DOCSLIB.ORG

Neonicotinoids and Honeybee Health

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Neonicotinoids and Honeybee Health Department of Ecology Neonicotinoids and honeybee health The effect of the neonicotinoid clothianidin, applied as a seed dressing in Brassica napus, on pathogen and parasite prevalence and quantities in free-foraging adult honeybees (Apis mellifera) Julia Goss European Master of Environmental Science (EnvEuro) Uppsala 2014 Independent project/Degree project / SLU, Department of Ecology 2014:4 Neonicotinoids and honeybee health The effect of the neonicotinoid clothianidin, applied as a seed dressing in Brassica napus, on pathogen and parasite prevalence and quantities in free-foraging adult honeybees (Apis mellifera) Supervisor: Dr. Joachim Rodrigues de Miranda, SLU, Department of Ecology Assistant Supervisor: Prof. Dr. Ingemar Fries, SLU, Department of Ecology Co-supervisor: Prof. Dr. Peter Rosenkranz, University of Hohenheim Examiner: Dr. Bengt Olsson, SLU, Department of Ecology Credits: 30 hec Level: A2E Course title: Independent Project in Environmental Science – Master’s thesis Course code: EX0431 Programme/education: European Master in Environmental Science (EnvEuro) Place of publication: Uppsala Year of publication: 2014 Cover picture: Foraging honeybee, Julia Goss 2013 Title of series: Independent project/Degree project / SLU, Department of Ecology Part no: 2014:4 Online publication: http://stud.epsilon.slu.se Keywords: honeybees; pathogens; parasites; virus; Nosema; Varroa; neonicotinoids; clothianidin Sveriges lantbruksuniversitet Swedish University of Agricultural Sciences Faculty of Natural Resources and Agricultural Sciences Department of Ecology Table of content Table of content Figures .................................................................................................................................................... IV Equations ................................................................................................................................................ V Tables ...................................................................................................................................................... V Abbreviations ......................................................................................................................................... VI Abstract ................................................................................................................................................. VII Svensk sammanfattning ....................................................................................................................... VIII Zusammenfassung ................................................................................................................................. IX 1. Introduction .................................................................................................................................... 1 1.1 The importance of bees .......................................................................................................... 2 1.2 Colony losses ........................................................................................................................... 3 1.3 Honeybee immunity................................................................................................................ 5 1.4 Parasites and Pathogens ......................................................................................................... 6 1.4.1 Varroa destructor ............................................................................................................ 6 1.4.2 Nosema ........................................................................................................................... 7 1.4.3 Viruses ............................................................................................................................. 7 1.5 Neonicotinoids ...................................................................................................................... 10 1.5.1 Lethal effects of neonicotinoids on honeybees ............................................................ 12 1.5.2 Sub-lethal effects of neonicotinoids on honeybees ..................................................... 12 1.6 Aim ........................................................................................................................................ 13 1.7 Hypothesis ............................................................................................................................. 13 2. Methods ........................................................................................................................................ 14 2.1 General structure of the study .............................................................................................. 14 2.2 Laboratory work .................................................................................................................... 17 2.2.1 Varroa destructor .......................................................................................................... 17 I Table of content 2.2.2 Preparation of a bee/water solution ............................................................................ 18 2.2.3 Determining the Nosema spp. prevalence and infestation rate ................................... 18 2.2.4 Nucleic acid detection ................................................................................................... 21 2.2.4.1 RNA and DNA extraction ............................................................................................... 21 2.2.4.2 Real time quantitative polymerase chain reaction (qPCR) ........................................... 22 2.2.4.3 DNA analysis for N. apis and N. ceranae ....................................................................... 23 2.2.4.4 RNA analysis for different viruses ................................................................................. 24 2.3 Statistical Analysis ................................................................................................................. 26 3. Results ........................................................................................................................................... 28 3.1 Varroa destructor .................................................................................................................. 28 3.2 Nosema spp. .......................................................................................................................... 29 3.3 Comparison of two methods to quantify Nosema spp. ........................................................ 31 3.4 Viral diseases ......................................................................................................................... 32 3.4.1 Black queen cell virus .................................................................................................... 32 1.1.1 Sacbrood virus ............................................................................................................... 32 1.1.2 Deformed wing virus ..................................................................................................... 34 2. Discussion ...................................................................................................................................... 35 2.1 Methods used ....................................................................................................................... 35 2.1.1 Field experimental setup .............................................................................................. 35 2.1.2 Laboratory work ............................................................................................................ 35 2.2 Results ................................................................................................................................... 36 2.2.1 Varroa destructor .......................................................................................................... 36 2.2.2 Nosema apis and Nosema ceranae ............................................................................... 37 2.2.3 Different methods used for Nosema ............................................................................ 38 2.2.4 Viruses ........................................................................................................................... 38 2.3 Social immunity versus individual immunity ........................................................................ 40 2.4 Sustainable use of pesticides ................................................................................................ 40 3. Conclusion ..................................................................................................................................... 43 II Table of content Acknowledgment .................................................................................................................................. 44 Literature .............................................................................................................................................. 45 Appendices ............................................................................................................................................ 53 Appendix 1: Primers used for RT-qPCR ............................................................................................. 53 Appendix 2: Code for SAS ................................................................................................................. 54 Appendices 3: SAS output for all tests .............................................................................................
