The Eye of the Parthenogenetic and Minute Moth Ectoedemia Argyropeza (Lepidoptera: Nepticulidae)

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The Eye of the Parthenogenetic and Minute Moth Ectoedemia Argyropeza (Lepidoptera: Nepticulidae) Eur. J. Entomol. 106: 619–629, 2009 http://www.eje.cz/scripts/viewabstract.php?abstract=1496 ISSN 1210-5759 (print), 1802-8829 (online) The eye of the parthenogenetic and minute moth Ectoedemia argyropeza (Lepidoptera: Nepticulidae) ANNA HONKANEN1* and VICTOR BENNO MEYER-ROCHOW1,2 1Department of Biology (Zoological Museum), University of Oulu, SF-90014 Oulu, Finland 2Faculty of Engineering and Sciences, Jacobs University Bremen, P.O. Box 750561, D-28725 Bremen, Germany; e-mail: [email protected]; [email protected] Key words. Nepticuloidea, Microlepidoptera, vision, facets, retinal ultrastructure Abstract. Ectoedemia argyropeza (Zeller, 1839) possesses a compound eye that exhibits features of both apposition and superposi- tion 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 With screening pigments withdrawn, tracheal tapetum exposed, and distal rhabdom diameters reduced, the proximal and in the dark enlarged rhabdom is then in a position to capture photons that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. INTRODUCTION 1963; Døving & Miller, 1969; Horridge, 1971; Gokan & Ectoedemia argyropeza (Zeller, 1839) is an all-female, Meyer-Rochow, 2000). parthenogenetic species of moth (Fig. 1), whose com- For scarab beetles and moths the clear-zone eye is a pound eyes (because of E. argyropeza’s phylogenetic characteristic feature. Yet, Meyer-Rochow & Gál (2004) position as part of the Neolepidoptera) are expected to be on the basis of careful calculations, concluded that a com- of the clear-zone kind (Yagi & Koyama, 1963). The pres- pound eye had to reach a certain size before the clear- ence of a pigment-free zone between, on the one hand, zone in concert with the optics of the dioptric structures the distal dioptric structures of the eye like corneae and could lead to an improvement of overall sensitivity. So cones and, on the other, the proximal light-perceiving ele- far support for this conclusion has come only from spe- ments of the retina like rhabdoms and retinula cells, is cies of scarab beetles with small body sizes and small one essential requirement for superposition vision to eyes (Gokan & Meyer-Rochow, 2000). Caught in the occur (Land, 1981). The other requirement is the ability constraints of their phylogenetic background, these bee- of the optics of a wide patch of facets to focus a parallel tles had found ways of ‘re-constructing’ their eyes and beam of incoming light rays onto one small spot on the changing the clear-zone anatomies of their ancestors into retina (Land, 1981; Warrant & McIntyre, 1993). For this something more akin to the apposition eye. The clear- latter purpose mirror optics are employed by some zones were reduced or absent and radial gradients of decapod crustaceans, but lens cylinders with a radial gra- optical densities in cornea and cone unnecessary. The dient of refractive index are the rule in insects (Land, small species of scarabs had apparently found a way to 1981). Vision with superposition optics is particularly abandon superposition as their eyes would not have had useful for species in which the objective is not simply to sufficient space to allow clear-zones to become effective increase sensitivity to light, but to retain a certain amount in focusing light rays entering the eye through multiple of resolving power (Warrant & McIntyre, 1996). Thus, it facets. is not surprising to find compound eyes with large clear- However, although small scarab beetles have found a zones mainly in species of insects that are nocturnal fliers. way to cope with their phylogenetic legacy of superposi- For some insect taxa the presence of a clear-zone can be tion vision, ways other than those exhibited by the afore- said to be “diagnostic” (Exner, 1891; Yagi & Koyama, mentioned beetles are theoretically possible (Horridge, 1971). Towards this end, we decided to examine the eyes * Present address: Department of Physics, Division of Biophysics, University of Oulu, P.O. Box 3000, SF-90014 Oulu, Finland. 