Compound eye fine structure in Paralomis multispina Benedict, an anomuran half-crab from 1200 m depth (crustacea; decapoda; anomura).
Animals that live in or colonize greater oceanic depths face three major physical challenges (Marshall, 1957; Thorson, 1972): (a) atmospheric pressure increases by 1 with every 10 m of water; (b) ambient light levels become progressively reduced, and the spectral composition of the downwelling light changes as depth increases; and (c) the temperature of the water falls as the distance to the surface increases, except in the polar oceans (where bottom temperatures may actually lie a few degrees above those of the surface) and near hydrothermal vents.
The eyes of animals are usually attuned to the photic conditions under which they operate (Forward et al., 1988), but environmental temperature and pressure also influence certain structural and functional parameters of photoreception through their effects on membrane fatty acid content and composition (Cossins and Macdonald, 1989; Sebert et al., 1992; Kashiwagi et al., 1996). Based on a number of light microscopical (Beddard, 1890; Welsh and Chace, 1937, 1938; Zharkova, 1970, 1975; Bursey, 1975) and electron microscopical studies of deep-water crustacean eyes (Elofsson and Hallberg, 1977; Ball, 1977; Hallberg, 1977; Meyer-Rochow and Walsh, 1977, 1978; Hallberg et al., 1980; Gaten et al., 1992; Gaten, 1994; Nuckley et al., 1996), certain general trends concerning their anatomy and performance in relation to depth have become apparent.
Bath pelagic and benthic species of depths exceeding 1000 m usually exhibit small and degenerate eyes similar to those of species known from marine caves (Meyer-Rochow and Juberthie-Jupeau, 1987). Crustaceans inhabiting zones above 1000 m, on the other hand, frequently possess adaptations such as enlarged ommatidia, more voluminous rhabdoms, presence of retinal reflectors, etc., to improve the efficiency of photon capture. Often such adaptations enhance overall sensitivity at the expense of acuity, but in cases where acuity apparently suffers little degradation, regional eye modifications and special optical designs may be employed as, for instance, in the Euphausiaceae (Land et al., 1979; Hiller-Adams and Case, 1984). Most euphausiids, however, are luminescent and thus not necessarily representative of other groups of crustaceans. For that reason and the fact that few species of deep-sea crustaceans have had their photoreceptors studied, we decided to examine the eyes of the anomuran decapod half-crab Paralomis multispina from a depth of 1200 m and compare them with those of shallow-water anomurans investigated earlier (Eguchi et al., 1982; Meyer-Rochow et al., 1990; Gaten, 1994).
Materials and Methods
Several unsexed specimens of Paralomis multispina Benedict (Decapoda, Anomura, Galatheoidea) with carapace widths ranging from 5 to 11 cm and maximum body lengths (from head to tail) of 11.5 cm [ILLUSTRATION FOR FIGURE 1A OMITTED] were obtained in March 1992. Collections were made from the "Hatsushima seep" (Ohta et al., 1987) at a depth of 1200 m about 5 km off Hatsushima Island in Sagami Bay (Shizuoka Prefecture, Japan) during a cruise of the manned research submersible Shinkai 2000 (JAMS-TEC). The half-crabs themselves are not considered to be thermophilic, although they occurred in association with the giant clam Calyptogena soyae, vestimentiferan tube worms, gastropods, and polychaetes (Hashimoto et al., 1987) in an area that was characterized by an extremely high methane content. The half-crabs were picked up from the seafloor with remotely controlled artificial arms and put in a basket attached to the outside of the submersible. It took about 1 h for the submersible, with the collected animals, to reach the surface at about 1700 h.
During capture, the animals were exposed to 10,000-20,000 lux bright sunlight for about 20 min, but immediately after they had been hauled on board the mothership Natsushima, the compound eyes of three individuals were fixed for 12 h at 4 [degrees] C in 2% glutaraldehyde and 2% paraformaldehyde solution, buffered to a pH of 7.3 with 0.1 M cacodylate buffer. The dissections were carried out under dim red light to minimizer further exposure to light and structural damage (cf. Meyer-Rochow, 1994). After a brief wash in buffer, the specimens were postfixed for 2 h in 2% Os[O.sub.4] solution, using the same buffer as before, and dehydrated in a graded series of acetone before being embedded in Epon 812. Ultra-thin sections, cut with a diamond knife, were picked up on uncoated 200-mesh copper grids and stained with uranyl acetate and lead citrate for a few minutes. Observations were carried out under a JEM 1200EX transmission electron microscope, operated at 80 kV.