Load more

Recommended publications
  • Evidence for and Against Deformed Wing Virus Spillover from Honey Bees to Bumble Bees: a Reverse Genetic Analysis Olesya N
    www.nature.com/scientificreports OPEN Evidence for and against deformed wing virus spillover from honey bees to bumble bees: a reverse genetic analysis Olesya N. Gusachenko1*, Luke Woodford1, Katharin Balbirnie‑Cumming1, Eugene V. Ryabov2 & David J. Evans1* Deformed wing virus (DWV) is a persistent pathogen of European honey bees and the major contributor to overwintering colony losses. The prevalence of DWV in honey bees has led to signifcant concerns about spillover of the virus to other pollinating species. Bumble bees are both a major group of wild and commercially‑reared pollinators. Several studies have reported pathogen spillover of DWV from honey bees to bumble bees, but evidence of a sustained viral infection characterized by virus replication and accumulation has yet to be demonstrated. Here we investigate the infectivity and transmission of DWV in bumble bees using the buf-tailed bumble bee Bombus terrestris as a model. We apply a reverse genetics approach combined with controlled laboratory conditions to detect and monitor DWV infection. A novel reverse genetics system for three representative DWV variants, including the two master variants of DWV—type A and B—was used. Our results directly confrm DWV replication in bumble bees but also demonstrate striking resistance to infection by certain transmission routes. Bumble bees may support DWV replication but it is not clear how infection could occur under natural environmental conditions. Deformed wing virus (DWV) is a widely established pathogen of the European honey bee, Apis mellifera. In synergistic action with its vector—the parasitic mite Varroa destructor—it has had a devastating impact on the health of honey bee colonies globally1,2.
    [Show full text]
  • Bee Viruses: Routes of Infection in Hymenoptera
    fmicb-11-00943 May 27, 2020 Time: 14:39 # 1 REVIEW published: 28 May 2020 doi: 10.3389/fmicb.2020.00943 Bee Viruses: Routes of Infection in Hymenoptera Orlando Yañez1,2*, Niels Piot3, Anne Dalmon4, Joachim R. de Miranda5, Panuwan Chantawannakul6,7, Delphine Panziera8,9, Esmaeil Amiri10,11, Guy Smagghe3, Declan Schroeder12,13 and Nor Chejanovsky14* 1 Institute of Bee Health, Vetsuisse Faculty, University of Bern, Bern, Switzerland, 2 Agroscope, Swiss Bee Research Centre, Bern, Switzerland, 3 Laboratory of Agrozoology, Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium, 4 INRAE, Unité de Recherche Abeilles et Environnement, Avignon, France, 5 Department of Ecology, Swedish University of Agricultural Sciences, Uppsala, Sweden, 6 Environmental Science Research Center, Faculty of Science, Chiang Mai University, Chiang Mai, Thailand, 7 Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai, Thailand, 8 General Zoology, Institute for Biology, Martin-Luther-University of Halle-Wittenberg, Halle (Saale), Germany, 9 Halle-Jena-Leipzig, German Centre for Integrative Biodiversity Research (iDiv), Leipzig, Germany, 10 Department of Biology, University of North Carolina at Greensboro, Greensboro, NC, United States, 11 Department Edited by: of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, United States, 12 Department of Veterinary Akio Adachi, Population Medicine, College of Veterinary Medicine, University of Minnesota, Saint Paul, MN, United States,
    [Show full text]
  • Bee Viruses: Routes of Infection in Hymenoptera
