Pollen nutrition affects honey bee stress resistance

in Terrestrial Arthropod Reviews
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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.

Pollen nutrition affects honey bee stress resistance

in Terrestrial Arthropod Reviews



AlauxC.DuclozF.CrauserD. and Le ConteY.. 2010. Diet effects on honeybee immunocompetence. Biology Letters6:562565.

AlauxC.DantecC. H. Dantec ParrinelloY. and Le ConteY.. 2011. Nutrigenomics in honey bees: digital gene expression analysis of pollen’s nutritive effects on healthy and varroa-parasitized bees. BMC Genomics12:496.

AmdamG. V.SimoesZ. L. P.HagenA.NorbergK.SchroderK.MikkelsenO.KirkwoodT. B. L. and OmholtS. W.. 2004. Hormonal control of the yolk precursor vitellogenin regulates immune function and longevity in honeybees. Experimental Gerontology39:767773.

BarkerR. J.1977. Some carbohydrates found in pollen and pollen substitutes are toxic to honey bees. Journal of Nutrition107:18591862.

BrodschneiderR.CrailsheimK.. 2010. Nutrition and health in honey bees. Apidologie41: 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.

ChenY. P.EvansJ. D.SmithJ. B. and PettisJ. 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 Pathology97:186188.

CrailsheimK.1991. Interadult feeding of jelly in honeybee (Apis mellifera L.) colonies. Journal of Comparative Physiology B161:5560.

CrailsheimK.1992. The flow of jelly within a honeybee colony. Journal of Comparative Physiology B162:681689.

CremonezT. M.De JongD. and BitondiM. M. G.. 1998. Quantification of hemolymph proteins as a fast method for testing protein diets for honey bees (Hymenoptera: Apidae). Journal of Economic Entomology91:12841289.

De GrootA. P.1953. Protein and amino acid requirements of the honey bee (Apis mellifera L.). 3197285. Physiologia Comparata et Oecologia 3:197-285.

DeJongD.1997. Mites: varroa and other parasites of brood. pp. 279–328. InMorseR.A.FlottumK. (Editors). Honey Bee Pests Predators and Diseases. Third Edition. The A. I. Root Company. Medina, Ohio, USA. 718 pp.

De JongD.Junqueira da SilvaE.KevanG. P. and AtkinsonL. J.. 2009. Pollen substitutes increase honey bee haemolymph protein levels as much as or more than does pollen. Journal of Apicultural Research48:3437.

DeGrandi-HoffmanG.WardellG.Ahumada-SeguraF.RindererT.DankaR. and PettisJ.. 2008. Comparisons of pollen substitute diets for honey bees: consumption rates by colonies and effects on brood and adult populations. Journal of apicultural research47:265270.

DeGrandi-HoffmanG.ChenY.HuangE. and HuangM. 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 Physiology56:11841191.

EischenF. A.GrahamR. H.. 2008. Feeding overwintering honey bee colonies infected with Nosema ceranae. American Bee Journal148:555.

EischenF. A.GrahamjR. H. and RiverajR.. 2008. Overwintering nutritionally stressed honey bee colonies infested with Varroa destructor. American Bee Journal148: 555556.

FluriP.LüscherM.WilleH. and GerigL.. 1982. Changes in weight of the pharyngeal gland and haemolymph titres of juvenile hormone and vitellogenin in worker honeybees. Journal of Insect Physiology28:6168.

GallaiN.SallesJ.SetteleJ. and VaissièreB. E.. 2009. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics68:81021.

GenerschE.von der OheW.KaatzH.SchroederA.OttenC.BüchlerR.BergS.RitterW.MülhenW.GisderS.MeixnerM.LiebigG. and RosenkranzP.. 2010. The German Bee Monitoring Project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie41:332352.

GregoryP. G.2006. Protein diets and their effects on worker weight, longevity, consumption and haemolymph protein levels of Apis mellifera. American Bee Journal146:447.

Guzmán-NovoaE.EcclesL.CalveteY.McGowanJ.KellyP. and Correa-BenitezA.. 2010. Varroa destructor is the main culprit for death and reduced populations of overwintered honey bees in Ontario, Canada. Apidologie4:443451.

HaydakM. H.1967. Bee nutrition and pollen substitutes. Apiacta1:38.

