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Photoresponses of the compound eye of the sandhopper Talitrus saltator (Crustacea, Amphipoda) in the ultraviolet-blue range.

Introduction

The sandhopper Talitrus saltator (Montague) is known to use clues from the sky for orientation irrespective of whether the sun is visible or not (Pardi and Papi, 1952, 1953; Ugolini et al., 1993, 1996, 2004). In particular, spectral-filtering experiments during celestial orientation have shown that sandhoppers perceive directional information important for zonal recovery, using wavelengths in the ultraviolet (UV)-blue range (Ugolini et al., 1993, 1996). Additionally, they can also use terrestrial landmarks (Ugolini et al., 1986, 2006), and it has recently been demonstrated that blue and green wavelengths are ecologically significant for individuals of T. saltator, since an artificial, colored landscape influences the direction of orientation--that is, their directions were dispersed widely around the direction of terrestrial cues (Ugolini et al., 2006).

Despite clear reports on the importance of vision in the orientation of sandhoppers, investigations on their visual capacity are not numerous and often have a preliminary character. Ercolini and Scapini (1976), by behavioral tests, assessed only a general preference for short wavelengths of the visible spectrum in T. saltator, without performing any test of visual perception in the UV range. Electrophysiological investigations in the past indicated sensitivity only in the blue range (450 nm), with a suggestion of sensitivity also in the green (Mezzetti and Scapini, 1995; Ugolini et al., 1996). An ability to perceive UV may be used for communication, in foraging for food, in navigation, and in mate selection; and it occurs widely in both vertebrates (with the exception of mammals) and invertebrates (Hunt et al., 2001; Johnson et al., 2002). Therefore, studies on spatial orientation must also take into account the perception of spectral cues and spectral sensitivities in the UV-blue region.

The aim of this paper is to investigate the existence of UV-blue photoresponses in the eyes of T. saltator, which has long been controversial. Two types of experiments were carried out: behavior-based responses (binary choice) and electrophysiological tests (elecroretinogram). In addition, the eye structure of T. saltator was clarified.

Materials and Methods

Adult individuals of Talitrus saltator (Montagu) were collected in the spring and summer of 2006 and 2007 on a sandy beach in southern Tuscany (42[degrees]46'N, 11[degrees]6'E; Albegna, Grosseto, Italy) and transported to the laboratory in plastic boxes containing wet sand. They were fed weekly with dry fish food placed on blotting paper. The animals were subjected to an artificial light:dark cycle corresponding in phase and duration to natural dawn and dusk. All experiments were performed during the day from 1000 to 1600 h.

Behavioral test

To assess whether sandhoppers are able to respond to UV light, behavioral trials were performed in the dark. The experimental apparatus (Fig. 1) consisted of a transparent plastic tube (length 60 cm, diameter 6.3 cm) placed horizontally. At one of the two extremities, an interference filter (360 nm, full-width-half-max: 35 nm, Andover Corporation, Salem, NH) was placed in a black cap: the only light transmitted in the tube was that transmitted by the filters, and the other side was protected to prevent entry of light. The emitting source was a Xenon lamp (lamp: XBO150W, Osram, Munich, Germany), with the beam collimated by a lens. To exclude any external influence on the sandhoppers' response, light was projected onto the animals from either end of the tube, alternating with each trial. A neutral-density filter was used to equalize the light irradiance of each beam. A power meter (receptor head PD300UV, Nova Display, Ophir Optronics) centered in the middle of the tube measured light irradiance, which in this experiment was 1.8 X [10.sup.13] quanta/[cm.sup.2]/s. For each release, 10-12 specimens were corralled in the container used to keep them in the laboratory and placed at the middle of the tube with the help of a transparent narrow acrylic plastic cylinder vertically inserted into the hole. Sandhoppers were thus prevented from escaping in any direction and were kept in dry conditions, in the dark. After 20 min, the UV beam was allowed to penetrate the tube from one end, and sandhoppers were released by the removal of the vertical cylinder. The numbers of specimens that fell into pitfall traps at the two ends of the corridor were counted 2 min after release. Data were statistically analyzed by a G test (Zar, 1984).