    fmicb-11-00943 May 27, 2020 Time: 14:39 # 1 View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Bern Open Repository and Information System (BORIS) REVIEW published: 28 May 2020 doi: 10.3389/fmicb.2020.00943 Bee Viruses: Routes of Infection in Hymenoptera Orlando Yañez1,2*, Niels Piot3, Anne Dalmon4, Joachim R. de Miranda5, Panuwan Chantawannakul6,7, Delphine Panziera8,9, Esmaeil Amiri10,11, Guy Smagghe3, Declan Schroeder12,13 and Nor Chejanovsky14* 1 Institute of Bee Health, Vetsuisse Faculty, University of Bern, Bern, Switzerland, 2 Agroscope, Swiss Bee Research Centre, Bern, Switzerland, 3 Laboratory of Agrozoology, Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium, 4 INRAE, Unité de Recherche Abeilles et Environnement, Avignon, France, 5 Department of Ecology, Swedish University of Agricultural Sciences, Uppsala, Sweden, 6 Environmental Science Research Center, Faculty of Science, Chiang Mai University, Chiang Mai, Thailand, 7 Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai, Thailand, 8 General Zoology, Institute for Biology, Martin-Luther-University of Halle-Wittenberg, Halle (Saale), Germany, 9 Halle-Jena-Leipzig, German Centre for Integrative Biodiversity Research (iDiv), Leipzig, Germany, 10 Department of Biology, University of North Carolina at Greensboro, Greensboro, NC, United States, 11 Department Edited by: of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, United States, 12 Department
    [Show full text]
  • Virus Prevalence and Genetic Diversity Across a Wild Bumblebee Community
    fmicb-12-650747 April 16, 2021 Time: 19:12 # 1 ORIGINAL RESEARCH published: 22 April 2021 doi: 10.3389/fmicb.2021.650747 Virus Prevalence and Genetic Diversity Across a Wild Bumblebee Community David J. Pascall1,2*, Matthew C. Tinsley3, Bethany L. Clark4,5, Darren J. Obbard6 and Lena Wilfert2,7* 1 Institute of Biodiversity, Animal Health and Comparative Medicine, Boyd Orr Centre for Population and Ecosystem Health, University of Glasgow, Glasgow, United Kingdom, 2 Centre for Ecology and Conservation, University of Exeter, Cornwall, United Kingdom, 3 Biological and Environmental Sciences, University of Stirling, Stirling, United Kingdom, 4 BirdLife International, The David Attenborough Building, Cambridge, United Kingdom, 5 Environment and Sustainability Institute, University of Exeter, Cornwall, United Kingdom, 6 Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, United Kingdom, 7 Institute of Evolutionary Ecology and Conservation Genomics, Ulm University, Ulm, Germany Edited by: Akio Adachi, Viruses are key population regulators, but we have limited knowledge of the diversity Kansai Medical University, Japan and ecology of viruses. This is even the case in wild host populations that provide Reviewed by: ecosystem services, where small fitness effects may have major ecological impacts Scott McArt, Cornell University, United States in aggregate. One such group of hosts are the bumblebees, which have a major Michelle Flenniken, role in the pollination of food crops and have suffered population declines and Montana State University, range contractions in recent decades. In this study, we investigate the diversity of United States four recently discovered bumblebee viruses (Mayfield virus 1, Mayfield virus 2, River *Correspondence: David J. Pascall Liunaeg virus, and Loch Morlich virus), and two previously known viruses that infect [email protected] both wild bumblebees and managed honeybees (Acute bee paralysis virus and Slow Lena Wilfert [email protected] bee paralysis virus) from isolates in Scotland.
