1932

Abstract

Although nectar is consumed, primarily as a supplemental food, by a broad range of insects spanning at least five orders, it is processed and stored by only a small number of species, most of which are bees and wasps in the superfamily Apoidea. Within this group, has evolved remarkable adaptations facilitating nectar processing and storage; in doing so, this species utilizes the end product, honey, for diverse functions with few if any equivalents in other phytophagous insects. Honey and its phytochemical constituents, some of which likely derive from propolis, have functional significance in protecting honey bees against microbial pathogens, toxins, and cold stress, as well as in regulating development and adult longevity. The distinctive properties of honey appear to have arisen in multiple ways, including genome modification; partnerships with microbial symbionts; and evolution of specialized behaviors, including foraging for substances other than nectar. That honey making by involves incorporation of exogenous material other than nectar, as well as endogenous products such as antimicrobial peptides and royal jelly, suggests that regarding honey as little more than a source of carbohydrates for bees is a concept in need of revision.

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2021-01-07
2024-04-16
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Literature Cited

  1. 1. 
    Adler LS. 2000. The ecological significance of toxic nectar. Oikos 91:409–20
    [Google Scholar]
  2. 2. 
    Ahmed S, Sulaiman SA, Baig AA, Ibrahim M, Liaqat S et al. 2018. Honey as a potential natural antioxidant medicine: an insight into its molecular mechanisms of action. Oxid. Med. Cell. Longev. 2018:8367846
    [Google Scholar]
  3. 3. 
    Ajibola A, Chamunorwa JP, Erlwanger KH 2012. Nutraceutical values of natural honey and its contribution to human health and wealth. Nutr. Metab. 9:61
    [Google Scholar]
  4. 4. 
    Aliyazıcıoglu R, Sahin H, Erturk O, Ulusoy E, Kolayli S 2013. Properties of phenolic composition and biological activity of propolis from turkey. Int. J. Food Prop. 16:277–87
    [Google Scholar]
  5. 5. 
    Alonso-Torre SR, Cavia MM, Fernández-Muiño MA, Moreno G, Huidobro JF, Sancho MT 2006. Evolution of acid phosphatase activity of honeys from different climates. Food Chem 97:750–55
    [Google Scholar]
  6. 6. 
    Alqarni AS, Rushdi AI, Owayss AA, Raweh HS, El-Mubarak AH, Simoneit BRT 2015. Organic tracers from asphalt in propolis produced by urban honey bees, Apis mellifera Linn. PLOS ONE 10:6e0128311
    [Google Scholar]
  7. 7. 
    Amdam GV, Omholt SW. 2002. The regulatory anatomy of honeybee lifespan. J. Theor. Biol. 216:209–28
    [Google Scholar]
  8. 8. 
    Auzinger A. 1910. Über Fermente im Honig und den Wert ihres Nachweises für die Honigbeurteilung. Z. Unters. Nahr. Genußm. Gebrauchsgegenstände 19:65–83
    [Google Scholar]
  9. 9. 
    Avila S, Beux MR, Ribani RH, Zambizi RC 2018. Stingless bee honey: quality parameters, bioactive compounds, health-promotion properties and modification detection strategies. Trends Food Sci. Technol. 81:37–50
    [Google Scholar]
  10. 10. 
    Azzous-Olden F, Hunt A, DeGrandi-Hoffman G 2018. Transcriptional response of honey bee (Apis mellifera) to differential nutritional status and Nosema infection. BMC Genom 19:628
    [Google Scholar]
  11. 11. 
    Berenbaum MR, Johnson RM. 2015. Xenobiotic metabolism in honey bees. Curr. Opin. Insect Sci. 10:51–58
    [Google Scholar]
  12. 12. 
    Bernklau E, Bjostad L, Hogeboom A, Carlisle A, Arathi HS 2019. Dietary phytochemicals, honey bee longevity and pathogen tolerance. Insects 10:14–26
    [Google Scholar]
  13. 13. 
    Bijlsma L, De Bruijn LLM, Martens EP, Sommeijer MJ 2006. Water content of stingless bee honeys (Apidae. Meliponini): interspecfic variation and comparison with honey of Apis mellifera. Apidologie 37:480–86
    [Google Scholar]
  14. 14. 
    Bocian A, Buczkowicz J, Jaromin M, Hus KK, Legáth J 2019. An effective method of isolating honey proteins. Molecules 24:2399
    [Google Scholar]
  15. 15. 
    Borrell BJ. 2007. Scaling of nectar foraging in orchid bees. Am. Nat. 169:569–80
    [Google Scholar]
  16. 16. 
    Borutinskaite V, Treigyte G, Čeksteryte V, Kurtinaitiene B, Navakauskiene R 2018. Proteomic identification and enzymatic activity of buckwheat (Fagopyrum esculentum) honey based on different assays. J. Food Nutr. Res. 57:57–69
    [Google Scholar]
  17. 17. 
