The perils of forcing a generalist to be a specialist: lack of dietary essential amino acids impacts honey bee pollen foraging and colony growth

References

• Abou-Shaara, H. F. (2012). Notes on water collection by honey bees. Bee World, 89(4), 86–87. doi:10.1080/0005772X.2012.11417501
   Google Scholar
• Abou-Shaara, H. F. (2014). The foraging behaviour of honey bees, Apis mellifera: A review. Veterinární Medicína, 59(No. 1), 1–10. doi:10.17221/7240-VETMED
   Web of Science ®Google Scholar
• Alaux, C., Ducloz, F., Crauser, D., & Le Conte, Y. (2010). Diet effects on honeybee immunocompetence. Biology Letters, 6(4), 562–565. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/20089536 doi:10.1098/rsbl.2009.0986
   PubMed Web of Science ®Google Scholar
• Anderson, K. E., Carroll, M. J., Sheehan, T., Lanan, M. C., Mott, B. M., Maes, P., & Corby-Harris, V. (2014). Hive-stored pollen of honey bees: Many lines of evidence are consistent with pollen preservation, not nutrient conversion. Molecular Ecology, 23(23), 5904–5917. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/25319366 doi:10.1111/mec.12966
   PubMed Web of Science ®Google Scholar
• Arien, Y., Dag, A., Zarchin, S., Masci, T., & Shafir, S. (2015). Omega-3 deficiency impairs honey bee learning. Proceedings of the National Academy of Sciences of the United States of America, 112(51), 15761–15766. doi:10.1073/pnas.1517375112 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/26644556
   Google Scholar
• Auclair, J. L., & Jamieson, C. A. (1948). A qualitative analysis of amino acids in pollen collected by bees. Science (New York, N.Y.), 108(2805), 357–358. Retrieved from http://www.jstor.org/stable/1677287 doi:10.1126/science.108.2805.357
   PubMed Web of Science ®Google Scholar
• Beekeeping, K. (2019). Sundance pollen trap: Assembly and usage instructions. Clarkson, KY: Kelley Beekeeping.
   Google Scholar
• Beekman, M., & Ratnieks, F. L. W. (2000). Long-range foraging by the honey-bee, Apis mellifera L. Functional Ecology, 14(4), 490–496. doi:10.1046/j.1365-2435.2000.00443.x
   Web of Science ®Google Scholar
• Bordier, C., Dechatre, H., Suchail, S., Peruzzi, M., Soubeyrand, S., Pioz, M., … Alaux, C. (2017). Colony adaptive response to simulated heat waves and consequences at the individual level in honeybees (Apis mellifera). Scientific Reports, 7(1), 3760. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/28630407 doi:10.1038/s41598-017-03944-x
   PubMed Web of Science ®Google Scholar
• Brodschneider, R., & Crailsheim, K. (2010). Nutrition and health in honey bees. Apidologie, 41(3), 278–294. doi:10.1051/apido/2010012
   Web of Science ®Google Scholar
• Camazine, S. (1993). The regulation of pollen foraging by honey bees: How foragers assess the colony's need for pollen. Behavioral Ecology and Sociobiology, 32(4), 265–272. Retrieved from doi:10.1007/BF00166516
   Web of Science ®Google Scholar
• DeGroot, A. P. (1953). Protein and the amino acid requirements of the honey bee (Apis Mellifica L.). Paper Presented at the 67th Communication of the Research Institute of Animal Husbandry April 26, 1953. The Hague, Netherlands: Netherlands Organization for Applied Scientific Research.
