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Nutritional Physiology and Metabolism of Honey Bees

Year 2019, Volume: 60 Issue: 1, 67 - 74, 28.06.2019
https://doi.org/10.29185/hayuretim.523081

Abstract

Nutrition in honey bees is studied at three different stages; colony, individuals and broods. Nectar, honeydew (insect secretions with carbohydrate rich), pollen, royal jelly and water are the main food sources of honey bees. While pollen collection is more directly proportional to the needs of the colony, nectar harvesting depends on the foragers, season and flora. Water has an important role for brood’s food and to adjust the temperature of the brood area. The physiological age-related division of labor in honey bees has also show a specialization in food collection, storage, feeding of broods and adults. The amount and quality of foods directly affect the continuity of colony life, defense against diseases and pests, but the demographic structure of the colony population also determines the amount of foods collected and stored. The main carbohydrate source of honey bees is nectar and protein source is pollen and royal jelly. The aim of this study is to review nutritional physiology in the growth, development and reproductive requirements of honey bees at individuals and colony level. In addition, it is aimed to compile information about protein and carbohydrate metabolism.

References

  • Alaux C, Dantec C, Parrinello H, Le Conte Y. 2011. Nutrigenomics in honey bees: digital gene expression analysis of pollen’s nutritive effects on healthy and varroa-parasitized bees. BMC Genomics, 12:496.
  • Balderrama NM, Almeida LO, Núñez JA. 1992. Metabolic rate during foraging in the honeybee. Journal of Comparative Physiology B 162: 440–447.
  • Barker R J, Lehner Y. 1974. Acceptance and sustenance value of naturally occurring sugars fed to newly emerged adult workers of honey bees (Apis mellifera L.). Journal of Experimental Zoology 187: 277–285.
  • Barker RJ, Lehner Y. 1976. Galactose a sugar toxic to honey bees found in exudate of tulip flowers. Apidologie 7: 109–112.
  • Barker RJ. 1977. Some carbohydrates found in pollen and pollen substıtutes are toxic to honey bees. Journal of Nutrition 107: 1859-1862.
  • Bogdanov S. 2017. Pollen: production, nutrition and health: a review. Bee Product Science. Available: http: //www.bee-hexagon.net/(23.01.2019).
  • Bogdanov S. 2017. Royal jelly, bee brood: composition, nutrition, health. The Royal Jelly Book, Chapter 2. Bee Product Science, Available: http: //www.bee-hexagon.net/ (23.01.2019).
  • Brodschneider R, Crailsheim K. 2010. Nutrition and health in honey bees. Apidologie 41: 278–294.
  • Brouwers EVM, Ebert R, Beetsma J. 1987. Behavioural and physiological aspects of nurse bees in relation to the composition of larval food during caste differentiation in the honeybee. Journal of Apicultural Research 26: 11-23.
  • Campos MGR, Bogdanov S, Almeida-Muradian LB, Szczesna B, Mancebo Y, Frigerio C, Ferreira F. 2008. Pollen composition and standardisation of analytical methods. Journal of Apicultural Research 47(2): 154-161.
  • Carter C, Shafir S,Yehonatan L, Palmer RG, Thornburg R. 2006. A novel role for proline in plant floral nectars. Naturwissenschaften 93: 72–79.
  • Corbet SA. 2003. Nectar sugar content: estimating standing crop and secretion rate in the field. Apidologie 34: 1–10.
  • Crailsheim K, Schneider LHW, Hrassnigg N, Bühlmann G, Brosch U, Gmeinbauer R, Schöffmann B. 1992. Pollen consumption and utilization in worker honeybees (Apis mellifera carnica): dependence on individual age and function. Journal of Insect Physiology 38: 409–419.
  • Crailsheim K. 1990. The protein balance of the honey bee worker. Apidologie 21: 417–429.
  • Crailsheim K. 1992. The flow of jelly within a honeybee colony. Journal of Comparative Physiology B 162: 681–689.
