Nosema Ceranae DNA in Honey Bee Haemolymph and Honey Bee Mite Varroa Destructor/DNK Nosema Ceranae U Hemolimfi Pčela I Pčelinjem Krpelju Varroa Destructor

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Abstract

Honey bee mite Varroa destructor and microsporidium Nosema ceranae are currently considered the most important threats to honey bees and beekeeping. It has been believed that both N. apis and N. ceranae invade exclusively epithelial cells of the honey bee ventriculus. However, some fi ndings suggest that these microsporidia may infect other tissues of honey bees. There are indications that these pathogens could be found in honey bee haemolymph, as the medium for its distribution to anatomically distant tissues. Knowing that V. destructor being an ectoparasitic mite feeds on the honey bee’s haemolymph, the aim of this study was to investigate if DNA of Nosema spp. microsporidia could be found in honey bee haemolymph and in V. destructor.

The study was conducted on bee haemolymph and V. destructor mites from 44 Apis mellifera colonies. From each hive five mite individuals and 10 μL of haemolymph (from 4-5 bees) were used as samples for DNA isolation and PCR detection of Nosema spp.

The DNA of N. ceranae was confi rmed in 61.36% of V. destructor mites and 68.18% of haemolymph samples. This is the first report of N. ceranae DNA in honey bee haemolymph and in V. destructor mites. The finding of DNA of N. ceranae in V. destructor could be interpreted as the result of mite feeding on N. ceranae infected bee haemolymph. However, for a full confi rmation of the vector role of V. destructor in spreading of nosemosis, further microscopy investigations are required for the detection of spores in both investigated matrices (haemolymph and V. destructor internal tissues).

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  • 1. Fries I: Nosema ceranae in European honey bees (Apis mellifera). J Invertebr Pathol 2010 103:73-79.

  • 2. Higes M Martín-Hernández R Meana A: Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie 2010 41:375-392.

  • 3. Botias C Martín-Hernández R Garrido-Bailón E González-Porto A Martínez-Salvador A De La Rúa P Meana A Higes M: 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.

  • 4. Higes M Meana A Bartolomé C Botías C Martín-Hernández R: Nosema ceranae (Microsporidia) a controversial 21st century honey bee pathogen. Environ Microbiol Rep 2013 5:17-29.

  • 5. Stevanovic J Simeunovic P Gajic B Lakic N Radovic D Fries I Stanimirovic Z: Characteristics of Nosema ceranae infection in Serbian honey bee colonies. Apidologie 2013 44:522-536.

  • 6. Huang W-F Solter LF: Comparative development and tissue tropism of Nosema apis and Nosema ceranae. J Invertebr Pathol 2013 113:35-41.

  • 7. Steche W: A atiologie und therapie der nosematose der honigbiene. Zeitung Bienenfarsche 1960 5:49-52.

  • 8. Sokolov VP Grobov OF: Nosema spores in the hemolymph of the bee. Pchelovodstvo 1963 7:39.

  • 9. Copley TR Jabaji SH: Honeybee glands as possible infection reservoirs of Nosema ceranae and Nosema apis in naturally infected forager bees. J Appl Microb 2011 112:15-24.

  • 10. Chen YP Evans JD Murphy CA Gutell R Zuker M Gundersen-Rindal DE Pettis JS: Morphological molecular and phylogenetic characterization of Nosema ceranae a microsporidian parasite isolated from the European honey bee Apis mellifera. J Euk Microb 2009 56:142-147.

  • 11. 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. Environ Microbiol 2010 76:3032-3038.

  • 12. Giersch T Berg T Gale F Hornitzky M: Nosema ceranae infects honey bees (Apis mellifera) and contaminates honey in Australia. Apidologie 2009 40:117-123.

  • 13. Higes M Martın-Hernandez R Garrido-Bailon E Garcia-Palencia P Meana A: Detection of infective Nosema ceranae (Microsporidia) spores in corbicular pollen of forager honeybees. J Invertebr Pathol 2008 97:76-78.

  • 14. Malone LA Gatehouse HS: Effects of Nosema apis infection on honey bee (Apis mellifera) digestive proteolytic enzyme activity. J Invertebr Pathol 1998 71:169-174.

  • 15. Cox-Foster DL Conlan S Holmes EC Palacios G Evans JD Moran NA Quan PL Briese T Hornig M Geiser DM Martinson V Van Engelsdorp D Kalkstein AL Drysdale A Hui J Zhai J Cui L Hutchison SK Simons JF Egholm M Pettis JS Lipkin WI: A metagenomic survey of microbes in honey bee colony collapse disorder. Science 2007 318:283-287.

  • 16. Van der Zee R: Colony losses in the Netherlands. J Apic Res 2010 49:121-123.

  • 17. Higes M Martín-Hernández R Garrido-Bailón E Botias C García-Palencia P Meana A: Regurgitated pellets of Merops apiaster as fomites of infective Nosema ceranae (Microsporidia) spores. Environ Microbiol 2008 10:1374-1379.

