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Pollen nutrition affects honey bee stress resistance

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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.

Affiliations: 1: Department of Entomology, Michigan State University, East Lansing, Michigan 48824, USA,


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1. Alaux C. , Ducloz F. , Crauser D. ,, and Le Conte Y. . 2010. "Diet effects on honeybee immunocompetence". Biology Letters Vol 6: 562565.
2. 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 Vol 12: 496.
3. 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 Vol 39: 767773.
4. Barker R. J. 1977. "Some carbohydrates found in pollen and pollen substitutes are toxic to honey bees". Journal of Nutrition Vol 107: 18591862.
5. Brodschneider R. , Crailsheim K. . 2010. "Nutrition and health in honey bees". Apidologie Vol 41: 278294.
6. 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.
7. Chen Y. P. , Evans J. D. , Smith J. B. ,, and Pettis J. S. . 2008. " Nosema ceranaeis a long-present and wide-spread microsporidian infection of the European honey bee ( Apis mellifera) in the United States". Journal of Invertebrate Pathology Vol 97: 186188.
8. Crailsheim K. 1991. "Interadult feeding of jelly in honeybee ( Apis melliferaL.) colonies". Journal of Comparative Physiology B Vol 161: 5560.
9. Crailsheim K. 1992. "The flow of jelly within a honeybee colony". Journal of Comparative Physiology B Vol 162: 681689.
10. 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 Vol 91: 12841289.
11. De Groot A. P. 1953. Protein and amino acid requirements of the honey bee ( Apis melliferaL.)., Vol 3, 197285. Physiologia Comparata et Oecologia3:197-285.
12. 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. 718pp.
13. 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 Vol 48: 3437.
14. 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 Vol 47: 265270.
15. 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 melliferaL.)". Journal of Insect Physiology Vol 56: 11841191.
16. Eischen F. A. , Graham R. H. . 2008. "Feeding overwintering honey bee colonies infected with Nosema ceranae ". American Bee Journal Vol 148: 555.
17. Eischen F. A. , Grahamj R. H. ,, and Riveraj R. . 2008. "Overwintering nutritionally stressed honey bee colonies infested with Varroa destructor ". American Bee Journal Vol 148: 555556.
18. 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 Vol 28: 6168.
19. 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 Vol 68: 81021.
20. 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 Vol 41: 332352.
21. Gregory P. G. 2006. "Protein diets and their effects on worker weight, longevity, consumption and haemolymph protein levels of Apis mellifera ". American Bee Journal Vol 146: 447.
22. Guzmán-Novoa E. , Eccles L. , Calvete Y. , McGowan J. , Kelly P. ,, and Correa-Benitez A. . 2010. " Varroa destructoris the main culprit for death and reduced populations of overwintered honey bees in Ontario, Canada". Apidologie Vol 4: 443451.
23. Haydak M. H. 1967. "Bee nutrition and pollen substitutes". Apiacta Vol 1: 38.
24. Haydak M. H. 1970. "Honey bee nutrition". Annual Review of Entomology. Vol 15: 143156.
25. 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 Vol 13: 2128.
26. 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.
27. 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 ceranaecauses honeybee colony collapse". Environmental Microbiology Vol 10: 26592669.
28. Huang Z. Y. , 2008. "The colony collapse disorder crisis for honey bees". pp. 15-18. In, Cullen C. (Editor). Encyclopedia of Life Science. Volume Vol I. Infobase Publishing. New York, NY, USA. 401pp.
29. Huang Z. Y. 2010. "Bees worth a billion $ in Michigan". . Visited March 16, 2012.
30. 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 Vol 20: 455464.
31. Iqbal J. , Mueller U. . 2007. "Virus infection causes specific learning deficits in honeybee foragers". Royal Soceity Proceedings of Biological Sciences Vol 274: 15171521.