[FIGURE 1 OMITTED]

Electrophysiological recordings

The whole animal was used for the electrophysiological experiments. The head of the animal was glued to a stage and fixed using melted beeswax and resin (1:1). The rest of the body was covered by paper wet with filtered seawater, and covered again by dental wax to hold the body and to prevent its dehydration. The reference electrode, a chlorided silver wire, was placed into the head and the small wound was covered with beeswax. For electroretinogram (ERG) recordings, a glass electrode filled with seawater was introduced at the surface of the crystalline cone layer just below the cornea.

The end of the light guide was placed near the compound eye. Responses were amplified with a high-impedance preamplifier (Nihon Kohden MZ 8201) and a high-gain amplifier (Nihon Kohden AVH-10). The magnitude of the responses (peak amplitude) was monitored on an oscilloscope (Nihon Kohden VC10). Permanent recordings were made with a paper recorder (Graphtec Linearecorder FWR 3701).

A two-channel optical system was used, with a 500-W Xenon arc lamp (Ushio Inc., Type UXL-500D-O, Japan) with a regulated power supply (Sanso XD-25, Japan): one beam was for testing and the other for chromatic adaptation (Fig. 2). At each channel, quartz lenses produced a parallel beam of light, which passed through a heat-absorption filter (Toshiba IRA-25S), one of a set of 16 narrow-band interference color filters (Vacuum Optics Corp., Japan) for the testing light, and two different (380 nm or 580 nm) narrowband interference filters for the adapting light. The half bandwidths of all interference filters used both in behavioral tests and in electrophysiological recordings were about 15 nm. The light intensities of the testing and adapting lights were measured with a silicon photodiode (S876-1010BQ, Hamamatsu Photonics K.K.) calibrated by Hamamatsu Photonics K.K. using a photo-electron bulb, and each monochromatic light was adjusted with the aid of several neutral-density filters so that each contained an equal number of photons. At all wavelengths, the maximum irradiances available at the surface of the eye were 1.8 X [10.sup.14] quanta/[cm.sup.2]/s for testing, and 6.0 X [10.sup.14] quanta/[cm.sup.2]/s for chromatic adaptation. The light irradiance of the testing light was altered with quartz neutral-density filters (Vacuum Optics Corp., Japan) to obtain intensity-response curves. To get the spectral-response curves, the light irradiance of each testing light was 1.8 X [10.sup.13] quanta/[cm.sup.2]/s, which corresponds with 1 log unit lower than the maximum irradiance. The test and chromatic-adaptation beams were interrupted by shutters (Uniblitz photographic and Copal) controlled for the duration of the test flash and adaptation times by a stimulator (Nihon Kohden SEN-7103). The eye was stimulated by a 250-ms pulse of light, and the interstimulus interval was 30 s. Experiments were performed from 1000 to 1700 h during the day.

[FIGURE 2 OMITTED]

Morphological observations

Animals were kept for 30 min in the dark, and all fixation was performed under dim deep-red light (< 640 nm). The compound eye of T. saltator is sessile and was easily broken by the pressure from scissors or a scalpel when attempting to remove the eye from the body. Therefore, the head was first removed from the body with a small piece of razor blade dipped in a primary fixative solution (2.5% glutaraldehyde in 0.1 mol [l.sup.-1] sodium cacodylate buffer, pH 7.4). The separated heads were then immersed in primary fixative solution and placed in a refrigerator (4 [degrees]C) for 2 h, and rinsed in cacodylate buffer twice. The eyes isolated from the head under the microscope were post-fixed for 2 h with 1% [OsO.sub.4] in the same buffer. After being rinsed, the fixed eyes were dehydrated through a graded series of ethanol solutions, transferred to propylene oxide, and embedded in Epon 812.

For transmission electron microscopy, sections were cut with a Porter-Blum MT-2B microtome and picked up with 100-mesh copper grids. They were double-stained with 1% uranyl acetate and 0.1% lead citrate solution for 20 min and 30 min, respectively. Observations were performed using a JEOL JEM1220 transmission electron microscope.

