Estimation of honey bee colony infection with Nosema ceranae and Varroa destructor using fluorescence spectroscopy in combination with differential scanning calorimetry of honey samples

References

• Bacandritsos, N., Granato, A., Budge, G., Papanastasiou, I., Roinioti, E., Caldon, M., Falcaro, C., Gallina, A., & Mutinelli, F. (2010). Sudden deaths and colony population decline in Greek honey bee colonies. Journal of Invertebrate Pathology, 105(3), 335–340. https://doi.org/10.1016/j.jip.2010.08.004
   PubMed Web of Science ®Google Scholar
• Bartolić, D., Stanković, M., Mutavdžić, D., Stanković, S., Jovanović, D., & Radotić, K. (2018). Multivariate curve resolution - Alternate least square analysis of excitation-emission matrices for maize flour contaminated with aflatoxin B1. Journal of Fluorescence, 28(3), 729–733. https://doi.org/10.1007/s10895-018-2246-z
   PubMed Web of Science ®Google Scholar
• Beaurepaire, A. L., Krieger, K. J., & Moritz, R. F. (2017). Seasonal cycle of inbreeding and recombination of the parasitic mite Varroa destructor in honeybee colonies and its implications for the selection of acaricide resistance. Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases, 50, 49–54. https://doi.org/10.1016/j.meegid.2017.02.011
   PubMed Web of Science ®Google Scholar
• Berthoud, H., Imdorf, A., Haueter, M., Radloff, S., & Neumann, P. (2010). Virus infections and winter losses of honey bee colonies (Apis mellifera). Journal of Apicultural Research, 49(1), 60–65. https://doi.org/10.3896/IBRA.1.49.1.08
   Web of Science ®Google Scholar
• Borneck, R., Viry, A., Martín-Hernández, R., & Higes, M. (2010). Honey bee colony losses in the Jura Region, France and related pathogens. Journal of Apicultural Research, 49(4), 334–336. https://doi.org/10.3896/IBRA.1.49.4.06
   Web of Science ®Google Scholar
• Bortolotti, A., Wong, Y. H., Korsholm, S. S., Bahring, N. H. B., Bobone, S., Tayyab, S., van de Weert, M., & Stella, L. (2016). On the purported “backbone fluorescence” in protein three-dimensional fluorescence spectra. RSC Advances, 6(114), 112870–112876. https://doi.org/10.1039/C6RA23426G
   Web of Science ®Google Scholar
• Brodschneider, R., Moosbeckhofer, R., & Crailsheim, K. (2010). Surveys as a tool to record winter losses of honey bee colonies: A two year case study in Austria and South Tyrol. Journal of Apicultural Research, 49(1), 23–30. https://doi.org/10.3896/IBRA.1.49.1.04
   Web of Science ®Google Scholar
• Carreck, N. L., Ball, B. V., & Martin, S. (2010). Honey bee colony collapse and changes in viral prevalence associated with Varroa destructor. Journal of Apicultural Research, 49(1), 93–94. https://doi.org/10.3896/IBRA.1.49.1.13
   Web of Science ®Google Scholar
• COLOSS BEEBOOK. (2013). COLOSS BEEBOOK Volume I: Standard Methods for Apis mellifera Research. edited by Vincent Dietemann, James D Ellis, Peter Neumann, pp. 636. ISBN-13: 978-0-86098-283-8
   Google Scholar
• Cordella, C., Moussa, I., Martel, A. C., Sbirrazzuoli, N., & Lizzani-Cuvelier, L. (2002). Recent developments in food characterization and adulteration detection: Technique-oriented perspectives. Journal of Agricultural and Food Chemistry, 50(7), 1751–1764. https://doi.org/10.1021/jf011096z
   PubMed Web of Science ®Google Scholar
• Csáki, T., Heltai, M., Markolt, F., Kovács, B., Békési, L., Ladányi, M., Péntek-Zakar, E., Meana, A., Botías, C., Martín-Hernández, R., & Higes, M. (2015). Permanent prevalence of Nosema ceranae in honey bees (Apis mellifera) in Hungary. Acta Veterinaria Hungarica, 63(3), 358–369. https://doi.org/10.1556/004.2015.034
   PubMed Web of Science ®Google Scholar
• Dainat, B., Evans, J. D., Chen, Y. P., Gauthier, L., & Neumann, P. (2012a). Dead or alive: deformed wing virus and Varroa destructor reduce the life span of winter honeybees. Applied and Environmental Microbiology, 78(4), 981–987. https://doi.org/10.1128/AEM.06537-11
   PubMed Web of Science ®Google Scholar
