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Annual Review of Entomology

Volume 63, 2018

Nutritional Physiology and Ecology of Honey Bees

Abstract

Honey bees feed on floral nectar and pollen that they store in their colonies as honey and bee bread. Social division of labor enables the collection of stores of food that are consumed by within-hive bees that convert stored pollen and honey into royal jelly. Royal jelly and other glandular secretions are the primary food of growing larvae and of the queen but are also fed to other colony members. Research clearly shows that bees regulate their intake, like other animals, around specific proportions of macronutrients. This form of regulation is done as individuals and at the colony level by foragers.

Keyword(s): Apis mellifera, honey bee, nectar, nutrition, pollen, royal jelly
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2018-01-07
2024-04-18
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Literature Cited

  1. Afik O, Dag A, Kerem Z, Shafir S. 1.  2006. Analyses of avocado (Persea americana) nectar properties and their perception by honey bees (Apis mellifera). J. Chem. Ecol. 32:1949–63 [Google Scholar]
  2. Afik O, Shafir S. 2.  2007. Effect of ambient temperature on crop loading in the honey bee, Apis mellifera (Hymenoptera: Apidae). Entomol. Gen. 29:135–48 [Google Scholar]
  3. Alaux C, Ducloz F, Crauser D, Le Conte Y. 3.  2010. Diet effects on honeybee immunocompetence. Biol. Lett. 6:562–65 [Google Scholar]
  4. Albert Š, Spaethe J, Grübel K, Rössler W. 4.  2014. Royal jelly-like protein localization reveals differences in hypopharyngeal glands buildup and conserved expression pattern in brains of bumblebees and honeybees. Biol. Open 3:281–88 [Google Scholar]
  5. Altaye SZ, Pirk CWW, Crewe RM, Nicolson SW. 5.  2010. Convergence of carbohydrate-biased intake targets in caged worker honeybees fed different protein sources. J. Exp. Biol. 213:3311–18 [Google Scholar]
  6. Anderson KE, Carroll MJ, Seehan T, Mott BM, Maes P, Corby-Harris V. 6.  2014. Hive-stored pollen of honey bees: Many lines of evidence are consistent with pollen preservation, not nutrient conversion. Mol. Ecol. 23:5904–17 [Google Scholar]
  7. Archer CR, Kohler A, Pirk CWW, Oosthuizen V, Apostolides Z, Nicolson SW. 7.  2014. Antioxidant supplementation can reduce the survival costs of excess amino acid intake in honeybees. J. Insect Physiol. 71:78–86 [Google Scholar]
  8. Archer CR, Pirk CWW, Wright GA, Nicolson SW. 8.  2014. Nutrition affects survival in African honeybees exposed to interacting stressors. Funct. Ecol. 28:913–23 [Google Scholar]
  9. Arganda S, Bouchebti S, Bazazi1 S, Le Hesran S, Puga C. 9.  et al. 2017. Parsing the life-shortening effects of dietary protein: effects of individual amino acids. Proc. R. Soc. B 284:20162052 [Google Scholar]
  10. Arien Y, Dag A, Zarchin S, Masci T, Shafir S. 10.  2015. Omega-3 deficiency impairs honey bee learning. PNAS 112:15761–66 [Google Scholar]
  11. Asencot M, Lansky Y. 11.  1988. The effect of soluble sugars in stored royal jelly on the differentiation of female honeybee (Apis mellifera L.) larvae to queens. Insect Biochem 18:127–33 [Google Scholar]
  12. Avni D, Dag A, Shafir S. 12.  2009. Pollen sources for honey bees in Israel: source, periods of shortage and influence on population growth. Isr. J. Plant Sci. 57:263–75 [Google Scholar]
  13. Avni D, Hendriksma HP, Dag A, Uni Z, Shafir S. 13.  2014. Nutritional aspects of honey bee-collected pollen and constraints on colony development in the eastern Mediterranean. J. Insect Physiol. 69:65–73 [Google Scholar]
