Behavioral Ecology and Sociobiology

, Volume 68, Issue 1, pp 13–20 | Cite as

Preferences and tradeoffs in nectar temperature and nectar concentration in the Asian hive bee Apis cerana

  • Ken Tan
  • Tanya Latty
  • Zongwenu Hu
  • Zhengwei Wang
  • Shuang Yang
  • Weiweng Chen
  • Benjamin P. Oldroyd
Original Paper

Abstract

Honey bee foragers need to asses and make trade-offs between a number of potentially conflicting floral attributes. Here, we investigate multi-attribute decision making in the eastern honey bee, Apis cerana, when foraging on food sources that varied in warmth and sucrose concentration. We show that foragers prefer warm (30 °C) sucrose solution over cool (10 °C) sucrose solution and concentrated (30 % w/w) sucrose solution over dilute (15 % w/w) sucrose solution. When we offered the preferred sucrose concentration (30 % w/w) at the less-preferred temperature (10 °C), and the less-preferred sucrose concentration (15 % w/w) at the preferred temperature (30 °C), foragers prioritized warmth by choosing the warmer, but lower concentration solution. When the temperature difference was less extreme, bees preferred more concentrated cooler syrup (30 % ww at 15 °C over 15 % 30 °C). However, the addition of a decoy item to the choice set had a significant effect on the bees' preferences. Our results highlight the critical importance of considering context effects when measuring the foraging preferences of animals.

Keywords

Apis cerana Multi-attribute Decision making 

Notes

Acknowledgements

This work was supported by the Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Science and China National Research Fund (31260585) to KT. TL is funded by the Australian Research Council (DP110102998), and the Natural Sciences and Engineering Research Council of Canada.

Conflicts of interest

The authors declare that they have no conflicts of interest.

