Eur. J. Entomol. 106 (4): 619-629, 2009 | DOI: 10.14411/eje.2009.078

The eye of the parthenogenetic and minute moth Ectoedemia argyropeza (Lepidoptera: Nepticulidae)

Anna HONKANEN*,1, Victor Benno MEYER-ROCHOW1,2
1 Department of Biology (Zoological Museum), University of Oulu, SF-90014 Oulu, Finland
2 Faculty of Engineering and Sciences, Jacobs University Bremen, P.O. Box 750561, D-28725 Bremen, Germany; e-mail: vmr@cc.oulu.fi; b.meyer-rochow@jacobs-university.de

Ectoedemia argyropeza (Zeller, 1839) possesses a compound eye that exhibits features of both apposition and superposition type eyes. Like apposition eyes, the eye of E. argyropeza lacks a clear-zone, which in superposition eyes separates the distal dioptric from the proximal light-perceiving structures. On the other hand, a tracheal layer around the proximal ends of the rhabdom as well as a well-developed corneal nipple array on the corneal surfaces are features that E. argyropeza shares with the larger moths. Unique, and so far only seen to this extreme degree in any insect, is the hourglass-shape of E. argyropeza's rhabdom, in which two almost equally voluminous regions (one distal, one proximal and formed in both cases by seven rhabdomeres) are connected by a narrow waist-like region of the retinula. An eighth retinula cell, not participating in rhabdom formation, is developed as a basal cell, just above the basement membrane. The eye responds with photomechanical changes to dark/light adaptation, but while the proximal rhabdom moiety slightly expands (as expected) in the dark, the distal rhabdom increases its diameter only upon light-adaptation. Owing to the tandem position of the two rhabdom moities, it is in the light-adapted state that the distally-placed rhabdom is favoured, while the proximal rhabdom plays a more important role at low ambient light levels. With screening pigments withdrawn, tracheal tapetum exposed, and distal rhabdom diameters reduced, the proximal and in the dark enlarged rhabdom is then in a position to capture photons that have entered the eye through not only the ommatidial window above, but other facets as well even in the absence of a clear-zone and superposition optics.

Keywords: Nepticuloidea, Microlepidoptera, vision, facets, retinal ultrastructure

