No Trade-Off between Learning Speed and Associative Flexibility in Bumblebees: A Reversal Learning Test with Multiple Colonies

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Raine, Nigel E ^a,b   Chittka, Lars ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTHROPOD COMMUNITY; ARTICLE; ASSOCIATION; BUMBLEBEE; COGNITION; COGNITIVE FLEXIBILITY; COLOR DISCRIMINATION; CONTROLLED STUDY; LEARNING; LEARNING SPEED; LEARNING TEST; MEMORY CONSOLIDATION; NONHUMAN; REWARD; WORKER (INSECT);

ANIMALS; ASSOCIATION LEARNING; BEES; CHOICE BEHAVIOR; COLOR; FEEDING BEHAVIOR; FLOWERS; HIERARCHY, SOCIAL; REVERSAL LEARNING;

APOIDEA; BOMBUS TERRESTRIS;

EID: 84866702333     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0045096     Document Type: Article

References (67)

1. Dukas R, Bernays EA, (2000) Learning improves growth rate in grasshoppers. Proceedings of the National Academy of Sciences of the United States of America 97: 2637-2640.
2. Dukas R, Duan JJ, (2000) Fitness consequences of associative learning in a parasitoid wasp. Behavioral Ecology 11: 536-543.
3. Mery F, Kawecki TJ, (2003) A fitness cost of learning ability in Drosophila melanogaster. Proceedings of the Royal Society B: Biological Sciences 270: 2465-2469.
4. Mery F, Kawecki TJ, (2004) An operating cost of learning in Drosophila melanogaster. Animal Behaviour 68: 589-598.
5. Mery F, Kawecki TJ, (2005) A cost of long-term memory in Drosophila. Science 308: 1148.
6. Raine NE, Chittka L, (2008) The correlation of learning speed and natural foraging success in bumble-bees. Proceedings of the Royal Society B: Biological Sciences 275: 803-808.
7. Mery F, Belay AT, So AKC, Sokolowski MB, Kawecki TJ, (2007) Natural polymorphism affecting learning and memory in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 104: 13051-13055.
8. Papaj DR, Snell-Rood EC, (2007) Memory flies sooner from flies that learn faster. Proceedings of the National Academy of Sciences of the United States of America 104: 13539-13540.
9. Bolhuis JJ, (1991) Mechanisms of avian imprinting- a review. Biological Reviews of the Cambridge Philosophical Society 66: 303-345.
10. Dukas R, Real LA, (1993) Effects of nectar variance on learning by bumble bees. Animal Behaviour 45: 37-41.
11. Dukas R (1998) Evolutionary ecology of learning. In: Dukas R, ed. Cognitive Ecology: the Evolutionary Ecology of Information Processing and Decsion Making, University of Chicago Press: Chicago/USA. pp. 129-174.
12. Pavlov IP (1927) Lectures on Conditioned Reflexes. New York: International Publishers.
13. Bitterman ME, (1965) Phyletic differences in learning. American Psychologist 20: 396-410.
14. Bond AB, Kamil AC, Balda RP, (2007) Serial reversal learning and the evolution of behavioral flexibility in three species of North American corvids (Gymnorhinus cyanocephalus, Nucifraga columbiana, Aphelocoma californica). Journal of Comparative Pyschology 121: 373-379.
15. Kehagia AA, Murray GK, Robbins TW, (2010) Learning and cognitive flexibility: frontostriatal function and monoaminergic modulation. Current Opinion in Neurobiology 20: 199-204.
16. Rygula R, Walker SC, Clarke HF, Robbins TW, Roberts AC, (2010) Differential contributions of the primate ventrolateral prefrontal and orbitofrontal cortex to serial reversal learning. Journal of Neuroscience 30: 14552-14559.
17. Parker MO, Gaviria J, Haigh A, Millington ME, Brown VJ, Combe FJ, Brennan CH, (2012) Discrimination reversal and attentional sets in zebrafish (Danio rerio). Behavioural Brain Research 232: 264-268.
18. Eisenhardt D, Menzel R, (2007) Extinction learning, reconsolidation and the internal reinforcement hypothesis. Neurobiology of Learning and Memory 87: 167-173.
19. Brown VJ, Tait DS (2010) Behavioral flexibility: attentional shifting, rule switching and response reversal. In: Stolerman IP, ed. Encyclopedia of Psychopharmacology, Springer-Verlag: Berlin. pp. 209-213.
