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Biological parameters of the invasive brown marmorated stink bug, Halyomorpha halys, in southern Europe

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Abstract

The brown marmorated stink bug, Halyomorpha halys, is an invasive pest species, first detected in Italy in 2012. Only 2 years after this first detection, increasing damage was reported in fruit orchards in the Emilia Romagna region, the first invaded area, which is one of the most important regions for the Italian and European fruit production. In the present study, life table parameters of H. halys populations were investigated in Italy under typical temperate/Mediterranean climate conditions representative of southern Europe. Our findings indicate that in Italy H. halys has two generations/year and very high reproductive rates for both generations (R 0 = 24.04 and 5.44 for the overwintering and summer generation, respectively). The huge growth rates explain why in 2015 a massive outbreak of H. halys was observed in Italy, and these rates confirm that the pest is a threat for agricultural production in southern Europe. The parameters obtained in this study are essential for the development and optimization of sustainable management strategies.

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Acknowledgements

This research was partially supported by the grant ‘Innovative tools and protocols for monitoring and sustainable control of the alien stink bug Halyomorpha halys, a new phytosanitary threat, and of other harmful heteropterans for the fruit crops of the territory of Modena’ (2013.065) of ‘Fondazione Cassa di Risparmio di Modena’. We are also grateful to the UNIMORE students Giulia Pinotti and Valentina Mammi who helped with the experimental work.

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Correspondence to E. Costi.

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Communicated by M. Traugott.

Special Issue: The brown marmorated stink bug Halyomorpha halys an emerging pest of global concern.

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Costi, E., Haye, T. & Maistrello, L. Biological parameters of the invasive brown marmorated stink bug, Halyomorpha halys, in southern Europe. J Pest Sci 90, 1059–1067 (2017). https://doi.org/10.1007/s10340-017-0899-z

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