  14. Babendreier D, Kalberer N, Romeis J, Fluri P, Bigler F. 14.  2004. Pollen consumption in honey bee larvae: a step forward in the risk assessment of transgenic plants. Apidologie 35:293–300 [Google Scholar]
  15. Behmer ST. 15.  2009. Insect herbivore nutrient regulation. Annu. Rev. Entomol. 54:165–87 [Google Scholar]
  16. Billiet A, Meeus I, Van Nieuwerburgh F, Deforce D, Wackers F, Smagghe G. 16.  2017. Colony contact contributes to the diversity of gut bacteria in bumblebees (Bombus terrestris). Insect Sci 24:270–77 [Google Scholar]
  17. Black J. 17.  2006. Honeybee Nutrition: Review of Research and Practices RIRDC Publ. 06/052, Proj. JLB-2A Rural Industries Research and Development Corporation Canberra, Aust.:
  18. Bogdanov S, Ruoff K, Persano Oddo L. 18.  2004. Physico-chemical methods for the characterisation of unifloral honeys: a review. Apidologie 35:S4–17 [Google Scholar]
  19. Bonvehi JS, Jorda RE. 19.  1997. Nutrient composition and microbiological quality of honeybee-collected pollen in Spain. J. Agric. Food Chem. 45:725–32 [Google Scholar]
  20. Brodschneider R, Crailsheim K. 20.  2010. Nutrition and health in honey bees. Apidologie 41:278–94 [Google Scholar]
  21. Buttstedt A, Ihling CH, Pietzsch M, Moritz RFA. 21.  2016. Royalactin is not a royal making of a queen. Nature 537:E10–12 [Google Scholar]
  22. Buttstedt A, Moritz RFA, Erler S. 22.  2014. Origin and function of the major royal jelly proteins of the honeybee (Apis mellifera) as members of the yellow gene family. Biol. Rev. 89:255–69 [Google Scholar]
  23. Camazine S. 23.  1991. Self-organizing pattern-formation on the combs of honey bee colonies. Behav. Ecol. Sociobiol. 28:61–76 [Google Scholar]
  24. Carroll MJ, Brown N, Goodall C, Downs AM, Sheenan TH, Anderson KE. 24.  2017. Honey bees preferentially consume freshly-stored pollen. PLOS ONE 12:e0175933 [Google Scholar]
  25. Ciulu M, Floris I, Nurchi VM, Panzanelli A, Pilo MI. 25.  et al. 2013. HPLC determination of pantothenic acid in royal jelly. Anal. Methods 5:6682–85 [Google Scholar]
  26. Crailsheim K. 26.  1986. Dependence of protein-metabolism on age and season in the honeybee (Apis mellifica carnica Pollm). J. Insect Physiol. 32:629–34 [Google Scholar]
  27. Crailsheim K. 27.  1990. The protein balance of the honey bee worker. Apidologie 21:417–29 [Google Scholar]
  28. Crailsheim K. 28.  1992. The flow of jelly within a honeybee colony. J. Comp. Physiol. B 162:681–89 [Google Scholar]
  29. Crailsheim K, Schneider LHW, Hrassnigg N, Bühlmann G, Brosch U. 29.  et al. 1992. Pollen consumption and utilization in worker honeybees: dependence on individual age and function. J. Insect Physiol. 38:409–19 [Google Scholar]
  30. Cremonez TM, De Jong D, Bitondi MMG. 30.  1998. Quantification of hemolymph proteins as a fast method for testing protein diets for honey bees (Hymenoptera: Apidae). J. Econ. Entomol. 91:1284–89 [Google Scholar]
  31. Day S, Beyer R, Mercer A, Ogden S. 31.  1990. The nutrient composition of honeybee-collected pollen in Otago, New Zealand. J. Apic. Res. 29:138–46 [Google Scholar]
  32. de Groot AP. 32.  1953. Protein and amino acid requirements of the honey bee (Apis mellifica L.). Physiol. Comp. Oecologia 3:1–83 [Google Scholar]
  33. DeGrandi-Hoffman G, Chen YP, Rivera R, Carroll M, Chambers M. 33.  et al. 2016. Honey bee colonies provided with natural forage have lower pathogen loads and higher overwinter survival than those fed protein supplements. Apidologie 47:186–96 [Google Scholar]