  • Dade HA. 1962. Anatomy and dissection of the honeybee. International Bee Research Association&Northern Bee Books. 2017. 196 p.
  • DeGrandi-Hoffman G, Chen Y. 2015. Nutrition, immunity and viral infections in honey bees. Current Opinion in Insect Science 10: 170–176.
  • De Groot AP. 1953. Protein and amino acid requirements of the honeybee (Apis mellifica L.). Physiologia Comparata et Oecologia 3: 197–285.
  • Deseyn J, Billen J. 2005. Age-dependent morphology and ultrastructure of the hypopharyngeal gland of Apis mellifera workers (Hymenoptera, Apidae). Apidologie 36(1): 49-57.
  • Engel P, Martinson VG, Moran NA. 2012. Functional diversity within the simple gut microbiota of the honey bee. Proceedings National Academy of Sciences of the USA 109:11002–11007.
  • Gardener MC, Gillman MP. 2001. Analyzing variability in nectar amino acids: composition is less variable than concentration. Journal of Chemical Ecology 27: 2545–2558.
  • Haunerland NH, Shirk PD. 1995. Regional and functional differentiation in the insect fat body. Annual Review of Entomology 40: 121–145.
  • Herbert EW, Shimanuki H. 1978. Chemical composition and nutritive value of bee-collected and bee-stored pollen. Apidologie 9: 33–40.
  • Hrassnigg N, Crailsheim K. 1998. The influence of brood on the pollen consumption of worker bees (Apis mellifera L.). J. Insect Physiology 44: 393–404.
  • Jay SC. 1963. The development of honeybees in their cells. Journal of Apicultural Research 2: 117–134.
  • Kuhnholz S, Seeley TD. 1997. The control of water collection in honey bee colonies. Behavioral Ecology and Sociobiology 41: 407-422.
  • Kunert K, Crailsheim K. 1988. Seasonal changes in carbohydrate, lipid and protein content in emerging worker honeybees and their mortality. Journal of Apicultural Research 27: 13–21.
  • Kunieda T, Fujiyuki T, Kucharski R, Foret S, Ament SA, Toth AL, Ohashi K, Takeuchi H, Kamikouchi A, Kage E, Morioka M, Beye M, Kubo T, Robinson GE, Maleszka R. 2006. Carbohydrate metabolism genes and pathways in insects: insights from the honey bee genome. Insect Molecular Biology 15(5): 563-576.
  • Kwong WK, Moran NA. 2016. Gut microbial communities of social bees. Nature Reviews Microbiology 14:374-384.
  • Lau PW, Nieh JC. 2016. Salt preferences of honey bee water foragers. Journal of Experimental Biology 219:790–6.
  • Le Conte Y, Mohammedi A, Robinson GE. 2001. Primer effects of a brood pheromone on honeybee behavioural development. Proceedings of the Royal Society B 268:163–168.
  • Martinson VG, Moy J, Moran NA. 2012. Establishment of characteristic gut bacteria during development of the honeybee worker. Applied and Environmental Microbiology 78:2830-2840.
  • Nation JL. 2015. Insect physiology and biochemistry. CRC Press.Taylor&Francis Group. 690 p.
  • Nicolson SW, Thornburg RW. 2007. Nectar chemistry. In nectar and nectaries. ed. SW Nicolson, M Nepi, E Pacini. Dordrecht, Neth. Springer.
  • Nicolson SW. 2011. Bee food: the chemistry and nutritional value of nectar, pollen and mixtures of the two. African Zoology 46(2): 197–204.
  • O’Toole C, Raw A. 1991. Bees of the world. London: Blanford, 192 p.
  • 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.). European Journal of Biochemistry 265: 127–133.
  • Pankiw T, Page RE Jr, Fondrk MK. 1998. Brood pheromone stimulates pollen foraging in honey bees (Apis mellifera). Behavioral Ecology and Sociobiology 44:193–198.
  • Pernal SF, Currie RW. 2001. The influence of pollen quality on foraging behavior in honeybees (Apis mellifera L.). Behavioral Ecology and Sociobiology 51:53–68.
  • Ramadan M, Al-Ghamdi A. 2012. Bioactive compounds and health-promoting properties of royal jelly: A review. Journal of Functional Foods 4: 39–52.
  • Raymann K, Moran NA. 2018. The role of the gut microbiome in health and disease of adult honey bee workers. Current Opinion in Insect Science 26: 97–104.
