Brain GABA and glutamate levels in workers of two ant species (Hymenoptera: Formicidae): Interspecific differences and effects of queen presence/absence

Insect Science

Volumn 21, Issue 5, 2014, Pages 647-658

  Wnuk, Andrzej ^a,b,c   Kostowski, Wojciech ^b   Korczyńska, Julita ^a   Szczuka, Anna ^a   Symonowicz, Beata ^a   Bieńkowski, Przemysław ^b   Mierzejewski, Paweł ^b   Godzińska, Ewa Joanna ^a  

^a NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^b INSTITUTE OF PSYCHIATRY AND NEUROLOGY   (Poland)

^c WARSAW UNIVERSITY OF LIFE SCIENCES   (Poland)

Author keywords

Formica polyctena; GABA; Glutamate; Interspecific differences; Myrmica ruginodis; Queen

Indexed keywords

FORMICA POLYCTENA; FORMICIDAE; HYMENOPTERA; MYRMICA RUGINODIS;

4 AMINOBUTYRIC ACID; GLUTAMIC ACID;

AGGRESSION; ANIMAL; ANT; BRAIN; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; SOCIAL BEHAVIOR; SPECIES DIFFERENCE;

AGGRESSION; ANIMALS; ANTS; BRAIN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; SIGNAL TRANSDUCTION; SOCIAL BEHAVIOR; SPECIES SPECIFICITY;

EID: 84907876851     PISSN: 16729609     EISSN: 17447917     Source Type: Journal    
DOI: 10.1111/1744-7917.12076     Document Type: Article

References (83)