  34. Démares FJ, Crous KL, Pirk CWW, Nicolson SW, Human H. 34.  2016. Sucrose sensitivity of honey bees is differently affected by dietary protein and a neonicotinoid pesticide. PLOS ONE 11:6e0156584 [Google Scholar]
  35. Detzel A, Wink M. 35.  1993. Attraction, deterrence or intoxication of bees (Apis mellifera) by plant allelochemicals. Chemoecology 4:8–18 [Google Scholar]
  36. Di Pasquale G, Salignon M, Le Conte Y, Belzunces LP, Decourtye A. 36.  et al. 2013. Influence of pollen nutrition on honey bee health: Do pollen quality and diversity matter?. PLOS ONE 8:e72016 [Google Scholar]
  37. Dietz A, Haydak MH. 37.  1971. Caste determination in honey bees. I. The significance of moisture in larval food. J. Exp. Zool. 177:353–58 [Google Scholar]
  38. Dobson HEM. 38.  1988. Survey of pollen and pollenkitt lipids—chemical cues to flower visitors?. Am. J. Bot. 75:170–82 [Google Scholar]
  39. Doner L. 39.  1977. The sugars of honey—a review. J. Sci. Food Agric. 28:443–56 [Google Scholar]
  40. Donkersley P, Rhodes G, Pickup RW, Jones KC, Wilson K. 40.  2014. Honeybee nutrition is linked to landscape composition. Ecol. Evol. 4:4195–206 [Google Scholar]
  41. Drezner-Levy T, Smith BH, Shafir S. 41.  2009. The effect of foraging specialization on various learning tasks in the honey bee (Apis mellifera). Behav. Ecol. Sociobiol. 64:135–48 [Google Scholar]
  42. Eyer M, Neumann P, Dietemann V. 42.  2016. A look into the cell: honey storage in honey bees. Apis mellifera. PLOS ONE 11:8e0161059 [Google Scholar]
  43. Ferioli F, Armaforte E, Caboni MF. 43.  2014. Comparison of the lipid content, fatty acid profile and sterol composition in local Italian and commercial royal jelly samples. J. Am. Oil Chem. Soc. 91:875–84 [Google Scholar]
  44. Fewell JH, Winston ML. 44.  1992. Colony state and regulation of pollen foraging in the honey bee, Apismellifera L. Behav. Ecol. Sociobiol. 30:387–93 [Google Scholar]
  45. Fischer MK, Shingleton AW. 45.  2001. Host plant and ants influence the honeydew sugar composition of aphids. Funct. Ecol. 15:544–50 [Google Scholar]
  46. Free JB. 46.  1963. The floral constancy of honeybees. J. Anim. Ecol. 32:119–32 [Google Scholar]
  47. Garcia-Amoedo LH, de Almeida-Muradian LB. 47.  2007. Physicochemical composition of pure and adulterated royal jelly. Quim. Nova 30:257–59 [Google Scholar]
  48. Gardener MC, Gillman MP. 48.  2001. Analyzing variability in nectar amino acids: Composition is less variable than concentration. J. Chem. Ecol. 27:2545–58 [Google Scholar]
  49. Gardener MC, Gillman MP. 49.  2002. The taste of nectar—a neglected area of pollination ecology. Oikos 98:552–57 [Google Scholar]
  50. Gilliam M. 50.  1997. Identification and roles of non-pathogenic microflora associated with honey bees. FEMS Microbiol. Lett. 155:1–10 [Google Scholar]
  51. Gmeinbauer R, Crailsheim K. 51.  1993. Glucose utilization during flight of honeybee (Apis mellifera) workers, drones and queens. J. Insect Physiol. 39:959–67 [Google Scholar]
  52. Goulson D. 52.  2003. Bumblebees: Their Behaviour and Ecology Oxford, UK: Oxford Univ. Press
  53. Gruter C, Ratnieks FLW. 53.  2011. Flower constancy in insect pollinators—adaptive foraging behavior or cognitive limitation?. Commun. Integr. Biol. 4:633–36 [Google Scholar]
  54. Guler A, Bakan A, Nisbet C, Yavuz O. 54.  2007. Determination of important biochemical properties of honey to discriminate pure and adulterated honey with sucrose (Saccharum officinarum L.) syrup. Food Chem 105:1119–25 [Google Scholar]
  55. Haydak MH. 55.  1943. Larval food and development of castes in the honeybee. J. Econ. Entomol. 36:778–92 [Google Scholar]