  • Robinson GE, Page RE. 1989. Genetic determination of nectar foraging, pollen foraging, and nest-site scouting in honey bee colonies. Behavioral Ecology and Sociobiology 24:317–323.
  • Rortais A, Arnold G, Halm MP, Touffet-Briens F. 2005. Modes of honeybees exposure to systemic insecticides: estimated amounts of contaminated pollen and nectar consumed by different categories of bees. Apidologie 36: 71–83.
  • Roubik DW, Buchmann SL 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.
  • Roulston TH, Cane JH. 2000. Pollen nutritional content and digestibility for animals. Plant Systematics and Evolution 222: 187–209.
  • Sabatini AG, Marcazzan G, Caboni MF, Bogdanov S, Almeida-Muradian L.B. 2009. Quality and standardisation of royal jelly. Journal of ApiProduct and ApiMedical Science, 1:1-6.
  • Sagili RR, Pankiw T. 2009. Effects of brood pheromone modulated brood rearing behaviors on honey bee (Apis mellifera L.) colony growth. Journal of Insect Behavior 22:339–349.
  • Schmickl T, Crailsheim K, 2001. Cannibalism and early capping: strategy of honeybee colonies in times of experimental pollen shortages. The Journal of Comparative Physiology A 187: 541-547.
  • Schmickl T, Crailsheim K. 2002. How honeybees (Apis mellifera L.) change their broodcare behavior in response to non-foraging conditions and poor pollen conditions. Behavioral Ecology and Sociobiology 51: 415–425.
  • Schmickl T, Crailsheim K. 2004. Inner nest homeostasis in a changing environment with special emphasis on honey bee brood nursing and pollen supply. Apidologie 35: 249–263.
  • Seeley TD. 1985. Honeybee ecology, A study of adaptation in social life, Princeton University Press, Princeton. 214 p.
  • Seeley TD.1989. The honey bee colony as a superorganism. American Sciencist 77(6): 546–553.
  • Simpson J, Riedel IBM, Wilding M. 1968. Invertase in the hypopharyngeal glands of the honeybee. Journal of Apicultural Research 7: 29-36.
  • Snodgrass RE 1910. The Anatomy of the honey bee. Pickle Partners Publishing, 2018. 214 p.
  • Standifer LN, Moeller FE, Kauffeld NM, Herbert EW, Shimanuki H. 1977. Supplemental feeding of honey bee colonies. USDA Agriculture Information Bulletin No.413, 8 p.
  • Szczęsna T. 2006. Protein content and amino acid composition of bee-collected pollen from selected botanical origins. Journal of Apicultural Science,50:81–90.
  • Tarpy DF, Mattila HR, Newton ILG. 2015. Development of the honey bee gut microbiome throughout the queen-rearing process. Applied and Environmental Microbiology 81:3182-3191.
  • Thorp RW. 1979. Structural, behavioral, and physiological adaptations of bees (Apoidea) for collecting pollen. Annals of the Missouri Botanical Garden 66: 788–812.
  • Topal E, Strant M, Yücel B, Kösoğlu M, Mărgăoan R, Dayıoğlu M. 2018. Ana ve Erkek Arı Larvalarının Biyokimyasal Özellikleri ve Apiterapötik Kullanımı. Hayvansal Üretim 59 (2): 77-82.
  • Vásquez A, Olofsson TC. 2009. The lactic acid bacteria involved in the production of bee pollen and bee bread, Journal of Apicultural Research 48: 189–195.
  • White JWJr, Subers MH, Schepartz AI. 1963. The identification of inhibine, antibacterial factor in honey, as hydrogen peroxide, and its origin in a honey glucose oxidase system. Biochimica et Biophysica Acta 73, 57-70.
  • Winston ML. 1987. The biology of the honey bee. Harvard University Press, Cambridge, MA, USA. 281 p.
  • Wright GA, Nicolson SW, Shafir S. 2018. Nutritional physiology and ecology of honey Bees. Annual Review of Entomology 63:327-344.
  • Zheng B, Wu Z, Xu B. 2014. The effects of dietary protein levels on the population growth, performance, and physiology of honey bee workers during early spring. Journal of Insect Science 14:191.
  • Zheng H, Powell JE, Steele MI, Dietrich C, Moran NA. 2017. Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling. Proceedings National Academy of Sciences of the USA 114:4775-4780.

