Pollen nutrition affects honey bee stress resistance

In: Terrestrial Arthropod Reviews
Author: Zachary Huang1
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  • 1 Michigan State University, East Lansing, Michigan 48824, USA

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The honey bee, Apis, is perhaps the most beneficial insect to humans because most of our fruits and vegetables depend on them for pollination. Yet these iconic insects have been plagued by many types of stresses. This paper reviews many lines of evidence pointing to the importance of pollen nutrition in honey bee health. In laboratory studies that used caged honey bees, poor pollen nutrition led to a reduction of worker bees’ resistance to the microsporidian, Nosema apis, an increase of bee’s sensitivity to pesticides, and an increased titer of bee virus. On the other hand, polyfloral pollen made bees more resistant to stresses by enhancing their immune related enzyme activities. At the colony level, good pollen nutrition increased honey bee’s resistance to Nosema ceranae or the ectoparasitic mite, Varroa destructor. The effects of both transportation and habitat changes on honey bees seem most likely mediated via decreased diversity, or amount, of pollen to the colonies. Pollen nutrition, therefore, might work together with other factors in reducing the bees’ resistance and exacerbate the effects of viruses, pesticides, or parasites, eventually resulting in Colony Collapse Disorder. Besides paying attention to all of these other factors, pollen nutrition should be an important focus in the future for maintaining healthy bee colonies.

  • Alaux C., Ducloz F., Crauser D., , and Le Conte Y.. 2010. Diet effects on honeybee immunocompetence. Biology Letters 6:562565.

  • Alaux C., Dantec C., , H. Dantec, Parrinello Y., , and 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.

    • Search Google Scholar
    • Export Citation
  • Amdam G. V., Simoes Z. L. P., Hagen A., Norberg K., Schroder K., Mikkelsen O., Kirkwood T. B. L., , and Omholt S. W.. 2004. Hormonal control of the yolk precursor vitellogenin regulates immune function and longevity in honeybees. Experimental Gerontology 39:767773.

    • Search Google Scholar
    • Export Citation
  • Barker R. J.1977. Some carbohydrates found in pollen and pollen substitutes are toxic to honey bees. Journal of Nutrition 107:18591862.

    • Search Google Scholar
    • Export Citation
  • Brodschneider R., Crailsheim K.. 2010. Nutrition and health in honey bees. Apidologie 41: 278294.

  • Costanza, R, R., d’Arge, R. S. de, Groot, S., Farber, M., Grasso, B., Hannon, K., Limburg, R. V., Naeem, J., O’Neill, R.G., Paruelo, P., Raskin, P., Sutton, and M., van den Belt. 1997. The value of the world’s ecosystem services and natural capital. Nature 387:253-60.

  • Chen Y. P., Evans J. D., Smith J. B., , and Pettis J. S.. 2008. Nosema ceranae is a long-present and wide-spread microsporidian infection of the European honey bee (Apis mellifera) in the United States. Journal of Invertebrate Pathology 97:186188.

    • Search Google Scholar
    • Export Citation
  • Crailsheim K.1991. Interadult feeding of jelly in honeybee (Apis mellifera L.) colonies. Journal of Comparative Physiology B 161:5560.

  • Crailsheim K.1992. The flow of jelly within a honeybee colony. Journal of Comparative Physiology B 162:681689.

  • Cremonez T. M., De Jong D., , and Bitondi M. M. G.. 1998. Quantification of hemolymph proteins as a fast method for testing protein diets for honey bees (Hymenoptera: Apidae). Journal of Economic Entomology 91:12841289.

    • Search Google Scholar
    • Export Citation
  • De Groot A. P.1953. Protein and amino acid requirements of the honey bee (Apis mellifera L.)., 3, 197285. Physiologia Comparata et Oecologia 3:197-285.

    • Search Google Scholar
    • Export Citation
  • DeJong D., 1997. Mites: varroa and other parasites of brood. pp. 279–328. In, Morse R.A., Flottum K. (Editors). Honey Bee Pests, Predators, and Diseases. Third Edition. The A. I. Root Company. Medina, Ohio, USA. 718 pp.

    • Search Google Scholar
    • Export Citation
  • De Jong D., Junqueira da Silva E., Kevan G. P., , and Atkinson L. J.. 2009. Pollen substitutes increase honey bee haemolymph protein levels as much as or more than does pollen. Journal of Apicultural Research 48:3437.

