Hostname: page-component-76fb5796d-x4r87 Total loading time: 0 Render date: 2024-04-29T12:26:38.832Z Has data issue: false hasContentIssue false
  • English
  • Français

Diversity and nutritional value of pollen harvested by honey bee (Hymenoptera: Apidae) colonies during lowbush blueberry and cranberry (Ericaceae) pollination

Published online by Cambridge University Press:  26 May 2020

Claude Dufour Open the ORCID record for Claude Dufour [Opens in a new window] ,
Valérie Fournier  and
Pierre Giovenazzo
Claude Dufour*
Affiliation:
Département de biologie, Université Laval, 2325, rue de l’Université, Ville de Québec, Québec, G1V 0A6, Canada
Valérie Fournier
Affiliation:
Centre de recherche et innovation sur les végétaux, Université Laval, 2480, boulevard Hochelaga, Ville de Québec, Québec, G1V 0A6, Canada
Pierre Giovenazzo
Affiliation:
Département de biologie, Université Laval, 2325, rue de l’Université, Ville de Québec, Québec, G1V 0A6, Canada
*
*Corresponding author. Email: claude.dufour.5@ulaval.ca
Get access Rights & Permissions [Opens in a new window]

Abstract

The growth of the commercial pollination industry raises important concerns regarding honey bee (Apis mellifera Linnaeus; Hymenoptera: Apidae) health and development. While providing such services, honey bees are often exposed to undiversified pollen sources that may contribute to nutritional deficiencies, notably in protein and amino acids. To understand how honey bees are affected during provision of pollination services, we compared honey bee colonies that pollinated lowbush blueberry (Vaccinium angustifolium Aiton; Ericaceae) and/or cranberry (Vaccinium macrocarpon Aiton; Ericaceae) crops (management strategies) with control colonies in a diversified farmland environment. We identified the floral species of pollen collected by honey bee colonies in those crops compared to pollen collected by control colonies. We also analysed the protein and essential amino acid content of collected pollen and bee bread and measured the nutritional impact of pollination services on honey bee colonies. We found that honey bees providing blueberry and/or cranberry pollination services are exposed to a less diversified pollen diet than colonies located in a farmland environment, especially in a cranberry field. There was a significantly lower proportion of crude protein content in collected and stored pollen during provision of blueberry pollination services, which led to a smaller brood population. Many nutritional deficiencies were measured with regards to essential amino acids.

Type
Research Papers
Information
The Canadian Entomologist , Volume 152 , Issue 5 , October 2020 , pp. 622 - 645
Check for updates
Copyright
© The Author(s), 2020. Published by Cambridge University Press on behalf of The Entomological Society of Canada

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Subject editor: Shelley Hoover