In their external appearance the compound eyes of the deep-sea anomuran Paralomis multispina [ILLUSTRATION FOR FIGURE 1B OMITTED] resemble those of other common anomuran shore-crabs (e.g., genus Petrolisthes: Eguchi et al., 1982; Meyer-Rochow et al., 1990), but overall the eyes are considerably larger. They are oval in outline and measure 3.5 x 2.5 mm in an individual of about 10 cm carapace width. Each eye sits at the tip of an eyestalk that is 4-5 mm thick and 12 mm long; thus inter-eye distances and the precise location of the eyes in space are to a certain extent variable. Ommatidial numbers increase with age: whereas a specimen with a carapace length of 5 cm has about 1500 facets, some 2400 were counted in a specimen with a carapace width of 10 cm.
Interommatidial angles apparently do not change significantly with age and measure about 3 [degrees] -5 [degrees] . Figure 2 provides a comparison between the ommatidia, shown in identical scale, of a shallow-water anomuran and the deep-water species Paralomis multispina. Biometrical data of the constituent parts of one representative central ommatidium of the compound eye of the two crustaceans are given in Table I. From Figure 2 and Table I it is evident that the ommatidium of the deep-sea half-crab is much larger than that of the shallow-water species, even if differences in body size are taken into consideration.
A single facet of the eye of Paralomis is about 3 times larger in diameter and has a corneal lens that is 1.8 times thicker than that of a comparable shallow-water Petrolisthes. No significant difference between the two types could be detected, however, in the 200 [[micro]meter] thick periodic layers, revealed in longitudinal sections of the cornea along the optic axis. Two corneagenous cells, not noticeably different from those of Petrolisthes or any other decapod crustacean, occupied the space between cornea and cone.
The crystalline cone of Paralomis tapered only very gently and retained a much wider proximal diameter [ILLUSTRATION FOR FIGURE 3A OMITTED] than that of Petrolisthes. Whereas in Petrolisthes, cross sections through distal and central regions of the cone displayed square profiles and a content of electron-dense material, sections through the cone of Paralomis at corresponding levels exhibited rather circular outlines and a content of much looser consistency [ILLUSTRATION FOR FIGURE 3B OMITTED]. When related to overall ommatidial length, the dioptric apparatus in the eye of Paralomis (though greatly enlarged in diameter) occupied significantly less space than the equivalent structure in the eye of the shallow-water Petrolisthes.
Retinula and rhabdom
In the eyes of other anomuran species - for example, Petrolisthes spp. (Eguchi et al., 1982; Meyer-Rochow et al., 1990) and Munida spp. (Bursey, 1975; Gaten, 1994) - a distal retinula cell (R8) with four cytoplasmic lobes occupies the tier between the crystalline cone and the seven regular retinular cells, but in Paralomis an ommatidial retinula is composed of only seven regular cells (1-7) and lacks the distal eighth cell. The distal end of the rhabdom is thus made up of seven regular retinula cells, which are in contact with the proximal end of the crystalline cone. It is in this region that the mottled retinula cell nuclei, with a maximum diameter of 7.5 [[micro]meter], can be found.
The rhabdoms in Paralomis are extraordinarily well developed and occupy up to 85% of the available cytoplasmic space in the distal and central regions of the retinula [ILLUSTRATION FOR FIGURE 4 OMITTED]. The estimated membrane surface of an ommatidial rhabdom of Paralomis (231 x [10.sup.4]), calculated [TABULAR DATA FOR TABLE I OMITTED] from the data in Table I, is about 27 times larger than that of Petrolisthes (8.5 x [10.sup.4]). Another comparison could be made with Limulus, which - even though it is not a crustacean - has a compound eye (Fahrenbach, 1969) superficially similar to that of Paralomis, but with rhabdom occupation ratios generally lower than 10%. On the other hand, the hydrothermal vent shrimp Rimicaris exoculata occurs in a habitat similar to that of Paralomis, but its eye is highly aberrant, with volume densities of rhabdoms reaching 70%-80% (O'Neill et al., 1995). The retinula cells do not form proper rhabdoms in the proximal region; instead they gradually turn into slender axonal processes [ILLUSTRATION FOR FIGURE 5 OMITTED].
