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Retinal anatomy of a new species of bresiliid shrimp from a hydrothermal vent field on the Mid-Atlantic Ridge.


In 1977, hydrothermal vents were first directly observed on the ocean floor along the Galapagos Ridge (Corliss et al., 1979). Additional active hydrothermal fields were discovered along spreading centers and back-arc basins in the Pacific and along the Mid-Atlantic Ridge (see Tunnicliffe, 1992, for a review). In 1986, the first two hydrothermal vent sites on the Mid-Atlantic Ridge (TAG Site and Snake Pit Site, Rona et al., 1986) were visited with the deep submergence vehicle (DSV) Alvin. Two more active vent fields (Lucky Strike Site and Broken Spur Site) were first visited with DSV Alvin during R/V Atlantis H cruise 129 in the early summer of 1993. Figure 1 shows the location of these four hydrothermal vent fields. More sites are likely to be discovered as exploration of the Mid-Atlantic Ridge continues.

Unlike the Pacific vents, where vestiform tube worms and bivalves dominate the biota, Mid-Atlantic Ridge vents have major populations of bresiliid shrimp, including many new species. Two of these species, Rimicaris exoculata (Williams and Rona, 1986) and Rimicaris sp., live in massive swarms on the sides of black smoker chimneys. Both species have large white structures on the anterior part of their dorsal surfaces, and in R. exoculata this structure has been shown to be an eye (Van Dover et al., 1989; O'Neill et al., 1995).

The discovery of an unusual and large eye on a hydrothermal vent species which lives 3500 to 3700 m below the ocean surface implies a heretofore unrecognized source of light. Previous to the discovery of the dorsal eye of R. exoculata, everyone assumed that, since no light reached hydrothermal vent fields from the surface, animals there lived in complete darkness (e.g., Tunnicliffe, 1992). Pelli and Chamberlain (1989) calculated that R. exoculata ought to be able to detect black-body radiation from the tops of the black smoker chimneys that are gushing 350 [degrees] C vent water. The light emitted from the tops of black smokers has now been photographed, although the mechanism by which it is produced is still uncertain (Van Dover et al., 1994).

We undertook R/V Atlantis II cruise 129-7 in May 1993 to investigate vision in hydrothermal vent shrimp more thoroughly. During the cruise, we realized that the small orange bresiliid shrimp we were collecting from the Snake Pit Site was very likely a distinct species. Individual live specimens survived well at the surface for many days, and, as a result, we achieved preliminary electrophysiological investigations of nerve fiber responses from the antennal nerves to tactile and chemosensory stimuli (Renninger et al., 1994, 1995). Here we present the structure and ultrastructure of the dorsal eye of the new, unnamed orange Rimicaris species from the Snake Pit Site. Two abstracts that mention this work have appeared (Chamberlain et al., 1994a,b).

Materials and Methods


Specimens of Rimicaris sp. for morphological study were collected on R/V Atlantis II cruise 129-7 during DSV Alvin dives #2613, #2618, and #2623 at the Snake Pit Site. The shrimp were collected with one of Alvin's mechanical arms, which sucked shrimp into a transparent chamber with a hose connected to a hydraulic pump. Specimens were brought to the surface and some were immediately dissected and fixed for morphological study while others remained alive in 10 [degrees] C seawater for over 2 weeks for electrophysiological investigations. Live animals were examined and compared with other vent shrimp with a Nikon SMZ-10 (Garden City, New York) stereomicroscope.

Fixation and histology

Under conditions of ambient light on board the R/V Atlantis II, live animals were coarsely chopped and fixed by immersion in a solution of 0.8% glutaraldehyde, 5% paraformaldehyde, 4.5% sucrose, and 3% NaCl in 0.1 M Sorensen's phosphate buffer at pH = 7.2. After 18 h at 4 [degrees] C in darkness, the central compartment of the dorsal carapace between the gills was dissected free from the anterior margin posteriorly to include both wings of the dorsal eye. The tissue was then washed in phosphate buffer with 8% sucrose and postfixed with 1% Os[O.sub.4] in phosphate buffer with 8% sucrose for 1 h at room temperature. Thereafter, it was rinsed in distilled water and dehydrated through a graded ethanol series to absolute ethanol. Finally, the tissue was transferred to propylene oxide, infiltrated with a series of propylene oxide/epoxy resin mixtures, rotated overnight in pure epoxy resin, and embedded in Epon-Araldite blocks for light and electron microscopy. For a discussion of alternate collection and fixation strategies see O'Neill et al. (1995).

