Hygienic behavior in the honey bee (Apis mellifera L.) and the modulatory role of octopamine

Journal of Neurobiology

Volumn 55, Issue 3, 2003, Pages 341-354

  Spivak, Marla ^a   Masterman, Rebecca ^a   Ross, Rocco ^a   Mesce, Karen A ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Antennal lobe; Biogenic amines; Electroantennogram; Epinastine; Olfaction

Indexed keywords

EPINASTINE; OCTOPAMINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTENNA; ARTICLE; BREEDING; GENOTYPE; HONEYBEE; HYGIENE; IMMUNOCYTOCHEMISTRY; INSECT; NERVE CELL; NONHUMAN; ODOR; OLFACTORY NERVOUS SYSTEM; PHENOTYPE; PRIORITY JOURNAL; SMELLING;

ADRENERGIC ALPHA-AGONISTS; ANIMALS; BEES; BEHAVIOR, ANIMAL; BRAIN; DIBENZAZEPINES; ELECTROPHYSIOLOGY; HISTAMINE H1 ANTAGONISTS; HYGIENE; IMAGE PROCESSING, COMPUTER-ASSISTED; IMIDAZOLES; IMMUNOHISTOCHEMISTRY; MICROSCOPY, CONFOCAL; NEURONS; OCTOPAMINE; SMELL;

EID: 0038028658     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.10219     Document Type: Article

References (58)