• Dainat, B., Evans, J. D., Chen, Y. P., Gauthier, L., & Neumann, P. (2012b). Predictive markers of honey bee colony collapse. PLOS One, 7(2), e3215. https://doi.org/10.1371/journal.pone.0032151
   Web of Science ®Google Scholar
• Dietemann, V., Nazzi, F., Martin, S. J., Anderson, D., Locke, B., Delaplane, K. S., Wauquiez, Q., Tannahill, C., Frey, E., Ziegelmann, B., Rosenkranz, P., & Ellis, J. D. (2013). Standard methods for Apis mellifera research. Journal of Apicultural Research, 52(1), 1–54. https://doi.org/10.3896/IBRA.1.52.1.09
   Google Scholar
• Francis, R. M., Nielsen, S. L., & Kryger, P. (2013). Varroa-virus interaction in collapsing honey bee colonies. PLOS One, 8(3), e57540. https://doi.org/10.1371/journal.pone.0057540
   PubMed Web of Science ®Google Scholar
• Genersch, E., Von der Ohe, W., Kaatz, H., Schroeder, A., Otten, C., Buchler, R., Berg, S., Ritter, W., Muhlen, W., Gisder, S., Meixner, M., Liebig, G., & Rosenkranz, P. (2010). The German bee monitoring project: A long term study to understand periodically high winter losses of honey bee colonies. Apidologie, 41(3), 332–352. https://doi.org/10.1051/apido/2010014
   Web of Science ®Google Scholar
• Hartel, R. W., Ergun, R., & Vogel, S. (2011). Phase/State Transitions of confectionery sweeteners: Thermodynamic and kinetic aspects. Comprehensive Reviews in Food Science and Food Safety, 10(1), 17–32. https://doi.org/10.1111/j.1541-4337.2010.00136.x
   Web of Science ®Google Scholar
• Hatjina, F., Tsoktouridis, G., Bouga, M., Charistos, L., Evangelou, V., Avtzis, D., Meeus, I., Brunain, M., Smagghe, G., & Graaf, D. C. (2011). Polar tube protein gene diversity among Nosema ceranae strains derived from a Greek honey bee health study. Journal of Invertebrate Pathology, 108(2), 131–134. https://doi.org/10.1016/j.jip.2011.07.003
   PubMed Web of Science ®Google Scholar
• Higes, M., Martín-Hernández, R., Botías, C., Garrido Bailón, E., González-Porto, A. V., Barrios, L., Del Nozal, M. J., Bernal, L. J., Jiménez, J. J., García Palencia, P., & Meana, A. (2008). How natural infection by Nosema ceranae causes honeybee colony collapse. Environmental Microbiology, 10(10), 2659–2669. https://doi.org/10.1111/j.1462-2920.2008.01687.x
   PubMed Web of Science ®Google Scholar
• Higes, M., Martín-Hernández, R., Garrido-Bailón, E., González-Porto, A. V., García Palencia, P., Meana, A., Del Nozal, M. J., Mayo, R., & Bernal, J. L. (2009). Honeybee colony collapse due to Nosema ceranae in professional apiaries. Environmental Microbiology Reports, 1(2), 110–113. https://doi.org/10.1111/j.1758-2229.2009.00014.x
   PubMed Web of Science ®Google Scholar
• Higes, M., Martín-Hernández, R., Martínez-Salvador, A., Garrido-Bailón, E., González-Porto, A. V., Meana, A., Bernal, J. L., Del Nozal, M. J., & Bernal, J. (2010). A preliminary study of the epidemiological factors related to honey bee colony loss in Spain. Environmental Microbiology Reports, 2(2), 243–250. https://doi.org/10.1111/j.1758-2229.2009.00099.x
   PubMed Web of Science ®Google Scholar
• Lang, M., Stober, F., & Lichtenthaler, H. K. (1991). Fluorescence emission spectra of plant leaves and plant constituents. Radiation and Environmental Biophysics, 30(4), 333–347. https://doi.org/10.1007/BF01210517
   PubMed Web of Science ®Google Scholar
• Le Conte, Y., Ellis, M., & Ritter, W. (2010). Varroamites and honey bee health: can varroa explain part of the colony losses? Apidologie, 41(3), 353–363. https://doi.org/10.1051/apido/2010017
   Web of Science ®Google Scholar
• Martín‐Hernández, R., Bartolomé, C., Chejanovsky, N., Le Cont, Y., Dalmon, A., Dussaubat, C., García‐Palencia, P., Meana, A., Pinto, M. A., Soroker, V., & Higes, M. (2018). Nosema ceranae in Apis mellifera: A 12 years postdetection perspective. Environmental Microbiology, 20(4), 1302–1329. https://doi.org/10.1111/1462-2920.14103
   PubMed Web of Science ®Google Scholar