Bal Arılarında Beslenme Fizyolojisi ve Metabolizması

Year 2019, Volume: 60 Issue: 1, 67 - 74, 28.06.2019
https://doi.org/10.29185/hayuretim.523081

Abstract

Bal arılarında beslenme; koloni düzeyinde, bireysel ve yavruların beslenmesi olmak üzere üç farklı aşamada irdelenmekte, nektar, karbonhidratça zengin böcek salgıları, polen, arı sütü ve su bal arılarının temel besin kaynaklarını oluşturmaktadır. Polen toplama daha çok koloninin ihtiyacı ile doğru orantılı iken, nektar toplama faaliyeti tarlacı işçi arı mevcuduna, mevsime ve floraya bağlıdır. Su, yavru besininde kullanılmak üzere ve yavru alanı sıcaklığının ayarlanmasında önemli role sahiptir. Bal arılarında fizyolojik yaşa bağlı iş bölümü; besin toplama, depolama, yavru ve ergin bireylerin beslenmesinde de özelleşme ortaya koymuştur. Besin miktarı ve kalitesi koloni yaşamının devamlılığını, hastalık ve zararlılara karşı savunmayı doğrudan etkilemekte, bununla birlikte koloni populasyonun demografik yapısı da toplanan ve depolanan besin miktarını belirlemektedir. Bal arılarının temel karbonhidrat kaynağı nektar, protein kaynağı ise polen ve arı sütüdür. Bu çalışmada bal arılarının bireysel ve koloni düzeyinde büyüme, gelişme ve üreme gereksinimlerinde beslenme fizyolojisi yanı sıra protein ve karbonhidrat metabolizması ile ilgili bilgilerin derlenmesi amaçlanmıştır.

