Skip to main content
SpringerLink
Log in

Characterization of the olfactory system of the giant honey bee, Apis dorsata

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Apis dorsata is an open-nesting, undomesticated, giant honey bee found in southern Asia. We characterized a number of aspects of olfactory system of Apis dorsata and compared it with the well-characterized, western honeybee, Apis mellifera, a domesticated, cavity-nesting species. A. dorsata differs from A. mellifera in nesting behavior, foraging activity, and defense mechanisms. Hence, there can be different demands on its olfactory system. We elucidated the glomerular organization of A. dorsata by creating a digital atlas for the antennal lobe and visualized the antennal lobe tracts and localized their innervations. We showed that the neurites of Kenyon cells with cell bodies located in a neighborhood in calyx retain their relative neighborhoods in the pedunculus and the vertical lobe forming a columnar organization in the mushroom body. The vertical lobe and the calyx of the mushroom body were found to be innervated by extrinsic neurons with cell bodies in the lateral protocerebrum. We found that the species was amenable to olfactory conditioning and showed good learning and memory retention at 24 h after training. It was also amenable to massed and spaced conditioning and could distinguish trained odor from an untrained novel odor. We found that all the above mentioned features in A. dorsata are very similar to those in A. mellifera. We thereby establish A. dorsata as a good model system, strikingly similar to A. mellifera despite the differences in their nesting and foraging behavior.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Abel R, Rybak J, Menzel R (2001) Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera. J Comp Neurol 437(3):363–383

    CAS  PubMed  Google Scholar 

  • Anton S, Homberg U (1999) Antennal lobe structure. Insect olfaction. Springer, Berlin, Heidelberg, pp 97–124

    Google Scholar 

  • Arias MC, Sheppard WS (2005) Phylogenetic relationships of honey bees (Hymenoptera: Apinae: Apini) inferred from nuclear and mitochondrial DNA sequence data. Mol Phylogenet Evol 37(1):25–35

    CAS  PubMed  Google Scholar 

  • 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(3):593–605

    Google Scholar 

  • Bastin F, Couto A, Larcher V, Phiancharoen M, Koeniger G, Koeniger N, Sandoz JC (2018) Marked interspecific differences in the neuroanatomy of the male olfactory system of honey bees (genus Apis). J Comp Neurol 526(18):3020–3034

    CAS  PubMed  Google Scholar 

  • Bicker G, Kreissl S, Hofbauer A (1993) Monoclonal antibody labels olfactory and visual pathways in Drosophila and Apis brains. J Comp Neurol 335(3):413–424

    CAS  PubMed  Google Scholar 

  • Bitterman M, Menzel R, Fietz A, Schäfer S (1983) Classical conditioning of proboscis extension in honeybees (Apis mellifera). J Comp Psychol 97(2):107

    CAS  PubMed  Google Scholar 

  • Brandt R, Rohlfing T, Rybak J, Krofczik S, Maye A, Westerhoff M, Menzel R (2005) Three-dimensional average shape atlas of the honeybee brain and its applications. J Comp Neurol 492(1):1–19

    PubMed  Google Scholar 

  • Brockmann A, Brückner D (1995) Projection pattern of poreplate sensory neurones in honey bee worker, Apis mellifera L. (Hymenoptera: Apidae). Int J Insect Morphol Embryol 24(4):405–411

    Google Scholar 

  • 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(2):78–81

    CAS  PubMed  Google Scholar 

  • Brockmann A, Brückner D (2003) Drone antennae and evolution of sex-pheromone communication in honey bees. Indian Bee J 65(3 & 4):131–138

    Google Scholar 

  • Carlsson MA, Galizia CG, Hansson BS (2002) Spatial representation of odours in the antennal lobe of the moth Spodoptera littoralis (Lepidoptera: Noctuidae). Chem Senses 27(3):231–244

    PubMed  Google Scholar 

  • Engel MS (1998) Fossil honey bees and evolution in the genus Apis (Hymenoptera: Apidae). Apidologie 29(3):265–281

    Google Scholar 

  • Esslen J, Kaissling KE (1976) Zahl und Verteilung antennaler Sensillen bei der Honigbiene (A. mellifera L.). Zoomorphologie 83(3):227–251

