Barreleye Fish Vision: Eyes Built for the Mesopelagic Zone

Introduction

At depths of about 600 to 800 metres in the Pacific Ocean, in the permanent darkness of the mesopelagic zone where the last traces of sunlight fade into an eternal dim blue, the barreleye fish hovers motionless in the water column, its body horizontal, its enormous green eyes directed straight upward. Barreleye fish vision is built for exactly this: collecting the faint light that filters down from far above.

The Barreleye Fish, Macropinna microstoma, is one of the most visually arresting animals discovered in the deep sea: its head is enclosed in a completely transparent, fluid-filled dome through which its brilliant green, barrel-shaped eyes are clearly visible, rotating slowly as the fish scans the water above it for the silhouettes of potential prey against the faint downwelling light.

This remarkable anatomy was not fully understood for roughly seven decades after the species was first described, because the transparent dome often collapses or is lost when fish are brought to the surface in trawl nets, leaving only a flat, structureless head from which the actual eyes project upward, leading scientists to misidentify the olfactory organs as the eyes, and to misunderstand the optical system entirely.

It was not until 2008, when researchers from the Monterey Bay Aquarium Research Institute published a description based on video footage of living Barreleye Fish recorded using remotely operated vehicles at depth, that the intact dome and the rotating eyes within it were first documented.

The Barreleye Fish is one of the most cited examples of the bizarre and poorly understood life that exists in the deep ocean, and it illustrates with elegant clarity how much of deep-sea biology remained unknown, or actively misunderstood, before the era of deep-sea ROV exploration.

Etymology and Classification

The common name ‘Barreleye’ is a direct reference to the tubular, barrel-shaped eyes visible through the transparent dome. ‘Spookfish’, the alternative common name used in some regions, reflects the eerie appearance of the fish’s transparent head.

The genus name Macropinna is formed from the Greek makros (large) and pinna (wing or fin), referring to the fish’s prominent fins. The species epithet microstoma combines the Greek mikros (small) and stoma (mouth), accurately describing the species’ tiny, downward-pointed mouth.

Macropinna microstoma is classified within the family Opisthoproctidae, the barreleyes or spookfishes, a small family of deep-sea fishes containing nine genera. Opisthoproctidae is placed within the order Argentiniformes, a group of deep-water fishes that includes smelts and argentines.

The opisthoproctids are notable as a group for their unusual eyes: most have upward-directed tubular eyes (like Macropinna), and the brownsnout spookfish Dolichopteryx longipes is the only vertebrate known to use a mirror, as well as a lens, to focus images in its eyes.

Barreleye Fish Physical Description

The Barreleye Fish’s body is stout and deep-bodied, approximately 15 centimetres long. Most of the body is covered in large scales and is dark brown. The fins are well-developed, including broad pectoral fins that support the horizontal hovering posture.

The defining feature is the transparent dome. This structure covers the top of the head and the eyes. The dome is a tough, flexible, transparent shield. Within it, fluid bathes the eyes, which can rotate up and forward.

The optical properties of the dome, and whether it functions as a focusing element, are not well established.

The eyes themselves are barrel-shaped and tipped with bright green lenses. The green pigments may filter out sunlight coming directly from the sea surface, helping the fish spot the bioluminescent glow of jellyfish or other animals overhead.

The two small, dark spots at the front of the fish’s head, immediately adjacent to the mouth, are the nares (nostrils), olfactory organs connected to the olfactory epithelium. These were long misidentified as eyes in dead specimens.

Barreleye Fish Habitat and Range

Macropinna microstoma inhabits the mesopelagic zone of the Pacific Ocean, at depths of about 600 to 800 metres. The confirmed distribution includes the eastern Pacific from the Bering Sea southward through California and Baja California, and the western Pacific in the vicinity of Japan.

Because the species is known primarily from specimens collected incidentally in research trawls (which damage the dome) and from ROV observations (which are geographically limited), the full distribution may be substantially more extensive.

