1. bookVolume 72 (2022): Issue 2 (June 2022)
Journal Details
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eISSN
1820-7448
First Published
25 Mar 2014
Publication timeframe
4 times per year
Languages
English
access type Open Access

Diet Supplementation Helps Honey Bee Colonies in Combat Infections by Enhancing their Hygienic Behaviour

Published Online: 04 Jul 2022
Volume & Issue: Volume 72 (2022) - Issue 2 (June 2022)
Page range: 145 - 166
Accepted: 20 May 2022
Journal Details
License
Format
Journal
eISSN
1820-7448
First Published
25 Mar 2014
Publication timeframe
4 times per year
Languages
English
Abstract

The hygienic behavior in honey bees is a complex polygenic trait that serves as a natural defense mechanism against bacterial and fungal brood diseases and Varroa destructor mites infesting brood cells. The aim of this study was to evaluate the effect of a dietary amino acids and vitamins supplement “BEEWELL AminoPlus” on hygienic behavior of Apis mellifera colonies combating microsporidial and viral infections. The experiment was performed during a one-year period on 40 colonies alloted to five groups: one supplemented and infected with Nosema ceranae and four viruses (Deformed wing virus - DWV, Acute bee paralysis virus - ABPV, Chronic bee paralysis virus - CBPV and Sacbrood virus – SBV), three not supplemented, but infected with N. ceranae and/ or viruses, and one negative control group. Beside the l isted pathogens, honey bee trypanosomatids were also monitored in all groups.

The supplement “BEEWELL AminoPlus” induced a significant and consistent increase of the hygienic behavior in spite of the negative effects of N. ceranae and viral infections. N. ceranae and viruses significantly and consistently decreased hygienic behavior, but also threatened the survival of bee colonies. The tested supplement showed anti-Nosema effect, since the N. ceranae infection level significantly and consistently declined only in the supplemented group. Among infected groups, only the supplemented one remained Lotmaria passim-free throughout the study. In conclusion, diet supplementation enhances hygienic behavior of honey bee colonies and helps them fight the most common infections of honey bees.

Keywords

1. Gallai N, Salles JM, Settele J, Vaissière BE: Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 2009, 68(3): 810-821.10.1016/j.ecolecon.2008.06.014 Search in Google Scholar

2. Stanimirovic Z, Glavinic U, Ristanic M, Aleksic N, Jovanovic N, Vejnovic B, Stevanovic J: Looking for the causes of and solutions to the issue of honey bee colony losses. Acta Vet-Beograd 2019, 69(1): 1–31. Search in Google Scholar

3. Neov B, Georgieva A, Shumkova R, Radoslavov G, Hristov P: Biotic and abiotic factors associated with colonies mortalities of managed honey bee (Apis mellifera). Diversity 2019, 11(12): 237.10.3390/d11120237 Search in Google Scholar

4. Sanchez-Bayo F, Goka K: Pesticide residues and bees - a risk assessment. PLoS One 2014, 9(4): e94482.10.1371/journal.pone.0094482398181224718419 Search in Google Scholar

5. Glavinic U, Tesovnik T, Stevanovic J, Zorc M, Cizelj I, Stanimirovic Z, Narat M: Response of adult honey bees treated in larval stage with prochloraz to infection with Nosema ceranae. PeerJ 2019, 7: e6325.10.7717/peerj.6325637191730775168 Search in Google Scholar

6. Tesovnik T, Zorc M, Ristanic M, Glavinic U, Stevanovic J, Narat M, Stanimirovic Z: Exposure of honey bee larvae to thiamethoxam and its interaction with Nosema ceranae infection in adult honey bees. Environ Pollut 2020, 256: 113443.10.1016/j.envpol.2019.11344331733951 Search in Google Scholar

7. Nikolic TV, Purac J, Orcic S, Kojic D, Vujanovic D, Stanimirovic Z, Grzetic I, Ilijevic K, Sikoparija B, Blagojevic DP: Environmental effects on superoxide dismutase and catalase activity and expression in honey bee. Arch Insect Biochem Physiol 2015, 90(40): 181-194.10.1002/arch.2125326314562 Search in Google Scholar

