Proboscis conditioning experiments with honeybees, Apis mellifera caucasica, with butyric acid and DEET mixture as conditioned and unconditioned stimuli

Journal of Insect Science

Volumn 10, Issue , 2010, Pages

  Abramson, Charles I ^a   Giray, Tugrul ^b   Mixson, T Andrew ^a   Nolf, Sondra L ^a   Wells, Harrington ^d   Kence, Aykut ^c   Kence, Meral ^c  

^a OKLAHOMA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF PUERTO RICO   (Puerto Rico)

^c MIDDLE EAST TECHNICAL UNIVERSITY   (Turkey)

^d UNIVERSITY OF TULSA   (United States)

Author keywords

classical conditioning; insect control; learning

Indexed keywords

ANIMALIA; APIDAE; APIS MELLIFERA; APIS MELLIFERA CAUCASICA; APOIDEA; CINNAMOMUM VERUM; HEXAPODA; HYMENOPTERA; LAVANDULA;

BUTYRIC ACID; DIETHYLTOLUAMIDE; INSECT REPELLENT;

ANIMAL; ARTICLE; BEE; CONDITIONED REFLEX;

ANIMALS; BEES; BUTYRIC ACID; CONDITIONING, CLASSICAL; DEET; INSECT REPELLENTS;

EID: 77957594358     PISSN: None     EISSN: 15362442     Source Type: Journal    
DOI: 10.1673/031.010.12201     Document Type: Article

References (64)

