Advertisement

Behavioral Ecology and Sociobiology

, Volume 54, Issue 6, pp 578–586 | Cite as

Multi-source odor-marking of food by a stingless bee, Melipona mandacaia

  • James C. NiehEmail author
  • Santiago Ramírez
  • Paulo Nogueira-Neto
Original Article

Abstract

Social bees can deposit specialized glandular secretions, or signals, that allow foragers to revisit rewarding and to avoid unrewarding food sources. However, it is not known if bees can orient towards olfactory cues such as excreta deposited near food sources. We report that Melipona mandacaia foragers (stingless bees) deposit an odor cue, anal droplets, and a previously undescribed ventro-abdominal odor on food sources. Surprisingly, foragers deposited attractive odor marks on good food sources to which they recruited and on poor food sources to which they did not recruit. Foragers left the most anal droplets on dilute food sources to which they did not recruit (1.25-M sucrose solution), yet returning foragers were attracted to anal droplets obtained on poor food sources and presented in bioassays. Foragers were attracted to ventro-abdominal odors obtained on good food sources (2.5-M sucrose solution). Chemical extractions suggest that odor marks contain attractive polar compounds. We also provide the first detailed description of forager waggling and spinning behavior on poor and good food sources. Waggling may be a method of dispersing anal droplets and spinning may help foragers learn local landmarks.

Keywords

Chemical communication Olfactory cues Anal droplets Excreta Stingless bees 

Notes

Acknowledgements

We thank Zilá Luz Paulino Simões for generously providing supplies for our odor extraction experiments; Felipe A. L. Contrera and Vera L. Imperatriz-Fonseca for valuable assistance with the setup of the experiments; and Patrick Kelley for help with videotaping feeder behaviors. We would also like to thank caretakers Maridalva Arauso Dias and her husband Paulo Rovirsso Sousa Dias for their hospitality and hard work at the Fazenda Aretuzina. Melissa Thomas and four anonymous reviewers significantly enhanced the quality of this manuscript with their comments.

