Pacific Science (1975), Vol. 29, No.3, p. 243-255 Printed in Great Britain

Transitory Eye Shapes and the Vertical Distribution of Two Midwater I

RICHARD EDWARD YOUNG 2

ABSTRACT: In two cranchiid squids, and pavo, the shapes of the eyes change with growth. Compressed eyes with ocular appendages occur in the larvae living in the upper few hundred meters of the ocean. Tubular eyes occur in juveniles that live within a depth zone between about 400 and 700 m. Nearly hemispherical eyes are found in adults living at depths greater than 700 m. The shapes of the compressed and tubular eyes offer strong countershading advantages to squids living at depths where downwelling light is important in prey-predator relationships.

MOST have eyes that have a more­ considered that the dimorphic eyes (one large or-less hemispherical shape. In a number of semitubular eye and one small hemispherical pelagic cephalopods, however, the eyes exhibit eye) in squids of the family Histioteuthidae various modifications of this shape. For support this assumption. example, the forward-looking eyes of Bathy­ In nearly all tubular-eyed the optical teuthis are somewhat less than hemispherical; axes of the eyes are parallel or nearly parallel, the eyes of the midwater octopus Amphitretus allowing binocular vision. Advantages of pelagicus are tubular; while the eyes of young binocular vision may be: better depth percep­ Sandalops melancholicus and" Doratopsis" lippula tion (Brauer 1908), lowered visual threshold are laterally compressed (Chun 1910, 1914). (Weale 1955), and/or increased signal-to-noise Modified shapes also occur widely in midwater ratio (Fremlin 1972). fishes. For example, Marshall (1971) listed 11 The value of the tubular shape (as well as families that have some members with tubular most of the other ocular shapes) remains un­ eyes. resolved, although Franz's (1907) suggestion Of the various ocular shapes in fishes and that the tubular eye is merely a large eye in a cephalopods, the tubular shape has been most compact form has considerable appeal (Munk widely discussed (e.g., Brauer 1908; Walls 1966). One of the major obstacles in explaining 1942; Munk 1966; Marshall 1954, 1971). A the various ocular shapes has been the lack of tubular eye is nearly cylindrical in shape and is reliable data on the habits and habitats of the stopped by a large lens at one end and by a animals involved. thick retina at the other. In this report are examined two midwater Munk (1966) demonstrated that the tubular squids that have eyes that change from com­ eye corresponds to the central core of a hemi­ pressed to tubular to nearly hemispherical as spherical eye. Most authors (e.g., Walls 1942, the animals grow. These ocular changes are Marshall 1971) have suggested (but not correlated with changes in the depth distribu­ demonstrated) that the tubular eye corresponds tions of the squids. to a large, hemispherical eye. Young (1975) MATERIALS AND METHODS I This study was supported by National Science Foundation grant GA 33659. Hawaii Institute of All specimens were captured off the island of Geophysics contribution no. 657. Manuscript received Oahu in the Hawaiian archipelago at approxi­ 15 July 1974. mately 158°20' W, 21°20' N over bottom 2 University of Hawaii: Department of Ocean­ ography and the Hawaii Institute of Geophysics, depths from about 1,500 to 4,500 m. Two Honolulu, Hawaii 96822. types of trawls were used: a modified 3-m 243 I~2 244 PACIFIC SCIENCE, Volume 29, July 1975