    Borutinskaitė V, Treigytė G, Matuzevičius D, Zaikova I, Čeksterytė V et al. 2017. Proteomic analysis of pollen and blossom honey from rape seed Brassica napus L. J. Apic. Sci. 61:73–92
    [Google Scholar]
  18. 18. 
    Brouwers EVM. 1982. Measurement of hypopharyngeal gland activity in the honeybee. J. Apic. Res. 21:193–98
    [Google Scholar]
  19. 19. 
    Brudzynski K, Sjaarda C. 2015. Honey glycoproteins containing antimicrobial peptides, jelleins of the major royal jelly protein 1, are responsible for the cell wall lytic and bactericidal activities of honey. PLOS ONE 10:e0120238
    [Google Scholar]
  20. 20. 
    Buawangpong N, Burgett M. 2019. Capped honey moisture content from four honey bee species; Apis dorsata F., Apis florea F.,. Apis cerana F., and Apis mellifera L. (Hymenoptera: Apidae) in northern Thailand. J. Apic 34:157–60
    [Google Scholar]
  21. 21. 
    Bucekova M, Valachova I, Kohutova L, Prochazka E, Klaudiny J, Majtan J 2014. Honeybee glucose oxidase—its expression in honeybee workers and comparative analyses of its content and H2O2-mediated antibacterial activity in natural honeys. Naturwissenschaften 101:661–70
    [Google Scholar]
  22. 22. 
    Bull E, Rapport L, Lockwood B 2000. What is a nutraceutical. The Pharmaceutical Journal Jul. 8. https://www.pharmaceutical-journal.com/1-what-is-a-nutraceutical/20002095.article?firstPass=false#Ref1
    [Google Scholar]
  23. 23. 
    Bull H, Murray PG, Thomas D, Fraser AM, Nelson PN 2002. Acid phosphatases. Mol. Pathol. 55:65–72
    [Google Scholar]
  24. 24. 
    Burgett DM. 1974. Glucose oxidase: a food protective mechanism in social Hymenoptera. Ann. Entomol. Soc. Am. 67:545–46
    [Google Scholar]
  25. 25. 
    Cane J, Harrison PA. 2011. Nectar and pollen sugars constituting larval provisions of the alfalfa leaf-cutting bee (Megachile rotundata) (Hymenoptera: Apiformes: Megachilidae). Apidologie 42:401–8
    [Google Scholar]
  26. 26. 
    Cardinal S, Danforth BN. 2013. Bees diversified in the age of eudicots. Proc. R. Soc. B 280:20122686
    [Google Scholar]
  27. 27. 
    Chanchao S, Pilalam CS, Sangvanich P 2008. Purification and characterization of α-glucosidase in Apis cerana indica. Insect Sci 15:217–24
    [Google Scholar]
  28. 28. 
    Chandrasekaran S, Nagendran A, Krishnankutty N, Pandiaraja D, Saravanan S, Balasubramanian K 2011. Disposed paper cups and declining bees. Curr. Sci. 101:1262
    [Google Scholar]
  29. 29. 
    Chauhan B, Kumar G, Kalam N, Ansari SH 2013. Current concepts and prospects of herbal nutraceutical: a review. J. Adv. Pharm. Technol. Res. 4:4–8
    [Google Scholar]
  30. 30. 
    Corby-Harris V, Jones BM, Walton A, Schwan MR, Anderson KE 2014. Transcriptional markers of sub-optimal nutrition in developing Apis mellifera nurse workers. BMC Genom 15:134
    [Google Scholar]
  31. 31. 
    Corona M, Hughes KA, Weaver DB, Robinson GE 2005. Gene expression patterns associated with queen honey bee longevity. Mech. Ageing Dev. 126:1230–38
    [Google Scholar]
  32. 32. 
    Corona M, Robinson GE. 2006. Genes of the antioxidant system of the honey bee: annotation and phylogeny. Insect Mol. Biol. 15:687–701
    [Google Scholar]
  33. 33. 
    Costa RAC, Cruz-Landim C. 2002. Enzymes in the hypopharyngeal gland extracts from workers of Scaptotrigona postica (Hymenoptera, Apinae, Meliponini) related to food storing in the colony. Sociobiology 40:413–20
    [Google Scholar]
  34. 34. 
    Couvillon MJ, Dornhaus A. 2009. Location, location, location: Larvae position inside the nest is correlated with adult body size in worker bumble-bees (Bombus impatiens). Proc. R. Soc. B 276:2411–18
    [Google Scholar]
  35. 35. 
    Crane E 1975. Honey: A Comprehensive Survey London: Heinemann
  36. 36. 
    Daimon T, Taguchi T, Meng Y, Katsuma S, Mita K, Shimada T 2008. β-fructofuranosidase genes of the silkworm, Bombyx mori: Insights into enzymatic adaptation of Β. mori to toxic alkaloids in mulberry latex. J. Biol. Chem. 283:15271–9
    [Google Scholar]
  37. 37. 
