Cell and Tissue Research

, Volume 363, Issue 3, pp 679–692 | Cite as

Novel antennal lobe substructures revealed in the small hive beetle Aethina tumida

  • Martin Kollmann
  • Anna Lena Rupenthal
  • Peter Neumann
  • Wolf Huetteroth
  • Joachim Schachtner
Regular Article


The small hive beetle, Aethina tumida, is an emerging pest of social bee colonies. A. tumida shows a specialized life style for which olfaction seems to play a crucial role. To better understand the olfactory system of the beetle, we used immunohistochemistry and 3-D reconstruction to analyze brain structures, especially the paired antennal lobes (AL), which represent the first integration centers for odor information in the insect brain. The basic neuroarchitecture of the A. tumida brain compares well to the typical beetle and insect brain. In comparison to other insects, the AL are relatively large in relationship to other brain areas, suggesting that olfaction is of major importance for the beetle. The AL of both sexes contain about 70 olfactory glomeruli with no obvious size differences of the glomeruli between sexes. Similar to all other insects including beetles, immunostaining with an antiserum against serotonin revealed a large cell that projects from one AL to the contralateral AL to densely innervate all glomeruli. Immunostaining with an antiserum against tachykinin-related peptides (TKRP) revealed hitherto unknown structures in the AL. Small TKRP-immunoreactive spherical substructures are in both sexes evenly distributed within all glomeruli. The source for these immunoreactive islets is very likely a group of about 80 local AL interneurons. We offer two hypotheses on the function of such structures.


Olfactory system Neuropeptide Serotonin Insect 3D reconstruction 



We thank Dr. Agricola for kindly providing the Locusta migratoria Tachykinin II antibody, as well as Dr. Buchner for the supply of the Drosophila melanogaster Synapsin I antibody. We thank the Department of Zoology and Entomology of the University of Pretoria (Pretoria/Tshwane South Africa) for providing kind local support and laboratory facilities. We also want to thank Martina Kern for expert technical assistance.

Supplementary material

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  1. Agnati Z, Zoli M, Strömberg I, Fuxe K (1995) Intercellular communication in the brain: wiring versus volume transmission. Neuroscience 69:711–726PubMedCrossRefGoogle Scholar
  2. Âgren L (1985) Architecture of a lamellicorn flagellum (Phyllopertha horticola, Scarabeidae, Coleoptera, Insecta). J Morphol 186:85–94CrossRefGoogle Scholar
  3. Allsopp PG (1990) Sexual dimorphism in the adult antennae of Antitrogus parvulus Britton and Lepidiota negatoria Blackburn (Coleoptera: Scarabaeidae: Melolonthinae). J Aust Entomol Soc 29:261–266CrossRefGoogle Scholar
  4. Anton S, Homberg U (1999) Antennal lobe structure. In: Hansson BS (ed) Insect olfaction. Springer, Berlin, pp 97–124CrossRefGoogle Scholar
  5. Arnaud L, Brostaux Y, Lallemand S, Haubruge E (2005) Reproductive strategies of Tribolium flour beetles. J Insect Sci 5:33PubMedCentralPubMedCrossRefGoogle Scholar
  6. Arnold G, Masson C, Budharugsa S (1985) Comparative study of the antennal lobes and their afferent pathway in the worker bee and the drone Apis mellifera. Cell Tissue Res 242:593–605CrossRefGoogle Scholar
  7. Berg BG, Schachtner J, Utz S, Homberg U (2007) Distribution of neuropeptides in the primary olfactory centre of the heliothine moth Heliothis virescens. Cell Tissue Res 327:385–398PubMedCrossRefGoogle Scholar
