Behavioral Ecology and Sociobiology

, Volume 70, Issue 8, pp 1209–1217 | Cite as

Hungry for quality—individual bumblebees forage flexibly to collect high-quality pollen

  • Fabian A. Ruedenauer
  • Johannes Spaethe
  • Sara D. Leonhardt
Original Article

Abstract

Nutritional deficits may be one factor contributing to the ongoing decline of wild and managed bees. As a consequence, interest in understanding the effect of floral resource availability on nutritional intake - and subsequently bee health and performance - has increased. However, the proximate mechanisms underlying bee foraging choices are still poorly understood. We do, for instance, not yet know whether and how bees assess the nutritional quality of pollen or whether they use information on pollen quality to adjust foraging patterns. In a previous study, we showed that Bombus terrestris workers use their sense of taste to discriminate pollen differing in concentration and, thus, nutrient content. We now investigated whether they translate this ability into foraging behavior by observing microcolonies offered the choice between two feeders containing different pollen types and concentrations and, thus, qualities. We examined whether bumblebees used direct (chemotactile) or indirect (olfactory) cues to assess pollen quality and whether they individually assessed pollen quality or relied on larval feedback. By changing pollen quality after 21 days, we further tested whether information on pollen quality was subsequently associated with other (faster assessable) cues (e.g., odor) or continuously re-assessed. We found that bees always preferred pollen of higher quality and individually assessed quality based on chemotactile cues. Moreover, changing pollen quality resulted in rapid equivalent changes in foraging behavior, even without feedback from larvae. Consequently, individual bumblebee foragers continuously re-assess pollen quality to provide their colonies with high-quality food.

Significance statement

The ongoing decline of wild and managed bees is likely driven by several factors with nutritional deficits being one of them. Because bees are amongst the most important pollinators, interest in understanding the effect of floral resource availability on nutritional intake and, subsequently, bee health and performance has increased. However, the proximate mechanisms underlying bee foraging choices are still poorly understood. In this study, we investigated how bumblebees differentiate between different pollen qualities by observing microcolonies offered the choice between different diets. We found that bees always preferred pollen of higher quality and individually assessed quality based on chemotactile cues. This finding increases our understanding of how social bees assess nutritional quality and make appropriate foraging choices.

Keywords

Bee decline Nutrients Nutrition Optimal foraging Pollen Protein 

Supplementary material

265_2016_2129_MOESM1_ESM.doc (268 kb)
Figure S1Palynological composition of honeybee-collected pollen. Given is the relative abundance of pollen of different plant genera/families in the mixture. Pollen was analyzed using DNA meta-barcoding following the protocol established and described by Keller et al. (2015) and Sickel et al. (2015). (DOC 268 kb)
265_2016_2129_MOESM2_ESM.doc (138 kb)
Figure S2Daily food collection [μg/individual] of two different pollen types by 6 Bombus terrestris microcolonies, being offered a choice between (A) pure apple or almond pollen (black) and apple or almond pollen diluted with cellulose at a ratio of 1:10 (grey) and (B) pure apple pollen (black) or pure almond pollen (grey). Each dot represents one data point (i.e. the amount of food collected [μg] per individual per day for each colony). Generalized additive mixed effect models were used to fit smoothers to the data showing mean trends [±95% confidence intervals, dashed lines] over time. (DOC 138 kb)
265_2016_2129_MOESM3_ESM.doc (130 kb)
Figure S3Daily food collection [μg/individual] of two different pollen types by 6 Bombus terrestris microcolonies, being offered a choice between (A) high quality (i.e. pure bee-collected) pollen (black) and low quality (i.e. bee-collected pollen diluted with cellulose at a ratio of 1:10) pollen (grey) and (B) the same treatment but with egg clumps taken out each day. Each dot represents one data point (i.e. the amount of food collected [μg] per individual per day for each colony). Generalized additive mixed effect models were used to fit smoothers to the data showing mean trends [±95% confidence intervals, dashed lines] over time. (DOC 130 kb)