1. Alaux, C., Sinha, S., Hasadsri, L., Hunt, G.J., Guzmán-Novoa, E., DeGrandi-Hoffman, G., Uribe-Rubio, J.L., Southey, B.R., Rodriguez-Zas, S. and Robinson, G.E. (2009) Honeybee aggression supports a link between gene regulation and behavioral evolution. Proceedings of the National Academy of Sciences of the United States of America, 106, 15400-15405.
2. Amdam, G.V. (2011) Social context, stress, and plasticity of aging. Aging Cell, 10, 18-27.
3. Beggs, K.T., Glendining, K.A., Marechal, N.M., Vergoz, V., Nakamura, I., Slessor, K.N. and Mercer, A.L. (2007) Queen pheromone modulates brain dopamine function in worker honey bees. Proceedings of the National Academy of Sciences of the United States of America, 104, 2460-2464.
4. Benois, A. (1972) Étude expérimentale de la fusion entre groupes chez la fourmi Camponotus vagus Scop., mettant en evidence la fermeture de la société. Comptes Rendus de l'Académie des Sciences, Paris, 274, 3564-3567.
5. Bernadou, A., Demares, F., Couret-Fauvel, T., Sandoz, J.C. and Gauthier, M. (2009) Effect of fipronil on side-specific antennal tactile learning in the honeybee. Journal of Insect Physiology, 55, 1099-1106.
6. Bicker, G. (1999) Histochemistry of classical neurotransmitters in antennal lobes and mushroom bodies of the honeybee. Microscopy Research and Technique, 45, 174-183.
7. Bicker, G., Schäfer, S., Ottersen, O.P. and Storm-Mathisen, J. (1988) Glutamate-like immunoreactivity in identified neuronal populations of insect nervous systems. The Journal of Neuroscience, 8, 2108-2122.
8. Boulay, R., Katzav-Gozansky, T., Vander Meer, R.K. and Hefetz, A. (2003) Colony insularity through queen control on worker social motivation in ants. Proceedings of the Royal Society of London Series B-Biological Sciences, 270, 971-977.
9. Canonaco, M., Bergamo, P., Tavolaro, R. and Miralto, A. (1991) Role of the GABA chloride ion channel component on aggressive behavior in the male crab. Physiology & Behavior, 49, 411-415.
10. Clarke, B.S. and Donnellan, J.F. (1982) Concentrations of some putative neurotransmitters in the CNS of quick-frozen insects. Insect Biochemistry, 12, 623-638.
11. Clarke, G., O'Mahony, S., Malone, G. and Dinan, T.G. (2007) An isocratic high performance liquid chromatography method for the determination of GABA and glutamate in discrete regions of the rodent brain. Journal of Neuroscience Methods, 160, 223-230.
12. Czechowski, W. (1985) Competition between Myrmica laevinodis Nyl. and Lasius niger (L.) (Hymenoptera, Formicoidea). Annales Zoologici, 39, 153-173.
13. Czechowski, W. (1996) Colonies of hybrids and mixed colonies; interspecific nest takeover in wood ants (Hymenoptera, Formicidae). Memorabilia Zoologica, 50, 1-116.
14. Czechowski, W. (2004) Submissive posture of Myrmica rugulosa Nyl. in its interspecific relations (Hymenoptera, Formicidae). Przegląd Zoologiczny, 48, 19-28 (in Polish with English summary).
15. Czechowski, W., Markó, B., Radchenko, A. and Ślipiński, P. (2013) Long-term partitioning of space between two territorial species of ants (Hymenoptera: Formicidae) and their effect on subordinate species. European Journal of Entomology, 110, 327-337.
16. Dang, Y.Y., Li, Y.N. and Bao, X.X. (2002) Distribution of GABA2-like immunoreactivity in the optic lobe neuropils of Camponotus japonicus. Journal of Northeast Normal University (Natural Science Edition), 34, 72-77 (in Chinese with English abstract).
17. De Almeida, R.M.M., Ferrari, P.F., Parmigiani, S. and Miczek, K.A. (2005) Escalated aggressive behavior: dopamine, serotonin and GABA. European Journal of Pharmacology, 526, 51-64.
18. Devi, L.A. and Fricker, L.D. (2013) Transmitters and peptides: basic principles. Neuroscience of the 21 Century: from Basic to Clinic (ed. D.W. Pfaff ), pp. 1487-1503. Springer Science + Business Media, New York, Heidelberg, Dordrecht, London.
19. El Hassani, A.K., Dacher, M., Gauthier, M. and Armengaud, C. (2005) Effects of sublethal doses of fipronil on the behavior of the honeybee. Pharmacology Biochemistry and Behavior, 82, 30-39.
20. Felisberti, F. and Ventura, D.F. (1996) Central extraocular photoreceptors in ants. Tissue & Cell, 28, 25-36.