References

  • Alaux C, Dantec C, Parrinello H, Le Conte Y. 2011. Nutrigenomics in honey bees: digital gene expression analysis of pollen’s nutritive effects on healthy and varroa-parasitized bees. BMC Genomics, 12:496.
  • Balderrama NM, Almeida LO, Núñez JA. 1992. Metabolic rate during foraging in the honeybee. Journal of Comparative Physiology B 162: 440–447.
  • Barker R J, Lehner Y. 1974. Acceptance and sustenance value of naturally occurring sugars fed to newly emerged adult workers of honey bees (Apis mellifera L.). Journal of Experimental Zoology 187: 277–285.
  • Barker RJ, Lehner Y. 1976. Galactose a sugar toxic to honey bees found in exudate of tulip flowers. Apidologie 7: 109–112.
  • Barker RJ. 1977. Some carbohydrates found in pollen and pollen substıtutes are toxic to honey bees. Journal of Nutrition 107: 1859-1862.
  • Bogdanov S. 2017. Pollen: production, nutrition and health: a review. Bee Product Science. Available: http: //www.bee-hexagon.net/(23.01.2019).
  • Bogdanov S. 2017. Royal jelly, bee brood: composition, nutrition, health. The Royal Jelly Book, Chapter 2. Bee Product Science, Available: http: //www.bee-hexagon.net/ (23.01.2019).
  • Brodschneider R, Crailsheim K. 2010. Nutrition and health in honey bees. Apidologie 41: 278–294.
  • Brouwers EVM, Ebert R, Beetsma J. 1987. Behavioural and physiological aspects of nurse bees in relation to the composition of larval food during caste differentiation in the honeybee. Journal of Apicultural Research 26: 11-23.
  • Campos MGR, Bogdanov S, Almeida-Muradian LB, Szczesna B, Mancebo Y, Frigerio C, Ferreira F. 2008. Pollen composition and standardisation of analytical methods. Journal of Apicultural Research 47(2): 154-161.
  • Carter C, Shafir S,Yehonatan L, Palmer RG, Thornburg R. 2006. A novel role for proline in plant floral nectars. Naturwissenschaften 93: 72–79.
  • Corbet SA. 2003. Nectar sugar content: estimating standing crop and secretion rate in the field. Apidologie 34: 1–10.
  • Crailsheim K, Schneider LHW, Hrassnigg N, Bühlmann G, Brosch U, Gmeinbauer R, Schöffmann B. 1992. Pollen consumption and utilization in worker honeybees (Apis mellifera carnica): dependence on individual age and function. Journal of Insect Physiology 38: 409–419.
  • Crailsheim K. 1990. The protein balance of the honey bee worker. Apidologie 21: 417–429.
  • Crailsheim K. 1992. The flow of jelly within a honeybee colony. Journal of Comparative Physiology B 162: 681–689.
  • Dade HA. 1962. Anatomy and dissection of the honeybee. International Bee Research Association&Northern Bee Books. 2017. 196 p.
  • DeGrandi-Hoffman G, Chen Y. 2015. Nutrition, immunity and viral infections in honey bees. Current Opinion in Insect Science 10: 170–176.
  • De Groot AP. 1953. Protein and amino acid requirements of the honeybee (Apis mellifica L.). Physiologia Comparata et Oecologia 3: 197–285.
  • Deseyn J, Billen J. 2005. Age-dependent morphology and ultrastructure of the hypopharyngeal gland of Apis mellifera workers (Hymenoptera, Apidae). Apidologie 36(1): 49-57.
  • Engel P, Martinson VG, Moran NA. 2012. Functional diversity within the simple gut microbiota of the honey bee. Proceedings National Academy of Sciences of the USA 109:11002–11007.
  • Gardener MC, Gillman MP. 2001. Analyzing variability in nectar amino acids: composition is less variable than concentration. Journal of Chemical Ecology 27: 2545–2558.
  • Haunerland NH, Shirk PD. 1995. Regional and functional differentiation in the insect fat body. Annual Review of Entomology 40: 121–145.
  • Herbert EW, Shimanuki H. 1978. Chemical composition and nutritive value of bee-collected and bee-stored pollen. Apidologie 9: 33–40.
  • Hrassnigg N, Crailsheim K. 1998. The influence of brood on the pollen consumption of worker bees (Apis mellifera L.). J. Insect Physiology 44: 393–404.
  • Jay SC. 1963. The development of honeybees in their cells. Journal of Apicultural Research 2: 117–134.
  • Kuhnholz S, Seeley TD. 1997. The control of water collection in honey bee colonies. Behavioral Ecology and Sociobiology 41: 407-422.
  • Kunert K, Crailsheim K. 1988. Seasonal changes in carbohydrate, lipid and protein content in emerging worker honeybees and their mortality. Journal of Apicultural Research 27: 13–21.
  • Kunieda T, Fujiyuki T, Kucharski R, Foret S, Ament SA, Toth AL, Ohashi K, Takeuchi H, Kamikouchi A, Kage E, Morioka M, Beye M, Kubo T, Robinson GE, Maleszka R. 2006. Carbohydrate metabolism genes and pathways in insects: insights from the honey bee genome. Insect Molecular Biology 15(5): 563-576.
  • Kwong WK, Moran NA. 2016. Gut microbial communities of social bees. Nature Reviews Microbiology 14:374-384.
  • Lau PW, Nieh JC. 2016. Salt preferences of honey bee water foragers. Journal of Experimental Biology 219:790–6.
  • Le Conte Y, Mohammedi A, Robinson GE. 2001. Primer effects of a brood pheromone on honeybee behavioural development. Proceedings of the Royal Society B 268:163–168.
  • Martinson VG, Moy J, Moran NA. 2012. Establishment of characteristic gut bacteria during development of the honeybee worker. Applied and Environmental Microbiology 78:2830-2840.
  • Nation JL. 2015. Insect physiology and biochemistry. CRC Press.Taylor&Francis Group. 690 p.
  • Nicolson SW, Thornburg RW. 2007. Nectar chemistry. In nectar and nectaries. ed. SW Nicolson, M Nepi, E Pacini. Dordrecht, Neth. Springer.
