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Pathology and parasitology

Occurrence of honey bee (Apis mellifera L.) pathogens in commercial and traditional hives

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Pages 433-443 | Received 17 Jul 2018, Accepted 23 Nov 2018, Published online: 16 Jan 2019

References

  • Aleksic, N., Stanimirovic, Z., & Stevanovic, J. (2012). External contaminants of honey bee products (invited paper). In R. Zivadinovic (Ed.), Apiecotech Serbia 2012, Apimondia Symposium, 2012 (pp. 46–63). Belgrade: The Serbian Federation of Beekeeping Organizations.
  • 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, 2284–2290. doi:10.1111/j.1462-2920.2009.01953.x
  • Belloy, L., Imdorf, A., Fries, I., Forsgren, E., Berthoud, H., Kuhn, R., & Charriere, J. D. (2007). Spatial distribution of Melissococcus plutonius in adult honey bees collected from apiaries and colonies with and without symptoms of European foulbrood. Apidologie, 38, 136–140. doi:10.1051/apido:2006069
  • Bordier, C., Suchail, S., Pioz, M., Devaud J. M., Collet, C., Charreton, M., … Alaux, C. (2017). Stress response in honeybees is associated with changes in task-related physiology and energetic metabolism. Journal of Insect Physiology, 98, 47–54. doi:10.1016/j.jinsphys.2016.11.013
  • Borum, A. E., & Ulgen, M. (2008). Chalkbrood (Ascosphaera apis) infection and fungal agents of honey bees in North-West Turkey. Journal of Apicultural Research, 47, 170–171. doi:10.3896/IBRA.1.47.2.16
  • Büchler, R., Costa, C., Hatjina, F., Andonov, S., Meixner, M. D., Conte, Y. L., … Drazic, M. (2014). The influence of genetic origin and its interaction with environmental effects on the survival of Apis mellifera L. colonies in Europe. Journal of Apicultural Research, 53, 205–214. doi:10.3896/IBRA.1.53.2.03
  • Budge, G. E., Barrett, B., Jones, B., Pietravalle, S., Marris, G., Chantawannakul, P., … Brown, M. A. (2010). The occurrence of Melissococcus plutonius in healthy colonies of Apis mellifera and the efficacy of European foulbrood control measures. Journal of Invertebrate Pathology, 105, 164–170. doi:10.1016/j.jip.2010.06.004
  • Chantawannakul, P., Ward, L., Boonham, N., & Brown, M. (2006). A scientific note on the detection of honeybee viruses using real-time PCR (TaqMan) in Varroa mites collected from a Tai honeybee (Apis mellifera) apiary. Journal of Invertebrate Pathology, 91, 69–73. doi:10.1016/j.jip.2005.11.001
  • Cirkovic, D. (2002). Reproductive-productive and hygienic-grooming characterization of honey bee ecotype from Sjenica and Pester region (Unpublished master’s thesis). University of Belgrade, Belgrade, Serbia.