1. Arathi HS, Burns I, Spivak M. 2000. Ethology of hygienic behaviour in the honey bee Apis mellifera L. (Hymenoptera: Apidae): behavioral repertoire of hygienic bees. Ethology 106:365-379.
2. Arathi HS, Spivak M. 2001. Influence of colony genotypic composition on the performance of hygienic behavior in the honeybee, Apis mellifera L. Anim Behav 62:57-66.
3. Bhagavan S, Smith BH. 1997. Olfactory conditioning in the honey bee, Apis mellifera: effects of CS intensity. Physiol Behav 61:107-117.
4. Beshers SN, Fewell JH. 2001. Models of division of labor in social insects. Annu Rev Entomol 46:413-440.
5. Bicker G. 1999. Biogenic amines in the brain of the honeybee: cellular distribution, development, and behavioral functions. Microsc Res Tech 44:166-178.
6. Boecking O, Drescher W. 1992. The removal response of Apis mellifera L. colonies to brood in wax and plastic cells after artificial and natural infestation with Varroa jacobsoni Oud. and to freeze-killed brood. Exp Appl Acarol 16:321-329.
7. Bonabeau E, Theraulaz G. 1999. Role and variability of response thresholds in the regulation of division of labor in insect societies. In: Detrain C, Deneubourg JL, Pasteels JM, editors. Information processing in social insects. Basel, Switzerland: Birkhäuser, p 141-163.
8. Crisp KM, Klukas KA, Gilchrist LS, Nartey AJ, Mesce KA. 2002. Distribution and development of dopamine- and octopamine-synthesizing neurons in the medicinal leech. J Comp Neurol 442:115-129.
9. Degen J, Gewecke M, Roeder T. 2000. Octopamine receptors in the honey bee and locust nervous system: pharmacological similarities between homologous receptors of distantly related species. Br J Pharmacol 130:587-594.
10. Dolzer J, Krannich S, Fischer K, Stengl M. 2001. Oscillations of the transepithelial potential of moth olfactory sensilla are influenced by octopamine and serotonin. J Exp Biol 204:2781-2794.
11. Eckert M, Rapus J, Nurnberger A, Penzlin H. 1992. A new specific antibody reveals octopamine-like immunoreactivity in cockroach ventral nerve cord. J Comp Neurol 322:1-15.
12. Edwards DH, Yeh S-R, Musolf BE, Antonsen BL, Krasne FB. 2002. Metamodulation of the crayfish escape circuit. Brain Behav Evol, 60:360-369.
13. Gilchrist LS, Klukas KA, Jellies J, Rapus J, Eckert, M, Mesce KA. 1995. Distribution and developmental expression of octopamine-immunoreactive neurons in the central nervous system of the leech. J Comp Neurol 353:451-463.
14. Grosmaitre X, Marion-Poll F, Renou M. 2001. Biogenic amine modulate olfactory receptor neurons firing activity in Mamestra brassicae. Chem Senses 26:653-661.
15. Hammer M. 1993. An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366:59-63.
16. Hammer M, Menzel R. 1995. Learning and memory in the honeybee (review). J Neurosci 15:1617-1630.
17. Harris JW, Woodring J. 1992. Effects of stress, age, season, and source colony on levels of octopamine, dopamine and serotonin in the honey bee (Apis mellifera L) brain. J Insect Physiol 38:29-35.
18. Hildebrandt H, Muller U. 1995. Octopamine mediates rapid stimulation of protein kinase A in the antennal lobe of honeybees. J Neurobiol 27:44-50.
19. Kreissl S, Eichmüller S, Bicker G, Rapus J, Eckert M. 1994. Octopamine-like immunoreactivity in the brain and subesophageal ganglion of the honey bee. J Comp Neurol 348:583-595.
20. Lapidge KL, Oldroyd BP, Spivak M. 2002. Seven suggestive quantitative trait loci influence hygienic behavior of honeybees. Naturwissenschaften 89:565-568.
21. Lehman HK, Klukas KA, Gilchrist LS, Mesce KA. 2000. Steroid regulation of octopamine expression during metamorphic development of the moth Manduca sexta. J Comp Neurol 424:283-296.
22. Lim CC, Wasserman GS. 2001. Categorical and prolonged potentials are evoked when brief, intermediate-intensity flashes stimulate horseshoe crab lateral eye photoreceptors during octopamine neuromodulation. Biol Signals Recept 10:399-415.
23. Masterman RM. 2000. Neuroethology of honey bee (Apis mellifera) hygienic behavior. PhD thesis. University of Minnesota, St. Paul, MN.
24. Masterman R, Ross R, Mesce K, Spivak M. 2001. Olfactory and behavioral response thresholds to odors of diseased brood differ between hygienic and non-hygienic honey bees (Apis mellifera L.) J Comp Physiol A 187:441-452.
25. Masterman R, Smith BH, Spivak M. 2000. Brood odor discrimination abilities in hygienic and non-hygienic honey bees (Apis mellifera L.) using proboscis extension reflex conditioning. J Insect Behav 13:89-101.
26. McCulloch CE, Searle SR. 2001. Generalized, linear, and mixed models. New York: Wiley.
27. Menzel R. 2001. Searching for the memory trace in a mini-brain. Learn Mem 8:53-62.
28. Mercer AR, Menzel R. 1982. The effects of biogenic amines on conditioned and unconditioned responses to olfactory stimuli in the honeybee Apis mellifera. J Comp Physiol A 145:363-368.