    • Search Google Scholar
    • Export Citation
  • DeGrandi-Hoffman G., Wardell G., Ahumada-Segura F., Rinderer T., Danka R., , and Pettis J.. 2008. Comparisons of pollen substitute diets for honey bees: consumption rates by colonies and effects on brood and adult populations. Journal of apicultural research 47:265270.

    • Search Google Scholar
    • Export Citation
  • DeGrandi-Hoffman G., Chen Y., Huang E., , and Huang M. H.. 2010. The effect of diet on protein concentration, hypopharyngeal gland development and virus load in worker honey bees (Apis mellifera L.). Journal of Insect Physiology 56:11841191.

    • Search Google Scholar
    • Export Citation
  • Eischen F. A., Graham R. H.. 2008. Feeding overwintering honey bee colonies infected with Nosema ceranae. American Bee Journal 148:555.

  • Eischen F. A., Grahamj R. H., , and Riveraj R.. 2008. Overwintering nutritionally stressed honey bee colonies infested with Varroa destructor. American Bee Journal 148: 555556.

    • Search Google Scholar
    • Export Citation
  • Fluri P., Lüscher M., Wille H., , and Gerig L.. 1982. Changes in weight of the pharyngeal gland and haemolymph titres of juvenile hormone and vitellogenin in worker honeybees. Journal of Insect Physiology 28:6168.

    • Search Google Scholar
    • Export Citation
  • Gallai N., Salles J., Settele J., , and Vaissière B. E.. 2009. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics 68:81021.

    • Search Google Scholar
    • Export Citation
  • Genersch E., von der Ohe W., Kaatz H., Schroeder A., Otten C., Büchler R., Berg S., Ritter W., Mülhen W., Gisder S., Meixner M., Liebig G., , and Rosenkranz P.. 2010. The German Bee Monitoring Project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie 41:332352.

    • Search Google Scholar
    • Export Citation
  • Gregory P. G.2006. Protein diets and their effects on worker weight, longevity, consumption and haemolymph protein levels of Apis mellifera. American Bee Journal 146:447.

    • Search Google Scholar
    • Export Citation
  • Guzmán-Novoa E., Eccles L., Calvete Y., McGowan J., Kelly P., , and Correa-Benitez A.. 2010. Varroa destructor is the main culprit for death and reduced populations of overwintered honey bees in Ontario, Canada. Apidologie 4:443451.

    • Search Google Scholar
    • Export Citation
  • Haydak M. H.1967. Bee nutrition and pollen substitutes. Apiacta 1:38.

  • Haydak M. H.1970. Honey bee nutrition. Annual Review of Entomology.15:143156.

  • Herbert W. E. J., Shimanuki H.. 1982. Effect of population density and available diet on the rate of brood rearing by honey bees offered a pollen substitute. Apidologie 13:2128.

    • Search Google Scholar
    • Export Citation
  • Herbert W. E. J., Shimanuki H., , and Shasha S. B.. 1980. Brood rearing and food consumption by honeybee colonies fed pollen substitutes supplemented with starch-encapsulated pollen extracts. Journal of Apicultural Research:115118.

    • Search Google Scholar
    • Export Citation
  • Higes M, Martín-Hernández R., Botías C., Bailón E. G., González-Porto A.V., Barrios L., Del Nozal M. J., Bernal J. L., Jiménez J. J., Palencia P. G., , and Meana A.. 2008 How natural infection by Nosema ceranae causes honeybee colony collapse. Environmental Microbiology 10:26592669.

    • Search Google Scholar
    • Export Citation
  • Huang Z. Y., 2008. The colony collapse disorder crisis for honey bees. pp. 15-18. In, Cullen C. (Editor). Encyclopedia of Life Science. Volume I. Infobase Publishing. New York, NY, USA. 401 pp.

    • Search Google Scholar
    • Export Citation
  • Huang Z. Y.2010. Bees worth a billion $ in Michigan. http://bees.msu.edu/2010/03/bees-worth-a-billion-in-michigan/. Visited March 16, 2012.

    • Search Google Scholar
    • Export Citation
  • Huang Z.-Y., Otis G. W., , and Teal P. E. A.. 1989. Nature of brood signal activating the protein synthesis of hypopharyngeal gland in honey bees, Apis mellifera (Apidae: Hymenoptera). Apidologie 20:455464.