References

  1. Abbott KR, Dukas R (2009) Honeybees consider flower danger in their waggle dance. Anim Behav 78:633–635CrossRefGoogle Scholar
  2. Avarguès-Weber A, Dyer AG, Combe M, Giurfa M (2012) Simultaneous mastering of two abstract concepts by the minature brain of bees. Proc Natl Acad Sci U S A 109:7481–7486PubMedCentralPubMedCrossRefGoogle Scholar
  3. Bartoshuk LM, Rennert K, Rodin J, Stevans JC (1982) Effects of temperature on the perceived sweetness of sucrose. Physiol Behav 28:905–910PubMedCrossRefGoogle Scholar
  4. Bateson M (2002) Context-dependent foraging choices in risk-sensitive starlings. Anim Behav 64:251–260CrossRefGoogle Scholar
  5. Bateson M, Healy SD (2005) Comparative evaluation and its implications for mate choice. Trends Ecol Evol 20:659–664PubMedCrossRefGoogle Scholar
  6. Bateson M, Healy SD, Hurly TA (2002) Irrational choices in hummingbird foraging behaviour. Anim Behav 63:587–596CrossRefGoogle Scholar
  7. Beckers R, Deneubourg JL, Goss S, Pasteels JM (1990) Collective decision making through food recruitment. Ins Soc 37:258–267CrossRefGoogle Scholar
  8. Brown JS, Kotler BP (2004) Hazardous duty pay and the foraging cost of predation. Ecol Let 7:999–1014CrossRefGoogle Scholar
  9. Cakmak I, Sanderson C, Blocker TD, Pham LL, Checotah S, Norman AA, Harader-Pate BK, Reidenbaugh RT, Nenchev P, Barthell JF, Wells H (2009) Different solutions by bees to a foraging problem. Anim Behav 77:1273–1280CrossRefGoogle Scholar
  10. Camazine S, Deneuborg JL, Franks NR, Sneyd J, Theraulaz G, Bonabeau E (2001) Self-organization in biological systems. Princeton University Press, Princeton, NJGoogle Scholar
  11. Chen L, Zhang SW, Srinivasan MV (2003) Global perception in small brains: topological pattern recognition in honey bees. Proc Natl Acad Sci U S A 100:6884–6889PubMedCentralPubMedCrossRefGoogle Scholar
  12. Corbet SA (1978) Bee visits and the nectar of Echium vulgare L. and Sinapis alba L. Ecol Entomol 3:25–37CrossRefGoogle Scholar
  13. Deco G, Rolls ET, Romo R (2009) Stochastic dynamics as a principle of brain function. Prog Neurobiol 88:1–16PubMedCrossRefGoogle Scholar
  14. Dukas R (2001) Effects of perceived danger on flower choice by bees. Ecol Let 4:327–333CrossRefGoogle Scholar
  15. Dyer AG, Whitney HM, Arnold SEJ, Glover BJ, Chittka L (2006) Bees associate warmth with floral colour. Nature 442:525PubMedCrossRefGoogle Scholar
  16. Kv F (1967) The dance language and orientation of bees. Harvard University Press, CambridgeGoogle Scholar
  17. Gigerenzer G (1997) Rounded rationality: Models of fast and frugal inference. Swiss J Econ Stat 133:201–218Google Scholar
  18. Giurfa M, Zhang SW, Jenett A, Menzel R, Srinivasan MV (2001) The concepts of ‘sameness’ and ‘difference’ in an insect. Nature 410:930–933PubMedCrossRefGoogle Scholar
  19. Hammer TJ, Hata C, Nieh JC (2009) Thermal learning in the honeybee, Apis mellifera. J Exp Biol 212:3928–3934PubMedCrossRefGoogle Scholar
  20. Hurly TA, Oseen MD (1999) Context-dependent, risk-sensitive foraging preferences in wild rufous hummingbirds. Anim Behav 58:59–66PubMedCrossRefGoogle Scholar
  21. Kevan PG (1975) Sun-tracking solar furnaces in high arctic flowers: significance for pollination and insects. Science 189:723–726PubMedCrossRefGoogle Scholar
  22. Köhler A, Pirk CWW, Nicolson SW (2012) Honeybees and nectar nicotine: deterrence and reduced survival versus potential health benefits. J Ins Physiol 58:286–292CrossRefGoogle Scholar
  23. Latty T, Beekman M (2010) Food quality and the risk of light exposure affect patch-choice decisions in the slime mould Physarum polycephalum. Ecology 91:22–27PubMedCrossRefGoogle Scholar
  24. Latty T, Beekman M (2011) Irrational decision-making in an amoeboid organism: transitivity and context-dependent preferences. Proc Roy Soc B 278:307–312CrossRefGoogle Scholar
  25. Liu F, Chen J, Chai J, Zhang X, Bai X, He D, Roubik DW (2006) Adaptive functions of defensive plant phenolics and a non-linear bee response to nectar components. Func Ecol 21:96–100Google Scholar
  26. Lotz CN, del Rio CM, Nicolson SW (2003) Hummingbirds pay a high cost for a warm drink. J Comp Physiol B 173:455–462PubMedCrossRefGoogle Scholar
  27. Luce RD (1959) Individual choice behavior: a theoretical analysis. Wiley, New YorkGoogle Scholar
  28. McArthur C, Orlando P, Banks PB, Brown JS (2012) The foraging tightrope between predation risk and plant toxins: a matter of concentration. Func Ecol 26:74–83CrossRefGoogle Scholar
  29. Nicolis SC, Deneubourg JL (1999) Emerging patterns and food recruitment in ants: an analytical study. J Theor Biol 198:575–592PubMedCrossRefGoogle Scholar
  30. Nicolis SC, Zabzina N, Latty T, Sumpter DJT (2011) Collective irrationality and positive feedback. PLoS One 6:e18901. doi: 10.1371/journal.pone.0018901 PubMedCentralPubMedCrossRefGoogle Scholar
  31. Nonacs P, Dill LM (1990) Mortality risk vs. food quality trade-offs in a common currency: ant patch preferences. Ecology 71:1886–1892CrossRefGoogle Scholar
