The status of honey bee health in Italy: Results from the nationwide bee monitoring network

PLoS ONE

Volumn 11, Issue 5, 2016, Pages

  Porrini, Claudio ^a   Mutinelli, Franco ^a,b   Bortolotti, Laura ^c   Granato, Anna ^b   Laurenson, Lynn ^d   Roberts, Katherine ^d   Gallina, Albino ^b   Silvester, Nicholas ^b   Medrzycki, Piotr ^c   Renzi, Teresa ^a   Sgolastra, Fabio ^a   Lodesani, Marco ^c  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b ISTITUTO ZOOPROFILATTICO SPERIMENTALE DELLE VENEZIE   (Italy)

^c ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

^d FOOD AND ENVIRONMENT RESEARCH AGENCY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COUMAFOS; ORGANOPHOSPHATE INSECTICIDE; PROPOLIS; PYRETHROID; TAU FLUVALINATE; UNCLASSIFIED DRUG; PESTICIDE;

ACUTE BEE PARALYSIS VIRUS; ADULT; ANIMAL HEALTH; APIS IRIDESCENT VIRUS; ARTICLE; AUTUMN; BEE BREAD QUALITY; BEE MONITORING NETWORK; BIOLOGICAL MONITORING; BLACK QUEEN CELL VIRUS; CHRONIC BEE PARALYSIS VIRUS; COLONY LOSS; CONTAMINATION; CONTROLLED STUDY; DEFORMED WING VIRUS; ENVIRONMENTAL EXPOSURE; GEOGRAPHIC DISTRIBUTION; HEALTH STATUS; HONEYBEE; INSECTICIDE CONTAMINATION; ISRAELI ACUTE PARALYSIS VIRUS; ITALY; KASHMIR BEE VIRUS; LAND USE; MORTALITY; NONHUMAN; NOSEMA CERANAE; PARAMETERS; PARASITE PREVALENCE; PROTEIN CONTENT; QUALITY CONTROL; SACBROOD VIRUS; SEASONAL VARIATION; SPRING; VIRUS; VIRUS IDENTIFICATION; VIRUS INFECTION; ANIMAL; APICULTURE; BEE; CHEMISTRY; ECOSYSTEM MONITORING; ENVIRONMENTAL MONITORING; GEOGRAPHY; HEALTH SURVEY; HOST PATHOGEN INTERACTION; PHYSIOLOGY; POLLEN;

ANIMALS; BEEKEEPING; BEES; ECOLOGICAL PARAMETER MONITORING; ENVIRONMENTAL MONITORING; GEOGRAPHY; HEALTH STATUS; HOST-PATHOGEN INTERACTIONS; ITALY; PESTICIDES; POLLEN; POPULATION SURVEILLANCE;

EID: 84969722247     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0155411     Document Type: Article

References (63)