   Google Scholar
• Delaplane, K. S., Dag, A., Danka, R. G., Freitas, B. M., Garibaldi, L. A., Goodwin, R. M., & Hormaza, J. I. (2013). Standard methods for estimating strength parameters of Apis mellifera colonies. Journal of Apicultural Research, 52(4), 1–12. doi:10.3896/IBRA/1.52.1.03
   Web of Science ®Google Scholar
• Donkersley, P., Rhodes, G., Pickup, R. W., Jones, K. C., Power, E. F., Wright, G. A., & Wilson, K. (2017). Nutritional composition of honey bee food stores vary with floral composition. Oecologia, 185(4), 749. Retrieved from doi:10.1007/s00442-017-3968-3
   PubMed Web of Science ®Google Scholar
• Dreller, C., Page, R. E., Jr., & Fondrk, M. K. (1999). Regulation of pollen foraging in honeybee colonies: Effects of young brood, stored pollen, and empty space. Behavioral Ecology and Sociobiology, 45(3–4), 227–233. Retrieved from doi:10.1007/s002650050557
   Web of Science ®Google Scholar
• Fefferman, N. H., & Starks, P. T. (2006). A modeling approach to swarming in honey bees (Apis mellifera). Insectes Sociaux, 53(1), 37–45. doi:10.1007/s00040-005-0833-x
   Web of Science ®Google Scholar
• Feltham, H., Park, K., Minderman, J., & Goulson, D. (2015). Experimental evidence that wildflower strips increase pollinator visits to crops. Ecology and Evolution, 5(16), 3523–3530. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/26380683 doi:10.1002/ece3.1444
   PubMed Web of Science ®Google Scholar
• Goulson, D., Lye, G. C., & Darvill, B. (2008). Decline and conservation of bumble bees. Annual Review of Entomology, 53(1), 191–208. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/17803456 doi:10.1146/annurev.ento.53.103106.093454
   PubMed Web of Science ®Google Scholar
• Haaland, C., Naisbit, R. E., & Bersier, L.-F. (2011). Sown wildflower strips for insect conservation: A review. Insect Conservation and Diversity, 4(1), 60–80. doi:10.1111/j.1752-4598.2010.00098.x
   Web of Science ®Google Scholar
• Haydak, M. H. (1970). Honey bee nutrition. Annual Review of Entomology, 15(1), 143–156. doi:10.1146/annurev.en.15.010170.001043
   Web of Science ®Google Scholar
• Hendriksma, H. P., & Shafir, S. (2016). Honey bee foragers balance colony nutritional deficiencies. Behavioral Ecology and Sociobiology, 70, 1–9. Retrieved from doi:10.1007/s00265-016-2067-5
   Web of Science ®Google Scholar
• Herbert, E. W. J., & Hill, D. A. (2015). Honey bee nutrition. In J. M. Graham (Ed.), The hive and the honey bee (Extensively Revised ed., pp. 237–268). Hamilton, IL: Dadant & Sons, Inc.
   Google Scholar
• Herbert, E. W. J., & Shimanuki, H. (1978). Mineral requirements for brood-rearing by honeybees fed a synthetic diet. Journal of Apicultural Research, 17(3), 118–122. doi:10.1080/00218839.1978.11099916
   Web of Science ®Google Scholar
• Imdorf, A., Rickli, M., Kilchenmann, V., Bogdanov, S., & Wille, H. (1998). Nitrogen and mineral constituents of honey bee worker brood during pollen shortage. Apidologie, 29(4), 315–325. doi:10.1051/apido:19980402
   Web of Science ®Google Scholar
• Klatt, B. K., Holzschuh, A., Westphal, C., Clough, Y., Smit, I., Pawelzik, E., & Tscharntke, T. (2014). Bee pollination improves crop quality, shelf life and commercial value. Proceedings of the Royal Society B: Biological Sciences, 281(1775). doi:10.1098/rspb.2013.2440
   PubMed Web of Science ®Google Scholar
• Klein, A.-M., Vaissière, B. E., Cane, J. H., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C., & Tscharntke, T. (2007). Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences, 274(1608), 303–313. Retrieved from http://rspb.royalsocietypublishing.org/royprsb/274/1608/303.full.pdf doi:10.1098/rspb.2006.3721
   PubMed Web of Science ®Google Scholar
• Li, X. A., Huang, C., & Xue, Y. (2013). Contribution of lipids in honeybee (Apis mellifera) royal jelly to health. Journal of Medicinal Food, 16(2), 96–102. doi:10.1089/jmf.2012.2425
   PubMed Web of Science ®Google Scholar
• Loper, G. M., & Cohen, A. C. (1987). Amino acid content of dandelion pollen, a honey bee (Hymenoptera: Apidae) nutritional evaluation. Journal of Economic Entomology, 80(1), 14–17. Retrieved from doi:10.1093/jee/80.1.14
   Web of Science ®Google Scholar
• Maxfield-Taylor, S. A., Mujic, A. B., & Rao, S. (2015). First detection of the larval chalkbrood disease pathogen Ascosphaera apis (Ascomycota: Eurotiomycetes: Ascosphaerales) in adult bumble bees. PLoS One, 10(4), e0124868. Retrieved from http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4401763/ doi:10.1371/journal.pone.0124868
   PubMed Web of Science ®Google Scholar
• Millius, S. (Producer). (2017). The mystery of vanishing honeybees is still not definitively solved. ScienceNews. Retrieved from https://www.sciencenews.org/article/mystery-vanishing-honeybees-still-not-definitively-solved
   Google Scholar
• National Bee Unit (2018). Hive cleaning and sterilization. In National Bee Unit (Ed.), APHA, National Agri-Food innovation campus. Sand Hutton, York: Animal and Plant Health Agency.