References

Alaux, C., Ducloz, F., Crauser, D., and Le Conte, Y. 2010. Diet effects on honeybee immunocompetence. Biology Letters, 6: 562–565. https://doi.org/10.1098/rsbl.2009.0986.CrossRefGoogle ScholarPubMed
Beekman, M. and Ratnieks, F.L.W. 2000. Long-range foraging by the honey bee, Apis mellifera L. Functional Ecology, 14: 490–496.CrossRefGoogle Scholar
Bidlingmeyer, B.A., Cohen, S.A., Tarvin, T.L., and Frost, B. 1987. A new, rapid, high-sensitivity analysis of amino-acids in food type samples. Association of Official Analytical Chemists, 70: 241–247Google ScholarPubMed
Brodschneider, R. and Crailsheim, K. 2010. Nutrition and health in honey bees. Apidologie, 41: 278–294. https://doi.org/10.1051/apido/2010012.CrossRefGoogle Scholar
Chagnon, M. 2007. Gestion et aménagement des pollinisateurs de la canneberge : vers un rendement accru [online]. Available from www.agrireseau.net/apiculture/documents/cdaq%20canneberge%20rapport%20pollinisation%202007.pdf [accessed 23 March 2020].Google Scholar
Chagnon, M. 2008. Causes et effets du déclin mondial des pollinisateurs et les moyens d’y remédier [online]. Available from éhttps://www.agrireseau.net/apiculture/documents/Déclin%20poll_FR_MC3_M_Chagnon.pdf [accessed 23 March 2020].Google Scholar
Colwell, M.J., Williams, G.R., Evans, R.C., Shutler, D. 2017. Honey bee-collected pollen in agro-ecosystems reveals diet diversity, diet quality, and pesticide exposure. Ecology and Evolution, 7: 7243–7253. https://doi.org/10.1002/ece3.3178.CrossRefGoogle ScholarPubMed
Cook, S.M., Awmack, C.S., Murray, D.A., and Williams, I.H. 2003. Are honey bees’ foraging preferences affected by pollen amino acid composition? Ecological Entomology, 28: 622–627. https://doi.org/10.1046/j.1365-2311.2003.00548.x.CrossRefGoogle Scholar
Couvillon, M.J., Riddell Pearce, F.C., Accleton, C., Fensome, K.A., Quah, S.K.L., Taylor, E.L., and Ratnieks, F.L.W. 2014. Honey bee foraging distance depends on month and forage type. Apidologie, 46: 61–70. https://doi.org/10.1007/s13592-014-0302-5.CrossRefGoogle Scholar
Crailsheim, K., Schneider, L.H.W., Hrassnigg, N., Bühlmann, G., Brosch, U., Gmeinbauer, R., and 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. http://doi.org/10.1016/0022-1910(92)90117-V.CrossRefGoogle Scholar
Danner, N., Keller, A., Hartel, S., and Steffan-Dewenter, I. 2017. Honey bee foraging ecology: season but not landscape diversity shapes the amount and diversity of collected pollen. Public Library of Science One, 12: e0183716. http://doi.org/10.1371/journal.pone.0183716.Google Scholar
Darrach, M. and Page, S. 2016. Aperçu statistique de l’industrie apicole canadienne et contribution économique des services de pollinisation rendus par les abeilles domestiques, 2013–2014 [online]. Agriculture et Agroalimentaire Canada, Ottawa, Ontario, Canada. Available from www.honeycouncil.ca/images2/pdfs/HoneyReport_2014_FR.pdf [accessed 23 March 2020]Google Scholar
Davies, G.M. and Gray, A. 2015. Don’t let spurious accusations of pseudoreplication limit our ability to learn from natural experiments (and other messy kinds of ecological monitoring). Ecology and Evolution, 5: 5295–5304. http://doi.org/10.1002/ece3.1782.CrossRefGoogle Scholar
DeGrandi-Hoffman, G. and Chen, Y. 2015. Nutrition, immunity and viral infections in honey bees. Current Opinion in Insect Science, 10: 170–176. http://doi.org/10.1016/j.cois.2015.05.007.CrossRefGoogle ScholarPubMed
DeGrandi-Hoffman, G., Chen, Y., Rivera, R., Carroll, M., Chambers, M., Hidalgo, G., and Watkins de Jong, E. 2016. Honey bee colonies provided with natural forage have lower pathogen loads and higher overwinter survival than those fed protein supplements. Apidologie, 47: 186–196. http://doi.org/10.1007/s13592-015-0386-6.CrossRefGoogle Scholar