For scanning electron microscopy, whole animals were prefixed overnight in 2% glutaraldehyde and 2% paraformaldehyde, buffered with 0.1 mol [1.sup.-1] sodium cacodylate buffer adjusted to pH 7.4. The specimens were then rinsed several times in 0.1 mol [1.sup.-1] sodium cacodylate buffer solution, postfixed for 2 h in 1% [OsO.sub.4] in phosphate-buffered saline (0.13 mol [1.sup.-1], pH 7.4) at room temperature, dehydrated through a graded series of ethanol solutions, and rinsed in 100% t-butyl alcohol three times at 37 [degrees]C. Next, the specimens were frozen at -20 [degrees]C and freeze-dried for several hours at 2 [degrees]C. The dried specimens were then coated with [OsO.sub.4] (Meiwa, Plasma multicoater PMC-5000) and observed with a scanning electron microscope (Hitachi, S-4800).

Results

Behavioral tests and electrophysiological recordings

Animals placed in the acrylic tube for 30 min in the dark moved around very actively at the center of the tube where they were caged (see Fig. 1). When irradiated with UV light, the sandhoppers displayed apparent phototaxis to the light. Three trials were performed using 35 released animals. Indeed, about 70% of the animals moved toward the UV light and about 30% to the dark; no specimens remained in the center of the tube. This result indicates that the animals were motivated enough in dry conditions to move to a brighter area and could detect and respond to the UV light (P < 0.001 G test).

The ERGs were recorded from the surface of the crystalline cones of the compound eyes after at least 30 min of dark adaptation. The response was an "on" negative potential consisting of an initial phasic component followed by a maintained or plateau component that lasted for the duration of the illumination. At low and intermediate levels of illumination for this spectral-response measurement, only the plateau component was recorded. The response height of the plateau component was measured. When irradiated by the highest light irradiance (1.8 X [10.sup.14] quanta/[cm.sup.2]/s), the response height was less than 1 mV. Under -2.0 log light irradiance, the signals of each response were at the limit for detection above noise level. Figure 3 shows the amplitude of the plateau component of the ERG plotted as a function of log irradiance of stimuli at different wavelengths. The slopes of these V-log I response functions vary with stimulus wavelength, suggesting the presence of different receptor types.

[FIGURE 3 OMITTED]

The spectral response curve (SR [[lambda]]) of dark-adapted compound eyes of T. saltator showed broad responses from UV (350 nm) to red (630 nm) (Fig. 4A, B). The maximum response was observed between 390 and 450 nm, and a secondary peak was observed at around 550 nm. To clarify the existence of different spectral receptor types, a selective light-adaptation experiment was performed. Monochromatic light, either 380 nm or 580 nm, irradiated the eyes for 3 min of initial light adaptation and then throughout the spectral response measurements. Ultraviolet-light adaptation produced a large decrease in sensitivity but did not isolate the different receptor types (Fig. 4A, uv), whereas yellow-light (580 nm)-adaptation experiments revealed an apparent sensitivity change at about the secondary sensitivity range (Fig. 4A, y). Each response was normalized to the highest response of the spectral response curve under dark conditions (Fig. 4B). Compared with the dark-adapted curve, ultraviolet-light adaptation showed a higher response above 450 nm, and the yellow-light adaptation showed a lower response in the same spectral range. The ratio of the UV response (average 350-410 nm) to green response (average 470-550 nm) was significantly different for UV-adapted (uv) and yellow-adapted (y) animals (Fig. 4D, P < 0.001, Mann-Whitney U test).

[FIGURE 4 OMITTED]

Morphological observations

The eyes of T. saltator are compound and sessile, occupying the dorsolateral region of the head. They are spherical, with a diameter of about 0.6 mm. When the eyes were observed with a dissection light-microscope, a black pseudopupil and a number of ommatidia could be observed (Fig. 5A). The ommatidia (the structural unit of the compound eye) form a hexagonal lattice (Fig. 5A, insertion). The ommatidial center-to-center distances were about 35 [micro]m. As reported in earlier studies (Meyer-Rochow, 1978; Mayrat, 1981), scanning microscopy revealed that the cornea itself was identical to that of other, similar species of amphipods (Fig. 5B)--that is, the entire compound eye was smoothly convex like a camera eye. No apparent borders between each ommatidium or between the compound eye and the head were observed. The cornea itself is about 15 [micro]m thick and consists of five layers (Fig. 5C). The crystalline cone, which is the product of two cells, lies directly below the cornea and is attached to the tip of the rhabdom of the retinula cells. In the dorsal regions of the eye, the length of the crystalline cone was about 60 [micro]m and the maximum diameter was 35 [micro]m just below the cornea (Fig. 5C).