References

  1. Altaye SZ, Pirk CWW, Crewe RM, Nicolson SW (2010) Convergence of carbohydrate-biased intake targets in caged worker honeybees fed different protein sources. J Exp Biol 213:3311–3318CrossRefPubMedGoogle Scholar
  2. Baker HG (1977) Non-sugar chemical constituents of nectar. Apidologie 8:349–356CrossRefGoogle Scholar
  3. Behmer ST (2009) Insect herbivore nutrient regulation. Annu Rev Entomol 54:165–187CrossRefPubMedGoogle Scholar
  4. Brodschneider R, Crailsheim K (2010) Nutrition and health in honey bees. Apidologie 41:278–294CrossRefGoogle Scholar
  5. Brunner FS, Schmid-Hempel P, Barribeau SM (2014) Protein-poor diet reduces host-specific immune gene expression in Bombus terrestris. Proc R Soc B-Biol Sci. 281Google Scholar
  6. Camazine S (1993) The regulation of pollen foraging by honey bees—how foragers assess the colony need for pollen. Behav Ecol Sociobiol 32:265–272CrossRefGoogle Scholar
  7. Campbell NA (1997) Biologie. Spektrum Akademischer VerlagGoogle Scholar
  8. Chapman RF (1998) The insects: structure and function. Cambridge university pressGoogle Scholar
  9. DeGroot AP (1953) Protein and amino acid requirements of the honey bee (Apis mellifica L.). Phys Comp Oecol 3:197–285Google Scholar
  10. Di Pasquale G, Salignon M, Le Conte Y, Belzunces LP, Decourtye A, Kretzschmar A, Suchail S, Brunet JL, Alaux C (2013) Influence of pollen nutrition on honey bee health: do pollen quality and diversity matter? PLoS One 8:e72016CrossRefPubMedPubMedCentralGoogle Scholar
  11. Dobson HEM, Bergstrom G (2000) The ecology and evolution of pollen odors. Plant Syst Evol 222:63–87CrossRefGoogle Scholar
  12. Duchateau MJ, Velthuis HHW (1989) Ovarian development and egg laying in workers of Bombus terrestris. Entomol Exp Appl 51:199–213Google Scholar
  13. Dussutour A, Simpson SJ (2008) Carbohydrate regulation in relation to colony growth in ants. J Exp Biol 211:2224–2232CrossRefPubMedGoogle Scholar
  14. Dussutour A, Simpson SJ (2009) Communal nutrition in ants. Curr Biol 19:740–744CrossRefPubMedGoogle Scholar
  15. Eckhardt M, Haider M, Dorn S, Müller A (2014) Pollen mixing in pollen generalist solitary bees: a possible strategy to complement or mitigate unfavourable pollen properties? J Anim Ecol 83:588–597CrossRefPubMedGoogle Scholar
  16. Erhardt GM (1996) Blütenökologische Untersuchungen an Aconitum lycoctonum (Ranunculaceae) und Bombus gerstaeckeri (Hymenoptera, Apidae). PhD ThesisGoogle Scholar
  17. Falibene A, Roces F, Rössler W (2015) Long-term avoidance memory formation is associated with a transient increase in mushroom body synaptic complexes in leaf-cutting ants. Front Behav Neurosci 9:84CrossRefPubMedPubMedCentralGoogle Scholar
  18. Genissel A, Aupinel P, Bressac C, Tasei JN, Chevrier C (2002) Influence of pollen origin on performance of Bombus terrestris micro-colonies. Entomol Exp Appl 104:329–336CrossRefGoogle Scholar
  19. Goulson D (2003) Bumblebees: their behaviour and ecology. Oxford University PressGoogle Scholar
  20. Haydak MH (1970) Honey bee nutrition. Annu Rev Entomol 15:143–156CrossRefGoogle Scholar
  21. Herbert EW, Shimanuki H, Caron D (1977) Optimum protein levels required by honey bees (Hymenoptera, Apidae) to initiate and maintain brood rearing. Apidologie 8:141–146CrossRefGoogle Scholar
  22. Höcherl N, Siede R, Illies I, Gätschenberger H, Tautz J (2012) Evaluation of the nutritive value of maize for honey bees. J Insect Physiol 58:278–285CrossRefPubMedGoogle Scholar