  8. Berg BG, Schachtner J, Homberg U (2009) Distribution of GABA and neuropeptides in the antennal lobe of the heliothine moth Heliothis virescens. Cell Tissue Res 335:593–605PubMedCrossRefGoogle Scholar
  9. Beutel RG, Pohl H, Hünefeld F (2005) Strepsipteran brains and effects of miniaturization (Insecta). Arthropod Struct Dev 34:301–313CrossRefGoogle Scholar
  10. Bicker G (1999) Histochemistry of classical neurotransmitters in antennal lobes and mushroom bodies of the honeybee. Microsc Res Tech 45:174–183PubMedCrossRefGoogle Scholar
  11. Binzer M, Heuer CM, Kollmann M et al (2014) Neuropeptidome of Tribolium castaneum antennal lobes and mushroom bodies. J Comp Neurol 522:337–357PubMedCrossRefGoogle Scholar
  12. Bohbot J, Pitts RJ, Kwon HW, Rützler M, Robertson HM, Zwiebel LJ (2007) Molecular characterization of the Aedes aegypti odorant receptor gene family. Insect Mol Biol 16:525–537PubMedCentralPubMedGoogle Scholar
  13. Brandt R, Rohlfing T, Rybak J, Krofczik S, Maye A, Westerhoff M, Hege HC, Menzel R (2005) Threedimensional average-shape atlas of the honeybee brain and its applications. J Comp Neurol 492:1–19PubMedCrossRefGoogle Scholar
  14. Breidbach O, Wegerhoff R (1994) FMRFamide-like immunoreactive neurons in the brain of the beetle, Tenebrio molitor L. (coleoptera – tenebrionidae): constancies and variations in development from the embryo to the adult. Int J Insect Morphol Embryol 4:383–404CrossRefGoogle Scholar
  15. Brockmann A, Brückner D (2001) Structural differences in the drone olfactory system of two phylogenetically distant Apis species, A. florea and A. mellifera. Naturwissenschaften 88:78–81PubMedCrossRefGoogle Scholar
  16. Cachero S, Ostrovsky AD, Yu JY, Dickson BJ, Jefferis GSXE (2010) Sexual dimorphism in the fly brain. Curr Biol 20:1589–1601PubMedCentralPubMedCrossRefGoogle Scholar
  17. Carlsson MA, Diesner M, Schachtner J, Nässel D (2010) Multiple neuropeptides in the Drosophila antennal lobe suggest complex modulatory circuits. J Comp Neurol 518:3359–3380PubMedCrossRefGoogle Scholar
  18. Chou YH, Spletter ML, Yaksi E, Leong JC, Wilson RI, Luo L (2010) Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe. Nat Neurosci 13:439–449PubMedCentralPubMedCrossRefGoogle Scholar
  19. Clements AN (1999) The biology of mosquitoes: sensory reception and behaviour. CABI, WallingfordGoogle Scholar
  20. Dacks AM, Christensen TA, Hildebrand JG (2006) Phylogeny of a serotonin-immunoreactive neuron in the primary olfactory center of the insect brain. J Comp Neurol 498:727–746PubMedCrossRefGoogle Scholar
  21. Dacks AM, Green DS, Root CM, Nighorn AJ, Wang JW (2009) Serotonin modulates olfactory processing in the antennal lobe of Drosophila. J Neurogenet 23:366–377PubMedCentralPubMedCrossRefGoogle Scholar
  22. Davis RL (2004) Olfactory learning. Neuron 44:31–48PubMedCrossRefGoogle Scholar
  23. De Guzman LI, Frake AM, Rinderer TE, Arbogast RT (2011) Effect of height and color on the efficiency of pole traps for Aethina tumida (Coleoptera: Nitidulidae). J Econ Entomol 104:26–31PubMedCrossRefGoogle Scholar
  24. Dreyer D, Vitt H, Dippel S, Goetz B, el Jundi B, Kollmann M, Huetteroth W, Schachtner J (2010) 3D standard brain of the red flour beetle Tribolium castaneum: a tool to study metamorphic development and adult plasticity. Front Syst Neurosci 4:3PubMedCentralPubMedGoogle Scholar
  25. Ehmer B, Gronenberg W (2004) Mushroom body volumes and visual interneurons in ants: comparison between sexes and castes. J Comp Neurol 469:198–213PubMedCrossRefGoogle Scholar
