Journal of comparative physiology

, Volume 113, Issue 1, pp 55–72 | Cite as

Insect pupil mechanisms

I. On the pigment migration in the retinula cells of Hymenoptera (suborder Apocrita)
  • D. G. Stavenga
  • J. W. Kuiper


The pupil mechanism of Hymenoptera (suborder Apocrita) has been studied by simultaneous recordings of transmission and reflection from the compound eye of virtually intact animals. It is confirmed that the light flux in the photoreceptors is controlled by pigment granules in the retinula cells; the pigment migration serves a pupil function. Experimental methods are described for investigation of the pupil process using only reflection measurements. Using polarised light, it is found that backscattered light from the rhabdom is more strongly depolarised than light backscattered from retinula cell pigment granules.

The dynamic characteristics of the pigment migration are determined more accurately than could be done previously with histological methods (Menzel, 1972a, b; Kolb and Autrum, 1972, 1974). The hymenopteran pupil mechanism has a familiar sigmoid intensity dependence; the time constant is 5–15 s. The pupil absorbance spectrum is broad, peaking at about 520 nm. The correspondence of this spectrum with known spectral sensitivities exemplifies that the pupil mechanism is a useful part of the visual system.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Autrum, H., Zwehl, V. von: Spektrale Empfindlichkeit einzelner Sehzellen des Bienenauges. Z. vergl. Physiol.48, 357–384 (1964)Google Scholar
  2. Brunnert, A., Wehner, R.: Fine structure of light- and dark adapted eyes of desert ants,Cataglyphis bicolor (Formicidae, Hymenoptera). J. Morph.140, 15–30 (1973)Google Scholar
  3. Butler, R.: The identification and mapping of spectral cell types in the retina ofPeriplaneta americana. Z. vergl. Physiol.72, 67–80 (1971)Google Scholar
  4. Exner, S.: Die Physiologie der facettirten Augen von Krebsen und Insekten. Leipzig und Wien: Franz Deuticke 1891Google Scholar
  5. Franceschini, N.: Sur le traitement optique de l'information visuelle dans l'oeil à facettes de la drosophile. Thesis, Grenoble (1972a)Google Scholar
  6. Franceschini, N.: Pupil and pseudopupil in the compound eye ofDrosophila. In: Information processing in the visual systems of arthropods (Wehner, R., ed.), pp. 75–82. Berlin-Heidelberg-New York: Springer 1972bGoogle Scholar
  7. Franceschini, N.: Sampling of the visual environment by the compound eye of the fly: Fundamentals and applications. In: Photoreceptor optics (A.W. Snyder and R. Menzel, eds.), pp. 98–125. Berlin-Heidelberg-New York: Springer 1975Google Scholar
  8. Franceschini, N., Kirschfeld, K.: Etude optique in vivo des éléments photorécepteurs dans l'oeil composé deDrosophila. Kybernetik8, 1–13 (1971a)Google Scholar
  9. Franceschini, N., Kirschfeld, K.: Les phénomènes de pseudo-pupille dans l'oeil composé deDrosophila. Kybernetik9, 159–182 (1971b)Google Scholar
  10. Franceschini, N., Kirschfeld, K.: Le contrôle automatique du flux lumineux dans l'oeil composé des Diptères. Propriétés spectrales, statiques et dynamiques du mécanisme. Biol. Cybernetics21, 181–203 (1976)Google Scholar
  11. Goldsmith, T.H., Bernard, G.D.: The visual system of insects. In: The physiology of insecta. 2 Ed. (Rockstein, M., ed.), Vol. II, pp. 165–272. New York: Academic Press 1974Google Scholar
  12. Gribakin, F.G.: The distribution of the long wave photoreceptors in the compound eye of the honeybee as revealed by selective osmic staining. Vision Res.12, 1225–1230 (1972)Google Scholar
  13. Gribakin, F.G.: Functional morphology of the compound eye of the bee. In: The compound eye and vision of insects (G.A. Horridge, ed.), pp. 154–176. Oxford: Clarendon Press 1975Google Scholar
  14. Höglund, G., Langer, H., Struwe, G., Thorell, B.: Spectral absorption by screening pigment granules in the compound eyes of a moth and a wasp. Z. vergl. Physiol.67, 238–242 (1970)Google Scholar
  15. Kirschfeld, K.: Projektion der optischen Umwelt auf das Raster der Rhabdomere im Komplexauge vonMusca. Exp. Brain Res.3, 248–270 (1967)Google Scholar
  16. Kirschfeld, K.: Absorption properties of photopigments in single rods, cones and rhabdomeres. In: Processing of optical data by organisms and machines (Reichardt, W., ed.), pp. 116–136. New York-London: Academic Press 1969Google Scholar
  17. Kirschfeld, K.: Optomotorische Reaktionen der Biene auf bewegte „Polarisations-Muster“. Z. Naturforsch.28c, 329–338 (1973)Google Scholar
  18. Kirschfeld, K., Franceschini, N.: Optische Eigenschaften der Ommatidien im Komplexauge vonMusca. Kybernetik5, 47–52 (1968)Google Scholar
  19. Kirschfeld, K., Franceschini, N.: Ein Mechanismus zur Steuerung des Lichtflusses in den Rhabdomeren des Komplexauges vonMusca. Kybernetik6, 13–22 (1969)Google Scholar
