Polarized light detection in spiders
1 Department of Zoology, University of Lund, Helgonavägen 3, S-223 54 Lund, Sweden and
2 Department of Zoology, University of Washington, Box 351800 Seattle, WA 98195, USA
*Author for correspondence (e-mail: marie.dacke{at}zool.lu.se)
Accepted April 19, 2001
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Summary |
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Key words: polarized light detection, simple eye, spider, vision, retinal tiering.
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Introduction |
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Unlike the compound eyes of many other arthropods, spiders evolved simple eyes as their main visual organs. These are highly developed in some species, with acuity that rivals that of primates (Land, 1985). Not only do spiders have the best-developed simple eyes of arthropods, but they also luxuriate in their multiplicity, having up to four pairs. Morphological and embryological differences allow these eyes to be arranged into two groups. A single pair of principal eyes, the anterio-median (AM) pair, is directed forwards. In some species, these eyes have a small field of view, which in part is compensated by a movable retina (Land, 1985). The remaining three pairs, the so-called secondary eyes, are named for their relative position on the head. The anterio-lateral (AL) eyes flank the principal eyes and are positioned in front of and below the posterio-median (PM) and posterio-lateral (PL) eyes (Fig.1). With few exceptions, the secondary eyes have a reflecting tapetum lining the back of the eye, while the AM eyes lack a tapetum in all species (Land, 1985).
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In this paper, we consider the possibility that the evolution of multiple eye pairs has allowed some spider eyes to become specialized for the task of orientation to patterns of polarized light in the sky. Together with new findings, we present an overview of polarized light detection and polarizing optics in the principal and secondary eyes of spiders.
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Optical basis for polarization sensitivity |
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Opponency between different receptors tuned to different angles of polarization facilitates the analysis of polarization, independent of the brightness of the stimulus (Nilsson and Warrant, 1999). In insects, specialized structures have evolved for this task, such as the well-studied dorsal rim area within which photoreceptors are sensitive to short-wavelength blue or ultraviolet light and have rhabdomeres with orthogonal microvilli (Burghause, 1979; Labhart, 1980). Although large receptive fields are not essential for polarization vision, these polarization analysers typically have very poor spatial acuity (Aepli et al., 1985; Labhart, 1983). It has been argued that large receptive fields allow integration of signals over large regions of sky, permitting e-vector detection even when the blue sky is partially obscured by cloud or vegetation (Labhart et al., 1984; Labhart et al., 1992; Labhart et al., 2001; Meyer and Labhart, 1993).
Orthogonally arranged microvilli have also been described in the eyes of spiders (Blest and Carter, 1988; Blest and OCarroll, 1990; Blest et al., 1981; Dacke et al., 1999; Eakin and Brandenburger, 1971; Land, 1969; Melamed and Trujillo-Cenóz, 1966; Schröer, 1971; Schröer, 1974). In addition, the reflecting sheet of crystals forming the tapetum of the secondary eyes can act as a polarizer to enhance the polarization sensitivity of the entire eye (Dacke et al., 1999).
Behavioural evidence for polarized light detection by spiders comes from three families, the ground-dwelling lycosid Arctosa variana (Magni et al., 1964), the agelenid funnel web spider Agelena labyrinthica (Görner, 1962; Görner and Claas, 1985) and the gnaphosid spider Drassodes cupreus (Dacke et al., 1999). Of these three, only the gnaphosid appears to use its secondary eyes for the task.
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Evidence for polarized light navigation by wolf spiders |
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Despite a detailed anatomical and physiological investigation, however, subsequent work failed to find either a structural basis for this polarization sensitivity in the AM eyes (Bacetti and Bedini, 1964; Melamed and Trujillo-Cenóz, 1966) or any convincing physiological evidence for these eyes being strongly polarization sensitive (Magni et al., 1965). Enigmatically, the same studies were able to find a consistent microvillar orientation and demonstrate some polarization sensitivity in the secondary eyes, even though the latter were not, apparently, involved in the behaviour.
Wolf spiders exhibit an optomotor response to rotation of polarized light
To further investigate the possibility that lycosids orient themselves in relation to the e-vector of polarized light, we designed an experiment based on qualitative observations made in the earlier studies. Spiders (Pardosa tristis) were waxed to a stick by the cephalothorax and placed with their legs in contact with a lightweight ball (circumference 120mm) that was free to rotate on an air cushion (Fig.2A). An ultraviolet-rich (Xenon) light source was viewed by spiders through a 72mm diameter linear polarizer (Hoya, 50% cut-off at 375nm) that could be rotated by a DC motor and placed at the zenith (Fig.2A). To minimize polarized reflections from objects within the spiders fields of view, the spider was suspended at the centre of a vertically oriented cylinder, 22.5cm in diameter and 15.5cm high, lined with fibrous white architectural paper. The orientation of the cylinder ensured that polarized grazing-incidence reflections from the paper were directed to below the spiders position. Motion of the spider on the ball was analysed by a 2-dimensional optical motion sensor (a Microsoft optical mouse connected to a Macintosh computer). This was positioned so that we could distinguish between progress (motion in a direction that would maintain the spiders orientation relative to the polarization stimulus), and rotation (yaw). Spiders were stimulated to run on the ball by the touch of a probe on the abdomen or rear legs. Typical running bouts lasted between 5 and 10s and rotation of the filter was only turned on after spiders had been in motion for 2 or more seconds. Data were only collected while the spider continued to run on the ball.
