Circadian oscillation of sensitivity of spider eyes: diurnal and nocturnal spiders

The anterior median eyes of the orb-weaving spiders Argiope bruennichii and Argiope amoena have three types of visual cells, with maximum sensitivities at approximately 360 nm (ultraviolet cell), 480–500 nm (blue cell) and 540 nm (green cell). The blue cells are the most sensitive and have a circadian oscillation of sensitivity (Yamashita and Tateda, 1978). Argiope sp. appears to be active both during the day and at night (a noct-diurnal spider); during the day, it stays in the hub of its web and attacks its prey. In the present study, we examined the circadian oscillation of sensitivity of the anterior median eye of the garden spider Araneus ventricosus and the jumping spider Menemerus confusus. Araneus ventricosus constructs its web each day after sunset and destroys the web before sunrise, i.e. Araneus ventricosus is active only at night. Menemerus confusus is a typical diurnal hunting spider, and a number of its behavioural activities are initiated by visual stimuli (for reviews, see Forster, 1985; Land, 1985; Yamashita, 1985).

The animals used in this study were female garden spiders Araneus ventricosus and male and female jumping spiders Menemerus confusus. They were collected in open fields. Preparation and recording methods were similar to those described previously (Yamashita and Tateda, 1978). A tungsten electrode was inserted into the eye to record electroretinograms (ERGs) from intact animals. For white light stimulation, light emitted by a Xenon arc lamp or a tungsten filament lamp was delivered to the eye via a quartz light guide, 0.2 mm in diameter, positioned in front of the corneal lens. The maximum intensity of the white light was referred to as unit intensity (logI=0). The duration of illumination was controlled by an electromagnetic shutter, and the intensity was adjusted by calibrated neutral-density filters and wedges. A monochromatic light beam was produced using interference filters. The energy of the selected monochromatic light was measured at the cornea of the eye using a radiometer. Monochromatic light (520 nm) of 10¹⁴ quanta cm⁻² s⁻¹ and white light of logI=—2 generated ERGs with a similar amplitude.

The anterior median eye of Araneus ventricosus showed a marked circadian oscillation of sensitivity. An example is shown in Fig. 1. After the cessation of background illumination at 17:00 h, the ERG amplitude increased gradually for over 3 h. It then showed a circadian oscillation with a period of approximately 24–25 h under a constant dark background for 9 days. ERGs of constant low and high amplitude were recorded for approximately 9–11 h and 8–10 h, respectively. We call the former period ‘subjective day’ or briefly ‘day’, and the latter period ‘subjective night’ or briefly ‘night’.

Fig. 2 shows ERGs in response to white light stimuli of 0.1 s duration at various intensities recorded during the subjective day and night. The waveforms of night-time ERGs at logI=—7, —5 and —3 are similar to those of daytime ERGs at logI =—5, —3 and —1, respectively. The intensity/response relationships for daytime and night-time ERGs are shown in Fig. 3. The threshold intensity for the night-time ERG was approximately 2 log units lower than that for the daytime ERG.

The spectral sensitivity of the anterior median eye was examined by recording ERGs (Fig. 4). Under a constant dark 0.2 s background, daytime ERGs in response to a flash of 10¹⁴ quanta cm⁻² s⁻¹ and night-time ERGs in response to a flash of 10¹² quanta cm⁻² s⁻¹ showed similar amplitudes at each wavelength. Each curve had a broad peak at approximately 520 nm in the visible region and a smaller peak or a shoulder in the ultraviolet region (approximately 360 nm). There was no significant difference between the daytime and night-time spectral response curves, as reported for Argiope spp. (Yamashita and Tateda, 1978). Chromatic light adaptation did not change the spectral response characteristics. Fig. 4 shows the amplitude of the night-time ERG in response to a flash of 10¹⁴ quanta cm⁻² s⁻¹ during adaptation to 540 nm light. These observations suggest that the anterior median eye of Araneus ventricosus has a single spectral type of photoreceptor that has a circadian oscillation of sensitivity.

No circadian oscillation of sensitivity was observed in the anterior median eye of Menemerus confusus. An example is shown in Fig. 5. After the cessation of background illumination at 16:00 h, the ERG amplitude increased rapidly within 1 min to a plateau level (Fig. 5A). The ERG amplitude then remained almost constant for approximately 1 month (Fig. 5B). Similar results were obtained from the anterior lateral eye and the posterior lateral eye. The intensity/response relationships obtained from the dark-adapted anterior median eye at 10:00 h and at 20:00 h are shown in Fig. 6. The two curves are almost identical. The ERG threshold for Menemerus confusus was approximately 100 times higher than that for Araneus ventricosus during the subjective night (cf. Fig. 3). We conclude that photoreceptor cells in the eyes of Menemerus confusus do not show a circadian sensitivity rhythm.

Yamashita and Tateda (1978) reported that the more-sensitive blue cells in the anterior median eye of noct-diurnal spiders, Argiope spp., show a circadian oscillation of sensitivity, but that the less-sensitive green and ultraviolet cells do not. As shown in the present study, the anterior median eye of a nocturnal spider, Araneus ventricosus, showed marked circadian oscillation of sensitivity, but the anterior median eye of a diurnal spider, Menemerus confusus, did not. The posterior median eye and the posterior lateral eye of Argiope spp. demonstrate the morphological characteristics of noct-diurnal spiders: i.e. they have two types of retina in the same eye (Uehara et al., 1978). In one type, the rhabdomic layer of the retina is backed by a tapetal reflecting layer. In the other type, the rhabdomic layer is backed by a pigmented layer. These observations suggest that Argiope is an intermediate type of spider between typical nocturnal spiders such as Araneus ventricosus and typical diurnal spiders such as Menemerus confusus.

Circadian sensitivity changes in the eye that are controlled by efferent optic nerve fibres have been reported for Limulus polyphemus (for a review, see Barlow et al., 1989), scorpions Androctonus australis (for a review, see Fleissner and Fleissner, 1988) and Argiope bruennichii and Argiope amoena (Yamashita and Tateda, 1981). Nakamura and Yamashita (1997) recorded efferent impulses from the optic nerve of Araneus ventricosus. In Araneus ventricosus, efferent optic nerve fibres may also control the sensitivity of the eye. The eye of Menemerus confusus showed no circadian oscillation of sensitivity. We observed no efferent activity in the optic nerve of Menemerus confusus, suggesting that Menemerus confusus may lack efferent optic nerve fibres.

The eyes of spiders have various spectral types of receptor cells (for a review, see Yamashita, 1985). Walla et al. (1996) made intracellular recordings from photoreceptor cells of the eyes of the ctenid spider Cupiennius salei, a nocturnal hunting spider, and found three spectral groups of cells with sensitivity maxima in the blue (480 nm), green (520 nm) and ultraviolet (340 nm) regions. In the present study, we have demonstrated that the anterior median eye of Araneus ventricosus has a single spectral type of photoreceptor. It seems that the anterior median eye of Araneus ventricosus is not capable of colour discrimination.

This research was supported in part by a Grant-in-Aid for Scientific Research from the Ministry of Education, Science and Culture of Japan.