8. Monchanin C, Drujont E, Devaud JM, Lihoreau M, Barron AB: Metal pollutants have additive negative effects on honey bee cognition. J Exp Biol 2021, 224(12): jeb241869.10.1242/jeb.24186934002230 Search in Google Scholar

9. McMenamin AJ, Genersch E: Honey bee colony losses and associated viruses. Curr Opin Insect Sci 2015, 8: 121-129.10.1016/j.cois.2015.01.01532846659 Search in Google Scholar

10. Sánchez-Bayo F, Goulson D, Pennacchio F, Nazzi F, Goka K, Desneux N: Are bee diseases linked to pesticides?—A brief review. Environ Int 2016, 89: 7-11.10.1016/j.envint.2016.01.00926826357 Search in Google Scholar

11. Goulson D, Nicholls E, Botías C, Rotheray EL: Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 2015, 347(6229), 1255957.10.1126/science.125595725721506 Search in Google Scholar

12. Durant JL: Where have all the flowers gone? Honey bee declines and exclusions from floral resources. J Rural Stud 2019, 65: 161-171.10.1016/j.jrurstud.2018.10.007 Search in Google Scholar

13. Higes M, Martin-Hernandez R, Meana A: Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie 2010, 41(3): 375-392.10.1051/apido/2010019 Search in Google Scholar

14. Ravoet J, Maharramov J, Meeus I, De Smet L, Wenseleers T, Smagghe G, De Graaf DC: Comprehensive bee pathogen screening in Belgium reveals Crithidia mellificae as a new contributory factor to winter mortality. PLoS One 2013, 8(8): e72443.10.1371/journal.pone.0072443375327523991113 Search in Google Scholar

15. Goblirsch M, Huang ZY, Spivak M: Physiological and behavioral changes in honey bees (Apis mellifera) induced by Nosema ceranae infection. PLoS One 2013, 8(3): e58165.10.1371/journal.pone.0058165359017423483987 Search in Google Scholar

16. Goblirsch M: Nosema ceranae disease of the honey bee (Apis mellifera). Apidologie 2018, 49(1) 131-150.10.1007/s13592-017-0535-1 Search in Google Scholar

17. Martín-Hernández R, Bartolomé C, Chejanovsky N, Le Conte Y, Dalmon A, Dussaubat C, García-Palencia P, Meana A, Pinto MA, Soroker V, Higes M: Nosema ceranae in Apis mellifera: a 12 years postdetection perspective. Environ Microbiol 2018, 20(4): 1302-1329.10.1111/1462-2920.1410329575513 Search in Google Scholar

18. Liu Q, Lei J, Darby AC, Kadowaki T: Trypanosomatid parasite dynamically changes the transcriptome during infection and modifies honey bee physiology. Commun Biol 2020, 3(1): 1-8.10.1038/s42003-020-0775-x699460832005933 Search in Google Scholar

19. Gómez-Moracho T, Buendía-Abad M, Benito M, García-Palencia P, Barrios L, Bartolomé C, Maside X, Meana A, Jiménez-Antón MD, Olías-Molero AI, Alunda JM, Martín-Hernández R, Higes M: Experimental evidence of harmful effects of Crithidia mellificae and Lotmaria passim on honey bees. Int J Parasitol 2020, 50(13) 1117-1124.10.1016/j.ijpara.2020.06.00932822679 Search in Google Scholar

20. Buendía-Abad M, García-Palencia P, de Pablos LM, Alunda JM, Osuna A, Martín-Hernández R, Higes M: First description of Lotmaria passim and Crithidia mellificae haptomonad stages in the honeybee hindgut. Int J Parasitol 2022, 52(1): 65-75.10.1016/j.ijpara.2021.06.00534416272 Search in Google Scholar

21. McMenamin AJ, Genersch E: Honey bee colony losses and associated viruses. Curr Opin Insect Sci 2015, 8: 121-129.10.1016/j.cois.2015.01.01532846659 Search in Google Scholar

22. Natsopoulou ME, McMahon DP, Doublet V, Frey E, Rosenkranz P, Paxton RJ: The virulent, emerging genotype B of deformed wing virus is closely linked to overwinter honeybee worker loss. Sci Rep 2017, 7(1): 1-9.10.1038/s41598-017-05596-3550792628701778 Search in Google Scholar