  • Cirkovic, D., Stevanovic, J., Glavinic, U., Aleksic, N., Djuric, S., Aleksic, J., & Stanimirovic, Z. (2018). Honey bee viruses in Serbian colonies of different strength. Peer Journal, 6, e5887. doi:10.7717/peerj.5887
  • Colwell, R. K., Mao, C. X., & Chang, J. (2004). Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology, 85, 2717–2727. doi:10.1890/03-0557 doi:10.1890/03-0557
  • Colwell, R. K., Chao, A., Gotelli, N. J., Lin, S. Y., Mao, C. X., Chazdon, R. L., & Longino, J. T. (2012). Models and estimators linking individual-based and sample-based rarefaction, extrapolation, and comparison of assemblages. Journal of Plant Ecology, 5, 3–21. doi:10.1093/jpe/rtr044
  • de Graaf, D. C., Vandekerchove, D., Dobbelaere, W., Peeters, J. E., & Jacobs, F. J. (2001). Influence of the proximity of American foulbrood cases and apicultural management on the prevalence of Paenibacillus larvae spores in Belgian honey. Apidologie, 32, 587–599. doi:10.1051/apido:2001146
  • de Guzman, L. I., Frake, A.M., & Simone-Finstrom, M. (2017). Comparative flight activities and pathogen load of two stocks of honey bees reared in gamma-irradiated combs. Insects, 8, 127. doi:10.3390/insects8040127
  • Delaplane, K. S., van der Steen, J., & Guzman-Novoa, E. (2013). Standard methods for estimating strength parameters of Apis mellifera colonies. In V. Dietemann, J. D. Ellis, & P. Neumann (Eds.), The COLOSS Beebook, Volume I: Standard methods for Apis mellifera research. Journal of Apicultural Research, 52, 1–12. doi:10.3896/IBRA.1.52.1.03
  • Dobbelaere, W., De Graaf, C. D., & Peeters, E. J. (2001). Development of a fast and reliable diagnostic method for American foulbrood disease (Paenibacillus larvae subsp. larvae) using a 16S rRNA gene based PCR. Apidologie, 32, 363–370. doi:10.1051/apido:2001136
  • Forsgren, E. (2010). European foulbrood in honey bees. Journal of Invertebrate Pathology, 103, S5–S9. doi:10.1016/j.jip.2009.06.016
  • Forsgren, E., Lundhagen, A. C., Imdorf, A., & Fries, I. (2005). Distribution of Melissococcus plutonius in honeybee colonies with and without symptoms of European foulbrood. Microbial Ecology, 50, 369–374. doi:10.1007/s00248-004-0188-2
  • Francis, R. M., Amiri, E., Meixner, M. D., Kryger, P., Gajda, A., Andonov, S., … Wilde, J. (2014). Effect of genotype and environment on parasite and pathogen levels in one apiary – A case study. Journal of Apicultural Research, 53, 230–232. doi:10.3896/IBRA.1.53.2.14
  • Gauthier, L., Tentcheva, D., Tournaire, M., Dainat, B., Cousserans, F., Colin, M. E., & Bergoin, M. (2007). Viral load estimation in asymptomatic honey bee colonies using the quantitative RT-PCR technique. Apidologie, 38, 426–435. doi:10.1051/apido:2007026
  • Genersch, E. (2010). Honey bee pathology: Current threats to honey bees and beekeeping. Applied Microbiology & Biotechnology, 87, 87–97. doi:10.1007/s00253-010-2573-8
  • Glavinic, U., Stankovic, B., Draskovic, V., Stevanovic, J., Petrovic, T., Lakic, N., & Stanimirovic, Z. (2017). Dietary amino acid and vitamin complex protects honey bee from immunosuppression caused by Nosema ceranae. PLoS One, 12(11), e0187726. doi:10.1371/journal.pone.0187726
  • Glavinic, U., Stevanovic, J., Gajic, B., Simeunovic, P., Djuric, S., Vejnovic, B., & Stanimirovic, Z. (2014). Nosema ceranae DNA in honey bee haemolymph and honey bee mite Varroa destructor. Acta Veterinaria, 64, 349–357. doi:10.2478/acve-2014-0033
