A role for octopamine in honey bee division of labor

Brain, Behavior and Evolution

Volumn 60, Issue 6, 2002, Pages 350-359

  Schulz, David J ^a   Barron, Andrew B ^a   Robinson, Gene E ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Apis mellifera; Behavioral development; Biogenic amines; Division of labor; Honey bees; Juvenile hormone; Neuromodulation; Octopamine; Response thresholds

Indexed keywords

BIOGENIC AMINE; JUVENILE HORMONE; METHOPRENE; OCTOPAMINE; PHEROMONE;

AGE; ANIMAL BEHAVIOR; ANTENNA; ANTICIPATION; BEHAVIORAL SCIENCE; BRAIN LEVEL; BRAIN REGION; CONFERENCE PAPER; DEVELOPMENT; DISSECTION; FORAGING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HONEYBEE; INSECT SOCIETY; MANUAL LABOR; MUSHROOM BODY; NEUROMODULATION; NEUROPIL; NONHUMAN; ORGANISM COLONY; PRIORITY JOURNAL; SOCIAL BEHAVIOR; TISSUE LEVEL;

ANIMALS; APPETITIVE BEHAVIOR; BEES; BRAIN; JUVENILE HORMONES; NERVE NET; NEURONAL PLASTICITY; NEUROTRANSMITTER AGENTS; OCTOPAMINE; PERIPHERAL NERVOUS SYSTEM; PHEROMONES; RECEPTORS, SENSORY; SOCIAL BEHAVIOR; SOCIAL ENVIRONMENT;

APINAE; APIS MELLIFERA; APOIDEA; BASIDIOMYCOTA; HEXAPODA;

EID: 0036979049     PISSN: 00068977     EISSN: None     Source Type: Journal    
DOI: 10.1159/000067788     Document Type: Conference Paper

References (83)