  23. Huang T, Jander G, de Vos M (2011) Non-protein amino acids in plant defense against insect herbivores: representative cases and opportunities for further functional analysis. Phytochemistry 72:1531–1537CrossRefPubMedGoogle Scholar
  24. Kay AD, Bruning AJ, van Alst A, Abrahamson TT, Hughes WOH, Kaspari M (2014) A carbohydrate-rich diet increases social immunity in ants. Proc R Soc B-Biol Sci 281:20132374CrossRefGoogle Scholar
  25. Keller A, Danner N, Grimmer G, Ankenbrand M, von der Ohe K, von der Ohe W, Rost S, Härtel S, Steffan-Dewenter I (2015) Evaluating multiplexed next-generation sequencing as a method in palynology for mixed pollen samples. Plant Biol 17:558–566CrossRefPubMedGoogle Scholar
  26. Kitaoka TK, Nieh JC (2009) Bumble bee pollen foraging regulation: role of pollen quality, storage levels, and odor. Behav Ecol Sociobiol 63:501–510CrossRefGoogle Scholar
  27. Konzmann S, Lunau K (2014) Divergent rules for pollen and nectar foraging bumblebees—a laboratory study with artificial flowers offering diluted nectar substitute and pollen surrogate. PLoS One 9:e91900CrossRefPubMedPubMedCentralGoogle Scholar
  28. Leadbeater E, Florent C (2014) Foraging bumblebees do not rate social information above personal experience. Behav Ecol Sociobiol 68:1145–1150CrossRefGoogle Scholar
  29. London-Shafir I, Shafir S, Eisikowitch D (2003) Amygdalin in almond nectar and pollen—facts and possible roles. Plant Syst Evol 238:87–95CrossRefGoogle Scholar
  30. Manning R (2001) Fatty acids in pollen: a review of their importance for honey bees. Bee World 82:60–75CrossRefGoogle Scholar
  31. Mapalad KS, Leu D, Nieh JC (2008) Bumble bees heat up for high quality pollen. J Exp Biol 211:2239–2242CrossRefPubMedGoogle Scholar
  32. Mevi-Schutz J, Erhardt A (2005) Amino acids in nectar enhance butterfly fecundity: a long-awaited link. Am Nat 165:411–419CrossRefPubMedGoogle Scholar
  33. Nicolson SW (2011) Bee food: the chemistry and nutritional value of nectar, pollen and mixtures of the two. Afr Zool 46:197–204CrossRefGoogle Scholar
  34. Pernal SF, Currie RW (2001) The influence of pollen quality on foraging behavior in honeybees (Apis mellifera L.). Behav Ecol Sociobiol 51:53–68CrossRefGoogle Scholar
  35. Pernal SF, Currie RW (2002) Discrimination and preferences for pollen-based cues by foraging honeybees, Apis mellifera L. Anim Behav 63:369–390CrossRefGoogle Scholar
  36. Persson AS, Smith HG (2013) Seasonal persistence of bumblebee populations is affected by landscape context. Agr Ecosyst Environ 165:201–209CrossRefGoogle Scholar
  37. Pirk CWW, Boodhoo C, Human H, Nicolson S (2010) The importance of protein type and protein to carbohydrate ratio for survival and ovarian activation of caged honeybees (Apis mellifera scutellata). Apidologie 41:62–72CrossRefGoogle Scholar
  38. Regali A, Rasmont P (1995) New bioassays to evaluate diet in Bombus terrestris (L) (Hymenoptera, Apidae). Apidologie 26:273–281CrossRefGoogle Scholar
  39. Roulston TH, Cane JH (2000) Pollen nutritional content and digestibility for animals. Plant Syst Evol 222:187–209CrossRefGoogle Scholar
  40. Ruedenauer FA, Spaethe J, Leonhardt SD (2015) How to know which food is good for you: bumblebees use taste to discriminate between different concentrations of food differing in nutrient content. J Exp Biol 218:2233–2240CrossRefPubMedGoogle Scholar
  41. Sadd BM, Barribeau SM, Bloch G, De Graaf DC, Dearden P, Elsik CG, Gadau J, Grimmelikhuijzen CJ, Hasselmann M, Lozier JD (2015) The genomes of two key bumblebee species with primitive eusocial organization. Genome Biol 16:1–32CrossRefGoogle Scholar