Longitudinal sections reveal that the regular "bands," so typical for the rhabdoms of other decapods (including those of the shallow-water anomuran species), are almost lost in Paralomis and are replaced by microvilli running in many directions. This gives the rhabdom a somewhat irregular, disorderly appearance. Individual microvilli in Paralomis [ILLUSTRATION FOR FIGURE 6 OMITTED] were thicker (0.11 [[micro]meter]) than those of fully grown shallow-water Petrolisthes (0.08 [[micro]meter]: Eguchi et al., 1982; Meyer-Rochow and Reid, 1996). This difference has to be interpreted with caution, since it is known from other crustacean eyes (e.g., Orchomene sp.: Meyer-Rochow, 1981; Mysis relicta: Lindstrom et al., 1988) that rhabdom microvilli have a tendency to swell and increase in diameter when suddenly exposed to very bright light.
A core-filament, usually identifiable in the lumen of a single rhabdom microvillus of the crustacean eye, was mostly lost or fragmented into smaller pieces [ILLUSTRATION FOR FIGURE 7 OMITTED]. Some of the rhabdom microvilli exhibited flattened or swollen structures in the place where core-filaments with their associated side-arms should have been. Since core-filaments and their associated side-arms in compound eyes are fragile and easily destroyed by irradiation with bright light (Blest et al., 1982; Tsukita et al., 1988), their disruption in our material could stem from the brief exposure to sunlight during capture.
The eye of Paralomis lacks secondary pigment cells; two primary pigment cells are found around the crystalline cones and contain spherical electron-opaque pigment grains of about 0.4 [[micro]meter] in diameter [ILLUSTRATION FOR FIGURE 3A OMITTED]. The density of these granules seems not to differ from that of granules in the shallow-water half-crabs, but screening pigment granules in the retinula cells are far less numerous in Paralomis. In place of secondary pigment cells are an unknown number of cells presumed to contain reflecting granules.
The distance between the proximal end of the rhabdom and the basement membrane of an ommatidium is relatively short in Petrolisthes and other shallow-water decapods. In Paralomis, however, this same distance is strikingly long (ca. 180 [[micro]meter]). In the proximal layer, the retinula cells become slender as shown in Figure 5. The space thus made available is filled with enormously developed cells containing large amounts of reflecting pigments. The extensions of the reflecting pigment cells, which are easily identifiable by their innumerable 0.3[[micro]meter]-wide vesicles, penetrate between the retinula cells of individual ommatidial units, thus apparently increasing their effectiveness in reflecting light towards the more distally placed rhabdom.
Eguchi et al. (1982) suggested that anomuran half-crabs of the superfamily Galatheoidea possess reflecting superposition eyes. Research by Meyer-Rochow et al. (1990) on the galatheid Petrolisthes elongatus and by Gaten (1994) on Munida rugosa lent further support to this notion, but specified that this was true only for the dark-adapted eye; in the light-adapted state apposition optics were used. It is generally assumed that superposition eyes are more useful than apposition eyes in dim light, for the former are typical of many nocturnal crustaceans and deep-sea forms.
It is, therefore, a little surprising to find that the eye of the deep-sea anomuran galatheid Paralomis multispina (a) lacks a wide clear-zone, which is normally considered a prerequisite for any form of superposition vision (Land, 1981), and (b) possesses roundish rather than regular, square cones, which are an essential requirement for reflecting superposition (Land, 1976; Vogt, 1980). The species does, however, exhibit other kinds of modifications that are more in keeping with adaptations to an extremely dim environment: compared with the shallow-water half-crabs of the genus Petrolisthes (Eguchi et al., 1982; Meyer-Rochow et al., 1990), in Paralomis the corneal diameter is three times greater, and cone as well as rhabdom diameters are even more enlarged (Table I). The reflecting tapetum on the proximal side of the retinula is massively developed, and it is evident that the eye is designed to maximize photon capture. The fine-structural disruptions and larger diameters of the rhabdom microvilli seen in Paralomis are almost identical to those reported from the eyes of deep-water amphipods from the Antarctic (Meyer-Rochow, 1981) and are most likely caused by the exposure to bright light during capture. Indirectly the disruptions thus point to a high absolute sensitivity to light, but at the same time they obscure signs for or against membrane shedding (cf. Chamberlain and Barlow, 1984).
On the basis of the definition that Land (1981) provided for "absolute sensitivity," we calculated sensitivities of light-adapted eyes of Paralomis and those of shallow-water Petrolisthes: the eye of Paralomis was 150 times more sensitive. The comparison is based on the assumptions that the extinction coefficient (k) is the same for the two species and that the types and densities of pigments found in the rhabdoms are identical (cf. discussion in Ziedins and Meyer-Rochow, 1990). If one assumes a superior photopigment content in the dark-adapted Paralomis eye and considers thermal noise reduction at low environmental temperatures (Aho et al., 1988), the overall sensitivity advantage of Paralomis over Petrolisthes to extended light sources may be even higher.