1. Adamo, S.A., C.E. Linn, and R.R. Hoy (1995) The role of neurohormonal octopamine during 'fight or flight' behaviour in the field cricket Gryllus bimaculatus. J. Exp. Biol., 198: 1691-1700.
2. Barron, A.B., D.J. Schulz, and G.E. Robinson (2002) Octopamine modulates responsiveness to foraging-related stimuli in honey bees (Apis mellifera). J. Comp. Physiol. A., 188: 603-610.
3. Ben-Shahar, Y., A. Robichon, M.B. Sokolowski, and G.E. Robinson (2002) Influence of gene action across different time scales on behavior. Science, 296: 741-744.
4. Bicker, G. (1999) Biogenic amines in the brain of the honeybee: cellular distribution, development and behavioural functions. Micro. Res. Tech., 44: 166-178.
5. Blenau, W., and A. Baumann (2001) Molecular and pharmacological properties of insect biogenic amine receptors: lessons from Drosophila melanogaster and Apis mellifera. Arch. Insect Biochem. Physiol., 48: 13-38.
6. Bloch, G., and G.E. Robinson (2001) Reversal of honeybee behavioural rhythms. Nature, 410: 1048.
7. Bloch, G., D.L. Wheeler, and G.E. Robinson (2002) Endocrine influences on the organization of insect societies. In Hormones, Brain and Behavior (ed. by D. Pfaff). Academic Press, San Diego, California., vol. 3, 195-235.
8. Braun, G., and G. Bicker (1992) Habituation of an appetitive reflex in the honeybee. J. Neurophysiol., 67: 588-598.
9. Burrell, B.D., and B.H. Smith (1995) Modulation of the honey bee (Apis mellifera) sting response by octopamine. J. Insect Physiol., 41: 671-680.
10. Corbet, S.A. (1991) A fresh look at the arousal syndrome of insects. Adv. Invert. Physiol., 23: 81-116.
11. Erber, J., P. Kloppenburg, and A. Scheidler (1993) Neuromodulation by serotonin and octopamine in the honeybee: behaviour, neuroanatomy and electrophysiology. Experientia, 49: 1073-1083.
12. Evans, P.D. (1980) Biogenic amines in the insect nervous system. Adv. Insect Physiol., 15: 317-473.
13. Evans, P.D., and M.V.S. Siegler (1982) Octopamine mediated relaxation of maintained and catch tension in locust skeletal muscle. J. Physiol., 324: 93-112.
14. Fahrbach, S.E., and G.E. Robinson (1996) Juvenile hormone, behavioral maturation and brain structure in the honey bee. Dev. Neurosci., 18: 102-114.
15. Fuchs, E., J.H. Dustmann, H. Stadler, and F.W. Schürmann (1989) Neuroactive compounds in the brain of the honeybee during imaginal life. Comp. Biochem. Physiol. C, 92: 337-342.
16. Galizia, C.G., and R. Menzel (2001) The role of glomeruli in the neural representation of odors: results from optical recording studies. J. Insect Physiol., 47: 115-130.
17. Gillette, R., and J. Jing (2001) The role of escape swim motor network in the organization of behavioral hierarchy and arousal in Pleuro-branchaea. Am. Zool., 41: 983-992.
18. Hammer, M. (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature, 366: 59-63.
19. Hammer, M. (1997) The neural basis of associative reward learning in honeybees. Trends Neurosci, 20: 245-252.
20. Hammer, M., and R. Menzel (1995) Learning and memory in the honeybee. J. Neurosci., 15: 1617-1630.
21. Hammer, M., and R. Menzel (1998) Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn. Mem., 5: 146-156.
22. Harris, J.W., and J. Woodring (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.
23. Harrison, J.M. (1986) Caste-specific changes in honeybee flight capacity. Physiol. Zool., 59: 175-187.
24. Huang, Z.Y., and G.E. Robinson (1996) Regulation of honey bee division of labor by colony age demography. Behav. Ecol. Sociobiol., 39: 147-158.
25. Jing, J., and R. Gillette (2000) Escape swim network interneurons have diverse roles in behavioral switching and putative arousal in Pleuro-branchaea. J. Neurophysiol., 83: 1346-1355.
26. Joerges, J., A. Küttner, C.G. Galizia, and R. Menzel (1997) Representations of odours and odour mixtures visualized in the honeybee brain. Nature, 387: 285-288.
27. Kaatz, H., S. Eichmüller, and S. Kreissl (1994) Stimulatory effect of octopamine on juvenile hormone biosynthesis in honey bees (Apis mellifera): physiological and immunocytochemical evidence. J. Insect Physiol., 40: 865-872.
28. Katz, P.S., P.A. Getting, and W.N. Frost (1994) Dynamic neuromodulation of synaptic strength intrinsic to a central pattern generator circuit. Nature, 367: 729-731.
29. King, L.E., J.E. Steele, and S.W. Bajura (1986) The effect of flight on the composition of haemolymph in the cockroach, Periplaneta americana. J. Insect Physiol., 32: 649-655.