  56. Haydak MH. 56.  1970. Honey bee nutrition. Annu. Rev. Entomol. 15:143–56 [Google Scholar]
  57. Hendriksma HP, Oxman KL, Shafir S. 57.  2014. Amino acid and carbohydrate tradeoffs by honey bee nectar foragers and their implications for plant-pollinator interactions. J. Insect Physiol. 69:56–64 [Google Scholar]
  58. Hendriksma HP, Shafir S. 58.  2016. Honey bee foragers balance colony nutritional deficiencies. Behav. Ecol. Sociobiol. 70:509–17 [Google Scholar]
  59. Herbert EW, Shimanuki H. 59.  1978. Chemical composition and nutritive value of bee-collected and bee-stored pollen. Apidologie 9:33–40 [Google Scholar]
  60. Höcherl N, Siede R, Illies I, Gätschenberger H, Tautz J. 60.  2012. Evaluation of the nutritive value of maize for honey bees. J. Insect Physiol. 58:278–85 [Google Scholar]
  61. Howe SR, Dimick PS, Benton AW. 61.  1985. Composition of freshly harvested and commercial royal jelly. J. Apic. Res. 24:52–61 [Google Scholar]
  62. Hrassnigg N, Crailsheim K. 62.  1998. Adaptation of hypopharyngeal gland development to the brood status of honeybee (Apis mellifera L.) colonies. J. Insect Physiol. 44:929–39 [Google Scholar]
  63. Huang C-Y, Chi L-L, Huang W-J, Chen Y-W, Chen W-J. 63.  et al. 2012. Growth stimulating effect on queen bee larvae of histone deacetylase inhibitors. J. Agric. Food Chem. 60:6139–49 [Google Scholar]
  64. Human H, Nicolson SW. 64.  2003. Digestion of maize and sunflower pollen by the spotted maize beetle Astylus atromaculatus (Melyridae): Is there a role for osmotic shock?. J. Insect Physiol. 49:633–43 [Google Scholar]
  65. Human H, Nicolson SW. 65.  2006. Nutritional content of fresh, bee-collected and stored pollen of Aloe greatheadii var. davyana (Asphodelaceae). Phytochemistry 67:1486–92 [Google Scholar]
  66. Human H, Nicolson SW, Strauss K, Pirk CWW, Dietemann V. 66.  2007. Influence of pollen quality on ovarian development in honeybees (Apis mellifera scutellata). J. Insect Physiol. 53:649–55 [Google Scholar]
  67. Jumarie C, Aras P, Boily M. 67.  2017. Mixtures of herbicides and metals affect the redox system of honey bees. Chemosphere 168:163–70 [Google Scholar]
  68. Jung-Hoffman I. 68.  1966. Die Determination von Königin und Arbeiterin der Honigbiene. Z. Bienenforsch 8:296–322 [Google Scholar]
  69. Kaftanoglu O, Linksvayer TA, Page RE Jr.. 69.  2011. Rearing honey bees, Apis mellifera, in vitro 1: effects of sugar concentrations on survival and development. J Insect Sci 11:96 [Google Scholar]
  70. Kamakura M. 70.  2011. Royalactin induces queen differentiation in honeybees. Genes Genet. Syst. 86:384 [Google Scholar]
  71. Kodai T, Umebayashi K, Nakatani T, Ishiyama K, Noda N. 71.  2007. Compositions of royal jelly II. Organic acid glycosides and sterols of the royal jelly of honeybees (Apis mellifera). Chem. Pharm. Bull. 55:1528–31 [Google Scholar]
  72. Kroon GH, van Praagh JP, Velthuis HHW. 72.  1974. Osmotic shock as a prerequisite to pollen digestion in the alimentary tract of the worker honeybee. J. Apic. Res. 13:177–88 [Google Scholar]
  73. Kwakman PHS, te Velde AA, de Boer L, Speijer D, Vandenbroucke-Grauls CMJE, Zaat SAJ. 73.  2010. How honey kills bacteria. FASEB J 24:2576–82 [Google Scholar]
  74. Kwong WK, Moran NA. 74.  2016. Gut microbial communities of social bees. Nat. Rev. Microbiol. 14:374–84 [Google Scholar]
  75. Lass A, Crailsheim K. 75.  1996. Influence of age and caging upon protein metabolism, hypopharyngeal glands and trophallactic behavior in the honey bee (Apis mellifera L.). Insectes Sociaux 43:347–58 [Google Scholar]