   Google Scholar
• Nicolson, S. W., & Human, H. (2013). Chemical composition of the ‘low quality’ pollen of sunflower (Helianthus annuus, Asteraceae). Apidologie, 44(2), 144–152. doi:10.1007/s13592-012-0166-5
   Web of Science ®Google Scholar
• Pernal, S. F., & Currie, R. W. (2001). The influence of pollen quality on foraging behavior in honeybees (Apis mellifera L.). Behavioral Ecology and Sociobiology, 51(1), 53–68. Retrieved from doi:10.1007/s002650100412
   Web of Science ®Google Scholar
• Phillips, B. B., Shaw, R. F., Holland, M. J., Fry, E. L., Bardgett, R. D., Bullock, J. M., & Osborne, J. L. (2018). Drought reduces floral resources for pollinators. Global Change Biology, 24(7), 3226–3235. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/29652102 doi:10.1111/gcb.14130
   PubMed Web of Science ®Google Scholar
• Potts, S. G., Biesmeijer, J. C., Kremen, C., Neumann, P., Schweiger, O., & Kunin, W. E. (2010). Global pollinator declines: Trends, impacts and drivers. Trends in Ecology & Evolution, 25(6), 345–353. Retrieved from http://www.sciencedirect.com/science/article/pii/S0169534710000364 doi:10.1016/j.tree.2010.01.007
   PubMed Web of Science ®Google Scholar
• Potts, S. G., Roberts, S. P. M., Dean, R., Marris, G., Brown, M. A., Jones, R., … Settele, J. (2010). Declines of managed honey bees and beekeepers in Europe. Journal of Apicultural Research, 49(1), 15–22. doi:10.3896/IBRA.1.49.1.02
   Web of Science ®Google Scholar
• Pywell, R. F., Heard, M. S., Woodcock, B. A., Hinsley, S., Ridding, L., Nowakowski, M., & Bullock, J. M. (2015). Wildlife-friendly farming increases crop yield: Evidence for ecological intensification. Proceedings of the Royal Society B, 282(1816) doi:10.1098/rspb.2015.1740 Retrieved from < Go to ISI>://MEDLINE:26423846 http://rspb.royalsocietypublishing.org/content/royprsb/282/1816/20151740.full.pdf
   Google Scholar
• R Development Core Team (2008). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
   Google Scholar
• Rader, R., Bartomeus, I., Garibaldi, L. A., Garratt, M. P., Howlett, B. G., Winfree, R., … Woyciechowski, M. (2016). Non-bee insects are important contributors to global crop pollination. Proceedings of the National Academy of Sciences of the United States of America, 113(1), 146–151. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/26621730 doi:10.1073/pnas.1517092112
   Web of Science ®Google Scholar
• Richardson, L. L., Bowers, M. D., & Irwin, R. E. (2016). Nectar chemistry mediates the behavior of parasitized bees: Consequences for plant fitness. Ecology, 97(2), 325–337. doi:10.1890/15-0263.1
   PubMed Web of Science ®Google Scholar
• Robinson, F. A., & Oertel, E. (1975). Sources of Nectar and Pollen. In D. Sons (Ed.), The hive and the honey bee (pp. 283–302). Hamilton, IL: Dadant & Sons.