The embedded tissue was taken to Syracuse University where serial 1-[[micro]meter] sections and selected gold and silver thin sections were cut using glass knives and a Sorvall MT2-B ultramicrotome (Dupont-Sorvall, Newtown, Connecticut). Sections were cut either in a plane tangential to the surface of one wing of the eye or in a plane perpendicular to that surface.

The 1-[[micro]meter] sections were stained with 1% toluidine blue saturated with [Li.sub.2]C[O.sub.3] for high resolution light microscopy with a Nikon Biophot or Optiphot microscope. Thin sections were collected on naked copper mesh grids and stained with uranyl acetate and lead citrate before being observed with a JEOL JEM-100CX II transmission electron microscope at the Department of Anatomy and Cell Biology, SUNY, Health Science Center, Syracuse.


Quantitative measurements from light and electron micrographs were used to determine the entrance aperture of the eye, the number of ommatidia, the volume density of the rhabdom, and the area of microvillar membrane per unit volume of rhabdom. The total surface area of the retina was determined from 1-[[micro]meter] sections. The average area occupied by an individual ommatidium was then measured and the number of ommatidia calculated from the total retinal area. The volume density of the rhabdom was determined from high magnification light micrographs using point-counting stereology. The average dimensions of the microvilli were determined from electron micrographs and the surface area of membrane per unit volume of microvillar array was then calculated assuming hexagonal close packing of the microvilli.



The small orange shrimp aggregates in swarms of hundreds, probably thousands of individuals on the sides of black smoker chimneys at the Beehive Mound of the Snake Pit Site at a depth of 3500 meters. Figure 2A shows a group of orange Rimicaris sp. above a mass of grey R. exoculata. Swarms of Rimicaris sp. consistently occupy particular regions of the environment and reestablish their position after they are disturbed by Alvin's collection activities. Temperature measurements suggest that Rimicaris sp. prefers an average ambient temperature of about 10 [degrees] C compared to a higher average ambient temperature of 28 [degrees] C preferred by R. exoculata (C. L. Van Dover, pers. comm.). Compared to R. exoculata, Rimicaris sp. individuals move less actively within their swarm and are only very rarely seen swimming singly in the water column.

Gross anatomy

Figure 2B shows a frame from a dive videotape of a group of Rimicaris sp. The bright white dorsal eye is clearly visible on each animal. This species lacks R. exoculata's characteristic bulged gill coverings and is more cylindrical. Figure 2C shows a picture of a single live animal perched on a piece of sulfide chimney wall in an aquarium on board the R/V Atlantis H several days after it was collected. In a living animal, the dorsal eye appears as a distinctive white structure with two wings beneath the transparent colorless cornea. The bilaterally symmetric pair of rounded wings is joined anteriorly across the mid-line by a thin cylindrical strand. Subsequent dissection and sectioning revealed that each of the wings has a ventral extension along its lateral edge that increases the size of the retina. Unlike those of shallow-water shrimp, the eyes are not stalked, but lie under the anterior and dorsal carapace. There are no compound eyes in Rimicaris sp.

Stereomicroscopic examination of a wing of the dorsal eye through the pellucid cornea of a living animal reveals a roughly polygonal, hexagonal honeycomb with pale pinkish-purple transparent ommatidia separated by white partitions. The partitions have ruffles along the top edge next to the cornea. Away from the cornea, the partitions close off each compartment with a textured surface that resembles the bottom of a lobed gelatin mold. Where the lobes meet in the center there is a ring of tiny holes formed by the axons from the individual photoreceptors passing through the bottom of each compartment in the honeycomb. Counting either the lobes or the number of holes in the ring shows that most ommatidia have seven photoreceptors, although a few have six, or even five, photoreceptors. Dissecting the eye of a live animal reveals that the inner surface of the white retinal matrix is lined with scattered aggregations of brownish-purple pigment. The colorless photoreceptor axons leaving the inner surface of the retinal wing on each side funnel ventrally toward the brain like the bristles of a bilateral pair of brooms. Each broom connects to one of a pair of dorsal visual neuropils that sit laterally on the brain.