20. Bouton ME, (2004) Context and behavioral processes in extinction. Learning & Memory 11: 485-494.
21. Dalley JW, Cardinal RN, Robbins TW, (2004) Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neuroscience and Biobehavioral Reviews 28: 771-784.
22. Myers KM, Davis M, (2002) Behavioral and neural analysis of extinction. Neuron 36: 567-584.
23. Stollhoff N, Menzel R, Eisenhardt D, (2005) Spontaneous recovery from extinction depends on the reconsolidation of the acquisition memory in an appetitive learning paradigm in the honeybee (Apis mellifera). Journal of Neuroscience 25: 4485-4492.
24. Heinrich B, (1976) The foraging specializations of individual bumblebees. Ecological Monographs 46: 105-128.
25. Raine NE, Chittka L, (2007) Nectar production rates of 75 bumblebee-visited flower species in a German flora (Hymenoptera: Apidae: Bombus terrestris). Entomologia Generalis 30: 191-192.
26. Willmer PG, Stone GN, (2004) Behavioral, ecological, and physiological determinants of the activity patterns of bees. Advances in the Study of Behavior 34: 347-466.
27. Raine NE, Ings TC, Ramos-Rodríguez O, Chittka L, (2006) Intercolony variation in learning performance of a wild British bumblebee population (Hymenoptera: Apidae: Bombus terrestris audax). Entomologia Generalis 28: 241-256.
28. Mallon EB, Brockmann A, Schmid-Hempel P, (2003) Immune response inhibits associative learning in insects. Proceedings of the Royal Society B: Biological Sciences 270: 2471-2473.
29. Alghamdi A, Dalton L, Phillis A, Rosato E, Mallon EB, (2008) Immune response impairs learning in free-flying bumble-bees. Biology Letters 4: 479-481.
30. Alghamdi A, Raine NE, Rosato E, Mallon EB, (2009) No evidence for an evolutionary trade-off between learning and immunity in a social insect. Biology Letters 5: 55-57.
31. McGaugh JL, (2000) Memory- a century of consolidation. Science 287: 248-251.
32. Chittka L, (1998) Sensorimotor learning in bumblebees: long-term retention and reversal training. Journal of Experimental Biology 201: 515-524.
33. Chittka L, Thomson JD, (1997) Sensori-motor learning and its relevance for task specialization in bumble bees. Behavioral Ecology and Sociobiology 41: 385-398.
34. Woodward GL, Laverty TM, (1992) Recall of flower handling skills by bumble bees: a test of Darwin's interference hypothesis. Animal Behaviour 44: 1045-1051.
35. Dudai Y, (2004) The neurobiology of consolidations, or, how stable is the engram? Annual Review of Psychology 55: 51-86.
36. Hadar R, Menzel R, (2010) Memory formation in reversal learning of the honeybee. Frontiers in Behavioral Neuroscience 4: 186.
37. Bitterman ME, (1976) Incentive contrast in honeybees. Science 192: 380-382.
38. Mota T, Giurfa M, (2010) Multiple reversal olfactory learning in honeybees. Frontiers in Behavioral Neuroscience 4: 1-9.
39. Brandes C, (1988) Estimation of heritability of learning behaviour in honeybees (Apis mellifera capensis). Behavior Genetics 18: 119-132.
40. Latshaw JS, Smith BH, (2005) Heritable variation in learning performance affects foraging preferences in the honey bee (Apis mellifera). Behavioral Ecology and Sociobiology 58: 200-207.
41. Laloi D, Pham-Delègue MH, (2010) Patriline-level variability in olfactory learning in the honey bee. Apidologie 41: 436-442.
42. Raine NE, Ings TC, Dornhaus A, Saleh N, Chittka L, (2006) Adaptation, genetic drift, pleiotropy, and history in the evolution of bee foraging behavior. Advances in the Study of Behavior 36: 305-354.
43. Lunau K, Wacht S, Chittka L, (1996) Colour choices of naive bumble bees and their implications for colour perception. Journal of Comparative Physiology A 178: 477-489.