21. de Freitas Silva, D.M., Ferraz, V.P. and Ribeiro, A.M. (2009) Improved high-performance liquid chromatographic method for GABA and glutamate determination in regions of the rodent brain. Journal of Neuroscience Methods, 177, 289-293.
22. Fuchs, E., Dustmann, J.H., Stadler, H. and Schürmann, F.W. (1989) Neuroactive compounds in the brain of the honeybee during imaginal life. Comparative Biochemistry & Physiology C, Comparative Pharmacology & Toxicology, 92, 337-342.
23. Galizia, C.G. and Szyszka, P. (2008) Olfactory coding in the insect brain: molecular receptive ranges, spatial and temporal coding. Entomologia Experimentalis et Applicata, 128, 81-92.
24. Ganeshina, O. and Menzel, R. (2001) Immunoreactive neurons in the mushroom bodies of the honeybee: an electron microscopic study. Journal of Comparative Neurology, 437, 335-349.
25. Gauthier, M. and Grünewald, B. (2012) Neurotransmitter systems in the honey bee brain. Honeybee Neurobiology and Behavior: A Tribute to Randolf Menzel (eds. C.G. Galizia, D. Eisenhardt & M. Giurfa ), pp. 155-169. Springer Science + Business Media, Heidelberg.
26. Giraldo, Y.M., Patel, E., Gronenberg, W. and Traniello, J.F.A. (2013) Division of labor and structural plasticity in an extrinsic serotonergic mushroom body neuron in the ant Pheidole dentata. Neuroscience Letters, 534, 107-111.
27. Gisselmann, G., Plonka, J., Pusch, H. and Hatt, A. (2004) Drosophila melanogaster GRD and LCCH3 subunits form heteromultimeric GABA-gated cation channels. British Journal of Pharmacology, 142, 409-413.
28. Grünewald, B. (2012) Cellular physiology of the honey bee brain. Honeybee Neurobiology and Behavior: A Tribute to Randolf Menzel (eds. C.G. Galizia, D. Eisenhardt & M. Giurfa ), pp. 185-198. Springer Science + Business Media, Heidelberg.
29. Harris, J.W. and 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. Journal of Insect Physiology, 38, 29-35.
30. Harris, J.W. and Woodring, J. (1995) Elevated brain dopamine levels associated with ovary development in queenless worker honey bees (Apis mellifera L.). Comparative Biochemistry & Physiology C, Pharmacology, Toxicology & Endocrinology, 111, 271-279.
31. Hölldobler, B. and Wilson, E.O. (1990) The Ants. Springer Verlag, Berlin. 732 pp.
32. Hölldobler, B. and Wilson, E.O. (2009) The Superorganism. The Beauty, Elegance and Strangeness of Insect Societies. W.W. Norton, New York-London. 522 pp.
33. Hunt, G.J. (2007) Fight and flight: a comparative view of the neurophysiology and genetics of honey bee defensive behavior. Journal of Insect Physiology, 53, 399-410.
34. Hunt, G.J., Amdam, G.V., Schlipalius, D., Emore, C., Sardesai, N., Williams, C.E., Rueppell, O., Guzmán-Novoa, E., Arechavaleta-Velasco, M., Chandra, S., Fondrk, K.M., Beye, M. and Page, R.E.J. Jr. (2007) Behavioral genomics of honeybee foraging and nest defense. Naturwissenschaften, 94, 247-267.
35. Kiya, T. and Kubo, T. (2010) Analysis of GABAergic and non-GABAergic neuron activity in the optic lobes of the forager and re-orienting worker honeybee (Apis mellifera L.). PLoS ONE, 5: e8833.
36. Kostowski, W., Tarchalska-Kryńska, B. and Markowska, L. (1975) Aggressive behavior and brain serotonin and catecholamines in ants (Formica rufa). Pharmacology Biochemistry & Behavior, 3, 717-719.
37. Kršiak, M. (1979) Effects of drugs on behaviour of aggressive mice. British Journal of Pharmacology, 65, 525-533.
38. Leboulle, G. (2012) Glutamate neurotransmission in the honey bee central nervous system. Honeybee Neurobiology and Behavior: A Tribute to Randolf Menzel (eds. C.G. Galizia, D. Eisenhardt & M. Giurfa ). pp. 171-184. Springer Science + Business Media, Heidelberg.
39. Lee, C.C. and Sherman, M.S. (2009) Glutamatergic inhibition in sensory neocortex. Cerebral Cortex, 19, 2281-2289.
40. Liang, Z.S., Nguyen, T., Mattila, H.R., Rodriguez-Zas, S.L., Seeley, T.D. and Robinson, G.E. (2012) Molecular determinants of scouting behavior in honey bees. Science, 335, 1225-1228.
41. Marques de Sá, J.P. (2007) Applied Statistics. Using SPS, Statistics, Matlab and R, 2nd edn. Springer Verlag, Berlin Heidelberg, 506 pp.
