Macropinna microstoma and the Paradox of Its Tubular Eyes Author(s): Bruce H. Robison and Kim R.

Reisenbichler Reviewed work(s): Source: Copeia, Vol. 2008, No. 4 (Dec. 18, 2008), pp. 780-784 Published by: American Society of Ichthyologists and Herpetologists (ASIH) Stable URL: . Accessed: 07/03/2012 08:07
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the Paradox




fish subarctic tubular

H. Robison1
opisthoproctid in the


R. Reisenbichler1
microstoma North tiny, occupies Pacific. Like mouth. lower several This mesopelagic other species depths in the is such in Monterey family, that Bay and has upright

Macropinna and eyes temperate and a

elsewhere upward-directed

Macropinna in their



understand Macropinna paradox. protection

the visual field of these highly
how can The for eyes the feeding change are eyes takes position contained from the place. from within tentacles

In situ dorsally-directed a transparent of

eyes does not
and to shield one of

include the mouth,
laboratory studies which top sources of



it difficult
the the eyes apparent provide




rostrally-directed, covers the the apparent

resolves the of head the and food



of Macropinna.








lagic fishes confer distinct optical advantages within the dim light regime they inhabit. A tubular eye has a large-aperture lens for enhanced typically light gathering, coupled through a cylindrical tube to a densely
structured main retina at the base. The tubular shape

Gigantura also hangs vertically, sculling its caudal fin slowly, with its pectorals fanned out to stabilize the head (BHR,
unpubl. in situ obs.).

maximizes the increased light intake and accommodates focal length of a large lens, without the greater structural costs of a large spherical eye. A pair of adjacent tubular eyes
improves sensitivity, increases contrast perception, and

broad binocular fields to overlap of the visual (Munk, 1966; Lythgoe, provide accurate depth perception 1979; Johnson and Bertelsen, 1991; Herring, 2002; Warrant and Locket, 2004). There are also some drawbacks to this high level of specialization. The field of view is significantly reduced when compared with spherical eyes, and while accessory retinal tissues may line the tubes, images in this
region are not focused.


Several fish species with tubular eyes have additional structural adaptations that help to compensate for their restricted visual fields. Some scopelarchids have a pad of fibrous light-guides that direct light from the side and below, to the accessory retinal tissue inside the tube (Locket, have retinal diverticula that may 1977). Opisthoproctids to bioluminescence, but do provide peripheral sensitivity not produce 1966; Frederiksen, (Munk, images 1973). Tubular eyes occur in 11 fish families and in some nocturnal terrestrial animals as well (Marshall, 1971; Lythgoe, 1979). Inmany such fishes the eyes are directed upward, but other their tubular eyes directed species have rostrally (e.g., Stylephorus chordatus, Gigantura indica, Winteria telescopa). Parallel, upward directed, tubular eyes allow a fish to see its prey silhouetted against the lighted waters above (at least In during the day) and to accurately judge its distance. general, the position of tubular eyes has been assumed to be fixed (Locket, 1977; Collin et al., 1997). Fishes with rostrally directed tubular eyes are believed to orient their bodies which situates them appropriately to locate and vertically, strike upward at their prey. In the case of Stylephorus, the fish hangs vertically, uses its eyes to align its head with the prey, and then quickly expands its buccal cavity, creating a large suction to pull the prey in (Locket, 1977; Pietsch, 1978).
Bay Aquarium (KRR) Submitted: 4 April 2007. 1 Monterey Research Send Institute, 7700 2008. Sandholdt Associate Road, Editor:

it is readily apparent that a fish with forward it looking tubular eyes can keep its prey in view while strikes, it is not obvious how prey are tracked when the eyes are directed upward and the mouth is outside the field of view. In Argyropelecus and Hierops the mouth is large and is angled strongly upward, which precludes the problem. But Macropinna and Opisthoproctus have tiny, terminal mouths and eyes that are aimed off in another direction. How one such paradoxically configured fish can see to ingest its prey has been resolved by in situ observations. Macropinna is a solitary, opisthoproctid microstoma species that occurs at lower mesopelagic depths beneath temperate and subarc tic waters of the North Pacific from the Bering Sea to Japan and Baja California, Mexico (Chapman, 1939; Bradbury and 1958; Pearcy et al., 1979; Willis and Pearcy, 1982). Cohen, While MATERIALS AND METHODS
Five specimens of Macropinna microstoma were encountered

in or near Monterey Bay, California. Three individuals were observed in situ with remotely operated vehicles (ROV) and two specimens were collected by midwater trawl nets. Direct were made with high-resolution observations color video cameras mounted on MBARI's ROVs Ventana (Robison, 1993) and Tiburon (Robison, 2000). The first two fish were at 36?42'N, over the axis of the observed 122?02'W Submarine Canyon where the bottom depth is Monterey 1600 m. The third was at 35?38'N, 122?44'W approximately over the Davidson Seamount. Water depth at this latter site
was about 1800 m.

The first of the individuals examined in situ (36 mm SL) was encountered during the descent phase of a dive, at a depth of 616 m and was observed for 12 min. This fish was collected but did not survive. The second subsequently from the video recording to be 110 mm SL) was (estimated spotted during the ascent portion of another dive at 770 m and was observed for 7 min. This fish evaded capture. The third fish (estimated to be 112 mm SL) was found at 682 m
and Moss was observed California for 4 min. E-mail: and




? 2008 by the American Society of Ichthyologists and Herpetologists DOI: 10.1643/CG-07-082 ^jjj

reprint requests 25 February Accepted:

to BHR. J. F.Webb.





of Macropinna




at a depth of 744 m, showing the intact, transparent of Macropinna microstoma shield that covers the top of the head. The Fig. 1. Video frame-grab are the eye lenses, each sitting atop a silvery tube. Visible on the right eye, just below the lens on the forward part of the tube, is the green spheres are olfactory above and behind the mouth video frame external expression of a retinal diverticulum. The pigmented capsules. patches High-definition on the web at: in situ are posted microstoma grabs of Macropinna

One of the trawl-caught (116 mm SL) was specimens collected by an RMT-8 net that fished discretely at 600 m depth, over the axis of the canyon at the 1600 m site. The second trawl specimen (52 mm SL) was collected by a small to 1000 m at 36?25'N, Tucker net that fished obliquely from Monterey the water 123?19'W, offshore Bay where column depth is 3600 m. The latter fish reached the surface alive and in excellent condition. This specimen remained seawater for active in a shipboard aquarium of chilled
several hours.

Separating the eyes is a thin, bony septum that expands posteriorly to enclose the brain. Rostral to each eye, to the mouth, is a large rounded but caudal pocket chamber.
containing lenses eye an are rosette. olfactory a vivid color. green In living specimens, the

RESULTS The most striking aspect of these fishes when first viewed in situ is the transparent, cowl-like shield that covers the top of tubular eyes within the head, and the prominent (Fig. 1). that attaches to The shield is a tough, flexible integument dorsal and medial scales behind the head, and to the broad, transparent subocular bones that protect the eyes laterally. This fragile structure is typically lost or collapsed during capture by nets, and it has not been previously described or figured. Beneath the shield is a fluid-filled chamber that
surrounds and protects the eyes. Scales are present just


the eyes


the nape


the back, within


in two Undisturbed fishes were oriented horizontally, cases with the head slightly down and in the third, with the head slightly up (<10? of inclination for all). In all cases the as the vehicle approached. All of fish remained motionless the fins were the pectorals held out spread wide, with and the pelvics angled a little downward (about horizontally The broad spread of the very large 30? from horizontal). pelvic fins of Macropinna appeared to give them a great deal the fish moved of stability. When slowly away from the came all of the fins remained spread and propulsion vehicle, from the caudal and pectorals. The only time the pelvic fins were employed for motion was when the second specimen into the dome of the camera and turned sharply bumped away from it.When we attempted to collect this animal and it contacted the inside of the sampler, it folded the pectoral and pelvic fins along the body and was last seen accelerating upward, before the sampler could be closed. As we maneuvered the vehicle around the first individual, we observed that its eyes rotated in the sagittal plane, from






