Appl. Entomol. Zool. 38 (3): 281ミ291 (2003)

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Appl. Entomol. Zool. 38 (3): 281ミ291 (2003) Appl. Entomol. Zool. 38 (3): 281–291 (2003) Post-embryonic photoreceptor development and dark/light adaptation in the stick insect Carausius morosus (Phasmida, Phasmatidae) V. Benno MEYER-ROCHOW1,* and Essi KESKINEN2 1 School of Engineering and Science, International University Bremen (IUB); D-28725 Bremen, Germany 2 Department of Biology, University of Oulu; P.O. Box 3000, SF-90014 Oulu, Finland (Received 28 October 2002; Accepted 7 March 2003) Abstract The aims of this paper have been (a) to document postembryonic eye growth in the common laboratory stick insect Carausius morosus and (b) to examine whether the capacity of the eye to adapt to changing light intensities varied with age. We found that number of facets, corneal thickness, ommatidial diameter, widths of cone and retinal layers, and rhabdom volume increased linearly. Interommatidial angles, pigment grain sizes, and microvillar diameters, how- ever, remained approximately the same. On the basis of the morphometric data we calculated that sensitivity in the adult stick insect eye was at least tenfold that of the eye of first instar nymphs and could show that adults would be able to perceive a similar amount of detail at considerably dimmer ambient light than the smaller individuals. In terms of resolving power this means that light- and dark-adapted first instar stick insects possess acceptance angles of 5.3° and 8°, respectively and that the corresponding figures for the adult eye are 4.7° and 7.3°. The bigger (and more light- sensitive) eye of fully grown C. morosus makes protection against radiation damage a more serious issue in the adult individual than the small first instar. The findings explain why smaller (5younger) stick insects are less nocturnal than mature, fully-grown individuals. It is, thus, not surprising to see that dark/light adaptational photomechanical changes affecting pigment position and rhabdom widths, are more pronounced in the eyes of the adults. Key words: Vision; compound eye; growth; optics; visual behaviour down position. Observations like these, supple- INTRODUCTION mented by electroretinogramme (ERG) recordings With the exception of the extreme northern and from the surface of the eye (Kugel, 1997), demon- southern regions of the globe, phasmids can be strated that stick insects were able to make use of found in virtually any terrestrial ecosystem. How- visual signals, provided ambient light levels were ever, of the approximately 2,500 extant species, sufficiently bright for the insect’s photoreceptors to only one, the common stick insect Carausius moro- detect such signals. sus, has become a widely used laboratory species. In spite of this awareness of the stick insect’s vi- It reproduces parthenogenetically, is easy to keep, sual ability, the only existing studies to date, occu- shows interesting behavioural patterns and has pying themselves with developmental aspects of been used in studies on population ecology, genet- this insect’s photoreceptors, are those by Such ics, embryology as well as locomotion, colour (1969, 1975, 1978). Such’s research, however, cov- change, mechanoreception, and vision. ered mainly embryological and cytological aspects Adult specimens are primarily active at night and was neither concerned with developmental (Godden, 1973) and their visual capacity was origi- changes that occurred during the post-embryologi- nally considered to be poor. However, Jander and cal, nymphal life stages of the insect nor with pho- Volk-Heinrichs (1970) could show that stick in- tomechanical responses upon dark/light adaptation. sects are able to distinguish vertical patterns from Against the background of the worldwide use of C. slanted and horizontal ones and Frantsevich and morosus as a laboratory insect and the paucity of Frantsevich (1996) later discovered that a stick in- information on its postembryonic eye development sect’s preference for certain figures depended on and dark/light adaptational phenomena, a thorough whether it found itself in an upright or upside- study of these neglected aspects of stick insect * To whom correspondence should be addressed at: E-mail: vmr@cc.oulu.fi 281 282 V. B. MEYER-ROCHOW and E. KESKINEN photobiology seemed overdue. overall light sensitivity of the eye, provided the Arthropod photoreceptors, generally, are rather amount of the photopigment per receptor cell does flexible organs that vary widely with regard to not decline between moults. The larger size of the structure and function, reflecting species-specific eye and the greater volume of visual membrane adaptational needs as well as phylogenetic affilia- material in older individuals are likely to make tions (Land and Nilsson, 2002). Moreover, in many mechanisms capable of protecting the eye more species the eyes change in size, shape, inner organ- important. One would, therefore, expect dark/light ization, and performance as the