1. Abramson CI. 1994. A primer of invertebrate learning: the behavioral perspective. American Psychological Association.
2. Abramson CI 1986. Aversive conditioning in honeybees (Apis mellifera). Journal of Comparative Psychology 100: 108-116.
3. Abramson CI, Bitterman ME 1986a. Latent inhibition in honeybees. Animal Learning and Behavior 13: 184-189.
4. Abramson CI, Bitterman ME 1986b. The US-preexposure effect in honeybees. Animal Learning and Behavior 14: 374-379.
5. Abramson CI, Boyd BJ 2001. An automated apparatus for conditioning proboscis extension in honeybees (Apis mellifera L.). Journal of Entomological Science 36: 78-92.
6. Abramson CI, Aquino SI, Azeredo GA, Filho JR, Price JM.1997. The attraction of africanized honeybees (Apis mellifera L.) to soft drinks and perfumes. Journal of General Psychology 124: 166-181.
7. Abramson CI, Nolf SL, Mixson TA, Wells H 2010. Can honey bees learn the removal of a stimulus as a conditioning cue? Ethology, in press
8. Abramson CI, Singleton JB, Wilson MK, Wanderley PA, Ramalho FS, Michaluk LM. 2006a. The effect of an organic pesticide on mortality and learning in africanized honeybees (Apis mellifera L.) in Brasil. American Journal of Environmental Sciences 2: 37-44.
9. Abramson CI, Wilson MK, Singleton JB, Wanderley PA, Wanderley MJ, Michaluk LM. 2006b. Citronella is not a repellent to Africanized honeybees Apis mellifera L. (Hymenoptera: Apidae). BioAssay 1: 1-7.
10. Agarwal VM, Rastogi N. 2008. Role of floral repellents in the regulation of flower visits of extrafloral nectar-visiting ants in an Indian crop plant. Ecological Entomology 33: 59-65.
11. Apfelbach R, Blanchard CD, Blanchard RJ, Hayes RA, McGregor IS. 2005. The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neuroscience and Biobehavioral Reviews 29: 1123-1144.
12. Atkins Jr. EL, McDonald RL, Greywood-Hale EA. 1975a. Repellent additives to reduce pesticide hazards to honeybees: field tests. Journal of Environmental Entomology 4: 207-210.
13. Atkins Jr., EL, McDonald, RL, McGouern TD, Beroza M., Greywood-Hale E. 1975b. Repellent additives to reduce pesticide hazards to honeybees: laboratory testing. Journal of Apiculture Research 14: 85-97.
14. Averill AL, Prokopy RJ. 1987. Residual activity of oviposition-detering pheremone in Rhagoletis pomonella (Diptera: Tephritidae) and female response to infested fruit. Journal of Chemical Ecolology 13: 167-177.
15. Baayen RH, Davidson DJ, Bates DM. 2008. Mixed-effects modeling with crossed random effects for subjects and items. Journal of Memory and Language 59: 390-412.
16. Baker SE, Elwood SA, Watkins R, MacDonald DW. 2005. Non-lethal control of wildlife: using chemical repellents as feeding deterrents for the European badger Meles meles. Journal of Applied Ecolology 42: 921-931.
17. Blum MS, Fales HM, Tucker KW, Collins AM. 1978. Chemistry of the sting apparatus of the worker honeybee. Journal of Apiculture Research 17: 218-221.
18. Bodur C, Kence M, Kence A. 2007. Genetic structure of honeybee, Apis mellifera L. (Hymenoptera: Apidae) populations of Turkey inferred from microsatellite analysis. Journal of Apicultre Research 46: 60-67.
19. Brunner E, Puri ML. 2001. Non-parametric methods in factorial designs. Statistical Papers 42: 1-52.
20. Carroll JF, Benante JP, Klun JA, White CE, Debboun M, Pound JM., et al. 2008. Twelve-hour duration testing of cream formulations of three repellents against Ambylomma americanum. Medical and Veterinary Entomology 22: 144-151.
21. Cochran WG. 1950. The comparison of percentages in matched samples. Biometrika 37: 256-266.
22. Crittenden JR., Skoulakis, EMC., Han, K-A., Kalderon D., Davis, R.L. 1998. Tripartice mushroom body architecture revealed by antigenic markers. Learning and Memory 5:38-51.
23. D'Agostino R. 1971. A second look at analysis of variance on dichotomous data. Journal of Educational Measurement 8: 327-333.
24. Davis RL. 1993. Mushroom bodies and Drosophila learning. Neuron 11: 1-14.
25. Davis CS. 2002. Statistical methods for analysis of repeated measurements. Springer Verlag.
26. Ditzen M, Pellegrino M, Vosshall LB. 2008. Insect odorant receptors are molecular targets of the insect repellent DEET. Science 319: 1838-1842.
27. Dupuy F, Sandoz J-C, Giurfa M, Josens R. 2006. Individual olfactory learning in Camponotus ants. Animal Behavior 72: 1081-1091.
28. Erber J, Masuhr T, Menzel R. 1980. Localization of short-term memory in the brain of the bee, Apis mellifera. Physiological Entomology 5: 343-358.
29. Estes WK, Skinner BF. 1941. Some quantitative properties of anxiety. Journal of Experimental Psychology 29: 390-400.
30. Fahrbach SE, Robinson GE. 1995. Behavioral development in the honeybee: toward the study of learning under natural conditions. Learning and Memory 2: 199-224.
31. Fahrbach SE, Giray T, Robinson GE. 1995. Volume changes in the mushroom bodies of adult honeybee queens. Neurobiology of Learning and Memory 63:181-191.
32. Fahrbach SE, Giray, T, Farris SM, Robinson GE. 1997. Expansion of the neuropil of the mushroom bodies in male honeybees is coincident with initiation of flight. Neuroscience Letters 236: 135-138.
33. Free JB. 1987. Pheremones of social bees. Chapman Hall.