  42. Saverschek N, Herz H, Wagner M, Roces F (2010) Avoiding plants unsuitable for the symbiotic fungus: learning and long-term memory in leaf-cutting ants. Anim Behav 79:689–698CrossRefGoogle Scholar
  43. Sickel W, Ankenbrand MJ, Grimmer G, Holzschuh A, Härtel S, Lanzen J, Steffan-Dewenter I, Keller A (2015) Increased efficiency in identifying mixed pollen samples by meta-barcoding with a dual-indexing approach. BMC Ecol 15:1–9CrossRefGoogle Scholar
  44. Simpson SJ, Raubenheimer D (2009) Macronutrient balance and lifespan. Aging-US 1:875–880CrossRefGoogle Scholar
  45. Simpson SJ, Raubenheimer D (2012) The nature of nutrition: a unifying framework from animal adaptation to human obesity. Princeton University PressGoogle Scholar
  46. Somerville DC (2001) Nutritional value of bee collected pollens. RIRDC Publication, NSW AgricultureGoogle Scholar
  47. 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 46:92–106CrossRefGoogle Scholar
  48. Standifer LN, McCaughey WF, Todd FE, Kemmerer AR (1960) Relative availability of various proteins to the honey bee. Ann Entomol Soc Am 53:618–625CrossRefGoogle Scholar
  49. Szymas B, Jedruszuk A (2003) The influence of different diets on haemocytes of adult worker honey bees, Apis mellifera. Apidologie 34:97–102CrossRefGoogle Scholar
  50. Tasei JN, Aupinel P (2008) Nutritive value of 15 single pollens and pollen mixes tested on larvae produced by bumblebee workers (Bombus terrestris, Hymenoptera : Apidae). Apidologie 39:397–409CrossRefGoogle Scholar
  51. Tiedeken EJ, Stout JC, Stevenson PC, Wright GA (2014) Bumblebees are not deterred by ecologically relevant concentrations of nectar toxins. J Exp BiolGoogle Scholar
  52. Togasawa Y, Katsumata T, Fukada M, Motoi T (1967a) Biochemical studies on pollen: part VII. Vitamins of pollen. Nippon Nogeik Kaishi 41:184–188CrossRefGoogle Scholar
  53. Togasawa Y, Katsumata T, Ota T (1967b) Biochemical studies on pollen: part VI. Inorganic components and phosphorus compounds of pollen. Nippon Nogeik Kaishi 41:178–183CrossRefGoogle Scholar
  54. Vanderplanck M, Leroy B, Wathelet B, Wattiez R, Michez D (2014a) Standardized protocol to evaluate pollen polypeptides as bee food source. Apidologie 45:192–204CrossRefGoogle Scholar
  55. Vanderplanck M, Moerman R, Rasmont P, Lognay G, Wathelet B, Wattiez R, Michez D (2014b) How does pollen chemistry impact development and feeding behaviour of polylectic bees? PLoS One 9:e86209CrossRefPubMedPubMedCentralGoogle Scholar
  56. Vaudo AD, Patch HM, Mortensen DA, Grozinger CM, Tooker JF (2014) Bumble bees exhibit daily behavioral patterns in pollen foraging. Arthropod-Plant Interact 8:273–283Google Scholar
  57. Vaudo AD, Tooker JF, Grozinger CM, Patch HM (2015) Bee nutrition and floral resource restoration. Curr Opin Insect Sci 10:133–141CrossRefGoogle Scholar
  58. Weiner CN, Hilpert A, Werner M, Linsenmair KE, Blüthgen N (2010) Pollen amino acids and flower specialisation in solitary bees. Apidologie 41:476–487CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Fabian A. Ruedenauer
    • 1
  • Johannes Spaethe
    • 2
  • Sara D. Leonhardt
    • 1
  1. 1.Department of Animal Ecology and Tropical Biology, BiozentrumUniversity of WürzburgWürzburgGermany
  2. 2.Department of Behavioral Physiology and Sociobiology, BiozentrumUniversity of WürzburgWürzburgGermany

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