Macropinna microstoma and the Paradox of Its Tubular EyesAuthor(s): Bruce H. Robison and Kim R. ReisenbichlerReviewed work(s):Source: Copeia, Vol. 2008, No. 4 (Dec. 18, 2008), pp. 780-784Published by: American Society of Ichthyologists and Herpetologists (ASIH)Stable URL: http://www.jstor.org/stable/25512162 .Accessed: 07/03/2012 08:07

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Copeia 2008, No. 4, 780-784

Macropinna microstoma and the Paradox of Its

Tubular Eyes Bruce H. Robison1 and Kim R. Reisenbichler1

The opisthoproctid fish Macropinna microstoma occupies lower mesopelagic depths in Monterey Bay and

elsewhere in the subarctic and temperate North Pacific. Like several other species in the family, Macropinna has

upward-directed tubular eyes and a tiny, terminal mouth. This arrangement is such that in their upright

position, the visual field of these highly specialized eyes does not include the mouth, which makes it difficult to understand how feeding takes place. In situ observations and laboratory studies reveal that the eyes of

Macropinna can change position from dorsally-directed to rostrally-directed, which resolves the apparent

paradox. The eyes are contained within a transparent shield that covers the top of the head and may provide

protection for the eyes from the tentacles of cnidarians, one of the apparent sources of the food of Macropinna.

THE upward-looking, tubular eyes of some mesope

lagic fishes confer distinct optical advantages within the dim light regime they inhabit. A tubular eye

typically has a large-aperture lens for enhanced light gathering, coupled through a cylindrical tube to a densely structured main retina at the base. The tubular shape

maximizes light intake and accommodates the increased 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

creates broad binocular overlap of the visual fields to

provide accurate depth perception (Munk, 1966; Lythgoe, 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, 1977). Opisthoproctids have retinal diverticula that may

provide peripheral sensitivity to bioluminescence, but do not produce images (Munk, 1966; Frederiksen, 1973). Tubular eyes occur in 11 fish families and in some nocturnal terrestrial animals as well (Marshall, 1971; Lythgoe, 1979). In many such fishes the eyes are directed upward, but other

species have their tubular eyes directed 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

during the day) and to accurately judge its distance. In

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

vertically, which situates them appropriately to locate and 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).

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

While it is readily apparent that a fish with forward

looking tubular eyes can keep its prey in view while it

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 microstoma is a solitary, opisthoproctid 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

Cohen, 1958; Pearcy et al., 1979; Willis and Pearcy, 1982).

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 observations were made with high-resolution color video cameras mounted on MBARI's ROVs Ventana (Robison, 1993) and Tiburon (Robison, 2000). The first two fish were observed at 36?42'N, 122?02'W over the axis of the

Monterey Submarine Canyon where the bottom depth is

approximately 1600 m. The third was at 35?38'N, 122?44'W 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

subsequently collected but did not survive. The second

(estimated from the video recording to be 110 mm SL) was

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 was observed for 4 min.

1 Monterey Bay Aquarium Research Institute, 7700 Sandholdt Road, Moss Landing, California 95039; E-mail: (BHR) robr@mbari.org; and

(KRR) reki@mbari.org. Send reprint requests to BHR.

Submitted: 4 April 2007. Accepted: 25 February 2008. Associate Editor: J. F. Webb. ? 2008 by the American Society of Ichthyologists and Herpetologists ^jjj DOI: 10.1643/CG-07-082

Robison and Reisenbichler?Tubular eyes of Macropinna microstoma 781 J

Fig. 1. Video frame-grab of Macropinna microstoma at a depth of 744 m, showing the intact, transparent shield that covers the top of the head. The

green spheres 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

external expression of a retinal diverticulum. The pigmented patches above and behind the mouth are olfactory capsules. High-definition video frame

grabs of Macropinna microstoma in situ are posted on the web at: http://www.mbari.org/midwater/macropinna.

One of the trawl-caught specimens (116 mm SL) was 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

Tucker net that fished obliquely to 1000 m at 36?25'N, 123?19'W, offshore from Monterey Bay where the water column depth is 3600 m. The latter fish reached the surface alive and in excellent condition. This specimen remained active in a shipboard aquarium of chilled seawater for several hours.

RESULTS

The most striking aspect of these fishes when first viewed in situ is the transparent, cowl-like shield that covers the top of the head, and the prominent tubular eyes within (Fig. 1).

The shield is a tough, flexible integument that attaches to 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 behind the eyes at the nape of the back, within this

chamber. Separating the eyes is a thin, bony septum that

expands posteriorly to enclose the brain. Rostral to each eye, but caudal to the mouth, is a large rounded pocket containing an olfactory rosette. In living specimens, the

eye lenses are a vivid green color.

Undisturbed fishes were oriented horizontally, in two cases with the head slightly down and in the third, with the head slightly up (<10? of inclination for all). In all cases the fish remained motionless as the vehicle approached. All of the fins were spread wide, with the pectorals held out

horizontally and the pelvics angled a little downward (about 30? from horizontal). The broad spread of the very large pelvic fins of Macropinna appeared to give them a great deal of stability. When the fish moved slowly away from the

vehicle, all of the fins remained spread and propulsion came from the caudal and pectorals. The only time the pelvic fins

were employed for motion was when the second specimen bumped into the dome of the camera and turned sharply 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

782 Copeia 2008, No. 4

Fig. 2. Lateral views of the head of a living specimen of Macropinna microstoma, in a shipboard laboratory aquarium: (A) with the tubular eyes directed dorsally; (B) with the eyes directed rostrally. The apparent differences in lip pigmentation between (A) and (B) are because they were

photographed at slightly different angles. (A) was shot from a more dorsal perspective and it shows the lenses of both eyes; the mouth is not sharply in focus. (B) shows only the right eye, with the lips in sharper focus.