Tucker trawl and a 3-m Isaacs-Kidd midwater of a broad, flat pen that tapers rapidly to a trawl (IKMT). The Tucker trawl opens and point, and oftwo pedunculate fins (Figure 2A). doses at the fishing depth; hence specimens The fin insertion lies well in advance of the cannot be captured during setting and retriev­ apex of the pen. The liver, with its associated ing of the trawl. Because this trawl has a ink sac, is spindle-shaped and covered by tendency to wander somewhat during fishing, silvery iridophores. the range as well as the principal fishing depth The brachial crown is supported on a long, (usually the modal depth) is indicated in the muscular stalk which can probably bend in any distribution charts. The opening-closing mech­ of several directions. In preservation, the anism utilizes a mechanical release activated brachial crown points anteriorly in young by weighted messengers sent down the towing larvae, but tends to arch dorsally in older cable. larvae. The arms are minute and the tentacles The IKMT is always open, and occasionally are long and robust. The larva is transparent specimens are captured during the raising and except for the eyes and liver and bears a few lowering of the trawl. This contamination is chromatophores. minimized by dropping the trawl as rapidly as The eyes (Figure 2B, C) are located on long possible and retrieving it with the ship moving stalks and are laterally compressed. The length slowly ahead. The net is pulled horizontally at (dorsal-ventral) of the eye is about three times 3 to 4 knots. The modal depth ofthe net during the lens diameter, while its width is only the horizontal phase is assumed to be the depth slightly greater than the lens diameter. The of capture. Depth records for both trawls were retina is likewise compressed into a broad obtained with a Benthos time-depth recorder. dorsal-ventral strip, which is rounded at either One eye of Sandalops melancholicus was fixed end and slightly broader in the ventral half. I in Bouin's solution in seawater and embedded could not detect an iris. in Epon 812 for sectioning. Sections approxi­ Attached to the ventral surface of the eye is mately 2 pm thick were cut on a A.a. rotary the ocular appendage-a cone-shaped projec­ microtome with a steel knife and stained with tion of tissue with a thick layer of silvery Richardson's stain. iridophores. The rest of the eye, except for the is especially prone to injury in dark dorsal surface, is covered with silver or the trawl and most specimens captured were green iridophores. badly damaged. As the eyes of the largest adults were damaged, the illustrations and JUVENILE (Figures IB, C; 2D, E): The thin­ description of the adult eye given here are walled is about three times as long as based on a specimen of T. pavo that was broad. The pen and small fins at the posterior captured in good condition off southern end of the mantle retain the characteristic California. There seem to be no significant arrangement found in the larva. The arms are differences in the adults from these two locali­ very small. The tentacles were broken off in all ties. Measurements of retinal thickness in adult specimens; however, the remnants indicate Sandalops melancholicus and all Taonius pavo were comparatively robust tentacles. The normal made from hand-cut aqueous mounts. These position of the brachial crown appears to be measurements are not very accurate and those tilted dorsally about 60° from the body axis. presented are conservative. Although the muscular stalk of the brachial crown indicates that this structure is capable of some movement, two living but moribund RESULTS individuals showed the dorsal tilt as did all preserved specimens. In contrast, the funnel Sandalops melancholicus Chun, 1906 maintains a typical orientation to the body axis. LARVA (Figure lA): The mantle is elongate The juvenile is very transparent except for the (about three times as long as broad), thin­ eyes, the liver with its associated ink sac, and a walled, and saccular. The posterior end of the few scattered chromatophores on the head and larva has a characteristic appearance consisting arms. The liver is long and spindle-shaped and Eye Shapes and Vertical Distribution of Two Midwater Squids-YoUNG 245

A

o

FIGURE 1. A-C-Sandalops melancholicus: A, ventral view of larva; B, anterior view of the juvenile head (camera lucida); C, lateral view ofthe juvenile head (camera lucida). D-I-Taoniuspavo: D, cutaway lateral view ofthe tubular eye (reconstructed); E, cutaway anterior view of the tubular eye (reconstructed); F,cutaway lateral view of the adult hemispherical eye; G, ventral view of the adult; H, ventral view of the juvenile; I, ventral view of the larva. PACIFIC SCIENCE, Volume 29, July 1975 246

c

FIGURE 2. Sandalops 111elancholicus. A, dorsal view of the posterior end of the larva; B, lateral view of the larval eye; C, frontal view ofthe larval eye; D, anterior photograph ofa moribund juvenile; E, lateral photograph ofa moribund juvenile (orientation artificial); F, cross section of the main retina of a tubular eye; G, cross section of the accessory retina from the same tubular eye at identical magnification; H, frontal section of the main retina from the same tubular eye; I, frontal section of the accessory retina from the same tubular eye (magnification the same as in H). Photographs F-I were taken through a differential interference contrast microscope. Eye Shapes and Vertical Distribution of Two Midwater Squids-YOUNG 247