  76. Lau PW, Nieh JC. 76.  2016. Salt preferences of honey bee water foragers. J. Exp. Biol. 219:790–6 [Google Scholar]
  77. Lee FJ, Rusch DB, Stewart FJ, Mattile HR, Newton ILG. 77.  2014. Saccharide breakdown and fermentation by the honey bee gut microbiome. Environ. Microbiol. 17:796–815 [Google Scholar]
  78. Leonhardt SD, Blüthgen N. 78.  2011. The same, but different: pollen foraging in honeybee and bumblebee colonies. Apidologie 43:449–64 [Google Scholar]
  79. Lercker G, Capella P, Conte LS, Ruini F, Giordani G. 79.  1982. Components of royal jelly II. The lipid fraction, hydrocarbons and sterols. J. Apic. Res. 21:178–84 [Google Scholar]
  80. Lercker G, Savioli S, Vecchi MA, Sabatini AG, Nanetti A, Piana L. 80.  1986. Carbohydrate determination of Royal Jelly by high-resolution gas chromatography (HRGC). Food Chem 19:255–64 [Google Scholar]
  81. London-Shafir I, Shafir S, Eisikowitch D. 81.  2003. Amygdalin in almond nectar and pollen—facts and possible roles. Plant Syst. Evol. 238:87–95 [Google Scholar]
  82. Manning R. 82.  2001. Fatty acids in pollen: a review of their importance for honey bees. Bee World 82:60–75 [Google Scholar]
  83. Mao W, Schuler MA, Berenbaum MR. 83.  2013. Honey constituents up-regulate detoxification and immunity genes in the western honey bee Apis mellifera. PNAS 110:8842–46 [Google Scholar]
  84. Michener CD. 84.  2000. The Bees of the World Baltimore, MD: Johns Hopkins Univ. Press
  85. Minckley RL, Roulston TH. 85.  2006. Incidental mutualisms and pollen specialization among bees. Plant-Pollinator Interactions: From Specialization to Generalization NM Waser, J Ollerton Chicago: Univ. Chicago Press [Google Scholar]
  86. Moritz B, Crailsheim K. 86.  1987. Physiology of protein digestion in the midgut of the honeybee (Apis mellifera L.). J. Insect Physiol. 33:923–31 [Google Scholar]
  87. Nabas Z, Haddadin M, Haddadin J, Nazer I. 87.  2014. Chemical composition of royal jelly and effects of synbiotic with two different locally isolated probiotic strains on antioxidant activities. Polish J. Food Nutr. Sci. 64:171–80 [Google Scholar]
  88. Nicolson SW. 88.  2007. Amino acid concentrations in the nectars of southern African bird-pollinated flowers, especially Aloe and Erythrina. J. Chem. Ecol. 33:1707–20 [Google Scholar]
  89. Nicolson SW. 89.  2011. Bee food: the chemistry and nutritional value of nectar, pollen and mixtures of the two. Afr. Zool. 46:197–204 [Google Scholar]
  90. Nicolson SW, Human H. 90.  2008. Bees get a head start on honey production. Biol. Lett. 4:299–301 [Google Scholar]
  91. Nicolson SW, Human H. 91.  2013. Chemical composition of the ‘low quality’ pollen of sunflower (Helianthus annuus, Asteraceae). Apidologie 44:144–52 [Google Scholar]
  92. Nicolson SW, Thornburg RW. 92.  2007. Nectar chemistry. Nectar and Nectaries SW Nicolson, M Nepi, E Pacini Dordrecht, Neth.: Springer [Google Scholar]
  93. Oertel E, Fieger EA, Williams VR, Andrews EA. 93.  1951. Inversion of cane sugar in the honey stomach of the bee. J. Econ. Entomol. 44:487–92 [Google Scholar]
  94. O'Rourke MK, Buchmann SL. 94.  1991. Standardized analytical techniques for bee-collected pollen. Environ. Entomol. 20:507–13 [Google Scholar]
  95. Ostwald MM, Smith ML, Seeley TD. 95.  2016. The behavioral regulation of thirst, water collection and water storage in honey bee colonies. J. Exp. Biol. 219:2156–65 [Google Scholar]
  96. Page REJ. 96.  2013. The Spirit of the Hive: The Mechanisms of Social Evolution Cambridge, MA: Harvard Univ. Press