23. McMenamin AJ, Flenniken ML: Recently identified bee viruses and their impact on bee pollinators. Curr Opin Insect Sci 2018, 26: 120–129.10.1016/j.cois.2018.02.00929764651 Search in Google Scholar

24. Grozinger CM, Flenniken ML: Bee viruses: Ecology, pathogenicity, and impacts. Annu Rev Entomol 2019, 64: 205-226.10.1146/annurev-ento-011118-11194230629896 Search in Google Scholar

25. Yañez O, Piot N, Dalmon A, de Miranda JR, Chantawannakul P, Panziera D, Amiri E, Smagghe G, Schroeder D, Chejanovsky N: Bee viruses: Routes of infection in Hymenoptera. Front Microbiol 2020, 11: 943.10.3389/fmicb.2020.00943727058532547504 Search in Google Scholar

26. Bacandritsos N, Granato A, Budge G, Papanastasiou I, Roinioti E, Caldon M, Falcaro C, Gallina A, Mutinelli F: Sudden deaths and colony population decline in Greek honey bee colonies. J Invertebr Pathol 2010, 105(3): 335–340.10.1016/j.jip.2010.08.00420804765 Search in Google Scholar

27. 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: Evaluation of colony losses in Israel in relation to the incidence of pathogens and pests. Apidologie 2011, 42(2): 192–199.10.1051/apido/2010047 Search in Google Scholar

28. Zheng HQ, Gong HR, Huang SK, Sohr A, Hu FL, Chen YP: Evidence of the synergistic interaction of honey bee pathogens Nosema ceranae and deformed wing virus. Vet Microbiol 2015, 177(1-2): 1-6.10.1016/j.vetmic.2015.02.00325752367 Search in Google Scholar

29. D’Alvise P, Seeburger V, Gihring K, Kieboom M, Hasselmann M: Seasonal dynamics and co-occurrence patterns of honey bee pathogens revealed by high-throughput RT-qPCR analysis. Ecol Evol 2019, 9(18): 10241-10252.10.1002/ece3.5544678784331624548 Search in Google Scholar

30. Arismendi N, Caro S, Castro MP, Vargas M, Riveros G, Venegas T: Impact of mixed infections of gut parasites Lotmaria passim and Nosema ceranae on the lifespan and immune-related biomarkers in Apis mellifera. Insects 2020, 11(7), 420.10.3390/insects11070420741207732650366 Search in Google Scholar

31. Wilson-Rich N, Spivak M, Fefferman NH, Starks PT: Genetic, individual, and group facilitation of disease resistance in insect societies. Annu Rev Entomol 2009, 54: 405-423.10.1146/annurev.ento.53.103106.09330118793100 Search in Google Scholar

32. Evans JD, Spivak M: Socialized medicine: individual and communal disease barriers in honey bees. J Invertebr Pathol 2010, 103, S62-S72.10.1016/j.jip.2009.06.01919909975 Search in Google Scholar

33. Leclercq G, Pannebakker B, Gengler N, Nguyen BK, Francis F: Drawbacks and benefits of hygienic behavior in honey bees (Apis mellifera L.): a review. J Apic Res 2017, 56(4): 366-375.10.1080/00218839.2017.1327938 Search in Google Scholar

34. Boecking O, Spivak M: Behavioral defenses of honey bees against Varroa jacobsoni Oud. Apidologie 1999, 30(2-3): 141–158.10.1051/apido:19990205 Search in Google Scholar

35. Spivak M: Honey bee hygienic behavior and defense against Varroa jacobsoni. Apidologie 1996, 27(4): 245-260.10.1051/apido:19960407 Search in Google Scholar

36. Stanimirovic Z, Pejovic D, Stevanovic J, Vucinic M, Mirilovic M: Investigations of hygienic behaviour and disease resistance in organic beekeeping of two honeybee ecogeographic varieties from Serbia. Acta Vet-Beograd 2002, 52(2-3): 169-179.10.2298/AVB0203169S Search in Google Scholar