    Daliu P, Santini A, Novellino E 2018. A decade of nutraceutical patents: where are we now in 2018. Expert Opin. Ther. Patents 28:875–82
    [Google Scholar]
  38. 38. 
    Damiani N, Porrini MP, Lancia P, Alvarez E, Garrido PM et al. 2017. Effect of propolis oral intake on physiological condition of young worker honey bees, Apis mellifera L. J. Apic. Sci. 61:193–202
    [Google Scholar]
  39. 39. 
    De-Melo AAM, Almeida-Muradian LB, Sancho MT, Pascual-Maté A 2018. Composition and properties of Apis mellifera honey: a review. J. Apic. Res. 57:5–37
    [Google Scholar]
  40. 40. 
    de Sousa JMB, de Souza EL, Marques G, de Toledo Benassi M, Gullón B et al. 2016. Sugar profile, physicochemical and sensory aspects of monofloral honeys produced by different stingless bee species in Brazilian semi-arid region. LWT Food Sci. Technol. 65:645–51
    [Google Scholar]
  41. 41. 
    de Verges J, Nehring V 2016. A critical look at proximate causes of social insect senescence: damage accumulation or hyperfunction. Curr. Opin. Insect Sci. 16:69–75
    [Google Scholar]
  42. 42. 
    Di Girolamo F, D'Amato A, Righetti PG 2012. Assessment of the floral origin of honey via proteomic tools. J. Proteom. 75:3688–93
    [Google Scholar]
  43. 43. 
    Donaldson IA, Jørgensen JH. 1988. Barley powdery mildew “invertase” is an alpha-glucosidase. Carlsberg Res. Commun. 53:421
    [Google Scholar]
  44. 44. 
    Drescher N, Klein AM, Schmitt T, Leonhard SD 2018. A clue on bee glue: new insight into the sources and factors driving resin intake in honeybees (Apis mellifera). PLOS ONE 14:e0210594
    [Google Scholar]
  45. 45. 
    Elsik CG, Worley KC, Bennett AK, Beye M, Camara F et al. 2014. Finding the missing honey bee genes: lessons learned from a genome upgrade. BMC Genom 15:86–108
    [Google Scholar]
  46. 46. 
    Erban T, Shcherbachenko E, Talacko P, Harant K 2019. The unique protein composition of honey revealed by comprehensive proteomic analysis: allergens, venom-like proteins, antibacterial properties, royal jelly proteins, serine proteases, and their inhibitors. J. Nat. Prod. 82:1217–26
    [Google Scholar]
  47. 47. 
    Erler S, Moritz RFA. 2016. Pharmacophagy and pharmacophory: mechanisms of self-medication and disease prevention in the honeybee colony (Apis mellifera). Apidologie 47:389–411
    [Google Scholar]
  48. 48. 
    Ferri S, Kojima K, Sode K 2011. Review of glucose oxidases and glucose dehydrogenases: a bird's eye view of glucose sensing enzymes. J. Diabetes Sci. Technol. 5:1068–76
    [Google Scholar]
  49. 49. 
    Flanjak I, Strelec I, Kenjerić D, Primorac L 2016. Croatian produced unifloral honey characterized according to the protein and proline content and enzyme activities. J. Apic. Sci. 60:39–48
    [Google Scholar]
  50. 50. 
    Frankel S, Robinson GE, Berenbaum MR 1998. Antioxidant capacity and correlated characteristics of 14 unifloral honeys. J. Apic. Res. 37:27–31
    [Google Scholar]
  51. 51. 
    Gauhe A. 1940. Über ein glukoseoxydierendes Enzym in der Pharynxdrüse der Honigbiene. Z. Vgl. Physiol. 28:211–53
    [Google Scholar]
  52. 52. 
    Gherman BI, Denner A, Bobiş O, Dezmirean DS, Mărghitaş LA et al. 2014. Pathogen-associated self-medication in the honeybee Apis mellifera. Behav. Ecol. Sociobiol 68:1777–84
    [Google Scholar]
  53. 53. 
    Giannakou ME, Goss M, Jünger MA, Hafen E, Leevers SJ, Partridge L 2004. Long-lived Drosophila with overexpressed dFOXO in adult fat body. Science 305:361
    [Google Scholar]
  54. 54. 
    Gil MI, Ferreres F, Ortiz A, Subra E, Tomas-Barberan FA 1995. Plant phenolic metabolites and floral origin of rosemary honey. J. Agric. Food Chem. 34:2833–38
    [Google Scholar]
  55. 55. 
    Gilbert LE. 1972. Pollen feeding and reproductive biology of Heliconius butterflies. PNAS 69:1403–7
    [Google Scholar]
  56. 56. 
    Gillette CC. 1931. Honey catalase. J. Econ. Entomol. 24:605–6
    [Google Scholar]
  57. 57. 
    Giri K. 1938. The chemical composition and enzyme content of Indian honey. Madras Agric. J. 26:68–72
    [Google Scholar]
  58. 58. 
    Gismondi A, Di Marco G, Canini A 2017. Detection of plant microRNAs in honey. PLOS ONE 12:2e0172981
    [Google Scholar]
  59. 59. 