  97. Paoli PP, Donley D, Stabler D, Saseendranath A, Nicolson SW. 97.  et al. 2014. Nutritional balance of essential amino acids and carbohydrates of the adult worker honeybee depends on age. Amino Acids 46:1449–58 [Google Scholar]
  98. Park W. 98.  1925. The storing and ripening of honey by honeybees. J. Econ. Entomol. 18:405–10 [Google Scholar]
  99. Peng Y-S, Nasr ME, Marston JM. 99.  1986. Release of alfalfa, Medicagosativa, pollen cytoplasm in the gut of the honey bee, Apis mellifera (Hymenoptera: Apidae). Ann. Entomol. Soc. Am 79:804–7 [Google Scholar]
  100. Pernal SF, Currie RW. 100.  2000. Pollen quality of fresh and 1-year-old single pollen diets for worker honey bees (Apis mellifera L.). Apidologie 31:387–409 [Google Scholar]
  101. Petanidou T, van Laere A, Ellis WN, Smets E. 101.  2006. What shapes amino acid and sugar composition in Mediterranean floral nectars?. Oikos 115:155–69 [Google Scholar]
  102. Pirk CWW, Boodhoo C, Human H, Nicolson S. 102.  2010. The importance of protein type and protein to carbohydrate ratio for survival and ovarian activation of caged honeybees (Apis mellifera scutellata). Apidologie 41:62–72 [Google Scholar]
  103. Plettner E, Slessor KN, Winston ML, Oliver JE. 103.  1996. Caste-selective pheromone biosynthesis in honeybees. Science 271:1851–53 [Google Scholar]
  104. Podrižnik B, Božič J. 104.  2016. Maturation and stratification of antibacterial activity and total phenolic content of bee bread in honey comb cells. J. Apic. Res. 54:81–92 [Google Scholar]
  105. Powell JE, Martinson VG, Urban-Mead K, Moran NA. 105.  2014. Routes of acquisition of the gut microbiota of the honey bee Apis mellifera. Appl. Environ. Microbiol. 80:7378–87 [Google Scholar]
  106. Presoto AEF, Rios MDG, de Almeida-Muradian LB. 106.  2004. Simultaneous high performance liquid chromatographic analysis of vitamins B-1, B-2 and B-6 in royal jelly. J. Braz. Chem. Soc. 15:136–39 [Google Scholar]
  107. Requier F, Odoux JF, Tamic T, Moreau N, Henry M. 107.  et al. 2015. Honey bee diet in intensive farmland habitats reveals an unexpectedly high flower richness and a major role of weeds. Ecol. Appl. 25:881–90 [Google Scholar]
  108. Roberts SP, Elekonich MA. 108.  2005. Muscle biochemistry and the ontogeny of flight capacity during behavioral development in the honey bee. Apis mellifera. J. Exp. Biol. 208:4193–98 [Google Scholar]
  109. Robinson GE. 109.  2002. Genomics and integrative analyses of division of labor in honeybee colonies. Am. Nat. 160:S160–72 [Google Scholar]
  110. Robinson GE, Page RE. 110.  1989. Genetic determination of nectar foraging, pollen foraging, and nest-site scouting in honey bee colonies. Behav. Ecol. Sociobiol. 24:317–23 [Google Scholar]
  111. Roubik DW, Buchmann SL. 111.  1984. Nectar selection by Melipona and Apis mellifera (Hymenoptera: Apidae) and the ecology of nectar intake by bee colonies in a tropical forest. Oecologia 61:1–10 [Google Scholar]
  112. Roulston TH, Buchmann SL. 112.  2000. A phylogenetic reconsideration of the pollen starch-pollination correlation. Evol. Ecol. Res. 2:627–43 [Google Scholar]
  113. Roulston TH, Cane JH. 113.  2000. Pollen nutritional content and digestibility for animals. Plant Syst. Evol. 222:187–209 [Google Scholar]
  114. Roulston TH, Cane JH, Buchmann SL. 114.  2000. What governs protein content of pollen: pollinator preferences, pollen-pistil interactions, or phylogeny?. Ecol. Monogr. 70:617–43 [Google Scholar]
  115. Schmid-Hempel P, Kacelnik A, Houston AI. 115.  1985. Honeybees maximize efficiency by not filling their crop. Behav. Ecol. Sociobiol. 17:61–66 [Google Scholar]
