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Lotmaria Passim As Third Parasite Gastrointestinal Tract of Honey Bees Living in Tree Trunk

Open Access
|Jul 2020

References

  1. Adl, S.M., Simpson, A.G., Farmer, M.A., Andersen, R.A., Anderson, O.R., Barta, J.R., … Taylor, M.F. (2005). The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. Journal of Eukaryotic Microbiology, 52(5), 399–451. http://doi.org/10.1111/j.1550-7408.2005.00053
  2. Antúnez, K., Martín-Hernández, R., Prieto, L., Meana, A., Zunino, P., Higes, M. (2009). Immune suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environmental Microbiology, 11(9), 2284–2290. https://doi.org/10.1111/j.1462-2920.2009.01953.x
  3. Arismendi, N., Bruna, A., Zapata N., & Vargas, M. (2016). PCR-specific detection of recently described Lotmaria passim (Trypanosomatidae) in Chilean apiaries. Journal of Invertebrate Pathology, 134, 1–5. http://doi.org/10.1016/j.jip.2015.12.008
  4. Banaszak, J. (2009). Pollinating insects (Hymenoptera: Apoidea, Apiformes) as an example of changes in fauna. Fragmenta Faunistica, 52(2), 105–123.
  5. Barrett, J., Vardulaki, K.A., Conlon, C., Cooke, J., Daza-Ramirez, P., Evans, E.G.V., … Viscoli, C. (2003). A Systematic Review of the Antifungal Effectiveness and Tolerability of Amphotericin B Formulations. Clinical Therapeutic, 25, 1295–1320.
  6. Borsuk, G., Czerska, K., Olszewski, K., Strachecka, A., Paleolog, J., Chobotow, J. (2012). Aktualny stan wiedzy o Varroa destructor. Medycycna Weterynaryjna, 68(10), 579–584.
  7. Borsuk, G., Ptaszyńska, A., Olszewski, K., & Paleolog, J. (2013) Impact of nosemosis on the intestinal yeast flora of honey bees. Medycyna Weterynaryjna, 69(12), 726–729.
  8. Chen, Y., Evans, J.D., Smith, I.B., & Pettis, J.S. (2008). Nosema ceranae is a long-present and wide-spread microsporidian infection of the European honey bee (Apis mellifera) in the United States. Journal of Invertebrate Pathology, 97(2), 186–188. http://doi.org/10.1016/j.jip.2007.07.010
  9. Cornman, R.S., Tarpy, D.R., Chen, Y., Jeffreys, L., Lopez, D., van Pettis, J.S., Engelsdorp, D., Evans J.D. (2012). Pathogen webs in collapsing honey bee colonies PLoS ONE, 7, e43562. https://doi.org/10.1371/journal.pone.0043562
  10. Crane, E. (1999). The World History of Beekeeping and Honey Hunting. Gerald Duckworth & Co. Ltd, London.
  11. De la Rúa, P., Jaffé, R., Dall’Olio, R., Muñoz, I., Serrano, J. (2009). Biodiversity, conservation and current threats to European honey bees. Apidologie, 40(3), 263–284. http://doi.org/10.1051/apido/2009027
  12. Engelsdorp, D., Evans, J. D., Saegerman, C., Mullin, C., Haubruge, E., Nguyen, B. K., … Pettis, J. S. (2009). Colony collapse disorder: a descriptive study. PLoS ONE, 4(8), e6481. http://doi.org/10.1371/journal.pone.0006481
  13. Evans, J.D., Schwarz, S., Chen, Y., Budge, G., Cornman, R., De la Rua, P., … Pint, M.A. (2013). Standard methods for molecular research in Apis mellifera. Journal of Apicultural Research, 52(4), 1–53. https://doi.org/10.3896/IBRA.1.52.4.1
  14. Gegear, J.R. (2005). Multicomponent floral signals elicit selective foraging in bumblebees. Naturwissenhaften, 92(6), 269–271. http://doi.org/10.1007/s00114-005-0621-5
  15. Goulson, D., Nicholls, E., Botías, C., & Rotheray, E.L. (2015). Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science, 347, 1255957 http://doi.org/10.1126/science.1255957
  16. Higes, M., Meana, A., Bartolomé, C., Botías, C., Martín-Hernández, R. (2013). Nosema ceranae (Microsporidia), a controversial 21st century honey bee pathogen. Environmental Microbiology Reports, 5(1), 17–29. http://doi.org/10.1111/1758-2229.12024
  17. Hubert, J., Bicianova, M., Ledvinka, O., Kamler, M., Lester, P.J., Nesvorna, M., Kopecky, J., Erban, T. (2017). Changes in the bacteriome of honey bees associated with the parasite Varroa destructor, and pathogens Nosema and Lotmaria passim. Microbial Ecology, 73, 685–698.
