THE VISUAL MECHANISMS OF TENEBRIO MOLITOR: VARIATIONS TAKING PLACE IN THE ERG OF PUPA AND ADULT DURING DEVELOPMENT

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1 J. Exp. Biol. (1969), With 5 text-figures Printed in Great Britain THE VISUAL MECHANISMS OF TENEBRIO MOLITOR: VARIATIONS TAKING PLACE IN THE ERG OF PUPA AND ADULT DURING DEVELOPMENT BY URI YINON* AND EDGAR AUERBACH The Vision Research Laboratory, Hadassah University Hospital, Jerusalem, Israel (Received 1 April 1969) INTRODUCTION In the pupal eye of tenebrionids such as Tribolium confusum and Tribolium casataneum the number of the ommatidial rows changes as the animal grows older (Ho, 1961), marking the beginning of the development of the compound eye. Autrum (1958) and Eguchi, Naka & Kuwabara (1962) showed that histological and anatomical variations occur within the insect eye before maturity is reached. It is generally assumed that the development of the insect eye is finished when it enters the adult stage, but there is reason to doubt this because not only the body of the insect but also its eyes display changes even after emergence. The purpose of this study was to follow electrophysiologically the development of the eye, and to link the pupal stage with the adult. METHODS The experimental insect was Tenebrio molitor. It was raised on wheat bran, coarsely ground wheat, oat flakes and powdered yeast extract in the proportions (by weight) of 3:3:3:1. Liquid was provided by water-soaked cotton-wool. The breeding containers were kept in a dark incubator at 28 ± 2 C. The largest larvae were separated in a test tube containing food. Changes in the eyes of insects following pupation and emergence were observed by means of a binocular microscope. Twenty-three pupae (1-7 days) and 15 adults (2-14 days) were selected and used for the experiments. There were approximately equal numbers of both sexes of adult beetles. The insect was fixed with adhesive tape to a cork surface which was placed on a micrometric moving table. One eye from each insect was used. Left and right eyes were chosen alternately. The stimulating light was directed at right angle to the body axis of the beetle. As electrodes entomological stainless-steel needles were used with tip diameter of about 13 fi and an impedance of about 25 KQ. The recording electrode was inserted into the compound eye. A micromanipulator made it possible to penetrate just the cornea. The indifferent electrode was introduced into the frontal subcuticular region of the abdomen. For stimulation a tungsten lamp of 500W was used, and the light beam was directed Present address: Department of Ophthalmology, Duke University Medical Center, Durham, N.C., U.S.A.

2 636 URI YINON AND EDGAR AUERBACH into the eye of the animal by means of an optical system. Both animal and optical system were placed in an electrically shielded and light-protected cage. The intensity of the unfiltered light measured at the eye was between 7-5 and 8-o f.c. The animal was dark-adapted for 5 min. Preliminary tests showed that during this period some 90 % of the recovery was completed (Yinon, 1968). 50flashesof 25 msec, duration were applied at a rate of one per second. Different intensities were used. They were changed by a calibrated neutral density circular wedge over a range of 3 log units. Intervals of 2-3 min. in the dark were allowed between successive series of 50 flashes. A CAT (Computer of Average Transients, 400B, T.M.C.) was used for recording. The averaged responses were photographed from the screen of an oscilloscope on four channels. The number of pulses was measured by an electronic counter. The CAT was triggered by a photoelectric cell. The polarity of the response was determined by comparison with a 3V D.C. pulse. The upward deflections indicate positive polarity. RESULTS Morphology. During the development of the pupa it could be observed that the number of ommatidial rows gradually increased. While there were only 4-5 ommatidial rows in the white eye of the i-day-old pupa, they increased to 7-9 rows in the 2-day-old pupa, and to 9-13 in the 3-4-day-old insect. They were arranged in a straight line along the whole width of the frontal margins, and each ommatidium was clearly distinguishable. At the age of 4 days the eyes were still white, but became clearly visible, by contrast with a pigment which accumulated in the cells. Later at 5 days the eye sbecame dark but the individual ommatidia were still distinguishable. However, the visible interspace between the ommatidia had now disappeared owing both to the increase in their size and to the pigment concentration. A day later the eye became brownish-black because of the more densely pigmented ommatidia, which no longer could be distinguished individually. One day before emergence, in the 7-day-old pupa, the eyes became dark brown, as in the i-day-old adult. Occasionally the eyes of the pupa did not contain any pigment and remained colourless. From such a pupa a pearl-eye-mutation emerges. These animals were not used for this work. Up to the fourth day the cornea of the pupa was very soft. During the following 3 days it became harder and remained so until the third day of the adult stage. Thereafter the hardening continued up to the age of 3-4 weeks, when the cornea became as hard as the cuticular cover of the body. Thus ommatidial and corneal development, which started in the pupal stage, continued in the adult. Because of technical reasons it was not possible to measuie the optical density of the cornea, which may change during the development. This would also change the electrical response. Physiology. A very small ERG of negative polarity measuring a few microvolts was already recordable in the i-day old pupa of T. molitor. It became clearly measurable a day later and gradually increased in amplitude during the following days. From the pupal stage to the adult there was a gradual transition in the development of the ERG, whose wave pattern became more and more complex (Fig. 1). The ERG was essentially characterized by a negative potential followed by a slow positive wave which gradually swung back to the baseline. Sometimes the negative wave was preceded by a small positive deflection.

