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«SPECTRAL SENSITIVITIES OF THE EYES OF THE ORB WE B SPIDER ARGIOPE ARGENTATA (FABRICIUS ) Klaus B. Tiedemann, Dora Fix Ventura and Cesar Ade s ...»

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Tiedemann, K. B., D. F. Ventura and C. Ades. 1986. Spectral sensitivities of the eyes of the orb we

b

spider Argiope argentata (Fabricius). J. Arachnol., 14 :71-78.

SPECTRAL SENSITIVITIES OF THE EYES OF THE ORB WE B

SPIDER ARGIOPE ARGENTATA (FABRICIUS )

Klaus B. Tiedemann, Dora Fix Ventura and Cesar Ade s

Department of Experimental Psychology

Institute of Psychology

University of Sao Paul o Sao Paulo, Brazil

ABSTRACT

Spectral sensitivity curves to light between 425 and 650 nm for the four eyes of the spider Argiope argentata were determined. Maximum sensitivity was observed at 530 nm for the secondary eyes an d at 525 nm for the principal ones. Chromatic adaptation did not affect this maximum, which suggest s that there is only one receptor and photopigment in this spectral region.

INTRODUCTIO N

Recordings from the anterior median eyes of jumping spiders demonstrated th e existence of different photoreceptor types, thus confirming earlier behavioral dat a suggestive of color vision in these animals (Peckham and Peckham 1887, Cran e 1949, Kastner 1950, Young and Wanless 1967). According to DeVoe's (1975 ) intracellular recordings, color vision in the principal eyes of the jumping spide r Phidippus regius (C. L. Koch) is mediated by three photoreceptor types : UV cells with peak sensitivity at 370 nm ; green cells with peak at 532 nm, and UV-gree n cells, peaking at 370 and 532 nm. In the secondary eyes of this spider DeVo e found only green cells. In the jumping spider Menemerus confusus (Bosenberg and Strand), Yamashita and Tateda (1976) found, in addition to UV and gree n receptors, a blue receptor at 490 nm and along-wave-length receptor at 580 nm.

Their data were based both on intracellular recordings and on chromati c adaptation effects on the electroretinogram (ERG).

Other families of spiders did not exhibit the same color vision abilities as foun d in jumping spiders. Young and Wanless (1967) conducted a T-maze preferenc e study in seven spider families, and found that only Salticidae exhibited behavior s suggestive of color vision. In ERGs from Lycosidae, DeVoe, Small and Zvarguli s (1969) found only one photopigment (green) in the secondary eyes. The principa l eyes contained variable amounts of this pigment in addition to an UV absorbin g one.

Color vision was only recently studied in spiders of the Araneidae family. Th e anterior median eyes of Argiope bruenchini (Scopoli) and Argiope amoena (L.

Koch) were found to have three photoreceptors, with maxima at about 360 nm, 480-500 nm and 540 nm (Yamashita and Tateda 1978, 1981). No recordings wer e reported for the secondary eyes.

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The present study, which was started before the publication of Yamashita an d Tateda's reports (Tiedemaan 1975), brings information about the color visio n system of Argiope argenta t a (Fabricius), an orb web spider whose behavior has been extensively studied (Robinson 1969, Robinson and Olazarri 1971, Ade s 1973). Argiope argentata lives in sunny areas and is diurnal, but it is capable o f hunting and of building its web in the dark. Its characteristic thermoregulatory posture (Robinson and Robinson 1978) was shown to be controlled by ligh t rather than by heat (Ades and Kanner 1978). Its choice of the side of the web on which to stand is also light dependent (Ades and Kanner 1979). It can rel y on visual stimuli when placing the first threads of the web, as do othe r orbweavers (Tilquin 1942). There is no doubt that visual cues are of grea t relevance to several aspects of behavior of this species. There is not, however, an y information regarding its color vision abilities. In this report we describe the ERG measured spectral sensitivities of the dark-adapted eyes of Argiop e argentata, and the results obtained under chromatic adaptation, showing that i t has only one receptor type in the spectral range from 425 to 625 nm.