HaydakM. H.1970. Honey bee nutrition. Annual Review of Entomology.15:143156.

HerbertW. E. J.ShimanukiH.. 1982. Effect of population density and available diet on the rate of brood rearing by honey bees offered a pollen substitute. Apidologie13:2128.

HerbertW. E. J.ShimanukiH. and ShashaS. B.. 1980. Brood rearing and food consumption by honeybee colonies fed pollen substitutes supplemented with starch-encapsulated pollen extracts. Journal of Apicultural Research:115118.

HigesMMartín-HernándezR.BotíasC.BailónE. G.González-PortoA.V.BarriosL.Del NozalM. J.BernalJ. L.JiménezJ. J.PalenciaP. G. and MeanaA.. 2008How natural infection by Nosema ceranae causes honeybee colony collapse. Environmental Microbiology10:26592669.

HuangZ. Y.2008. The colony collapse disorder crisis for honey bees. pp. 15-18. In CullenC. (Editor). Encyclopedia of Life Science. Volume I. Infobase Publishing. New York, NY, USA. 401 pp.

HuangZ. Y.2010. Bees worth a billion $ in Michigan. http://bees.msu.edu/2010/03/bees-worth-a-billion-in-michigan/. Visited March 16 2012.

HuangZ.-Y.OtisG. W. and TealP. E. A.. 1989. Nature of brood signal activating the protein synthesis of hypopharyngeal gland in honey bees, Apis mellifera (Apidae: Hymenoptera). Apidologie20:455464.

IqbalJ.MuellerU.. 2007. Virus infection causes specific learning deficits in honeybee foragers. Royal Soceity Proceedings of Biological Sciences274:15171521.

JanmaatA. F.WinstonM. L.. 2000. Removal of Varroa jacobsoni infested brood in honey bee colonies with different pollen stores. Apidologie31:377385.

KellerI.FluriP. and ImdorfA.. 2005. Pollen nutrition and colony development in honey bees-Part 2. Bee World86:2734.

KleinschmidtG.KondosA.. 1976. The influence of crude protein levels on colony production. The Australasian Beekeeper78:3639.

KleinschmidtG.KondosA.. 1977. The effect of dietary protein on colony performance. pp. 357-361. InMeletinovC. (Editor) Proceedings of the 26th International Apicultural Congress Oct 13-19 1977. Apimondia Bucharest. 615 pp.

KnoxD. A.ShimanukiH. and HerbertE. W.. 1971. Diet and the longevity of adult honey bees. Journal of Economic Entomology64:14151416.

KraljJ.FuchsS.. 2010. Nosema sp. influences flight behavior of infected honey bee (Apis mellifera) foragers. Apidologie41:2128.

KraljJ.BrockmannA.FuchsS. and TautzJ.. 2007. The parasitic mite Varroa destructor affects non-associative learning in honey bee foragers, Apis mellifera L. Journal of Comparative Physiology A193:363370.

ManningR.RutkayA.. 2007. Lipid-enhanced pollen and lipid-reduced flour diets and their effect on the longevity of honey bees (Apis mellifera L.). Australian Journal of Entomology46:251257.

MattilaH. R.OtisG. W.. 2006. Influence of pollen diet in spring on development of honey bee (Hymenoptera: Apidae) colonies. Journal of Economic Entomology99:604613.

MattilaH. R.OtisbG. 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 Entomology35:708717.

MaurizioA.1950. The influence of pollen feeding and brood rearing on the length of life and physiological conditions of the honeybee. Bee World31:912.

MorimotoT.KojimaY.TokiT.KomedaY.YoshiyamaM.KimuraK.NirasawaK. and KadowakiT.. 2011. The habitat disruption induces immune-suppression and oxidative stress in honey bees. Ecology and Evolution1:201217.

MorseR. A.CalderoneN. W.. 2000. The value of honey bees as pollinators of U.S. crops in 2000. Bee Culture128:215.

NaugD.2009. Nutritional stress due to habitat loss may explain recent honeybee colony collapses. Biological Conservation142: 23692372.

NeumannP.ElzenP. J.. 2004. The biology of the small hive beetle (Aethina tumida, Coleoptera: Nitidulidae): Gaps in our knowledge of an invasive species. Apidologie35:229247.