[FIGURE 5 OMITTED]

The rhabdomeres are fused to each other to form a fused type of rhabdom that is observed in transverse section (Fig. 5D, E). The mean rhabdom length is 70 [micro]m in the central ommatidia, while the ommatidia at the edge of the eye are shorter. In each retinula cell, the microvilli composing the rhabdomere are oriented toward the center of the rhabdom. Each ommatidium contains four large retinula cells (R1-4) and one small (R5). Retinula cells 2 and 4 are located opposite each other and have a similar microvillar orientation; and cells 1 and 3 are similarly oriented but with their microvilli orthogonal to those of cells 2 and 4 (Fig. 5E). The rhabdomere of the fifth retinula cell is much smaller than those of the other four (only about 15% of the rhabdomal area in cross-section). Each retinula cell contains, in addition to the normal organelles, a large number of electron-dense pigment granules (mean diameter 0.4 [micro]m) surrounding the rhabdom (Fig. 5D, E).

Discussion

Since the ground-breaking report by Karl von Frisch (1967), many papers have focused on the homing behavior of social insects such as honeybees and ants, and showed that eyes are essential to detect a variety of environmental clues (Wehner, 1992). In addition to those findings on social insects, Hironaka et al. (2003) reported that the female of the subsocial shield bug, Parastrachia japonensis, loses directional orientation with respect to its foraging site when visual information is disturbed. It should be underlined that the ecological problem Talitrus saltator has to solve is to reach the goal represented by a belt of damp sand (i.e., no homing behavior). To do that, sandhoppers use visual clues for their orientation in order to follow the shortest path to return to the belt of damp sand on the beach. They can orient using the sun or skylight celestial cues when the sun is not visible (Pardi and Papi, 1953; Ugolini et al., 1993, 1996, 2004).

Spectral-filtering experiments carried out with the sun blocked, allowing only the vision of the sky, showed that T. saltator could orient when the "sky" was covered with filters of below 450 nm, indicating the possibility that T. saltator perceives the ultraviolet (UV)-blue range. However, no direct proof of real UV perception in sandhoppers had been demonstrated, even though UV perception has often been hypothesized in the past (Ugolini et al., 1993, 1996, 2004). The binary choice experiments clearly showed that T. saltator responds to UV light by photopositive behavior: UV light attracted about 70% of the experimental animals.

To verify the UV sensitivity demonstrated in the behavioral experiments, spectral responses were measured electrophysiologically. A broad peak was observed at about 390-450 nm, with a secondary peak observed at about 500-550 nm (the dark-adapted eye). UV-light adaptation produced a decrease in the total response, while yellow-light (580 nm) adaptation induced a diminishment of the secondary peak. Analyses following the methods of Cohen and Frank (2007) demonstrated that the ratio of the mean UV response to the mean green response was significantly different under conditions of UV adaptation versus yellow adaptation. These results strongly suggest the existence of at least two spectral cell types: a UV cell and a yellow cell. The spectral absorbance curves of the two different visual pigments peaked with one [alpha]-band at 510 nm and a [beta]-band at around 380 nm; and the other [alpha]-band at 380 nm as predicted by the template of Stavenga et al. (1993), as shown in Fig. 4C. The UV light might be absorbed both by the shorter wavelength peak ([beta]-band) of the yellow-absorbing visual pigment in the yellow cell and by the main peak ([alpha]-band) of the UV-absorbing visual pigment in the UV cell. Because UV light is absorbed by both these two different cells, the presence of two peaks in the dark-adapted spectral sensitivity curve measured as a whole by the ERG might be decreased under UV chromatic adaptation. The visual pigment with an [alpha]-band peaking in the UV region cannot absorb yellow light, so yellow-light adaptation caused the apparent change in the shape of the spectral-response curve.