32. Janmaat A. F. , Winston M. L. . 2000. "Removal of Varroa jacobsoniinfested brood in honey bee colonies with different pollen stores". Apidologie Vol 31: 377385.
33. Keller I. , Fluri P. ,, and Imdorf A. . 2005. "Pollen nutrition and colony development in honey bees-Part 2". Bee World Vol 86: 2734.
34. Kleinschmidt G. , Kondos A. . 1976. "The influence of crude protein levels on colony production". The Australasian Beekeeper Vol 78: 3639.
35. 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. 615pp.
36. Knox D. A. , Shimanuki H. ,, and Herbert E. W. . 1971. "Diet and the longevity of adult honey bees". Journal of Economic Entomology Vol 64: 14151416.
37. Kralj J. , Fuchs S. . 2010. " Nosemasp. influences flight behavior of infected honey bee ( Apis mellifera) foragers". Apidologie Vol 41: 2128.
38. Kralj J. , Brockmann A. , Fuchs S. ,, and Tautz J. . 2007. "The parasitic mite Varroa destructoraffects non-associative learning in honey bee foragers, Apis melliferaL". Journal of Comparative Physiology A Vol 193: 363370.
39. Manning R. , Rutkay A. . 2007. "Lipid-enhanced pollen and lipid-reduced flour diets and their effect on the longevity of honey bees ( Apis melliferaL.)". Australian Journal of Entomology Vol 46: 251257.
40. 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 Vol 99: 604613.
41. 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 Vol 35: 708717.
42. Maurizio A. 1950. "The influence of pollen feeding and brood rearing on the length of life and physiological conditions of the honeybee". Bee World Vol 31: 912.
43. 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 Vol 1: 201217.
44. Morse R. A. , Calderone N. W. . 2000. "The value of honey bees as pollinators of U.S. crops in 2000". Bee Culture Vol 128: 215.
45. Naug D. 2009. "Nutritional stress due to habitat loss may explain recent honeybee colony collapses". Biological Conservation Vol 142: 23692372.
46. 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 Vol 35: 229247.
47. 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 Vol 26: 7778.
48. Oldroyd B.P. 2007. "What’s Killing American Honey Bees?" PLoS Biol Vol 5( 6): e168. doi: 10.1371/journal.pbio.0050168.
49. 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 Vol 47: 8486.
50. Richards K. W. 1993. "Non- Apisbees as crop pollinators". Revue Suisse de Zoologie Vol 100: 807822.
51. 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 unedoas a food source for Bombus terrestris(Hymenoptera: Apidae)". Journal of Economic Entomology Vol 98: 656663.
52. Rinderer E. T. , Kathleen E. D. . 1977. "Worker honey bee response to infection with Nosema apis: Influence of diet". Journal of Economic Entomology Vol 70: 431433.
53. 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 Vol 70: 617643.
54. Schmidt J. O. 1984. "Feeding preference of Apis melliferaL. (Hymenoptera: Apidae): individual versus mixed pollen species". Journal of Kansas Entomological Soceity Vol 57: 323327.
55. 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 Vol 88: 15911595.
56. 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 Vol 80: 176183.
57. 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.
58. 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 Vol 46: 141149.
59. Stace, P. 1996. Protein content and amino acid profiles of honeybee-collected pollens. Bees ‘N trees Consultants. Lismore, New South Wales, Australia. .
60. 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 Vol 4: e6481.
61. Wahl O. , Kurt U. . 1983. "Influence of pollen feeding and physiological condition on pesticide sensitivity of the honeybee Apis mellifera carnica ". Oecologia Vol 59: 106128.
62. 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 Vol 95: 227236.
63. 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. 718pp.
64. 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 Vol 102: 74707475.
65. Zhang Y. , Liu X. , Zhang W. ,, and Han R. . 2010. "Differential gene expression of the honey bees Apis melliferaand A. ceranainduced by Varroa destructorinfection". Journal of Insect Physiology Vol 56: 12071218.

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