    Gloss AD, Abbot P, Whiteman NK 2019. How interactions with plant chemicals shape insect genomes. Curr. Opin. Insect Sci. 36:149–56
    [Google Scholar]
  60. 60. 
    González-Teuber M, Heil M. 2009. Nectar chemistry is tailored for both attraction of mutualists and protection from exploiters. Plant Signal. Behav. 4:809–13
    [Google Scholar]
  61. 61. 
    Good AP, Gauthier M-PL, Vannette RL, Fukami T 2014. Honey bees avoid nectar colonized by three bacterial species, but not by a yeast species, isolated from the bee gut. PLOS ONE 9:e86494
    [Google Scholar]
  62. 62. 
    Gothe F. 1914. Die fermente des honigs. Z. Unters. Nahr. Genußm. Gebrauchsgegenstände 28:273–86
    [Google Scholar]
  63. 63. 
    Haddad LS, Kelbert L, Hulbert AJ 2007. Extended longevity of queen honey bees compared to workers is associated with peroxidation-resistant membranes. Exp. Gerontol. 42:601–9
    [Google Scholar]
  64. 64. 
    Harpel D, Cullen DA, Ott SR, Jiggins CD, Walters JR 2015. Pollen feeding proteomics: salivary proteins of the passion flower butterfly. Heliconius melpomene. Insect Biochem. Mol. Biol. 63:7–13
    [Google Scholar]
  65. 65. 
    Harvey JA, Cloutier J, Visser B, Ellers J, Wäckers F, Gols R 2012. The effect of different dietary sugars and honey on longevity and fecundity in two hyperparasitoid wasps. J. Insect Physiol. 58:816–23
    [Google Scholar]
  66. 66. 
    Huidobro JF, Sánchez MP, Muniategui S, Sancho MT 2019. Precise method for the measurement of catalase activity in honey. J. AOAC Int. 88:800–4
    [Google Scholar]
  67. 67. 
    Jamaluddin MD. 2015. Advances in Food Processing and Preservation New Delhi: Anmol Publ.
  68. 68. 
    Johnson RM, Harpur BA, Dogantzis KA, Zayed A, Berenbaum MR 2018. Genomic footprint of evolution of eusociality in bees: floral food use and CYPome “blooms.”. Insectes Soc 65:445–54
    [Google Scholar]
  69. 69. 
    Johnson RM, Mao W, Pollock HS, Niu G, Schuler MA, Berenbaum MR 2012. Ecologically appropriate xenobiotics induce cytochrome P450s in Apis mellifera. PLOS ONE 7:2e31051
    [Google Scholar]
  70. 70. 
    Joshi SR, Pechhacker H, William A, Von Der Ohe W 2000. Physico-chemical characteristics of Apis dorsata, A. cerana and A. mellifera honey from Chitwan district, central Nepal. Apidologie 31:367–75
    [Google Scholar]
  71. 71. 
    Kapheim KM, Pan H, Li C, Salzberg SL, Puiu D et al. 2015. Genomic signatures of evolutionary transitions from solitary to group living. Science 348:1139–43
    [Google Scholar]
  72. 72. 
    Kaškonienė V, Venskutonis PR. 2010. Floral markers in honey of various botanical and geographic origins: a review. Compr. Rev. Food Sci. Saf. 9:620–34
    [Google Scholar]
  73. 73. 
    Keeling CI, Yuen MM, Liao NY, Docking TR, Chan SK et al. 2013. Draft genome of the mountain pine beetle, Dendroctonus ponderosae Hopkins, a major forest pest. Genome Biol 14:R27
    [Google Scholar]
  74. 74. 
    Kevan PG, Eisikowitch D, Fowle S, Thomas K 1988. Yeast-contaminated nectar and its effects on bee foraging. J. Apic. Res. 27:26–29
    [Google Scholar]
  75. 75. 
    Khalifa SAM, Elashal M, Kielszek M, Ghazala NE, Farag MA et al. 2020. Recent insights into chemical and pharmacological studies of bee bread. Trends Food Sci. Technol. 97:300–16
    [Google Scholar]
  76. 76. 
    Kubo T, Sasaki M, Nakamura J, Sasagawa H, Ohashi K et al. 1996. Change in the expression of hypopharyngeal-gland proteins of the worker honeybees (Apis mellifera) with age and/or role. J. Biochem. 119:291–95
    [Google Scholar]
  77. 77. 
    Kubota M, Tsuji M, Nishimoto M, Wongchawalit J, Okuyama M et al. 2004. Localization of α-glucosidases I, II, and III in organs of European honeybees, Apis mellifera L., and the origin of α-glucosidase in honey. Biosci. Biotechnol. Biochem. 68:2346–52
    [Google Scholar]
  78. 78. 
    Kumar S, Narwal S, Kumar V, Prakash O 2011. α-Glucosidase inhibitors from plants: a natural approach to treat diabetes. Pharmacogn. Rev. 5:19–29
    [Google Scholar]
  79. 79. 