NeupaneK. R.ThapaR. B.. 2005. Alternative to Off-Season Sugar Supplement Feeding of Honeybees. Journal of the Institute of Agriculture and Animal Science26:7778.

OldroydB.P.2007. What’s Killing American Honey Bees?PLoS Biol5(6): e168. doi: .

PajueloG. A.TorresC. and BermejoJ. 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 Research47:8486.

RichardsK. W.1993. Non-Apis bees as crop pollinators. Revue Suisse de Zoologie100:807822.

RasmontP.RegaliA.IngsT. C.LognayG.BaudartE.MarlierM.DelcarteE.VivilleP.MarotC.FalmagneP.VerhaegheJ.-C. and ChittkaL.. 2005. Analysis of pollen and nectar of Arbutus unedo as a food source for Bombus terrestris (Hymenoptera: Apidae). Journal of Economic Entomology98:656663.

RindererE. T.KathleenE. D.. 1977. Worker honey bee response to infection with Nosema apis: Influence of diet. Journal of Economic Entomology70:431433.

RoulstonT. H.CaneJ. H. and BuchmannS. L.. 2000. What governs protein content of pollen: pollinator preferences, pollen-pistil interactions, or phylogeny?Ecological Monographs70:617643.

SchmidtJ. O.1984. Feeding preference of Apis mellifera L. (Hymenoptera: Apidae): individual versus mixed pollen species. Journal of Kansas Entomological Soceity57:323327.

SchmidtL. S.SchmidtJ. O.RaoH.WangW. and XuL.. 1995. Feeding preference of young worker honey bees (Hymenoptera: Apidae) fed rape, sesame, and sunflower pollen. Journal of Economical Entomology88:15911595.

SchmidtO. J.ThoenesC. S. and LevinD. M.. 1987. Survival of honey bees, Apis mellifera (Hymenoptera: Apidae), fed various pollen sources. Annals of the Entomological Society of America80:176183.

SomervilleD. C.2004. The floral resources of New South Wales of primary importance to commercial beekeeping. Ph.D. Dissertation Australian National University. 255 pp.

SomervilleD. C.NicolH. 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 Agriculture46:141149.

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.

vanEngelsdorpD.EvansJ. D.SaegermanC.MullinC.HaubrugeE.NguyenB. K.FrazierM. J. Frazier Cox-FosterD.ChenY.UnderwoodR.TarpyD. R. and PettisJ. S.. 2009. Colony collapse disorder: A descriptive study. PLoS ONE4: e6481.

WahlO.KurtU.. 1983. Influence of pollen feeding and physiological condition on pesticide sensitivity of the honeybee Apis mellifera carnica. Oecologia59:106128.

WeickJ.ThornR. 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 Entomology95:227236.

WilsonW. T.PettisJ. S.HendersonC. E. and MorseR. A.. 1997. Tracheal Mites. pp. 253-278. InMorseR.A.FlottumK. (Editors). Honey Bee Pests Predators and Diseases. Third Edition. The A.I. Root Company. Medina, Ohio, USA. 718 pp.

YangX.Cox-FosterD. 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 USA102:74707475.

ZhangY.LiuX.ZhangW. and HanR.. 2010. Differential gene expression of the honey bees Apis mellifera and A. cerana induced by Varroa destructor infection. Journal of Insect Physiology56:12071218.


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    A worker honey bee collecting pollen from a spiderwort (Tradescantia virginiana L., Commelinaceae), a commonly cultivated garden flower. Photo by Zachary Huang.

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    Proportion (%) of the 10 essential amino acids needed by honey bees (after De Groot, 1953).

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    Longevity (days ± SE) of caged worker bees that were fed with pollen, without pollen, and then either infected with Nosema apis (black) or not infected as a control (grey) (data from Rinderer and Kathleen, 1977, Table 1, Experiment 1). Bars with different letters were significantly different (P<0.05) by LSD after ANOVA.

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    Survival of caged honey bee workers that were fed with pollen (black), or without (blue), and then infected with Nosema ceranae (solid lines), or not infected with Nosema ceranae (broken lines) (Z.Y. Huang, unpublished data).

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    Correlation between honey bee colony numbers (millions, solid circles) and areas of rangeland (million km2, open circles) (modified from Naug, 2010).

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