Macropinna microstoma and the Paradox of Its Tubular Eyes
Transcription
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 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. PersonIdentityServiceImpl 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) [email protected]; and (KRR) [email protected]. 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. LITERATURE CITED Bertelsen, E., and O. Munk. 1964. Rectal light organs in the argentinoid fishes Opisthoproctus and Winteria. Dana Report 62, Copenhagen, Denmark. Bone, Q., and N. B. Marshall. 1982. The Biology of Fishes. Blackie, Glasgow. Bradbury, M. G., and D. M. Cohen. 1958. 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