42. Meyer, W., Schlesinger, C., Poehling, H.M. and Ruge, W. (1984) Comparative quantitative aspects of putative neurotransmitters in the central nervous system of spiders (Arachnida: Araneida). Comparative Biochemistry & Physiology Part C: Comparative Pharmacology, 78, 357-362.
43. Miczek, K.A. and Fish, E.W. (2005) Monoamines, GABA, glutamate, and aggression. Biology of Aggression (ed. R.J. Nelson ), pp. 114-150. Oxford University Press, New York.
44. Montero, V.M., Wright, L.S. and Siegel, F. (2001) Increased glutamate, GABA and glutamine in lateral geniculate nucleus but not in medial geniculate nucleus caused by visual attention to novelty. Brain Research, 916, 152-158.
45. Motulsky, H.J. (1999) Analyzing Data with GraphPad Prism. GraphPad Software Inc., San Diego CA, www.graphpad.com, p. 379.
46. Osborne, N.N. and Neuhoff, V. (1974) Amino acid and serotonin content in the nervous system, muscle and blood of the cockroach Periplaneta americana. Brain Research, 80, 251-264.
47. Owens, D., Boyce, L.H., Davis, M.B. and Kriegstein, A. (1996) Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramidicin perforated patch recording and calcium imaging. The Journal of Neuroscience, 16, 6414-6423.
48. Pisarski, B. and Czechowski, W. (1994) Ways to reproductive success of wood ant queens. Memorabilia Zoologica, 48, 181-186.
49. Pisarski, B. and Vepsäläinen, K. (1989) Competitive hierarchy in ant communities (Hymenoptera, Formicidae). Annales Zoologici, 42, 321-329.
50. Poshivalov, V.P. (1981) Pharmaco-ethological analysis of social behaviour of isolated mice. Pharmacology Biochemistry & Behavior, 14(Suppl 1), 53-59.
51. Punzo, F. and Glancey, B.M. (1985) Arginine concentration and free amino acids in the brain of various worker subcastes of the red imported fire ant, Solenopsis invicta (Hymenoptera: Formicidae). Comparative Biochemistry & Physiology Part B: Biochemistry & Molecular Biology, 81, 761-765.
52. Punzo, F. and Williams, D.F. (1994) Free amino acids and biogenic amines in the brain of the carpenter ant, Camponotus floridanus Buckley (Hymenoptera, Formicidae). Comparative Biochemistry & Physiology Part C: Toxicology & Pharmacology, 107, 387-392.
53. Ray, J.W. (1964) The free amino acid pool of the cockroach (Periplaneta americana) central nervous system and the effect of insecticides. Journal of Insect Physiology, 10, 587-597.
54. Robinson, G.E. (2002) Genomics and integrative analyses of division of labor in honeybee colonies. The American Naturalist (Supplement), 160, 160-171.
55. Robinson, G.E., Fahrbach, S.E. and Winston, M.L. (1997) Insect societies and the molecular biology of social behavior. BioEssays, 19, 1099-1108.
56. Rowley, H.L., Martin, K.F. and Marsden, C.A. (1995) Determination of in vivo amino acids neurotransmitters by high-performance liquid chromatography with o-phthalaldehyde-sulphite derivatisation. Journal of Neuroscience Methods, 57, 93-99.
57. Sasaki, K. and Nagao, T. (2001) Distribution and levels of dopamine and its metabolites in brains of reproductive workers in honeybees. Journal of Insect Physiology, 47, 1205-1216.
58. Sasaki, K. and Nagao, T. (2002) Brain tyramine and reproductive states of workers in honeybees. Journal of Insect Physiology, 48, 1075-1085.
59. Savolainen, R. and Vepsäläinen, K. (1988) A competition hierarchy among boreal ants: impact on resource partitioning and community structure. Oikos, 51, 135-155.
60. Savolainen, R. and Vepsäläinen, K. (1989) Niche differentiation of ant species within territories of the wood ant Formica polyctena. Oikos, 56, 3-16.
61. Savolainen, R., Vepsäläinen, K. and Wuorenrinne, H. (1988) Ant assemblages in the taiga biome: testing the role of territorial wood ants. Oecologia, 81, 481-486.
62. Schäfer, S. and Bicker, G. (1986) Distribution of GABA-like immunoreactivity in the brain and suboesophagal ganglion of the honeybee. Journal of Comparative Neurology, 246, 287-300.
63. Schulz, D.J., Barron, A.B. and Robinson, G.E. (2002) A role for octopamine in honey bee division of labor. Brain, Behavior and Evolution, 60, 350-359.