DeGrandi-Hoffman, G., Eckholm, B., and Huang, M. 2015. Methods for comparing nutrients in beebread made by Africanized and European honey bees and the effects on hemolymph protein titers. Journal of Visualized Experiments, e52448. http://doi.org/10.3791/52448.Google ScholarPubMed
De Groot, A.P. 1953. Protein and amino acid requirements of the honeybee (Apis mellifica L.). Physiologia Comparata et Oecologia, 3: 197–285.Google Scholar
Delaplane, K.S., van der Steen, J., and Guzman-Novoa, E. 2013. Standard methods for estimating strength parameters of Apis mellifera colonies. Journal of Apicultural Research, 52: 1–12.CrossRefGoogle Scholar
Dias, J.M.V.A., Morais, M.M., Francoy, T.M., Pereira, R.A., Turcatto, A.P., and Jong, D.D. 2018. Fermentation of a pollen substitute diet with beebread microorganisms increases diet consumption and hemolymph protein levels of honey bees (Hymenoptera, Apidae). Sociobiology, 65: 760–765. http://doi.org/10.13102/sociobiology.v65i4.3293.CrossRefGoogle Scholar
Di Pasquale, G., Alaux, C., Le Conte, Y., Odoux, J.-F., Pioz, M., Vaissière, B.E., et al. 2016. Variations in the availability of pollen resources affect honey bee health. Public Library of Science One, 11:e0162818. https://doi.org/10.1371/journal.pone.0162818.Google ScholarPubMed
Di Pasquale, G., Salignon, M., Le Conte, Y., Belzunces, L.P., Decourtye, A., Kretzschmar, A., et al. 2013. Influence of pollen nutrition on honey bee health: do pollen quality and diversity matter? Public Library of Science One, 8:e72016. https://doi.org/10.1371/journal.pone.0072016.Google ScholarPubMed
Donkersley, P., Rhodes, G., Pickup, R.W., Jones, K.C., Power, E.F., Wright, G.A., and Wilson, K. 2017. Nutritional composition of honey bee food stores vary with floral composition. Oecologia, 185: 749–761. http://doi.org/10.1007/s00442-017-3968-3.CrossRefGoogle ScholarPubMed
Donkersley, P., Rhodes, G., Pickup, R.W., Jones, K.C., and Wilson, K. 2014. Honeybee nutrition is linked to landscape composition. Ecology and Evolution, 4: 4195–4206. http://doi.org/10.1002/ece3.1293.CrossRefGoogle ScholarPubMed
Ferguson, J.A., Northfield, T.D., and Lach, L. 2018. Honey bee (Apis mellifera) pollen foraging reflects benefits dependent on individual infection status. Microbial Ecology, 76: 482–491. http://doi.org/10.1007/s00248-018-1147-7.CrossRefGoogle ScholarPubMed
Giovenazzo, P. and Dubreuil, P. 2011. Evaluation of spring organic treatments against Varroa destructor (Acari: Varroidae) in honey bee Apis mellifera (Hymenoptera: Apidae) colonies in eastern Canada. Experimental and Applied Acarology, 55: 65–76. http://doi.org/10.1007/s10493-011-9447-3.CrossRefGoogle ScholarPubMed
Girard, M., Chagnon, M., and Fournier, V. 2012. Pollen diversity collected by honey bees in the vicinity of Vaccinium spp. crops and its importance for colony development. Botany, 90: 545–555. http://doi.org/10.1139/b2012-049.CrossRefGoogle Scholar
Hendriksma, H.P. and Shafir, S. 2016. Honey bee foragers balance colony nutritional deficiencies. Behavioral Ecology and Sociobiology, 70: 509–517. http://doi.org/10.1007/s00265-016-2067-5.CrossRefGoogle Scholar
Herbert, E.W. and Hill, D.A. 2015. Honey bee nutrition. In The hive and the honey bee. Edited by Graham, J.M.. Dadant and Sons, Hamilton, Illinois, United States of America. Pp. 237–268.Google Scholar
Herbert, E.W. and Shimanuki, H. 1978. Chemical composition and nutritive-value of bee-collected and bee-stored pollen. Apidologie, 9: 33–40.CrossRefGoogle Scholar
Huang, Z. 2012. Pollen nutrition affects honey bee stress resistance. Terrestrial Arthropod Reviews, 5: 175–189. http://doi.org/10.1163/187498312x639568.CrossRefGoogle Scholar