   Google Scholar
• Rosov, S. A. (1944). Food consumption by bees. Bee World, 25(12), 94–95. doi:10.1080/0005772X.1944.11094302
   Google Scholar
• Roulston, T. H., & Cane, J. H. (2000). Pollen nutritional content and digestibility for animals. Plant Systematics and Evolution, 222(1–4), 187–209. Retrieved from doi:10.1007/BF00984102
   Web of Science ®Google Scholar
• Schmickl, T., & Crailsheim, K. (2001). Cannibalism and early capping: Strategy of honeybee colonies in times of experimental pollen shortages. Journal of Comparative Physiology A, 187(7), 541–547. Retrieved from doi:10.1007/s003590100226
   PubMed Web of Science ®Google Scholar
• Seitz, N., Traynor, K. S., Steinhauer, N., Rennich, K., Wilson, M. E., Ellis, J. D., … vanEngelsdorp, D. (2016). A national survey of managed honey bee 2014–2015 annual colony losses in the USA. Journal of Apicultural Research, 54, 292–304. doi:10.1080/00218839.2016.1153294
   Web of Science ®Google Scholar
• Somerville, D. (2001). Nutritional value of bee collected pollens. In A. Somerville (Ed.), A report for the rural industries research and development corporation. Goldburn, Australia: NSW Agriculture.
   Google Scholar
• Standifer, L. N., Mccaughey, W. F., Dixon, S. E., Gilliam, M., & Loper, G. M. (1980). Biochemistry and microbiology of pollen collected by honey bees (Apis mellifera L.) from almond, Prunus dulcis II. Protein, amino acids and enzymes (1). Apidologie, 11(2), 163–171. doi:10.1051/apido:19800206
   Web of Science ®Google Scholar
• Steffan-Dewenter, I., & Kuhn, A. (2003). Honeybee foraging in differentially structured landscapes. Proceedings of the Royal Society B, 270(1515), 569–575. doi:10.1098/rspb.2002.2292 Retrieved from < Go to ISI>://WOS:000181769800003 http://rspb.royalsocietypublishing.org/content/royprsb/270/1515/569.full.pdf
   PubMed Web of Science ®Google Scholar
• Szymas, B., & Jedruszuk, A. (2003). The influence of different diets on haemocytes of adult worker honey bees, Apis mellifera. Apidologie, 34(2), 97–102. doi:10.1051/apido:2003012
   Web of Science ®Google Scholar
• The National Drought Mitigation Center, United States Department of Agriculture, & National Oceanic and Atmospheric Administration (2018). United States drought monitor. Retrieved from http://droughtmonitor.unl.edu/.
   Google Scholar
• Todd, F. E., & Bishop, R. K. (1940). Trapping honeybee-gathered pollen and factors affecting yields. Journal of Economic Entomology, 33(6), 866–870. doi:10.1093/jee/33.6.866
   Google Scholar
• van Engelsdorp, D., Hayes, J., Jr., Underwood, R. M., & Pettis, J. (2008). A survey of honey bee colony losses in the U.S., fall 2007 to spring 2008. PLoS One, 3(12), e4071. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/19115015 doi:10.1371/journal.pone.0004071
   PubMed Web of Science ®Google Scholar
• Vaudo, A. D., Patch, H. M., Mortensen, D. A., Tooker, J. F., & Grozinger, C. M. (2016). Macronutrient ratios in pollen shape bumble bee (Bombus impatiens) foraging strategies and floral preferences. Proceedings of the National Academy of Sciences of the United States of America, 113(28), E4035–4042. Retrieved from http://www.pnas.org/content/113/28/E4035.abstract doi:10.1073/pnas.1606101113
   PubMed Web of Science ®Google Scholar
• Visscher, P. K., & Seeley, T. D. (1982). Foraging strategy of honeybee colonies in a temperate deciduous forest. Ecology, 63(6), 1790–1801. Retrieved from < Go to ISI>://WOS:A1982PS51900021. doi:10.2307/1940121
   Web of Science ®Google Scholar
• Winfree, R., Gross, B. J., & Kremen, C. (2011). Valuing pollination services to agriculture. Ecological Economics, 71(Supplement C), 80–88. Retrieved from http://www.sciencedirect.com/science/article/pii/S092180091100334X doi:10.1016/j.ecolecon.2011.08.001
   Web of Science ®Google Scholar
• Winston, M. L. (1987). The biology of the honey bee. Cambridge, MA: Harvard University Press.
   Google Scholar