    [Show full text]
  • The Spread and Evolution of RNA Viruses Among Honey Bees and the Wider Insect Community with Particular Emphasis on Deformed Wing Virus (DWV)
    The spread and evolution of RNA viruses among honey bees and the wider insect community with particular emphasis on Deformed wing virus (DWV). Laura Emily BRETTELL Ph.D. Thesis 2017 School of Environment and Life Sciences University of Salford CONTENTS CONTENTS ............................................................................................................................................... 1 LIST OF FIGURES ...................................................................................................................................... 5 General Introduction........................................................................................................................... 5 Chapter 1: A comparison of Deformed wing virus in deformed and asymptomatic honey bees. ..... 5 Chapter 2: Oldest Varroa tolerant honey bee population provides insight into the origins of the global decline of honey bees. ............................................................................................................. 7 Chapter 4: Moku virus; a new Iflavirus found in wasps, honey bees and Varroa. ............................. 8 Chapter 5: Common apiary pests as a potential source of honey bee – associated viruses in a Hawaiian apiary environment. ............................................................................................................ 9 LIST OF TABLES ...................................................................................................................................... 10 Chapter 1: A comparison
    [Show full text]
  • Identification of New Viruses Specific to the Honey Bee Mite Varroa Destructor
    bioRxiv preprint doi: https://doi.org/10.1101/610170; this version posted April 16, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Identification of new viruses specific to the honey bee mite Varroa destructor Salvador Herrero*, Sandra Coll, Rosa M. González-Martínez, Stefano Parenti, Anabel Millán-Leiva, Joel González-Cabrera* ERI BIOTECMED. Department of Genetics. Universitat de València, Valencia, Spain. *Corresponding authors: Email: [email protected], tel: +34 96 354 3006 Email: [email protected], tel: +34 96 354 3122 Keywords: iflavirus, picornavirus, insobevirus, qPCR, +ssRNA virus 1 bioRxiv preprint doi: https://doi.org/10.1101/610170; this version posted April 16, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Abstract Large-scale colony losses among managed Western honey bees have become a serious threat to the beekeeping industry in the last decade. There are multiple factors contributing to these losses but the impact of Varroa destructor parasitism is by far the most important, along with the contribution of some pathogenic viruses vectored by the mite. So far, more than 20 viruses have been identified infecting the honey bee, most of them RNA viruses. They may be maintained either as covert infections or causing severe symptomatic infections, compromising the viability of the colony. In silico analysis of available transcriptomic data obtained from mites collected in the USA and Europe as well as additional investigation with new samples collected locally allowed the description of three novel RNA viruses.
    [Show full text]
  • H SURREY the Food and Environment Research Agency Proquest Number: U583701
    Epidemiology and Taxonomy of Honey Bee Viruses in England and Wales by Guido Cordoni Submitted for the degree of Doctor of Philosophy Faculty of Health and Medical Sciences University of Surrey August 2011 © Guido Cordoni 2011 ^ UNIVERSITY OF H fifa h SURREY The Food and Environment Research Agency ProQuest Number: U583701 All rights reserved INFORMATION TO ALL USERS The quality of this reproduction is dependent upon the quality of the copy submitted. In the unlikely event that the author did not send a com plete manuscript and there are missing pages, these will be noted. Also, if material had to be removed, a note will indicate the deletion. uest ProQuest U583701 Published by ProQuest LLO (2019). Copyright of the Dissertation is held by the Author. All rights reserved. This work is protected against unauthorized copying under Title 17, United States C ode Microform Edition © ProQuest LLO. ProQuest LLO. 789 East Eisenhower Parkway P.Q. Box 1346 Ann Arbor, Ml 48106- 1346 This dissertation and the work to which it refers are the results of my own efforts. Any ideas, data, images or text resulting from the work of others (whether published or unpublished) are fully identified as such within the work and attributed to their originator in the text, bibliography or in footnotes. This thesis has not been submitted in whole or in part for any other academic degree or professional qualification. I agree that the University has the right to submit my work to a plagiarism detection service for originality checks. Contents Abstract 7 Acknowledgements
    [Show full text]
  • (ABPV, BQCV, CBPV, DWV, LSV3 and SBV) in Healthy and Clinically Affected Honeybees with Taqman Quantitative Real-Time RT-PCR Assays