    • Search Google Scholar
    • Export Citation
  • Iqbal J., Mueller U.. 2007. Virus infection causes specific learning deficits in honeybee foragers. Royal Soceity Proceedings of Biological Sciences 274:15171521.

    • Search Google Scholar
    • Export Citation
  • Janmaat A. F., Winston M. L.. 2000. Removal of Varroa jacobsoni infested brood in honey bee colonies with different pollen stores. Apidologie 31:377385.

    • Search Google Scholar
    • Export Citation
  • Keller I., Fluri P., , and Imdorf A.. 2005. Pollen nutrition and colony development in honey bees-Part 2. Bee World 86:2734.

  • Kleinschmidt G., Kondos A.. 1976. The influence of crude protein levels on colony production. The Australasian Beekeeper 78:3639.

  • Kleinschmidt G., Kondos A., . 1977. The effect of dietary protein on colony performance. pp. 357-361. In, Meletinov C., (Editor), Proceedings of the 26th International Apicultural Congress, Oct 13-19, 1977. Apimondia, Bucharest. 615 pp.

    • Search Google Scholar
    • Export Citation
  • Knox D. A., Shimanuki H., , and Herbert E. W.. 1971. Diet and the longevity of adult honey bees. Journal of Economic Entomology 64:14151416.

  • Kralj J., Fuchs S.. 2010. Nosema sp. influences flight behavior of infected honey bee (Apis mellifera) foragers. Apidologie 41:2128.

  • Kralj J., Brockmann A., Fuchs S., , and Tautz J.. 2007. The parasitic mite Varroa destructor affects non-associative learning in honey bee foragers, Apis mellifera L. Journal of Comparative Physiology A 193:363370.

    • Search Google Scholar
    • Export Citation
  • Manning R., Rutkay A.. 2007. Lipid-enhanced pollen and lipid-reduced flour diets and their effect on the longevity of honey bees (Apis mellifera L.). Australian Journal of Entomology 46:251257.

    • Search Google Scholar
    • Export Citation
  • Mattila H. R., Otis G. W.. 2006. Influence of pollen diet in spring on development of honey bee (Hymenoptera: Apidae) colonies. Journal of Economic Entomology 99:604613.

    • Search Google Scholar
    • Export Citation
  • Mattila H. R., Otisb G. W.. 2006. Effects of pollen availability and nosema infection during the spring on division of labor and survival of worker honey bees (Hymenoptera: Apidae). Environmental Entomology 35:708717.

    • Search Google Scholar
    • Export Citation
  • Maurizio A.1950. The influence of pollen feeding and brood rearing on the length of life and physiological conditions of the honeybee. Bee World 31:912.

    • Search Google Scholar
    • Export Citation
  • Morimoto T., Kojima Y., Toki T., Komeda Y., Yoshiyama M., Kimura K., Nirasawa K., , and Kadowaki T.. 2011. The habitat disruption induces immune-suppression and oxidative stress in honey bees. Ecology and Evolution 1:201217.

    • Search Google Scholar
    • Export Citation
  • Morse R. A., Calderone N. W.. 2000. The value of honey bees as pollinators of U.S. crops in 2000. Bee Culture 128:215.

  • Naug D.2009. Nutritional stress due to habitat loss may explain recent honeybee colony collapses. Biological Conservation 142: 23692372.

    • Search Google Scholar
    • Export Citation
  • Neumann P., Elzen P. J.. 2004. The biology of the small hive beetle (Aethina tumida, Coleoptera: Nitidulidae): Gaps in our knowledge of an invasive species. Apidologie 35:229247.

    • Search Google Scholar
    • Export Citation
  • Neupane K. R., Thapa R. B.. 2005. Alternative to Off-Season Sugar Supplement Feeding of Honeybees. Journal of the Institute of Agriculture and Animal Science 26:7778.

    • Search Google Scholar
    • Export Citation
  • Oldroyd B.P.2007. What’s Killing American Honey Bees? PLoS Biol 5(6): e168. doi: .

  • Pajuelo G. A., Torres C., , and Bermejo J. O. F.. 2008. Colony losses: a double blind trial on the influence of supplementary protein nutrition and preventative treatment with fumagillin against Nosema ceranae. Journal of Apicultural Research 47:8486.

