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Journal of Comparative Physiology A

, Volume 197, Issue 6, pp 641–651 | Cite as

Diminishing returns: the influence of experience and environment on time-memory extinction in honey bee foragers

  • Darrell MooreEmail author
  • Byron N. Van Nest
  • Edith Seier
Original Paper

Abstract

Classical experiments demonstrated that honey bee foragers trained to collect food at virtually any time of day will return to that food source on subsequent days with a remarkable degree of temporal accuracy. This versatile time-memory, based on an endogenous circadian clock, presumably enables foragers to schedule their reconnaissance flights to best take advantage of the daily rhythms of nectar and pollen availability in different species of flowers. It is commonly believed that the time-memory rapidly extinguishes if not reinforced daily, thus enabling foragers to switch quickly from relatively poor sources to more productive ones. On the other hand, it is also commonly thought that extinction of the time-memory is slow enough to permit foragers to ‘remember’ the food source over a day or two of bad weather. What exactly is the time-course of time-memory extinction? In a series of field experiments, we determined that the level of food-anticipatory activity (FAA) directed at a food source is not rapidly extinguished and, furthermore, the time-course of extinction is dependent upon the amount of experience accumulated by the forager at that source. We also found that FAA is prolonged in response to inclement weather, indicating that time-memory extinction is not a simple decay function but is responsive to environmental changes. These results provide insights into the adaptability of FAA under natural conditions.

Keywords

Honey bees Time-memory Foraging Circadian rhythms Food-anticipatory activity 

Notes

Acknowledgments

We thank Trevor England, Neha Barakam, Brad Barker, Arianna Bruno, Stefani Coleman, Christopher Cronan, Patrick Doherty, Erica Edmund, Alison Gagan, Forrest Harrison, Jenny Hoekstra, Jonathan Humberd, Nathan Humphrey, Jennifer Johnson, Tannille King, Guy Kramer, Adam Lewis, Christopher Litchfield, T.J. Metcalf, Jaime McManus, Charles Miller, Samara Miller, Somer Miller, Mary Ann Moore, Matt Otto, Caleb Paquette, Lia Pun-Chuen, Ryan Rice, Lindsay Slemp, Will Smith, Kim Stroup, Jack Whitaker, Jeremey Whitaker, Anthony Whitted, Ashley Williams, and Dmitri Yampolsky for help with the field experiments. We also thank two anonymous reviewers for valuable suggestions that strengthened the manuscript. This work was supported by funds from the National Research Initiative of the USDA Cooperative State Research, Education, and Extension Service, Grant No. 2006-35302-17278 (D.M.) and the Department of Biological Sciences, East Tennessee State University, Denise I. Pav Research Award (B.V.N.). The present study complies with the current laws of the country in which the experiments were performed, including the ‘Principles of Animal Care’, Publication No. 86-23, revised 1985 of the National Institutes of Health.