Fig. 2.



of the


directed dorsally; (B) with the eyes directed rostrally.The apparent differences in lip pigmentation between (A) and (B) are because they were
at slightly different (A) was photographed angles. in focus. (B) shows the only the right eye, with shot from a more dorsal perspective and it shows the lenses of both eyes; the mouth is not sharply lips in sharper focus.

of a living specimen

of Macropinna


in a shipboard



(A) with




dorsal to rostral and back. That is, the fish was able to move its tubular eyes to look forward as well as upward. In the
laboratory, with a living, net-caught specimen, the same

DISCUSSION (1942) described and provided a figure (Fig. 3) of Chapman the eye musculature of Macropinna, and he noted that the in eye position from lateral to vertical evolutionary change had resulted in changes to the locations of muscle insertion. can now be seen as appropriate These differences for rotating the eye in the sagittal plane, with the obliquus muscles pulling the eye forward and down, and the rectus it to an upright superior and rectus internus returning The position of the rectus inferior, at the center of position. the mesial tube wall, is such that its insertion serves as a the eye can pivot. Likewise, the optic node around which
nerve rotation, enters which the near the eye reduces twisting same at point, rotation. during the axis Anatom of

this fish repeated (Fig. 2). When we positioned in an aquarium, its eyes were directed upward horizontally toward the top of the tank. When we rotated the fish into a to look upward, its eyes continued head-up vertical position, although they were directed forward relative to its body. Eye rotation, or tilt, did not occur every time the fish was moved, but in 12 trials the eyes moved eight times. The size of the arc of rotation depended on the degree to which the
fish about was 75 moved, degrees. and the maximum arc we observed was

action was

We examined the visceral anatomy of three specimens and found elongate intestines and multiple cecae, which are associated with diets of mixed zooplankton, including both and crustacean prey (Robison, 1984). As Chap gelatinous man (1942) noted, the gullet is broad, without a narrowed esophagus. The smallest restriction on prey size before the
stomach is the mouth. Two of the stomachs we opened

the default position of the eyes is ically and behaviorally, upright. When the eyes are directed the olfactory rostrally, chambers may partially obscure a portion of the visual field
in front of each eye. However, there is a central, unobstruct

contained cnidarian remains. Opisthoproctid fishes, with terminal mouths like that of Macropinna, have been tiny, and siphonophore reported to browse on siphonophores, tentacles and nematocysts have been found in the stomachs of several species (Cohen, 1964; Haedrich and Craddock, 1968; Marshall, 1971, 1979).

ed area of the presumably binocular visual field that is lined The forward-looking tubular eyes of up over the mouth. males of Linophryne also look through metamorphosed 1982). In transparent olfactory organs (Bone and Marshall, his examination ofthe skull of Macropinna, Chapman (1942) noted that the large, translucent suborbital bones do not





of Macropinna




of counterillumination the bioluminescent against which prey will then stand out (Muntz, 1976; Herring, 2002). In this is probably well equipped for scanning respect, Macropinna the waters above for bioluminescent prey. of the genus Apole siphonophores Large, bioluminescent in at lower mesopelagic mia are very common depths or more, lengths of ten meters Monterey Bay. Reaching
these slow-moving colonies accumulate a broad variety of

view of (1942) mesial Fig. 3. Chapman's rectus RS = Abbreviations: microstoma. 01 = obliquus inferior, obliquus superior, OP = rectus inferior, RE = rectus extemus,

the left eye of Macropinna = L = lens, OS superior, = RIN = rectus internus, Rl nerve. optic




leaving the above

"... mesethmoid."


