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Detection of Pesticides and Viruses in Dead Honey Bees and Other Matrices

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Detection of Pesticides and Viruses in Dead Honey Bees and Other Matrices Journal of Apicultural Research ISSN: 0021-8839 (Print) 2078-6913 (Online) Journal homepage: http://www.tandfonline.com/loi/tjar20 Spring mortality in honey bees in northeastern Italy: detection of pesticides and viruses in dead honey bees and other matrices Marianna Martinello, Chiara Baratto, Chiara Manzinello, Elena Piva, Alice Borin, Marica Toson, Anna Granato, Maria Beatrice Boniotti, Albino Gallina & Franco Mutinelli To cite this article: Marianna Martinello, Chiara Baratto, Chiara Manzinello, Elena Piva, Alice Borin, Marica Toson, Anna Granato, Maria Beatrice Boniotti, Albino Gallina & Franco Mutinelli (2017): Spring mortality in honey bees in northeastern Italy: detection of pesticides and viruses in dead honey bees and other matrices, Journal of Apicultural Research To link to this article: http://dx.doi.org/10.1080/00218839.2017.1304878 View supplementary material Published online: 04 Apr 2017. Submit your article to this journal View related articles View Crossmark data Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=tjar20 Download by: [Istituto Zooprofilatico] Date: 04 April 2017, At: 02:49 Journal of Apicultural Research, 2017 http://dx.doi.org/10.1080/00218839.2017.1304878 ORIGINAL RESEARCH ARTICLE Spring mortality in honey bees in northeastern Italy: detection of pesticides and viruses in dead honey bees and other matrices Marianna Martinelloa , Chiara Barattoa, Chiara Manzinelloa, Elena Pivaa, Alice Borina, Marica Tosonb, Anna Granatoa, Maria Beatrice Boniottic, Albino Gallinaa and Franco Mutinellia* aNational Reference Laboratory for Beekeeping, Istituto Zooprofilattico Sperimentale delle Venezie, Legnaro, Padua, Italy; bVeterinary Epidemiology Department, Istituto Zooprofilattico Sperimentale delle Venezie, Legnaro, Padua, Italy; cIstituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia Romagna, Brescia, Italy (Received 28 October 2016; accepted 7 March 2017) In spring there is often a rise in honey bee mortality incidents. The aim of this study was to investigate the potential correlation, in the reported incidents, between exposure to pesticide treatments and virus infections. Here we summa- rize the situation in northeastern Italy during spring 2014, evaluated by monitoring 150 active ingredients and three honey bee viruses in dead honey bees and other matrices. At least one active ingredient was found in 72.2% of the 79 dead honey bee samples, with the most abundant (59.4%) being insecticides, mainly belonging to the class of neonicoti- noids (41.8%), followed by fungicides (40.6%). Imidacloprid, chlorpyrifos, tau-fluvalinate, and cyprodinil were the most frequently detected active ingredients. Multiple virus infections were monitored, revealing a high prevalence of chronic bee paralysis virus (CBPV) and deformed wing virus (DWV), detected in all samples except one. 71 and 37% of the CBPV- and DWV positive samples, respectively, showed a high number of viral copies per bee (>107). This work emphasizes the possible relationship between spring mortality in honey bees and pesticide treatments. Honey bee viruses could synergistically exacerbate the negative impact of pesticides on honey bee health, endangering the survival of colonies. Mortalidad primaveral en las abejas melı´feras del noreste de Italia: deteccio´n de los plaguicidas y los virus en las abejas melı´feras muertas y en otras matrices En primavera suele haber un aumento en los incidentes de mortalidad de las abejas. El objetivo de este estudio fue investigar la correlacio´n potencial entre los incidentes comunicados y la exposicio´n a tratamientos con plaguicidas y las infecciones vı´ricas. Aquı´ resumimos la situacio´n en el noreste de Italia durante la primavera de 2014, evaluada mediante la monitorizacio´n de 150 ingredientes y tres virus de la abeja melı´fera en las abejas muertas y en otras matrices. Se encontro´ al menos un ingrediente activo en un 72.2% de las 79 muestras de abejas de la miel muertas, siendo los ma´s abundantes los insecticidas (59.4%), principalmente pertenecientes a la clase de los neonicotinoides (41.8%), seguidos por los fungicidas (40.6%). Los ingredientes activos detectados con mayor frecuencia fueron: imidacloprid, clorpirifos, taufluvalinato, y ciprodinil. Se monitorizaron mu´ltiples infecciones vı´ricas, revelando una alta prevalencia del virus de la para´lisis cro´nica de las abejas (VPCA) y el virus de las alas deformadas (VAD), que se detectaron en todas las muestras excepto en una. El 71% y 37% de las muestras positivas a VPCA y VAD, respectivamente, mostraron un alto nu´mero de copias del virus por abeja (>107). Este trabajo enfatiza la posible