References

  1. Aguilar I, Sommeijer MJ (1996) Communication in stingless bees: are the anal substances deposited by Melipona favosa scent marks? Proc Sect Exp Appl Entomol Neth Entomol Soc 7:57−63Google Scholar
  2. Aguilar I, Sommeijer M (2001) The deposition of anal excretions by Melipona favosa foragers (Apidae: Meliponinae): behavioural observations concerning the location of food sources. Apidologie 32:37–48CrossRefGoogle Scholar
  3. Bakeman R, Gottman JM (1986) Observing interaction: an introduction to sequential analysis. Cambridge University Press, New YorkGoogle Scholar
  4. Bertsch A (1984) Foraging in male bumblebees ( Bombus lucorum L.): maximizing energy or minimizing water load? Oecologia 62:325–336Google Scholar
  5. Biesmeijer JC, de Vries H (2001) Exploration and exploitation of food sources by social insect colonies: a revision of the scout−recruit concept. Behav Ecol Sociobiol 49:89–99CrossRefGoogle Scholar
  6. Bradbury J, Vehrencamp SL (1988) Principles of animal communication. Sinauer, Sunderland, Mass.Google Scholar
  7. Capaldi EA, Dyer FC (1999) The role of orientation flights on homing performance in honeybees. J Exp Biol 202:1655–1666PubMedGoogle Scholar
  8. Cartwright BA, Collett TS (1983) Landmark learning in bees. J Comp Physiol A 151:521–543Google Scholar
  9. Cruz-Landim Dd (1967) Estudo comparativo de algumas glândulas das abelhas (Hymenoptera, Apoidea) e respectivas implicações evolutivas. Arq Zool (Sao Paulo) 15:177–290Google Scholar
  10. Cruz-López L, Patricio EFLRA, Morgan DE (2001) Sections of stingless bees: the Dufour gland of Nannotrigona testaceicornis. J Chem Ecol 27:69–80CrossRefPubMedGoogle Scholar
  11. Dusenbery DB (1992) Sensory ecology: how organisms acquire and respond to information. Freeman, New YorkGoogle Scholar
  12. Free JB, Williams IH (1983) Scent-marking of flowers by honeybees. J Apic Res 22:86–90Google Scholar
  13. Free JB, Williams I, Pickett JA, Ferguson AW, Martin AP (1982) Attractiveness of (Z)-11-eicosen-1-ol to foraging honeybees. J Apic Res 21:151–156Google Scholar
  14. Frisch K von (1967) The dance language and orientation of bees. Belknap, Cambridge, Mass.Google Scholar
  15. Goulson D, Stout JC, Langley J, Hughes WOH (2000) Identity and function of scent marks deposited by foraging bumblebees. J Chem Ecol 26:2897–2911Google Scholar
  16. Greenfield MD (2002) Signalers and receivers: mechanisms and evolution of arthropod communication. Oxford University Press, New YorkGoogle Scholar
  17. Hölldobler B, Wilson EO (1978) The multiple recruitment systems of the African weaver ant Oecophylla longinoda (Latreille) (Hymenoptera: Formicidae). Behav Ecol Sociobiol 3:19–60Google Scholar
  18. Hölldobler B, Wilson EO (1990) The ants. Belknap, Cambridge, Mass.Google Scholar
  19. Hrncir M, Jarau S, Zucchi R, Barth FG (2003) On the origin and properties of scent marks deposited at the food source by a stingless bee, Melipona seminigra Friese 1903. Apidologie (in press)Google Scholar
  20. Jander R (1997) Macroevolution of a fixed action pattern for learning: the exploration flights of bees and wasps. In: Greenberg G, Tobach E (eds) Comparative psychology of invertebrates: the field and laboratory study of insect behavior. Garland, New York, pp 79–99Google Scholar
  21. Jander U, Jander R (2002) Allometry and resolution of bee eyes (Apoidea). Arthropod Struct Dev 30:179–193CrossRefGoogle Scholar
  22. Jarau S, Hrncir M, Zucchi R, Barth FG (2002) Footprint pheromones used to mark food sources by stingless bees. In: Billen J (ed) XIV International Congress of IUSSI: The golden jubilee proceedings. Hokkaido University Coop, Hokkaido University, Sapporo, JapanGoogle Scholar
  23. Johnson LK (1981) Effect of flower clumping on defense of artificial flowers by aggressive stingless bees. Biotropica 13:151–157Google Scholar
  24. Kerr WE (1972) Orientação pelo sol em Trigona spinipes. Cienc Cult [Suppl]:341–342Google Scholar
  25. Kerr WE (1973) Sun compass orientation in the stingless bees, Trigona ( Trigona) spinipes (Fabricius, 1793) (Apidae). Anais Acad Bras Cien 45:301–308Google Scholar
  26. Kerr WE, Rocha R (1988) Comunicação em Melipona rufiventris e Melipona compressipes. Cien Cult 40:1200–1203Google Scholar
  27. Kerr W, Ferreira A, Simões de Mattos N (1963) Communication among stingless bees−additional data (Hymenoptera: Apidae). J NY Entomol Soc 71:80–90Google Scholar
  28. Lehrer M (1991) Bees which turn back and look. Naturwissenschaften 78:274–276Google Scholar
  29. Lehrer M (1993) Why do bees turn back and look? J Comp Physiol A 172:549–563Google Scholar
