Fishes
Fishes are aquatic vertebrates which have gills and fins. 99% of the extant 32,000 species are ray-finned fish (in the Class Actinoptergii), so-called because they have bony or horny spines (rays) in their fins. Their vertebrae are also made of bone. Ray-finned fishes appeared 400mya. Teleosts, a sub-class of ray-finned fishes, account for 96% of extant species. Chondrichthyes is a class of fish where the skeleton is made of cartilage. Sharks, rays and skates belong to a subclass of cartilaginous fish called Elasmobranchii. Cartilaginous fish first appeared about 430Mya.
Some sharks have well-formed upper and lower eyelids which are mobile. Some also have a nictitating membrane, consisting of a fold in the lower eyelid which is drawn upwards and backwards across the eye by levator palpebrae nictitans, a muscle behind the eye innervated by the oculomotor (IIIrd cranial) nerve (Gruber S. a., 1975) (Gruber S. , 1977). The membrane is dense, opaque, covered by tiny tooth-like scales, and only protective, there being no requirement to moisten the cornea.
Nictitating membrane in a Lemon shark (Negaprion brevivirostris) from Gruber 1977
In the whale shark, Rhincodon typus (Elasmobranchii, Rhincodontidae), the eyeball can rotate and retract, protecting it from injury. During this process, white connective tissue from the retrobulbar space is displaced around the eyeball and partially fills the space where the eye used to be (Tomita, et al., 2020).
Schematic representation of rotation and retraction of the eyeball in a whale shark.
'Adipose' eyelids
Most bony fish do not blink; some have transparent ‘adipose eyelids’ which may cover most or all of the eye (Stewart, 1962). These are immobile.
One bony fish which can blink is the mudskipper (Takita, Larson, & Ishimatsu, 2011), which spends much of its time with its eyes protruding out of water while living in shallow waters. It can also climb onto the adjacent mud flats and live for prolonged periods out of the water. There are 10 genera and 32 living species of mudskipper. In the videos below played back at 20% of the recording speed, blinks and winks (unilateral blinks) are seen in two Australian species.
Giant mudskipper (Periophthalmodon freycineti)
Blink: globe retraction
Side view of a blink in a specimen* in a tidal creek in the Botanical Gardens in Cairns. The globe with a horizontally elongated pupil sits partially embedded on the top of a black pigmented turret with no obvious separation into upper or lower (medial or lateral) lids. During the blink, the globes retract into the head of the fish. As the globe retracts it disappears behind the 'lower lid’ or dermal cup. The 'upper lid' sinks with the eyeball during retraction. The dermal cup contains water and each time the globe retracts, the cornea is moistened. Also seen is the imbibing of water which causes swelling in the region of the gills. The fish absorbs oxygen from this water before releasing it through its gills. *Identified by Dr Helen Larson, Curator Emeritus, Fishes, Museum and Art Gallery of the Northern Territory.
Stills of a blink: a) Pre-blink. b) The globes start to retract into the head of the fish. c) The right globe disappears behind the dermal cup. The 'upper lid' sinks with the eyeball during retraction.
Wink in the same specimen seen from the front. The left globe retracts and the left 'lower lid' rises, partially then fully.
Barred mudskipper (Periophthalmus argentilineatus)
Blink: Globe retraction
Blink in a smaller species of mudskipper, also in Cairns. The pupil is elongated in the horizontal plane. *Identified by Dr Helen Larson, Curator Emeritus, Fishes, Museum and Art Gallery of the Northern Territory.
A wink followed by a blink in the same specimen
Comments
The dorsal position of the eyes and their elevation on turrets, suggests that the transition mudskippers made from water to land involved acquiring aerial vision while remaining partially submerged in water. This would enable them to prey on flying insects while lessening their chance of being preyed on themselves. As their pectoral fins evolved, allowing them to walk, they were able to make sorties onto land – mainly mudbanks, rocky shores and sandy beaches. Unless these sorties were brief, they now had to deal with corneas which were drying out and, as a result, unable to absorb atmospheric oxygen. There were of course, many other adaptations to a terrestrial life such as absorbing oxygen through the skin and gills, but these are not the subject of this book.