    Kunieda T, Fujiyuki T, Kucharski R, Foret S, Ament SA et al. 2006. Carbohydrate metabolism genes and pathways in insects: insights from the honey bee genome. Insect Mol. Biol. 15:563–76
    [Google Scholar]
  80. 80. 
    Lashmanova E, Zemskaya N, Proshkina E, Kudryavtseva A, Volosnikova M et al. 2017. The evaluation of geroprotective effects of selected flavonoids in Drosophila melanogaster and Caenorhabditis elegans. Front. Pharmacol 8:884
    [Google Scholar]
  81. 81. 
    Leonov A, Arlia-Ciommo A, Piano A, Svistkova V, Lutchman V et al. 2015. Longevity extension by phytochemicals. Molecules 20:6544–72
    [Google Scholar]
  82. 82. 
    Lewkowski O, Mureşan CI, Dobritzsch D, Fuszard M, Erler S 2019. The effect of diet on the composition and stability of proteins secreted by honey bees in honey. Insects 10:282–92
    [Google Scholar]
  83. 83. 
    Li K, Yao F, Xue Q, Fan H, Yang L et al. 2018. Inhibitory effects against α-glucosidase and α-amylase of the flavonoids-rich extract from Scutellaria baicalensis shoots and interpretation of structure–activity relationship of its eight flavonoids by a refined assign-score method. Chem. Cent. J. 12:82
    [Google Scholar]
  84. 84. 
    Liao LH, Wu WY, Berenbaum MR 2017. Impacts of dietary phytochemicals in the presence and absence of pesticides on longevity of honey bees (Apis mellifera). Insects 8:22–35
    [Google Scholar]
  85. 85. 
    Linley E, Denyer SP, McDonnell G, Simons C, Maillard J-Y 2012. Use of hydrogen peroxide as a biocide: new consideration of its mechanisms of biocidal action. J. Antimicrob. Chemother. 67:1589–96
    [Google Scholar]
  86. 86. 
    Liu F, He J, Fu W 2005. Highly controlled nest homeostasis of honey bees helps deactivate phenolics in nectar. Naturwissenschaften 92:297–99
    [Google Scholar]
  87. 87. 
    Ma J-N, Ma C-M. 2015. Antifungal inhibitory activities of caffeic and quinic acid derivatives. Coffee in Health and Disease Prevention VR Preedy 635–41 Amsterdam: Elsevier
    [Google Scholar]
  88. 88. 
    Mani R, Natesan V. 2018. Chrysin: sources, beneficial pharmacological activities and molecular mechanisms of action. Phytochemistry 143:187–96
    [Google Scholar]
  89. 89. 
    Manjon C, Troczka BJ, Zaworra M, Beadle K, Randall E et al. 2018. Unravelling the molecular determinants of bee sensitivity to neonicotinoid insecticides. Curr. Biol. 28:1137–43.e5
    [Google Scholar]
  90. 90. 
    Mao W, Rupasinghe SG, Johnson RM, Zangerl AR, Schuler MA, Berenbaum MR 2009. Quercetin-metabolizing CYP6AS enzymes of the pollinator Apis mellifera (Hymenoptera: Apidae). Comp. Biochem. Physiol. B 154:427–34
    [Google Scholar]
  91. 91. 
    Mao W, Schuler MA, Berenbaum MR 2011. CYP9Q-mediated detoxification of acaricides in the honey bee (Apis mellifera). PNAS 31:12657–62
    [Google Scholar]
  92. 92. 
    Mao W, Schuler MA, Berenbaum MR 2013. Honey constituents upregulate detoxification and immunity genes in the western honey bee Apis mellifera. PNAS 110:8842–46
    [Google Scholar]
  93. 93. 
    Mao W, Schuler MA, Berenbaum MR 2015. A dietary phytochemical alters caste-associated gene expression in honey bees. Sci. Adv. 1:e1500795
    [Google Scholar]
  94. 94. 
    Mao W, Schuler MA, Berenbaum MR 2017. Disruption of quercetin metabolism by fungicide affects energy production in honey bees (Apis mellifera). PNAS 114:2538–43
    [Google Scholar]
  95. 95. 
    Mavric E, Wittmann S, Barth G, Henle T 2008. Identification and quantification of methylglyoxal as the dominant antibacterial constituent of Manuka (Leptospermum scoparium) honeys from New Zealand. Mol. Nutr. Food Res. 52:483–89
    [Google Scholar]
  96. 96. 
    McMenamin AJ, Brutscher LM, Glenny W, Flenniken ML 2016. Abiotic and biotic factors affecting the replication and pathogenicity of bee viruses. Curr. Opin. Insect Sci. 16:14–21
    [Google Scholar]
  97. 97. 
    Mitton GA, Szawarski N, Mitton FM, Iglesias A, Eguaras MJ et al. 2020. Impacts of dietary supplementation with p-coumaric acid and indole-3-acetic acid on survival and biochemical response of honey bees treated with tau-fluvalinate. Ecotox. Environ. Saf. 189:109917
    [Google Scholar]
  98. 98. 
