Journal of Chemical Ecology

, Volume 31, Issue 12, pp 2791–2804 | Cite as

Feeding Responses of Free-flying Honeybees to Secondary Compounds Mimicking Floral Nectars

  • Natarajan Singaravelan
  • Gidi Nee'man
  • Moshe Inbar
  • Ido Izhaki
Article

Abstract

The role of secondary compounds (SC) in deterring herbivores and pathogens from vegetative parts of plants is well established, whereas their role in plant reproductive organs such as floral nectar is unclear. The present study aimed to reveal the response of free-flying honeybees to naturally occurring concentrations of four SC in floral nectar. We selected nicotine, anabasine, caffeine, and amygdalin, all of which are found in nectar of various plants. In repeated paired-choice experiments, we offered 20% sucrose solution as control along with test solutions of 20% sucrose with various concentrations of the above SC. Except for anabasine, naturally occurring concentrations of SC did not have a deterring effect. Furthermore, low concentrations of nicotine and caffeine elicited a significant feeding preference. SC can, therefore, be regarded as postingestive stimulants to pollinators, indicating that the psychoactive alkaloids in nectar may be a part of their mutualistic reward. Further studies are needed to test our hypothesis that psychoactive alkaloids in nectar impose dependence or addiction effects on pollinators.

Key Words

Nectar secondary compounds naturally occurring concentrations honeybees attraction deterrence 

Notes

Acknowledgements

This work was supported by a grant from Israel Science Foundation (ISF 600/03) and University of Haifa. We thank three anonymous reviewers for constructive criticisms and comments on earlier version of the manuscript.

References

  1. Adler, L. S. 2000The ecological significance of toxic nectarOikos91409420CrossRefGoogle Scholar
  2. Adler, L. S., Karban, R., Strauss, S. Y. 2001Direct and indirect effects of alkaloids on plant fitness via herbivory and pollinationEcology8220322044Google Scholar
  3. Agrawal, A. A., Laforsch, C., Tollrian, R. 1999Transgenerational induction of defenses in animals and plantsNature4016063CrossRefGoogle Scholar
  4. Baker, H. G. 1977Non-sugar chemical constituents of nectarApidologie8349356Google Scholar
  5. Baker, H. G. 1978

    Chemical aspects of the pollination biology of woody plants in the tropics

    Tomlinson, P. B.Zimmerman, M. H. eds. Tropical Trees as Living SystemsCambridge University PressCambridge5782
    Google Scholar
  6. Baker, H. G., Baker, I. 1975

    Studies of nectar-constitution and pollinator–plant coevolution

    Gilbert, L. E.Raven, P. H. eds. Coevolution of Animals and PlantsUniversity of Texas PressTexas100140
    Google Scholar
  7. Bainton, R. J., Tsai, L. T. Y., Singh, C. M., Moore, M. S., Neckameyer, W. S., Heberlein, U. 2000Dopamine modulates acute responses to cocaine, nicotine and ethanol in DrosophilaCurr. Biol.10187194PubMedCrossRefGoogle Scholar
  8. Bernays, E. A. 1983

    Nitrogen in defense against insects

    Lee, J. A.McNeil, S.Rorison, I. H. eds. Nitrogen as an Ecological FactorBlackwell ScientificOxford321344
    Google Scholar
  9. Bernays, E. A., Oppenheim, S., Chapman, R. F., Kwon, H., Gould, F. 2000Taste sensitivity of insect herbivores to deterrents is greater in specialists than in generalists: A behavioral test of the hypothesis with two closely related caterpillarsJ. Chem. Ecol.26547563Google Scholar
  10. Boppré, M. 1999Drug-addicted insects in AfricaMetamorphosis10315Google Scholar
  11. Bush, L. P., Crowe, M. W. 1992