37. Stanimirovic Z, Stevanovic J, Cirkovic D: Behavioural defenses of the honey bee ecotype from Sjenica – Pester against Varroa destructor. Acta Vet-Beograd 2005, 55(1), 69-82.10.2298/AVB0501069S Search in Google Scholar

38. Swanson JA, Torto B, Kells SA, Mesce KA, Tumlinson JH, Spivak M: Odorants that induce hygienic behavior in honeybees: identification of volatile compounds in chalkbrood-infected honeybee larvae. J Chem Ecol 2009, 35(9): 1108-1116.10.1007/s10886-009-9683-819816752 Search in Google Scholar

39. Toufailia HM, Amiri E, Scandian L, Kryger P, Ratnieks FL: Towards integrated control of varroa: effect of variation in hygienic behaviour among honey bee colonies on mite population increase and deformed wing virus incidence. J Apic Res 2014, 53(5): 555-562.10.3896/IBRA.1.53.5.10 Search in Google Scholar

40. Lin Z, Page P, Li L, Qin Y, Zhang Y, Hu F, Neumann P, Zheng H, Dietemann V: Go east for better honey bee health: Apis cerana is faster at hygienic behavior than A. mellifera. PLoS One 2016, 11(9): e0162647.10.1371/journal.pone.0162647501585327606819 Search in Google Scholar

41. Harbo JR, Harris JW: Heritability in honey bees (Hymenoptera: Apidae) of characteristics associated with resistance to Varroa jacobsoni (Mesostigmata: Varroidae). J Econ Entomol 1999, 92(2): 261-265.10.1093/jee/92.2.261 Search in Google Scholar

42. Boecking O, Bienefeld K, Drescher W: Heritability of the Varroa-specific hygienic behaviour in honey bees (Hymenoptera: Apidae). J Anim Breed Genet 2000, 117(6): 417-424.10.1046/j.1439-0388.2000.00271.x Search in Google Scholar

43. Stanimirovic Z, Stevanovic J, Mirilovic M, Stojic V: Heritability of hygienic behaviour in grey honey bees (Apis mellifera carnica). Acta Vet-Beograd 2008, 58(5-6): 593-601.10.2298/AVB0806593S Search in Google Scholar

44. Pernal SF, Sewalem A, Melathopoulos AP: Breeding for hygienic behaviour in honeybees (Apis mellifera) using free-mated nucleus colonies. Apidologie 2012, 43(4): 403-416.10.1007/s13592-011-0105-x Search in Google Scholar

45. Guarna MM, Hoover SE, Huxter E, Higo H, Moon KM, Domanski D, Bixby ME, Melathopoulos AP, Ibrahim A, Peirson M, Desai S, Micholson D, White R, Borchers CH, Currie RW, Pernal SF, Foster LJ: Peptide biomarkers used for the selective breeding of a complex polygenic trait in honey bees. Sci Rep 2017, 7(1): 1-10.10.1038/s41598-017-08464-2556695928827652 Search in Google Scholar

46. Zakar E, Javor A, Kusza S: Genetic bases of tolerance to Varroa destructor in honey bees (Apis mellifera L.). Insectes Soc 2014, 61(3): 207-215.10.1007/s00040-014-0347-5 Search in Google Scholar

47. Hoppe A, Du M, Bernstein R, Tiesler FK, Kärcher M, Bienefeld K: Substantial genetic progress in the international Apis mellifera carnica population since the implementation of genetic evaluation. Insects 2020, 11(11): 768.10.3390/insects11110768769499533171738 Search in Google Scholar

48. Lapidge KL, Oldroyd BP, Spivak M: Seven suggestive quantitative trait loci influence hygienic behavior of honey bees. Naturwissenschaften 2002, 89(12): 565–568.10.1007/s00114-002-0371-612536279 Search in Google Scholar

49. Oxley PR, Spivak M, Oldroyd BP: Six quantitative trait loci influence task thresholds for hygienic behaviour in honeybees (Apis mellifera). Mol Ecol 2010, 19(7): 1452-1461.10.1111/j.1365-294X.2010.04569.x20298472 Search in Google Scholar