    Mo Y, Nagel C, Taylor LP 1992. Biochemical complementation of chalcone synthase mutants defines a role for flavonols in functional pollen. PNAS 89:7213–17
    [Google Scholar]
  99. 99. 
    Na Ayutthaya PP, Chanchao C, Chunsrivirot S 2018. Insight into the substrate specificity change caused by the Y227H mutation of α-glucosidase III from the European honeybee (Apis mellifera) through molecular dynamics simulations. PLOS ONE 13:e0198484
    [Google Scholar]
  100. 100. 
    Nafea EA, Nehad MG, Enas ND, Hajar AS 2014. Physiochemical and antimicrobial properties of four Egyptian honeys with references to American foul Brood disease. Life Sci. J. 11:10s40–46
    [Google Scholar]
  101. 101. 
    Natl. Acad. Sci. 2007. Status of Pollinators in North America Washington, DC: Natl. Acad. Sci.
  102. 102. 
    Negri P, Maggi MD, Ramirez L, de Feudis L, Szawarski N et al. 2015. Abscisic acid enhances the immune response in Apis mellifera and contributes to the colony fitness. Apidologie 46:542–57
    [Google Scholar]
  103. 103. 
    Negri P, Ramirez L, Quintana S, Szawarski N, Maggi M et al. 2020. Immune-related gene expression of Apis mellifera larvae in response to cold stress and abscisic acid (ABA) dietary supplementation. J. Apic. Res. 59:669–76
    [Google Scholar]
  104. 104. 
    Negri P, Villalobos E, Szawarski N, Damiani N, Gende L et al. 2019. Towards precision nutrition: a novel concept linking phytochemicals, immune response and honey bee health. Insects 10:401–30
    [Google Scholar]
  105. 105. 
    Nepi M, Grasso DA, Mancuso S 2018. Nectar in plant-insect mutualistic relationships: from food reward to partner manipulation. Front. Plant Sci. 9:1063–79
    [Google Scholar]
  106. 106. 
    Nicolson SW. 2011. Bee food: the chemistry and nutritional value of nectar, pollen and mixtures of the two. Afr. Zool. 46:197–204
    [Google Scholar]
  107. 107. 
    Nicolson SW, Human H. 2008. Bees get a head start on honey production. Biol. Lett. 4:299–301
    [Google Scholar]
  108. 108. 
    Nicolson SW, Thornburg RW. 2007. Nectar chemistry. Nectaries and Nectar S Nicolson, M Nepi, E Pacini 215–63 Berlin: Springer
    [Google Scholar]
  109. 109. 
    Niu G, Johnson RM, Berenbaum MR 2011. Toxicity of mycotoxins to honeybees and its amelioration by propolis. Apidologie 42:79–87
    [Google Scholar]
  110. 110. 
    Nolan VC, Harrison J, Cox AGC 2019. Dissecting the antimicrobial composition of honey. Antibiotics 8:251
    [Google Scholar]
  111. 111. 
    Ohashi K, Natori S, Kubo T 1999. Expression of amylase and glucose oxidase in the hypopharyngeal gland with an age-dependent role change of the worker honeybee (Apis mellifera L.). Eur. J. Biochem. 265:127–33
    [Google Scholar]
  112. 112. 
    Ohashi K, Sawata M, Takeuchi H, Natori S, Kubo T 1996. Molecular cloning of cDNA and analysis of expression of the gene for α-glucosidase from the hypopharyngeal gland of the honeybee Apis mellifera L. Biochem. Biophys. Res. Commun. 221:380–85
    [Google Scholar]
  113. 113. 
    Ostwald MM, Smith ML, Seeley TD 2016. The behavioral regulation of thirst, water collection and water storage in honey bee colonies. J. Exp. Biol. 219:2156–65
    [Google Scholar]
  114. 114. 
    Othman Z, Zakaria R, Hussain NHN, Hassan A, Shafin N et al. 2015. Potential role of honey in learning and memory. Med. Sci. 3:3–15
    [Google Scholar]
  115. 115. 
    Palmer-Young EC, Farrell IW, Adler LS, Milano NJ, Egan PA et al. 2019. Chemistry of floral rewards: intra- and interspecific variability of nectar and pollen secondary metabolites across taxa. Ecol. Monogr. 89:e01335
    [Google Scholar]
  116. 116. 
    Palmer-Young EC, Tozkar , Schwarz RS, Chen Y, Irwin RE et al. 2017. Nectar and pollen phytochemicals stimulate honey bee (Hymenoptera: Apidae) immunity to viral infection. J. Econ. Entomol. 110:1959–72
    [Google Scholar]
  117. 117. 
    Pasini F, Gardini S, Marcazzan GL, Caboni MF 2013. Buckwheat honeys: screening of composition and properties. Food Chem 141:2802–11
    [Google Scholar]
  118. 118. 