arthropod grows adaptational phenomena to be more pronounced and matures. Further flexibility, manifesting itself and more effective in older individuals, but scien- anatomically through cell movements and appear- tific data to back up this prediction have not been ance as well as location of organelles and mem- available till now. The aim of this paper has, there- branes, assures that the eyes can cope not only with fore, been not only to document postembryonic eye the regularly recurring oscillations of day and growth in the stick insect C. morosus, but also to night, but also with sudden changes in ambient carry out a parallel investigation on the capacity light levels, temperature fluctuations and even dif- for dark/light adaptation in newly hatched and fully ferences in nutritional supplies (Meyer-Rochow, mature specimens. 1999). Eguchi and Waterman (1979) used the terms MATERIALS AND METHODS adaptive and supportive to describe the two main mechanisms involved in protecting the arthropod Individuals, representing all size and age groups eye as well as optimizing its performance. Adap- of the stick insect Carausius morosus, were housed tive mechanisms prepare the developing eye for in spacious containers in the laboratory under a particular, largely predictable, photic conditions re- light:dark regimen of 12:12 h (on: 07.00; off: lated to a species’ habitat and life-style. Except for 19.00). The temperature was maintained at a con- species living in caves, the deep-sea, and the polar stant 123°C and the insects were fed a diet of regions, all arthropods experience day and night stinging nettle, dandelion, lettuce, and other sea- rhythms and their eyes, often through endoge- sonally available leaves. In order to obtain fully nously regulated processes, adjust their sensitivity dark-adapted individuals, specimens were kept in accordingly (Meyer-Rochow and Nilsson, 1999). total darkness for 24 h prior to decapitation; light- Absolute sensitivity to light is usually greater at adapted individuals faced illuminations of approxi- night, because screening pigment granules move mately 1,000 lx in intensity for 24 h prior to decapi- out of the light path, ommatidial apertures widen, tation. and amounts of visual membrane and photopig- Specimens sacrificed for transmission electron ment increase. During the day, however, reverse microscopic (TEM) observations were decapitated processes lead to sharper vision, i.e., increases in at 12.00 h and 24.00 h (referred to in the text and acuity, but at the expense of sensitivity. Sudden and figures as noon and midnight specimens, irrespec- unpredictable exposures to bright lights trigger tive of their state of adaptation). Dark adapted and faster responses than those involved in connection light adapted specimens, decapitated at both noon with the adaptive mechanisms and are primarily and midnight, are referred to as DA-noon and LA- aimed at protecting the eye against photic damage noon, and DA-midnight and LA-midnight samples, through overstimulation and dangerous forms of respectively. Each specimen was measured with a radiation, e.g., solar UV (Meyer-Rochow, 2000). ruler to its closest 1 mm and then had its severed In insects of the hemimetabolous kind, newly head immersed for 12 h at 14°C in the first fixative hatched individuals usually possess tiny compound solution (i.e., 2% paraformaldehyde and 2% glu- eyes with a limited number of facets. As the indi- taraldehyde in 0.1 M phosphate buffer, buffered to a viduals grow through moulting, they add omma- pH of 7.2). Prior to postfixation in ice-cold, phos- tidia and, therefore, increase the number of pho- phate-buffered 2% osmiumtetroxide solution for toreceptive cells in the eye (Bernard, 1937). Such 30 min, the specimens were rinsed three times for changes, which often affect not only the size of the 10 min in buffer. Following postfixation, the speci- eye, but also its shape, must lead to a heightened mens were rinsed once again, but this time in dis- Eye Dynamics in the Stick Insect Carausius morosus 283 tilled water, before being passed through a graded noon and measuring 1.2, 1.5, 2.0, 2.2, 3.0, 3.5, 4.2, series of ethanol. At the completion of dehydration, 4.3, 6.0, 7.5, and 8.0 cm in body length) and an- the specimens were immersed in propylene oxide other 10 (fixed at midnight and measuring 1.3, 1.7, twice for 10 min, stepwise embedded in epon- 2.2, 3.0, 4.1, 5.5, 6.0, 7.9, and 8.0 cm in body araldite, and hardened at 60°C in an oven for two length) served as material for TEM-studies of ul- days. trastructural observations on dark/light adapta- Semithin sections for light microscopy were cut tional changes. At least 4, but most frequently 10 with a glass knife on an ultramicrotome and or more, measurements were taken on each of the stained for 10–15 s with toluidine-blue on a hot- regularly monitored anatomical features of the cen- plate. Measurements were made from digital cam- tral regions of either the left or the right eye.
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