Human, H. and Nicolson, S.W. 2006. Nutritional content of fresh, bee-collected and stored pollen of Aloe greatheadii var. davyana (Asphodelaceae). Phytochemistry, 67: 1486–1492. http://doi.org/10.1016/j.phytochem.2006.05.023.CrossRefGoogle Scholar
Hurlbert, S.H. 1984. Pseudoreplication and the design of ecological field experiments. Ecological Monographs, 54: 187–211.CrossRefGoogle Scholar
Institut de la statistique du Québec. 2018. Faits saillants de l’enquête sur l’apiculture au Québec - Campagne apicole 2017 [online]. Available from www.stat.gouv.qc.ca/statistiques/agriculture/apiculture-miel/FS_apicole17.pdf [accessed 23 March 2020].Google Scholar
Javorek, S.K., Mackenzie, K.E., and Kloet, S.P.V. 2002. Comparative pollination effectiveness among bees (Hymenoptera: Apoidea) on lowbush blueberry (Ericaceae: Vaccinium angustifolium). Annals of the Entomological Society of America, 95: 345–351. http://doi.org/10.1603/0013-8746(2002)095[0345:cpeabh]2.0.co;2.CrossRefGoogle Scholar
Keller, I., Fluri, P., and Imdorf, A. 2015. Pollen nutrition and colony development in honey bees: part 1. Bee World, 86: 3–10. http://doi.org/10.1080/0005772x.2005.11099641.CrossRefGoogle Scholar
Klein, A.-M., Vaissière, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A., Kremen, C., and Tscharntke, T. 2007. Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences, 274: 303–313. https://doi.org/10.1098/rspb.2006.3721.CrossRefGoogle Scholar
Kleinschmidt, G.J., Kondos, A.C., Harden, J., and Turner, J.W. 1974. Colony management for eucalypt honey flows. Australian Beekeeper, 75: 261–264.Google Scholar
Lamontagne-Drolet, M., Giovenazzo, P., and Fournier, V. 2019. The impacts of two protein supplements on commercial honey bee (Apis mellifera L.) colonies. Journal of Apicultural Research, 58: 800–813.CrossRefGoogle Scholar
Landry, J. and Delhaye, S. 1994. Determination of tryptophan in feedstuffs - comparison of sodium-hydroxide and barium hydroxide as hydrolysis agents. Food Chemistry, 49: 95–97. http://doi.org/10.1016/0308-8146(94)90238-0.CrossRefGoogle Scholar
Louveaux, J. 1958. Recherche sur la récolte du pollen par les abeilles (Apis mellifica L.). Ph.D. dissertation. Université de Paris, Paris, France. Available from www.apidologie.org/articles/apido/pdf/1958/04/Ann.Abeille_0044-8435_1958_1_4_ART0001.pdf [accessed 30 March 2020].CrossRefGoogle Scholar
Mattila, H.R. and Otis, G.W. 2006. Influence of pollen diet in spring on development of honey bee (Hymenoptera: Apidae) colonies. Journal of Economic Entomology, 99: 604–613. http://doi.org/10.1603/0022-0493-99.3.604.CrossRefGoogle ScholarPubMed
Maurizio, J., Louveaux, A., and Vorwohl, G. 1978. Les méthodes de la mélisso-palynologie. Apidologie, 1: 211–227.Google Scholar
McCaughey, W., Gilliam, M., and Standifer, L. 1980. Amino acids and protein adequacy for honey bees of pollens from desert plants and other floral sources. Apidologie, 11: 75–86.CrossRefGoogle Scholar
Moisan-De Serres, J., Bourgouin, F., and Lebeau, M.-O. 2014. Guide d’identification et de gestion - pollinisateurs et plantes mellifères. Centre de référence en agriculture et agroalimentaire du Québec, Québec, Canada.Google Scholar
Moore, P.D. and Webb, J.A. 1978. An illustrated guide to pollen analysis. Hodder and Stoughton, London, United Kingdom.Google Scholar
Naug, D. 2009. Nutritional stress due to habitat loss may explain recent honeybee colony collapses. Biological Conservation, 142: 2369–2372. http://doi.org/10.1016/j.biocon.2009.04.007.CrossRefGoogle Scholar
Nicolson, S.W. and Human, H. 2013. Chemical composition of the ‘low quality’ pollen of sunflower (Helianthus annuus, Asteraceae). Apidologie, 44: 144–152. http://doi.org/10.1007/s13592-012-0166-5.CrossRefGoogle Scholar