If a retinula cell possesses a visual pigment, the absorption of the long wavelength quanta has the same effect on a receptor as the absorption of a short wavelength quanta (the principle of univariance; Naka and Rushton, 1966). Therefore, the slopes of the V-log I functions should be the same when measured at different wavelengths. The V-log I functions in the ERG measurements showed different slopes (Fig. 3)--that is, a lack of the principle of univariance--suggesting the existence of different receptor types. The narrow spectral-sensitivity curves were calculated only around each peak, using the light-adapted response curve and the V-log I function of the peak wavelength. These spectral-sensitivity curves, calculated using the mean values of spectral responses and the V-log I curves of each peak, are shown by dashed lines in Figure 4C. The dashed line "y" (adaptation to light of 580 nm) fits well to the [alpha]-band curve of the predicted UV-absorbing visual pigment. However, the dashed line "uv" (adaptation to ultraviolet light) possesses broader sensitivity in the longer wavelength region, suggesting the existence of other cells that respond at longer wavelengths (Fig. 4C).

These behavioral and electrophysiological experiments revealed the existence of UV perception in T. saltator. UV perception is well known in insects (e.g., see Wehner, 1992) and in some crustaceans such as the semi-terrestrial species Ligia (Hariyama et al., 1993) and tropical stomatopods (Marshall et al., 2007). However, this is the first report to clarify that T. saltator responds to UV light.

It should be noted that the ERG is a gross response from the whole eye, and that selective light-adaptation experiments may sometimes poorly separate different receptor types when the spectral regions of each receptor are close together. Because of this difficulty of receptor isolation, there is a possibility, especially in the broad peak between 390 nm and 450 nm, that other color receptors may exist (e.g., see the presence of intracerebral ocelli in T. saltator (Frelon-Raimond et al., 2001). Further study using intracellular recording or microspectrophotometry is needed to clarify all the spectral cell types.

Morphological observations show that T. saltator, like some other amphipods, possesses an undifferentiated cornea, a fused-type rhabdom attached to the crystalline cone, and five retinula cells in each ommatidium (Ball, 1977; Meyer-Rochow, 1978; Hallberg et al., 1980; Mayrat, 1981), including one small cell producing a rhabdomere and four other larger retinula cells (Ercolini, 1964). Because the crystalline cone directly abuts the rhabdom, the eye of T. saltator can be classified as an apposition compound eye. Investigations on eye structure and spectral sensitivity have been carried out in many arthropod species (e.g., see Goldsmith and Fernandez, 1968; Land, 1981; Frank and Widder, 1999; Meyer-Rochow, 1999; Osorio and Vorobyev, 2005), and some studies have shown that a relationship exists between the lens system and the light environment and that the two are related by some behavioral traits (Nilsson, 1983). Animals that possess superposition eyes live in dim environments or are active at night; whereas those with apposition eyes live in bright environments and are active during the day. However, recent studies show that some animals have evolved to be nocturnal despite their apposition eyes (Warrant, 2008). T. saltator is crepuscular and nocturnal (Geppetti and Tongiorgi, 1967a, b) and can orient both during the day and at night, using celestial cues such as the sun and the moon (Ugolini et al., 2007). The apposition eye in T. saltator seems to be suited for both diurnal and nocturnal vision. The results of release experiments carried out both under natural and artificial light indicated that the UV-blue region of the spectrum is important for T. saltator in order to select the ecologically relevant (sea or land) direction (Ugolini et al., 1993, 1996). Because UV sensitivity seems redundant at night (Lythgoe, 1979; White et al., 1994), these characteristics of the vision system of sand-hoppers seem better adapted for vision in daylight than in nocturnal light. It may therefore be that T. saltator, like the antarctic amphipod Orchomene plebs (Meyer-Rochow and Tiang, 1979) adapts its visual system to the light conditions.

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A. UGOLINI (1), G. BORGIOLI (1), G. GALANTI (1), L. MERCATELLI (2), AND T. HARIYAMA (3), *

(1) Dipartimento di Biologia Evoluzionistica, Universita di Firenze, Via Romana 17, 50143 Firenze, Italy;

(2) Istituto Nazionale di Ottica Applicata-CNR, Largo E. Fermi 6, 50143 Firenze, Italy; and (3) Department of Biology, Hamamatsu University School of Medicine, 1-20-1, Handayama, Higashi-ku, Hamamatsu 431-3192, Japan

Received 20 September 2009; accepted 31 May 2010.

* To whom correspondence should be addressed. E-mail: hariyama@hama-med.ac.jp
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Author:Ugolini, A.; Borgioli, G.; Galanti, G.; Mercatelli, L.; Hariyama, T.
Publication:The Biological Bulletin
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Date:Aug 1, 2010
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