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Honey bee foragers balance colony nutritional deficiencies

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Abstract

Honey bee colonies, foraging predominantly on a single pollen source, may encounter nutritional deficits. In the present study, we examined the nutritional resilience of honey bee colonies, testing whether foragers shift their foraging effort towards resources that complement a nutritional deficit. Eight honey bee colonies were kept in screened enclosures and fed for 1 week a pollen substitute diet deficient in a particular essential amino acid. Foragers were subsequently tested for a preference between the same diet previously fed, a different diet that was similarly deficient, or a diet that complemented the deficiency. Foragers preferred the complementary diet over the same or similar diets. Appetitive conditioning tests showed that bees were able to discriminate also between the same and similar diets. Overall, our results support the hypothesis that honey bees prefer dietary diversity, and that they do not just include novel sources but specifically target nutritionally complementary ones. Whereas we specifically focused on deficiencies in essential amino acids, we cannot rule out that bees were also complementing correlated imbalances in other nutrients, most notably essential fatty acids. The ability of honey bees to counter deficient nutrition contributes to the mechanisms which social insects use to sustain homeostasis at the colony level.

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References

  • Abisgold JD, Simpson SJ (1987) The physiology of compensation by locusts for changes in dietary-protein. J Exp Biol 129:329–346

    Google Scholar 

  • Afik O, Dag A, Shafir S (2008) Honey bee (Apis mellifera) round dance is influenced by trace element composition of floral nectar. Anim Behav 75:371–377

    Article  Google Scholar 

  • Alaux C, Ducloz F, Crauser D, Le Conte Y (2010) Diet effects on honeybee immunocompetence. Biol Lett 6:562–565. doi:10.1098/rsbl.2009.0986

    Article  PubMed  PubMed Central  Google Scholar 

  • Archer CR, Köhler A, Pirk CWW, Oosthuizen V, Apostolides Z, Nicolson SW (2014) Antioxidant supplementation can reduce the survival costs of excess amino acid intake in honeybees. J Insect Physiol 71:78–86

    Article  CAS  PubMed  Google Scholar 

  • Arganda S, Nicolis SC, Perochain A, Pechabadens C, Latil G, Dussutour A (2014) Collective choice in ants: the role of protein and carbohydrates ratios. J Insect Physiol 69:19–26. doi:10.1016/j.jinsphys.2014.04.002

    Article  CAS  PubMed  Google Scholar 

  • Arien Y, Dag A, Zarchin S, Masci T, Shafir S (2015) Omega-3 deficiency impairs honey bee learning. PNAS 112:15761–15766

  • Avni D, Dag A, Shafir S (2009) Pollen sources for honeybees in Israel: source, periods of shortage, and influence on population growth. Isr J Plant Sci 57:263–275. doi:10.1560/IJPS573263, Special Issue: Developments in Plant-Pollinator Interactions

    Article  Google Scholar 

  • Avni D, Hendriksma HP, Dag A, Uni Z, Shafir S (2014) Nutritional aspects of honey bee-collected pollen and constraints on colony development in the eastern Mediterranean. J Insect Physiol 69:65–73. doi:10.1016/j.jinsphys.2014.07.001

    Article  CAS  PubMed  Google Scholar 

  • Behmer S (2009) Insect herbivore nutrient regulation. Annu Rev Entomol 54:165–187

    Article  CAS  PubMed  Google Scholar 

  • Behmer S (2014) Animal behaviour: feeding the superorganism. Curr Biol 19:R366

    Article  Google Scholar 

  • Bidlingmeyer BA, Cohen SA, Tarvin TL (1984) Rapid analysis of amino acids using pre-column derivatization. J Chromatogr 336:93–104

    Article  CAS  PubMed  Google Scholar 

  • Bjordal M, Arquier N, Kniazeff J, Pin JP, Léopold P (2014) Sensing of amino acids in a dopaminergic circuitry promotes rejection of an incomplete diet in Drosophila. Cell 156:510–521