3 Visual mechanisms of Tenebrio molitor 637 There were considerable differences in the amplitude of the negative potentials at different ages of the pupa and the adult. The response of the first-day pupa was about six times smaller than that of the seven-day-old pupa (Fig. 2), and the average height greatly increased. The morphology appeared to be correlated with the change in the response. A9 Fig. 1. The ERGs of pupae and adults of Tenebrio molitor of various ages. Voltage and time calibrations for each response are seen at the right of each recording (horizontal line in all figures = 25 msec.). P = pupa; A = adult. The number indicates the age in days. The recordings with four tracings show the responses to stimuli in decreasing intensities (log units) (from top to bottom: o-o; o-8; 1-6; 2-4).

4 638 URI YINON AND EDGAR AUERBACH The response of the adult eye immediately after emergence was about twice that of the seven-day-old-pupa, and continued to increase greatly up to the fifth day, when it reached about 3 mv. Thereafter the increase in the amplitude was slowed, and reached finally a maximum of about 5 mv at the fourteenth day. The maximal adult response is then about 14 times that of the pupa's maximum. 10,000 r 1, Pupa- -Adult Age (days) Fig. 2. The changes in the negative potential of the ERG with age of pupa and adult T. molitor Fig. 3. Amplitude changes in the negative potential of the ERG as a function of stimulus intensity (on the second and on the fourteenth day of the adult T. molitor). With regard to the peak latency of the negative potential the variations were not related to the age of pupae or adults and generally ranged from 50 to 80 msec. The negative wave characteristic of the ERG in the pupa was measured as a function of the stimulus strength. It was found that it increased with the intensity over a range

5 Visual mechanisms of Tenebrio molitor 639 of two log units to a maximum beyond which it decreased. Although the variability was very great, this tendency was observed in pupae no matter the age. Less variability was found in the adult insect. Here the amplitude of the negative potential increased approximately linearly with the stimulus intensity, and the rate of the increase changed with age (Fig. 3). The negative amplitude of the ERG of the adult was about 20 times larger than that of the pupa (Table 1). 160 r 120 e Log./ Fig. 4. Peak latency changes in the negative potential of the ERG as a function of stimulus intensity; (each point is the average of the various ages measured in the pupae.) -2-4 Fig. 5. Peak latency changes in the negative potential of the ERG as a function of stimulus intensity (on the second and on the fourteenth day of the adult T. molitor). To elicit a just visible negative potential a much smaller amount of energy was necessary than for the preceding and following positive potential. The slower positive potential appeared only at high stimulus strength and became suppressed with the further increase. The faster positive potential could be elicited with a still higher stimulus strength and increased in amplitude up to the limit of the light source used (see Fig. 1 for the fast and slow positive potentials in A3). The threshold sensitivity of the negative potential increased with age, i.e. gradually less energy was necessary to elicit this wave.