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To quantify this difference in degree of compensatory rotation, we selected two small (30 pixels wide) progress windows, corresponding to approximately 30°, or 10mm of forward travel (if the spider was running freely on a flat surface). These prerotation and perirotation analysis windows were symmetrically located either side of a zone 20 pixels wide at the point of commencement of rotation (arrowheads in Fig.2B). This allowed us to account for uncertainty in the exact rotation commencement point (which was marked onto each trace by hand). For any point on the spiders response path, the slope of a tangent to the path defines the strength of the turning response (yaw) relative to forward progress. A slope of 0 would represent a straight trajectory, whereas large values indicate that the spider is turning on the spot, either clockwise or anti-clockwise. We measured the response by calculating this local rotational slope, defined as the height (in pixels) of the path at each of the 30 successive pixels traced out by the spiders progress within each window. Our initial analysis suggested that the spiders turning direction was random (clockwise versus anti-clockwise) so we took the mean absolute value of the 30 local slopes as a measure of the response.
Fig.3 shows that rotation of the polarizer elicited a highly significant (Students paired t-test) increase in the degree of rotation, while rotation of the neutral density filter evoked no significant response. Since the most obvious cue available to distinguish the polarizer from the control is the e-vector of light, our results suggest that wolf spiders are able to perceive this signal and use it to generate an optomotor response. Our stimulus was placed symmetrically at the dorsal pole in relation to the body axis, subtending an angle of approximately 30°. This region of space is viewed only by the AM eyes and the most dorsal margins of fields of view of the PM and PL eyes (Land, 1985). Although we have not, as yet, used selective ablation of the eyes to demonstrate that this behaviour is indeed mediated by the AM eyes, the earlier studies strongly suggest that this is the case (Magni et al., 1964). From these results we can expect the analyser of polarized light to be located in the most ventral part of the retina in the AM eyes, since simple eyes form an upside-down image on the retina. Do the AM eyes of hunting spiders have an organization consistent with this prediction?
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Exceptions to this rule, however, are the well-studied AM eyes of jumping spiders (Salticidae). In this family, specialization of different eye pairs is taken to an extreme. The AM eyes have small, densely packed photoreceptors and a long focal length (Land, 1969; Land, 1985). The extremely high acuity that results from this combination is augmented by a tiered structure, with four layers of photoreceptors each sensitive to different wavelengths of light (Land, 1969; Blest et al., 1981; Blest et al., 1990), suggesting a role for these eyes in colour discrimination (Land, 1985).
This remarkable tiered structure was believed to have evolved originally as a solution to the problem of chromatic aberration resulting from the optics of long focal length (Blest et al., 1990; Land, 1969) rather than for polarization analysis. Nevertheless, the most distal layer is ultraviolet-sensitive (Blest et al., 1981) and microvilli of this layer are oriented horizontally in the peripheral retina and vertically in the central retina (Eakin and Brandenburger, 1971; Blest and Carter, 1988). As mentioned above, this orthogonal organization is consistent with a potential role in polarization analysis.
Are such retinal specializations unique to salticids? To address this question, we have now re-examined the structure of the AM retina in a number of hunting spider species, including lycosids. We find that several families, including the Lycosidae, Pisauridae, Oxyopidae and Thomisidae (subfamily Misumeninae), indeed have local regions in which the AM retina is tiered into two layers (Blest and OCarroll, 1990). In misumenine thomisids, the tiered region is small, with just a dozen or so photoreceptors. The tiered regions in lycosids and their sister family the Pisauridae are, however, much larger and have a structure highly suggestive of a role in polarization analysis.
The lycosid AM retina contains a ventral strip of orthogonal, tiered photoreceptors
The tiered region in lycosids is a small, strip-like sub-region in the ventral retina, while the remainder of the retina has a networked organization similar to the typical spider arrangement. In the tiered region, however, photoreceptors have square profiles and only two parallel rhabdomeres, on opposite faces of the cell (Fig.4). To avoid confusion, we will refer to the more common, networked type receptive segments with multiple rhabdomeres as type 1 and those from this ventral region, with paired rhabdomeres, as type 2 (see Table1).