Received: May 21, 2009; Accepted: July 14, 2009; Published: November 20, 2009

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References

  1. ANTON-ERXLEBEN F. & LANGER H. 1988: Functional morphology of the ommatidia in the compound eye of the moth, Antherea polyphemus (Insecta: Saturniidae). Cell Tiss. Res. 252: 385-396 Go to original source...
  2. AUTRUM H. 1981: Light and dark adaptation in invertebrates. In Autrum H. (ed.): Handbook of Sensory Physiology. Vol. VII/6C. Springer, Berlin, pp. 1-91
  3. BARLOW H.B. 1952: The size of ommatidia in apposition eyes. J. Exp. Biol. 29: 667-674
  4. BERNARD G.D., OWENS E.D. & VOSS-HURLEY A. 1984: Intracellular optical physiology of the eye of the pyralid moth Amyelois. J. Exp. Zool. 229: 173-187 Go to original source...
  5. DEANE C. 1932: New species of Corylophidae. Proc. Linn. Soc. N.S. Wales 57: 336-386
  6. DOVING K.B. & MILLER W.H. 1969: Function of insect compound eyes containing crystalline tracts. J. Gen. Physiol. 54: 250-267 Go to original source...
  7. EGUCHI E. 1982: Retinular fine structure in compound eyes of diurnal and nocturnal shingid moths. Cell Tiss. Res. 223: 29-42 Go to original source...
  8. EXNER S. 1891: Die Physiologie der facettierten Augen von Krebsen und Insekten. Franz Deuticke, Leipzig/Wien
  9. FISCHER A. & HORSTMANN G. 1971: Der Feinbau des Auges der Mehlmotte Ephestia kuehniella Zeller (Lepidoptera, Pyralidae). Z. Zellforsch. 116: 275-304 Go to original source...
  10. FRENCH A.S., SNYDER A.W. & STAVENGA D.G. 1977: Image degradation by an irregular retinal mosaic. Biol. Cybernetics 27: 299-233 Go to original source...
  11. GOKAN N. & MEYER-ROCHOW V.B. 2000: Morphological comparisons of compound eyes in Scarabaeoidea (Coleoptera) related to the beetles' daily activity maxima and phylogenetic positions. J. Agric. Sci. 45: 15-61
  12. GRENACHER H. 1879: Untersuchungen ueber das Sehorgan der Arthropoden insbesondere das der Spinnen, Insekten und Crustaceen. Vandenhoek and Ruprecht, GGttingen
  13. HAMDORF K. 1979: The physiology of invertebrate visual pigments. In Horridge G.A. (ed.): The Compound Eye and Vision in Insects. Clarendon, Oxford, pp. 145-224
  14. HEGEDUS R., HORVATH A. & HORVATH G. 2006: Why do duskactive cockchafers detect polarization in the green? The polarization vision in Melolontha melolontha is tuned to the high polarized intensity of downwelling light under canopies during sunset. J. Theor. Biol. 238: 230-244 Go to original source...
  15. HOGLUND G. 1966: Pigment migration, light screening and receptor sensitivity in the compound eye of nocturnal Lepidoptera. Acta Physiol. Scand. (Suppl. 282) 69: 1-56
  16. HORRIDGE G.A. 1971: Alternatives to superposition images in clear zone compound eyes. Proc R. Soc. Lond. (B) 179: 97-124 Go to original source...
  17. HORRIDGE G.A. 1975: Optical mechanisms of clear-zone eyes. In Horridge G.A. (ed.): The Compound Eye and Vision in Insects. Clarendon, Oxford, pp. 255-298
  18. HORRIDGE G.A. & GIDDINGS C. 1971: The retina of Ephestia (Lepidoptera). Proc. R. Soc. Lond. (B) 179: 87-95 Go to original source...
  19. HORRIDGE G.A., NINHAM B.W., DIESENDORF M. 1972: Theory of the summation of scattered light in clear zone compound eyes. Proc R. Soc. Lond. (B) 181: 137-156 Go to original source...
  20. HORVATH G. 1995: Reflection-polarization patterns at flat water surfaces and their relevance for insect polarization vision. J. Theor. Biol. 175: 27-37 Go to original source...
  21. HORVATH G. & VARJU D. 2004: Polarized Light in Animal Vision - Polarization Patterns in Nature. Springer, Heidelberg, 476 pp
  22. HORVATH G., GAL J., LABHART T. & WEHNER R. 2002: Does reflection polarization by plants influence colour perception in insects? Polarimetric measurements applied to a polarization-sensitive model retina of Papilio butterflies. J. Exp. Biol. 205: 3281-3298
  23. JOHANSSON R., NIELSEN E.S., NIEUKERKEN E.J. VAN & GUSTAFSSON B. 1989: The Nepticulidae and Opostegidae (Lepidoptera) of North West Europe. Fauna Entomol. Scand. 23: 1-739
  24. KIRSCHFELD K. 1972: Die notwendige Anzahl von Rezeptoren zur Bestimmung der Richtung des elektrischen Vektors linear polarisierten Lichtes. Z. Naturforsch. (B) 27: 578-579 Go to original source...
