Eur. J. Entomol. 104 (2): 247-258, 2007 | DOI: 10.14411/eje.2007.039

The compound eye of Orgyia antiqua (Lepidoptera: Lymantriidae): Sexual dimorphism and light/dark adaptational changes

Ting Fan (Stanley) LAU1, Victor Benno MEYER-ROCHOW1,2
1 Faculty of Engineering and Sciences, Jacobs University Bremen, P.O. Box 750561, D-28725 Bremen, Germany
2 Department of Biology (Zoological Museum), University of Oulu, P.O. Box 3000, SF-90014 Oulu, Finland; e-mail: vmr@cc.oulu.fi and b.meyer-rochow@iu-bremen.de

Structure and photomechanical changes upon light/dark adaptation in the superposition compound eyes of the highly sexually dimorphic Orygia antiqua were studied by light and electron microscopy. The eyes of the fully winged male differ from those of the wingless, sedentary female in several respects: they are significantly larger, display a more regular ommatidial array, have a wider clearzone and possess a much more substantial tracheal tapetum. However, the eyes of the female exhibit more pronounced photomechanical changes upon light/dark adaptation than those of the male. We believe that for females, on account of their limited mobility, it is necessary that their eyes can cope with widely fluctuating brightnesses, but that visual sensitivity and resolving power are less important to them than to the actively flying males. Although the latter may be attracted to the females by pheromones, males in their diurnal searches will have to visually avoid obstacles and predators. Moreover, because of their ability to fly, males can seek shelters or shaded areas and unlike the sedentary females avoid prolonged exposures to potentially hazardous light levels. This could explain why the eyes of the females exhibit more pronounced photomechanical responses to changes in ambient light levels.

Keywords: Lymantriidae, vision, retinal ultrastructure, photic environment, visual behaviour

Received: September 11, 2006; Accepted: November 16, 2006; Published: April 25, 2007Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
LAU, T.F.(., & MEYER-ROCHOW, V.B. (2007). The compound eye of Orgyia antiqua (Lepidoptera: Lymantriidae): Sexual dimorphism and light/dark adaptational changes. Eur. J. Entomol.104(2), 247-258. doi: 10.14411/eje.2007.039.
Download citation