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We found this retinal organization in five lycosid species, Geolycosa godeffroyi, an undescribed Geolycosa species and a further unidentified lycosid species (termed here species A), all collected in South Australia. Incomplete series of sections in fewer orientations were obtained from the British species Pardosa prativaga and Alopecosa pulverulenta. However, all sections obtained are consistent with the organization described above. In particular, both layers of type 1 photoreceptors are clearly visible in the ventral region of the retina, so that this organization seems to be common to all lycosids.
Large fields of view and poor spatial vision in the tiered part of the retina
The inter-receptor angle, , is an anatomical measure of the acuity of an eye (Land, 1985). This can be calculated from the receptor spacing determined histologically, and the focal length measured optically using the hanging drop technique (Homann, 1928; Land, 1985). The results of such measurements are given in Table1. Because of the rectangular transverse profiles of distal layer type 2 receptive segments, the inter-receptor angle measured parallel to the long axes of rhabdomeres (the vertical inter-receptor angle,
v) is typically larger than that measured perpendicular to this orientation (the horizontal inter-receptor angle,
h). Indeed, their diameter along the dorso-ventral axis (dv) is greater than their depth (receptor length), again suggesting that these photoreceptors are turned on their side. The inter-receptor angles are large compared with the 11.5 degrees estimated for lycosid secondary eyes or in typical insects (Land, 1985), suggesting that the AM eyes have comparatively poor acuity, especially in the tiered strip, where
is close to 5°. The very low F-numbers (focal length/lens aperture) measured in the same four species (species A, 0.70; G. godeffroyi, 0.73; Geolycosa sp., 0.71; P. prativaga, 0.75) confirm that these eyes are designed for efficient light-gathering, rather than for high acuity (Land, 1985; Warrant and McIntyre, 1991).
In addition to poor anatomical resolution, the photoreceptors lack any optical isolation from their neighbours by screening pigment, and the rhabdomeres of adjacent photoreceptors are also contiguous. In a low-F-number eye such as these, most light focused onto the retina enters through the margins of the lens and therefore enters photoreceptors at a large angle. In the absence of screening pigment, this light will rapidly stray into the adjacent photoreceptors, with the net effect of further increasing the receptive field size (acceptance angle) of each (Warrant and McIntyre, 1991). A further optical blurring effect must result from the fact that the three photoreceptor types (type 1, distal and proximal type 2) lie at three discrete depths relative to the centre of curvature of the cornea (Fig.5). Low F-numbers give a small depth of field, and all three layers could thus not possibly lie in the plane of focus.
The short focal lengths and semi-spherical retinae found in all four lycosid species suggest that the overall fields of view of the principal eyes are large, covering an extensive region of the space towards which they are directed (forwards and upwards in most species) and overlapping at the front. This is in accordance with the fields of view of different pairs of eyes in the lycosid Arctosa variana (Magni et al., 1964). Because the tiered region occupies the ventral margin of the retina, however, it is directed skywards, towards the most dorsal part of this field (Fig.5). It is in this part of the visual world that we find the cues for polarized light navigation (Wehner, 1989).
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Polarized light detection in secondary eyes |
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Polarized light navigation in Drassodes cupreus involves a unique compass organ
As the sun sets, the gnaphosid spider Drassodes cupreus leaves its well hidden and tightly spun silk nest to search for prey. The spider then returns to its shelter, provided it is given a polarization pattern similar to that of the evening sky. As soon as this pattern is removed, or the secondary eyes are covered with black, opaque paint, the spider can no longer find its way home (Dacke et al., 1999). This leaves Drassodes cupreus as the single known navigator shown to use its secondary eyes for this task.
The morphology and electrophysiology of the secondary eyes of this spider reveal a series of specializations that work together to provide an ideal compass organ. The majority of the photoreceptors in the PM eyes of Drassodes cupreus have their microvilli arranged parallel to the long axis of the eye (Fig.6A,B) so that the whole eye will be maximally sensitive to a single direction of polarization. This characteristic retinal arrangement is found in all the secondary eyes of the spider. As to be expected for receptors with such well-aligned microvilli, intracellular recordings reveal high polarization sensitivity ratios (Snyder, 1973), in this case as high as 9.1 (Fig.7) (Dacke et al., 1999).
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Many spider secondary eyes are equipped with polarizing optics
Weak lenses are not a novelty restricted to the secondary eyes of Drassodes cupreus; many spiders have lenses that form images well below the retina (Land, 1985). Such strange optics are still an enigma. In these eyes, as in the eyes of Drassodes cupreus, the tapetum is typically shaped a little like a boat, hence the name canoe-shaped tapetum (Fig.6C). This form of tapetum is extremely common, being found in 21 other families of spider (Land, 1985). Given our finding that the PM eyes of Drassodes cupreus are polarization analysers, is it possible that this type of eye is adapted to a similar role in other spider families? As many of the spiders with this type of eye are web-builders, it has been suggested that they could make use of a compass for the orientation of their webs (Marshall, 1999).