34. Free JB, Ferguson AW, Simpkins JR. 1989. Honeybee responses to chemical components from the worker sting apparatus mandibular glands in field tests. Journal of Apiculture Research 28: 7-21.
35. Ganesan K, Mendki MJ, Suryanarayana MV, Prakash S, Malhotra RC. 2006. Studies of Aedes aegypti (Diptera: Culicidae) ovipositional reponses ot newly identified semiochemcials from conspecific eggs. Australian Journal of Entomology 45: 75-80.
36. Giurfa M. 2007. Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well. Journal of Comparative Physiology A 193: 801-824.
37. Graham JM (editor). 1992. The hive and the honeybee. Dadant and Sons.
38. Griswold CK, Gomulkiewicz R, Heckman N. 2008. Hypothesis testing in experimental studies of function-valued traits. Evolution 62: 1229-1242.
39. Heffernan DJ, Andelt WF, Shivik JA. 2007. Coyote investigative behavior following removal of novel stimuli. Journal of Wildlife Management 71: 587-593.
40. Heisenberg M. 1980. Mutants of brain structure and function: what is the significance of the mushroom bodies for behaviour? In: Siddigui O, Babu P, Hall LM, Hall JC, editors. pp. 337-390, Development and Biology of Drosophila. Plenum.
41. Heisenberg M, Borst A, Wagner S, Byers D. 1985. Drosophila mushroom body mutants are deficient in olfactory learning. Journal of Neurogenetics 2: 1-30.
42. Isaac B, Hoffman CM. 2002. n-Butyric anhydride-abiotic biodegradation: hydrolysis. Final Report #1204-HYD. Prepared by Eastman Kodak Company.
43. Isman MB. 2006. Botanical insecticides, deterrents, and repellents in modern agriculture in an increasingly regulated world. Annual Review of Entomology 51: 45-66.
44. Kandemir I, Kence M, Kence A. 2000. Genetic and morphometirc variation in honeybee (Apis mellifera) populations of Turkey. Apidologie 31: 343-356.
45. Katz BM. 1986. Analyzing dichotomous data from two correlated samples measured at two points in time. Journal of Experimental Education 54: 153-155.
46. Kessler D, Baldwin IT. 2006. Making sense of nectar scents: the effects of nectar secondary metabolites on floral visitors of Nicotiana attenuata. The Plant Journal 49: 840-854.
47. Lunney G. 1970. Using analysis of variance with a dichotomous dependent variable: an empirical study. Journal of Educational Measurement 7: 263-269.
48. Malerbo-Souza DT, Nogueira-Couto RH. 2004. Efficiency of n-Octyl-Acetate, 2-Heptanone and citronella in repelleing bees from Brasil (Ocimum sellowii-Labiatae). Brazilian Archives of Bioliology and Technology 47: 121-125.
49. Masetti A, Maini S. 2006. Arm in cage tests to compare skin repellents against bites of Aedes albopictus. Bulletin of Insectology 59: 157-160.
50. Mattila HR, Smith BH. 2008. Learning and memory in workers reared by nutritinonally stressed honeybee (Apis mellifera L.) colonies. Physiology and Behavior 95: 609-616.
51. Menzel R, Giurfa M. 2001. Cognitive architecture of a mini-brain: the honeybee. Trends in Cognitive Sciences 5: 62-71.
52. Quené H, van den Bergh H. 2008. Examples of mixed-effects modeling with cross random effects and with biomial data. Journal of Memory and Language 59: 413-425.
53. Page RE Jr., Erber J, Fondrk MK. 1998. The effect of genotype on response thresholds to sucrose and foraging behavior of honeybees (Apis mellifera L.). Journal of Comparative Physiology A 182: 489-500.
54. Raguso RA. 2008. Start making scents: the challenge of integrating chemistry into pollination ecology. Entomologia Experimentalis et Applicata 128: 196-207.
55. Schreck CE. 1977. Techniques for the evaluation of insect repellents: a critical review. Annual Review of Entomology 22: 101-119.
56. Schröter U, Menzel R. 2003. A new ascending sensory tract to the calyces of the honeybee mushroom body, the subesophageal-calycal tract. Journal of Comparative Neurology 465:168-178.
57. Seidelmann K, Weiner H, Ferenz HJ. 2003. Wings and legs are productions sites for the desert locust courtship-inhibition pheremone, phenylacetonitrile. Journal of Insect Physiology 49: 1125-1133.
58. Smith BH, Abramson CI, Tobin TR. 1991. Conditioned withholding of proboscis extension in honeybees (Apis mellifera) during discriminative punishment. Journal of Comparative Psychology 105: 345-356.
59. Syed Z, Leal WS. 2008. Mosquitoes smell and avoid the insect repellent DEET. Proceedings of the National Academy of Sciences, USA 105:!13598-13603.
60. Werner SJ, Cummings JL, Tupper SK, Hurley, JC, Stahl RS, Primus TM. 2007. Caffeine formulation for avian repellency. Journal of Wildlife Management 71: 1676-1681.
61. Winer BJ, Brown DR, Michels KM. 1991. Statistical principles in experimental design. McGraw-Hill.
62. Withers GS, Fahrbach SE, Robinson GE. 1993. Selective neuroanatomical plasticity and division of labour in the honeybee. Nature 364: 238-239.
63. Xue RD, Barnard DR, Ali A. 2001. Laboratory and field evaluation of insect repellents as oviposition deterrents against the mosquito Aedes albopictus. Medical and Veterinary Entomology 15: 126-131.
64. Zhang S, Bock F, Si A, Tautz J, Srinivasan MV. 2005. Visual working memory in decision making by honeybees. Proceedings of the National Academy of Sciences, USA 102: 5250-5255.