References

  1. Beier W (1968) Beeinflussung der inneren Uhr der Bienen durch Phasenverschiebung des Licht-Dunkel-Zeitgebers. Z Bienenforschung 9:356–378Google Scholar
  2. Beier W, Lindauer M (1970) Der Sonnenstand als Zeitgeber für die Biene. Apidologie 1:5–28CrossRefGoogle Scholar
  3. Beling I (1929) Über das Zeitgedächtnis der Bienen. Z vergl Physiol 9:259–388CrossRefGoogle Scholar
  4. Bitterman ME, Menzel R, Fietz A, Schäfer S (1983) Classical conditioning of proboscis extension in honeybees (Apis mellifera). J Comp Psychol 97:107–119PubMedCrossRefGoogle Scholar
  5. Bouton ME (2007) Learning and behavior: a contemporary synthesis. Sinauer, Sunderland, MassachusettsGoogle Scholar
  6. Brady J (1981) Behavioral rhythms in invertebrates. In: Aschoff J (ed) Handbook of behavioral neurobiology, vol 4. Plenum Press, New York, pp 125–144Google Scholar
  7. Butler CG (1945) The influence of various physical and biological factors of the environment on honeybee activity. An examination of the relationship between activity and nectar concentration and abundance. J Exp Biol 21:5–12Google Scholar
  8. Corbet SA, Delfosse ES (1984) Honeybees and the nectar of Echium plantagineum L. in southeastern Australia. Aust J Ecol 9:125–139CrossRefGoogle Scholar
  9. Daan S, Beersma DGM, Borbély AA (1984) Timing of human sleep: recovery process gated by a circadian pacemaker. Am J Physiol 246:R161–R183PubMedGoogle Scholar
  10. Frisch B, Aschoff J (1987) Circadian rhythms in honeybees: entrainment by feeding cycles. Physiol Entomol 12:41–49CrossRefGoogle Scholar
  11. Gallistel CR (1990) The organization of learning. The MIT Press, CambridgeGoogle Scholar
  12. Giurfa M, Núñez JA (1992) Foraging by honeybees on Carduus acanthoides: pattern and efficiency. Ecol Entomol 17:326–330CrossRefGoogle Scholar
  13. Hogan JA (1997) Energy models of motivation: a reconsideration. Appl Anim Behav Sci 53:89–105CrossRefGoogle Scholar
  14. Jenkins J, Dallenbach K (1924) Oblivescence during sleep and walking. Am J Psych 35:605–612CrossRefGoogle Scholar
  15. Kleber E (1935) Hat das Zeitgedächtnis der Bienen biologische Bedeutung? Z vergl Physiol 22:221–262CrossRefGoogle Scholar
  16. Lindauer M (1948) Über die Einwirkung von Duft- und Geschmacksstoffen sowie anderer Faktoren auf die Tänze der Bienen. Z vergl Physiol 31:348–412CrossRefGoogle Scholar
  17. Meder E (1958) Über die Einberechtung der Sonnenwanderung bei der Orientierung der Honigbiene. Z vergl Physiol 40:610–641CrossRefGoogle Scholar
  18. Menzel R (1999) Memory dynamics in the honeybee. J Comp Physiol A 185:323–340CrossRefGoogle Scholar
  19. Minami H, Dallenbach K (1946) the effect of activity upon learning and retention in the cockroach, Periplaneta americana. Am J Psych 59:1–58CrossRefGoogle Scholar
  20. Moore D (2001) Honey bee circadian clocks: behavioral control from individual workers to whole-colony rhythms. J Insect Physiol 47:843–857CrossRefGoogle Scholar
  21. Moore D, Doherty P (2009) Acquisition of a time-memory in forager honey bees. J Comp Physiol A 195:741–751CrossRefGoogle Scholar
  22. Moore D, Rankin MA (1983) Diurnal changes in the accuracy of the honeybee foraging rhythm. Biol Bull 164:471–482CrossRefGoogle Scholar
  23. Moore D, Siegfried D, Wilson R, Rankin MA (1989) The influence of time of day on the foraging behavior of the honeybee, Apis mellifera. J Biol Rhythms 4:305–325PubMedCrossRefGoogle Scholar
  24. Pittendrigh CS (1958) Perspectives in the study of biological clocks. In: Buzzati-Traverso AA (ed) Perspectives in marine biology. University of California Press, Berkeley, pp 239–268Google Scholar
  25. Rabinowitch HD, Fahn A, Meir T, Lensky Y (1993) Flower and nectar attributes of pepper (Capsicum annuum L.) plants in relation to their attractiveness to honeybees (Apis mellifera L.). Ann Appl Biol 123:221–232CrossRefGoogle Scholar
  26. Renner M (1955) Über die Haltung von Bienen in geschlossenen, künstlich beleuchteten Räumen. Naturwissenschaften 42:539–540CrossRefGoogle Scholar
  27. Renner M (1957) Neue Versuche über den Zietsinn der Honigbiene. Z vergl Physiol 40:85–118CrossRefGoogle Scholar
  28. Sandoz J-C, Pham-Delegue M-H (2004) Spontaneous recovery after extinction of the conditioned proboscis extension response in the honeybee. Learn Mem 11:586–597PubMedCrossRefGoogle Scholar
  29. Sangha S, McComb C, Lukowiak K (2003) Forgetting and the extension of memory in Lymnaea. J Exp Biol 206:71–77PubMedCrossRefGoogle Scholar
  30. Saunders DS (2002) Insect clocks. Elsevier Press, BostonGoogle Scholar
  31. Seeley TD (1986) Social foraging by honeybees: how colonies allocate foragers among patches of flowers. Behav Ecol Sociobiol 19:343–354CrossRefGoogle Scholar
  32. Seeley TD (1989) Social foraging in honeybees: how nectar foragers assess their colony’s nutritional status. Behav Ecol Sociobiol 24:181–199CrossRefGoogle Scholar
  33. Seeley TD, Towne WF (1992) Tactics of dance choice in honey bees: do foragers compare dances? Behav Ecol Sociobiol 30:59–69CrossRefGoogle Scholar
  34. Seeley TD, Camazine S, Sneyd J (1991) Collective decision-making in honey bees: how colonies choose among nectar sources. Behav Ecol Sociobiol 28:277–290CrossRefGoogle Scholar
  35. Seeley TD, Kühnholz S, Weidenmüller A (1996) The honey bee’s tremble dance stimulates additional bees to function as nectar receivers. Behav Ecol Sociobiol 39:419–427CrossRefGoogle Scholar
  36. Takeda K (1961) Classical conditioned responses in the honey bee. J Insect Physiol 6:168–179CrossRefGoogle Scholar
  37. Tautz J (2008) The buzz about bees. Springer, BerlinCrossRefGoogle Scholar
  38. Terry WS (2003) Learning and memory: basic principles, processes, and procedures. Allyn and Bacon, BostonGoogle Scholar
  39. Visscher PK, Seeley TD (1982) Foraging strategy of honeybee colonies in a temperate deciduous forest. Ecology 63:1790–1801CrossRefGoogle Scholar
  40. von Frisch K (1950) Die Sonne als Kompass im Leben der Bienen. Experientia 6:65–69CrossRefGoogle Scholar
  41. von Frisch K (1967) The dance language and orientation of bees. Harvard University Press, CambridgeGoogle Scholar
  42. von Frisch K, Lindauer M (1954) Himmel und Erde in Konkurrenz bei der Orientierung der Bienen. Naturwissenschaften 41:245–253CrossRefGoogle Scholar
  43. Wahl O (1932) Neue Untersuchungen über das Zeitgedächtnis der Bienen. Z vergl Physiol 16:529–589Google Scholar
  44. Wahl O (1933) Beitrag zur Frage der biologischen Bedeutung des Zeitgedächtnisses der Bienen. Z vergl Physiol 18:709–717Google Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Darrell Moore
    • 1
    Email author
  • Byron N. Van Nest
    • 1
  • Edith Seier
    • 2
  1. 1.Department of Biological SciencesEast Tennessee State UniversityJohnson CityUSA
  2. 2.Department of Mathematics and StatisticsEast Tennessee State UniversityJohnson CityUSA

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