1. Aizen MA, Harder LD. The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr Biol 2009; 19: 1-4.
2. Potts SG, Roberts SPM, Dean R, Marris G, Brown MA, Jones HR, et al. Declines of managed honey bees and beekeepers in Europe. J Apic Res 2010; 49, 15-22.
3. Cox-Foster DL, Conlan S, Holmes EC, Palacios G, Evans JD, Moran NA, et al. A metagenomic survey of microbes in honey bee colony collapse disorder. Science 2007; 318, 283-287. PMID: 17823314
4. vanEngelsdorp D, Underwood R, Caron D, Hayes J. An estimate of managed colony losses in the winter of 2006-2007: A report commissioned by the apiary inspectors of America. Am Bee J 2007; 147, 599-603.
5. Underwood RM, vanEngelsdorp D. Colony Collapse Disorder: have we seen this before? Bee Culture 2007; 135: 13-18.
6. vanEngelsdorp D, Evans JD, Saegerman C, Mullin C, Haubruge E, Nguyen BK, et al. Colony Collapse Disorder: A Descriptive Study. PLoS ONE 2009; 4: e6481. doi: 10.1371/journal.pone.0006481 PMID: 19649264
7. Lee KV, Steinhauer N, Rennich K, Wilson ME, Tarpy DR, Caron DM et al. A national survey of managed honey bee 2013-2014 annual colony losses in the USA. Apidologie 2015; 46: 292-305.
8. Bortolotti L, Sabatini AG, Mutinelli F, Astuti M, Lavazza A, Piro R, et al. Spring honey bee losses in Italy. Julius-Kühn Archives 2009; 423: 148-152.
9. Van der Zee R, Brodschneider R, Brusbardis V, Charrière J-D, Chlebo R, Coffey MF, et al. Results of international standardised beekeeper surveys of colony losses for winter 2012-2013: analysis of winter loss rates and mixed effects modelling of risk factors for winter loss. J Apicult Res 2014; 53: 19-34.
10. Mutinelli F, Costa C, Lodesani M, Baggio A, Medrzycki P, Formato G, et al. Honey bee colony losses in Italy. J Apicult Res 2010; 49: 119-120.
11. Maini S, Medrzycki P, Porrini C. The puzzle of honey bee losses: a brief review. B Insectol 2010; 63: 153-160.
12. Alaux C, Brunet JL, Dussaubat C, Mondet F, Tchamitchan S, Cousin M, et al. Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environ Microbiol 2010; 12: 774-782. doi: 10.1111/j.1462-2920.2009.02123.x PMID: 20050872
13. Doublet V, Labarussias M, de Miranda JR, Moritz RFA, Paxton RJ. Bees under stress: sublethal doses of a neonicotinoid pesticide and pathogens interact to elevate honey bee mortality across the life cycle. Environ Microbiol 2015; 17: 969-983. doi: 10.1111/1462-2920.12426 PMID: 25611325
14. Nazzi F, Brown SP, Annoscia D, Del Piccolo F, Di Prisco G, Varricchio P, et al. Synergistic parasitepathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLoS Pathog 2012; 8: e1002735. doi: 10.1371/journal.ppat.1002735 PMID: 22719246
15. Pettis J, vanEngelsdorp D, Johnson J, Dively G. Pesticide exposure in honey bee results in increased levels of the gut pathogen Nosema. Naturwissenschaften 2012; 99: 153-158. doi: 10.1007/s00114-011-0881-1 PMID: 22246149
16. Di Prisco G, Cavaliere V, Annoscia D, Varricchio P, Caprio E, Nazzi F, et al. Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. Proc Nat Acad Sci USA 2013; 110: 18466-18471. doi: 10.1073/pnas.1314923110 PMID: 24145453
17. Sgolastra F, Renzi T, Draghetti S, Medrzycki P, Lodesani M, Maini S, et al. Effects of neonicotinoid dust from maize seed-dressing on honey bees. B Insectol 2012; 65: 273-280.
18. David A, Botìas C, Abdul-Sada A, Nicholls E, Rotheray EL, Hill EM, et al. Widespread contamination of wildflower and bee-collected pollen with complex mixtures of neonicotinoids and fungicides commonly applied to crops. Environ Int 2016; 88: 169-178. doi: 10.1016/j.envint.2015.12.011 PMID: 26760714
19. Ravoet J, Reybroeck W, de Graaf DC. Pesticides for apicultural and/or agricultural application found in Belgian honey bee wax combs. B Environ Contam Tox 2015; 94: 543-548.
20. Chauzat MP, Martel AC, Cougoule N, Porta P, Lachaize J, Zeggane S, et al. An Assessment of Honeybee Colony Matrices, Apis Mellifera (Hymenoptera Apidae) to Monitor Pesticide Presence in Continental France. Environ Toxicol Chem 2011; 30: 103-111. doi: 10.1002/etc.361 PMID: 20853451
21. Bernal J, Garrido Bailén E, Del Nozal MJ, González-Porto AV, Martín HR, Diego JC, et al. Overview of pesticide residues in stored pollen and their potential effect on bee colony (Apis mellifera) losses in Spain. J Econ Entomol 2010; 103: 1964-1971. PMID: 21309214
22. Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R, van Engelsdorp D, et al. High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS ONE 2010; 5: e9754. doi: 10.1371/journal.pone.0009754 PMID: 20333298
23. Lambert O, Piroux M, Puyo S, Thorin C, L'Hostis M, Wiest L, et al. Widespread Occurrence of Chemical Residues in Beehive Matrices from Apiaries Located in Different Landscapes of Western France. PLoS ONE 2013; 8: e67007. doi: 10.1371/journal.pone.0067007 PMID: 23799139
24. Simon-Delso N, San Martin G, Bruneau E, Minsart LA, Mouret C, Hautier L. Honeybee Colony Disorder in Crop Areas: The Role of Pesticides and Viruses. PLoS ONE 2014; 9: e103073. doi: 10.1371/journal. pone.0103073 PMID: 25048715
25. Genersch E, von der Ohe W, Kaatz H, Schroeder A, Otten C, Buchler R, et al. The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie 2010; 41: 332-352.
26. Berthoud H, Imdorf A, Haueter M, Radloff S, Neumann P. Virus infections and winter losses of honey bee colonies (Apis mellifera). J Apicult Res 2010; 49: 60-65.
27. Ravoet J, Maharramov J, Meeus I, De Smet L, Wenseleers T, Smagghe G, et al. Comprehensive Bee Pathogen Screening in Belgium Reveals Crithidia mellificae as a New Contributory Factor to Winter Mortality. PLoS ONE 2013; 8: e72443. doi: 10.1371/journal.pone.0072443 PMID: 23991113
28. Bollan KA, Hothersall JD, Moffat C, Durkacz J, Saranzewa N, Wright GA, et al. The microsporidian parasites Nosema ceranae and Nosema apis are widespread in honeybee (Apis mellifera) colonies across Scotland. Parasitol Res 2013; 112: 751-759. doi: 10.1007/s00436-012-3195-0 PMID: 23180128
29. Botìas C, Martin-Hernandez R, Garrido-Bailon E, Gonzalez-Porto A, Martinez-Salvador A, De La Rua P, et al. The growing prevalence of Nosema ceranae in honey bees in Spain, an emerging problem for the last decade. Res Vet Sci 2012; 93: 150-155. doi: 10.1016/j.rvsc.2011.08.002 PMID: 21906767
30. Chauzat MP, Carpentier P, Madec F, Bougeard S, Cougoule N, Drajnudel P, et al. The role of infectious agents and parasites in the health of honey bee colonies in France. J Apicult Res 2010; 49: 31-39.
31. Odoux JF, Feuillet D, Aupinel P, Loublier Y, Tasei JN, Mateescu C. Territorial biodiversity and consequences on physico-chemical characteristics of pollen collected by honey bee colonies. Apidologie 2012; 43: 561-575.
32. Alaux C, Ducloz F, Crauser D, Le Conte Y. Diet effects on honeybee immunocompetence. Biol Lett 2010; 6: 562-565. doi: 10.1098/rsbl.2009.0986 PMID: 20089536
33. Tosi S, Medrzycki P, Bogo G, Bortolotti L, Grillenzoni F, Forlani G. Role of food quality in bee susceptibility to fipronil and clothianidin. Julius-Kühn-Archives 2012; 437: 106.
34. EC. Commission implementing Regulation No 485/2013 of 24 May 2013 amending Implementing Regulation (EU) No 540/2011, as regards the conditions of approval of the active substances clothianidin, thiamethoxam and imidacloprid, and prohibiting the use and sale of seeds treated with plant protection products containing those active substances. OJ EU 25.05.2013; L139: 12-26.
35. Greatti M, Barbattini R, Stravisi A, Sabatini AG, Rossi S. Presence of the a.i. imidacloprid on vegetation near corn fields sown with Gaucho® dressed seeds. B Insectol 2006; 59: 99-103.
36. Mutinelli F, Sgolastra F, Gallina A, Medrzycki P, Bortolotti L, Lodesani M, et al. A network for monitoring honeybee mortality and colony losses in Italy as a part of the APENET research project. Am Bee J 2010; 150: 389-390.
37. Porrini C, Sgolastra F, Sabatini AG. Rete per il monitoraggio dei fenomeni di spopolamento e mortalità degli alveari in Italia (APENET). APOidea 2008; 5: 83-87.
38. OIE. Nosemosis of honey bees 2008. Chapter 2.2.4. In Manual of Diagnostic Tests and Vaccines for Terrestrial Animals. 6th Edition. Paris.
39. Higes M, Martìn R, Meana A. Nosema ceranae, a new microsporidian parasite in honey bees in Europe J Invertebr Pathol 2006; 92: 93-95. PMID: 16574143
40. Webster TC, Pomper KW, Hunt G, Thacker EM, Jones SC. Nosema apis infection in worker and queen Apis mellifera. Apidologie 2004; 35: 49-54.
41. Martin SJ, Highfield AC, Brettel L, Villalobos EM, Budge GE, Powell M, et al. Global honey bee viral landscape altered by a parasitic mite. Science 2012; 336: 1034-1036.