c o

FIGURE 3. Sandalops melancholicus. A, lateral view of adult female (camera lucida); B, lateral view of adult male (camera lucida); C, cutaway lateral view of tubular eye (reconstructed); D, cutaway anterior view of tubular eye (reconstructed); E, cutaway lateral view of hemispherical eye of adult female (reconstructed). is covered with iridophores which reflect gold The walls consist of the pigmented epithelial to purple light. body that supports the lens and a broad, The eyes are tubular (Figures lB, C; 2D, E; heavily pigmented epithelial layer below. The 3C, D). Each, except for a bulge on the pos­ retina consists of two portions: a thick main terior wall, is a nearly straight-sided cylinder. retina and a thin accessory retina. The main 248 PACIFIC SCIENCE, Volume 29; July 1975 retina occupies the circular base of the eye. the apex of the appendage comes to lie between Posteriorly it thins to become the accessory the two of the tubular eye. retina, which extends up the bulging mid­ posterior wall of the eye from a broad base to a ADULT (Figure 3A, B): Two adults of narrow rounded tip near the epithelial body Sandalops melancholicus, a mature male and an (Figure 3C, D). Capture and fixation invariably immature female, were captured. The mantles result in considerable distortion of the eyes, of these animals are broader at the anterior end preventing a precise measure of the distance than are those of the juveniles. The small between the accessory retina and the lens. posterior fins in each maintain their However, the best determination indicates that characteristic relationship to the broad terminal nearly all of the accessory retina is too close to portion of the pen. The head and brachial the lens for images to be in focus (see Figure crown are greatly enlarged relative to the 2E). juvenile condition. This is especially true in the The distal segments (photosensitive pro­ male, where the arms are much longer and cesses) of the retinal cells of the main retina are thicker than in the female. The brachial crown long (290 p,m), and slender (3-4 p,m); they have of the large female still has a slight dorsal tilt a uniform cross-sectional shape and are which is nearly absent in the male. In the male, regularly arranged (Figure 2F, H). In contrast, the distal halves of arms I-III have no protec­ the distal segments of the retinal cells of the tive membranes, ana the suckers are reduced accessory retina are relatively short (90 p,m) and to small knobs in numerous irregular rows. No broad (5-10 p,m); they have an irregular cross trace of the tentacles remains in the male. In section and are irregularly arranged (Figure both specimens the liver is long and spindle­ 2G, I). Both retinas have a rather uniform shaped and exhibits a trace of iridescence. The thickness except for the narrow transitional head and arms have a dense concentration of region between them. chromatophores. Since the outer integument As in most squids, the muscular integument of the mantle was missing in both specimens, of the head covers the eyes and forms a circular I could not determine the mantle pigmentation. eyelid around the lens. A very narrow iris The eyes in both specimens approach a leaves a broad pupil about the same diameter as hemispherical shape. Although the eye was the lens. The eyes are aligned parallel to each damaged in the female, it appears to differ from other and, along with the brachial crown, tilt a hemispherical eye only in being slightly com­ strongly in a dorsal direction (about 60° from pressed. The divisions ofthe retina found in the the body axis). The sides of the eyes, except juvenile eye could still be detected (Figure 3E). where they attach to the head, are covered by A thick portion (distal segments about 240 iridophores reflecting purple to gold light. The p,m long) is located in the ventral-posterior bottom of the eye is covered by a large photo­ portion of the"visual" hemisphere and has a phore which, except for an anterior indentation circular shape with about the same diameter as and a posterior bulge, is nearly circular. A the lens. The rest of the retina is much thinner second smaller is situated in this and covers most of the remaining surface ofthe indentation and extends up the anterior face of "visual" hemisphere of the eye. the eye. The reflective characteristics of both The retina of the adult male retains no trace photophores indicate that they shine in the of the tubular condition. Along the midline of opposite direction to which the eye is facing. the eye in a dorsal-ventral direction, most of Photophore development coincides with the the retina is thick with the central portion being transition of the eye from the larval form to the slightly thicker. However, thin areas of the tubular form. Just prior to transition a large retina are present but are restricted to a narrow photophore appears on the proximal side of the ribbon along the ventral margin and to the ocular appendage. The appendage progressively medial and lateral margins of the "visual" shortens and, when only a remnant remains, hemisphere with the dorsal areas being some­ the second, smaller ocular photophore appears what more extensive. In a dorsal-ventral section on the distal face of the eye. Thus, what was the shape of the eye is an almost perfect semi- Eye Shapes and Vertical Distribution of Two Midwater Squids-YOUNG 249