  26. el Jundi B, Huetteroth W, Kurylas AE, Schachtner J (2009) Anisometric brain dimorphism revisited: implementation of a volumetric 3D standard brain in Manduca sexta. J Comp Neurol 517:210–225PubMedCrossRefGoogle Scholar
  27. Elzen PJ, Baxter JR, Westervelt D, Randall C, Wilson WT (2000) A scientific note on observations of the small hive beetle, Aethina tumida Murray (Coleoptera Nitidulidae) in Florida, USA. Apidologie 31:593–594CrossRefGoogle Scholar
  28. Esslen J, Kaissling KE (1976) Zahl und Verteilung antennaler Sensillen bei der Honigbiene (Apis mellifera L.). Zoomorphologie 83:227–251CrossRefGoogle Scholar
  29. Farris SM, Roberts NS (2005) Coevolution of generalist feeding ecologies and gyrencephalic mushroom bodies in insects. Proc Natl Acad Sci U S A 102:17394–17399PubMedCentralPubMedCrossRefGoogle Scholar
  30. Flanagan D, Mercer AR (1989) An atlas and 3-D reconstruction of the antennal lobes in the worker honey bee, Apis mellifera L. (Hymenoptera: Apidae). Int J Insect Morphol Embryol 18:145–159CrossRefGoogle Scholar
  31. Friedrich M, Rambold I, Melzer RR (1996) The early stages of ommatidial development in the flour beetle Tribolium castaneum (Coleoptera; Tenebrionidae). Dev Genes Evol 206:136–146PubMedCrossRefGoogle Scholar
  32. Fusca D, Schachtner J, Kloppenburg P (2015) Colocalization of allatotropin and tachykinin-related peptides with classical transmitters in physiologically distinct subtypes of olfactory local interneurons in the cockroach (Periplaneta americana). J Comp Neurol 523:1569–1586PubMedCrossRefGoogle Scholar
  33. Gatellier L, Nagao T, Kanzaki R (2004) Serotonin modifies the sensitivity of the male silkmoth to pheromone. J Exp Biol 207:2487–2496PubMedCrossRefGoogle Scholar
  34. Ghaffar H, Larsen JR, Booth GM, Perkes R (1984) General morphology of the brain of the blind cave beetle, Neaphaenops tellkampfii Erichson (Coleoptera - Carabidae). Int J Insect Morphol Embryol 13:357–371CrossRefGoogle Scholar
  35. Graham JR, Ellis JD, Carroll MJ, Teal PEA (2011) Aethina tumida (Coleoptera: Nitidulidae) attraction to volatiles produced by Apis mellifera (Hymenoptera: Apidae) and Bombus impatiens (Hymenoptera: Apidae) colonies. Apidologie 3:326–336CrossRefGoogle Scholar
  36. Greco MK, Hoffmann D, Dollin A, Duncan M, Spooner-Hart R, Neumann P (2010) The alternative Pharaoh approach: stingless bees mummify beetle parasites alive. Naturwissenschaften 97:319–323PubMedCrossRefGoogle Scholar
  37. Grimm R (2001) Faunistik und Taxonomie einiger Arten der Gattung Tribolium Macleay, 1825, mit Beschreibung von drei neuen Arten aus Afrika. (Coleoptera, Tenebrionidae). Entomofauna 22:393–404Google Scholar
  38. Gronenberg W, Liebig J (1999) Smaller brains and optic lobes in reproductive workers of the ant Harpegnathos. Naturwissenschaften 86:343–345CrossRefGoogle Scholar
  39. Halcroft M, Spooner-Hart R, Neumann P (2011) Behavioural defence strategies of the stingless bee, Austroplebeia australis, against the small hive beetle, Aethina tumida. Insect Soc 58:245–253CrossRefGoogle Scholar
  40. Hansson BS (1997) Antennal lobe projection patterns of pheromone-specific olfactory receptor neurons in moths. In: Cardé RT, Minks AK (eds) Insect pheromone research. Springer, New York, pp 164–183Google Scholar
  41. Hansson BS, Stensmyr MC (2011) Evolution of insect olfaction. Neuron 72:698–711PubMedCrossRefGoogle Scholar
  42. Heisenberg M (2003) Mushroom body memoir: from maps to models. Nat Rev Neurosci 4:266–275PubMedCrossRefGoogle Scholar