42. Chantawannakul P, Ward L, Boonham N, Brown MA. A scientific note on the detection of honeybee viruses using real-time PCR (TaqMan) in Varroa mites collected from a Thai honeybee (Apis mellifera) apiary. J Invertebr Pathol 2006; 91: 69-73. PMID: 16376930
43. Kajobe R, Marris G, Budge G, Laurenson L, Cordoni G, Jones B, et al. First molecular detection of a viral pathogen in Ugandan honey bees. J Invertebr Pathol 2010; 104: 153-156. doi: 10.1016/j.jip.2010. 02.007 PMID: 20219470
44. Zar JH. Biostatistical analysis. Biostatistical Analysis. Prentice-Hall, Upper Saddle River, New Jersey, 663 pp; 1999.
45. Fries I. Nosema ceranae in European honey bees (Apis mellifera). J Invertebr Pathol 2010; 103: S73-S79. doi: 10.1016/j.jip.2009.06.017 PMID: 19909977
46. Gisder S, Hedtke K, Mockel N, Frielitz MC, Linde A, Genersch E. Five-Year Cohort Study of Nosema spp. in Germany: Does Climate Shape Virulence and Assertiveness of Nosema ceranae? Appl Environ Microb 2010; 76: 3032-3038.
47. Traver BE, Williams MR, Fell RD. Comparison of within hive sampling and seasonal activity of Nosema ceranae in honey bee colonies. J Invertebr Pathol 2012; 109: 187-193. doi: 10.1016/j.jip.2011.11.001PMID: 22085836
48. Higes M, Martín-Hernández R, Martínez-Salvador A, Garrido-Bailón E, González-Porto AV, Meana A, et al. A preliminary study of the epidemiological factors related to honey bee colony loss in Spain. Environ Microbiol Rep 2010; 2: 243-250. doi: 10.1111/j.1758-2229.2009.00099.x PMID: 23766075
49. de Miranda JR, Cordoni G, Budge G. The acute bee paralysis virus-Kashmir bee virus-Israeli acute paralysis virus complex. J Invert Pathol 2010; 103: S30-S47.
50. de Miranda JR, Genersch E. Deformed wing virus. J Invert Pathol 2010; 103: S48-S61.
51. Ball BV, Allen MF. The Prevalence of Pathogens in Honey Bee (Apis-Mellifera) Colonies Infested with the Parasitic Mite Varroa-Jacobsoni. Ann Appl Biol 1988; 113: 237-244.
52. De Smet L, Ravoet J, de Miranda JR, Wenseleers T, Mueller MY, Moritz RFA, et al. BeeDoctor, a Versatile MLPA-Based Diagnostic Tool for Screening Bee Viruses. PLoS ONE 2012; 7: e47953. doi: 10. 1371/journal.pone.0047953 PMID: 23144717
53. Di Pasquale G, Salignon M, Le Conte Y, Belzunces LP, Decourtye A, Kretzschmar A, et al. Influence of Pollen Nutrition on Honey Bee Health: Do Pollen Quality and Diversity Matter? PLoS ONE 2013; 8: e72016. doi: 10.1371/journal.pone.0072016 PMID: 23940803
54. Brodschneider R, Crailsheim K. Nutrition and health in honey bees. Apidologie 2010; 41: 278-294.
55. Roulston TH, Cane JH. Pollen nutritional content and digestibility for animals. Plant Syst Evol 2000; 222: 187-209.
56. Johnson RM, Ellis MD, Mullin CA, Frazier M. Pesticides and honey bee toxicity-USA. Apidologie 2010; 41: 312-331.
57. Cornman RS, Tarpy DR, Chen Y, Jeffreys L, Lopez D, Pettis JS, et al. Pathogen Webs in Collapsing Honey Bee Colonies. PLoS ONE 2012; 7: e43562. doi: 10.1371/journal.pone.0043562 PMID: 22927991
58. Costa C, Tanner G, Lodesani M, Maistrello L, Neumann P. Negative correlation between Nosema ceranae spore loads and deformed wing virus infection levels in adult honey bee workers. J Invertebr Pathol 2011; 108: 224-225. doi: 10.1016/j.jip.2011.08.012 PMID: 21939664
59. Doublet V, Natsopoulou ME, Zschiesche L, Paxton RJ. Within-host competition among the honey bees pathogens Nosema ceranae and Deformed wing virus is asymmetric and to the disadvantage of the virus. J Invertebr Pathol 2015; 124: 31-34. doi: 10.1016/j.jip.2014.10.007 PMID: 25450738
60. Clermont A, Eickermann M, Kraus F, Hoffmann L, Beyer M. Correlations between land covers and honey bee colony losses in a country with industrialized and rural regions. Science of Total Environment 2015; 532: 1-13.
61. McMenamin AJ, Genersch E. Honey bee colony losses and associated viruses. Current Opinion in Insect Science 2015; 8: 121-129.
62. Nguyen BK, Ribière M, VanEngelsdorp D, Snoek C, Saegerman C, Kalkstein AL, et al. Effects of honey bee virus prevalence, Varroa destructor load and queen condition on honey bee colony survival over the winter in Belgium. J Apicult Res 2011; 50: 195-202.
63. Higes M, Martin-Hernandez R, Garrido-Bailon E, Gonzalez-Porto AV, Garcia-Palencia P, Meana A, et al. Honeybee colony collapse due to Nosema ceranae in professional apiaries. Env Microbiol Rep 2009; 1: 110-113.