Pernal, S. and Currie, R. 2000. Pollen quality of fresh and 1-year-old single pollen diets for worker honey bees (Apis mellifera L.). Apidologie, 31: 387–409.CrossRefGoogle Scholar
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: 617–643. http://doi.org/10.1890/0012-9615(2000)070[0617:WGPCOP]2.0.CO;2.Google Scholar
SAS Institute. 2018. SAS quick start guide for students with visual impairments, version 2.7 9.4. SAS Institute, Cary, North Carolina, United States of America.Google Scholar
Schmidt, J.O. and Hanna, A. 2006. Chemical nature of phagostimulants in pollen attractive to honeybees. Journal of Insect Behavior, 19: 521–532. http://doi.org/10.1007/s10905-006-9039-y.CrossRefGoogle Scholar
Scofield, H.N. and Mattila, H.R. 2015. Honey bee workers that are pollen stressed as larvae become poor foragers and waggle dancers as adults. Public Library of Science One, 10: e0121731. http://doi.org/10.1371/journal.pone.0121731.Google ScholarPubMed
Simone-Finstrom, M., Li-Byarlay, H., Huang, M.H., Strand, M.K., Rueppell, O., and Tarpy, D.R. 2016. Migratory management and environmental conditions affect lifespan and oxidative stress in honey bees. Science Report, 6: 1–10. https://doi.org/10.1038/srep32023.CrossRefGoogle ScholarPubMed
Singh, R.P. and Singh, P.N. 1996. Amino acid and lipid spectra of larvae of honey bee (Apis cerana Fabr.) feeding on mustard pollen. Apidologie, 27: 21–28.CrossRefGoogle Scholar
Somerville, D.C. 2001. Nutritional value of bee collected pollens. Publication 01/047. Rural Industries Research and Development Corporation, New South Wales Agriculture, Goulburn, New South Wales, Australia.Google Scholar
Somerville, D.C. 2005. Fat bees skinny bees - a manual on honey bee nutrition for beekeepers. Rural Industries Research and Development Corporation, Goulburn, Australia.Google Scholar
Somerville, D.C. and 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: 141–149.CrossRefGoogle Scholar
Stabler, D., Power, E.F., Borland, A.M., Barnes, J.D., and Wright, G.A. 2018. A method for analysing small samples of floral pollen for free and protein-bound amino acids. Methods in Ecology and Evolution, 9: 430–438. http://doi.org/10.1111/2041-210X.12867.CrossRefGoogle ScholarPubMed
Stace, P. and White, E. 1994. The use of isoleucine as a supplement feed for honey bees (Apis mellifera) in Australia. Australian Beekeeper, 96: 159–161.Google Scholar
Standifer, L.N. 1967. A comparison of the protein quality of pollens for growth-stimulation of the hypopharyngeal glands and longevity of honey bees, Apis mellifera L. (Hymenoptera: Apidae). Insectes Sociaux, 14: 415–425. http://doi.org/10.1007/bf02223687.CrossRefGoogle Scholar
Standifer, L.N., McCaughey, W., Dixon, S., Gilliam, M., and Loper, G. 1980. Biochemistry and microbiology of pollen collected by honey bees (Apis mellifera L.) from almond, Prunus dulcis. II. Protein, amino acids and enzymes. Apidologie, 11: 163–171.CrossRefGoogle Scholar
Szczęsna, T. 2006. Long-chain fatty acids composition of honeybee-collected pollen. Journal of Apicultural Science, 50: 65–79.Google Scholar
Visscher, P.K. and Seeley, T.D. 1982. Foraging strategy of honeybee colonies in a temperate deciduous forest. Ecology, 63: 1790–1801. http://doi.org/10.2307/1940121.CrossRefGoogle Scholar
von Frisch, K. 2011. Vie et moeurs des abeilles. Albin Michel, Paris, France.Google Scholar
Winston, M.L. 1987. The biology of the honey bee. Harvard University Press, Cambridge, Massachusetts, United States of America.Google Scholar
Zarchin, S., Dag, A., Salomon, M., Hendriksma, H.P., and Shafir, S. 2017. Honey bees dance faster for pollen that complements colony essential fatty acid deficiency. Behavioral Ecology and Sociobiology, 71: 172 (171-111). http://doi.org/10.1007/s00265-017-2394-1.CrossRefGoogle Scholar