  43. Hepburn HR, Radloff SE (1998) Honeybees of Africa. Springer, BerlinCrossRefGoogle Scholar
  44. Heuer CM, Kollmann M, Binzer M, Schachtner J (2012) Neuropeptides in insect mushroom bodies. Arthropod Struct Dev 41:199–226PubMedCrossRefGoogle Scholar
  45. Hill ES, Okada K, Kanzaki R (2003) Visualization of modulatory effects of serotonin in the silkmoth antennal lobe. J Exp Biol 206:345–352PubMedCrossRefGoogle Scholar
  46. Homberg U (2002) Neurotransmitters and neuropeptides in the brain of the locust. Microsc Res Tech 56:189–209PubMedCrossRefGoogle Scholar
  47. Homberg (2008) Evolution of the central complex in the arthropod brain with respect to the visual system. Arthropod Struct Dev 37(5):347–362PubMedCrossRefGoogle Scholar
  48. Hu JH, Wang ZY, Sun F (2011) Anatomical organization of antennal-lobe glomeruli in males and females of the scarab beetle Holotrichia diomphalia (Coleoptera: Melolonthidae). Arthropod Struct Dev 40:420–428PubMedCrossRefGoogle Scholar
  49. Huetteroth W, Schachtner J (2005) Standard three-dimensional glomeruli of the Manduca sexta antennal lobe: a tool to study both developmental and adult neuronal plasticity. Cell Tissue Res 319:513–524PubMedCrossRefGoogle Scholar
  50. Husch A, Paehler M, Fusca D, Paeger L, Kloppenburg P (2009) Distinct electrophysiological properties in subtypes of nonspiking olfactory local interneurons correlate with their cell type-specific Ca2+ current profiles. J Neurophysiol 29:11582.11592Google Scholar
  51. Ignell R, Dekker T, Ghaninia M, Hansson BS (2005) Neuronal architecture of the mosquito deutocerebrum. J Comp Neurol 493:207–240PubMedCrossRefGoogle Scholar
  52. Ignell R, Root CM, Birse RT, Wang JW, Nässel DR, Winther ÅM (2009) Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila. Proc Natl Acad Sci U S A 106:13070–13075PubMedCentralPubMedCrossRefGoogle Scholar
  53. Kaissling KE (1971) Insect olfaction. In: Handbook of sensory physiology, vol 4. Springer, Berlin, pp 351–431Google Scholar
  54. Kelber C, Rössler W, Kleineidam CJ (2010) Phenotypic plasticity in number of glomeruli and sensory innervation of the antennal lobe in leaf-cutting ant workers (A. vollenweideri). Dev Neurobiol 70:222–234PubMedCrossRefGoogle Scholar
  55. Klagges BRE, Heimbeck G, Godenschwege TA, Hofbauer A, Pflugfelder GO, Reifegerste R, Reisch D, Schaupp M, Buchner S, Buchner E (1996) Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J Neurosci 16:3154–3165PubMedGoogle Scholar
  56. Kleineidam CJ, Obermayer M, Halbich W, Rössler W (2005) A macroglomerulus in the antennal lobe of leaf-cutting ant workers and its possible functional significance. Chem Senses 30:383–392PubMedCrossRefGoogle Scholar
  57. Kloppenburg P, Hildebrand JG (1995) Neuromodulation by 5-hydroxytryptamine in the antennal lobe of the sphinx moth Manduca sexta. J Exp Biol 198:603–611PubMedGoogle Scholar
  58. Kollmann M, Minoli S, Bonhomme J, Homberg U, Schachtner J, Tagu D, Anton S (2011a) Revisiting the anatomy of the central nervous system of a hemimetabolous model insect species: the pea aphid Acyrthosiphon pisum. Cell Tissue Res 343:343–355PubMedCrossRefGoogle Scholar
  59. Kollmann M, Huetteroth W, Schachtner J (2011b) Brain organization in Collembola (springtails). Arthropod Struct Dev 40:304–316PubMedCrossRefGoogle Scholar
  60. Kondoh Y, Kaneshiro KY, Kimura K, Yamamoto D (2003) Evolution of sexual dimorphism in the olfactory brain of Hawaiian Drosophila. Proc R Soc Lond B 270:1005–1013CrossRefGoogle Scholar
