Skip to main content
SpringerLink
Log in

Dancing for their supper: Do honeybees adjust their recruitment dance in response to the protein content of pollen?

  • Research Article
  • Published:
Insectes Sociaux Aims and scope Submit manuscript

Abstract

Honeybees use the dance language to communicate the location of profitable food resources to nestmates. During nectar foraging, bees alter the duration of the return phase of the dance to reflect the source’s quality. For more profitable resources, the return phase is shorter; this effectively makes the dance ‘livelier’. Bees also increase the number of dance circuits when the nectar source is more profitable, and they are more likely to dance for such sources. As a result, the colony focuses on high-quality nectar sources. Here we ask whether foragers similarly adjust aspects of their dance when foraging for pollen according to the pollen’s protein content. Pollen is essential for raising brood, and protein content varies substantially across plant species. We offered bees pollen, pollen substitutes or mixtures that differed in protein content and determined whether the duration of the return phase decreased and the number of dance circuits increased with increasing protein content. We further examined whether bees adjust return phase duration based on the protein content of naturally collected pollen. Lastly, we examined whether foragers are more likely to dance for pollen high in protein. Honeybees did not adjust the duration of the return phase or the number of dance circuits when mixtures contained more protein. Similarly, there was no relationship between protein content of natural pollen and return phase duration. Our results suggest that foragers cannot assess pollen’s protein content. Bees were more likely to dance when collecting pure pollen, suggesting an important role of pollen-based cues in the regulation of pollen foraging.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

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

    PubMed  PubMed Central  Google Scholar 

  • Arenas A, Farina WM (2012) Learned olfactory cues affect pollen-foraging preferences in honeybees, Apis mellifera. Anim Behav 83:1023–1033

    Article  Google Scholar 

  • Arenas A, Farina WM (2014) Bias to pollen odors is affected by early exposure and foraging experience. J Insect Phys 66:28–36

    Article  CAS  Google Scholar 

  • Beekman M (2005) How long will honey bees (Apis mellifera L.) be stimulated by scent to revisit past-profitable forage sites? J Comp Phys A 191:1115–1120

    Article  Google Scholar 

  • Beekman M, Ratnieks FLW (2000) Long range foraging by the honeybee Apis mellifera L. Funct Ecol 14:490–496

    Article  Google Scholar 

  • Boch R (1982) Relative attractiveness of different pollens to honeybees when foraging in a flight room and when fed in the hive. J Apic Res 21:104–106

    Google Scholar 

  • Brodschneider R, Crailsheim K (2010) Nutrition and health in honey bees. Apidologie 41:278–294

    Article  Google Scholar 

  • Camazine S (1993) The regulation of pollen foraging by honey bees: how foragers assess the colony’s need for pollen. Behav Ecol Sociobiol 32:265–272

    Article  Google Scholar 

  • Camazine S, Sneyd J (1991) A model of collective nectar source selection by honey bees: self-organization through simple rules. J Theor Biol 149:547–571

    Article  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 

  • Couvillon MJ, Schürch R, Ratnieks FLW (2014) Dancing bees communicate a foraging preference for rural lands in high-level agri-environment schemes. Curr Biol 24:1212–1215

    Article  PubMed  CAS  Google Scholar 

  • De Marco RJ (2006) How bees tune their dancing according to their colony’s nectar influx: re-examining the role of the food-receivers’ ‘eagerness’. J Exp Biol 209:421–432

    Article  PubMed  Google Scholar 

  • Dobson HEM, Bergström G (2000) The ecology and evolution of pollen odors. Plant Syst Evol 222:63–87

    Article  CAS  Google Scholar 

  • Fewell JH, Winston ML (1992) Colony state and regulation of pollen foraging in the honey bee Apis mellifera. Behav Ecol Sociobiol 30:387–393

    Article  Google Scholar 

  • Granovskiy B, Latty T, Duncan M, Sumpter DJT, Beekman M (2012) How dancing honey bees keep track of changes: the role of inspector bees. Behav Ecol 23:588–596