30. Kloppenburg, P., D. Ferns, and A.R. Mercer (1999) Serotonin enhances central olfactory neuron responses to female sex pheromones in the male sphinx moth Manduca sexta. J. Neurosci., 19: 8172-8181.
31. Kreissl, S., S. Eichmüller, G. Bicker, J. Rapus, and M. Eckert (1994) Octopamine-like immunore-activity in the brain and subesophageal ganglion of the honeybee. J. Comp. Neurol., 348: 583-595.
32. Kucharski, R., and R. Maleszka (2002) Molecular profiling of behavioural development: differential expression of mRNAs for inositol 1,4,5-trisphosphate 3-kinase isoforms in naive and experienced honeybees(Apis mellifera). Mol. Brain Res., 99: 92-101.
33. Kupfermann, I., and K.R. Weiss (1981) The role of serotonin in arousal of feeding behavior of Aplysia. In Serotonin Neurotransmission and Behavior, M.I.T. Press, Cambridge, MA, pp. 255-287.
34. Le Conte, Y., G. Arnold, J. Trouiller, and C. Masson (1990) Identification of a brood pheromone in honeybees. Naturwissenschaften, 77: 334-336.
35. Le Conte, Y., A. Mohammedi, and G.E. Robinson (2001) Primer effects of a brood pheromone on honeybee behavioural development. Proc. Roy. Soc. Lond. B., 268: 163-168.
36. Le Conte, Y., L. Sreng, and S.H. Poitout (1995) Brood pheromone can modulate the feeding behavior of Apis mellifera workers (Hymenoptera: Apidae). J. Econ. Entomol., 88: 798-804.
37. Lindauer, M. (1954) Temperaturregulierung und Wasserhaushalt im Bienenstaat. Z. Vgl. Physiol.36: 391-432.
38. Linn, C.E., and W.L. Roelofs (1986) Modulatory effects of octopamine and serotonin on male sensitivity and periodicity of response to sex pheromones in the cabbage looper moth, Trichoplusia ni. Arch. Insect Biochem. Physiol., 3: 161-171.
39. Linn, C.E., M.G. Campbell, and W.L. Roelofs (1992) Photoperiod cues and the modulatory action of octopamine and 5-hydroxytryptamine on locomotor and pheromone response in male gypsy moths, Lymantria dispar. Arch. Insect Biochem. Physiol., 20: 265-284.
40. Linn, C.E., K.R. Poole, and W.L. Roelofs (1994) Studies on biogenic amines and their metabolites in nervous tissue and hemolymph of male cabbage looper moths - III. fate of injected octopamine, 5-hydroxytryptamine and dopamine. Comp. Biochem. Physiol. C, 108: 99-106.
41. Malamud, J.G., A.P. Mizisin, and R.K. Josephson (1988) The effects of octopamine on contraction kinetics and power output of a locust flight muscle. J. Comp. Physiol. A, 162: 827-835.
42. Menzel, R., and U. Müller (1996) Learning and memory in honeybees: from behavior to neural substrates. Ann. Rev. Neurosci., 19: 379-404.
43. Mercer, A.R., and J. Erber (1983) The effects of amines on evoked action potentials recorded in the mushroom bodies of the bee brain. J. Comp. Physiol. A, 151: 469-476.
44. Mercer, A.R., and R. Menzel (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.
45. Moore, D., J.E. Angel, I.M. Cheeseman, S.E. Fahrbach, and G.E. Robinson (1998) Timekeeping in the honey bee colony: integration of circadian rhythms and division of labor. Behav. Ecol. Sociobiol., 43: 147-160.
46. Nijhout, H.F. (1994) Insect Hormones. Princeton University Press, Princeton, NJ.
47. Ohashi, K., S. Natori, and T. Kubo (1997) Change in the mode of gene expression of the hypopharyngeal gland cells with an age-dependent role change of the worker honeybee Apis mellifera. Eur. J. Biochem., 249: 797-802.
48. Oster, G.F., and E.O. Wilson (1978) Caste and Ecology in Social Insects. Princeton University Press, Princeton, NJ.
49. Page, R.E., G.E. Robinson, D.S. Britton, and M.K. Fondrk (1992) Genotypic variability for rates of behavioral development in worker honeybees (Apis mellifera L.). Behav. Ecol., 3: 173-180.
50. Pankiw, T., R.E. Page, and M.K. Fondrk (1998) Brood pheromone stimulates pollen foraging in honey bees (Apis mellifera). Behav. Ecol. Sociobiol., 44: 193-198.
51. Pfaff, D., J. Frohlich, and M. Morgan (2002) Hormonal and genetic influences on arousal - sexual and otherwise. Trends Neurosci., 25: 45-50.
52. Pophof, B. (2000) Octopamine modulates the sensitivity of silkmoth pheromone receptor neurons. J. Comp. Physiol. A, 186: 307-313.
53. Pribbenow, B., and J. Erber (1996) Modulation of antennal scanning in the honeybee by sucrose stimuli, serotonin and octopamine: behavior and electrophysiology. Neurobiol. Learn. Mem., 66: 109-120.
54. Ratnieks, F.L.W. (1993) Egg-laying, egg-removal, and ovary development by workers in queen-right honey bee colonies. Behav. Ecol. Sociobiol., 32: 191-198.
55. Ribbands, R. (1953) The Behaviour and Social Life of Honeybees. Bee Research Association Ltd., London.