METHOD

Preparation.—The ani m was lightly anesthetized with CO2 and fixed to a black cardboard with a d esive tape over the legs. The cephalothorax wa s immobilized with acrylic ( implex dental acrylic). The recording electrode was a cotton wick held in a glas s ube pulled out at one end to a capillary tip and filled with insect physiological s lution. Contact with the recording system was done through a nonpolarizable Ag-AgCI wire. The indifferent electrode was a Microtode 415 (Transidyne General Corporation) inserted in a leg of the first o r second pair just below th e surface. Such a preparation could last for at least 1 2 hours and longer than a w e k, if the spider received water by means of a capillary tube. The temperature was aintained at 22 to 24°C during the recordings. ERGs were measured with a Tekt ~ onix 122 AC amplifier with a 1 s time constant and 50 Hz filter, and a Tektr nix 5103/D13 dual beam storage oscilloscope and photographed with a Grass -4 camera.

The preparation was pla ed in a light tight box inside a recording chamber.

The optical equipment co sisted of a double Maxwellian view system with a tungsten halide quartz la p (Osram 58.8105 100W) as the light source, which permitted focussing throug a light pipe (Fiber Lite) of a 3 mm diameter ligh t spot on the eyes. Intensit was controlled by means of glass-mounted Koda k Wratten 96 neutral density filters and duration of the stimulus flash through a photographic shutter (Woll :nsack). Monochromatic light was filtered out throug h (Veril S-200-Leitz), corrected with neutral densit y an interference color wed n filters Kodak-Wratten 9 6 f r equal light energy for wavelengths between 425 nr and 675 nm in steps of 25 nm. The light passed through a 3 mm slit yieldin g a halfband width of ca. 8 5 nm. A second light source, for the adapting ligh t was a Fiber Lite Illum in tor Mod. 172 with a simple Maxwellian system, perpendicular to the fir s. In the experiments with ultraviolet light, an incandescent UV-lamp, w. hi h emitted light between 320 nm and 440 nm with a maximum output at 380 n (GE Purple X - 250W) was used in connection with an UV filter with a maxim m transmittance at 38 0 nm and an edge at 400 nrn m (Kodak 18 A), directly on t h preparation.





TIEDEMANN ETAL.-SPECTRAL SENSITIVITIES 73

The stimulating light produced at the end of the light pipe a light intensity of (4.24). 10 -6 W at 500 nm, so that a 20 ms flash corresponded to about (2.76).

10" photons. The adapting light yielded, with a red filter with transmittance fro m 570 nm to infrared (Kodak 23 A), an intensity of (3.60). 10 -5 W and with a narrow band blue filter with maximum output at 430 nm (Kodak 48 B), (1.60). 10 S W. Calibrations of ND filters at each of the wavelengths used were mad e with a Tektronix radiometer J 16 with J 6502 probe and a Zeiss DMR-2 1 spectrophotometer.

Procedure. —All recordings were done during the day, between 8 a.m. and 5 p.m. The preparation was dark adapted for at least 30 minutes prior to eac h experimental session.

For each eye (anterior median, posterior median, anterior lateral and posterio r lateral eye) the energy-response functions were determined under conditions o f dark adaptation and red-, blue- and white-light adaptations for each of th e calibrated monochromatic lights between 425 and 675 nm. Data collected unde r light-adapted conditions were preceded by 10 min of exposure to the adaptin g light before measurements were begun. Energy-response functions were obtaine d at each of these adapting conditions by measurements of ERG amplitude fo r stimuli of the following mean attenuations : 0 ; 0.21 ; 0.53 ; 0.95 ; 1.26 ; 1.60 ; and 2.1 3 log. At each attenuation value the spectrum was scanned twice, at 25 nm steps, in opposite directions, with 20 ms long flashes presented at 30 s intervals.

A standard of 550 nm was used throughout the experiment for frequent check s of the stability of the preparation. All data reported are from preparations whic h remained quite stable, within 2% variation.

RESULTS AND DISCUSSION

Waveform of the ERGs.—The waveform of the ERGs recorded in A. argentata is similar for all four eyes and does not differ as a function of wavelength of th e test flash, as can be observed in Figure 1. Changes in waveform were only notice d in connection with variation in light intensity. Recordings shown in Figure 2 exemplify such waveform changes. At high intensities the waveform was typically a single rapid negative wave followed by a slow uniform decay. The small positive wave is an artifact of capacity coupling of the AC recording amplifier. At low intensities the ERG consisted of a double negative wave in all eyes except th e principal. In the latter, peak latency was • intermediate between the two negative waves found for the other eyes.