  • Hedtke, K., Jensen, P. M., Jensen, A. B., & Genersch, E. (2011). Evidence for emerging parasites and pathogens influencing outbreaks of stress-related diseases like chalkbrood. Journal of Invertebrate Pathology, 108, 167–173. doi:10.1016/j.jip.2011.08.006
  • Higes, M., Martín-Hernández, R., & Meana, A. (2010). Nosema ceranae in Europe: An emergent type C nosemosis. Apidologie, 41, 375–392. doi:10.1051/apido/2010019
  • James, R. R., & Skinner, J. S. (2005). PCR diagnostic methods for Ascosphaera infections in bees. Journal of Invertebrate Pathology, 90, 98–103. doi:10.1016/j.jip.2005.08.004
  • Jensen, A. B., Aronstein, K., Flores, J. M., Vojvodic, S., Palacio, M. A., & Spivak, M. (2013). Standard methods for fungal brood disease research. Journal of Apicultural Research, 52, 1–20. doi:10.3896/IBRA.1.52.1.13
  • Locke, B., & Fries, I. (2011). Characteristics of honey bee colonies (Apis mellifera) in Sweden surviving Varroa destructor infestation. Apidologie, 42, 533–542. doi:10.1007/s13592-011-0029-5
  • Locke, B., Le Conte, Y., Crauser, D., & Fries, I. (2012). Host adaptations reduce the reproductive success of Varroa destructor in two distinct European honey bee populations. Ecology & Evolution, 2, 1144–1150. doi:10.1002/ece3.248
  • Malfroy, S. F., Roberts, J. M., Perrone, S., Maynard, G., & Chapman, N. (2016). A pest and disease survey of the isolated Norfolk Island honey bee (Apis mellifera) population. Journal of Apicultural Research, 55, 202–211. doi:10.1080/00218839.2016.1189676
  • Martín-Hernández, R., Botías, C., Barrios, L., Martínez-Salvador, A., Meana, A., Mayack, C., & Higes, M. (2011). Comparison of the energetic stress associated with experimental Nosema ceranae and Nosema apis infection of honeybees (Apis mellifera). Parasitology Research, 109, 605–612. doi:10.1007/s00436-011-2292-9
  • Mattila, H. R., Rios, D., Walker-Sperling, V. E., Roeselers, G., & Newton, I. L. (2012). Characterization of the active microbiotas associated with honey bees reveals healthier and broader communities when colonies are genetically diverse. PLoS One, 7(3), e32962. doi:10.1371/journal.pone.0032962
  • Mayack, C. & Naug, D. (2009). Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection. Journal of Invertebrate Pathology, 100, 185–188. doi:10.1016/j.jip.2008.12.001
  • Mayack, C. & Naug, D. (2010). Parasitic infection leads to decline in hemolymph sugar levels in honeybee foragers. Journal of Insect Physiology, 56, 1572–1575. doi:10.1016/j.jinsphys.2010.05.016
  • Moritz, R. F. A., Härtel, S., & Neumann, P. (2005). Global invasions of the western honeybee (Apis mellifera) and the consequences for biodiversity. Ecoscience, 12, 289–301. doi:10.2980/i1195-6860-12-3-289.1
  • Muñoz, I., Stevanovic, J., Stanimirovic, Z., & De la Rúa, P. (2012). Genetic variation of Apis mellifera from Serbia inferred from mitochondrial analysis. Journal of Apicultural Science, 56(1), 59–69. doi:10.2478/v10289-012-0007-9
  • Neumann, P., & Carreck, N. L. (2010). Honey bee colony losses. Journal of Apicultural Research, 49, 1–6. doi:10.3896/IBRA.1.49.1.01
  • Neumann, P. & Blacquière, T. (2017). The Darwin cure for apiculture? Natural selection and managed honeybee health. Evolutionary Applications, 10, 226–230. doi:10.1111/eva.12448
  • Nikolic, T. V., Purac, J., Orcic, S., Kojic, D., Vujanovic, D., Stanimirovic, Z., … Blagojevic, D. P. (2015). Environmental effects on superoxide dismutase and catalase activity and expression in honey bee. Archives of Insect Biochemistry & Physiology, 90, 181–194. doi:10.1002/arch.21253