  • 18. Valera F Martín-Hernández R Higes M: Evaluation of large-scale dissemination of Nosema ceranae spores by European bee-eaters Merops apiaster. Environ Microbiol Rep 2011 3:47-53.

  • 19. Martin-Hernandez R Meana A Prieto L Salvador AM Garrido-Bailon E Higes M: Outcome of colonization of Apis mellifera by Nosema ceranae. Appl Environ Microbiol 2007 73:6331-6338.

  • 20. Higes M Martín-Hernández R Botías C Garrido-Bailón E González-Porto AV Barrios L Del Nozal MJ Bernal JL Jiménez JJ García-Palencia P Meana A: How natural infection by Nosema ceranae causes honeybee colony collapse. Environ Microbiol 2008 10:2659-2669.

  • 21. Higes M Martín-Hernández R Garrido-Bailón E González-Porto AV García-Palencia P Meana A Del Nozal MJ Mayo R Bernal JL: Honeybee colony collapse due to Nosema ceranae in professional apiaries. Environ Microbiol Rep 2009 1:110-3.

  • 22. Gilliam M Shimanuki H: In vitro phagocytosis of Nosema apis spores by honeybee haemocytes. J Invertebr Pathol 1967 9:387-389.

  • 23. Anderson DL Trueman JWH: Varroa jacobsoni (Acari: Varroidae) is more than one species. Exp Appl Acarol 2000 24:165-189.

  • 24. Gajic B Radulovic Z Stevanovic J Kulisic Z Vucicevic M Simeunovic P Stanimirovic Z: Variability of the honey bee mite Varroa destructor in Serbia based on mtDNA analysis. Exp Appl Acarol 2013 61:97-105.

  • 25. Rosenkranz P Aumeier P Ziegelmann B: Biology and control of Varroa destructor. J Invertebr Pathol 2010 103:96-119.

  • 26. Genersch E Aubert M: Emerging and re-emerging viruses of the honey bee (Apis mellifera L.). Vet Res 2010 41:54.

  • 27. Križek I Horvatek D Gottstein Ž Steiner Z Galović D Ervaćinović Ž Prukner-Radovčić E: Epidemiological study of Chlamydophila psittaci in pet birds in Croatia. Acta Vet 2012 62:325-331.

  • 28. Kumar D Pate M Hubad B Avberšek J Logar K Lapanje A Zrimec A Ocepek M: Detection of Bacillus anthracis in the air soil and animal tissue. Acta Vet 2012 62:77-89.

  • 29. Stevanovic J Stanimirovic Z Genersch E Kovacevic RS Ljubenkovic J Radakovic M Aleksic N: Dominance of Nosema ceranae in honey bees in the Balkan countries in the absence of symptoms of colony collapse disorder. Apidologie 2011 42:49-58.

  • 30. Genersch E: Honey bee pathology: current threats to honey bees and beekeeping. Appl Microbiol Biotechnol 2010 87:87-97.

  • 31. Le Conte Y Ellis M Ritter W: Varroa mites and honey bee health: can Varroa explain part of the colony losses? Apidologie 2010 41:353-363.

  • 32. Genersch E Von der Ohe W Kaatz H Schroeder A Otten C Büchler R Berg S Ritter W Mühlen W Gisder S Meixner M Liebig G Rosenkranz P: The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie 2010 41:332-352.

  • 33. Guzman-Novoa E Eccles L Calvete Y Mcgowan J Kelly PG Correa-Benítez A: Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario Canada. Apidologie 2010 41:443-450.

  • 34. Dainat B Evans JD Chen YP Gauthier L Neumann P: Predictive markers of honey bee colony collapse. PLoS ONE 2012 7:e32151.

  • 35. Alaux C Brunet JL Dussaubat C Mondet F Tchamitchan S Cousin M Brillard J Baldy A Belzunces LP Le Conte Y: Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environ Microbiol 2010 12:774-782.

  • 36. Vidau C Diogon M Aufauvre J Fontbonne R Viguès B: Exposure to sublethal doses of fi pronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. PLoS ONE 2011 6:e21550.

  • 37. Stanimirovic Z Stevanovic J Jovanovic S Andjelkovic M: Evaluation of genotoxic effects of Apitol® (cymiazole hydrochloride) in vitro by measurement of sister chromatid exchange. Mutat Res 2005 588:152-157.

  • 38. Stanimirovic Z Stevanovic J Bajic V Radovic I: Evaluation of genotoxic effects of fumagillin (dicyclohexylamine) by citogenetic tests in vivo. Mutat Res 2007 628:1-10.

  • 39. Van der Geest LPS Elliot SL Breeuwer JAJ Beerling EAM: Diseases of mites. Exp Appl Acarol 2000 24:497-560.

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