0 midwater trawling that has been done in I I I I I 1 Hawaiian waters with open nets, the capture of I I I some specimens (i.e., contaminants) during I - 200 - I setting and retrieval of deep tows is expected. ~ I Four specimens are considered to be contami­ : ~ nants. Six specimens were captured in oblique 400 I- 0c} - • tows, and their depth of capture within the e ~~o 0 depth range of each tow is unknown. :%: • :;:600 t- . o90~ - Day captures and night captures reveal no w ° t 0 . ~ clear differences in depth distribution. Appar­ ently, diel vertical migration does not occur. 800 I- 1- Sandalops melancholicus exhibits a clear pattern of ontogenetic descent in which progressively 1000 t- - larger individuals occupy progressively greater • depths. Correlated with these depth changes are IIII r changes in the morphology of the eyes. 1200 ...... -'---2....0---1.----'4....0---'----'6'-0--'-----'80-.1..-...1.'0-0...... 0 MANTlE LENGTH,mm VERTICAL DISTRIBUTION AND EYE STRUCTURE: FIGURE 4. Vertical distribution ofSandalops melaneholi­ Thirteen larval specimens of S. melancholicus of etls. Open circles represent day captures; closed circles 28 mm mantle length (ML) or less have com­ represent night captures. A bar with a circle indicates an pressed eyes with ocular appendages, while opening-closing tow with the bar representing the range one 28-mm specimen has eyes intermediate of the tow and the circle the most likely depth of capture. A circle without a bar indicates a capture in an between the larval and the tubular conditions. open tow. A bar without a circle indicates an oblique All of the specimens with larval eyes (except tow. Solid bars represent night captures. Bars with large two probable contaminants) were captured in dashes represent day captures. Bars with small dashes the upper 400 m. The specimen with inter­ represent twilight captures. Small dots represent mediate eyes was taken at 425 m. The twenty probable contaminants from open tows. specimens of30-52 mm ML probably captured between 450 and 625 m all have tubular eyes. circle. In a lateral-medial section the eye is The specimen of 66 mm ML captured probably rather compressed, and much of the thinner at 675 m has eyes that have a tubular appearance retina may not be at the focal plane. The lens but are somewhat more globular than the is surrounded by a narrow epithelial body and a typical tubular eyes. The 105-mm ML specimen large, wide, pigmented epithelium that is some­ captured probably at 800 m was the adult what broader ventral to the lens. female, and the 100-mm ML specimen captured Each eye in the female has a slight dorsal tilt at 1,075 m was the adult male; both have and an anterior-lateral tilt from about 30° to nearly hemispherical eyes. 40° from the body axis. Therefore, the optical axes are no longer parallel but diverge some 60° to 80°. The eyes in the male, except for having Taonius pavo (LeSueur, 1821) a lesser dorsal tilt, show the same orientation. Both specimens have large heavily pigmented LARVA (Figure 1I): The mantle is thin walled irises. The ocular photophores are greatly and very long and attenuate. The liver is enlarged, with the larger of the two covering spindle shaped and has a golden metallic sheen. much oftheposterior-ventralsurface ofeach eye. A muscular stalk supports the brachial crown. The arms are small, and the tentacles are long VERTICAL DISTRIBUTION: The 37 captures of and robust. Except for the eyes, the liver and S. melancholicus present a clear general picture of associated ink sac, and a few chromatophores, the vertical distribution of the (Figure the larva is transparent. 4). Some interpretation of the data is necessary, A single larva with slightly damaged eyes however, as many specimens were taken in was captured. The eyes are located on long open nets. Because of the large amount of stalks and seem to be identical in shape (i.e., 250 PACIFIC SCIENCE, Volume 29, July 1975

0 I I ! I I I I I I I

200 f- - • e400 - - ...~ • • w , 6 °600 b ~o • - I ,0 ::0;00 ? 0 - , O' 9 o 0 ' , , : : '? . 0 0 . ? 0 800 t- o -

0 1000 I I· I I I I I I I I 40 60 80 100 120 140 160 180 200 220 MANTLE LENGTH,mm FIGURE 5. Vertical distribution of Taoniu.f pavo. See legend to Figure 4 for explanation of symbols.

laterally compressed) to the eyes of larval to a rounded apex beneath the epithelial body. Sandalops. The outer tissue has been lost from The transition between the main and accessory the eyeballs so no trace of ocular appendages retinas is more gradual than it is in S. melaneholi­ remain. Because they probably do exist in un­ eus, and the accessory retina continues to thin damaged eyes, I have included them in the toward its periphery; however, the distal drawing (Figure 11) as dotted lines. segments over much of the accessory retina are 25-50 p,m long or less. JUVENILE (Figure 1H): The mantle and fins The eyes appear to have parallel alignment, are long and attenuate, and the mantle wall is but this is uncertain due to damage. The iris is thin. The liver with its associated ink sac is narrow, and the pupil is nearly the same diam­ long and spindle shaped and is covered with a eter as the lens. The entire base of the eye is layer of purple iridophores. The tentacles are covered by two large, adjacent photophores, three to four times the length of the short arms. which together have a circular outline that Scattered chromatophores are present in the covers the circular base of the eyes. The more mantle, funnel, head, and arms. With con­ posterior photophore has a broad V-shaped tracted chromatophores the living animal un­ indentation into which the smaller, mbre doubtedly is very transparent. anterior photophore fits. Although the eye had The eyes are tubular (Figure 1D, E). Their been damaged, portions of the thin covering walls, except for a bulge on the medial side, remaining on the dorsal, ventral, and lateral appear to be nearly cylindrical. The epithelial surfaces of the eye have a purple metallic sheen. body forms the distal half of the cylinder; most of the remainder consists of heavily pigmented ADULT (Figure 1G): The body shape of the epithelium. The retina is divided into two adult is long and attentuate. The arms and portions: a thick main retina and a very thin tentacles are relatively larger than in the accessory retina. The main retina, which juvenile. The liver and its associated ink sac occupies the circular base of the eye, has distal form a spindle-shaped structure which is dark segments about 180 p,m long. The accessory brown and lacks any trace of iridescence. retina has a broad base which nearly encircles Chromatophores are densely cor..centrated on the main retina and extends up the medial wall the head, arms, and mantle. Eye Shapes and Vertical Distribution of Two Midwater Squids-YOUNG 251