44. Worden BD, Skemp AK, Papaj DR, (2005) Learning in two contexts: the effects of interference and body size in bumblebees. Journal of Experimental Biology 208: 2045-2053.
45. Riveros AJ, Gronenberg W, (2009) Olfactory learning and memory in the bumblebee Bombus occidentalis. Naturwissenschaften 96: 851-856.
46. Spaethe J, Brockmann A, Halbig C, Tautz J, (2007) Size determines antennal sensitivity and behavioral threshold to odors in bumblebee workers. Naturwissenschaften 94: 733-739.
47. Spaethe J, Chittka L, (2003) Interindividual variation of eye optics and single object resolution in bumblebees. Journal of Experimental Biology 206: 3447-3453.
48. Ings TC, Raine NE, Chittka L, (2009) A population comparison of the strength and persistence of innate colour preference and learning speed in the bumblebee Bombus terrestris. Behavioral Ecology and Sociobiology 63: 1207-1218.
49. Cnaani J, Thompson JD, Papaj DR, (2006) Flower choice and learning in foraging bumblebees: effects of variation in nectar volume and concentration. Ethology 112: 278-285.
50. Scheiner R, Page RE, Erber J, (2001) Responsiveness to sucrose affects tactile and olfactory learning in preforaging honey bees of two genetic strains. Behavioural Brain Research 120: 67-73.
51. Bell AM, (2007) Future directions in behavioural syndromes research. Proceedings of the Royal Society B: Biological Sciences 274: 755-761.
52. Briffa M, Rundle SD, Fryer A, (2008) Comparing the strength of behavioural plasticity and consistency across situations: animal personalities in the hermit crab Pagurus bernhardus. Proceedings of the Royal Society B: Biological Sciences 275: 1305-1311.
53. Sih A, Bell A, Johnson JC, (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends in Ecology & Evolution 19: 372-378.
54. Deary IJ (2001) Intelligence: a very short introduction. Oxford: Oxford University Press.
55. Roth G, Dicke U, (2005) Evolution of the brain and intelligence. Trends in Cognitive Sciences 9: 250-257.
56. Reader SM, Hager Y, Laland KN, (2011) The evolution of primate general and cultural intelligence. Proceedings of the Royal Society B: Biological Sciences 366: 1017-1027.
57. Chittka L, Skorupski P, Raine NE, (2009) Speed-accuracy tradeoffs in animal decision making. Trends in Ecology & Evolution 24: 400-407.
58. Heinrich B, (1979) "Majoring" and "minoring" by foraging bumblebees, Bombus vagans: an experimental analysis. Ecology 60: 245-255.
59. Raine NE, Chittka L, (2007) Flower constancy and memory dynamics in bumblebees (Hymenoptera: Apidae: Bombus). Entomologia Generalis 29: 179-199.
60. Menzel R, Greggers U, Hammer M (1993) Functional organization of appetitive learning and memory in a generalist pollinator, the honey bee. In: Papaj D, Lewis AC, eds. Insect Learning: Ecological and Evolutionary Perspectives, Chapman & Hall: New York. pp. 79-125.
61. Menzel R, (1968) Das Gedächtnis der Honigbiene für Spektralfarben. I. Kurzzeitiges und langzeitiges Behalten. Zeitschrift fur Vergleichende Physiologie 60: 82-102.
62. Scheiner R, Erber J, Page RE, (1999) Tactile learning and the individual evaluation of the reward in honey bees (Apis mellifera L.). Journal of Comparative Physiology A 185: 1-10.
63. Menzel R, (1993) Associative learning in honeybees. Apidologie 24: 157-168.
64. Menzel R, (1969) Das Gedächtnis der Honigbiene für Spektralfarben. II. Umlernen und Mehrfachlernen. Zeitschrift fur Vergleichende Physiologie 63: 290-309.
65. Tighe TJ, (1965) Effect of overtraining on reversal and extradimensional shifts. Journal of Experimental Psychology 70: 13-17.
66. Komischke B, Giurfa M, Lachnit H, Malun D, (2002) Successive olfactory reversal learning in honeybees. Learning and Memory 9: 122-129.
67. Scheiner R, Page RE, Erber J, (2004) Sucrose responsiveness and behavioral plasticity in honey bees (Apis mellifera). Apidologie 35: 133-142.