50. Le Conte Y, Alaux C, Martin JF, Harbo JR, Harris JW, Dantec C, Séverac D, Cros-Arteil S, Navajas M: Social immunity in honeybees (Apis mellifera): Transcriptome analysis of Varroa–hygienic behaviour. Insect Mol Biol 2011, 20(3): 399-408.10.1111/j.1365-2583.2011.01074.x21435061 Search in Google Scholar

51. Tsuruda JM, Harris JW, Bourgeois L, Danka RG, Hunt GJ: High-resolution linkage analyses to identify genes that influence varroa sensitive hygiene behavior in honey bees. PLoS One 2012, 7(11): e48276.10.1371/journal.pone.0048276348772723133626 Search in Google Scholar

52. Boutin S, Alburaki M, Mercier PL, Giovenazzo P, Derome N: Differential gene expression between hygienic and non-hygienic honeybee (Apis mellifera L.) hives. BMC Genomics 2015, 16(1): 500.10.1186/s12864-015-1714-y449187026149072 Search in Google Scholar

53. Scannapieco AC, Mannino MC, Soto G, Palacio MA, Cladera JL, Lanzavecchia SB: Expression analysis of genes putatively associated with hygienic behavior in selected stocks of Apis mellifera L. from Argentina. Insectes Soc 2017, 64(4): 485-494.10.1007/s00040-017-0567-6 Search in Google Scholar

54. Harpur BA, Guarna MM, Huxter E, Higo H, Moon KM, Hoover SE, Ibrahim A, Melathopoulos AP, Desai S, Currie RW, Pernal SF: Integrative genomics reveals the genetics and evolution of the honey bee’s social immune system. Genome Biol Evol 2019, 11(3): 937-948.10.1093/gbe/evz018644738930768172 Search in Google Scholar

55. Teixeira ÉW, de Paiva Daibert RM, Glatzl Júnior LA, da Silva MV, Alves ML, Evans JD, Toth AL: Transcriptomic analysis suggests candidate genes for hygienic behavior in African-derived Apis mellifera honeybees. Apidologie 2021, 52(2): 447-462.10.1007/s13592-020-00834-6 Search in Google Scholar

56. Bigio G, Schürch R, Ratnieks FLW: Hygienic behavior in honey bees (Hymenoptera: Apidae): effects of brood, food, and time of the year. J Econ Entomol 2013, 106(6): 2280-2285.10.1603/EC1307624498725 Search in Google Scholar

57. Masaquiza D, Vargas J, Ortíz N, Salazar R, Curbelo L, Pérez A, Arenal A: Hygienic behavior of Apis mellifera and its relationship with Varroa destructor infestation and honey production in the central highlands of Ecuador. Insects 2021, 12(11): 966.10.3390/insects12110966861999834821767 Search in Google Scholar

58. Tison L, Riva C, Maisonnasse A, Kretzschmar A, Hervé MR, Le Conte Y, Mondet F: Seasonal and environmental variations influencing the Varroa Sensitive Hygiene trait in the honey bee. Entomol Gen 2022, 42: 1-10.10.1127/entomologia/2021/1280 Search in Google Scholar

59. Xonis C, Thrasyvoulou A, El Taj HF: Variability of hygienic behavior in bee Apis mellifera macedonica. Bulg J Agric Sci 2015, 21(3): 674-679. Search in Google Scholar

60. Valizadeh P, Guzman-Novoa E, Goodwin PH: Effect of immune inducers on Nosema ceranae multiplication and their impact on honey bee (Apis mellifera L.) survivorship and behaviors. Insects 2020, 11(9): 572.10.3390/insects11090572756369132858847 Search in Google Scholar

61. Wu-Smart J, Spivak M: Sub-lethal effects of dietary neonicotinoid insecticide exposure on honey bee queen fecundity and colony development. Sci Rep 2016, 6(1): 32108.10.1038/srep32108499979727562025 Search in Google Scholar

62. Neumann P, Blacquière T: The Darwin cure for apiculture? Natural selection and managed honeybee health. Evol Appl 2017, 10(3): 226-230.10.1111/eva.12448532240728250807 Search in Google Scholar