  • OIE. (2016). World Organisation for Animal Health, Manual of diagnostic tests and vaccines for terrestrial animals 2016, Chapter 2.2.2. American foulbrood of Honey Bees (infection of honey bees with Paenibacillus larvae). Retrieved from http://www.oie.int/fileadmin/Home/eng/Health_standards/tahm/2.02.02_AMERICAN_FOULBROOD.pdf
  • OIE. (2016). World Organisation for Animal Health, Manual of diagnostic tests and vaccines for terrestrial animals 2016, Chapter 2.2.3. European foulbrood of Honey Bees (infection of honey bees with Melissococcus plutonius). Retrieved from http://www.oie.int/fileadmin/Home/eng/Health_standards/tahm/2.02.03_EUROPEAN_FOULBROOD.pdf
  • Ruottinen, L., Berg, P., Kantanen, J., Kristensen, T. N., & Praebel, A. (2014). Status and conservation of the Nordic brown bee, Norway. The Nordic Genetic Resource Center (NOR). doi:10.13140/2.1.3597.9040
  • Seeley, T. D., & Smith, M. L. (2015). Crowding honeybee colonies in apiaries can increase their vulnerability to the deadly ectoparasite Varroa destructor. Apidologie, 46, 716–727. doi:10.1007/s13592-015-0361-2
  • Seeley, T.D., Tarpy, D. R., Griffin, S. R., Carcione, A., & Delaney, D. A. (2015). A survivor population of wild colonies of European honeybees in the northeastern United States: Investigating its genetic structure. Apidologie, 46, 654–666. doi:10.1007/s13592-015-0355-0
  • Simeunovic, P. (2015). Molecular detection and identification of microsporidia and viruses in honey bee colonies in Serbia (Doctoral dissertation). University of Belgrade, Belgrade, Serbia. Retrieved from http://uvidok.rcub.bg.ac.rs/bitstream/handle/123456789/252/Doktorat.pdf?sequence=1
  • Simeunovic, P., Stanimirovic, Z., Stevanovic, J., & Aleksic, N. (2012). The influence of pollen contaminated with pesticides on honey bees and their products. In R. Zivadinovic (Ed.), Apiecotech Serbia 2012, Apimondia Symposium 2012 (p. 45). Belgrade: The Serbian Federation of Beekeeping Organizations.
  • Simeunovic, P., Stevanovic, J., Vidanovic, D., Nisavic, J., Radovic, D., Stanisic, L., & Stanimirovic, Z. (2014). A survey of deformed wing virus and acute bee paralysis virus in honey bee colonies from Serbia using real-time RT-PCR. Acta Veterinaria, 64, 81–92. doi:10.2478/acve-2014-0009
  • Simeunovic, P., Stevanovic, J., Cirkovic, D., Radojicic, S., Lakic, N., Stanisic, Lj., & Stanimirovic, Z. (2014). Nosema ceranae and queen age influence the reproduction and productivity of the honey bee colony. Journal of Apicultural Research, 53, 545–554. doi:10.3896/IBRA.1.53.5.09
  • Simone-Finstrom, M., Li-Byarlay, H., Huang, M. H., Strand, M. K., Rueppell, O., & Tarpy, D. R. (2016). Migratory management and environmental conditions affect lifespan and oxidative stress in honey bees. Scientific Reports, 6, 32023; doi: 10.1038/srep32023
  • Stanimirovic, Z., Fister, S., & Stevanovic, J. (2003). Analysis of sister chromatid exchanges in cultured human lymphocytes treated with cymiazole hydrochloride. Acta Veterinaria, 53, 419–425. doi:10.2298/AVB0306419S
  • Stanimirovic, Z., Todorovic, D., Stevanovic, J., Mladenovic, M., Jankovic, L., & Djordjevic, M. (2003). Influence of cymiazole hydrochloride on mitotic and proliferative activities of cultured human lymphocytes. Acta Veterinaria, 53, 47–55. doi:10.2298/AVB0301047S
  • Stanimirovic, Z., Stevanovic, J., & Andjelkovic, M. (2005). Chromosomal diversity in Apis mellifera carnica from Serbia. Apidologie, 36, 31–42. doi:10.1051/apido:2004067
