Skip to main content
SpringerLink
Log in

Spectral heterogeneity of honeybee ommatidia

  • Short Communication
  • Published:
Naturwissenschaften Aims and scope Submit manuscript

Abstract

The honeybee compound eye is equipped with ultraviolet, blue, and green receptors, which form the physiological basis of a trichromatic color vision system. We studied the distribution of the spectral receptors by localizing the three mRNAs encoding the opsins of the ultraviolet-, blue- and green-absorbing visual pigments. The expression patterns of the three opsin mRNAs demonstrated that three distinct types ommatidia exist, refuting the common assumption that the ommatidia composing the bee compound eye contain identical sets of spectral receptors. We found that type I ommatidia contain one ultraviolet and one blue receptor, type II ommatidia contain two ultraviolet receptors, and type III ommatidia have two blue receptors. All the three ommatidial types contain six green receptors. The ommatidia appear to be distributed rather randomly over the retina. The ratio of type I, II, and III ommatidia was about 44:46:10. Type III ommatidia appeared to be slightly more frequent (18%) in the anterior part of the ventral region of the eye. Retinal heterogeneity and ommatidial randomness, first clearly demonstrated in butterflies, seems to be a common design principle of the eyes of insects.

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.

Fig. 1
Fig. 2

References

  • Arikawa K (2003) Spectral organization of the eye of a butterfly Papilio. J Comp Physiol A 189:791–800

    Article  CAS  Google Scholar 

  • Arikawa K, Mizuno S, Kinoshita M, Stavenga DG (2003) Coexpression of two visual pigments in a photoreceptor causes an abnormally broad spectral sensitivity in the eye of a butterfly, Papilio xuthus. J Neurosci 23:4527–4532

    PubMed  CAS  Google Scholar 

  • Arikawa K, Stavenga DG (1997) Random array of colour filters in the eyes of butterflies. J Exp Biol 200:2501–2506

    PubMed  Google Scholar 

  • Briscoe AD, Bernard GD, Szeto AS, Nagy LM, White RH (2003) Not all butterfly eyes are created equal: rhodopsin absorption spectra, molecular identification and localization of UV- blue- and green-sensitive rhodopsin encoding mRNA in the retina of Vanessa cardui. J Comp Neurol 458:334–349

    Article  PubMed  CAS  Google Scholar 

  • Chang BS, Ayers D, Smith WC, Pierce NE (1996) Cloning of the gene encoding honeybee long-wavelength rhodopsin: a new class of insect visual pigments. Gene 173:215–219

    Article  PubMed  CAS  Google Scholar 

  • Frisch Kv (1914) Der Farbensinn und Formensinn der Biene. Zool J Physiol 37:1–238

    Google Scholar 

  • Giurfa M, Vorobyev M, Brandt R, Posner B, Menzel R (1997) Discrimination of coloured stimuli by honeybees: Alternative use of achromatic and chromatic signals. J Comp Physiol A 180:235–243

    Article  Google Scholar 

  • Giurfa M, Zaccardi G, Vorobyev M (1999) How bees detect coloured targets using different regions of their compound eyes. J Comp Physiol A 185:591–600

    Article  Google Scholar 

  • Gribakin FG (1975) Functional morphology of the compound eye of the bee. In: Horridge GA (ed) The compound eye and vision of insects. Clarendon Press, Oxford, pp 154–176

    Google Scholar 

  • Hardie RC (1986) The photoreceptor array of the dipteran retina. Trends Neurosci 9:419–423

    Article  Google Scholar 

  • Hausen K, Egelhaaf M (1989) Neural mechanisms of visual course control in insects. In: Stavenga DG, Hardie RC (eds) Facets of vision. Springer-Verlag, Berlin Heidelberg New York, London, Paris, Tokyo, pp 391–424

    Google Scholar 

  • Kaiser W, Liske E (1974) Die optomotorische Reaktionen von fixiert fliegenden Bienen bei Reizung mit Spektrallichtern. J Comp Physiol 89:391–408

    Article  Google Scholar 

  • Land MF, Nilsson D-E (2002) Animal eyes. Oxford University Press, Oxford

    Google Scholar 

  • Lehrer M (1999) Dorsoventral asymmetry of colour discrimination in bees. J Comp Physiol A 184:195–206

    Article  Google Scholar 

  • Menzel R, Backhaus W (1991) Color vision in insects. In: Gouras P (ed) Vision and visual dysfunction the perception of color. Macmillan, London, pp 262–288

    Google Scholar 

  • Menzel R, Blakers M (1976) Colour receptors in the bee eye - Morphology and spectral sensitivity. J Comp Physiol 108:11–33