    Article  Google Scholar 

  • Hellmich RL, Rothenbuhler WC (1986) Relationship between different amounts of brood and the collection and use of pollen by the honey bee (Apis mellifera). Apidologie 17:13–20

    Article  Google Scholar 

  • Konzmann S, Lunau K (2014) Divergent rules for pollen and nectar foraging bumblebees—a laboratory study with artificial flowers offering diluted nectat substitite and pollen surrogate. PLoS One 9:e91900. doi:10.1371/journal.pone.0091900

    Article  PubMed  PubMed Central  Google Scholar 

  • Levin MD, Bohart GE (1955) Selection of pollens by honey bees. Am Bee J 95(392–393):402

    Google Scholar 

  • Lindauer M (1948) Über die Einwirkung von Duft- und Geschmacksstoffen sowie anderer Faktoren auf die Tänze der Bienen. Z Vgl Physiol 31:348–412

    Article  Google Scholar 

  • Lindauer M (1963) Allgemeine Sinnesphysiologie. Orientierung im Raum. Fortschr Zool 16:58–140

    PubMed  CAS  Google Scholar 

  • Mattila HR, Otis GW (2006) The effects of pollen availability during larval development on the behaviour and physiology of spring-reared honey bee workers. Apidologie 37:533–546

    Article  Google Scholar 

  • Nieh JC (2010) A negative feedback signal that is triggered by peril curbs honey bee recruitment. Curr Biol 20:310–315

    Article  PubMed  CAS  Google Scholar 

  • Oldroyd BP, Rinderer TE, Buco SM (1992) Intra-colonial foraging specialism by honey bees (Apis mellifera) (Hymenoptera: Apidae). Behav Ecol Sociobiol 30:291–295

    Article  Google Scholar 

  • Page RE, Erber J, Fondrk MK (1998) The effect of genotype on response threshold to sucrose and foraging behavior of honey bees (Apis mellifera L.). J Comp Phys A 182:489–500

    Article  Google Scholar 

  • Pankiw T, Page RE, Fondrk MK (1998) Brood pheromone stimulates pollen foraging in honey bees (Apis mellifera). Behav Ecol Sociobiol 44:193–198

    Article  Google Scholar 

  • 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 

  • Reinhard J, Srinivasan MV, Zhang S (2004) Scent-triggered navigation in honeybees. Nature 427:411

    Article  PubMed  CAS  Google Scholar 

  • Roulston TH, Cane JH (2000) Pollen nutritional content and digestibility for animals. Plant Syst Evol 222:187–209

    Article  CAS  Google Scholar 

  • Roulston TH, Cane JH, Buchmann SL (2000) What governs protein content of pollen: pollinator preferences, pollen-pistil interactions, or phylogeny? Ecol Monogr 70:617–643

    Google Scholar 

  • Sagili RR, Pankiw T (2007) Effects of protein-constrained brood food on honey bee (Apis mellifera L.) pollen foraging and colony growth. Behav Ecol Sociobiol 61:1471–1478

    Article  Google Scholar 

  • Sagili RR, Pankiw T, Zhu-Salzman K (2005) Effects of soybean trypsin inhibitor on hypopharyngeal gland protein content, total midgut protease activity and survival of the honey bee (Apis mellifera L.). J Insect Phys 51:953–957

    Article  CAS  Google Scholar 

  • Scheiner R, Page RE, Erber J (2004) Sucrose responsiveness and behavioral plasticity in honey bees (Apis mellifera). Apidologie 35:133–142

    Article  Google Scholar 

  • Schmidt JO (1982) Pollen foraging preferences of honey bees. Southwest Entomol 7:255–259

    Google Scholar 

  • Schmidt JO, Hanna A (2006) Chemical nature of phagostimulants in pollen attractive to honeybees. J Insect Beh 19:521–532

    Article  Google Scholar 

  • Schürch R, Couvillon MJ, Burns DDR, Tasman K, Waxman D, Ratnieks FL (2013) Incorporating variability in honey bee waggle dance decoding improves the mapping of communicated resource locations. J Comp Phys A 199:1143–1152

    Article  Google Scholar 

  • Scofield HN, Mattila HR (2015) Honey bee workers that are pollen stressed as larvae become poor foragers and waggle dancers as adults. PLoS One 10:e0121731. doi:10.1371/journal.pone.0121731