  25. LAND M.F. 1981: Optics and vision in invertebrates. In Autrum H. (ed.): Handbook of Sensory Physiology. Vol. VII/6C. Springer, Berlin, pp. 471-592 Go to original source...
  26. LAU S.T.F. & MEYER-ROCHOW V.B. 2007: The compound eye of Orgya antiqua (Lepidoptera: Lymantriidae): Sexual dimorphism and light/dark adaptational changes. Eur. J. Entomol. 104: 247-258 Go to original source...
  27. LAU S.T.F., GROSS E.M. & MEYER-ROCHOW V.B. 2007: Sexual dimorphism and light/dark adaptation in the compound eyes of male and female Acentria ephemerella (Lepidoptera: Pyraloidea: Crambidae). Eur. J. Entomol. 104: 459-470 Go to original source...
  28. LIU Z., CARPENTER S.B., BOURGEOIS W.J., YING Y., CONSTANTIN R.J., FALCON M.J. & ADAMS J.C. 1998: Variations in the secondary metabolite camptothecin in relation to tissue age and season in Camptotheca acuminate. Tree Physiol. 18: 265-270 Go to original source...
  29. MAZOKHIN-PORSHNYAKOV G.A. 1969: Insect Vision. Plenum, New York, 306 pp
  30. MEINECKE C.C. & LANGER H. 1984: Localization of visual pigments within the rhabdoms of the compound eye of Spodoptera exempta (Insecta, Noctuidae). Cell Tiss. Res. 238: 359-368 Go to original source...
  31. MEYER-ROCHOW V.B. 1975: The dioptric system in beetle compound eyes. In Horridge G.A. (ed.): The Compound Eye and Vision in Insects. Clarendon, Oxford, pp. 299-313
  32. MEYER-ROCHOW V.B. 1999: The compound eye: Circadian rhythmicity, illumination, and obscurity. In Eguchi E. & Tominaga Y. (eds): Atlas of Arthropod Sensory Receptors: Dynamic Morphology in Relation to Function. Springer, Tokyo, pp. 97-124
  33. MEYER-ROCHOW V.B. & GAL J. 2004: Dimensional limits for arthropod eyes with superposition optics. Vision Res. 44: 2213-2233 Go to original source...
  34. MEYER-ROCHOW V.B. & LAU S.T.F. 2008: Sexual dimorphism in the compound eye of the moth Operophtera brumata (Lepidoptera, Geometridae). Invertebr. Biol. 127: 201-216 Go to original source...
  35. MEYER-ROCHOW V.B. & MISHRA M. 2007: Structure and putative function of dark- and light-adapted as well as UV-exposed eyes of the food store pest Psyllipsocus ramburi SelysLongchamps (Insecta; Psocoptera; Psyllipsocidae). J. Insect Physiol. 53: 157-169. Go to original source...
  36. MEYER-ROCHOW V.B. & REID W.A. 1994: Male and female eyes of the Antarctic midge Belgica Antarctica (Dipera: Chironomidae) - a scanning electron microscope study. Appl. Entomol. Zool. 29: 439-442
  37. MEYER-ROCHOW V.B. & STRINGER I.A.N. 1993: A system of regular ridges instead of nipples on a compound eye that has to operate near the diffraction limit. Vision Res. 33: 2645-2647 Go to original source...
  38. MEYER-ROCHOW V.B. & TIANG K.M. 1984: The eye of Jasus edwardsii: electrophysiology, histology, and visual behaviour. Zoologica 45: 1-85
  39. MILLER W.H. 1979: Intraocular filters. In Autrum H. (ed.): Handbook of Sensory Physiology. Vol. VII/6A. Springer, Berlin, pp. 69-143
  40. PALO R.T. 1984: Distribution of birch (Betula spp.), willow (Salix spp.), and poplar (Populus spp.) secondary metabolites and their potential role as chemical defence against herbivores. J. Chem. Ecol. 10: 499-520 Go to original source...
  41. RANTA E., RITA H. & KOUKI J. 2005: Biometria: tilastotiedettae ekologeille. Yliopistopaino, Helsinki, 569 pp
  42. STRUWE G. 1973: Spectral sensitivity of the compound eye in a moth: intra- and extracellular recordings. Acta Physiol. Scand. 87: 63-68 Go to original source...
  43. WARRANT E.J. & MCINTYRE P.D. 1993: Arthropod eye design and the physical limits to spatial resolving power. Progr. Neurobiol. 40: 413-461 Go to original source...
  44. WARRANT E.J. & MCINTYRE P.D. 1996: The visual ecology of papillary action in superposition eyes. J. Comp. Physiol. (A) 178: 75-90 Go to original source...
  45. WELSCH B. 1977: Ultrastruktur und funktionelle Morphologie der Augen des Nachtfalters Deilephila elpenor (Lepidoptera, Sphingidae). Cytobiol. 14: 378-400
  46. YAGI N. & KOYAMA N. 1963: The Compound Eye of Lepidoptera: Approach from Organic Evolution. Shinkyo Press, Tokyo, 319 pp
  47. ZELLER P.C. 1839: Versuch einer naturgemaessen Eintheilung der Schaben. Isis 3: 167-220