29. Mesce KA, Klukas KA, Brelje TC. 1993. Improvements for the anatomical characterization of insect neurons in whole mount: the use of cyanine-derived fluorophores and laser scanning confocal microscopy. Cell Tissue Res 271:381-397.
30. Momot JP, Rothenbuhler WC. 1971. Behaviour genetics of nest cleaning in honeybees. VI. Interactions of age and genotype of bees, and nectar flow. J Apic Res 10:11-21.
31. Oldroyd BP. 1996. Evaluation of Australian commercial honey bees for hygienic behaviour, a critical character for tolerance to chalkbrood. Aust J Exp Agric 36:625-629.
32. Patte F, Etcheto M, Marfaing P, Laffort P. 1989. Electroantennogram stimulus-response curves for 59 odorants in the honey bee, Apis mellifera. J Insect Physiol A 35:667-675.
33. Pophof B. 2000. Octopamine modulates the sensitivity of silkmoth pheromone receptor neurons. J Comp Physiol A 186:307-313.
34. Pophof B. 2002. Octopamine enhances moth olfactory responses to pheromones, but not those to general odorants. J Comp Physiol A 188:659-662.
35. Ramirez J-M, Orchard I. 1990. Octopaminergic modulation of the forewing stretch receptor in the locust Locusta migratoria. J Exp Biol 149:255-279.
36. Roeder T. 1999. Octopamine in invertebrates. Prog Neurobiol 59:533-561.
37. Roeder T, Degen J, Gewecke M. 1998. Epinastine, a highly specific antagonist of insect neuronal octopamine receptors. Eur J Pharmacol 349:171-177.
38. Rothenbuhler WC. 1964. Behaviour genetics of nest cleaning in honey bees. IV. Responses of F1 and backcross generations to disease-killed brood. Am Zool 4:111-123.
39. R Statistical Software. 2002. The R development core team, version 1.5.1 (2002-07-17) www.r-project.org.
40. SAS Institute Inc. 989. SAS/STAT user's guide, version 6, 4th ed., vols. 1 and 2. Cary, NC: SAS Institute Inc.
41. Schneider H, Trimmer BA, Rapus J, Eckert M, Valentine DE, Kravitz EA. 1993. Mapping of octopmaine-immunoreactive neurons in the central nervous sytem of the lobster. J Comp Neurol 329:129-142.
42. Schulz DJ, Robinson GE. 1999. Biogenic amines and division of labor in honey bee colonies: behaviorally related changes in the antennal lobes and age-related changes in the mushroom bodies. J Comp Physiol A 184:481-488.
43. Schulz DJ, Robinson GE. 2001. Octopamine influences division of labor in honey bee colonies. J Comp Physiol A 187:53-61.
44. Spivak M. 1996. Honey bee hygienic behavior and defense against Varroa jacobsoni. Apidologie 27:245-260.
45. Spivak M, Downey D. 1998. Field assays for hygienic behavior in honey bees (Apidae: Hymenoptera). J Econ Entomol 91:64-70.
46. Spivak M, Gilliam M. 1993. Facultative expression of hygienic behaviour of honey bees in relation to disease resistance. J Apic Res 32:147-157.
47. Spivak M, Gilliam M. 1998. Hygienic behaviour of honey bees and its application for control of brood diseases and varroa Part II. Studies on hygienic behaviour since the Rothenbuhler era. Bee World 79:169-186.
48. Spivak M, Reuter GS. 1998. Performance of hygienic honey bee colonies in a commercial apiary. Apidologie 29:291-302.
49. Spivak M, Reuter GS. 2001a. Resistance to American foulbrood disease by honey bee colonies, Apis mellifera, bred for hygienic behavior. Apidologie 32:555-565.
50. Spivak M, Reuter GS. 2001b. Varroa jacobsoni infestation in untreated honey bee (Hymenoptera: Apidae) colonies selected for hygienic behavior. J Econ Entomol 94:326-331.
51. Stevenson PA, Pflüger H-J, Eckert M, Rapus J. 1992. Octopamine immunoreactive cell populations in the locust thoracic-abdominal nervous system. J Comp Neurol 315:382-397.
52. Thompson VC. 1964. Behaviour genetics of nest cleaning in honey bees. III. Effect of age of bees of a resistant line on their response to disease-killed brood. J Apic Res 3:25-30.
53. von Nickisch-Rosenegk EV, Krieger J, Kubick S, Laage R, Strobel J, Strotmann J, Breer H. 1996. Cloning of biogenic amine receptors from moths (Bombyx mori and Heliothis virescens). Insect Biochem Mol Biol 26:817-827.
54. Wagener-Hulme C, Kuehn JC, Schulz DJ, Robinson GE. 1999. Biogenic amines and division of labor in honey bee colonies. J Comp Physiol A 184:471-479.
55. Wolfinger R, O'Connell M. 1993. Generalized linear mixed models: a pseudo-likelihood approach. J Stat Comp Simul 48:233-243.
56. Woodrow AW, Holst EC. 1942. The mechanism of colony resistance to American foulbrood. J Econ Entomol 35:327-330.
57. Yeh S-R, Fricke RA, Edwards DH. 1996. The effect of social experience on serotonergic modulation of the escape circuit of crayfish. Science 271:366-369.
58. Zhang BG, Torkkeli PH, French AS. 1992. Octopamine selectively modifies the slow component of sensory adaptation in an insect mechanoreceptor. Brain Res 591:351-355.