Figure 3A shows a 1-[[micro]meter] section stained with toluidine blue cut through a wing of the dorsal eye tangential to the cornea where it overlies the center of the wing. The circumference of cornea and corneal epidermis surrounds darkly stained, light-sensitive rhabdom. Figure 3B shows a higher magnification view of the central region of Figure 3A. The rhabdomeral segments (R-segments) of the photoreceptors of each ommatidium cannot be individually distinguished as they contribute to the large volume of rhabdom. Thin partitions of white diffusing cells separate the ommatidia. Figure 3C shows a higher magnification view of the cornea, corneal epidermis, and underlying rhabdom. The cornea is smooth without evidence of any of the dioptric apparatus typical of an invertebrate compound eye. The corneal epidermis is separated from the layer of photoreceptors by a thin space filled with blood that occasionally contains hemocytes (Hose et al., 1990). There are no cells that correspond to cone cells in shallow-water shrimp.

The average cross-sectional area of the R-segments of an individual ommatidium (e.g., from Fig. 2B) and the total surface area of one half of the bilateral eye were used, in one animal, to estimate that each half of the eye contains between 3200 and 3400 ommatidia. In calculating the surface area of the eye, the ventral extensions on the lateral edges of the wings of the retina were included. From measurements of two 1-[[micro]meter] sections through the arrayed R-segments, we found that the rhabdom occupies between 80% and 85% of the total volume of the zone formed by the R-segments.

Figure 4 shows a section through the retina perpendicular to the corneal surface. The prominent blocky R-segments are separated and underlain by a layer of white diffusing cells. The ventral regions of the R-segment cytoplasm consistently contain small clusters of lipid droplets. The scattered nuclei of the white diffusing cells are angular in contrast with the more rounded photoreceptor nuclei that form a layer along the inner edge of the white diffusing cells. Below the zone of photoreceptor nuclei is a band of screening pigment, both in pigment cells and in the axons of photoreceptors. The pigment cells are uniformly ovoid with a range of pigment concentrations from very light grey to opaque black in toluidine blue-stained plastic sections. The arhabdomeral segment (A-segment) of the photoreceptor (analogous to the inner segment of a vertebrate photoreceptor) consists of a thin cylindrical strand that connects the base of the R-segment with the nucleus and, after swelling around the nucleus, continues as the axon. Granules of screening pigment in the photoreceptor axons are uniformly black and form elongated and striated arrays depending upon the plane of section.


Figure 5 shows the microvillar organization of the rhabdom. Most of the R-segment is occupied by geometrically ordered arrays of microvilli, and only a small volume is dedicated to the R-segment cytoplasm. The cylindrical microvilli are roughly hexagonally packed [ILLUSTRATION FOR FIGURE 5 OMITTED] and average only 0.09 [[micro]meter] in diameter with an average length of about 2.35 [[micro]meter]. The array provides about 40.3 [[[micro]meter].sup.2] of photosensitive membrane per 1 [[[micro]meter].sup.3] of rhabdom. The R-segment cytoplasm contains smooth endoplasmic reticulum, scattered mitochondria [ILLUSTRATION FOR FIGURE 5 OMITTED], and clusters of lipid droplets along the base of the R-segment [ILLUSTRATION FOR FIGURE 6A OMITTED]. The A-segment cytoplasm is relatively devoid of organelles except for the nucleus and a thin surrounding perikaryon [ILLUSTRATION FOR FIGURE 6B,C OMITTED] that contains mitochondria, but little else. Screening pigment granules are scattered in the cytoplasm of the axon below the photoreceptor nucleus. No structures typically associated with membrane shedding, such as lamellar bodies or multivesicular bodies, are found anywhere in the photoreceptor cytoplasm, nor are they found in the surrounding white diffusing cells.

The white diffusing cells have a complex shape with many long, thin branches. Sections show many small profiles with round vesicles in lucent cytoplasm. The white cell nucleus is prominently lobulated with distinct agglomerations of chromatin [ILLUSTRATION FOR FIGURE 6A OMITTED]. Screening pigment cells are elliptical with cytoplasm replete with pigment granules and lobulated nuclei with aggregated chromatin.


Figure 7 is a summary drawing of the anatomy of the large dorsal eye of the bresiliid shrimp, Rimicaris sp. The paired wings are connected anteriorly by a thin strand that crosses the midline [ILLUSTRATION FOR FIGURE 7B OMITTED]. The wings themselves have both a dorsal and lateral portion [ILLUSTRATION FOR FIGURE 7C OMITTED]. The retina underlies a smooth, transparent cornea devoid of any dioptrics. The massive array of photosensitive membrane in the mosaic of photoreceptor R-segments sits on top of a layer of white diffusing cells that presumably reflect any light that is not absorbed in the first pass through the rhabdom back into the rhabdom [ILLUSTRATION FOR FIGURE 7D OMITTED]. Beneath this matte reflecting layer is a zone of screening pigment. Thin strands of photoreceptor A-segments penetrate the white diffusing cell layer to swell around the photoreceptor nuclei and continue toward the brain as photoreceptor axons.