  • Nicolson SW. 2011. Bee food: the chemistry and nutritional value of nectar, pollen and mixtures of the two. African Zoology 46(2): 197–204.
  • O’Toole C, Raw A. 1991. Bees of the world. London: Blanford, 192 p.
  • 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.). European Journal of Biochemistry 265: 127–133.
  • Pankiw T, Page RE Jr, Fondrk MK. 1998. Brood pheromone stimulates pollen foraging in honey bees (Apis mellifera). Behavioral Ecology and Sociobiology 44:193–198.
  • Pernal SF, Currie RW. 2001. The influence of pollen quality on foraging behavior in honeybees (Apis mellifera L.). Behavioral Ecology and Sociobiology 51:53–68.
  • Ramadan M, Al-Ghamdi A. 2012. Bioactive compounds and health-promoting properties of royal jelly: A review. Journal of Functional Foods 4: 39–52.
  • Raymann K, Moran NA. 2018. The role of the gut microbiome in health and disease of adult honey bee workers. Current Opinion in Insect Science 26: 97–104.
  • Robinson GE, Page RE. 1989. Genetic determination of nectar foraging, pollen foraging, and nest-site scouting in honey bee colonies. Behavioral Ecology and Sociobiology 24:317–323.
  • Rortais A, Arnold G, Halm MP, Touffet-Briens F. 2005. Modes of honeybees exposure to systemic insecticides: estimated amounts of contaminated pollen and nectar consumed by different categories of bees. Apidologie 36: 71–83.
  • Roubik DW, Buchmann SL 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.
  • Roulston TH, Cane JH. 2000. Pollen nutritional content and digestibility for animals. Plant Systematics and Evolution 222: 187–209.
  • Sabatini AG, Marcazzan G, Caboni MF, Bogdanov S, Almeida-Muradian L.B. 2009. Quality and standardisation of royal jelly. Journal of ApiProduct and ApiMedical Science, 1:1-6.
  • Sagili RR, Pankiw T. 2009. Effects of brood pheromone modulated brood rearing behaviors on honey bee (Apis mellifera L.) colony growth. Journal of Insect Behavior 22:339–349.
  • Schmickl T, Crailsheim K, 2001. Cannibalism and early capping: strategy of honeybee colonies in times of experimental pollen shortages. The Journal of Comparative Physiology A 187: 541-547.
  • Schmickl T, Crailsheim K. 2002. How honeybees (Apis mellifera L.) change their broodcare behavior in response to non-foraging conditions and poor pollen conditions. Behavioral Ecology and Sociobiology 51: 415–425.
  • Schmickl T, Crailsheim K. 2004. Inner nest homeostasis in a changing environment with special emphasis on honey bee brood nursing and pollen supply. Apidologie 35: 249–263.
  • Seeley TD. 1985. Honeybee ecology, A study of adaptation in social life, Princeton University Press, Princeton. 214 p.
  • Seeley TD.1989. The honey bee colony as a superorganism. American Sciencist 77(6): 546–553.
  • Simpson J, Riedel IBM, Wilding M. 1968. Invertase in the hypopharyngeal glands of the honeybee. Journal of Apicultural Research 7: 29-36.
  • Snodgrass RE 1910. The Anatomy of the honey bee. Pickle Partners Publishing, 2018. 214 p.
  • Standifer LN, Moeller FE, Kauffeld NM, Herbert EW, Shimanuki H. 1977. Supplemental feeding of honey bee colonies. USDA Agriculture Information Bulletin No.413, 8 p.
  • Szczęsna T. 2006. Protein content and amino acid composition of bee-collected pollen from selected botanical origins. Journal of Apicultural Science,50:81–90.
  • Tarpy DF, Mattila HR, Newton ILG. 2015. Development of the honey bee gut microbiome throughout the queen-rearing process. Applied and Environmental Microbiology 81:3182-3191.
  • Thorp RW. 1979. Structural, behavioral, and physiological adaptations of bees (Apoidea) for collecting pollen. Annals of the Missouri Botanical Garden 66: 788–812.
  • Topal E, Strant M, Yücel B, Kösoğlu M, Mărgăoan R, Dayıoğlu M. 2018. Ana ve Erkek Arı Larvalarının Biyokimyasal Özellikleri ve Apiterapötik Kullanımı. Hayvansal Üretim 59 (2): 77-82.
  • Vásquez A, Olofsson TC. 2009. The lactic acid bacteria involved in the production of bee pollen and bee bread, Journal of Apicultural Research 48: 189–195.
  • White JWJr, Subers MH, Schepartz AI. 1963. The identification of inhibine, antibacterial factor in honey, as hydrogen peroxide, and its origin in a honey glucose oxidase system. Biochimica et Biophysica Acta 73, 57-70.
  • Winston ML. 1987. The biology of the honey bee. Harvard University Press, Cambridge, MA, USA. 281 p.
  • Wright GA, Nicolson SW, Shafir S. 2018. Nutritional physiology and ecology of honey Bees. Annual Review of Entomology 63:327-344.
  • Zheng B, Wu Z, Xu B. 2014. The effects of dietary protein levels on the population growth, performance, and physiology of honey bee workers during early spring. Journal of Insect Science 14:191.
  • Zheng H, Powell JE, Steele MI, Dietrich C, Moran NA. 2017. Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling. Proceedings National Academy of Sciences of the USA 114:4775-4780.
There are 65 citations in total.

Details

Primary Language Turkish
Journal Section Reviews
Authors

Gonca Özmen Özbakır 0000-0003-1695-4012

Duygu Gülru Alişiroğlu 0000-0002-2395-7927

Publication Date June 28, 2019
Submission Date February 6, 2019
Published in Issue Year 2019 Volume: 60 Issue: 1

Cite

APA Özmen Özbakır, G., & Alişiroğlu, D. G. (2019). Bal Arılarında Beslenme Fizyolojisi ve Metabolizması. Hayvansal Üretim, 60(1), 67-74. https://doi.org/10.29185/hayuretim.523081


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