  • Stanimirovic, Z., Stevanovic, J., & Cirkovic, D. (2005). Behavioural defenses of the honey bee ecotype from Sjenica – Pester against Varroa destructor. Acta Veterinaria, 55(1), 69–82. doi:10.2298/AVB0501069S
  • Stanimirovic, Z., Cirkovic, D., Pejin, I. I., & Pejovic, D. (2007). Strategija ekološke kontrole u borbi protiv Varroa destructor. [Strategy for ecologic control in fighting Varroa destructor]. Veterinarski glasnik, 61, 11–35. doi:10.2298/VETGL0702011S
  • Stanimirovic, Z., Stevanovic, J., Bajic, V., & Radovic, I. (2007). Evaluation of genotoxic effects of fumagillin by cytogenetic tests in vivo. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 628, 1–10. doi:10.1016/j.mrgentox.2006.09.014
  • Stanimirovic, Z., Aleksic, N., Stevanovic, J., Cirkovic, D., Mirilovic, M., Djelic, N., & Stojic, V. (2011). The influence of pulverised sugar dusting on the degree of infestation of honey bee colonies with Varroa destructor. Acta Veterinaria, 61, 309–325. doi:10.2298/AVB1103309S
  • 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, 67, 191–200. doi:10.1515/acve-2017-0017
  • Stevanovic, J. (2007). Ecological–ethological defence mechanisms of Apis mellifera carnica against ectoparasite Varroa destructor on the territory of Serbia (Doctoral dissertation), University of Belgrade, Belgrade, Serbia.
  • Stevanovic, J., Stanimirovic, Z., Radakovic, M., & Stojic, V. (2008). In vitro evaluation of the clastogenicity of fumagillin. Environmental & Molecular Mutagenesis, 49, 594–601. doi:10.1002/em.20409
  • Stevanovic, J., Stanimirovic, Z., Genersch, E., Kovacevic, R. S., Ljubenkovic, J., Radakovic, M., & Aleksic, N. (2011). Dominance of Nosema ceranae in honey bees in the Balkan countries in the absence of symptoms of colony collapse disorder. Apidologie, 42, 49–58. doi:10.1051/apido/2010034
  • Stevanovic, J., Stanimirovic, Z., Lakic, N., Djelic, N., & Radovic, I. (2012). Stimulating effect of sugar dusting on honey bee grooming behaviour. Entomologia Experimentalis et Applicata, 143, 23–30. doi:10.1111/j.1570-7458.2012.01231.x
  • Stevanovic, J., Stanimirovic, Z., Aleksic, N., Simeunovic, P., & Vucicevic, M. (2012). The influence of natural and synthetic substances applied in honey bee health care on the quality of bee products (invited paper). In R. Zivadinovic (Ed.), Apiecotech Serbia 2012, Apimondia Symposium 2012 (pp. 9–34). Belgrade: The Serbian Federation of Beekeeping Organizations.
  • Stevanovic, J., Simeunovic, P., Gajic, B., Lakic, N., Radovic, D., Fries, I., & Stanimirovic, Z. (2013). Characteristics of Nosema ceranae infection in Serbian honey bee colonies. Apidologie, 44, 522–536. doi:10.1007/s13592-013-0203-z
  • Stevanovic, J., Schwarz, R. S., Vejnovic, B., Evans, J. D., Irwin, R. E., Glavinic, U., Stanimirovic, Z. (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. doi:10.1016/j.jip.2016.07.001
  • Tlak Gajger, I., Kolodziejek, J., Bakonyi, T. & Nowotny, N. (2014). Prevalence and distribution patterns of seven different honeybee viruses in diseased colonies: A case study from Croatia. Apidologie, 45, 701–706. doi:10.1007/s13592-014-0287-0
  • vanEngelsdorp, 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. doi:10.1371/journal.pone.0006481
  • vanEngelsdorp, D., & Meixner, M. D. (2010). A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. Journal of Invertebrate Pathology, 103, S80–S95. doi:10.1016/j.jip.2009.06.011
  • 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. doi:10.1016/j.jip.2017.11.003

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