Comparison of Rimicaris sp. with R. exoculata

Rimicaris sp. and R. exoculata differ in several ways. The first species is bright reddish orange, and the second is ivory when freshly molted, turning gray and then black as sulfide particles build up in the gills, and finally brown as the sulfide particles oxidize. Rimicaris sp. lacks the lateral enlargement of the gill coverings so characteristic of R. exoculata, and the difference in shape becomes very clear when same-sized individuals of the two species are placed side by side. The largest Rimicaris sp. individuals we have observed are about 3 cm in length, but individuals of R. exoculata are commonly 6 cm long or longer. Finally, Rimicaris sp. clusters in regions with ambient temperatures of about 10 [degrees] C, sits relatively quietly in these clusters, and is rarely seen swimming in the water column. In contrast, R. exoculata prefers regions with warmer ambient temperatures of 28 [degrees] to 30 [degrees] C, is more active within its clusters, and is commonly seen swimming in the water column and exploring areas remote from the clusters.

Comparison of the primary visual organs shows that they have a common basic design, but differ in details. The position of the eye is similar in the two species, but the wings of Rimicaris sp. are nearly round whereas those of R. exoculata are elongated. Both eyes are fused across the midline anteriorly with slight ventral projections of the anterior margins; however, Rimicaris sp. has corneal bulges in the expected positions for compound eyes, whereas R. exoculata lacks any external remnant of anterior compound eye structures. The number and hexagonal packing of the ommatidia are similar, but the R-segments of each ommatidium of R. exoculata are elongated while those of Rimicaris sp. are nearly equant. The microvilli in the rhabdom of Rimicaris sp. are markedly smaller in diameter than those of R. exoculata (0.09 [[micro]meter] versus 0.15 [[micro]meter]). This leads to a greater concentration of photosensitive membrane in the rhabdom (40.3 [[[micro]meter].sup.2]/[[[micro]meter].sup.3] versus 24.18 [[[micro]meter].sup.2]/[[[micro]meter].sup.3]) which may compensate for the smaller overall size of the Rimicaris sp. eye (10 [mm.sup.2] versus 27 [mm.sup.2]). The clusters of lipid droplets present in the cytoplasm of the Rimicaris sp. photoreceptors are entirely absent from the photoreceptors of R. exoculata. Rimicaris sp. lacks any retinal cell type that could correspond to the cone cells that form the dioptrics of shallow-water shrimp, whereas the corneal epidermis of R. exoculata includes a minority cell type that appears to be an underdeveloped cone cell. The adaptation of the white diffusing cells, the attenuation of the A-segment, and the migration of the pigment granules in the photoreceptors and the pigment cells to the inner margin of the retina are shared features of the two species.

We conclude that Rimicaris exoculata and Rimicaris sp. are closely related, but distinct, species that have adapted for life in an unusual, low-light environment with similar modifications to their eyes. Both have enlarged, dorsal eyes that are similar in overall plan, but different in detail.

Comparison of Rimicaris sp. with Palaemonetes

We suggest that Rimicaris sp. is an evolutionary adaptation of a species of caridean shrimp that migrated from the surface at some time in the past, possibly in the last 5000 to 10,000 years - the typical lifetime of a hydrothermal vent field. This idea arises from the observation that three of the four vent fields on the Mid-Atlantic Ridge have different majority shrimp populations and seem not to share many species in common. It may, therefore, be interesting to compare the structure of the Rimicaris sp. eye with that of shallow-water species such as Palaemonetes pugio (Itaya, 1976; Doughtie and Rao, 1984) or P. vulgaris from which it may have evolved, perhaps through many intermediates.