    viruses Article The Comparison of Honeybee Viral Loads for Six Honeybee Viruses (ABPV, BQCV, CBPV, DWV, LSV3 and SBV) in Healthy and Clinically Affected Honeybees with TaqMan Quantitative Real-Time RT-PCR Assays Laura Šimenc 1,*, Tanja Knific 2 and Ivan Toplak 1 1 Virology Unit, Institute of Microbiology and Parasitology, Veterinary Faculty, University of Ljubljana, Gerbiˇceva60, 1115 Ljubljana, Slovenia; [email protected] 2 Institute of Food Safety, Feed and Environment, Veterinary Faculty, University of Ljubljana, Gerbiˇceva60, 1115 Ljubljana, Slovenia; tanja.knifi[email protected] * Correspondence: [email protected] Abstract: The viral loads of acute bee paralysis virus (ABPV), black queen cell virus (BQCV), chronic bee paralysis virus (CBPV), deformed wing virus (DWV), Lake Sinai virus 3 (LSV3), and sacbrood bee virus (SBV) were determined in samples with the use of quantitative TaqMan real-time reverse transcription and polymerase chain reaction (RT-qPCR). A total of 108 samples of healthy adult honeybees from four differently located apiaries and samples of honeybees showing different clinical signs of viral infections from 89 apiaries were collected throughout Slovenia. The aim of this study was to discover correlations between viral loads and clinical signs in adult honeybees and Citation: Šimenc, L.; Knific, T.; confirm previously set threshold viral load levels between healthy and clinically affected honeybees. Toplak, I. The Comparison of Within this study, two new RT-qPCR assays for quantification of LSV3 and SBV were developed. Honeybee Viral Loads for Six Honeybee Viruses (ABPV, BQCV, Statistically significant differences in viral loads of positive samples were identified between healthy CBPV, DWV, LSV3 and SBV) in and clinically affected honeybees for ABPV, CBPV, DWV, and SBV, while for BQCV and LSV3, no Healthy and Clinically Affected statistical differences were observed between both groups.
    [Show full text]
  • Condition-Dependent Virulence of Slow Bee Paralysis Virus in Bombus
    Oecologia DOI 10.1007/s00442-017-3851-2 HIGHLIGHTED STUDENT RESEARCH Condition‑dependent virulence of slow bee paralysis virus in Bombus terrestris: are the impacts of honeybee viruses in wild pollinators underestimated? Robyn Manley1 · Mike Boots1,2 · Lena Wilfert1 Received: 12 September 2016 / Accepted: 8 March 2017 © The Author(s) 2017. This article is an open access publication Abstract Slow bee paralysis virus (SBPV)—previously and starvation conditions. SBPV infection resulted in sig- considered an obligate honeybee disease—is now known nificant virulence under starvation conditions, with infected to be prevalent in bumblebee species. SBPV is highly viru- bees 1.6 times more likely to die at any given time point (a lent in honeybees in association with Varroa mites, but has median of 2.3 h earlier than uninfected bees), whereas there been considered relatively benign otherwise. However, was no effect under satiated conditions. This demonstrates condition-dependent pathogens can appear asymptomatic clear condition-dependent virulence for SBPV in B. ter- under good, resource abundant conditions, and negative restris. Infections that appear asymptomatic in non-stress- impacts on host fitness may only become apparent when ful laboratory assays may nevertheless have significant under stressful or resource-limited conditions. We tested impacts under natural conditions in the wild. For multi-host whether SBPV expresses condition-dependent virulence in pathogens such as SBPV, the use of sentinel host species in its bumblebee host, Bombus terrestris, by orally inoculat- laboratory assays may further lead to the underestimation ing bees with SBPV and recording longevity under satiated of pathogen impacts on other species in nature.
    [Show full text]
  • Highly Diverse Population of Picornaviridae and Other Members
    Yinda et al. BMC Genomics (2017) 18:249 DOI 10.1186/s12864-017-3632-7 RESEARCH ARTICLE Open Access Highly diverse population of Picornaviridae and other members of the Picornavirales,in Cameroonian fruit bats Claude Kwe Yinda1,2, Roland Zell3, Ward Deboutte1, Mark Zeller1, Nádia Conceição-Neto1,2, Elisabeth Heylen1, Piet Maes2, Nick J. Knowles4, Stephen Mbigha Ghogomu5, Marc Van Ranst2 and Jelle Matthijnssens1* Abstract Background: The order Picornavirales represents a diverse group of positive-stranded RNA viruses with small non- enveloped icosahedral virions. Recently, bats have been identified as an important reservoir of several highly pathogenic human viruses. Since many members of the Picornaviridae family cause a wide range of diseases in humans and animals, this study aimed to characterize members of the order Picornavirales in fruit bat populations located in the Southwest region of Cameroon. These bat populations are frequently in close contact with humans due to hunting, selling and eating practices, which provides ample opportunity for interspecies transmissions. Results: Fecal samples from 87 fruit bats (Eidolon helvum and Epomophorus gambianus), were combined into 25 pools and analyzed using viral metagenomics. In total, Picornavirales reads were found in 19 pools, and (near) complete genomes of 11 picorna-like viruses were obtained from 7 of these pools. The picorna-like viruses possessed varied genomic organizations (monocistronic or dicistronic), and arrangements of gene cassettes. Some of the viruses belonged to established families, including the Picornaviridae, whereas others clustered distantly from known viruses and most likely represent novel genera and families. Phylogenetic and nucleotide composition analyses suggested that mammals were the likely host species of bat sapelovirus, bat kunsagivirus and bat crohivirus, whereas the remaining viruses (named bat iflavirus, bat posalivirus, bat fisalivirus, bat cripavirus, bat felisavirus, bat dicibavirus and bat badiciviruses 1 and 2) were most likely diet-derived.