The shape of the ERG was also examined under chromatic light adaptation, because it has been reported to change in species that have differen t photoreceptor types, such as the jumping spider, M. confusus (Yamashita and Tateda 1976). In the eyes of Argiope argentata no change in waveform was observed as a function of wavelength of chromatic adaptation. This was a first indication of the absence of additional photopigments in the tested part of th e spectrum (400-600 nm) in the species.

Spectral Sensitivity.—To determine the spectral sensitivity curves of the fou r eyes, the ERG amplitudes in response to monochromatic lights presented to th e dark-adapted eye at 25 nm steps were measured as a function of light intensit y over a 2.0 log unit range. The energy-response functions thereby obtained ar e plotted in Figure 3. The functions are closely parallel for each of the eyes, but

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Fig. 1.-ERGs in response to stimuli of 425 nm and 600 nm obtained in the four eyes. Test flas h duration was about Is.

differ in slope from one e e to the other. The posterior median eyes exhibit th e shallowest curves, where a the posterior lateral eyes the steepest ones. The differences could be attri b ted either to different densities of photoreceptors, or, as suggested by Dahl (per comm.), who found similar differences in the eye s of Aphonopelma, to the p esence of the tapetum in the eyes that exhibited the lesser slope.

To draw the spectral se n itivity curves, the amplitude data collected above wer e transformed according t o he procedure described by Autrum and von Zweh l (1964). This consisted of lotting the mean energy function for each eye an d finding the intensity tha t would have been necessary to elicit a given ER G amplitude. The relative lens tivity is the reciprocal of that intensity.

The entire procedure was repeated under chromatic adaptation to blue and red lights with the purpose of determining whether any of the eyes contained more than one type of visual cell or pigment in the visible part of the spectrum. If thi s were so, the spectral s e sitivity curve obtained under selective chromatic adaptation would be displa ed relative to that obtained in the dark adapted stat e (Wald 1968, Yamashita and ateda 1976).

Figure 4 shows the spe tral sensitivity curves for the four eyes, under dark adaptation and the three 1 ght adapting conditions. As can be seen, chromatic adaptation did not change he shape of the spectral sensitivity curves for any of the four eyes. The smoot h lines are Dartnall nomogram curves (Dartnall 1953).

For the lateral and posteri o eyes, the best fitting was a 530 nm nomogram curve, whereas for the anterior m dian eye a 525 nm nomogram curve yielded the bes t fit. This discrepancy may be due not to a different photopigment but t o differences in the optic me is between principal and secondary eyes (Young an d Wanless 1967). In the sho r -wave range of the spectrum the fit of the Dartnal l

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nomogram curves was not so good. The sensitivity was less than predicted by th e nomogram for all four eyes. The same type of result was found by DeVoe, Smal l and Zvargulis (1969). This is not, however, the common finding in othe r arthropods, the rule being that sensitivity in the near UV is higher than predicte d by the nomogram curves, as found in the bee (Autrum and von Zwehl 1964), dragonfly (Autrum and Kolb 1968), Calliphora and Periplaneta (Walther an d Dodt 1959), Musca domestica (Eckert 1971), Atta sexdens (Martinoya, Bloch, Ventura, and Puglia 1975) and several species of crustacea (Scott and Mote 1974).

UV sensitivity is nevertheless present in A. argentata, as revealed by tests mad e with UV stimulation (GE Purple X lamp plus Kodak 18 A filter). These test s showed that responses in the UV are present in all four eyes, but are higher i n the anterior median eyes than in the other ones. This is in agreement wit h DeVoe's observations (DeVoe, Small and Zvargulis 1969, DeVoe 1972, 1975), wh o also found higher sensitivity in the anterior median eyes.

The reason why we did not find evidence for more than one visual pigmen t in the anterior median eyes of Argiope argentata, as found for the Japanes e

–  –  –

species, is not clear. This f ilure to isolate a blue receptor (their "green" cell wit h peak at 540 nm closely o erlaps our data, which peaks at 530 nm) could b e attributed either to specie s ifferences, or to a lower sensitivity of our technique.

It could have also been d u to the time of day in which the data were collected.

The blue cells found by Ya ashita and Tateda were recorded at night. Our dat a were always collected duri n the day. Alternatively, Yamashita and Tateda's clai m for the existence of a "b l e" receptor cannot be regarded as unquestionable.



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