosts. Here, we review the basic biology of Wolbachia, with emphasis on recent advances in our understanding of these fascinating endosymbionts.
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            Fungal endophytes: diversity and functional roles.

            All plants in natural ecosystems appear to be symbiotic with fungal endophytes. This highly diverse group of fungi can have profound impacts on plant communities through increasing fitness by conferring abiotic and biotic stress tolerance, increasing biomass and decreasing water consumption, or decreasing fitness by altering resource allocation. Despite more than 100 yr of research resulting in thousands of journal articles, the ecological significance of these fungi remains poorly characterized. Historically, two endophytic groups (clavicipitaceous (C) and nonclavicipitaceous (NC)) have been discriminated based on phylogeny and life history traits. Here, we show that NC-endophytes represent three distinct functional groups based on host colonization and transmission, in planta biodiversity and fitness benefits conferred to hosts. Using this framework, we contrast the life histories, interactions with hosts and potential roles in plant ecophysiology of C- and NC-endophytes, and highlight several key questions for future work in endophyte biology.
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              Habitat management to conserve natural enemies of arthropod pests in agriculture.

              Many agroecosystems are unfavorable environments for natural enemies due to high levels of disturbance. Habitat management, a form of conservation biological control, is an ecologically based approach aimed at favoring natural enemies and enhancing biological control in agricultural systems. The goal of habitat management is to create a suitable ecological infrastructure within the agricultural landscape to provide resources such as food for adult natural enemies, alternative prey or hosts, and shelter from adverse conditions. These resources must be integrated into the landscape in a way that is spatially and temporally favorable to natural enemies and practical for producers to implement. The rapidly expanding literature on habitat management is reviewed with attention to practices for favoring predators and parasitoids, implementation of habitat management, and the contributions of modeling and ecological theory to this developing area of conservation biological control. The potential to integrate the goals of habitat management for natural enemies and nature conservation is discussed.
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                Author and article information

                Contributors
                gerben.messelink@wur.nl
                Journal
                J Pest Sci (2004)
                J Pest Sci (2004)
                Journal of Pest Science
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                1612-4758
                1612-4766
                21 March 2016
                21 March 2016
                2016
                : 89
                : 295-311
                Affiliations
                [ ]Department of Plant Protection Biology, Swedish University of Agricultural Sciences, Växtskyddsvägen 3, P.O. Box 23053, Alnarp, Sweden
                [ ]Department of Plant Protection and Breeding, Siedlce University of Natural Sciences and Humanities, Prusa 14 Street, 08-110 Siedlce, Poland
                [ ]Research-Development Institute for Plant Protection, Bd. Ion Ionescu de la Brad nr. 8, Sector 1, P.O. Box 013813, Bucharest, Romania
                [ ]Department of Biological Control, Institute of Plant Protection – NRI, Władysława Węgorka 20 Street, 60-318 Poznań, Poland
                [ ]Department of Crop Sciences, Agricultural Entomology, Georg-August-University, Grisebachstrasse 6, 37077 Goettingen, Germany
                [ ]Department of Entomology, NeweYa’ar Research Center, P.O. Box 1021, 30095 Ramat Yishay, Israel
                [ ]Wageningen UR Greenhouse Horticulture, PO Box 20, 2265 ZG Bleiswijk, The Netherlands
                Author notes

                Communicated by N. Desneux.

                Author information
                http://orcid.org/0000-0002-5196-1229
                Article
                751
                10.1007/s10340-016-0751-x
                4880627
                27340390
                9a2b5eb7-4a3c-4f8d-aed6-5a32317261a0
                © The Author(s) 2016

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

                History
                : 20 November 2015
                : 16 February 2016
                : 7 March 2016
                Categories
                Review
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                © Springer-Verlag Berlin Heidelberg 2016

                Pests, Diseases & Weeds
                arthropod natural enemies,microbials,entomopathogens,endophytes,symbionts
                Pests, Diseases & Weeds
                arthropod natural enemies, microbials, entomopathogens, endophytes, symbionts

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