    Google Scholar 

  • 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(2-3):145–159

    Google Scholar 

  • Fonta C, Sun X, Masson C (1993) Morphology and spatial distribution of bee antennal lobe interneurones responsive to odours. Chem Senses 18(2):101–119

    Google Scholar 

  • Galizia CG (2008) Insect olfaction. In The Senses: A Comprehensive Reference. Vol 4. Olfaction & taste, ed. S Firestein GK Beauchamp San Diego: Academic: 725–70

  • Galizia CG, Menzel R (2000) Odour perception in honeybees: coding information in glomerular patterns. Curr Opin Neurobiol 10(4):504–510

    CAS  PubMed  Google Scholar 

  • Galizia CG, Rössler W (2010) Parallel olfactory systems in insects: anatomy and function. Annu Rev Entomol 55:399–420

    CAS  PubMed  Google Scholar 

  • Galizia CG, Szyszka P (2008) Olfactory coding in the insect brain: molecular receptive ranges, spatial and temporal coding. Entomologia experimentalis et applicata 128(1):81–92

    Google Scholar 

  • Galizia CG, McIlwrath SL, Menzel R (1999) A digital three-dimensional atlas of the honeybee antennal lobe based on optical sections acquired by confocal microscopy. Cell Tissue Res 295(3):383–394

    CAS  PubMed  Google Scholar 

  • Giurfa M (2007) Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well. J Comp Physiol A 193(8):801–824

    Google Scholar 

  • Giurfa M, Sandoz JC (2012) Invertebrate learning and memory: fifty years of olfactory conditioning of the proboscis extension response in honeybees. Learn Mem 19(2):54–66

    PubMed  Google Scholar 

  • Gowda V (2016) Allometric scaling of brain, brain components and neurons with body size of social bees. https://repository.arizona.edu/handle/10150/621438

  • Hammer M (1997) The neural basis of associative reward learning in honeybees. Trends Neurosci 20(6):245–252

    CAS  PubMed  Google Scholar 

  • Hansson BS, Anton S (2000) Function and morphology of the antennal lobe: new developments. Annu Rev Entomol 45(1):203–231

    CAS  PubMed  Google Scholar 

  • Hildebrand JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20(1):595–631

    CAS  PubMed  Google Scholar 

  • Ito I, Ong RC, Raman B, Stopfer M (2008) Sparse odor representation and olfactory learning. Nat Neurosci 11(10):1177–1184

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ito K, Shinomiya K, Ito M, Armstrong JD, Boyan G, Hartenstein V, Keshishian H (2014) A systematic nomenclature for the insect brain. Neuron 81(4):755–765

    CAS  PubMed  Google Scholar 

  • Jung J, Kim DI, Ilyasov R, Kim K, Kwon HW (2017) Comparative study of olfactory learning and memory in Apis cerana and Apis mellifera foragers. Jf Apicult 32(4):275–280

    Google Scholar 

  • Karpe SD, Jain R, Brockmann A, Sowdhamini R (2016) Identification of complete repertoire of Apis florea odorant receptors reveals complex orthologous relationships with Apis mellifera. Genome Biol Evol 8(9):2879–2895

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kaspi R, Shafir S (2012) Associative olfactory learning of the red dwarf honeybee Apis florea. Apidologie 44(1):100–109

    Google Scholar 

  • Kirschner S, Kleineidam CJ, Zube C, Rybak J, Grünewald B, Rössler W (2006) Dual olfactory pathway in the honeybee, Apis mellifera. J Comp Neurol 499(6):933–952

    PubMed  Google Scholar 

  • Kropf J, Kelber C, Bieringer K, Rossler W (2014) Olfactory subsystems in the honeybee: sensory supply and sex specificity. Cell Tissue Res 357(3):583–595

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar NR, Nayyar K, Sharma R, Anudeep A (2014) Ultramorphology of antennal sensilla of open-nesting honey bees Apis florea F. and Apis dorsata F.(Hymenoptera: Apidae). J Appl Nat Sci 6(1):315–319

    Google Scholar 

  • Laurent G (1997) Olfactory processing: maps, time and codes. Curr Opin Neurobiol 7(4):547–553