The adult eye of Taonius (Figure 1F) is tured at 310m at night. Two specimens with almost perfectly hemispherical. A very narrow stalked eyes partially transitional between the epithelial body surrounds the lens and a large, larval and the juvenile condition were captured pigmented epithelium forms most of the distal at 475 m at night. Tubular-eyed juveniles from wall of the eye. The pigmented epithelium is 50 to 140 mm ML were captured between 500 slightly broader ventral to the lens. The retina and 700 m, with most specimens (14 of 22 has the same thickness throughout except at its captures) being taken between 600 and 650 m. periphery, where it rapidly thins. The lengths The eyes of the 160-mm specimen (captured at of the distal segments of the retinal cells are 700 m) were severely damaged and their shape about 290 {tm. The photophores are greatly could not be determined. The 220-mm and enlarged and cover most of the ventral hemi­ 200-mm specimens have adult hemispherical sphere of the eye. Other than being present eyes, and the 210-mm specimen presumably around the photophores, iridophores are not had similar eyes; unfortunately the head of this present on the eye. There is a large, heavily specimen was missing. The latter animals came pigmented iris. from depths of about 730, 800, and 965 m. VERTICAL DISTRIBUTION: Vertical distribution based on 31 captures ofTaoniAs pavo is presented DISCUSSION in Figure 5. As with Sandalops melancholicus, some contlmination (one 63-mm specimen Vertical Distribution and Eye Shape placed at 980 m in Figure 5) apparently resulted The larvae of Sandalops melancholicus, which from a capture during the setting or retrieval of live in relatively near-surface waters, have the open IKMT. Another of contamina­ stalked, laterally cChnpressed eyes that bear tion seems tJ have occurred as well. A specimen ocular appendages. Juveniles ocopy greater entangled in the net may be washed into the depths and have tubular eyes with large cod-end collecting bucket in a subsequent tow. ventral photophores, while adults occupy still The IKMT net was not always carefully greater depths and have eyes that approach the examined after each tow, and one anomalous normal, hemispherical shape. Since there is capture (80-mm specimen at 50 m) may be a little difference in the mantle length between result of this type of contamination. large larvae and small juveniles, the transition Although the data on larvae and adults are from the larval eye to the tubular eye appears sparse, a pattern of ontogenetic descent appears to be abrupt, occurring at a depth of 400 to to be present: larvae occur in the upper 400 m; 450 m. From the few specimens available, it most juvenile3 occur between 600 and 650 m, appears that the transition from a tubular to a and larger juveniles and adults occur at 700 m nearly hemispherical eye is more gradual. or deeper. Other than one typical larva and two Tubular eyes are found in specimens captured metamorphosing larvae, nearly all of the as deep as 625 m. The initial stages of trans­ captures were made during the day. Most cap­ formation to a hemispherical eye are found in a tures were made between 500 and 700 m, yet in specimen captured near 675 m, while almost this zone night sampling was over 60 percent completely transformed adult eyes occur in the as extensive as day sampling. Indeed, all depths specimen captured near 800 m. If these two above 800 m were well sampled at night. Since specimens are representative, then a gradual the probably do not descend into transformation in shape occurs in animals greater depths at night, they simply may be living between about 675 to 800 m. able to avoid the net better at that time. The The stalked larval eyes of Taonius pavo capture depths of the few specimens taken at probably exhibit the same features as the larval night, including one in an opening-closing tow, eyes of Sandalops melancholicus. The evidence suggest that diel vertical migration does not indicates that as larvae descend from relatively occur. near-surface waters into the juvenile habitat VERTICAL DISTRIBUTION AND EYE STRUCTURE: (from about 500 to 700 m) the eyes transform The only specimen with larval eyes was cap- into a tubular shape, and as juveniles descend 252 PACIFIC SCIENCE, Volume 29, July 1975 farther into the adult habitat (below 700 m) the shapes, the lens sizes of Sandalops melancholicus eyes transform into a nearly hemispherical are comparable to those of the large eyes of shape. The overlap in mantle length between Phasmatopsis fisheri. In addition, although the larvae with transitional eyes and the specimens for comparison are few, the lenses of smallest juveniles suggests that as in S. the large adult eye of Sandalops melancholicus do melancholicus the transformation to tubular eyes appear to have about the same ratio to mantle is rapid. No evidence is available concerning length as do the lenses of the tubular eyes ofthe the rate of transformation from the tubular to juveniles. The more elongate body in Taonius the hemispherical eye. pavo prevents comparable measurements with Off Hawaii nearly all captures of the semi­ Phasmatopsisfisheri. In Sandalops the tubular eyes tubular-eyed squid Histioteuthis dofleini were correspond to the central core oflarge eyes, and also made in the 500-700 m depth zone (Young the same is probably true for Taonius. 