Macropinna microstoma and the Paradox of Its Tubular Eyes

Macropinna microstoma and the Paradox of Its Tubular Eyes
Author(s) :Bruce H. Robison and Kim R. Reisenbichler
Source: Copeia, 2008(4):780-784. 2008.
Published By: The American Society of Ichthyologists and Herpetologists
DOI:
URL: http://www.bioone.org/doi/full/10.1643/CG-07-082
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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.
T
HE upward-looking, tubular eyes of some mesopelagic 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).
1
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 forwardlooking 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 subarctic 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 36u429N, 122u029W over the axis of the
Monterey Submarine Canyon where the bottom depth is
approximately 1600 m. The third was at 35u389N, 122u449W
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.
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.
DOI: 10.1643/CG-07-082
F 2008 by the American Society of Ichthyologists and Herpetologists
Robison and Reisenbichler—Tubular eyes of Macropinna microstoma
781
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 36u259N,
123u199W, 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 (,10u 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
30u 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 Chapman (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. Anatomically 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, unobstructed 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 of the skull of Macropinna, Chapman (1942)
noted that the large, translucent suborbital bones do not
Robison and Reisenbichler—Tubular eyes of Macropinna microstoma
Fig. 3. Chapman’s (1942) mesial view of the left eye of Macropinna
microstoma. Abbreviations: RS 5 rectus superior, L 5 lens, OS 5
obliquus superior, OI 5 obliquus inferior, RIN 5 rectus internus, RI 5
rectus inferior, RE 5 rectus externus, OP 5 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 comparable 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,
783
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 Apolemia 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 Macropinna 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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