619 Fig. 1. Dorsal view of a museum specimen of a female Ectoedemia argyropeza. The orange scales on the head are brighter in living specimens. Scale bar: 2 mm (Photo: Marko Mutanen). of E. argyropeza, for body length in this species of moth For this research cocoons were collected in October by Dr. is rarely little more than 2 mm and, thus, superposition Marko Mutanen from aspen leaves in Taalintehdas (60°1.2´N; vision with the help of a clear-zone, according to Meyer- 22°30.7´E) and kept outdoors under a cover of snow until 10 th Rochow & Gál (2004) ought to be impossible given an of January, when they were brought indoors into an environ- ment of 20°C. Dozens of imagines appeared over a period of isometric reduction of eye size. Still, being a flying insect, about 10 days a few days later. That E. argyropeza is not always E. argyropeza must, of course, be able to avoid obstacles, that easy to obtain demonstrated our collections carried out the to locate a suitable landing place, to perceive the same way as before, but a year later. Only two individuals approach of danger, and to detect ambient brightness hatched from a large amount of pupae. fluctuations. In all of these tasks some photoreceptive Scanning and transmission electron microscopy abilities would clearly be advantageous, which is pre- For observations of the eye by scanning electron microscopy sumably why E. argyropeza individuals possess eyes at air-dried specimens were used. An Agar High-Resolution all. Sputter Coater (Agar Scientific Ltd, Stanstedt, England) was The principal objective of this research was, therefore, used to deposit an approximately 20 nm thick gold-palladium to examine the structure and ultrastructure of the eye of E. layer over the specimen, which was then examined under a Jeol argyropeza and to put on record how the eye differed JSM-6300F Field Emission Scanning Electron Microscope from that of larger moths. Secondly, in order to provide under a slow-scan digital image recording system. some evidence that the eye was responding to changes in For histological studies severed heads were pre-fixed in 0.1 M ambient light levels we conducted dark/light adaptation phosphate-buffered (pH 7.3) 1% glutaraldehyde solution plus experiments, for photomechanical changes are known to 4% formaldehyde for 21 days. Thereafter the specimens were take place in many insect eyes when the latter are exposed postfixed in 1% osmiumtetroxide for one hour, dehydrated in a graded series of acetone and embedded in Epon LX 112 (Ladd to darkness or a bright environment (Autrum, 1981; Research Industries, Vermont, USA) at a temperature of around Meyer-Rochow, 1999). 65°C for two to three days. MATERIAL AND METHODS Nighttime dark-adapted specimens were kept in an opaque black tube for two hours (19.30–21.30 h) prior to being killed Animals with chloroform and having their heads fixed in pre-fixative Ectoedemia argyropeza (Zeller, 1839) is a non-ditrysian moth (see above), while daytime, light-adapted specimens were with leaf-mining larvae that belongs to the family Nepticulidae. exposed to the light of a fluorescent lamp between 10.15 and It is widely distributed south of the polar circle throughout 12.15 h, because daytime weather conditions in January, due to Europe, excluding the Iberian Peninsula, southern Italy and the the winter season, provided only dim light from a cloudy sky. Balkans (Johansson et al., 1989). In Finland it is a univoltine, Semithin sections for light microscopy were cut with glass parthenogenetic species found as far north as Rovaniemi, knives on a Reichert-Jung Ultracut E microtome. Microscope achieving wing spans of 5.0–7.0 mm and reaching a body length slides were coated with 1:1 chrome gelatin (1% gelatin plus of 2 mm or little more (Fig. 1). The host plant of E. argyropeza 0.1% chrome) and the semi-thin sections were stained with a is aspen (Populus tremula). Pupae, attached to aspen leaves, drop of aqueous Toluidine Blue for a few seconds. Ultrathin overwinter among aspen leaf debris and hatch in Finland sections were cut with diamond knives, picked up on 100 mesh between 10 June and 15 July following a winter with at least pioloform-coated copper grids, and stained for 30 and 5 min some frosty nights. The life span of an adult is approximately with uranyl acetate and lead citrate, respectively. Observations one week.
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