    CAS  PubMed  Google Scholar 

  • Lin T, Li C, Liu J, Smith B H, Lei H, Zeng X (2018) Glomerular organization in the antennal lobe of the oriental fruit fly Bactrocera dorsalis. Front Neuroanat 12

  • Margulies C, Tully T, Dubnau J (2005) Deconstructing memory in Drosophila. Curr Biol 15(17):R700–R713

    CAS  PubMed  PubMed Central  Google Scholar 

  • Masante-Roca I, Gadenne C, Anton S (2005) Three-dimensional antennal lobe atlas of male and female moths, Lobesia botrana (Lepidoptera: Tortricidae) and glomerular representation of plant volatiles in females. J Exp Biol 208(6):1147–1159

    PubMed  Google Scholar 

  • Matsumoto Y, Menzel R, Sandoz JC, Giurfa M (2012) Revisiting olfactory classical conditioning of the proboscis extension response in honey bees: a step toward standardized procedures. J Neurosci Methods 211(1):159–167

    PubMed  Google Scholar 

  • Menzel R (1993) Associative learning in honey bees. Apidologie 24(3):157–168

    Google Scholar 

  • Menzel R (1999) Memory dynamics in the honeybee. J Comp Physiol A 185(4):323–340

    Google Scholar 

  • Menzel R (2012) The honeybee as a model for understanding the basis of cognition. Nat Rev Neurosci 13(11):758

    CAS  PubMed  Google Scholar 

  • Menzel R, Erber J (1978) Learning and memory in bees. Sci Am 239(1):102–111

    Google Scholar 

  • Menzel R, Müller U (1996) Learning and memory in honeybees: from behavior to neural substrates. Annu Rev Neurosci 19(1):379–404

    CAS  PubMed  Google Scholar 

  • Menzel R, Hammer M, Müller U, Rosenboom H (1996) Behavioral, neural and cellular components underlying olfactory learning in the honeybee. J Physiol 90(5–6):395–398

    CAS  Google Scholar 

  • Menzel R, Manz G, Menzel R, Greggers U (2001) Massed and spaced learning in honeybees: the role of CS, US, the inter trial interval, and the test interval. Learn Mem 8(4):198–208

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mobbs P (1982) The brain of the honeybee Apis mellifera. I The connections and spatial organization of the mushroom bodies. Phil Trans R Soc Lond B 298(1091):309–354

    Google Scholar 

  • Mombaerts P, Wang DC, Chao SK, Nemes A, Mendelsohn M, Axel R (1996) Visualizing an olfactory sensory map. Cell 87(4):675–686

    CAS  PubMed  Google Scholar 

  • Muller D, Abel R, Brandt R, Zockler M, Menzel R (2002) Differential parallel processing of olfactory information in the honeybee, Apis mellifera L. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 188(5):359–370

    CAS  PubMed  Google Scholar 

  • Müller D, Abel R, Brandt R, Zöckler M, Menzel R (2002) Differential parallel processing of olfactory information in the honeybee, Apis mellifera L. J Comp Physiol A 188(5):359–370

    Google Scholar 

  • Nawrot MP (2012) Dynamics of sensory processing in the dual olfactory pathway of the honeybee. Apidologie 43:269

    CAS  Google Scholar 

  • Nishino H, Nishikawa M, Mizunami M, Yokohari F (2009) Functional and topographic segregation of glomeruli revealed by local staining of antennal sensory neurons in the honeybee Apis mellifera. J Comp Neurol 515(2):161–180

    PubMed  Google Scholar 

  • Pareto A (1972) Die zentrale Verteilung der Fühlerafferenz bei Arbeiterinnen der Honigbiene, Apis mellifera L. Z Zellforsch Mikrosk Anat 131(1):109–140

    CAS  PubMed  Google Scholar 

  • 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(11):000–000

    Google Scholar 

  • Rospars JP (1988) Structure and development of the insect antennodeutocerebral system. Int J Insect Morphol Embryol 17(3):243–294

    Google Scholar 

  • Rössler W, Brill MF (2013) Parallel processing in the honeybee olfactory pathway: structure, function, and evolution. J Comp Physiol A 199(11):981–996