We estimate that each wing of the eye of Rimicaris sp. contains 3200 to 3400 ommatidia. This compares favorably with the 3600 [+ or -] 300 ommatidia reported for the eye of P. pugio or the 2800 ommatidia we estimated for the eye of P. vulgaris. The overall entrance aperture for one wing is nearly planar and about 5 [mm.sup.2] in Rimicaris sp. and spherical and about 5.6 [mm.sup.2] in P. vulgaris. When the retina is considered as a slab of tissue, the rhabdom comprises about 10% of the volume at the level of the R-segments in P. pugio and 13% in P. vulgaris. The corresponding volume density of rhabdom in Rimicaris sp. ranges from 80% to 85%.

The geometrically arranged dioptric apparatus of Palaemonetes [ILLUSTRATION FOR FIGURES 8A, AND 9 OMITTED] has been replaced in Rimicaris sp. by a smooth cornea [ILLUSTRATION FOR FIGURE 3A, C OMITTED] lined by a corneal epidermis without the cone cells that form the quadripartite dioptrics in Palaemonetes. The distal pigment cells in Palaemonetes that contain opaque screening pigment granules are probably represented by the ellipsoidal pigment cells along the inner surface of the retina in [TABULAR DATA FOR TABLE I OMITTED] Rimicaris sp. The reflecting pigment cells, which in Palaemonetes are filled with vesicles, are probably represented by the elaborated white diffusing cells in Rimicaris sp. The screening pigment granules in the photo-receptors that migrate between the axons and the R-segment in response to light and darkness in Palaemonetes are reduced in number in Rimicaris sp. and seem to be restricted to the axons and the A-segment below the nucleus. The geometrical, interleaved arrangement of microvilli from the rhabdomeres of individual photoreceptors in Palaemonetes [ILLUSTRATION FOR FIGURE 8B, C OMITTED] is replaced by a much larger, but less geometrical rhabdom in Rimicaris sp. Table I compares the classes of retinal cells of Palaemonetes and Rimicaris sp.

The suggested evolution of the stalked eyes of Palaemonetes into the dorsal eye of Rimicaris sp. can be summarized as follows (compare Figs. 7 and 9). The dioptric apparatus is gone. Although the number of ommatidia is unchanged, each is larger so that the volume of the eye is increased. The sensitivity of the retina is likely further enhanced by a sevenfold to eightfold increase in the volume density of photosensitive membrane in the rhabdomeres of the R-segments. Screening pigment granules have been removed from the light path between the cornea and the rhabdom and have been decreased in number and prominence. The array of white diffusing cells with high albedo that increases the quantum catch by back scattering light into the photoreceptors has been markedly increased compared to the reflecting pigment cells in Palaemonetes. Taken together, these adaptations represent a significant attempt to maximize quantum catch at the cost of a loss of imaging capabilities. The eye is no longer an organ for pattern vision, but has become a very sensitive light detector. These structural adaptations are consistent with those observed in three species of deep-water mysid crustaceans by Elofsson and Hallberg (1977).

The structural changes observed in the retina of Rimicaris sp. might be expected in an animal that is adapting to a dim-light environment (e.g., Lythgoe, 1979) and are consistent with the changes we have observed in other hydrothermal vent shrimp. In general, an animal's eye continues to enlarge as the environment becomes dimmer and dimmer until the "quit point" is reached where exploitation of light in the environment becomes impossible (Lythgoe, 1979). In animals that adapt to the darkness beyond the quit point, the eye shrinks or disappears altogether. The eyes of the bresiliid shrimp that live on the sides of black smoker chimneys at sites along the Mid-Atlantic Ridge have all enlarged (Chamberlain et al., 1994a,b; O'Neill et al., 1995); however the eye of the predator Alvinocaris markensis, which lives at the base of these chimneys, seems to be in the process of evolving past the quit point (Wharton et al., unpub. data).

Adaptation for vision at hydrothermal vents

Does any light reach this hydrothermal vent environment from the surface? Clarke and Denton (1962) estimated that in the very clearest seawater, fish ought to be able to detect daylight to a depth of 1000 m. Clarke and Kelly (1964) measured light penetration in the Indian Ocean and concluded that the greatest depth for vision might vary between 700 m and 1300 m. This is the very range of depths that separates the twilight zone inhabited by mesopelagic fauna with well-developed eyes from the dark zone inhabited by bathypelagic fauna that usually have regressed eyes. Foxton (1970) reported that a typical faunal break for decapod crustaceans occurred between 650 m and 700 m. Kampa (1970) reported that at this depth in the North Atlantic, the light energy from the surface is about [10.sup.-6] [[micro]watt] [cm.sup.-2] [nm.sup.-1] at 480 nm. In any case, at a depth of 3500 m there is negligible light penetrating from the surface.