63. Taric E, Glavinic U, Stevanovic J, Vejnovic B, Aleksic N, Dimitrijevic V, Stanimirovic Z: Occurrence of honey bee (Apis mellifera L.) pathogens in commercial and traditional hives. J Apic Res 2019, 58(3): 433-443.10.1080/00218839.2018.1554231 Search in Google Scholar

64. Taric E, Glavinic U, Vejnovic B, Stanojkovic A, Aleksic N, Dimitrijevic V, Stanimirovic Z: Oxidative stress, endoparasite prevalence and social immunity in bee colonies kept traditionally vs. those kept for commercial purposes. Insects 2020, 11(5): 266.10.3390/insects11050266729033032349295 Search in Google Scholar

65. Stevanovic J, Stanimirovic Z, Lakic N, Aleksic N, Simeunovic P, Kulisic Z: Safety assessment of sugar dusting treatments by analysis of hygienic behaviour in honey bee colonies. Arch Biol Sci 2011, 63(4): 1199-1207.10.2298/ABS1104199S Search in Google Scholar

66. Colin T, Lim MY, Quarrell SR, Allen GR, Barron AB: Effects of thymol on European honey bee hygienic behaviour. Apidologie 2019, 50(2): 141-152.10.1007/s13592-018-0625-8 Search in Google Scholar

67. Papežíková I, Palíková M, Syrová E, Zachová A, Somerlíková K, Kováčová V, Pecková L: Effect of feeding honey bee (Apis mellifera Hymenoptera: Apidae) colonies with honey, sugar solution, inverted sugar, and wheat starch syrup on nosematosis prevalence and intensity. J Econ Entomol 2020, 113(1): 26-33.10.1093/jee/toz25131560397 Search in Google Scholar

68. Frizzera D, Del Fabbro S, Ortis G, Zanni V, Bortolomeazzi R, Nazzi F, Annoscia D: Possible side effects of sugar supplementary nutrition on honey bee health. Apidologie 2020, 51(4), 594-608.10.1007/s13592-020-00745-6 Search in Google Scholar

69. Paray BA, Kumari I, Hajam YA, Sharma B, Kumar R, Albeshr MF, Farah MA, Khan JM: Honeybee nutrition and pollen substitutes: A review. Saudi J Biol Sci 2021, 28(1): 1167-1176.10.1016/j.sjbs.2020.11.053778383433424413 Search in Google Scholar

70. Glavinic U, Stankovic B, Draskovic V, Stevanovic J, Petrovic T, Lakic N, Stanimirovic Z: Dietary amino acid and vitamin complex protects honey bee from immunosuppression caused by Nosema ceranae. PLoS One 2017, 12(11): e0187726.10.1371/journal.pone.0187726567888729117233 Search in Google Scholar

71. Glavinic U, Stevanovic J, Ristanic M, Rajkovic M, Davitkov D, Lakic N, Stanimirovic Z: Potential of fumagillin and Agaricus blazei mushroom extract to reduce Nosema ceranae in honey bees. Insects 2021a, 12(4): 282.10.3390/insects12040282806445733806001 Search in Google Scholar

72. Glavinic U, Rajkovic M, Vunduk J, Vejnovic B, Stevanovic J, Milenkovic I, Stanimirovic Z: Effects of Agaricus bisporus mushroom extract on honey bees infected with Nosema ceranae. Insects, 2021b, 12(10): 915.10.3390/insects12100915854133334680684 Search in Google Scholar

73. Glavinic U: The Effects of various antimicrobials and supplements on the expression of immune-related genes, oxidative stress and survival of honey bee Apis mellifera infected with microsporidium Nosema ceranae. Ph.D. Thesis, Faculty of Veterinary Medicine, University of Belgrade, Belgrade, Serbia, 2019. Search in Google Scholar

74. Stevanovic J, Stanimirovic Z, Simeunovic P, Lakic N, Radovic I, Sokovic M, Van Griensven JLD: The effect of Agaricus brasiliensis extract supplementation on honey bee colonies. An Acad Bras Ciênc 2018, 90: 219-229.10.1590/0001-376520182015018229424386 Search in Google Scholar

75. Dolasevic S: The influence of diet on the quality of naturally and artificially obtained queen bees, and vitellogenin gene expression during their development. Ph.D. Thesis, Faculty of Agriculture, University of Belgrade, Belgrade, Serbia, 2020. Search in Google Scholar