1975). Apparently the tubular-eyed juveniles of One probable function of large eyes is to Sandalops melancholicus and Taonius pavo, as well increase visual sensitivity (Walls 1942). One as the semitubular-eyed squid Histioteuthis might expect that the ultimate sensitivity of an dofleini, all live within a depth zone that extends eye would be limited by the sensitivity of the from about 400 to 700 m in Hawaiian waters. receptor cells. However, in humans the Most tubular-eyed fishes off Hawaii are also absorption ofone photon will trigger a response restricted to these depths during the daytime in the retinal cell (Lewin 1972). If we assume (e.g., Argyropelecus, Ichtf(;ococcus, Opisthoproctus, this same sensitivity, together with efficient Danaphos) (T. Clarke and S. Amesbury, per­ absorption, in deep-sea animals, the limiting sonal communication). Other tubular-eyed factor may well be in the "noise" in the species (e.g., scopelarchids, evermannellids, system, this noise perhaps being due to giganturids) have ranges that extend well below spontaneous breakdown of retinal pigment these depths, and some (e.g., Batf(;leptus lisae) (see Denton and Warren 1957). If this is true, exhibit peak abundances below 700 m. How­ then to increase sensitivity the signal-to-noise ever, all of these deeper living tubular-eyed ratio must be increased by the reduction of species have ranges that extend upward to " noise." about 500 m (T. Clarke and S. Amesbury, Parts of the eye of Sandalops melancholicus may personal communication). The change in be modified to increase the signal-to-noise ocular shape in Sandalops and Taonius as they ratio. The main retina contains many long pass through these depths suggests that the slender cells as compared to the accessory tubular eye is an adaptation to this twilight retina (Figure 2F-I). Slender cells may have a zone. distinct advantage by increasing the signal-to­ The dwarf male angler fish of the family noise ratio. Although Walls (1942: 69) stated Linophrynidae, which have small, slightly that bulky cells and extensive summation downward-looking tubular eyes, are exceptions promote sensitivity, he also noted (p. 216) that to this distribution pattern (see Bertelsen 1951). in nocturnal animals the rods tend to be very The size and orientation of the tubular eyes in slender and numerous. Denton and Warren these animals is also unusual. The eyes in male (1957) and Denton (1959) have demonstrated linophrynids, however, represent a special case that there is an increased density of visual of adaptation that bears little relationship to the pigment in the retinae of deep-sea fishes. If the present discussion. spontaneous breakdown of visual pigment produces noise, then it would certainly be advantageous if the amount of pigment per cell Function of the Tubular Eye in the retina was reduced while high overall EYE SIZE: I have compared the lens sizes of retinal pigment densities were maintained. A Sandalops melancholic;/s and Phasmatopsis fisheri, a bulky cell with a large quantity of pigment cranchiid with large hemispherical eyes. Al­ might be in danger of almost constant dis­ though precise comparisons are difficult to charge. The smaller the amount of pigment in make, due to the somewhat different body a cell, the greater is the chance that a cell dis- Eye Shapes and Vertical Distribution of Two Midwater Squids-YoUNG 253 charge will represent the absorption of a to produce a downward beam of light that photon and not noise. Presumably a slender would ventrally countershade each tubular eye cell would carry less pigment than a broad cell if the eyes were directed vertically upward. In of the same length. A possible elaboration of addition, the sides of the eyes bear a strong this system occurs in deep-sea fish with purple to gold metallic sheen that would be multiple layers of rod aeromeres in their effective in countershading only ifthe eyes were retinas. Many deep-sea fishes exhibit this oriented vertically. Further, the head tilts condition, e.g., Batl!Ylagus benedicti, Winteria strongly in a dorsal direction (Figures 1C, 2D). telescopa, Gonostoma elongatum, Bathophilus metal­ This tilt is always present in preserved juveniles licus (Munk 1966), although the overall thick­ and seems to be a permanent and unique fea­ ness of the aeromere zone is no greater than it ture. Because of this strong dorsal tilt, the eyes is in species with elongated acromeres (Munk can be directed vertically upward if the body is 1966). Presumably, the pigment per cell is very tilted only slightly from the horizontal or if the low in those species with multiple layers in the head is tilted somewhat farther while the body retina. The same argument holds for other remains horizontal. In the photograph (Figure possible sources of noise related in magnitude 2D) I have assumed that the former situation to cell size. applies and have positioned and trimmed the photograph so that the eyes are directed SHAPE OF THE JUVENILE AND ADULT EYES: In vertically upward. discussing the shape of the tubular eye, we In contrast to S. melancholicus, the tubular eyes must note that the direction that the eye nor­ of Taonius pavo are directed anteriorly. Each eye mally faces in the water is of great importance. carries two large photophores that precisely Unfortunately evidence concerning the body cover the base of the eye. Assuming these to be orientation of S. me!ancholicus and T. pavo is countershading photophores, as in Sandalops meager. Clarke, Denton, and Gilpin-Brown melancholicus, the eyes must be directed vertically (1969) noted that Helicocranchia pfefferi floated in upward. This interpretation is supported by an aquarium with the head downward. I have the presence of iridophores on the ventral wall also observed this head-down position in ofthe eye, which indicates a vertical rather than several species ofyoung cranchiids. McSweeney a horizontal orientation. As extensive rotation (personal communication), on the other hand, ofthe eyes is unlikely, the squidprobably orients noted that large specimens of the cranchiid vertically with the head up and the tail down. Crystalloteuthis glacialis floated in the aquarium The tubular eyes in both of these species with the tail slightly downward. Unfortunately, probably point vertically upward. Young no observations of juvenile Taonius pavo have (1975) has presented evidence for the same been made in an aquarium and only inconclu­ vertical orientation of the semitubular eye of sive observations of juvenile Sandalops melan­ the squid Histioteuthis dofleini. Indeed, the up­ cholicus are available. The specimens