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

action was repeated (Fig. 2). When we positioned this fish

horizontally in an aquarium, its eyes were directed upward toward the top of the tank. When we rotated the fish into a

head-up vertical position, its eyes continued to look upward, 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 was moved, and the maximum arc we observed was

about 75 degrees. 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

gelatinous and crustacean prey (Robison, 1984). As Chap 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 contained cnidarian remains. Opisthoproctid fishes, with

tiny, terminal mouths like that of Macropinna, have been

reported to browse on siphonophores, and siphonophore tentacles and nematocysts have been found in the stomachs of several species (Cohen, 1964; Haedrich and Craddock, 1968; Marshall, 1971, 1979).

DISCUSSION

Chapman (1942) described and provided a figure (Fig. 3) of the eye musculature of Macropinna, and he noted that the

evolutionary change in eye position from lateral to vertical had resulted in changes to the locations of muscle insertion. These differences can now be seen as appropriate for

rotating the eye in the sagittal plane, with the obliquus muscles pulling the eye forward and down, and the rectus

superior and rectus internus returning it to an upright position. The position of the rectus inferior, at the center of the mesial tube wall, is such that its insertion serves as a node around which the eye can pivot. Likewise, the optic nerve enters the eye near the same point, at the axis of

rotation, which reduces twisting during rotation. Anatom

ically and behaviorally, the default position of the eyes is

upright. When the eyes are directed rostrally, the olfactory

chambers may partially obscure a portion of the visual field in front of each eye. However, there is a central, unobstruct

ed area of the presumably binocular visual field that is lined

up over the mouth. The forward-looking tubular eyes of

metamorphosed males of Linophryne also look through transparent olfactory organs (Bone and Marshall, 1982). In his examination ofthe skull of Macropinna, Chapman (1942) noted that the large, translucent suborbital bones do not

Robison and Reisenbichler?Tubular eyes of Macropinna microstoma 783 J

RIN 01 Fig. 3. Chapman's (1942) mesial view of the left eye of Macropinna

microstoma. Abbreviations: RS = rectus superior, L = lens, OS =

obliquus superior, 01 = obliquus inferior, RIN = rectus internus, Rl =

rectus inferior, RE = rectus extemus, OP = optic nerve.

meet anteriorly, leaving "... an unprotected space

anteromesially above the mesethmoid." Thus, while the

tubular eyes are protected laterally, their rostral view is

unobstructed by bone. Instead, the suborbitals verge on a "

. . . gelatinous mass between the olfactory capsule and the

frontal..." (Chapman, 1942). This skull structure allows a

clear, central view forward for both eyes when they are

directed rostrally. Tubular eyes appear almost exclusively in fishes that

occupy the lower reaches of the mesopelagic depth range (Marshall, 1971). This is a region of dim light and shadows,

where the ambient daylight is monochromatic and highly directional, and where visual trickery is common (Robison, 1999). Fishes of the family Opisthoproctidae typically inhabit the lower mesopelagic, and they exhibit more

examples of unusual eye modifications than any compara

ble group. Macropinna has obviously invested a considerable amount of evolutionary currency to develop its remarkably structured head and the tubular eyes it contains. Our 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

recognition process, coupled to the ventrally directed luminescence produced by its rectal light organ. No such

light organ has been found on Macropinna. It seems much more likely that the tubular eyes of Macropinna, coupled to

the great stability provided by its widespread pelvic fins, are

designed chiefly to enhance its ability to perceive and

capture prey in dim light. The green color of the eye lenses of Macropinna is due to the

presence of yellow pigment (McFall-Ngai et al., 1988). Several

deep-living fishes with tubular eyes (Stylephorus, Scopelarchus, Benthalbella, Argyropelecus) have yellow lenses (reviewed by Douglas et al., 1998), and Cohen (1964) has noted green lenses in a specimen of Opisthoproctus grimaldii. This feature is

believed to provide a specific filtering capability that decreases the apparent brightness of downwelling sunlight,

against which the bioluminescent counterillumination of

prey will then stand out (Muntz, 1976; Herring, 2002). In this

respect, Macropinna is probably well equipped for scanning the waters above for bioluminescent prey.

Large, bioluminescent siphonophores of the genus Apole mia are very common at lower mesopelagic depths in

Monterey Bay. Reaching lengths of ten meters or more, these slow-moving colonies accumulate a broad variety of

prey in their tentacles and gastrozooids, which except for

the presence of stinging tentacles, are open to appropriation by other animals (Robison, 1995, 2004). The ability of

Macropinna to scan the water overhead for potential prey, to

recognize bioluminescence against the background, and to move into a cluster of tentacles with its eyes protected, make

Apolemia a likely source of food. Fan-like fins have been

associated with fishes that maneuver around objects such as

siphonophores (Janssen et al., 1989).

Regardless of the specific source of prey, the particular morphology of the eyes of Macropinna would appear to allow at least two feeding modes: 1) with the body horizontal and the eyes directed upward, the fish spots food against the

lighted waters above. While the fish pivots its body to bring the mouth up for ingestion, the eyes remain locked on

target, rotating from dorsal to rostral relative to the body; 2) with the body horizontal, the eyes rotate from dorsal to

rostral while tracking the path of descending food, until it

reaches the level of the mouth. The discovery that Macro

pinna can change the position of its eyes resolves the

apparent paradox of how it can see to feed with eyes that are

directed away from its mouth. Whether this solution applies to Opisthoproctus, Dolichopteryx, and other fishes with

upward-directed tubular eyes, remains to be seen.

ACKNOWLEDGMENTS

We thank the pilots of the ROVs Ventana and Tiburon for their patience and skills in conducting these midwater

operations. The officers and crews of the R/V Point Lobos and

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.

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