    Nicotiana alkaloids

    Cheeke, P. R. eds. Toxicants of Plant OriginCRC Press Inc.Boca Raton, FL87107
    Google Scholar
  12. Cipollini, M. L., Levey, D. J. 1997Secondary metabolites of fleshy vertebrate-dispersed fruits: Adaptive hypotheses and implications for seed dispersalAm. Nat.150346372CrossRefGoogle Scholar
  13. Detzel, A., Wink, M. 1993Attraction, deterrence or intoxication of bees (Apis mellifera) by plant allelochemicalsChemoecology4818CrossRefGoogle Scholar
  14. Faegri, K., Pijl, L. 1979The Principles of Pollination Ecology3Pergamon PressNew YorkGoogle Scholar
  15. Gardener, M. C., Gillman, M. P. 2002The taste of nectar—a neglected area of pollination ecologyOikos98552557CrossRefGoogle Scholar
  16. Glendinning, J. I. 2000How do inostol and glucose modulate feeding in Manduca sexta caterpillars?J. Exp. Biol.20312991315PubMedGoogle Scholar
  17. Glendinning, J. I., Slansky, F. 1994Interactions of allelochemicals with dietary constituents—effects on deterrencyPhysiol. Entomol.19173186Google Scholar
  18. Gonzalez-Coloma, A., Reina, M., Medinaveitia, A., Guadano, A., Santana, O., Martinez-Diaz, R., Ruiz-Mesia, L., Alva, A., Grandez, M., Diaz, R., Gavin, J. A., Fuente, G. 2004Structural diversity and defensive properties of norditerpenoid alkaloidsJ. Chem. Ecol.3013931408PubMedGoogle Scholar
  19. Gronquist, M., Bezzerides, A., Attygalle, A., Meinwald, J., Eisner, M., Eisner, T. 2001Attractive and defensive functions of the ultraviolet pigments of a flower (Hypericum calycinum)Proc. Natl. Acad. Sci. USA981374513750PubMedCrossRefGoogle Scholar
  20. Guerreiro, O., Mazzafera, P. 2000Caffeine does not protect coffee against the leaf miner Perileucoptera coffeellaJ. Chem. Ecol.2614471464Google Scholar
  21. Hagler, J., Buchmann, L. S. 1993Honeybee (Hymenoptera: Apidae) foraging responses to phenolic-rich nectarsJ. Kans. Entomol. Soc.66223230Google Scholar
  22. Halladay, A. K., Schwartz, M., Wagner, G. C., Iba, M. M., Sekowski, A., Fisher, H. 1999Efficacy of providing nicotine in a liquid diet to ratsProc. Soc. Exp. Biol. Med.221215223PubMedCrossRefGoogle Scholar
  23. Harborne, J. B. 1993