    Article  CAS  PubMed  Google Scholar 

  • Camazine S, Crailsheim K, Hrassnigg N, Robinson GE, Leonhard B, Kropiunigg H (1998) Protein trophallaxis and the regulation of pollen foraging by honey bees (Apis mellifera L.). Apidologie 29:113–126

    Article  CAS  Google Scholar 

  • Chalisova NI, Kamyshev NG, Lopatina NG, Kontsevaya EA, Urtieva SA, Urtieva TA (2011) Effect of encoded amino acids on associative learning of honeybee Apis mellifera. J Evol Biochem Physiol 47:607–610

    Article  Google Scholar 

  • Cook SM, Awmack CS, Murray DA, Williams IH (2003) Are honey bees’ foraging preferences affected by pollen amino acid composition? Ecol Entomol 28:622–627

    Article  Google Scholar 

  • Cook SM, Sandoz JC, Martin AP, Murray DA, Poppy GM, Williams IH (2005) Could learning of pollen odours by honey bees (Apis mellifera) play a role in their foraging behaviour? Physiol Entomol 30:164–174

    Article  Google Scholar 

  • Crailsheim K (1991) Interadult feeding of jelly in honeybee (Apis mellifera L.) colonies. J Comp Physiol B 161:55–60

    Article  Google Scholar 

  • Crawley MJ (2007) The R book. Wiley, Chichester

    Book  Google Scholar 

  • De Brito Sanchez MG (2011) Taste perception in honey bees. Chem Senses 36:675–692. doi:10.1093/chemse/bjr040

    Article  PubMed  Google Scholar 

  • De Groot AP (1953) Protein and amino acid requirements of the honeybee (Apis mellifica L). Dissertation, University of Utrecht

  • Dussutour A, Simpson SJ (2009) Communal nutrition in ants. Curr Biol 19:740–744. doi:10.1016/j.cub.2009.03.015

    Article  CAS  PubMed  Google Scholar 

  • Dussutour A, Simpson SJ (2012) Ant workers die young and colonies collapse when fed a high-protein diet. Proc R Soc B 279:2402–2408. doi:10.1098/rspb.2012.0051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanley M, Franco M, Pichon S, Darvill B, Goulson D (2008) Breeding system, pollinator choice and variation in pollen quality in British herbaceous plants. Funct Ecol 22:592–598

    Article  Google Scholar 

  • Hendriksma HP, Oxman KL, Shafir S (2014) Amino acid and carbohydrate tradeoffs by honey bee nectar foragers and their implications for plant-pollinator interactions. J Insect Physiol 69:56–64

    Article  CAS  PubMed  Google Scholar 

  • Inouye DW, Waller GD (1984) Responses of honey bees (Apis mellifera) to amino acid solutions mimicking floral nectars. Ecology 65:618–625

  • Kim YS, Smith BH (2000) Effect of an amino acid on feeding preferences and learning behavior in the honey bee, Apis mellifera. J Insect Physiol 46:793–801

    Article  CAS  PubMed  Google Scholar 

  • Lihoreau J, Buhl J, Charleston MA, Sword GA, Raubenheimer D, Simpson SJ (2014) Modelling nutrition across organizational levels: from individuals to superorganisms. J Insect Physiol 69:2–11. doi:10.1016/j.jinsphys.2014.03.004

    Article  CAS  PubMed  Google Scholar 

  • Lihoreau M, Buhl J, Charleston MA, Sword GA, Raubenheimer D, Simpson SJ (2015) Nutritional ecology beyond the individual: a conceptual framework for integrating nutrition and social interactions. Ecol Lett 18:273–286

    Article  PubMed  PubMed Central  Google Scholar 

  • Linander N, Hempel de Ibarra N, Laska M (2012) Olfactory detectability of L-amino acids in the European honeybee (Apis mellifera). Chem Senses 37:631–638

    Article  CAS  PubMed  Google Scholar 

  • McLellan AR (1978) Growth and decline of honeybee colonies and inter-relationships of adult bees, brood, honey and pollen. J Appl Ecol 15:155–161