76. Dolasevic S, Stevanovic J, Aleksic N, Glavinic U, Deletic N, Mladenovic M, Stanimirovic Z: The effect of diet types on some quality characteristics of artificially reared Apis mellifera queens. J Apic Res 2020, 59(1): 115-123.10.1080/00218839.2019.1673965 Search in Google Scholar

77. Ricigliano VA, Simone-Finstrom M: Nutritional and prebiotic efficacy of the microalga Arthrospira platensis (spirulina) in honey bees. Apidologie 2020, 51: 898-910.10.1007/s13592-020-00770-5 Search in Google Scholar

78. Ricigliano VA, Ihle KE, Williams ST: Nutrigenetic comparison of two Varroa-resistant honey bee stocks fed pollen and spirulina microalgae. Apidologie 2021, 52(4): 873–886.10.1007/s13592-021-00877-3 Search in Google Scholar

79. Jovanovic NM, Glavinic U, Delic B, Vejnovic B, Aleksic N, Mladjan V, Stanimirovic Z: Plant-based supplement containing B-complex vitamins can improve bee health and increase colony performance. Prev Vet Med 2021, 190: 105322.10.1016/j.prevetmed.2021.10532233744676 Search in Google Scholar

80. Stevanovic J, Schwarz RS, Vejnovic B, Evans JD, Irwin RE, Glavinic U, Stanimirovic Z: Species-specific diagnostics of Apis mellifera trypanosomatids: A nine-year survey (2007–2015) for trypanosomatids and microsporidians in Serbian honey bees. J Invertebr Pathol 2016, 139: 6–11.10.1016/j.jip.2016.07.00127392956 Search in Google Scholar

81. Vejnovic B, Stevanovic J, Schwarz RS, Aleksic N, Mirilovic M, Jovanovic NM, Stanimirovic Z: Quantitative PCR assessment of Lotmaria passim in Apis mellifera colonies co-infected naturally with Nosema ceranae. J Invertebr Pathol 2018, 151:76-81.10.1016/j.jip.2017.11.00329113738 Search in Google Scholar

82. Michalczyk M, Sokół R, Bancerz-Kisiel A: Coexistence between selected pathogens in honey bee workers. J Apic Res 2021, https://doi.org/10.1080/00218839.2021.1994261. Search in Google Scholar

83. Dietemann V, Nazzi F, Martin SJ, Anderson D, Locke B, Delaplane KS, Wauquiez Q, Tannahill C, Frey E, Ziegelmann B, Rosenkarnz P, Ellis JD: Standard methods for Varroa research. J Apic Res 2013, 52(1): 1-54.10.3896/IBRA.1.52.1.09 Search in Google Scholar

84. Kefuss J, Taber S, Vanpoucke J, Rey F: A practical method to test for disease resistance in honey bees. Am Bee J 1996, 136: 31-32. Search in Google Scholar

85. De Miranda JR, Bailey L, Ball BV, Blanchard P, Budge GE, Chejanovsky N, Chen YP, Gauthier L, Genersch E, De Graaf DC, Ribiere M, Ryabov E, De Smet L, van der Steen JJM: Standard methods for virus research in Apis mellifera. J Apic Res 2013, 52(1): 1-36.10.3896/IBRA.1.52.4.22 Search in Google Scholar

86. Bailey L, Gibbs AJ: Acute infection of bees with paralysis virus. J Insect Pathol 1964, 6(4): 395-407. Search in Google Scholar

87. Bailey L, Ball BV: Honey Bee Pathology, second ed. Academic Press 1991, London.10.1016/B978-0-12-073481-8.50006-0 Search in Google Scholar

88. Fries I, Chauzat MP, Chen YP, Doublet V, Genersch E, Gisder S, Higes M, McMahon DP, Martín-Hernández R, Natsopoulou M, Paxton R, Tanner G, Webster TC, Williams GR: Standard methods for Nosema research. J Apic Res 2013, 52: 1-28.10.3896/IBRA.1.52.1.14 Search in Google Scholar