References

  1. ANTON-ERXLEBEN F. & LANGER H. 1988: Functional morphology of the ommatidia in the compound eye of the moth, Antheraea polyphemus (Insecta: Saturniidae). Cell Tissue Res. 252: 385-396 Go to original source...
  2. ARIKAWA K. 2003: Spectral organization of the eye of a butterfly, Papilio. J. Comp. Physiol. (A) 189: 791-800. Go to original source...
  3. ARIKAWA K., KAWAMATA K., SUZUKI T. & EGUCHI E. 1987: Daily changes of structure, function and rhodopsin content in the compound eye of the crab, Hemigrapsus sanguineus. J. Comp. Physiol. (A) 161: 161-174 Go to original source...
  4. ARIKAWA K., WAKAKUWA M., QIU X., KURASAWA M. & STAVENGA D.G. 2005: Sexual dimorphism of short-wavelength photoreceptors in the small white butterfly, Pieris rapae crucivora. J. Neurosci. 25: 5935-5942 Go to original source...
  5. AUTRUM H. 1981: Light and dark adaptation in invertebrate. In Autrum H. (ed.): Handbook of Sensory Physiology. Vol. VII/6C. Springer, Berlin, pp. 1-91
  6. BAKER G.T. 1990: Morphology of eyes and sensory receptors of larval and adult stages of Thyidopteryx ephemeraeformis Haworth (Lepidoptera: Psychidae). Mississippi Agric. Forest Exp. Sta. 170: 1- 11
  7. BERNARD G.D. & REMINGTON C.L. 1991: Color vision in Lycaena butterflies: Spectral tuning of receptor arrays in relation to behavioural ecology. Proc. Natl. Acad. Sci. 88: 2783-2787 Go to original source...
  8. CHAMBERLAIN S.C. & BARLOW R.B. 1984: Transient membrane shedding in Limulus photoreceptors: Mechanisms under natural lighting. J. Neurol. Sci. 11: 2792-2810
  9. CLEARY P., DEICHSEL G. & KUNZE P. 1977: The superposition image in the eye of Ephestia kuehniella. J. Comp. Physiol. 119: 73-84 Go to original source...
  10. COLLETT T.S. & LAND M.F. 1975: Visual control of flight behaviour in the hoverfly, Syritta pipiens L. J. Comp. Physiol. 99: 1-66 Go to original source...
  11. EGUCHI E. 1978: Comparative fine structure of Lepidopteran compound eyes, especially Skippers (Hesperioidea). Zool. Mag. 87: 32-43
  12. EGUCHI E. 1982: Retinula fine structure in compound eyes of diurnal and nocturnal sphingid moths. Cell Tissue Res. 223: 29-42 Go to original source...
  13. EISNER T., SILBERGLIED R.E., ANESHANSLEY D., CARREL J.E. & HOWLAND H.C. 1969: Ultraviolet video-viewing: The television camera as an insect eye. Science 166: 1172-1174 Go to original source...
  14. ESPERK T. & TAMMARU T. 2006: Determination of female-biased sexual size dimorphism in moths with a variable instar number: The role of additional instars. Eur. J. Entomol. 103: 575-586 Go to original source...
  15. FISCHER A. & HORSTMANN G. 1971: Der feinbau des augen der mehlmotte, Ephestia kuehniella zeller (Lepidoptera: Pyralididae). Z. Zellforsch. 116: 275-304 Go to original source...
  16. 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...
  17. GOKAN N. & MEYER-ROCHOW V.B. 2000: Morphological comparisons of compound eyes in Scarabaeoidae (Coleoptera) related to the beetle's daily activity maxima and phylogenetic positions. J. Agric. Sci. 45(1): 15-61
  18. GRANT G.G. & FRECH D. 1980: Disruption of pheromone communication of the rusty tussock moth, Orgyia antiqua (Lepidoptera: Lymantriidae), with (Z)-6-heneicosen-11-one. Can. Entomol. 112: 221-222 Go to original source...
  19. GUNTER E. 1994: Die Schmetterlinge Baden-Wuerttembergs, Bd. 4 Nachtfalter II. Eugen Ulmer, Stuttgart, 535 pp
  20. HACKMAN W. 1966: On wing reduction and loss of wings in Lepidoptera. Notul. Entomol. 46: 1-16
  21. HEPPNER J.B. 1991: Brachyptery and aptery in Lepidoptera. Trop. Lepid. 2: 11-40
  22. HORNSTEIN E.P., O'CARROLL D.C., ANDERSON J.C. & LAUGHLIN S.B. 2000: Sexual dimorphism matches photoreceptor performance to behavioural requirements. Proc. R. Soc. Lond. (B) 267: 2111-2117 Go to original source...
  23. HORRIDGE G.A. & GIDDINGS C. 1971: The retina of Ephestia (Lepidoptera). Proc. R. Soc. Lond. (B) 179: 87-95 Go to original source...
  24. HORRIDGE G.A., GIDDINGS C. & STANGE G. 1972: The superposition eye of skipper butterflies. Proc. R. Soc. Lond. (B) 182: 457-495 Go to original source...
  25. HORRIDGE G.A., MCLEAN M., STANGE G. & LILLYWHITE P.G. 1977: A diurnal moth superposition eye with high resolution Phalaenoides tristifica (Agaristidae). Proc. R. Soc. Lond. (B) 196: 233-250 Go to original source...