  30. Lehrer M, Collett TS (1994) Approaching and departing bees learn different cues to the distance of a landmark. J Comp Physiol A 175:171–177Google Scholar
  31. Lello E (1976) Adnexal glands of the sting apparatus in bees: anatomy and histology, V (Hymenoptera: Apidae). J Kans Entomol Soc 49:85–99Google Scholar
  32. Lindauer M, Kerr WE (1958) Die gegenseitige Verständigung bei den stachellosen Bienen. Z Vergl Physiol 41:405–434Google Scholar
  33. Linsenmair KE (1987) Kin recognition in subsocial arthropods, in particular in the desert isopod, Hemilepistus reaumuri. In: Fletcher DJC, Michener CD (eds) Kin recognition in animals. Wiley, New York, pp 121–208Google Scholar
  34. Nicolson SW (1990) Osmoregulation in a nectar-feeding insect, the carpenter bee, Xylocopa capitata: water excess and ion conservation. Physiol Entomol 15:433–440Google Scholar
  35. Nieh JC (1998) The role of a scent beacon in the communication of food location in the stingless bee, Melipona panamica. Behav Ecol Sociobiol 43:47–58CrossRefGoogle Scholar
  36. Nieh JC, Roubik DW (1995) A stingless bee ( Melipona panamica) indicates food location without using a scent trail. Behav Ecol Sociobiol 37:63–70CrossRefGoogle Scholar
  37. Nieh JC, Contrera FAL, Ramírez S, Imperatriz-Fonseca VL (2003) Variation in the ability to communicate 3-D resource location by stingless bees from different habitats. Anim Behav (in press)Google Scholar
  38. Nogueira-Neto P (1997) Vida e criação de abelhas indígenas sem ferrão. Nogueirapis, Sao PauloGoogle Scholar
  39. O'Neal MCA, Markin JP (1973) Brood nutrition and parental relationships of the imported fire ant, Solenopsis invicta. J Ga Entomol Soc 8:294–303Google Scholar
  40. Pasedach-Poeverlein K (1940) Über das "Spritzen" der Bienen und über die Konzentrationsänderung ihres Honigblaseninhalts. Z Vergl Physiol 28:197–210Google Scholar
  41. Pflumm W (1969) Beziehungen zwischen Putzverhalten und Sammelbereitschaft bei der Honigbiene. Z Vergl Physiol 64:1–36Google Scholar
  42. Pflumm W (1973) Zur Steuerung der Putzbewegungen der Honigbiene. Behaviour 45:104–122Google Scholar
  43. Pflumm W (1983) Zum Sammel− und Putzverhalten der Honigbiene auf einer Abblühenden Zwergmispel ( Cotoneaster horizontalis). Behaviour 83:112–131Google Scholar
  44. Qiu PY, Ding HB, Tang YK, Xu RJ (1999) Determination of chemical composition of commercial honey by near-infrared spectroscopy. J Agric Food Chem 47:2760–2765CrossRefPubMedGoogle Scholar
  45. Rau G (1970) Zur Steuerung der Honigmagenfüllung sammelnder Bienen an einer künstlichen Futterquelle. Z Vergl Physiol 66:1–21Google Scholar
  46. Rizzini CT (1997) Tratado de fitogeografia do Brasil, 2nd edn. Âmbito Cultural, Rio de JaneiroGoogle Scholar
  47. Rocha ESMO (1970) Raiding in Melipona rufiventris flavolineata. In: Ceccato S (ed) Proceedings of the 22nd annual meeting of the sociedade brasileira para o progresso da ciencia. Soc Bras Prog Cienc (Brazil)Google Scholar
  48. Roubik DW (1980) Foraging behavior of competing Africanized honeybees and stingless bees. Ecology 61:836–845Google Scholar
  49. Roubik DW (1989) Ecology and natural history of tropical bees. Cambridge University Press, New YorkGoogle Scholar
  50. Roubik DW, Yanega D, Aluja SM, Buchmann SL, Inouye DW (1995) On optimal nectar foraging by some tropical bees (Hymenoptera: Apidae). Apidologie 26:197–211Google Scholar
  51. Schmidt VM, Zucchi R, Barth FG (2003) A stingless bee marks the feeding site in addition to the scent path (Scaptotrigona aff. deplis). Apidologie 34:237–248Google Scholar
  52. Seeley TD (1989) The honey bee colony as a superorganism. Am Sci 77:546–553Google Scholar
  53. Snyder LR, Kirkland JJ (1979) Introduction to modern liquid chromatography, 2nd edn. Wiley, New YorkGoogle Scholar
  54. Stout JC, Goulson D (2001) The use of conspecific and interspecific scent marks by foraging bumblebees and honeybees. Anim Behav 62:183–189CrossRefGoogle Scholar
  55. Stout JC, Goulson D, Allen JA (1998) Repellent scent-marking of flowers by a guild of foraging bumblebees ( Bombus spp.). Behav Ecol Sociobiol 43:317–326Google Scholar
  56. Zeil J, Kelber A, Voss R (1996) Structure and function of learning flights in bees and wasps. J Exp Biol 199:245–252PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • James C. Nieh
    • 1
    Email author
  • Santiago Ramírez
    • 2
  • Paulo Nogueira-Neto
    • 3
  1. 1.University of California San DiegoLa JollaUSA
  2. 2.Department of Organismic and Evolutionary BiologyHarvard UniversityCambridgeUSA
  3. 3.Bee Laboratory, Instituto BiocienciasUniversity of São PauloSão Paulo Brazil

Personalised recommendations