89. Botías C, Martín-Hernández R, Meana A, Higes M: Critical aspects of the Nosema spp. diagnostic sampling in honey bee (Apis mellifera L.) colonies. Parasitol Res 2012, 110(6): 2557-2561.10.1007/s00436-011-2760-222193523 Search in Google Scholar

90. 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(5): 522-536.10.1007/s13592-013-0203-z Search in Google Scholar

91. 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(1): 49-58.10.1051/apido/2010034 Search in Google Scholar

92. Cirkovic D, Stevanovic J, Glavinic U, Aleksic N, Djuric S, Aleksic J, Stanimirovic Z: Honey bee viruses in Serbian colonies of different strength. Peer J 2018, 6: p.e5887.10.7717/peerj.5887624034030479890 Search in Google Scholar

93. Antunez K, Martín-Hernández R, Prieto L, Meana A, Zunino P, Higes M: Immune-suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environ Microbiol 2009, 11(9): 2284–2290.10.1111/j.1462-2920.2009.01953.x19737304 Search in Google Scholar

94. Chaimanee V, Chantawannakul P, Chen Y, Evans JD, Pettis JS: Differential expression of immune genes of adult honey bee (Apis mellifera) after inoculated by Nosema ceranae. J Insect Physiol 2012, 58(8): 1090–1095.10.1016/j.jinsphys.2012.04.01622609362 Search in Google Scholar

95. Aufauvre J, Misme-Aucouturier B, Viguès B, Texier C, Delbac F, Blot N: Transcriptome analyses of the honeybee response to Nosema ceranae and insecticides. PLoS One 2014, 9(3): e91686.10.1371/journal.pone.0091686396015724646894 Search in Google Scholar

96. Badaoui B, Fougeroux A, Petit F, Anselmo A, Gorni C, Cucurachi M, Cersini A, Granato A, Cardeti G, Formato G, Mutinelli F: RNA-sequence analysis of gene expression from honeybees (Apis mellifera) infected with Nosema ceranae. PLoS One 2017, 12(3): e0173438.10.1371/journal.pone.0173438537010228350872 Search in Google Scholar

97. Dussaubat C, Brunet JL, Higes M, Colbourne JK, Lopez J, Choi JH, Martin-Hernandez R, Botias C, Cousin M, McDonnell C, Bonnet M: Gut pathology and responses to the microsporidium Nosema ceranae in the honey bee Apis mellifera. PLoS One 2012, 7(5): e37017.10.1371/journal.pone.0037017335640022623972 Search in Google Scholar

98. Kurze C, Le Conte Y, Dussaubat C, Erler S, Kryger P, Lewkowski O, Müller T, Widder M, Moritz RF: Nosema tolerant honeybees (Apis mellifera) escape parasitic manipulation of apoptosis. PLoS One 2015, 10, e0140174.10.1371/journal.pone.0140174459655426445372 Search in Google Scholar

99. Martín-Hernández R, Higes M, Sagastume S, Juarranz Á, Dias-Almeida J, Budge GE, Meana A, Boonham N: Microsporidia infection impacts the host cell’s cycle and reduces host cell apoptosis. PLoS One 2017, 12(2): e0170183.10.1371/journal.pone.0170183528943728152065 Search in Google Scholar

100. de Sousa RT, Darnell R, Wright GA. Behavioural regulation of mineral salt intake in honeybees: a self-selection approach. Philosophical Transactions of the Royal Society B., 2022, 377(1853): 20210169. Search in Google Scholar

101. Rajković M, Glavinić U, Ristanić M, Ćosić M, Dimitrijević-Srećković V, Ilić I, Đelić N: Does organic sprouted whole wheat grain flourless bread decreases DNA damage in diabetic patients?. Acta Vet-Beograd, 2021, 71(3): 273-284.10.2478/acve-2021-0024 Search in Google Scholar

102. Petrović S, Maletić M, Lakić N, Aleksić N, Maletić J, Ristanić M, Stanimirović Z: The effects of antioxidants provided with feed on certain quality parameters of bull semen under heat stress conditions. Acta Vet-Beograd 2021, 70(4): 453-470.10.2478/acve-2020-0034 Search in Google Scholar

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