  26. IMAFUKU M., HIROSE Y. & TAKEUCHI T. 2002: Wing colors of Chrysozephyrus butterflies (Lepidoptera: Lycaenidae): Ultraviolet reflection by males. Zool. Sci. 19: 175-183 Go to original source...
  27. KUNZE P. 1979: Apposition and Superposition eyes. In Autrum H. (ed.): Handbook of Sensory Physiology. Vol. VII/6A. Springer, Berlin, Heidelberg, NewYork, pp. 441-502
  28. LABHART T. & MEYER P.E. 1999: Detectors for polarized skylight in insects: A survey of ommatidial specializations in the dorsal rim area of the compound eye. Microsc. Res. Tech. 47: 368-379 Go to original source...
  29. LAND M.F. 1981: Optics and visions in invertebrates. In Autrum H. (ed.): Handbook of Sensory Physiology. Vol. VII/6B. Springer, Berlin, Heidelberg, NewYork, pp. 471-592
  30. LAND M.F. 1989: Variations in the structure and design of compound eyes. In Stavenga D.G. & Hardie R.C. (eds): Facets of Vision. Springer, Berlin, Heidelberg, pp. 90-111
  31. LAND M.F. & ECKERT H. 1985: Maps of the acute zones of fly eyes. J. Comp. Physiol. (A) 156: 525-538 Go to original source...
  32. LAND M.F., GIBSON G., HORWOOD J. & ZEIL J. 1999: Fundamental differences in the optical structure of the eyes of nocturnal and diurnal mosquitoes. J. Comp. Physiol. (A) 185: 91-103 Go to original source...
  33. LAU S.T.F. & MEYER-ROCHOW V.B. 2006: Sexual dimorphism in the compound eye of Rhagophthalmus ohbai (Coleoptera: Rhagophthalmidae). J. Asia-Pac. Entomol. 9: 1-12
  34. LAUGHLIN S.B. & HORRIDGE G.A. 1971: Angular sensitivity of retinula cells of dark-adapted worker bee. Z. Vergl. Physiol. 74: 329- 335 Go to original source...
  35. LAUGHLIN S.B. & MCGINNESS S. 1978: The structures of dorsal and ventral regions of a Dragonfly retina. Cell Tissue Res. 188: 427-447 Go to original source...
  36. LAUGHLIN S.B. & WECKSTROM M. 1993: Fast and slow photoreceptors - a comparative study of the functional diversity of coding and conductances in the Diptera. J. Comp. Physiol. (A) 172: 593-609 Go to original source...
  37. MCINTYRE P. & CAVENEY S. 1998: Superposition optics and the time of flight in onitine dung bettles. J. Comp. Physiol. (A) 183: 45-60 Go to original source...
  38. MEINECKE C.C. 1981: The fine structure of the compound eye of the african armyworm moth, Spodoptera exempta Walk. (Lepidoptera: Noctuidae). Cell Tissue Res. 216: 333-347 Go to original source...
  39. MERRY J.W., MOREHOUSE N.I., YTURRALDE K. & RUTOWSKI R.L. 2006: The eye of a patrolling butterfly: Visual field and eye structure in the orange sulphur, Colias eurytheme (Lepidoptera: Pieridae). J. Insect Physiol. 52: 240-248 Go to original source...
  40. MEYER-ROCHOW V.B. 1981: Electrophysiology and histology of the eye of the bumblebee Bombus hortorum (L.) (Hymenoptera: Apidae). J. R. Soc. New Zealand 11: 123-153 Go to original source...
  41. MEYER-ROCHOW V.B. 1991: Differences in ultraviolet wing patterns in the New Zealand lycaenid butterflies, Lycaena salustius, L. rauparaha, and L. feredayi as a likely isolating mechanism. J. R. Soc. New. Zealand. 21: 169-177 Go to original source...
  42. MEYER-ROCHOW V.B. 1999: 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.
  43. MEYER-ROCHOW V.B. & GAL J. 2004: Dimensional limits for arthropod eyes with superposition optics. Vision Res. 44: 2213-2223 Go to original source...
  44. MEYER-ROCHOW V.B. & WALSH S. 1978: The eyes of mesopelagic crustaceans: III. Thysanopoda tricupidata (Euphausiacea). Cell Tissue Res. 195: 59-79 Go to original source...
  45. MILLER W.H. 1979: Ocular optical filtering. In Autrum H. (ed.): Handbook of Sensory Physiology. Vol. VII/6A. Springer, Berlin, Heidelberg, NewYork, pp. 69-143
  46. NASSEL D.R. & WATERMAN T.H. 1979: Massive diurnally modulated photoreceptor membrane turnover in crab light and dark adaptation. J. Comp. Physiol. 131: 205-216 Go to original source...
  47. NARVARRO R. & FRANCESCHINI N. 1998: On image quality of microlens arrays in diurnal superposition eyes. Pure. Appl. Opt. 7: L69-L78 Go to original source...
  48. OBARA Y. 1970: Studies on the mating behaviors of the white cabbage butterfly, Pieris rapae crucivora Boisduval III. Nearultra-violet reflection as the signal of intraspecific communication. Z. Vergl. Physiol. 69: 99-116 Go to original source...