    Pattrick JG, Symington HA, Federle W, Glover BJ 2020. The mechanics of nectar offloading in the bumblebee Bombus terrestris and implications for optimal concentrations during nectar foraging. J. R. Soc. Interface 17:20190632
    [Google Scholar]
  119. 119. 
    Pauchet Y, Wilkinson P, Vogel H, Nelson DR, Reynolds SE et al. 2010. Pyrosequencing the Manduca sexta larval midgut transcriptome: messages for digestion, detoxification and defence. Insect Mol. Biol. 19:61–75
    [Google Scholar]
  120. 120. 
    Pemberton RW, Wheeler GS. 2006. Orchid bees don't need orchids: evidence from the naturalization of an orchid bee in Florida. Ecology 87:1995–2001
    [Google Scholar]
  121. 121. 
    Penick CA, Crofton CA, Appler RH, Frank SD, Dunn RR, Tarpy DR 2016. The contribution of human foods to honey bee diets in a mid-sized metropolis. J. Urban Ecol. 2:juw001
    [Google Scholar]
  122. 122. 
    Proença C, Freitas M, Ribeiro D, Oliveira EFT, Sousa JLC et al. 2017. α-Glucosidase inhibition by flavonoids: an in vitro and in silico structure–activity relationship study. J. Enzyme Inhib. Med. Chem. 32:1216–28
    [Google Scholar]
  123. 123. 
    Pyrzynska K, Biesaga M. 2009. Analysis of phenolic acids and flavonoids in honey. Trends Anal. Chem. 28:894–902
    [Google Scholar]
  124. 124. 
    Ramirez L, Negri P, Sturla L, Guida L, Vigliarolo T et al. 2017. Abscisic acid enhances cold tolerance in honeybee larvae. Proc. R. Soc. B 284:185220162140
    [Google Scholar]
  125. 125. 
    Root AI. 1888. The ABC & XYZ of Bee Culture: An Encyclopedia Pertaining to the Scientific and Practical Culture of Honey Bees Medina, OH: A.I. Root Comp.
  126. 126. 
    Rossano R, Larocca M, Polito T, Perna AM, Padula MC et al. 2012. What are the proteolytic enzymes of honey and what they do tell us? A fingerprint analysis by 2-D zymography of unifloral honeys. PLOS ONE 7:e49164
    [Google Scholar]
  127. 127. 
    Rueppell O, Christine S, Mulcrone C, Groves L 2007. Aging without functional senescence in honey bee workers. Curr. Biol. 17:R274–75
    [Google Scholar]
  128. 128. 
    Ruiz-Argueso T, Rodrıguez-Navarro A. 1973. Gluconic acid-producing bacteria from honey bees and ripening honeys. J. Gen. Microbiol. 76:211–16
    [Google Scholar]
  129. 129. 
    Sabatier S, Amiot MJ, Tacchini M, Aubert S 1992. Identification of flavonoids in sunflower honey. J. Food Sci. 57:773–74
    [Google Scholar]
  130. 130. 
    Samarghandian S, Farkhondeh T, Samini F 2017. Honey and health: a review of recent clinical research. Pharmacogn. Res. 9:121–27
    [Google Scholar]
  131. 131. 
    Sann M, Niehuis O, Peters RS, Mayer C, Kozlov A et al. 2018. Phylogenomic analysis of Apoidea sheds new light on the sister group of bees. BMC Evol. Biol. 18:71
    [Google Scholar]
  132. 132. 
    Santos LM, Fonseca MS, Sokolonski AR, Deegan KR, Araujo RPC et al. 2019. Propolis: types, composition, biological activities, and veterinary product patent prospecting. J. Sci. Food. Agr. 100:1369–82
    [Google Scholar]
  133. 133. 
    Santos-Buelga C, Gonzalez-Paramas AM. 2017. Chemical composition of honey. Bee Products—Chemical and Biological Properties JM Alvarez-Suarez43–82 Berlin: Springer
    [Google Scholar]
  134. 134. 
    Sato T, Miyata G. 2000. The nutraceutical benefit, part III: honey. Nutrition 16:468–69
    [Google Scholar]
  135. 135. 
    Schepartz AI, Subers MH. 1966. Catalase in honey. J. Apic. Res. 5:37–43
    [Google Scholar]
  136. 136. 
    Schmidt JO, Thoenes SC, Levin MD 1987. Survival of honey bees, Apis mellifera (Hymenoptera: Apidae), fed various pollen sources. Ann. Entomol. Soc. Am. 80:176–83
    [Google Scholar]
  137. 137. 
    Shelomi M, Jasper WC, Atallah J, Kimsey LS, Johnson BR 2014. Differential expression of endogenous plant cell wall degrading enzyme genes in the stick insect (Phasmatodea) midgut. BMC Genom 15:917
    [Google Scholar]
  138. 138. 
    Simone-Finstrom M, Borba RS, Wilson M, Spivak M 2017. Propolis counteracts some threats to honey bee health. Insects 8:46–66
    [Google Scholar]
  139. 139. 