    Article  Google Scholar 

  • Nicholls E, Hempel de Ibarra N (2014) Bees associate colour cues with differences in pollen rewards. J Exp Biol 217:2783–2788. doi:10.1242/jeb.106120

    Article  PubMed  Google Scholar 

  • Paoli PP, Donley D, Stabler D, Saseendranath A, Nicolson SW, Simpson SJ, Wright GA (2014a) Nutritional balance of essential amino acids and carbohydrates of the adult worker honeybee depends on age. Amino Acids 46:1449–1458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paoli PP, Wakeling LA, Wright GA, Ford D (2014b) The dietary proportion of essential amino acids and Sir2 influence lifespan in the honeybee. Age 36:9649. doi:10.1007/s11357-014-9649-9

    Article  PubMed  PubMed Central  Google Scholar 

  • Pernal (2000) The influence of pollen quality and pollen-based cues on the nutrition and foraging behavior of honey bees, Apis mellifera L Dissertation, University of Manitoba

  • Pernal SF, Currie RW (2001) The influence of pollen quality on foraging behavior in honeybees (Apis mellifera L.). Behav Ecol Sociobiol 51:53–68

    Article  Google Scholar 

  • Pernal SF, Currie RW (2002) Discrimination and preferences for pollen-based cues by foraging honeybees, Apis mellifera L. Anim Behav 63:369–390

    Article  Google Scholar 

  • Pirk CWW, Boodhoo C, Human H, Nicolson SW (2010) The importance of protein type and protein to carbohydrate ratio for survival and ovarian activation of caged honeybees (Apis mellifera scutellata). Apidologie 41:62–72. doi:10.1051/apido/2009055

    Article  CAS  Google Scholar 

  • Potts SG, Bies-meijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353

    Article  PubMed  Google Scholar 

  • Povey S, Cotter SC, Simpson SJ, Wilson K (2013) Dynamics of macronutrient self-medication and illness-induced anorexia in virally infected insects. J Anim Ecol 83:245–255

    Article  PubMed  PubMed Central  Google Scholar 

  • Requier F, Odoux JF, Tamic T, Moreau N, Henry M, Decourtye A, Bretagnolle V (2015) Honey bee diet in intensive farmland habitats reveals an unexpectedly high flower richness and a major role of weeds. Ecol Appl 25:881–890

    Article  PubMed  Google Scholar 

  • Ribeiro C, Dickson BJ (2010) Sex peptide receptor and neuronal TOR/S6K signaling modulate nutrient balancing in Drosophila. Curr Biol 20:1000–1005

    Article  CAS  PubMed  Google Scholar 

  • Ricketts TH, Regetz J, Steffan-Dewenter I, Cunningham SA, Kremen C, Bogdanski A, Gemmill-Herren B, Greenleaf SS, Klein AM, Mayfield MM, Morandin LA, Ochieng A, Viana BF (2008) Landscape effects on crop pollination services: are there general patterns? Ecol Lett 11:499–515

    Article  PubMed  Google Scholar 

  • Schmidt JO (1984) Feeding preference of Apis mellifera L. (Hymenoptera: Apidae): individual versus mixed pollen species. J Kansas Entomol Soc 57:323–327

    Google Scholar 

  • Seeley TD (1995) The wisdom of the hive: the social physiology of honey bee colonies. Harvard Press, Cambridge

    Google Scholar 

  • Simcock NK, Gray HE, Wright GA (2014) Single amino acids in sucrose rewards modulate feeding and associative learning in the honeybee. J Insect Physiol 69:41–48. doi:10.1016/j.jinsphys.2014.05.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simpson SJ, Raubenheimer D (2012) The nature of nutrition: a unifying framework from animal adaptation to human obesity. Princeton University Press

  • Simpson SJ, Simpson CL (1992) Mechanisms controlling modulation by heamolymph amino acids of gustatory responsiveness in the locust. J Exp Biol 168:269–286