  20. Kolb, G., Autrum, H.: Die Feinstruktur im Auge der Biene bei Hell- und Dunkeladaptation. J. comp. Physiol.77, 113–125 (1972)Google Scholar
  21. Kolb, G., Autrum, H.: Selektive Adaptation und Pigmentwanderung in den Sehzellen des Bienenauges. J. comp. Physiol.94, 1–6 (1974)Google Scholar
  22. Kuiper, J.W.: The optics of the compound eye. In: Biological receptor mechanisms (J.W.L. Beament, ed.), pp. 58–71. London: Cambridge University Press 1962Google Scholar
  23. Langer, H.: Properties and functions of screening pigments in insect eyes. In: Photoreceptor optics (A.W. Snyder, R. Menzel, eds.), pp. 429–455. Berlin-Heidelberg-New York: Springer 1975Google Scholar
  24. Mazokhin-Porshnyakow, G.A.: Insect vision. New York: Plenum Press 1969Google Scholar
  25. Menzel, R.: Über den Farbensinn von Paravespula germanica F. (Hymenoptera): ERG und selektive Adaptation. Z. vergl. Physiol.75, 86–104 (1971)Google Scholar
  26. Menzel, R.: Feinstruktur des Komplexauges der Roten WaldameiseFormica polyctena (Hymenoptera, Formicidae). Z. Zellforsch.127, 356–373 (1972a)Google Scholar
  27. Menzel, R.: The fine structure of the compound eye ofFormica polyctena — Functional morphology of a hymenopteran eye. In: Information processing in the visual systems of arthropods (R. Wehner, ed.), pp. 37–47. Berlin-Heidelberg-New York: Springer 1972bGoogle Scholar
  28. Menzel, R., Lange, G.: Änderungen der Feinstruktur im Komplexauge vonFormica polyctena bei der Helladaptation. Z. Naturforsch.26b, 357–359 (1971)Google Scholar
  29. Menzel, R., Knaut, R.: Pigment movement during light and chromatic adaptation in the retinula cells ofFormica polyctena (Hymenoptera, Formicidae). J. comp. Physiol.86, 125–138 (1973)Google Scholar
  30. Perrelet, A.: The fine structure of the honeybee drone. An electron microscopical study. Z. Zellforsch.108, 530–562 (1970)Google Scholar
  31. Snyder, A.W.: Optical properties of invertebrate photoreceptors. In: The compound eye and vision of insects (G.A. Horridge, ed.), pp. 179–235. Oxford: Clarendon Press 1975Google Scholar
  32. Snyder, A.W., Horridge, G.A.: The optical function of changes in the medium surrounding the cockroach rhabdom. J. comp. Physiol.81, 1–8 (1972)Google Scholar
  33. Snyder, A.W., Menzel, R. (eds.): Photoreceptor optics. Berlin-Heidelberg-New York: Springer 1975Google Scholar
  34. Stavenga, D.G.: Adaptation in the compound eye. Proc. Int. Union Physiol. Sc. IX. 532. XXV Int. Congr. Munich (1971)Google Scholar
  35. Stavenga, D.G.: Waveguide modes and refractive index in photoreceptors of invertebrates. Vision Res.15, 323–330 (1975a)Google Scholar
  36. Stavenga, D.G.: Optical qualities of the fly eye — An approach from the side of geometrical, physical and waveguide optics. In: Photoreceptor optics (A.W. Snyder, R. Menzel, eds.), pp. 126–144. Berlin-Heidelberg-New York: Springer 1975bGoogle Scholar
  37. Stavenga, D.G.: Visual adaptation in butterflies. Nature (Lond.)254, 435–437 (1975c)Google Scholar
  38. Stavenga, D.G., Zantema, A., Kuiper, J.W.: Rhodopsin processes and the function of the pupil mechanism in flies. In: Biochemistry and physiology of visual pigments (H. Langer, ed.), pp. 175–180. Berlin-Heidelberg-New York: Springer 1973Google Scholar
  39. Stavenga, D.G., Flokstra, J.H., Kuiper, J.W.: Photopigment conversions expressed in pupil mechanism of blowfly visual sense cells. Nature (Lond.)253, 740–742 (1975)Google Scholar
  40. Stavenga, D.G., Numan, J.A.J., Tinbergen, J., Kuiper, J.W.: Insect pupil mechanisms. II. Pigment migration in retinula cells of butterflies. J. comp. Physiol.113, 73–93 (1977)Google Scholar
  41. Strother, G.K., Casella, A.J.: Microspectrophotometry of arthropod visual screening pigments. J. gen. Physiol.59, 616–636 (1972)Google Scholar
  42. Varela, F.G., Wiitanen, W.: The optics of the compound eye of the honeybee (Apis mellifera). J. gen. Physiol.55, 336–358 (1970)Google Scholar
  43. Vishnevskaya, T.M., Mazokhin-Porshnyakov, G.A.: Spectral sensitivity of single visual cells of the grasshopperTettigonia cantans and the bumblebeeBombus distinguendus. Biophysics17, 635–641 (1972)Google Scholar
  44. Vries, H.L. de: Physical aspects of the sense organs. Progr. Bioph.6, 208–264 (1956)Google Scholar
  45. Walcott, B.: Anatomical changes during light adaptation in insect compound eyes. In: The compound eye and vision of insects (Horridge, G.A., ed.), pp. 20–33. Oxford: Clarendon Press 1975Google Scholar

Copyright information

© Springer-Verlag 1977

Authors and Affiliations

  • D. G. Stavenga
    • 1
  • J. W. Kuiper
    • 1
  1. 1.Biophysical Department, Laboratorium voor Algemene NatuurkundeRijksuniversiteit GroningenGroningenThe Netherlands

Personalised recommendations