    • Search Google Scholar
    • Export Citation
  • Richards K. W.1993. Non-Apis bees as crop pollinators. Revue Suisse de Zoologie 100:807822.

  • Rasmont P., Regali A., Ings T. C., Lognay G., Baudart E., Marlier M., Delcarte E., Viville P., Marot C., Falmagne P., Verhaeghe J.-C., , and Chittka L.. 2005. Analysis of pollen and nectar of Arbutus unedo as a food source for Bombus terrestris (Hymenoptera: Apidae). Journal of Economic Entomology 98:656663.

    • Search Google Scholar
    • Export Citation
  • Rinderer E. T., Kathleen E. D.. 1977. Worker honey bee response to infection with Nosema apis: Influence of diet. Journal of Economic Entomology 70:431433.

    • Search Google Scholar
    • Export Citation
  • Roulston T. H., Cane J. H., , and Buchmann S. L.. 2000. What governs protein content of pollen: pollinator preferences, pollen-pistil interactions, or phylogeny? Ecological Monographs 70:617643.

    • Search Google Scholar
    • Export Citation
  • Schmidt J. O.1984. Feeding preference of Apis mellifera L. (Hymenoptera: Apidae): individual versus mixed pollen species. Journal of Kansas Entomological Soceity 57:323327.

    • Search Google Scholar
    • Export Citation
  • Schmidt L. S., Schmidt J. O., Rao H., Wang W., , and Xu L.. 1995. Feeding preference of young worker honey bees (Hymenoptera: Apidae) fed rape, sesame, and sunflower pollen. Journal of Economical Entomology 88:15911595.

    • Search Google Scholar
    • Export Citation
  • Schmidt O. J., Thoenes C. S., , and Levin D. M.. 1987. Survival of honey bees, Apis mellifera (Hymenoptera: Apidae), fed various pollen sources. Annals of the Entomological Society of America 80:176183.

    • Search Google Scholar
    • Export Citation
  • Somerville D. C.2004. The floral resources of New South Wales of primary importance to commercial beekeeping. Ph.D. Dissertation, Australian National University. 255 pp.

    • Search Google Scholar
    • Export Citation
  • Somerville D. C., Nicol H. I.. 2006. Crude protein and amino acid composition of honey bee-collected pollen pellets from south-east Australia and a note on laboratory disparity. Australian Journal of Experimental Agriculture 46:141149.

    • Search Google Scholar
    • Export Citation
  • Stace, P. 1996. Protein content and amino acid profiles of honeybee-collected pollens. Bees ‘N trees Consultants. Lismore, New South Wales, Australia. http://www.honeybee.com.au/Library/Pollenindex.html, accessed 3/1/2012.

  • vanEngelsdorp D., Evans J. D., Saegerman C., Mullin C., Haubruge E., Nguyen B. K., Frazier M., , J. Frazier, Cox-Foster D., Chen Y., Underwood R., Tarpy D. R., , and Pettis J. S.. 2009. Colony collapse disorder: A descriptive study. PLoS ONE 4: e6481.

    • Search Google Scholar
    • Export Citation
  • Wahl O., Kurt U.. 1983. Influence of pollen feeding and physiological condition on pesticide sensitivity of the honeybee Apis mellifera carnica. Oecologia 59:106128.

    • Search Google Scholar
    • Export Citation
  • Weick J., Thorn R. S.. 2002. Effects of acute sublethal exposure to coumaphos or diazinon on acquisition and discrimination of odor stimuli in the honey bee Hymenoptera: Apidae). Journal of Economic Entomology 95:227236.

    • Search Google Scholar
    • Export Citation
  • Wilson W. T., Pettis J. S., Henderson C. E., , and Morse R. A., . 1997. Tracheal Mites. pp. 253-278. In, Morse R.A., Flottum K. (Editors). Honey Bee Pests, Predators, and Diseases. Third Edition. The A.I. Root Company. Medina, Ohio, USA. 718 pp.

    • Search Google Scholar
    • Export Citation
  • Yang X., Cox-Foster D. L.. 2005. Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. Proceedings of National Academy of Sciences USA 102:74707475.

    • Search Google Scholar
    • Export Citation
  • Zhang Y., Liu X., Zhang W., , and Han R.. 2010. Differential gene expression of the honey bees Apis mellifera and A. cerana induced by Varroa destructor infection. Journal of Insect Physiology 56:12071218.

    • Search Google Scholar
    • Export Citation

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