    Article  Google Scholar 

  • Menzel R, Lieke E (1983) Antagonistic color effects in spatial vision of honeybees. J Comp Physiol A 151:441–448

    Article  Google Scholar 

  • Menzel R, Snyder AW (1974) Polarised light detection in the bee, Apis mellifera. J Comp Physiol A 88:247–270

    Article  Google Scholar 

  • Qiu X, Vanhoutte KAJ, Stavenga DG, Arikawa K (2002) Ommatidial heterogeneity in the compound eye of the male small white butterfly, Pieris rapae crucivora. Cell Tissue Res 307:371–379

    Article  PubMed  Google Scholar 

  • Ribi WA (1978) A unique hymenopteran compound eye. The retina fine structure of the digger wasp Sphex cognatus Smith (Hymenoptera, Sphecidae). Zool Jb Anat Bd 100:299–342

    Google Scholar 

  • Sauman I, Briscoe AD, Zhu H, Shi D, Froy O, Stalleicken J, Yuan Q, Casselman A, Reppert SM (2005) Connecting the navigational clock to sun compass input in monarch butterfly brain. Neuron 46:457–467

    Article  PubMed  CAS  Google Scholar 

  • Schwind R, Schlecht P, Langer H (1984) Microspectrophotometric characterization and localization of three visual pigments in the compound eye of Notonecta glauca L. (Heteroptera). J Comp Physiol A 116:183–207

    Google Scholar 

  • Spaethe J, Briscoe AD (2005) Molecular chracterization and expression of the UV opsin in bumblebees: three ommatidial subtypes in the retina and a new photoreceptor organ in the lamina. J Exp Biol 208:2347–2361

    Article  PubMed  CAS  Google Scholar 

  • Stavenga DG (2002) Reflections on colourful ommatidia of butterfly eyes. J Exp Biol 205:1077–1085

    PubMed  Google Scholar 

  • Townson SM, Chang BSW, Salcedo E, Chadwell LV, Pierce NE, Britt SG (1998) Honeybee blue-and ultraviolet-sensitive opsins: cloning, heterologous expression in Drosophila, and physiological characterization. J Neurosci 18:2412–2422

    PubMed  CAS  Google Scholar 

  • Wakakuwa M, Stavenga DG, Kurasawa M, Arikawa K (2004) A unique visual pigment expressed in green, red and deep-red receptors in the eye of the small white butterfly, Pieris rapae crucivora. J Exp Biol 207:2803–2810

    Article  PubMed  CAS  Google Scholar 

  • Waterman TH (1981) Polarization sensitivity. In: Autrum H (ed) Handbook of sensory physiology VII/6B. Springer-Verlag, Berlin Heidelberg New York, pp 281–469

    Google Scholar 

  • Wehner R, Rossel S (1985) The bee's celestial compass—A case study in behavioral neurobiology. In: Hoelldobler B, Lindauer M (eds) Experimental behavioral ecology and sociobiology. Fischer, Stuttgart New York, pp 11–53

    Google Scholar 

  • White RH, Xu H, Munch T, Bennett RR, Grable EA (2003) The retina of Manduca sexta: rhodopsin-expression, the mosaic of green-, blue-, and UV-sensitive photoreceptors and regional specialization. J Exp Biol 206:3337–3348

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgement

We thank Dr. D.G. Stavenga for critical comments. Dr. T Kubo from the University of Tokyo, provided some honeybee samples. The work was supported by the Grants-in Aid for Scientific Research from the JSPS (Japan Society for the Promotion of Science) and the Grant for Promotion of Science from Yokohama City University to which Kentaro Arikawa belongs. Martin Giurfa was supported by the University Paul Sabatier (ATUPS fellowship), Yokohama City University and the CNRS (Center de la recherche scientific).

Author information

Authors and Affiliations

  1. Graduate School of Integrated Science, Yokohama City University, 22-2 Seto, Kanazawa-ku, Yokohama, 236-0027, Japan

    Motohiro Wakakuwa, Masumi Kurasawa & Kentaro Arikawa

  2. Centre de Recherches sur la Cognition Animale, CNRS-Université Paul-Sabatier (UMR 5169), 118 route de Narbonne, 31062, Toulouse cedex 4, France

    Martin Giurfa

Authors
  1. Motohiro Wakakuwa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Masumi Kurasawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Martin Giurfa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kentaro Arikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kentaro Arikawa.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wakakuwa, M., Kurasawa, M., Giurfa, M. et al. Spectral heterogeneity of honeybee ommatidia. Naturwissenschaften 92, 464–467 (2005). https://doi.org/10.1007/s00114-005-0018-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-005-0018-5

Keywords

Search

Navigation