relacio´n entre la mortalidad primaveral de las abejas de la miel y los tratamientos con plaguicidas. Los virus de las abejas melı´feras podrı´an exacerbar sine´rgicamente el impacto negativo de los plaguicidas en la salud de las abejas de la miel, poniendo en peligro la supervivencia de las colmenas. Keywords: honey bees; spring mortality; plant protection products; pesticide; virus Introduction means, or would produce significantly less food In recent years, the gradual decline in wild or commer- (Kremen et al., 2007). The most recent estimate of the cially managed honey bee colonies (Goulson, Nicholls, global economic benefit of pollination amounts to a Botias, & Rotheray, 2015) is a much debated topic and value of US$ 235–US$ 577 billion, according to data by has attracted increasing interest not only from experts Lautenbach, Seppelt, Liebscher, and Dormann (2012), but also from the general public. Insect-mediated polli- actualized by IPBES in 2016 (IPBES, 2016). nation is critical to the maintenance of biodiversity and Managed honey bees are significant pollinators and global food security. Furthermore, it has been estimated their decline in recent years in North America and that without this “ecosystem service” about one third Europe (Brodschneider et al., 2016; Genersch et al., of the tonnage of the crops we eat (and most of the 2010; Higes et al., 2010; Lee et al., 2015; Potts, Roberts, wild plants) would have to be pollinated by other et al., 2010; Steinhauer et al., 2014; van der Zee et al., *Corresponding author. Email: [email protected] © 2017 International Bee Research Association 2 M. Martinello et al. 2012) has become a widely studied phenomenon. Differ- 2013a, 2013b, 2013c). In February 2015, EFSA was ent factors are involved in this problem, including honey requested by the European Commission to organize an bee diseases (Dietemann et al., 2012; Higes et al., 2010; open call for new scientific information regarding the Le Conte, Ellis, & Ritter, 2010; Traynor et al., 2016), risk to bees from three neonicotinoids, namely clothian- honey bee management practices and disease control idin, thiamethoxam and imidacloprid (EFSA, 2015b). In treatments (Giacobino et al., 2015), nutrition (Alaux, November 2016, EFSA published its conclusion reports Ducloz, Crauser, & Le Conte, 2010b; Archer, Pirk, on clothianidin and imidacloprid in the light of submitted Wright, & Nicolson, 2014; Brodschneider & Crailsheim, confirmatory data (EFSA, 2016a, 2016b). The evaluation 2010; Odoux et al., 2012), and climatic trends (Le was performed in the peer review setting requested by Conte & Navajas, 2008), but many recent publications the European Commission, following the submission and (Brittain, Vighi, Bommarco, Settele, & Potts, 2010; Gen- evaluation of confirmatory ecotoxicological data con- ersch et al., 2010; Krupke, Hunt, Eitzer, Andino, & cerning the risk assessment for bees. The conclusions Given, 2012; Lee et al., 2015; Mullin et al., 2010; Porrini were based on the evaluation of representative uses of et al., 2016; Potts, Biesmeijer et al., 2010; Potts, clothianidin as an insecticide on winter cereals, beet, Roberts, et al., 2010; vanEngelsdorp et al., 2009) suspect potato, maize/sweet maize, sorghum and forestry nurs- the profound impact of agricultural practices and the ery, and representative uses of imidacloprid as an insec- varied and massive use of chemicals. A fact sheet about ticide on winter cereals, beet, potato, leafy vegetables the European Union’s (EU) agri-environmental indicator and amenity vegetation. It also presented reliable end- on consumption of pesticides is available on the Euro- points deemed appropriate for use in regulatory risk stat website (Eurostat, 2016), providing an overview of assessment, derived from the available studies and litera- recent data, accompanied by exhaustive information on ture in the peer reviewed dossier. Missing information the definitions, measurement methods and context identified as being required to permit a complete risk needed to interpret them correctly. assessment was listed and concerns were identified. New growing seasons bring a rise in the amount and In 2013, EFSA developed a guidance document on number of plant protection product (PPP) applications the risk assessment of PPPs on bees (EFSA, 2013e). The and this may be related to increased honey bee mortal- document is intended to provide guidance for notifiers ity events. In Italy, for example, fairly isolated honey bee and authorities in the context of the review of PPPs and incidents have been described since 2000, but the sever- the active substances they contain under Regulation ity of events increased dramatically in the spring of 2008 (EC) No. 1107/2009. The guidance document suggested (Bortolotti et al., 2009). In 2009, a national monitoring the implementation
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