This possibility is further suggested by our recent finding that the polarization sensitivity of these eyes in Drassodes cupreus is not entirely accounted for by the structure of the photoreceptors themselves: the eyes also contain polarizing optics (Dacke et al., 1999). Light reflected from the tapetum of the PM eyes becomes polarized, with five times more light reflected parallel to the long axis of eye than perpendicular to it. As this direction of polarization coincides with the direction of maximal sensitivity of the receptors, it boosts the polarization signal by effectively attenuating the signals to which the photoreceptors are least sensitive. The only structures in the eye that could act as polarizing filters are the photoreceptors themselves and the tapetum. However, since the absorption of light by the retina would tend to polarize light along the short axis of the eye, orthogonal to the axis of polarization observed, we conclude that the tapetum itself acts as a polarizing reflector. The exact mechanism by which this selective reflection occurs is not yet known.
Might it be possible that the tapetum of other spiders also enhances polarized light detection? To answer this question, we measured the degree of polarization of the light reflected back from the secondary eyes of a number of families possessing canoe-shaped tapeta. We then examined the morphology of the PM eyes of at least one member of each family. The polarization measurements and the histology were according to the method described by Dacke et al. (Dacke et al., 1999). For comparison, identical measurements were also made on hunting spiders (Lycosidae, Thomisidae) with a grate-shaped type of tapetum. These families have previously been shown to have well-focused eyes (Land, 1985).
The data obtained (Table2) show that, in most of the eyes with a canoe-shaped tapetum, the reflections from one or more pairs of eyes are polarized. However, of the families studied, only the Gnaphosidae capitalise on this feature, by having retinae consisting almost entirely of photoreceptors with microvillar orientation parallel the plane of polarization reflected from the eyes. It is also in this family that we find the highest degree of polarization upon reflection. In the other families, the microvilli are arranged in several directions over the retina. Local arrangements could still support the analysis of polarized light in these other species of spider, but no obvious part of the retina has yet been identified for such a purpose. It is possible that variability in the degree of polarization of reflections is due to variability in the orientation of the guanine crystals that form the tapetum. Further work, using electron microscopic techniques, is required to establish whether this is the case.
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To conclude, it seems that, while the poorly focused secondary eyes of many spiders possess polarizing optics, with the notable exception of the gnaphosid Drassodes cupreus the overall structure in many cases suggests that they are not optimized for the analysis of polarized light. The roles of many of these secondary eyes remain enigmatic, with their polarizing optics only adding to the mystery.
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Concluding remarks |
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In lycosids, orthogonal receptors are tiered in two layers. This provides each axial pair of cells with a similar optical solution to that provided by compound optics, since the two analysers are now co-axial. Not only does this provide receptors in the two layers with a co-axial view of the sky, but the distal layer could potentially improve the polarization sensitivity of the proximal layer through its selective absorption of light orthogonal to its preferred direction (Snyder, 1973). The only problem with such a system is that, since the polarization sensitivity of distal receptors would not be perfect, they would also screen the receptors in the proximal layer, reducing their absolute sensitivity. Such screening effects could, in turn, be minimized by having very short receptive segments, which is exactly what we observe in the distal layer (Table1). In simple eyes with very low F-number optics, such as these, the absolute sensitivity of even short photoreceptors would still be very high (Land, 1985).
The gnaphosid spiders have come up with a slightly more drastic answer to the problem. By reducing the lens power of their polarization-sensitive eyes to a transparent window, individual photoreceptors will have almost as large a visual field as that of the whole eye. Coupled with an eye position that gives the two eyes completely overlapping visual fields, a reliable polarization analysis could then be obtained by opponent input summed across the left and right eye, which are oriented at 90° to one another. Such integration across the entire eye is possible because of the parallel arrangement of microvilli across the whole retina. However, a limitation to such a solution is that it will work only at dusk and dawn, when one single direction of polarization is present across the sky. Integration over the greater part of the sky during the day, when the polarization pattern is more complex, would only weaken the signal. Hence, for polarized light navigation during the day, the lycosid solution is superior.
Despite the remarkably diverse solutions to the detection of polarized light by the simple eyes of spiders, their use in orientation is known from only three families. While the morphological requirement for polarized light analysis exists in many more families, it is not known whether these spiders actually use their eyes for this purpose. With their unique webs, many spiders create an animated world full of other cues for orientation, and vision may play only a subordinate role that is hard to isolate.
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Acknowledgments |
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