    Article  PubMed  PubMed Central  Google Scholar 

  • Seeley TD (1986) Social foraging by honeybees: how colonies allocate foragers among patches of flowers. Behav Ecol Sociobiol 19:343–354

    Article  Google Scholar 

  • Seeley TD (1994) Honey bee foragers as sensory units of their colonies. Behav Ecol Sociobiol 34:51–62

    Article  Google Scholar 

  • Seeley TD (1995) The wisdom of the hive. Harvard University Press, Cambridge

    Google Scholar 

  • Seeley TD (2010) Honeybee Democracy. Princeton University Press, Princeton

    Google Scholar 

  • Seeley TD, Buhrman SC (1999) Group decision making in swarms of honeybees. Behav Ecol Sociobiol 45:19–31

    Article  Google Scholar 

  • Seeley TD, Buhrman SC (2001) Nest-site selection in honey bees: how well do swarms implement the “best-of-N” decision rule? Behav Ecol Sociobiol 49:416–427

    Article  Google Scholar 

  • Seeley TD, Towne WF (1992) Tactics of dance choice in honey bees: do foragers compare dances? Behav Ecol Sociobiol 30:59–69

    Article  Google Scholar 

  • Seeley TD, Camazine S, Sneyd J (1991) Collective decision-making in honey bees: how colonies choose among nectar sources. Behav Ecol Sociobiol 28:277–290

    Article  Google Scholar 

  • Seeley TD, Kühnholz S, Weidenmüller A (1996) The honey bee’s tremble dance stimulates additional bees to function as nectar receivers. Behav Ecol Sociobiol 39:419–427

    Article  Google Scholar 

  • Seeley TD, Mikheyev AS, Pagano GJ (2000) Dancing bees tune both duration and rate of waggle-run production in relation to nectar-source profitability. J Comp Phys A 186:813–819

    Article  CAS  Google Scholar 

  • Toufailia HA, Couvillon MJ, Ratnieks FLW, Grütter C (2013) Honey bee waggle dance communication: signal meaning and signal noise affect dance follower behaviour. Behav Ecol Sociobiol 67:549–556

    Article  Google Scholar 

  • Vogel S (1983) Ecophysiology of zoophilic pollination. In: Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) Physiological plant ecology III, vol 12., Encyclopedia of plant physiologySpringer, Berlin Heidelberg, pp 560–624

    Google Scholar 

  • von Frisch K (1967) The dance language and orientation of bees. Harvard University Press, Cambridge

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Wilson WT, Boelter AM (1984) Attempts to condition the pollen preference of honey bees. Am Bee J 124:609–610

    Google Scholar 

Download references

Acknowledgments

We would like to thank Julie Lim for help in the lab, Jarrad Barnes for his help collecting the field data, Nadine Chapman, Ben Oldroyd, Tom Seeley, three anonymous reviewers and the editor for constructive comments on an earlier version of this manuscript, and. We would also like to thank the Australian Proteome Analysis Facility (APAF) for amino acid analysis; this analysis was facilitated by the Australian Government through the National Collaborative Research Infrastructure Strategy (NCRIS). MB is supported by a Fellowship from the Australian Research Council (FT120100120). TMS is funded by the Australian Research Council via DP130101670.

Author information

Authors and Affiliations

  1. Behaviour and Genetics of Social Insects Lab, School of Biological Sciences, The University of Sydney, Sydney, NSW, 2006, Australia

    M. Beekman & K. Preece

  2. Animal Behaviour Lab, School of Biological Sciences, The University of Sydney, Sydney, NSW, 2006, Australia

    T. M. Schaerf

Authors
  1. M. Beekman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. Preece
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T. M. Schaerf
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Beekman.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Beekman, M., Preece, K. & Schaerf, T.M. Dancing for their supper: Do honeybees adjust their recruitment dance in response to the protein content of pollen?. Insect. Soc. 63, 117–126 (2016). https://doi.org/10.1007/s00040-015-0443-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00040-015-0443-1

Keywords

Search

Navigation