  18. Ilyasov, R.A., Kosarev, M.N., Neal, A., & Yumaguzhin, F.G. (2015). Burzyan Wild-Hive Honeybee A. m. mellifera in South Ural. Bee World, 92, 7–11. http://doi.org/10.1080/0005772x.2015.1047634
  19. Langridge, D.F., & McGhee, R.B. (1967). Crithidia mellificae n. sp. an acidophilic trypanosomatid of the honey bee Apis mellifera. Journal of Protozoology, 14(3), 485–487. https://doi.org/10.1111/j.1550-7408.1967.tb02033
  20. Łopieńska-Biernat E., Sokół R., Michalczyk M., Żółtowska K., Stryiński R. (2017). Biochemical status of feral honey bees (Apis mellifera) infested with various pathogens. Journal of Apicultural Research, 56(5), 606–615. https://doi.org/10.1080/00218839.2017.1343020
  21. Martin, S.J., Highfield, A.C., Brettell, L., Villalobos, E.M., Budge, G.E., Powell, M., Nikaido, S., Schroeder, D.C. (2012). Global honey bee viral landscape altered by a parasitic mite. Science, 336, 1304–1306. http://doi.org/10.1126/science.1220941.
  22. Maslov, D.A.,Votypka, J., Yurchenko, V., & Lukes, J. (2013). Diversity and phylogeny of insect trypanosomatids: all that is hidden shall be revealed. Trends Parasitology, 29(1), 43–52. http://doi.org/10.1016/j.pt.2012.11.001
  23. Michalczyk, M., Sokół, R., & Koziatek, S. (2015). Evaluation of the effectiveness of selected treatments of Nosema spp. infection by the hemocytometric method and multiplex PCR. Acta Veterinaria Beograd, 66(1), 115–124. https://doi.org/10.1515/acve-2016-0009
  24. Michalczyk, M., & Sokół, R. (2018). Estimation of the influence of selected products on co-infection with N. apis/N. ceranae in Apis mellifera using real-time PCR. Invertebrate Reproduction and Development. http://doi.org/10.1080/07924259.2018.1433726
  25. Moritz, R.F.A., de Miranda, J., Fries, I., Le Conte, Y., Neumann, P., Paxton, R. (2010). Research strategies to improve honeybee health in Europe. Apidologie, 41, 227–242. http://doi.org/10.1051/apido/2010010
  26. Nazzi, F., & Le Conte, Y. (2016). Ecology of Varroa destructor, the Major Ectoparasite of the Western Honey Bee, Apis mellifera. Annual Review of Entomology, 61, 417–32. http://doi.org/10.1146/annurevento-010715-023731
  27. Neumann, P., & Carreck, N. (2010). Honey bee colony losses. Journal of Apicultural Research, 49(1), 1–6. https://doi.org/10.3896/IBRA.1.49.1.01