  61. Kuebler LS, Kelber C, Kleineidam CJ (2010) Distinct antennal lobe phenotypes in the leaf-cutting ant (Atta vollenweideri). J Comp Neurol 518:352–365PubMedCrossRefGoogle Scholar
  62. Kurylas AE, Rohlfing T, Krofczik S, Jenett A, Homberg U (2008) Standardized atlas of the brain of the desert locust, Schistocerca gregaria. Cell Tissue Res 333:125–145PubMedCrossRefGoogle Scholar
  63. Kvello P, Løfaldli BB, Rybak J, Menzel R, Mustaparta H (2009) Digital, three-dimensional average shaped atlas of the Heliothis virescens brain with integrated gustatory and olfactory neurons. Front Syst Neurosci 3:14. doi: 10.3389/neuro.06.014.2009 PubMedCentralPubMedCrossRefGoogle Scholar
  64. Larsson MC, Hansson BS, Strausfeld NJ (2004) A simple mushroom body in an African scarabid beetle. J Comp Neurol 478:219–232PubMedCrossRefGoogle Scholar
  65. Linn CE, Roelofs WL (1986) Modulatory effects of octopamine and serotonin on male sensitivity and periodicity of response to sex pheromone in the cabbage looper moth, Trichoplusia ni. Arch Insect Biochem Physiol 3:161–171CrossRefGoogle Scholar
  66. Lundie AE (1940) The small hive beetle, Aethina tumida. Bulletin no 220, South African Department of Agriculture and Forestry, PretoriaGoogle Scholar
  67. McGuire SE, Le PT, Davis RL (2001) The role of Drosophila mushroom body signaling in olfactory memory. Science 10:1126–1129Google Scholar
  68. Menzel R (2001) Searching for the memory trace in a mini-brain, the honeybee. Learn Mem 8:53–62PubMedCrossRefGoogle Scholar
  69. Miura N, Nakagawa T, Tatsuki S, Touhara K, Ishikawa Y (2009) A male-specific odorant receptor conserved through the evolution of sex pheromones in Ostrinia moth species. Int J Biol Sci 5:319–330PubMedCentralPubMedCrossRefGoogle Scholar
  70. Montgomery SH, Ott SR (2014) Brain composition in Godyris zavaleta, a diurnal butterfly, reflects an increased reliance on olfactory information. J Comp Neurol 523:869–891PubMedCentralPubMedCrossRefGoogle Scholar
  71. Mutinelli F, Montarsi F, Federico G, Granato A, Ponti AM, Grandinetti G et al (2014) Detection of Aethina tumida Murray (Coleoptera: Nitidulidae.) in Italy: outbreaks and early reaction measures. J Apic Res 53:569–575CrossRefGoogle Scholar
  72. Mysore K, Subramanian KA, Sarasij RC, Suresh A, Shyamala BV, VijayRaghavan K, Rodrigues V (2009) Caste and sex specific olfactory glomerular organization and brain architecture in two sympatric ant species, Camponotus sericeus and Camponotus compressus (Fabricius, 1798). Arthropod Struct Dev 38:485–497PubMedCrossRefGoogle Scholar
  73. Nagel KI, Hong EJ, Wilson RI (2015) Synaptic and circuit mechanisms promoting broadband transmission of olfactory stimulus dynamics. Nat Neurosci 18:56–65PubMedCentralPubMedCrossRefGoogle Scholar
  74. Nakagawa T, Sakurai T, Nishioka T, Touhara K (2005) Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 307:1638–1642PubMedCrossRefGoogle Scholar
  75. Nässel DR (2002) Neuropeptides in the nervous system of Drosophila and other insects: multiple roles as neuromodulators and neurohormones. Prog Neurobiol 68:1–84PubMedCrossRefGoogle Scholar
  76. Neumann P (2015) Small hive beetle in Italy: what can we expect in the future? In: Carreck NL (ed) The small hive beetle in Europe. International Bee Research Association, GroombridgeGoogle Scholar
  77. Neumann P, Ellis JD (2008) The small hive beetle (Aethinatumida Murray, Coleoptera: Nitidulidae): distribution, biology and control of an invasive species. J Apic Res 47:181–183CrossRefGoogle Scholar
  78. Neumann P, Elzen PJ (2004) The biology of the small hive beetle (Aethina tumida Murray, Coleoptera: Nitidulidae): Gaps in our knowledge of an invasive species. Apidologie 35:229–247CrossRefGoogle Scholar