  32. Norgate M, Boyd-Gerny S, Simonov V, Rosa MGP, Heard TA, Dyer AG (2010) Ambient temperature influences Australian native stingless bee (Trigona carbonaria) preference for warm nectar. PLoS ONE 5(8):doi: 10.1371/journal.pone.0012000
  33. Pitz GF, Sachs NJ (1984) Judgement and decision: theory and application. Annu Rev Psychol 35:139–164PubMedCrossRefGoogle Scholar
  34. Rapoport A (1989) Decision theory and decision behaviour. Kluwer Academic Publishers, LondonGoogle Scholar
  35. Reinhard J, Srinivasan MV, Zhang SW (2006) Complex memories in honeybees: can there be more than two? J Comp Physiol A 192:409–416CrossRefGoogle Scholar
  36. Roubik DW, Buckman SL (1984) Nectar selection by Melipona and Apis mellifera (Hymenoptera: Apidae) and the ecology of nectar intake by bee colonies in a tropical forest. Oecologia 61:1–10CrossRefGoogle Scholar
  37. Schuck-Paim C, Kacelnik A (2007) Choice processes in multialternative decision making. Behav Ecol 18:541–550CrossRefGoogle Scholar
  38. Seymour RS (2001) Biophysics and physiology of temperature regulation on thermogenic flowers. Bioscience Reports 21:223–236PubMedCrossRefGoogle Scholar
  39. Seymour RS, Schultze-Motel P (1997) Heat-producing flowers. Endeavour 21:125–129CrossRefGoogle Scholar
  40. Shafir S (1994) Intrasitivity of preferences in honey bees: support for ‘comparative’ evaluation of foraging options. Anim Behav 48:55–67CrossRefGoogle Scholar
  41. Shafir S, Waite TA, Smith BH (2002) Context-dependent violations of rational choice in honeybees (Apis mellifera) and gray jays (Perisoreus canafensis). Behav Ecol Sociobiol 51:180–187CrossRefGoogle Scholar
  42. Simpson SJ, Sibly RM, Lee KP, Behmer ST, Raubenheimer D (2004) Optimal foraging when regulating uptake of multiple nutrients. Anim Behav 68:1299–1311CrossRefGoogle Scholar
  43. Srinivasan MV, Zhang SW, Zhu H (1998) Honeybees link sights to smells. Nature 396:637–638CrossRefGoogle Scholar
  44. Sumpter DJT (2006) The principles of collective animal behaviour. Phil Trans Biol Sci 361:5–22CrossRefGoogle Scholar
  45. Sumpter DJT, Pratt SC (2003) A modelling framework for understanding social insect foraging. Behav Ecol Sociobiol 53:131–144Google Scholar
  46. Tan K, Guo YH, Nicolson SW, Radloff SE, Song QS, Hepburn HR (2007) Honeybee (Apis cerana) foraging responses to the toxic honey of Tripterygium hypoglaucum (Celastraceae): changing threshold of nectar acceptability. J Chem Ecol 33:2209–2217PubMedCrossRefGoogle Scholar
  47. Tan K, Wang Z, Yang M, Fuchs S, Luo L, Zhang Z, Li H, Zhuang D, Yang S, Tautz J, Beekman M, Oldroyd BP (2012a) Asian hive bees, Apis cerana, modulate dance communication in response to nectar toxicity and demand. Anim Behav 84:1589–1594CrossRefGoogle Scholar
  48. Tan K, Yang S, Wang Z-W, Radloff SE, Oldroyd BP (2012b) Differences in foraging and broodnest temperature in the honey bees Apis cerana and A. mellifera. Apidologie 43:618–623CrossRefGoogle Scholar
  49. Tero A, Takagi S, Saigusa T, Ito K, Bebber DP, Fricker MD, Yumiki K, Kobayashi R, Nakagaki T (2010) Rules for biologically inspired adaptive networks. Science 327:439–442PubMedCrossRefGoogle Scholar
  50. Tversky A (1969a) Intrasitivity of preferences. Psych Rev 76:31–48CrossRefGoogle Scholar
  51. Tversky A (1969b) Substitutibility and similarity in binary choices. J Math Psychol 6:1–12CrossRefGoogle Scholar
  52. Tversky A, Simonson I (1993) Context-dependent preferences. Manag Sci 39:1179–1189CrossRefGoogle Scholar
  53. Waddington KD, Gottlieb N (1990) Actual vs. perceived profitability: a study of floral choice by honey bees. J Insect Behav 3:429–441CrossRefGoogle Scholar
  54. Waksberg AJ, Smith AB, Burd M (2009) Can irrational behaviour maximise fitness? Behav Ecol Sociobiol 63:461–471CrossRefGoogle Scholar
  55. Webster SJ, Dill LM (2006) The energetic equivalence of changing salinity and temperature to juvenile salmon. Func Ecol 20:621–629CrossRefGoogle Scholar
  56. Whitney HM, Dyer AG, Chittka L, Rands SA, Glover BJ (2008) The interaction of temperature and sucrose concentration preferences in bumblebees. Naturwissenschaften 95:845–850PubMedCrossRefGoogle Scholar
  57. Wilmer PG (1983) Thermal constraints on activity patterns in nectar-feeding insects. Ecol Entomol 8:455–469CrossRefGoogle Scholar
  58. Zhang SW, Srinivasan MV, Zhu H, Wong J (2004) Grouping of visual objects by honeybees. J Exp Biol 207:3289–3298PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Ken Tan
    • 1
  • Tanya Latty
    • 2
  • Zongwenu Hu
    • 3
  • Zhengwei Wang
    • 3
  • Shuang Yang
    • 3
  • Weiweng Chen
    • 3
  • Benjamin P. Oldroyd
    • 2
  1. 1.Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical GardenChinese Academy of SciencesXishuangbannaChina
  2. 2.Behaviour and Genetics of Social Insects Laboratory, School of Biological Sciences A12University of SydneyNSWAustralia
  3. 3.Eastern Bee Research InstituteYunnan Agricultural UniversityKunmingChina

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