At the depths this fish inhabits, the water is cold, under high pressure, and permanently dark except for the diffuse downwelling light that penetrates from above and the scattered bioluminescent signals produced by the many bioluminescent organisms of the mesopelagic zone. The fish is typically observed hovering motionless or moving very slowly, conserving energy in an environment where prey is sparse and metabolic rates must be low.

The fish is apparently closely associated with aggregations of siphonophores, colonial cnidarian organisms related to jellyfish that extend long, stinging tentacles into the water column to catch zooplankton. Barreleye Fish have been observed hovering beneath siphonophore colonies, their eyes directed upward toward the tentacles.

Barreleye Fish Vision in the Mesopelagic Zone

The visual system of the Barreleye Fish is adapted for detecting prey in the extreme low-light conditions of the mesopelagic zone. The primary adaptation is the large, tubular eyes with their wide aperture, which maximise the collection of available light, a strategy analogous to using a wide-aperture camera lens in low-light photography.

The retina is dominated by rod photoreceptors (which detect light intensity rather than colour) rather than cones (which detect colour), consistent with the emphasis on sensitivity over chromatic resolution in a dark environment.

The ability to rotate the eyes, from directly upward (to see objects silhouetted against the faint downwelling light above) to directly forward (to track prey that has been located and is being approached), is unusual among fish and allows the Barreleye to use two different visual strategies: silhouette detection above (using the downwelling light as a background) and direct image-forming vision ahead.

The leading hypothesis for the species’ primary foraging strategy involves hovering beneath siphonophore colonies and using the upward-directed eyes to observe prey items caught in the siphonophore tentacles, then swimming upward to steal these items. This strategy, kleptoparasitism (stealing from another animal’s hunting effort), would explain both the eye orientation and the association with siphonophores.

The fish’s small mouth and its apparent lack of speed or agility further support a feeding strategy based on small, immobile prey rather than active pursuit.

Discovery of the Transparent Dome

For approximately 70 years after the formal scientific description of the species, the transparent dome was unknown, because it is usually destroyed when specimens are brought up from depth. The species was first described by Chapman in 1939, and old drawings do not show the dome.

Marine biologists long believed that the eyes were fixed in the head and could only look upward. The rotation of the eyes was not directly observed until the ROV footage.

The resolution came in 2008, when Bruce Robison and Kim Reisenbichler of the Monterey Bay Aquarium Research Institute published a paper in the journal Copeia describing ROV video footage of living Barreleye Fish observed at depth off the California coast. The footage clearly showed the intact, fluid-filled dome and the rotation of the eyes within it, and the accompanying paper provided the first accurate anatomical description of the species’ visual system in the living state.

The findings were publicised by the institute in February 2009 and brought the species to widespread public attention.

Mesopelagic Ecology and the Deep-Ocean Food Web

The Barreleye Fish is one of many mesopelagic fish species that form a crucial, largely invisible trophic link in the global ocean food web. Mesopelagic fish, those inhabiting depths of roughly 200 to 1,000 metres, are very abundant in the open ocean.

They feed on zooplankton and smaller organisms, and are in turn consumed by tuna, billfish, cetaceans, and seabirds, making the mesopelagic zone a critical energy transfer pathway between the productive surface waters and the deep sea and upper water predators.

The Barreleye Fish plays its part in this system as a mesopelagic consumer, though its dietary habits, as noted, are unusual and possibly heavily dependent on kleptoparasitism of siphonophore-caught prey rather than direct predation of active animals.

Conservation Status

Deep-sea fish in general are poorly represented in formal conservation assessments because of the difficulty of population monitoring and the historical assumption that deep-sea environments were remote from human impacts.

In practice, mesopelagic species may be affected by several anthropogenic pressures including deep-sea trawling (which physically disturbs habitats and incidentally captures mesopelagic species), climate change (which affects the vertical temperature and oxygen structure of the ocean, potentially shifting the depth ranges of mesopelagic organisms), and the emerging interest in commercial harvesting of mesopelagic fish for fishmeal and omega-3 oil production.