  79. Neumann P, Hoffmann D, Duncan M, Spooner-Hart R, Pettis JS (2012) Long-range dispersal of small hive beetles. J Agic Res 51:214–215Google Scholar
  80. Neumann P, Evans J, Pettis JS, Pirk CWW, Schäfer MO, Tanner G, Ellis JD (2013) Standard methods for small hive beetle research. In: Dietemann V, Ellis JD, Neumann P (Eds) The COLOSS BEEBOOK, Volume II: standard methods for Apis mellifera pest and pathogen research. J Apic Res 52: 1–32Google Scholar
  81. Neupert S, Fusca D, Schachtner J, Kloppenburg P, Predel R (2012) Towards a single-cell-based analysis of neuropeptide expression in Periplaneta americana antennal lobe neurons. J Comp Neurol 520:694–716PubMedCrossRefGoogle Scholar
  82. Okada R, Awasaki T, Ito K (2009) Gamma-aminobutyric acid (GABA)-mediated neural connections in the Drosophila antennal lobe. J Comp Neurol 514:74–91PubMedCrossRefGoogle Scholar
  83. Olsen SR, Wilson RI (2008) Lateral presynaptic inhibition mediates gain control in an olfactory circuit. Nature 452:956–960PubMedCentralPubMedCrossRefGoogle Scholar
  84. Olsen SR, Bhandawat V, Wilson RI (2007) Excitatory interactions between olfactory processing channels in the Drosophila antennal lobe. Neuron 54:89–103PubMedCentralPubMedCrossRefGoogle Scholar
  85. Olsen SR, Bhandawat V, Wilson RI (2010) Divisive normalization in olfactory population codes. Neuron 66:287–299PubMedCentralPubMedCrossRefGoogle Scholar
  86. Petroski RJ, Bartelt RJ, Vetter RS (1994) Male-produced aggregation pheromone of Carpophilusobsoletus (Coleoptera, Nitidulidae). J Chem Ecol 20:1483–1493PubMedCrossRefGoogle Scholar
  87. Rein K, Zöckler M, Mader MT, Grübel C, Heisenberg M (2002) The Drosophila standard brain. Curr Biol 12:227–231PubMedCrossRefGoogle Scholar
  88. Renou M, Tauban D, Morin J-P (1998) Structure and function of antennal poreplate sensilla of Oryctes rhinoceros (L.) (Coleoptera : Dynastinae). Int J Insect Morphol Embryol 27:227–233CrossRefGoogle Scholar
  89. Robertson HM, Wanner KW (2006) The chemoreceptor superfamily in the honey bee, Apis mellifera: expansion of the odorant, but not gustatory, receptor family. Genome Res 16:1395–1403PubMedCentralPubMedCrossRefGoogle Scholar
  90. Root CM, Semmelhack JL, Wong AM, Flores J, Wang JW (2007) Propagation of olfactory information in Drosophila. Proc Natl Acad Sci U S A 104:11826–11831PubMedCentralPubMedCrossRefGoogle Scholar
  91. Rospars JP (1983) Invariance and sex-specific variations of the glomerular organization in the antennal lobes of a moth, Mamestra brassicae, and a butterfly, Pieris brassicae. J Comp Neurol 220:80–96PubMedCrossRefGoogle Scholar
  92. Rospars JP, Hildebrand JG (2000) Sexually dimorphic and isomorphic glomeruli in the antennal lobes of the sphinx moth Manduca sexta. Chem Senses 25:119–129PubMedCrossRefGoogle Scholar
  93. Ruther J, Reinecke A, Thiemann K, Tolasch T, Francke W, Hilker M (2000) Mate finding in the forest cockchafer, Melolontha hippocastani, mediated by volatiles from plants and females. Physiol Entomol 25:172–179CrossRefGoogle Scholar
  94. Sachse S, Galizia CG (2002) Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. J Neurophysiol 87:1106–1117PubMedGoogle Scholar
  95. Sakura M, Mizunami M (2001) Olfactory learning and memory in the cockroach Periplaneta americana. Zool Sci 18:21–28CrossRefGoogle Scholar
  96. Schachtner J, Schmidt M, Homberg U (2005) Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea and Hexapoda). Arthropod Struct Dev 34:257–299CrossRefGoogle Scholar