  116. Schmidt JO, Buchmann SL. 116.  1985. Pollen digestion and nitrogen utilization by Apis mellifera L. (Hymenoptera: Apidae). Comp. Biochem. Physiol. A Physiol. 82:499–503 [Google Scholar]
  117. Seeley TD. 117.  1986. Social foraging by honeybees: how colonies allocate foragers among patches of flowers. Behav. Ecol. Sociobiol. 19:343–54 [Google Scholar]
  118. Seeley TD. 118.  1995. The Wisdom of the Hive: The Social Physiology of Honey Bee Colonies Cambridge, MA: Harvard Univ. Press
  119. Serra Bonvehí J, Escolà Jordà R. 119.  1997. Nutrient composition and microbiological quality of honeybee-collected pollen in Spain. J. Agric. Food Chem. 45:725–32 [Google Scholar]
  120. Silva LR, Videira R, Monteiro AP, Valentão P, Andrade PB. 120.  2009. Honey from Luso region (Portugal): physicochemical characteristics and mineral contents. Microchem. J. 93:73–77 [Google Scholar]
  121. Simcock NK, Gray H, Bouchebti S, Wright GA. 121.  2017. Appetitive olfactory learning and memory in the honeybee depend on sugar reward identity. J. Insect Physiol. In press. https://doi.org/10.1016/j.jinsphys.2017.08.009 [Crossref]
  122. Simcock NK, Gray HE, Wright GA. 122.  2014. Single amino acids in sucrose rewards modulate feeding and associative learning in the honeybee. J. Insect Physiol. 69:41–48 [Google Scholar]
  123. Simone-Finstrom MD, Spivak M. 123.  2012. Increased resin collection after parasite challenge: a case of self-medication in honey bees?. PLOS ONE 7:e34601 [Google Scholar]
  124. Simpson SJ, Raubenheimer D. 124.  2012. The Nature of Nutrition Princeton, NJ: Princeton Univ. Press
  125. Somerville DC, Nicol HI. 125.  2006. Crude protein and amino acid composition of honey bee-collected pollen pellets from south-east Australia and a note on laboratory disparity. Aust. J. Exp. Agric. 46:141–49 [Google Scholar]
  126. Spannhoff A, Kim YK, Raynal NJ-M, Gharibyan V, Su M-B. 126.  et al. 2011. Histone deacetylase inhibitor activity in royal jelly might facilitate caste switching in bees. EMBO Rep 12:238–43 [Google Scholar]
  127. Stabler D, Paoli PP, Nicolson SW, Wright GA. 127.  2015. Nutrient balancing of the adult worker bumblebee (Bombus terrestris) depends on the dietary source of essential amino acids. J. Exp. Biol. 218:793–802 [Google Scholar]
  128. Stevenson PC, Nicolson SW, Wright GA. 128.  2017. Plant secondary metabolites in nectar: impacts on pollinators and ecological functions. Funct. Ecol. 31:65–75 [Google Scholar]
  129. Svoboda JA, Lusby WR. 129.  1986. Sterols of phytophagous and omnivorous species of Hymenoptera. Arch. Insect Biochem. Physiol. 3:13–18 [Google Scholar]
  130. Takenaka T, Takenaka Y. 130.  1996. Royal jelly from Apis cerana japonica and Apis mellifera. Biosci. Biotechnol. Biochem. 60:518–20 [Google Scholar]
  131. Tiedeken EJ, Stout JC, Stevenson PC, Wright GA. 131.  2014. Bumblebees are not deterred by ecologically relevant concentrations of nectar toxins. J. Exp. Biol. 217:1620–25 [Google Scholar]
  132. Todd FE, Bretherick O. 132.  1942. The composition of pollens. J. Econ. Entomol. 35:312–17 [Google Scholar]
  133. Toth AL, Kantarovich S, Meisel AF, Robinson GE. 133.  2005. Nutritional status influences socially regulated foraging ontogeny in honey bees. J. Exp. Biol. 208:4641–49 [Google Scholar]
  134. Vanderplanck M, Moerman R, Rasmont P, Lognay G, Wathelet B. 134.  et al. 2014. How does pollen chemistry impact development and feeding behaviour of polylectic bees?. PLOS ONE 9:e86209 [Google Scholar]
  135. Vásquez A, Olofsson TC. 135.  2009. The lactic acid bacteria involved in the production of bee pollen and bee bread. J. Apic. Res. Bee World 48:189–95 [Google Scholar]