unprotected Thus, while

space the

tubular eyes unobstructed
" gelatinous frontal..." . . .

are protected laterally, their rostral view is by bone. Instead, the suborbitals verge on a
mass (Chapman, between 1942). the olfactory This skull capsule structure and allows the a

prey in their tentacles and gastrozooids, which except for the presence of stinging tentacles, are open to appropriation 1995, 2004). The ability of (Robison, by other animals Macropinna to scan the water overhead for potential prey, to and to against the background, recognize bioluminescence move into a cluster of tentacles with its eyes protected, make Apolemia a likely source of food. Fan-like fins have been around objects such as associated with fishes that maneuver et al., 1989). (Janssen siphonophores Regardless of the specific source of prey, the particular of the eyes of Macropinna would appear to allow morphology and at least two feeding modes: 1) with the body horizontal the eyes directed upward, the fish spots food against the the fish pivots its body to bring lighted waters above. While the eyes remain locked on the mouth up for ingestion, target, rotating from dorsal to rostral relative to the body; 2) the eyes rotate from dorsal to with the body horizontal, rostral while tracking the path of descending food, until it that Macro The discovery reaches the level of the mouth. of its eyes resolves the the position pinna can change apparent paradox of how it can see to feed with eyes that are this solution applies directed away from itsmouth. Whether fishes with and other to Opisthoproctus, Dolichopteryx,
upward-directed tubular eyes, remains to be seen.

clear, central view forward for both eyes when they are directed rostrally. in fishes that Tubular eyes appear almost exclusively the lower reaches of the mesopelagic occupy depth range (Marshall, 1971). This is a region of dim light and shadows, is monochromatic and highly where the ambient daylight and where visual trickery is common (Robison, directional, 1999). Fishes of the family Opisthoproctidae typically and they exhibit more inhabit the lower mesopelagic,
examples of unusual eye modifications than any compara

ACKNOWLEDGMENTS We thank the pilots of the ROVs Ventana and Tiburon for these midwater their patience and skills in conducting The officers and crews of the R/V Point Lobos and operations. the R/V Western Flyer provided invaluable logistical support. R. Sherlock, J. Drazen, and K. Osborn helped us at sea and ashore. This research was supported by the David and Lucile Packard Foundation through MBARI. LITERATURECITED 1964. Rectal light organs in the Bertelsen, E., and O. Munk. Dana and Winteria. fishes Opisthoproctus argentinoid Denmark. 62, Copenhagen, Report 1982. The Biology of Fishes. Bone, Q., and N. B. Marshall.
Blackie, Bradbury, Glasgow. M. G., and D. M. Cohen. 1958. An illustration

invested a considerable ble group. Macropinna has obviously amount of evolutionary currency to develop its remarkably Our structured head and the tubular eyes it contains. observations suggest how it employs these structures. Bertelsen and Munk (1964) proposed that the function of the dorsally directed eyes of Opisthoproctus might be part of a to the ventrally directed process, coupled recognition luminescence produced by its rectal light organ. No such It seems much light organ has been found on Macropinna. more likely that the tubular eyes of Macropinna, coupled to the great stability provided by its widespread pelvic fins, are and to enhance its ability to perceive chiefly designed in dim light. capture prey The green color of the eye lenses of Macropinna is due to the presence of yellow pigment (McFall-Ngai et al., 1988). Several fishes with tubular eyes (Stylephorus, Scopelarchus, deep-living Benthalbella, Argyropelecus) have yellow lenses (reviewed by (1964) has noted green Douglas et al., 1998), and Cohen lenses in a specimen of Opisthoproctus grimaldii. This feature is a specific that to provide believed capability filtering decreases the apparent brightness of downwelling sunlight,

and a new Macropinna

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