If the lack of a clear-zone is real and not artifactual (clear-zones in the superposition eyes of deep-sea decapods can easily collapse and, on account of their fragility and delicateness, may remain undetected as shown by Nilsson, 1990), the closer approximation of the massively developed rhabdom to the much wider dioptric elements, in combination with the backing of a tapetum from behind, could be interpreted as an adaptation to improve sensitivity, especially to point sources. The shortening of both cornea and cone, relative to the overall length of one ommatidium, and the loss of the orderly arrangement of microvilli in the rhabdom also point toward an adaptation to minimize photon loss and maximize photon capture (Laughlin et al., 1975). The considerably greater rhabdom-occupation ratio in the eye of Paralomis as compared with the shallow-water species not only allows more photopigment molecules to be packed into the visual membranes, but also indicates low energy demand and slow cellular metabolism, both adaptations that are extremely useful in the deep-sea environment (Elofsson and Hallberg, 1977).
In the shallow-water Petrolisthes elongatus the eye enlarges as the half-crab grows; ommatidia are added and sensitivity to both extended and point sources increases. P. elongatus uses vision to detect and approach hiding places (Meyer-Rochow and Meha, 1994). Since signs of eye regression in adult Paralomis are missing, we must assume that the general growth pattern resembles that of Petrolisthes. This, however, raises the question of what Paralomis could possibly see at a depth of 1200 m, the "limit" beyond which sunlight can no longer be detected (Clarke and Kelly, 1964). Biological light sources, however, abound at this depth (Omori, 1974), and it may well be in the interest of a benthic, sedentary detritus and filter feeder to notice them. Any visual signal adult Paralomis could possibly be interested in would almost never come from below, and this could explain the lack of regional eye specializations seen in so many mesopelagic shrimps (Gaten et al., 1992).
We know nothing about the spectral sensitivity of Paralomis, but the visual pigments of eight other anomuran species all exhibit a single absorption peak in the bluegreen region of the spectrum (Cronin and Forward, 1988). Ziedins and Meyer-Rochow (1990) electrophysiologically measured spectral sensitivity peaks of dark-and light-adapted eyes of P. elongatus and also found them to lie in the bluegreen part of the spectrum. Since even the eyes of the hydrothermal vent species Rimicaris exoculata, which are strongly modified morphologically (O'Neill et al., 1995), possess a sensitivity peak in the bluegreen (Johnson et al., 1995), we do not expect the eyes of Paralomis to differ in this respect. However, the lack of secondary screening pigments and retinula cell 8 in Paralomis suggests that the eye of M. rugosa, for example, is less well adapted to the greatest depth of its range (shallow water down to 1250 m: Gaten, 1994) than that of Paralomis. M. rugosa appears to be a relative "newcomer" to the deep-sea, while Paralomis has been exploiting that habitat for a longer evolutionary period. How much longer is hard to say, but Nuckley et al. (1996) speculate that a hydrothermal vent shrimp with modified eyes may have "migrated from the surface possibly in the last 5,000-10,000 years" and over that period evolved its present eye morphology.
In conclusion, the hypertrophied rhabdoms in the eye of Paralomis, the loss of the orderly microvillus arrangement, the reduction of the cytoplasmic component of the retinula cells, the massively developed layer of reflecting vesicles in the proximal half of the retinula, and (considering overall ommatidial length) the relative shortening of the dioptric elements coincident with greatly enlarged diameters in the eye of Paralomis are all consistent with depth-related adaptations seen also in the eyes of deep-sea mysids (Elofsson and Hallberg, 1977), amphipods (Hallberg et al., 1980; Meyer-Rochow et al., 1991), and to some extent other benthic decapods (Hiller-Adams and Case, 1985) and mesopelagic shrimps (Gaten et al., 1992). However, the eyes of deep-water euphausiids (Hiller-Adams and Case, 1988) are least similar to those of Paralomis and this, we believe, has to do with (a) the widespread ability of euphausiids to produce light, (b) the greater mobility and pelagic lifestyles of euphausiids, and (c) the longer evolutionary period euphausiids have had to adapt their photoreceptors to the deep-sea environment.
We thank the Shinkai 2000 operation team and the Japan Marine Science and Technology Center (JAMSTEC) (Natsushimacho, Yokosuka, Japan) for their kind offer to assist in the procurement of the material. We also wish to acknowledge that through the constructive criticism of two anonymous referees we were able to improve the paper.
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