  97. Schmolke MD (1974) A study of Aethina tumida: the small Hive Beetle, Project Report. University of Rhodesia, HarareGoogle Scholar
  98. Schneider D (1992) 100 years of pheromone research: an essay on Lepidoptera. Naturwissenschaften 79:241–250CrossRefGoogle Scholar
  99. Seki Y, Kanzaki R (2008) Comprehensive morphological identification and GABA immunocytochemistry of antennal lobe local interneurons in Bombyx mori. J Comp Neurol 506:93–107PubMedCrossRefGoogle Scholar
  100. Seki Y, Rybak J, Wicher D, Sachse S, Hansson BS (2010) Physiological and morphological characterization of local interneurons in the Drosophila antennal lobe. J Neurophysiol 104:1007–1019PubMedCrossRefGoogle Scholar
  101. Settembrini BP, Villar MJ (2005) FMRFamide-like immunocyrochemistry in the brain and subesophageal ganglion of Triatoma infestans (Insecta: Heteroptera). Coexpression with ß-pigment-dispersing hormone and small cardioactive peptide. Cell Tissue Res 321:299–310PubMedCrossRefGoogle Scholar
  102. Shang Y, Claridge-Chang A, Sjulson L, Pypaert M, Miesenböck G (2007) Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell 128:601–612PubMedCentralPubMedCrossRefGoogle Scholar
  103. Siju KP, Schachtner J, Reifenrath A, Scheiblich H, Neupert S, Predel R, Hansson B, Ignell R (2014) Neuropeptides in the antennal lobe of the yellow fever mosquito, Aedes aegypti. J Neurophysiol 522:592–608Google Scholar
  104. Silbering AF, Galizia CG (2007) Processing of odor mixtures in the Drosophila antennal lobe reveals both global inhibition and glomerulus-specific interactions. J Neurosci 27:11966–11977PubMedCrossRefGoogle Scholar
  105. Slessor KN, Winston ML, Le Conte Y (2005) Pheromone communication in the honeybee (Apis mellifera L.). J Chem Ecol 31:2731–2745PubMedCrossRefGoogle Scholar
  106. Sokoloff A (1977) The biology of tribolium with special emphasis on genetic aspects. Oxford University Press, LondonGoogle Scholar
  107. Spiewok S, Neumann P (2006) Infestation of commercial bumblebee (Bombus impatiens) field colonies by small hive beetles (Aethina tumida). Ecol Entomol 31:623–628CrossRefGoogle Scholar
  108. Spiewok S, Neumann P (2012) Sex ratio and dispersal of small hive beetles. J Agric Res 51:216–217Google Scholar
  109. Stocker RF (2001) Drosophila as a focus in olfactory research: mapping of olfactory sensilla by fine structure, odor specificity, odorant receptor expression, and central connectivity. Microsc Res Tech 55:284–296PubMedCrossRefGoogle Scholar
  110. Stopfer M, Bhagavan S, Smith BH, Laurent G (1997) Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390:70–74PubMedCrossRefGoogle Scholar
  111. Strausfeld NJ (2005) The evolution of crustacean and insect optic lobes and the origins of chiasmata. Arthropod Struct Dev 34:235–256CrossRefGoogle Scholar
  112. Strauss R (2002) The central complex and the genetic dissection of locomotor behaviour. Curr Opin Neurobiol 12:633–638PubMedCrossRefGoogle Scholar
  113. Streinzer M, Kelber C, Pfabigan S, Kleineidam CJ, Spaethe J (2013) Sexual dimorphism in the olfactory system of a solitary and a eusocial bee species. J Comp Neurol 521:42–55CrossRefGoogle Scholar
  114. Suazo A, Torto B, Teal PEA, Tumlinson JH (2003) Response of the small hive beetle (Aethinatumida) to honey bee (Apis mellifera) and beehive-produced volatiles. Apidologie 34:525–533CrossRefGoogle Scholar
  115. Tanaka NK, Ito K, Stopfer M (2009) Odor-evoked neural oscillations in Drosophila are mediated by widely branching interneurons. J Neurosci 29:8595–8603PubMedCentralPubMedCrossRefGoogle Scholar