    [Show full text]
  • Putative Receptor for Israeli Acute Paralysis Virus of the Honey Bee (Apis Mellifera) Shunji Li Iowa State University
    Iowa State University Capstones, Theses and Graduate Theses and Dissertations Dissertations 2017 Putative receptor for Israeli acute paralysis virus of the honey bee (Apis mellifera) Shunji Li Iowa State University Follow this and additional works at: https://lib.dr.iastate.edu/etd Part of the Entomology Commons Recommended Citation Li, Shunji, "Putative receptor for Israeli acute paralysis virus of the honey bee (Apis mellifera)" (2017). Graduate Theses and Dissertations. 17252. https://lib.dr.iastate.edu/etd/17252 This Thesis is brought to you for free and open access by the Iowa State University Capstones, Theses and Dissertations at Iowa State University Digital Repository. It has been accepted for inclusion in Graduate Theses and Dissertations by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. Putative receptor for Israeli acute paralysis virus of the honey bee ( Apis mellifera ) by Shunji Li A thesis submitted to the graduate faculty in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE Major: Entomology Program of Study Committee: Bryony C. Bonning, Co-major Professor Amy L. Toth Co-major Professor Ryan C. Smith Iowa State University Ames, Iowa 2017 Copyright © Shunji Li, 2017. All rights reserved. ii TABLE OF CONTENTS Page ACKNOWLEDGEMENTS .......................................................................................................... iii ABSTRACT ..............................................................................................................................
    [Show full text]
  • Bee Viruses: Routes of Infection in Hymenoptera
    Bee viruses: routes of infection in Hymenoptera Article Published Version Creative Commons: Attribution 4.0 (CC-BY) Open Access Yañez, O., Piot, N., Dalmon, A., de Miranda, J. R., Chantawannakul, P., Panziera, D., Amiri, E., Smagghe, G., Schroeder, D. and Chejanovsky, N. (2020) Bee viruses: routes of infection in Hymenoptera. Frontiers in Microbiology, 11. 943. ISSN 1664-302X doi: https://doi.org/10.3389/fmicb.2020.00943 Available at http://centaur.reading.ac.uk/91209/ It is advisable to refer to the publisher’s version if you intend to cite from the work. See Guidance on citing . To link to this article DOI: http://dx.doi.org/10.3389/fmicb.2020.00943 Publisher: Frontiers All outputs in CentAUR are protected by Intellectual Property Rights law, including copyright law. Copyright and IPR is retained by the creators or other copyright holders. Terms and conditions for use of this material are defined in the End User Agreement . www.reading.ac.uk/centaur CentAUR Central Archive at the University of Reading Reading’s research outputs online fmicb-11-00943 May 27, 2020 Time: 14:39 # 1 REVIEW published: 28 May 2020 doi: 10.3389/fmicb.2020.00943 Bee Viruses: Routes of Infection in Hymenoptera Orlando Yañez1,2*, Niels Piot3, Anne Dalmon4, Joachim R. de Miranda5, Panuwan Chantawannakul6,7, Delphine Panziera8,9, Esmaeil Amiri10,11, Guy Smagghe3, Declan Schroeder12,13 and Nor Chejanovsky14* 1 Institute of Bee Health, Vetsuisse Faculty, University of Bern, Bern, Switzerland, 2 Agroscope, Swiss Bee Research Centre, Bern, Switzerland, 3 Laboratory of
    [Show full text]