of S. ward orientation probably applies to tubular­ melancholicus which I observed were dead or eyed fishes as well. In most midwater fishes with moribund and damaged. These specimens tubular eyes, the eyes are dorsally directed in floated in a horizontal position. I suspect, how­ species that probably orient horizontally (e.g., ever, that this squid could orient in almost any Argyrope!ecus, Opisthoproctus) and are anteriorly position with only the slightest effort. directed in species that may orient vertically A strong morphological clue to the normal (e.g., giganturids, Stylephorus), although there orientation of S. melancholicus is provided by is little evidence from living animals to confirm the large ocular photophores. Each eye bears a this upward orientation. large, nearly circular photophore that almost Thus, tubular eyes occur in fishes and squids covers the base of the tubular eye. A second, that are restricted to or, at least, that are much smaller circular photophore lies partially occasional inhabitants of the twilight zone within a small anterior notch of the large during the day. The eyes appear to be directed photophores on the anterior wall of each eye. vertically upward. They probably represent These two photophores are properly positioned large eyes in most species, and they usually 254 PACIFIC SCIENCE, Volume 29, July 1975 provide binocular VlSlon. The possession of SHAPE OF THE LARVAL EYE: The ocular large, upward-looking eyes in species inhabit­ appendages on the eyes of larval Sandalops are ing the twilight zone is presumably related to not unique structures. Similar appendages are the strong predominance of vertical down­ known in many cranchiid larvae (e.g., Leachia, welling light. But how are we to account for Helicocranchia, Bathothauma, Phasmatopsis) and in the fact that the eyes are tubular and not the larvae of Discoteuthis laciniosa (Cyclotheuti­ hemispherical? Large hemispherical eyes direc­ dae). They probably also occur in larval ted vertically upward would have all the Taonius. John Z. Young (1970) examined these advantages oftubular eyes and more. However, structures in detail in the larvae of Bathothauma they would also have a severe disadvantage: and suggested that they might be photophores they would bulge greatly from the sides of the which emit light through an apical pore. head, resulting in a presumably awkward shape Certainly in some species (e.g., Leachia spp.) for a streamlined, fast moving fish or squid. As the ocular appendages carry photophores on suggested by Franz (1907), the compactness of their outer surfaces. Whatever the role of these the tubular eye seems highly advantageous. appendages in light production, their primary However, for Sandalops melancholicus and Taonius function probably is one of countershading. pavo, compactness alone cannot explain the Larval Sandalops melancholicus and probably tubular shape of their eyes. These squids are larval Taonius pavo occur in the upper several quite capable of handling large bulging eyes, hundred meters of water during the day, and and, indeed, the adults have such eyes. I suggest the same is probably true for most other squid that the tubular shape in this instance has the larvae that possess ocular appendages. With advantage of being easier to camouflage than the exception of the eyes and liver-ink sac, an upward-directed hemispherical eye. these larvae are very transparent. The eyes of Many animals living in the twilight zone have Sandalops melancholicus and probably Taonius some means of camouflage, generally through pavo are countershaded laterally and distally with transparency or countershading. One of the mirrorlike iridophores and dorsally with dark most difficult problems in countershading is pigment. Because of the high ambient light elimination of the ventral shadow. In some intensities the eyes cannot be countershaded animals, this problem has been minimized by a ventrally with bioluminescent light. Other small horizontal cross section. For example, techniques must be utilized. The compressed . Argyropelecus is very thin, and some snipe eels shape of the larval eye, with the resulting are long and slender and orient vertically reduced horizontal cross-sectional area, lessens (Barham 1971). Many animals in this zone the extent of the shadow. Denton and Nicol apparently eliminate the ventral shadow by the (1965) have demonstrated that the presence in production of a ventral bioluminescent glow some fish of a ventral keel that bears silvery (Clarke 1963). sides can greatly reduce the shadow region Except for the eyes and the liver with its below the fish. The ocular appendages appear associated ink sac, juvenile Taonius and to be simply silvery keels on the eyes. The liver Sandalops are very transparent. Thus, only the of these animals is countershaded in a similar eyes and liver-ink sac need to be countershaded. fashion through its long spindlelike shape and The area of the shadow cast by a tubular eye is reflecting iridophores. The compressed eye less than 15 percent of a comparable-sized eye suffers from a loss oflateral vision; however, the (i.e., same dioptric dimensions) of hemispheri­ greater mobility of the eyes provided by the cal shape. Further, the tubular shape with long stalks may compensate for this loss. straight sides and flat bottom is more easily These specializations of the liver and eyes to countershaded laterally and ventrally. The liver reduce the ventral shadow would be meaning­ is long and spindle-shaped and presumably less if these organs did not maintain a vertical orients vertically, producing only a small orientation in the water. I have made some pre­ shadow. Thus, the tubular-shaped eyes allow liminary observations on living larval Phasmat­ these squids to have large, upward-looking opsis fisheri in a shipboard aquarium. (This eyes that are easily camouflaged. squid belongs to the same family as Sandalops Eye Shapes and Vertical Distribution of Two Midwater Squids-YOUNG 255