  116. Trhlin M, Rajchard J (2011) Chemical communication in the honeybee (Apis mellifera L.): a review. Vet Med 56:265–273Google Scholar
  117. Utz S, Huetteroth W, Vömel M, Schachtner J (2008) Mas-allatotropin in the developing antennal lobe of the sphinx moth Manduca sexta: distribution, time course, developmental regulation and colocalization with other neuropeptides. Dev Neurobiol 68:123–142PubMedCrossRefGoogle Scholar
  118. Van Haeften T (1993) Location and function of serotonin in the central and peripheral nervous system of the Colorado potato beetle. PhD thesis, University of Wageningen, The Netherlands. (ISBN 1993 90 5485 141 4)Google Scholar
  119. Veenstra JA, Lau GW, Agricola HJ, Petzel DH (1995) Immunohistochemical localization of regulatory peptides in the midgut of the female mosquito Aedes aegypti. Histochem. Cell Biol 104:337–347Google Scholar
  120. Vitzthum H, Homberg U (1998) Immunocytochemical demonstration of locustatachykinin‐related peptides in the central complex of the locust brain. J Comp Neurol 390:455–469PubMedCrossRefGoogle Scholar
  121. Vosshall LB, Stocker RF (2007) Molecular architecture of smell and taste in Drosophila. Annu Rev Neurosci 30:505–533PubMedCrossRefGoogle Scholar
  122. Vosshall LB, Wong AM, Axel R (2000) An olfactory sensory map in the fly brain. Cell 102:147–159PubMedCrossRefGoogle Scholar
  123. Wegerhoff R, Breidbach O, Lobemeier M (1996) Development of locustatachykinin immunopositive neurons in the central complex of the beetle Tenebrio molitor. J Comp Neurol 375:157–166PubMedCrossRefGoogle Scholar
  124. Wei H, el Jundi B, Homberg U, Stengl M (2010) Implementation of pigment-dispersing factor- immunoreactive neurons in a standardized atlas of the brain of the cockroach Leucophaea maderae. J Comp Neurol 518:4113–4133PubMedCrossRefGoogle Scholar
  125. Weissteiner S, Huetteroth W, Kollmann M, Weißbecker B, Romani R, Schachtner J, Schütz S (2012) Cockchafer larvae smell host root scents in soil. PLoS ONE 7(10)Google Scholar
  126. Wessnitzer J, Webb B (2006) Multimodal sensory integration in insects – towards insect brain control architectures. Bioinspir Biomim 1:63–75PubMedCrossRefGoogle Scholar
  127. Wilson RI (2013) Early olfactory processing in Drosophila: mechanisms and principles. Annu Rev Neurosci 36:217–241PubMedCentralPubMedCrossRefGoogle Scholar
  128. Wilson RI, Laurent G (2005) Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J Neurosci 25:9069–9079PubMedCrossRefGoogle Scholar
  129. Winther ÅME, Ignell R (2010) Local peptidergic signaling in the antennal lobe shapes olfactory behavior. Fly 4:167–171PubMedCrossRefGoogle Scholar
  130. Winther ÅME, Acebes A, Ferrús A (2006) Tachykinin-related peptides modulate odor perception and locomotor activity in Drosophila. Mol Cell Neurosci 31:399–406PubMedCrossRefGoogle Scholar
  131. Zhao X, Coptis V, Farri SM (2008) Metamorphosis and adult development of the mushroom bodies of the red flour beetle, Tribolium castaneum. Dev Neurobiol 68:1487–1502PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Martin Kollmann
    • 1
  • Anna Lena Rupenthal
    • 1
  • Peter Neumann
    • 2
  • Wolf Huetteroth
    • 1
    • 3
  • Joachim Schachtner
    • 1
  1. 1.Department of Biology, Animal PhysiologyPhilipps-University MarburgMarburgGermany
  2. 2.Institute of Bee Health, Vetsuisse FacultyUniversity of BernBernSwitzerland
  3. 3.Department of Biology, NeurobiologyUniversity of KonstanzKonstanzGermany

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