  49. PINDER P.S. & HAYES A.J. 1986: An outbreak of vapourer moth, Orgyia antiqua L. (Lepidoptera: Lymantridae) on Sitka spruce (Picea sitchensis (Bong.) Carr.) in central Scotland. Forestry 59(1): 97-105 Go to original source...
  50. QIU X. & ARIKAWA K. 2003: The photoreceptor localization confirms the spectral heterogeneity of ommatidia in the male small white butterfly, Pieris rapae crucivora. J. Comp. Physiol. (A) 189: 81-88
  51. ROSENBERG J. & LANGER H. 2001: Ultrastructural changes of rhabdoms of the eyes of Ocypode species in relation to different regimes of light and dark adaptation. J. Crust. Biol. 21: 345-353 Go to original source...
  52. ROBERTSON K.A. & MONTEIRO A. 2005: Female Bicyclus anynana butterflies choose males on the basis of their dorsal UVreflective eyespot pupils. Proc. R. Soc. (B) 272: 1541-1546 Go to original source...
  53. RUTOWSKI R.L. 1977: The use of visual cues in sexual and species discrimination by males of the small sulphur butterfly, Eurema lisa (Lepidoptera: Pieridae). J. Comp. Physiol. 115: 61-74 Go to original source...
  54. RUTOWSKI R.L. 2000: Variation of eye size in butterflies: interand intraspecific patterns. J. Zool. Lond. 252: 187-195 Go to original source...
  55. RUTOWSKI R.L. & WARRANT E.J. 2002: Visual field structure in the Empress Leilia, Asterocampa leilia (Lepidoptera: Nymphalidae): dimensions and regional variation in acuity. J. Comp. Physiol. (A) 188: 1-12 Go to original source...
  56. SAKURA M., TAKASUGA K., WATANABE M. & EGUCHI E. 2003: Diurnal and circadian rhythm in compound eye of cricket (Gryllus bimaculatus): Changes in structure and photo capture efficiency. Zool. Sci. 20: 833-840 Go to original source...
  57. SCHLECHT P., HAMDORF K. & LANGER H. 1978: The arrangement of colour receptors in a fused rhabdom of an insect. A Microspectrophotometric study of the moth Deilephila. J. Comp. Physiol. 123: 239-243 Go to original source...
  58. SHIMOHIGASHI M. & TOMINAGA Y. 1986: The compound eye of Parnara guttata (Insecta: Lepidoptera: Hesperiidae): Fine structure of the ommatidium. Zoomorphol. 106: 131-136 Go to original source...
  59. STAVENGA D.G., KINOSHITA M. & YANG E.C. 2001: Retinal regionalization and heterogeneity of butterfly eyes. Naturwissenschaften 88: 477-481 Go to original source...
  60. SVERSSON M. 1996: Sexual selection in moths: the role of chemical communication. Biol. Rev. 71: 113-135 Go to original source...
  61. TAMMARU T. & HAUKIOJA E. 1996: Captial breeders and income breeders among Lepidoptera-consequences to population dynamics. Oikos 77: 561-564 Go to original source...
  62. TAMMARU T., ESPERK T. & CASTELLANOS I. 2002: No evidence for costs of being large in females of Orgyia spp. (Lepidoptera: Lymantriidae): larger is always better. Oecologia 133: 430-438 Go to original source...
  63. TUNG L.C. & LIN J.T. 2000: Morphology of the compound eye of hevea tussock moth, Orgyia postica (Lepidoptera: Lymantridae). Chin. J. Entomol. 20: 179-185 [in Chinese, English abstr.]
  64. VILORIA A.L., PYRCZ T.W., WOJTUSIAK J., FERRER-PARIS J.R., BECCALONI G.W., SATTLER K. & LEES D.C. 2003: A brachypterous butterfly? Proc. R. Soc. Lond. (B) (Suppl.) 270: S21-S24 Go to original source...
  65. WARRANT E.J. & MCINTYRE P.D. 1990: Limitations to resolution in superposition eyes. J. Comp. Physiol. (A) 167: 785-803 Go to original source...
  66. WARRANT E.J. & MCINTYRE P.D. 1991: Strategies for retinal design in arthropod eyes of low F-number. J. Comp. Physiol. (A) 168: 499-512 Go to original source...
  67. WARRANT E., BARTSCH K. & GUNTHER C. 1999: Physiological optics in the hummingbird hawkmoth: A compound eye without ommatidia. J. Exp. Biol. 202: 497-511
  68. WILLIAMS D.S. 1982: Ommatidial structure in relation to turnover of photoreceptor membrane in the locust. Cell Tissue Res. 225: 595-617 Go to original source...
  69. YAGI N. & KOYAMA N. 1963: The Compound Eye of Lepidoptera: Approach from Organic Evolution. Shinkyo Press, Tokyo, 318 pp
  70. ZIEMBA K.S. & RUTOWSKI R.L. 2000: Sexual dimorphism in eye morphology in a butterfly, Astercampa leilia (Lepidoptera: Nymphalidae). Psyche 103: 25-36 Go to original source...