56. Robinson, G.E. (1987a) Regulation of honey bee age polyethism by juvenile hormone. Behav. Ecol. Sociobiol., 20: 329-338.
57. Robinson, G.E. (1987b) Modulation of alarm pheromone perception in the honey bee: evidence for division of labor based on hormonally regulated response thresholds. J. Comp. Physiol. A, 160: 613-619.
58. Robinson, G.E. (1992) Regulation of division of labor in insect societies. Ann. Rev. Entomol., 37: 637-665.
59. Robinson, G.E., and E.L. Vargo (1997) Juvenile hormone in adult eusocial Hymenoptera: gonadotropin and behavioural pacemaker. Arch. Insect Biochem. Physiol., 35: 559-583.
60. Robinson, G.E., L.M. Heuser, Y. Le Conte, F. Lenquette, and R.M. Hollingworth (1999) Neuro-chemicals aid bee nestmate recognition. Nature, 399: 534-535.
61. Robinson, G.E., R.E. Page, C. Strambi, and A. Strambi (1989) Hormonal and genetic control of behavioural integration in honey bee colonies. Science, 246: 109-112.
62. Robinson, G.E., R.E. Page, C. Strambi, and A. Strambi (1992) Colony integration in honey bees: mechanisms of behavioural reversion. Ethology, 90: 336-350.
63. Roeder, T. (1994) Biogenic amines and their receptors in insects. Comp. Biochem. Physiol. C, 107: 1-12.
64. Rösch, G.A. (1930) Untersuchungen über die Arbeitsteilung im Bienenstaat, II. Die Tätigkeiten der Arbeitsbienen unter experimentell veränderten Bedingungen. Z. Vgl. Physiol., 12: 1-71.
65. Satterlie, R.A., and T.P. Norekian (1996) Modulation of swimming speed in the pteropod mollusc Clione limacina: role of a compartmental serotonergic system. Invert. Neurosci., 2: 157-165.
66. Schulz, D.J., and G.E. Robinson (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.
67. Schulz, D.J., and G.E. Robinson (2001) Octopamine influences division of labor in honey bee colonies. J. Comp. Physiol. A, 187: 53-61.
68. Schulz, D.J., M.M. Elekonich, and G.E. Robinson (2002a) Biogenic amines in the antennal lobes and the initiation and maintenance of foraging behavior in honey bees. J. Neurobiol., in press.
69. Schulz, D.J., J.P. Sullivan, and G.E. Robinson (2002b) Juvenile hormone and octopamine in the regulation of division of labor in honey bee colonies. Horm. Behav., 42: 222-231.
70. Seeley, T.D., and S.A. Kolmes (1991) Age polyethism for hive duties in honey bees - illusion or reality. Ethology, 87: 287-297.
71. Seigel, G.J., B.W. Agranoff, R.W. Albers, S.K. Fisher, and M.D. Uhler (1999) Basic Neurochemis-try: Molecular, Cellular and Medical Aspects. Lippincott-Raven, Philadelphia, PA.
72. Shapira, M., C.K. Thompson, H. Soreq, and G.E. Robinson (2001) Changes in neuronal acetylcholinesterase gene expression and division of labor in honey bee colonies. J. Mol. Neurosci., 17: 1-12.
73. Sigg, D., C.M. Thompson, and A.R. Mercer (1997) Activity-dependent changes to the brain and behavior of the honey bee, Apis mellifera. J. Neurosci., 17: 7148-7156.
74. Sombati, S., and G. Hoyle (1984) Central nervous sensitization and dishabituation of reflex action in an insect by the neuromodulator octopamine. J. Neurobiol., 15: 481-506.
75. Sullivan, J.P., O. Jassim, S.E. Fahrbach, and G.E. Robinson (2000) Juvenile hormone paces behavioral development in the adult worker honey bee. Horm. Behav., 37: 1-14.
76. Taylor, D.J., G.E. Robinson, B.J. Logan, R. Laverty, and A.R. Mercer (1992) Changes in brain amine levels associated with the morphological and behavioural development of the worker honeybee. J. Comp. Physiol. A, 170: 715-721.
77. Toma, D.P., Bloch, G., Moore, D., and G.E. Robin-son (2000) Changes in period expression in the brain and division of labor in honey bee colonies. Proc. Natl. Acad. Sci. USA, 97: 6914-6919.
78. Tinbergen, N. (1951) The Study of Instinct. Oxford University Press, New York.
79. Visscher, P.K. (1996) Reproductive conflict in honey bees: a stalemate of worker egg-laying and policing. Behav. Ecol. Sociobiol., 39: 237-244.
80. Wagener-Hulme, C., J.C. Kuehn, D.J. Schulz, and G.E. Robinson (1999) Biogenic amines and division of labor in honey bee colonies. J. Comp. Physiol. A, 184: 471-479.
81. Winnington, A.P., R.M. Napper, and A.R. Mercer (1996) Structural plasticity of identified glomeruli in the antennal lobes of the adult worker honey bee. J. Comp. Neurol., 365: 479-490.
82. Winston, M.L. (1987) The Biology of the Honey Bee. Harvard University Press, Cambridge, MA.
83. Withers, G.S., S.E. Fahrbach, and G.E. Robinson (1993) Selective neuroanatomical plasticity and division of labor in the honeybee. Nature, 364: 238-240.