  28. Oleksa, A., Gawroński, R., & Tofilski, A. (2013). Rural avenues as a refuge for feral honey bee population. Journal of Insect Conservation, 17, 465–472. DOI: 10.1007/s10841-012-9528-6
  29. Potts, S.G., Biesmeijer J.C., Kremen, C., Neumann, P., Schweiger, O., Kunin, W.E. (2010). Global pollinator declines: drivers and impacts. Trends Ecology. Evolution, 25(6), 345–353. http://doi.org/10.1016/j.tree.2010.01.007
  30. Ptaszyńska, A., Paleolog, J., & Borsuk, G. (2016). Nosema ceranae infection promotes proliferation of yeasts in honey bee intestines. PloS ONE, 11(10), 1–16. https://doi.org/10.1371/journal.pone.0164477
  31. Ptaszyńska, A., Borsuk, G., Mułenko, W., & Demetraki-Paleolog, J. (2017). Differentiation of Nosema apis and Nosema ceranae spores under Scanning Electron Microscopy. Journal of Apicultural Research, 53, 537–544. https://doi.org/10.3896/IBRA.1.53.5.02
  32. Ptaszyńska, A., Gancarz, M., Hurd, P.J., Borsuk, G., Wiącek, D., Nawrocka, A., … Paleolog, J. (2018). Changes in the bioelement content of summer and winter western honeybees (Apis mellifera) induced by Nosema ceranae infection. Plos ONE, 13(5), 1–18. https://doi.org/10.3896/IBRA.1.53.5.02
  33. Ravoet, J., Maharramov, J., Meeus, I., de Smet, L., Wenseleers, T., Smagghe, G., de Graaf, D.C. (2013). Comprehensive bee pathogen screening in Belgium reveals Crithidia mellificae as a new contributory factor to winter mortality PLoS ONE, 8, e72443 http://doi.org/10.1371/journal.pone.0072443
  34. Retschnig, G., Williams, G.R., Schneeberger, A., & Neumann, P. (2017). Cold Ambient Temperature Promotes Nosema spp. intensity in honey bees (Apis mellifera). Insects, 8(1), 1–20. http://doi.org/10.3390/insects8010020
  35. Rodríguez, M., Vargas, M., Gerding, M., Navarro, H., Antúnez, K. (2012). Viral infection and Nosema ceranae in honey bees (Apis mellifera) in Chile. Journal of Apicultural Research, 51(3), 285–287. https://doi.org/10.3896/IBRA.1.51.3.12
  36. Rodríguez, M., Vargas, M., Antúnez, K., Gerding, M., Castro, F.O., Zapata, N., Chilean, J. (2014). Prevalence and phylogenetic analysis of honey bee viruses in the Biobío Region of Chile and their association with other honey bee pathogens. Agricultural Research, 74(2), 170–177. http://dx.doi.org/10.4067/S0718-58392014000200007
  37. Rosenkranz, P., Aumeier, P., & Ziegelmann, B. (2010). Biology and control of Varroa destructor. Journal of Invertebrate Pathology, 103(1), 96–119. DOI: 10.1016/j.jip.2009.07.016.