  136. Vaudo AD, Stabler D, Patch HM, Tooker JF, Grozinger CM, Wright GA. 136.  2016. Bumble bees regulate their intake of essential protein and lipid pollen macronutrients. J. Exp. Biol. 219:3962–70 [Google Scholar]
  137. Villette C, Berna A, Compagnon V, Schaller H. 137.  2015. Plant sterol diversity in pollen from angiosperms. Lipids 50:749–60 [Google Scholar]
  138. Waller GD. 138.  1972. Evaluating responses of honeybees to sugar solutions using an artificial-flower feeder. Ann. Entomol. Soc. Am. 65:857–62 [Google Scholar]
  139. Waller GD, Carpenter EW, Ziehl OA. 139.  1972. Potassium in onion nectar and its probable effect on attractiveness of onion flowers to honey bees. J. Am. Soc. Hortic. Sci. 97:535–39 [Google Scholar]
  140. Wang T-H, Jian C-H, Hsieh Y-K, Wang F-N, Wang C-F. 140.  2013. Spatial distributions of inorganic elements in honeybees (Apis mellifera L.) and possible relationships to dietary habits and surrounding environmental pollutants. J. Agric. Food Chem. 61:5009–15 [Google Scholar]
  141. Wang Y, Ma L, Zhang W, Cui X, Wang H, Xu B. 141.  2016. Comparison of the nutrient composition of royal jelly and worker jelly of honey bees (Apis mellifera). Apidologie 47:48–56 [Google Scholar]
  142. Weaver N. 142.  1957. Experiments on dimorphism in the female honey bee. J. Econ. Entomol. 50:759–61 [Google Scholar]
  143. Weiner CN, Hilpert A, Werner M, Linsenmair KE, Bluthgen N. 143.  2010. Pollen amino acids and flower specialisation in solitary bees. Apidologie 41:476–87 [Google Scholar]
  144. Wheeler MM, Ament SA, Rodriguez-Zas SL, Southey B, Robinson GE. 144.  2015. Diet and endocrine effects on behavioral maturation-related gene expression in the pars intercerebralis of the honey bee brain. J. Exp. Biol. 218:4005–14 [Google Scholar]
  145. Wirtz P. 145.  1973. Differentiation in the Honeybee Larva: A Histological, Electron-Microscopical and Physiological Study of Caste Induction in Apis mellifera L. Wageningen, Neth.: Veenman [Google Scholar]
  146. Wright GA, Baker DD, Palmer MJ, Stabler D, Mustard JA. 146.  et al. 2013. Caffeine in floral nectar enhances a pollinator's memory of reward. Science 339:1202–4 [Google Scholar]
  147. Wright GA, Mustard JA, Simcock NK, Ross-Taylor AAR, McNicholas LD. 147.  et al. 2010. Parallel reinforcement pathways for conditioned food aversions in the honeybee. Curr. Biol. 20:2234–40 [Google Scholar]
  148. Yeamans RL, Roulston TH, Carr DE. 148.  2014. Pollen quality for pollinators tracks pollen quality for plants in Mimulus guttatus. Ecosphere 5:791 [Google Scholar]
  149. Zarchin S, Dag A, Salomon M, Hendriksma HP, Shafir S. 149.  2017. Honey bees dance faster for pollen that complements colony essential fatty acid deficiency. Behav. Ecol. Sociobiol. In press
  150. Zheng B, Wu Z, Xu B. 150.  2014. The effects of dietary protein levels on the population growth, performance, and physiology of honey bee workers during early spring. J. Insect Sci. 14:191 [Google Scholar]
  151. Zhu K, Liu M, Fu Z, Zhou Z, Kong Y. 151.  et al. 2017. Plant microRNAs in larval food regulate honeybee caste development. PLOS Genet 13:8e1006946 [Google Scholar]
/content/journals/10.1146/annurev-ento-020117-043423
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Nutritional Physiology and Ecology of Honey Bees
Annual Review of Entomology 63, 327 (2018); https://doi.org/10.1146/annurev-ento-020117-043423
/content/journals/10.1146/annurev-ento-020117-043423
/content/journals/10.1146/annurev-ento-020117-043423
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