    Google Scholar 

  • Sachse S, Galizia CG (2006) In microcircuits: the interface between neurons and global brain function. Topography and dynamics of the olfactory system. MIT press, Cambridge, MA, pp 251–273

    Google Scholar 

  • Sandoz JC, Menzel R (2001) Side-specificity of olfactory learning in the honeybee: generalization between odors and sides. Learn Mem 8(5):286–294

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schäfer S, Bicker G (1986) Distribution of GABA-like immunoreactivity in the brain of the honeybee. J Comp Neurol 246(3):287–300

    PubMed  Google Scholar 

  • Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Tinevez JY (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9(7):676

    CAS  PubMed  Google Scholar 

  • Sinakevitch IT, Smith AN, Locatelli F, Huerta R, Bazhenov M, Smith BH (2013) Apis mellifera octopamine receptor 1 (AmOA1) expression in antennal lobe networks of the honey bee (Apis mellifera) and fruit fly (Drosophila melanogaster). Front Syst Neurosci 7:70

    PubMed  PubMed Central  Google Scholar 

  • Smith BH, Menzel R (1989) The use of electromyogram recordings to quantify odourant discrimination in the honey bee, Apis mellifera. J Insect Physiol 35(5):369–375

    CAS  Google Scholar 

  • Soucy ER, Albeanu DF, Fantana AL, Murthy VN, Meister M (2009) Precision and diversity in an odor map on the olfactory bulb. Nat Neurosci 12(2):210–220

    CAS  PubMed  Google Scholar 

  • Squire LR (1987) Memory and brain. Oxford Univ. Press, New York/Oxford

    Google Scholar 

  • Stopfer M, Jayaraman V, Laurent G (2003) Intensity versus identity coding in an olfactory system. Neuron 39(6):991–1004

    CAS  PubMed  Google Scholar 

  • Suzuki H (1975) Antennal movements induced by odour and central projection of the antennal neurones in the honey-bee. J Insect Physiol 21(4):831–847

    Google Scholar 

  • Tully T, Preat T, Boynton S, Del Vecchio M (1994) Genetic dissection of consolidated memory in Drosophila. Cell 79(1):35–47

    CAS  PubMed  Google Scholar 

  • Wang Z, Tan K (2013) Comparative analysis of olfactory learning of Apis cerana and Apis mellifera. Apidologie 45(1):45–52

    Google Scholar 

  • Witthöft W (1967) Absolute anzahl und verteilung der zellen im him der honigbiene. Zeitschrift für Morphologie der Tiere 61(1):160–184

    Google Scholar 

  • Zwaka H, Münch D, Manz G, Menzel R, Rybak J (2016) The circuitry of olfactory projection neurons in the brain of the honeybee, Apis mellifera. Front Neuroanat 10:90

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to thank Uttam Krishna Sharma for his support in procuring Apis dorsata and Shilpi Singh for her support in carrying out electrophysiology and in editing the manuscript. We thank Ravindra Kumar Pydi (National Institute of Rural Development, Hyderabad) for providing Apis mellifera bees. We also thank Prasad Miriyala (Central Instruments Laboratory, University of Hyderabad) and Nalini Manthapuram (Centre for Nanotechnology, University of Hyderabad) for their support in confocal imaging. We are grateful to the UPE scheme of University Grants Commission, India, and DST Purse for providing funding to the University of Hyderabad.

Funding

The study was funded by UPE-UGC, CSIR, and DST Purse.

Author information

Authors and Affiliations

  1. Centre for Neural and Cognitive Sciences, University of Hyderabad, Gachibowli, Hyderabad, Telangana, 500046, India

    Sandhya Mogily, Meenakshi VijayKumar & Joby Joseph

  2. Bhabha Atomic Research Centre, Mumbai, Maharashtra, 400085, India

    Sunil Kumar Sethy

Authors
  1. Sandhya Mogily
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Meenakshi VijayKumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sunil Kumar Sethy
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Joby Joseph
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joby Joseph.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mogily, S., VijayKumar, M., Sethy, S.K. et al. Characterization of the olfactory system of the giant honey bee, Apis dorsata. Cell Tissue Res 379, 131–145 (2020). https://doi.org/10.1007/s00441-019-03078-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-019-03078-8

Keywords

Search

Navigation