• Martín-Hernández, R., Meana, A., Prieto, L., Salvador, A. M., Garrido-Bailón, E., & Higes, M. (2007). Outcome of colonization of Apis mellifera by Nosema ceranae. Applied and Environmental Microbiology, 73(20), 6331–6338. https://doi.org/10.1128/AEM.00270-07
   PubMed Web of Science ®Google Scholar
• Mendieta, J., Díaz-Cruz, M. S., Esteban, M., & Tauler, R. (1998). Multivariate curve resolution: a possible tool in the detection of intermediate structures in protein folding. Biophysical Journal, 74(6), 2876–2888. https://doi.org/10.1016/S0006-3495(98)77994-9
   PubMed Web of Science ®Google Scholar
• Milovanovic, P., Hrncic, D., Radotic, K., Stankovic, M., Mutavdzic, D., Djonic, D., Rasic-Markovic, A., Djuric, D., Stanojlovic, O., & Djuric, M. (2017). Moderate hyperhomocysteinemia induced by short-term dietary methionine overload alters bone microarchitecture and collagen features during growth. Life Sciences, 191, 9–16. https://doi.org/10.1016/j.lfs.2017.10.008
   PubMed Web of Science ®Google Scholar
• Mutinelli, F., Costa, C., Lodesani, M., Baggio, A., Medrzycki, P., Formato, G., & Porrini, C. (2010). Honey bee colony losses in Italy. Journal of Apicultural Research, 49(1), 119–120. https://doi.org/10.3896/IBRA.1.49.1.24
   Web of Science ®Google Scholar
• Nazarian, H., Taghavizad, R., & Majd, A. (2010). Origin of honey proteins and method for its quality control. Pakistan Journal of Botany, 42, 3221–3228.
   Web of Science ®Google Scholar
• Negri, P., Villalobos, E., Szawarski, N., Damiani, N., Gende, L., Garrido, M., Maggi, M., Quintana, S., Lamattina, L., & Eguaras, M. (2019). Towards precision nutrition: A novel concept linking phytochemicals, immune response and honey bee health. Insects, 10(11), 401. https://doi.org/10.3390/insects10110401
   PubMed Web of Science ®Google Scholar
• Ruoff, K., Luginbu, W., Künzli, R., Bogdanov, S., Bosset, J. O., Von Der, K., Von Der Ohe, W., & Amado, R. (2006). Authentication of the botanical and geographical origin of honey by front-face fluorescence spectroscopy. Journal of Agricultural and Food Chemistry, 54(18), 6858–6866. https://doi.org/10.1021/jf060697t
   PubMed Web of Science ®Google Scholar
• Snow, J. W., Ceylan Koydemir, H., Karinca, D. K., Liang, K., Tseng, D., & Ozcan, A. (2019). Rapid imaging, detection, and quantification of Nosema ceranae spores in honey bees using mobile phone-based fluorescence microscopy. Lab on a Chip, 19(5), 789–797. https://doi.org/10.1039/C8LC01342J
   PubMed Web of Science ®Google Scholar
• Soroker, V., Hetzroni, A., Yakobson, B., David, D., David, A., Voet, H., Slabezki, Y., Efrat, H., Levski, S., Kamer, Y., Klinberg, E., Zioni, N., Inbar, S., & Chejanovsky, N. (2011). Evaluation of colony losses in Israel in relation to the incidence of pathogens and pests. Apidologie, 42(2), 192–199. https://doi.org/10.1051/apido/2010047
   Web of Science ®Google Scholar
• Stanković, M., Bartolić, D., Šikoparij, B., Spasojević, D., Mutavdžić, D., Natić, M., & Radotić, K. (2019). Variability estimation of the protein and phenol total content in honey using front face fluorescence spectroscopy coupled with MCR-ALS analysiss. Journal of Applied Spectroscopy, 86(2), 256–249. https://doi.org/10.1007/s10812-019-00809-1
   Web of Science ®Google Scholar
• Stanković, M., Nikčević, M., & Radotić, K. (2020). Annual variation of proteins and phenols in honey of a bee society using fluorescence spectroscopy: a way to assess effects of antivarroa treatments on honey composition. European Food Research and Technology, 246(7), 1515–1518. https://doi.org/10.1007/s00217-020-03507-x
   Web of Science ®Google Scholar
• Wegener, J., Ruhnke, H., Scheller, K., Mispagel, S., Knollmann, U., Kamp, G., & Bienefeld, K. (2016). Pathogenesis of varroosis at the level of the honey bee (Apis mellifera) colony. Journal of Insect Physiology, 91-92, 1–9. https://doi.org/10.1016/j.jinsphys.2016.06.004
   PubMed Web of Science ®Google Scholar