Vision in the deep sea

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Abstract
The deep sea is the largest habitat on earth. Its three great faunal environments – the twilight mesopelagic zone, the dark bathypelagic zone and the vast flat expanses of the benthic habitat – are home to a rich fauna of vertebrates and invertebrates. In the mesopelagic zone (150–1000 m), the down‐welling daylight creates an extended scene that becomes increasingly dimmer and bluer with depth. The available daylight also originates increasingly from vertically above, and bioluminescent point‐source flashes, well contrasted against the dim background daylight, become increasingly visible. In the bathypelagic zone below 1000 m no daylight remains, and the scene becomes entirely dominated by point‐like bioluminescence. This changing nature of visual scenes with depth – from extended source to point source – has had a profound effect on the designs of deep‐sea eyes, both optically and neurally, a fact that until recently was not fully appreciated. Recent measurements of the sensitivity and spatial resolution of deep‐sea eyes – particularly from the camera eyes of fishes and cephalopods and the compound eyes of crustaceans – reveal that ocular designs are well matched to the nature of the visual scene at any given depth. This match between eye design and visual scene is the subject of this review. The greatest variation in eye design is found in the mesopelagic zone, where dim down‐welling daylight and bioluminescent point sources may be visible simultaneously. Some mesopelagic eyes rely on spatial and temporal summation to increase sensitivity to a dim extended scene, while others sacrifice this sensitivity to localise pinpoints of bright bioluminescence. Yet other eyes have retinal regions separately specialised for each type of light. In the bathypelagic zone, eyes generally get smaller and therefore less sensitive to point sources with increasing depth. In fishes, this insensitivity, combined with surprisingly high spatial resolution, is very well adapted to the detection and localisation of point‐source bioluminescence at ecologically meaningful distances. At all depths, the eyes of animals active on and over the nutrient‐rich sea floor are generally larger than the eyes of pelagic species. In fishes, the retinal ganglion cells are also frequently arranged in a horizontal visual streak, an adaptation for viewing the wide flat horizon of the sea floor, and all animals living there. These and many other aspects of light and vision in the deep sea are reviewed in support of the following conclusion: it is not only the intensity of light at different depths, but also its distribution in space, which has been a major force in the evolution of deep‐sea vision.

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