  38. Runcke, I C., Flenniken, M.L., Engel, J.C., Ruby, J.G., Ganem, D., Andino, R., DeRisi, J.L. (2011). Temporal analysis of the honey bee microbiome reveals four novel viruses and seasonal prevalence of known viruses, Nosema, and Crithidia. PLoS ONE, 6 p. e20656 http://doi.org/10.1371/journal.pone.0020656
  39. Ruttner, F. (1988). Biogegraphy and Taxonomy of Honeybees. Springer-Verlag. ISBN 3-540-17781-7. https://doi.org/10.1002/mmnd.19890360109
  40. Sammataro, D., Gerson, U., & Needham, G. (2000). Parasitic mites of honey bees: life history, implications, and impact. Annual Review of Entomology, 45, 519–548. http://doi.org/10.1146/annurev.ento.45.1.519
  41. Schwarz, R.S., Bauchan, G.R., Murphy, C., Ravoet, J., de Graaf, D.C., Evans, J.D. (2015). Characterization of two species of Trypanosomatidae from the honey bee Apis mellifera: Crithidia mellificae Langridge and McGhee, and Lotmaria passim. Journal of Eukaryotic Microbiology, 62, 567–583. http://doi.org/10.1111/jeu.12209
  42. Seeley, T.D. (1985). Honeybee Ecology: A Study of Adaptation in Social Life. Princeton: Princeton University Press
  43. Seeley, T.D. (2007). Honey bees of the Arnot Forest: a population of feral colonies persisting with Varroa destructor in the northeastern United States. Apidologie. 38, 19–29. http://doi.org/10.1051/apido:2006055
  44. Sokół, R., & Michalczyk, M. (2016). Detection of Nosema spp. in worker bees, pollen and bee bread during the honey flow season. Acta Veterinaria Brno, 85(3), 261–266. http://doi.org/10.2754/avb201685030261
  45. Stanimirovic, Z., Glavinic, U., Lakic, N., Radovic, D, Ristanic, M., Taric, E., Stevanovic, J. (2017). Efficacy of plant-derived formulation “Argus Ras” in Varroa destructor control. Acta Veterinaria Beograd, 67(1), 191–200.
  46. Stevanovic, R.S. Schwarz, B. Vejnovic, J.D. Evans, R.E. Irwin, U. Glavinic, Z. Stanimirovic. (2016). Species-specific diagnostics of Apis mellifera trypanosomatids: a nine-year survey (2007–2015) for trypanosomatids and microsporidians in Serbian honey bees. Journal of Invertebrate Pathology, 139, 6–11. http://doi.org/10.1016/j.jip.2016.07.001
  47. Sulborska, A., Horecka, B., Cebrat, M., Kowalczyk, M., Skrzypek, T.H., Kazimierczak, W., Trytek, M., Borsuk, G. (2019). Microsporidia Nosema spp. - obligate bee parasites are transmitted by air. Scientific Reports, 9, 14376. https://doi.org/10.1038/s41598-019-50974-8
  48. Tritschler, M., Retschnig, G., Yañez, O., Williams, G.R., Neumann, P. (2017). Host sharing by the honey bee parasites Lotmaria passim and Nosema ceranae. Ecology Evolution, 7(6), 1850–1857. doi: 10.1002/ece3.2796
  49. Webster, T.C., Pompe,r K.W., Hunt, G., Thacker, E.M., Jones, S.C. (2004). Nosema apis infection in worker and queen Apis mellifera. Apidologie. 35, 49–54. http://doi.org/10.1051/apido:2003063
  50. van Dooremalen, C., Gerritsen, L., Cornelissen, B., van der Steen, J.J.M., van Langevelde, F., Blacquière, T. (2012). Winter survival of individual honey bees and honey bee colonies depends on level of Varroa destructor infestation. PLoS ONE. 7(4):e36285. http://doi.org/10.1371/journal.pone.0036285
  51. Vejnovic, B., Stevanovic, J., Schwarz, R.S., Aleksic, N., Mirilovic, M., Jovanovic, N.M., Stanimirovic, Z. (2018). Quantitative PCR assessment of Lotmaria passim in Apis mellifera colonies co-infected naturally with Nosema ceranae. Journal of Invertebrate Pathology, 151, 76–81. http://doi.org/10.1016/j.jip.2017.11.003
DOI: https://doi.org/10.2478/jas-2020-0012 | Journal eISSN: 2299-4831 | Journal ISSN: 1643-4439
Language: English
Page range: 143 - 151
Submitted on: Nov 15, 2019
Accepted on: Apr 1, 2020
Published on: Jul 2, 2020
Published by: Research Institute of Horticulture
In partnership with: Paradigm Publishing Services
Publication frequency: 2 issues per year

© 2020 Maria Michalczyk, Agata Bancerz-Kisiel, Rajmund Sokół, published by Research Institute of Horticulture
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.