6 640 URI YINON AND EDGAR AUERBACH The peak latency of the negative potential in the pupa (average of pooled data for 23 pupae at all ages, see Fig. 4) gradually shortened with the increase in stimulus intensity. Over two log units the peak latency decreased to less than half the value obtained at lowest intensity used. No systematic change in the peak latency with age could be observed either in the pupa or in the adult (Fig. 5). The latent period of the ERG and also the peak latencies of the negative and the following positive potentials were longer in the pupa than in the adult. The latent period of the preceding positive wave was too variable for measurement (Table 1). Table 1. Average responses of pupae and adults of all ages under the same conditions (log I = o*o) Following positive potential Stage Pupa Adult Parameter Latency (msec.) Amplitude (jiy) Latency (maec.) Amplitude (/*V) Latent period Negative potential DISCUSSION There is a clear relationship in Tenebrio molitor between morphology and function in that the sensitivity of the eye gradually increases during the pupal and adult stages as a function of the increase in the number of light-sensitive elements. This is reflected by the increase in amplitude of the ERG with age. Two facts are of importance. First, the increase in sensitivity is gradual; there is no abrupt or sudden change in its kinetics at the transition from the pupa to the adult. Secondly, the emergence does not mark the end of development. The sensitivity of the eye continues to increase for another 14 days. This observation should be examined and confirmed histologically. The ERG assumes its final biphasic shape only gradually after emergence. Autrum & Gallwitz (1951) and Autrum (1958) found in Aeschna cyanea that this is connected with the position of the optic ganglion relative to the ommatidial zone. The increase in sensitivity during development is reflected by the finding of Ruck (1965). He found in electrophysiological measurements in the eye of Libellula Uictuosa that there are more different groups of photoreceptors in the adult stage than in the nymphal. It therefore seems possible that the addition of new visual pigments contributes to the increase in sensitivity at least as much as does the optic ganglion. In contrast to the findings reported here, Eguchi (1962) and Eguchi et al. (1962) were unable to demonstrate an ERG in Bombyx mori before the fifth day of the pupal stage. However, an averaging technique might have revealed a response much earlier. Moreover, no information is found in this work on any development of the electrical response during and after the transformation from the pupa to the adult. The findings of the present study make it likely that such development is found not only in Tenebrio molitor but in other insect species as well.

7 Visual mechanisms of Tenebrio molitor 641 SUMMARY 1. The changes in the ERG of the compound eye of Tenebrio molitor were measured and followed in both the pupal and the adult stages. 2. In the pupal stage the generally monophasic ERG was found to appear on the second day, and within 7 days reached an amplitude of 0-35 mv. The more complex ERG of the adult beetle increased in amplitude to more than 5 mv. during the following 14 days. 3. The latent periods and peak latencies of the pupal and adult ERGs differed only slightly and did not display any consistent changes with age. 4 The morphological development of the eye was compared with the changes in the ERG. REFERENCES AUTRUM H. (1958). Electrophysiological analysis of the visual systems in insects. Expl Cell Res. (Suppl.) S, AUTRUM H. & GALLWITZ U. (1951). Zur Analyse der Belichtungspotentiale des Insektenauges. Z. vergl. Pkyiiol. 33, 4 7-3S- EGUCHI, E. (1962). The fine structure of the eccentric retinula cell in the insect compound eye {Bombyx mori). Ultrattruct. Ret. 7, EGUCHI, E., NAKA, K. & KUWABARA, M. (1962): The development of the rhabdom and the appearance of the electrical response in the insect eye. J. gen. Pkytiol. 46, Ho, F. K. (1961). Optic organs of Tribolium confuntm and T. cattaneum and their usefulness in age determination (Coleoptera: Tenebrionidae). Ann. ent. Soc. Am. 54, RUCK, P. (1965). The components of the visual system of a Dragonfly. J. gen. Pkyiiol. 49, YINON, U. (1968). Studies on the physiology of vision of granary beetles. Ph.D. Thesis, The Hebrew University of Jerusalem, Israel.

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