    Simpson J, Riedel IBM, Wilding N 1968. Invertase in the hypopharyngeal glands of the honeybee. J. Apic. Res. 7:29–36
    [Google Scholar]
  140. 140. 
    Sommeijer MJ, Rooijakkers EF, Jacobusse C, Kerkvliet JD 2009. Larval food composition and food plants of the solitary bee Colletes halophilus (Hymenoptera: Colletidae. J. Apic. Res. 48:149–55
    [Google Scholar]
  141. 141. 
    Spivak M, Goblirsch M, Simone-Finstrom M 2019. Social-medication in bees: the line between individual and social regulation. Curr. Opin. Insect Sci. 33:49–55
    [Google Scholar]
  142. 142. 
    Stamatakis A. 2014. RaxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–13
    [Google Scholar]
  143. 143. 
    Stevenson PC, Nicolson SW, Wright GA 2017. Plant secondary metabolites in nectar: impacts on pollinators and ecological functions. Funct. Ecol. 31:65–75
    [Google Scholar]
  144. 144. 
    Szweda P. 2017. Antimicrobial activity of honey. Honey Analysis V De Alencar Arnaut De Toledo, ch. 67117 London: InTech Open
    [Google Scholar]
  145. 145. 
    Terra WR, Barroso IG, Dias RO, Ferreira C 2019. Molecular physiology of insect midgut. Adv. Insect Physiol. 56:118–54
    [Google Scholar]
  146. 146. 
    Tomas-Barberan FA, Ferreres F, Garcia-Vignera C, Tomas-Lorente F 1993. Flavonoids in honey of different geographical origin. Z. Lebensm. Unters. Forsch. 196:38–44
    [Google Scholar]
  147. 147. 
    Vannette RL, Mohamed A, Johnson BR 2015. Forager bees (Apis mellifera) highly express immune and detoxification genes in tissues associated with nectar processing. Sci. Rep. 5:16224
    [Google Scholar]
  148. 148. 
    Wang C, Li S. 2015. Functional foods and nutraceuticals: potential role in human health. Clinical Aspects of Functional Foods and Nutraceuticals D Ghosh, D Debasis Bagchi, T Konishi 51–72 Boca Raton, FL: CRC Press
    [Google Scholar]
  149. 149. 
    Weston RJ. 2000. The contribution of catalase and other natural products to the antibacterial activity of honey: a review. Food Chem 71:235–39
    [Google Scholar]
  150. 150. 
    Wheeler MM, Robinson GE. 2014. Diet-dependent gene expression in honey bees: honey versus sucrose or high fructose corn syrup. Sci. Rep. 4:5726
    [Google Scholar]
  151. 151. 
    White JW Jr 1975. Composition of honey. See Reference 35 157–206
    [Google Scholar]
  152. 152. 
    White JW Jr., Subers MH, Schepartz AI. 1963. The identification of inhibine, the antibacterial factor in honey, as hydrogen peroxide and its origin in a honey glucose-oxidase system. Biochim. Biophys. Acta 73:57–70
    [Google Scholar]
  153. 153. 
    Willmer P. 2011. Pollination and Floral Ecology Princeton, NJ: Princeton Univ. Press
  154. 154. 
    Winston ML. 1987. The Biology of the Honey Bee Cambridge, MA: Harvard Univ. Press
  155. 155. 
    Wollstonecroft MM. 2011. Investigating the role of food processing in human evolution: a niche construction approach. Archaeol. Anthropol. Sci. 3:141–50
    [Google Scholar]
  156. 156. 
    Wong MJ, Liao LH, Berenbaum MR 2018. Biphasic concentration-dependent interaction between imidacloprid and dietary phytochemicals in honey bees (Apis mellifera). PLOS ONE 13:e0206625
    [Google Scholar]
  157. 157. 
    Wright GA, Baker DD, Palmer MJ, Stabler D, Mustard JA et al. 2013. Caffeine in floral nectar enhances a pollinator's memory of reward. Science 339:1202–4
    [Google Scholar]
  158. 158. 
    Yaacob M, Rajab NF, Shahar S, Sharif R 2018. Stingless bee honey and its potential value: a systematic review. Food Res 2:124–33
    [Google Scholar]
  159. 159. 
    Zhang H, Wang G, Beta T, Dong J 2015. Inhibitory properties of aqueous ethanol extracts of propolis on alpha-glucosidase. Evid.-Based Complement. Alternat. Med. 2015:587383
    [Google Scholar]
  160. 160. 
    Zhao C, Doucet D, Mittapalli O 2014. Characterization of horizontally transferred β-fructofuranosidase (ScrB) genes in Agrilus planipennis. Insect Mol. Biol 23:821–32
    [Google Scholar]
  161. 161. 
    Zhu K, Liu M, Fu Z, Zhou Z, Kong Y et al. 2017. Plant microRNAs in larval food regulate honeybee caste development. PLOS Genet 13:8e1006946
    [Google Scholar]
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