64. Schulz, D.J., Elekonich, M.M. and Robinson, G.E. (2003) Biogenic amines in the antennal lobes and the initiation and maintenance of foraging behavior in honey bees. Journal of Neurobiology, 54, 406-416.
65. Schulz, D.J. and Robinson, G.E. (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. Journal of Comparative Physiology A, 184, 481-488.
66. Seid, M.A., Goode, K., Li, C. and Traniello, J.F.A. (2008) Age- and subcaste-related patterns of serotonergic immunoreactivity in the optic lobes of the ant Pheidole dentata. Developmental Neurobiology, 68, 1325-1333.
67. Seid, M.A. and Traniello, J.F.A. (2005) Age-related changes in biogenic amines in individual brains of the ant Pheidole dentata. Naturwissenschaften, 92, 198-201.
68. Skibińska, E. (1982) L'étude du phénomene de la monogynie et de la polygynie chez Formica (Coptoformica) exsecta Nyl. Memorabilia Zoologica, 38, 67-111.
69. Smith, B.H., Huerta, R., Bazhenov, M. and Sinakevitch, I. (2012) Distributed plasticity for olfactory learning and memory in the honey bee brain. Honeybee Neurobiology and Behavior: A Tribute to Randolf Menzel (eds. C.G. Galizia, D. Eisenhardt & M. Giurfa ), pp. 393-408. Springer Science +Business Media, Heidelberg.
70. Smith, S. and Sharp, T. (1994) Measurement of GABA in rat brain microdialysates using opthaldialdehyde-sulphite derivatization and high-performance liquid chromatography with electrochemical detection. Journal of Chromatography B, 652, 228-233.
71. Šustková-Fišerová, M., Vávrová, J. and Kršiak, M. (2009) Brain levels of GABA, glutamate and aspartate in sociable, aggressive and timid mice: an in vivo microdialysis study. Neuroendocrinology Letters, 30, 79-84.
72. Szczuka, A. and Godzińska, E.J. (1997) The effect of past and present group size on responses to prey in the ant Formica polyctena Först. Acta Neurobiologiae Experimentalis, 57, 135-150.
73. Szczuka, A. and Godzińska, E.J. (2004) The role of group size in the control of expression of predatory behavior in workers of the red wood ant Formica polyctena (Hymenoptera: Formicidae). Sociobiology, 43, 295-325.
74. Taylor, D.J., Robinson, G.E., Logan, B.J., Laverty, R. and Mercer, A.R. (1992) Changes in brain amine levels associated with the morphological and behavioural development of the worker honeybee. Journal of Comparative Physiology A, 170, 715-721.
75. Vander Meer, R.K. and Alonso, L.E. (2002) Queen primer pheromone affects conspecific fire ant (Solenopsis invicta) aggression. Behavioral Ecology and Sociobiology, 51, 122-130.
76. Vander Meer, R.K., Preston, C.A. and Hefetz, A. (2008) Queen regulates biogenic amine level and nestmate recognition in workers of the fire ant, Solenopsis invicta. Naturwissenschaften, 95, 1155-1158.
77. Vepsäläinen, K. and Pisarski, B. (1982) Assembly of island ant communities. Annales Zoologici Fennici, 19, 327-335.
78. Vepsäläinen, K. and Savolainen, R. (1990) The effect of interference by formicine ants on the foraging of Myrmica. Journal of Animal Ecology, 59, 643-654.
79. Wagener-Hulme, C., Kuehn, J.C., Schulz, D.J. and Robinson, G.E. (1999) Biogenic amines and division of labor in honey bee colonies. Journal of Comparative Physiology A, 184, 471-479.
80. Wnuk, A. (2012) Neurochemical and Social Determinants of Ant Aggressive Behaviour. PhD Thesis (in Polish), Nencki Institute of Experimental Biology PAS, Warsaw, p. 212.
81. Wnuk, A., Kostowski, W., Korczyńska, J., Szczuka, A., Symonowicz, B., Bieńkowski, P., Mierzejewski, P. and Godzińska, E.J. (2012) Participation in aggressive encounters masks differences in brain GABA and Glu levels related to behavioural status of ant workers. FENS Abstract, Vol. 6, p. 157.07.
82. Wnuk, A., Wiater, M. and Godzińska, E.J. (2011) Effect of past and present behavioural specialization on brain levels of biogenic amines in workers of the red wood ant Formica polyctena. Physiological Entomology, 36, 54-61.
83. Zwarts, L., Magwire, M.M., Carbone, M.A., Versteven, M., Herteleer, L., Anholt, R.R., Callaerts, P. and Mackay, T.F.C. (2011) Complex genetic architecture of Drosophila aggressive behavior. Proceedings of the National Academy of Sciences of the United States of America, 108, 17070-17075.