melancholicus and Taonius pavo). In this species CLARKE, M. R., E. J. DENTON, and J. B. the eyes and liver have the characteristic GILPIN-BROWN. 1969. On the buoyancy of modifications, and, indeed, they maintain a squid of the families Histioteuthidae, Octo­ constant orientation with their long axes poteuthidae and Chiroteuthidae. J. Physiol. vertical whether the animal is tilted upward or (London) 203: 49-50. downward. CLARKE, W. D. 1963. Function of biolumines­ It thus appears that the compressed shape and cence in mesopelagic organisms. Nature ocular appendages of the larval eye and the (London) 198: 1244--1246. tubular shape ofthe juvenile eye in these squids DENTON, E. J. 1959. The contributions of the have evolved primarily for countershading oriented photosensitive and other molecules purposes. to the absorption of whole retina. Proc. R. Soc. London 150: 78-94. DENTON, E. J., and J. A. C. NICOL. 1965. ACKNOWLEDGMENTS Reflexion of light by external surfaces of the herring, Clupea harengus. Mar. BioI. Assoc. I thank Andrew Packard, University Medical J. u.K. 45: 711-738. School, Edinburgh, Ole Munk, University of DENTON, E. and F. J. WARREN. 1957. The Copenhagen, and Sherwood Maynard and John J., photosensitive pigments in the retinae of Walters, University of Hawaii, for reading and deep-sea fish. J. Mar. BioI. Assoc. 36: commenting on the manuscript. I thank u.K. 651-662. Thomas Clarke of the University of Hawaii for FRANZ, V. 1907. Bau des Eulenauges und supplying most of the specimens taken in open Theorie des Teleskopauges. BioI. Zbl. 27: tows. The photographs (Figure 2D, E) were 271, 341. taken by John Walters. The specimens of FREMLIN, J. 1972. How stereoscopic vision Taonius pavo from off southern California were evolved. New Sci. 56: 26-28. provided by John S. Garth, University of LESUEUR, C. A. 1821. Descriptions of several Southern California. new species of cuttlefish. J. Acad. Nat. Sci. Philadelphia 2: 86-101. LEWIN, R. 1972. How the eye's amplifier works. LITERATURE CITED New Sci. 54: 612-615. BARHAM, E. G. 1971. Deep-sea fishes: lethargy MARSHALL, N. B. 1954. Aspects of deep-sea and vertical orientation. Pages 100-116 in biology. Hutchinsons, London. 380 pp. Proc. Intern. Symp. Bioi. Sound Scattering ---. 1971. Explorations in the life of fishes. in the Ocean. Maury Center for Ocean Harvard University Press, Cambridge. 204 Science, Washington. pp. BERTELSEN, E. 1951. The ceratioid fishes: MUNK, O. 1966. Ocular anatomy ofsome deep­ ontogeny, , distribution and biol­ sea teleosts. Dana-Rep. Carlsberg Found. 70. ogy. Dana-Rep. Carlsberg Found. 39. 276 pp. 62 pp., 16 plates. BRAUER, A. 1908. Die Tiefsee-Fische. 2. Anat. WALLS, G. L. 1942. The vertebrate eye. Bull. Teil. Wiss. Ergebn. "Valdivia" 15(2). Cranbrook Inst. Sci. 19. 785 pp. 266 pp. WEALE, R. A. 1955. Binocular vision and deep­ CHUN, C. 1906. System der Cranchien. Zool. sea fish. Nature (London) 175: 996. Anz. 31: 82-86. YOUNG, J. Z. 1970. The stalked eyes of --.1910. Die Cephalopoden. 1. . Bathothau1lJa (, Cephalopoda). J. Wiss. Ergebn. "Valdivia" 18(1).410 pp. Zoo!' 162: 437-447. --.1914. Die Cephalopoden. II. Myopsida, YOUNG, R. E. 1975. Function of the dimorphic Octopoda. Wiss. Ergebn. "Valdivia" 18(2). eyes in the midwater squid Histioteuthis 150 pp. dofleini. Pac. Sci. 29(2): 211-218.