During our dive series, one of us (E. D. H.) tested whether a profoundly dark-adapted human observer could detect any light in the ambient environment at the TAG Site and saw nothing. This observation was repeated at the Snake Pit Site (Carolyn Eberhard, pers. comm.) with the same negative results. Since bioluminescence should be visible to human observers, this suggests that there is no significant bioluminescence, or light from any other source bright enough to be visible to human observers, under the conditions of a visit with DSV Alvin. We are left, then, with the light apparently emitted at the top of the black smoker chimneys (Van Dover et al., 1994) as the most likely possibility. This light might well be blackbody radiation, but other mechanisms that could produce such light have recently been suggested (Van Dover et al., 1994). The intensity, spectrum, and distribution of light emitted at hydrothermal vents needs to be investigated experimentally before firm conclusions can be reached about the underlying mechanisms of light production. The spectral sensitivity of the dorsal eye of R. exoculata seems to be maximum around 500 nm whether determined from scans of retinal extracts (Van Dover et al., 1989) or electroretinographic responses to lights of varying wavelength (Johnson et al., 1995).

The masses of Rimicaris sp. which swarm around the sides of the chimneys would, then, likely be in the shadow that the chimney lip would cast. The dorsal position of the eye would be appropriate, for example, to signal that an animal had moved away from the mass and out of the shadow into the light that is coming from above. This could provide a local navigational cue to guide an animal back to the mass if it swam far enough away to emerge into the light. Likewise, as animals crept higher and higher on the sides on the chimney toward the lethally hot water of the emerging jets, the shadow would become narrower and they would more easily emerge into brighter light which could warn them of the potential danger of being swept into the hot jet.

It is likely that hydrothermal vent communities lack daily environmental cues. Do vent organisms continue to show the daily rhythms in physiology and behavior typical of their shallow-water relatives? We observed no organelles typical of a cyclic shedding and renewal of the photosensitive rhabdom in the photoreceptors or accessory retinal cells of Rimicaris sp. Except at the corneal surface, the R-segments are completely sheathed in white diffusing cells whose cytoplasm is filled with diffusing vesicles and little else. The corneal epidermis is separated from the tips of the R-segments by a blood space. Thus it seems unlikely that a mechanism of extracellular rhabdom shedding is employed. Within the photoreceptors, the volume density of rhabdom is so high (80%-85%) that there is little space available for rhabdom shedding to occur compared to a species such as Limulus polyphemus where the rhabdom occupies about 2% of the retina overall or 35% to 40% of the photoreceptor R-segment. However, the high volume density itself is not conclusive evidence for the absence of rhabdom shedding since squid (Tsukita et al., 1988), which sheds its rhabdom, has a volume density of rhabdom in its photoreceptors (75%) that is comparable to Rimicaris sp., but the rest of the squid photoreceptor is not attenuated.

The small size of the A-segment in Rimicaris sp., especially compared to the very large amount of microvillar membrane in the R-segment, makes it unlikely that significant cycling of photosensitive membrane can be occurring (Hornstein and Chamberlain, 1991; Chamberlain and Hornstein, 1993). This conclusion is reinforced by the restricted cytoplasm around the nucleus and the very limited amount of endoplasmic reticulum of any kind for protein synthesis and subsequent membrane assembly. Indeed, the large array of microvillar membrane in a mature photoreceptor with so little synthesis machinery in evidence raises questions about how the array is produced during the growth and development of the juvenile animal and suggests that the relative atrophy of the A-segment may be a feature only of the mature animal.


We thank the DSV Alvin team and the crew of the R/V Atlantis II for facilitating the expedition in search of hydrothermal vent shrimp. We thank Bill Dossert for technical assistance and instruction essential to the completion of this work. We acknowledge the contributions of Ryan Lakin, Rich Kuenzler, Patrick O'Neill, Jeff Kwasniewski, and Joao Valerio. We thank Nikon, Inc., and Micro Video Instruments, Inc., for their loan of equipment. This research was supported by NSF grant BNS 91-11248, NIH grant EY03446, the Department of Bioengineering and Neuroscience, and the College of Engineering and Computer Science at Syracuse University.

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Author:Nuckley, David J.; Jinks, Robert N.; Battelle, Barbara-Anne; Herzog, Erik D.; Kass, Leonard; Renning
Publication:The Biological Bulletin
Date:Feb 1, 1996
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