    CAS  Google Scholar 

  • Simpson CL, Simpson SJ, Abisgold JD (1990) The role of various amino acids in the protein compensatory response of Locusta migratoria. Symp Biol Hungar 39:39–46

    Google Scholar 

  • Somme L, Vanderplanck M, Michez D, Lombaerde I, Moerman R, Wathelet B, Wattiez R, Lognay G, Jacquemart AL (2015) Pollen and nectar quality drive the major and minor floral choices of bumble bees. Apidologie 46:92–106

    Article  Google Scholar 

  • Stabler D, Paoli PP, Nicolson SW, Wright GA (2015) Nutrient balancing of the adult worker bumblebee (Bombus terrestris) depends on its dietary source of essential amino acids. J Exp Biol 218:793–802. doi:10.1242/jeb.114249

    Article  PubMed  PubMed Central  Google Scholar 

  • Toshima N, Tanimura T (2012) Taste preference for amino acids is dependent on internal nutritional state in Drosophila melanogaster. J Exp Biol 215:2827–2832

    Article  CAS  PubMed  Google Scholar 

  • USDA (2014) United States Department of Agriculture’s National Nutrient Database for Standard Reference, Release 23 nutrient data laboratory home page. http://www.ars.usda.gov/ba/bhnrc/ndl

  • Vanderplanck M, Moerman R, Rasmont P, Lognay G, Wathelet B, Wattiez R, Michez D (2014) How does pollen chemistry impact development and feeding behaviour of polylectic bees? PLoS One 9, e86209. doi:10.1371/journal.pone.0086209

    Article  PubMed  PubMed Central  Google Scholar 

  • Vargas MA, Luo N, Yamaguchi A, Kapahi P (2010) A role for S6 kinase and serotonin in postmating dietary switch and balance of nutrients in D. melanogaster. Curr Biol 20:1006–1011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Von Frisch K (1934) Ueber den Geschmackssinn der Biene. Ein Beitrag zur vergleichenden Physiologie des Geschmacks. Z Vergl Physiol 21:1–156

    Article  Google Scholar 

  • Waddington KD, Nelson CM, Page RE Jr (1998) Effects of pollen quality and genotype on the dance of foraging honey bees. Anim Behav 56:35–39

    Article  PubMed  Google Scholar 

  • Zuur AF, Ieno EN, Elphick CS (2009) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14

    Article  Google Scholar 

Download references

Acknowledgments

This work was funded jointly by a grant from the BBSRC, NERC, the Wellcome Trust, Defra, and the Scottish Government under the Insect Pollinators Initiative (grant no: BB/I000968/1), and with partial support from the Orion Foundation. We thank Tania Masci, Karmi Oxman, and Haim Kalev for their valuable contribution to the work at the apiary and the laboratory.

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Correspondence to Harmen P. Hendriksma.

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Communicated by O. Rueppell

Significance statement

Honey bees forage for floral nectar as their main carbohydrate source and for pollen as their main source of amino acids, fatty acids, and micronutrients. It is becoming increasingly appreciated that honey bee colonies require a diet that is nutritionally balanced. Our main finding is that honey bee colonies do not only attempt to diversify their foraging but also that they bias their foraging effort towards a pollen substitute diet that specifically balances colony nutritional deficits. This finding adds a novel ability to honey bee foragers in evaluating collected diet macronutrient composition and in adjusting their foraging effort towards colony nutritional needs. The mechanism by which this is achieved remains to be elucidated. The implication of our study is that honey bee colonies strive to balance their nutrition if appropriate floral resources are available to them.

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Supplementary to the main paper, (1) methods and results of a diet screening experiment are provided, including (2) diet profiles of amino acid and fatty acid contents, (3) a data table with other nutritional and non-nutritional diet parameters, and (4) analyses of diet colors. (PDF 522 kb)

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Hendriksma, H.P., Shafir, S. Honey bee foragers balance colony nutritional deficiencies. Behav Ecol Sociobiol 70, 509–517 (2016). https://doi.org/10.1007/s00265-016-2067-5

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