    Insect feeding preferences

    Harborne, J. B. eds. Introduction to Ecological Biochemistry4Academic PressNew York128161
    Google Scholar
  24. Harrison, M. J., Baldwin, I. T. 2004Biotic interactions: Ploy and counter-ploy in the biotic interactions of plantsCurr. Opin. Plant Biol.7353355CrossRefGoogle Scholar
  25. Heinrich, B. 1979Resource heterogeneity and patterns of movement in foraging bumblebeesOecologia40235245CrossRefGoogle Scholar
  26. Heyne, A., Wolffgramm, J. 1998The development of addiction to d-amphetamine in an animal model: same principles as for alcohol and opiatePsychopharmacology140510518PubMedCrossRefGoogle Scholar
  27. Holopainen, J. K. 2004Multiple functions of inducible plant volatilesTrends Plant Sci.9529533PubMedCrossRefGoogle Scholar
  28. Ish-Am, G., Eisikowitch, D. 1998Low attractiveness of avocado (Persea americana Mill.) flowers to honeybees (Apis mellifera L.) limits fruit set in IsraelJ. Hortic. Sci. Biotechnol.73195204Google Scholar
  29. Izhaki, I. 2002Emodin—a secondary metabolite with multiple ecological functions in higher plantsNew Phytol.155205217CrossRefGoogle Scholar
  30. Jakobsen, H. B., Kristjansson, K., Rohde, B., Terkildsen, M., Olsen, C. E. 1995Can social bees be influenced to choose a specific feeding station by adding the scent of the station to the hive air?J. Chem. Ecol.2116351648CrossRefGoogle Scholar
  31. Karban, R., Baldwin, I. T. 1997Induced Responses to HerbivoryUniversity of Chicago PressChicagoGoogle Scholar
  32. Kingsbury, J. M. 1964Poisonous Plants of the United States and CanadaPrentice-HallEnglewood Cliffs, NJGoogle Scholar
  33. Kretschmar, J. A., Baumann, T. W. 1999Caffeine in Citrus flowersPhytochemistry52 1923CrossRefGoogle Scholar
  34. Laska, M., Galizia, C. G., Giurfa, M., Menzel, R. 1999Olfactory discrimination ability and odour structure–activity relationships in honeybeesChem. Senses24429438PubMedGoogle Scholar
  35. Laviolette, S. R., Kooy, D. 2004The neurobiology of nicotine addiction: Bridging the gap from molecules to behaviourNat. Rev., Neurosci.55565CrossRefGoogle Scholar
  36. London-Shafir, I., Shafir, S., Eisikowitch, D. 2003Amygdalin in almond nectar and pollen—facts and possible rolesPlant Syst. Evol.2388795Google Scholar
  37. Manly, B. F. J. 1993Comments on design and analysis of multiple-choice feeding-preference experimentsOecologia93149152Google Scholar
  38. Masson, C., Pham-Del'Egue, M. H., Fonta, C., Gascuel, J., Arnold, G., Nicolas, G., Kerszberg, M. 1993Recent advances in the concept of adaptation to natural odour signals in the honeybee, Apis mellifera LApidologie24169194Google Scholar
  39. Menzel, R. 1993Associative learning in honeybeesApidologie24157168Google Scholar
  40. Naef, R., Jaquier, A., Velluz, A., Bachofen, B. 2004From the linden flower to linden honey—volatile constituents of linden nectar, the extract of bee-stomach and ripe honeyChem. Biodivers.118701879Google Scholar
  41. Ohnmeiss, T. E., Baldwin, I. T. 2000Optimal defense theory predicts the ontogeny of an induced nicotine defenseEcology8117651783Google Scholar
  42. Paldi, N., Zilber, S., Shafir, S. 2003Associative olfactory learning of honeybees to differential rewards in multiple contexts—Effect of odor component and mixture similarityJ. Chem. Ecol.2925152538PubMedCrossRefGoogle Scholar
  43. Renwik, J. A. A. 2001. Variable diets and changing taste in plant–insect relationships. J. Chem. Ecol. 1063–1075.Google Scholar
  44. Renwick, J. A. A., Lopez, K. 1999Experience-based food consumption by larvae of Pieris rapae: Addiction to glucosinolates?Entomol. Exp. Appl.915158CrossRefGoogle Scholar
  45. Rhoades, D. F., Bergdahl, J. C. 1981Adaptive significance of toxic nectarAm. Nat.117798803CrossRefGoogle Scholar
  46. Rosenthal, J. P., Berenbaum, M. R. 1991Herbivores: Their Interactions with Secondary Plant MetabolitesAcademic PressSan DiegoGoogle Scholar
  47. Schafer, W. R. 2004Addiction research in a simple animal model: the nematode Caenorhabditis elegansNeuropharmacology47123131PubMedCrossRefGoogle Scholar
  48. Shields, V. D. C., Mitchell, B. K. 1995The effect of phagostimulant mixtures on deterrent receptor(s) in two crucifer-feeding lepidopterous speciesPhilos. Trans. R. Soc. Lond., B347459464Google Scholar
  49. Singaravelan, N., Inbar, M., Ne'eman, G., Detzel, A., Wink, M., and Izhaki, I. 2006. The effects of nectar–nicotine on colony fitness of caged honeybees. J. Chem. Ecol. (In press).Google Scholar
  50. Struempf, H. M., Schondube, J. E., Rio, C. M. 1999The cyanogenic glycoside amygdalin does not deter consumption of ripe fruit by cedar waxwingsAuk116749758Google Scholar
  51. Sultana, I., Ikeda, I., Ozoe, Y. 2002Structure–activity relationships of benzylidene anabasines in nicotinic acetylcholine receptors of cockroach nerve cordsBioorg. Med. Chem.1029632971PubMedGoogle Scholar
  52. Tadmor-Melamed, H., Markman, S., Arieli, A., Distl, M., Wink, M., Izhaki, I. 2004Limited ability of Palestine sunbirds (Nectarinia osea) to cope with pyridine alkaloids in nectar of tree tobacco (Nicotiana glauca)Funct. Ecol.18844850CrossRefGoogle Scholar
  53. Dam, N. M., Jong, T. J., Iwasa, Y., Kubo, T. 1996Optimal distribution of defenses, are plants smart investors?Funct. Ecol.10128136Google Scholar
  54. Vitiello, M., Woods, S. C. 1977Caffeine: preferential consumption by ratsPharmacol. Biochem. Behav.3147149Google Scholar
  55. Wink, M. 1999. Function of plant secondary metabolites and their exploitation in biotechnology. Sheffield Academic Press and CRC Press, Annual Plant Reviews, Vol. 3, pp. 362.Google Scholar
  56. Wolf, F. W., Heberlein, U. 2003Invertebrate models of drug abuseJ. Neurobiol.54161178PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media, Inc. 2005

Authors and Affiliations

  • Natarajan Singaravelan
    • 1
  • Gidi Nee'man
    • 1
  • Moshe Inbar
    • 1
    • 2
  • Ido Izhaki
    • 1
  1. 1.Department of BiologyUniversity of Haifa at OranimTivonIsrael
  2. 2.Department of Evolutionary & Environmental BiologyUniversity of HaifaHaifaIsrael

Personalised recommendations