Mudskippers moisten their eyes by retracting them into their head where the equivalent of a lower lid, the dermal cup, contains a water reservoir – topped up while the fish is in water (Clayton, 1992). Such a system will only work while the fish spends part of its time in water. In order to venture afield, creatures exchanging a marine environment for a terrestrial one had to evolve another means of producing moisture for the corneas. Retracting the eyes into the head also affords them some protection, important for example in species preying on potentially injurious creatures such as crabs (Clayton, 1992).
The extraocular muscles of mudskippers are similar to, although longer (due to the turret) than other fish (Clayton, 1992). Indeed, the pattern of four rectus and two oblique muscles innervated by cranial nerves, III, IV and VI is common to all vertebrates (Cunha CM, Oliveira LE and Kfoury Jr. 2016) According to Walls (Walls, 1943), fish do not have retractor muscles and there is little information available on how mudfish retract their eyes. How this is done varies from species to species. For example, the giant guitarfish uses the inferior oblique extra-ocular muscle to retract the eye (Taketeru Tomita, 2016). Nor is there information on how mudskippers unretract their eyes.
Mudskippers often blink with one eye only (winking) which allows them to lubricate that eye while still keeping the other eye out for prey or predators.
While in water, the cornea exerts no refracting power, as the refractive indices of the cornea and water are the same. In most fishes, focussing on the retina is done by an almost spherical lens. Accommodation is done by to and fro movement of the lens. A spherical lens is less amenable to changes in shape, which is the means by which accommodation occurs in, for example, reptiles (Duke-Elder, 1958). In air, the addition of refraction by the fish cornea would cause myopia. The myopia has been corrected for in mudskippers by flattening of the lens (Kuciel et al., 2017).
Diagram of fishes eyes in water (left column) and air (right column): (a) Fully aquatic fish eye with a spherical lens focussing light on the retina (R) in water but, in combination with the cornea in air focussing before the retina (myopia). b) Mudskipper where a slightly flattened lens allows focussing of light on the retina in air but beyond the retina in water (hypermetropia) (Sayer, 2005)
References
Clayton, D. (1992). Mudskippers. Oceanogr. Mar. Biol. Annu. Rev, 31: 507-577.
Cunha, C. O. (2016). Comparative anatomy of the extraocular muscles in four Myliobatoidei rays (Batoidea, Myliobatiformes). J of Anatomy, 228 (5), 877-886.
Duke-Elder, S. (1958). Volume 1 of System of Ophthalmology; The eye in evolution. Mosby.
Gruber, S.H. 1977. "The Visual System of Sharks: Adaptations and Capability." Amer. Zool. 17:453-469.
Gruber, S.H. and Schneiderman, N. 1975. "Classical conditioning of the nictitating membrane response of the lemon shark (Negaprion brevirostris)." Behaviour Research Methods and Instrumentation 7(5):430-434.
Kuciel, M., Żuwała, K., Lauriano, E., Polgar, G., Malavasi, S., & Zaccone, G. (2017). Structure and Function of Sensory Organs. In Fishes out of water (pp. 138-169). Taylor and Francis.
Sayer, M. (2005). Adaptations of amphibious fish for surviving life out of water. Fish and Fisheries, 6(3):186 - 211.
Stewart, K.,W. June 1962. “Observations on the Morphology and Optical Properties of the Adipose Eyelid of Fishes”. Journal of the Fisheries Board of Canada, Volume 19, Number 6.
Takita, T., Larson H.K. and Ishimatsu A. 2011. "The natural history of mudskippers in northern Australia, with field identification characters." The Beagle. Records of the Museums and Art Galleries of the Northern Territory 27:189-204.
Taketeru Tomita, Kiyomi Murakumo Kei Miyamoto Keiichi Sato Shin-ichiro Oka Haruka Kamisako Minoru Toda. 2016. “Eye retraction in the giant guitarfish, Rhynchobatus djiddensis (Elasmobranchii: Batoidea): a novel mechanism for eye protection in batoid fishes”. Zoology, Volume 119, Issue 1, February 2016, Pages 30-35.
Tomita, T., Murakumo, Komoto, S., Dove, A., Kino, M., & Miyamoto, K. e. (2020). Armored eyes of the whale shark. PLoS ONE , 15(6): e0235342. https://doi.org/10.1371/journal.pone.0235342.
Walls, G. (1943). The vertebrate eye and its adaptive radiation. Bloomfield Hills, Mich.: Cranbrook Institute of Science. Cranbrook Press. Bulletin no 19.