Crocodilia
Crocodilia have evolved a unique way of protecting their eyes whereby the upper eyelid, in some species heavily reinforced with a bony moveable ‘brow’ covered in horny scales (scutes), closes like a trapdoor on a hinge over the orbit as the eyeball retracts. Like lizards, crocodilia have two types of blink:
1) Nictitating membrane blink
Here, the movement of the nictitating membrane occurs with minimal globe retraction.
Nictitating membrane blink with minimal globe retraction (shown by the slight sinking of both upper lids) in an adult freshwater crocodile (Crocodylus johnsoni).
ANTERIOR POSTERIOR
The thickened leading edge is seen at 160ms and the cornea is covered by 400ms. Vessels are visible in the transparent nictitating membrane.
Nictitating membrane blink with minimal eyelid movement (due to globe retraction) in a hatchling American alligator (Alligator mississippiensis).
The membrane has just covered the pupil at 80ms and has covered the cornea completely by 120ms. The membrane is almost transparent.
Nictitating membrane blink in a saltwater crocodile (Crocodylus porosus).There is almost no globe retraction and the eye moves as the body turns. Played at 30% speed.
Nictitating membrane blink in a saltwater crocodile. There is minimal globe retraction causing slight movement of the upper and lower lids. Played at 30% speed.
ANTERIOR POSTERIOR
The thick upper and lower eyelids remain still as the opaque nictitating membrane moves diagonally across the eyeball which has not retracted. Also seen is the heavy ‘brow’ to which the upper eyelid is attached.
Nictitating membrane blink with globe retraction in a Phillipine crocodile (Crocodylus mindorensis). Played back at 30% speed.
2) Eyelid blinks
Here, either eyelid or more commonly both eyelids are involved in conjunction with the nictitating membrane There is also globe retraction.
Eyelid blink in which the globe retracts, the nictitating membrane crosses and the lids come slowly together, the lower lid moving more than the upper lid, in an adult American alligator. Played at 30% speed.
The two lines mark the positions of the upper and lower lids at rest. At 240ms, the nictitating membrane is moving across and the lower eyelid is elevating. The upper eyelid has also moved down slightly.
Compared with their pre-blink positions, at 1880ms the upper lid has descended a little, but the lower eyelid has risen more.
Eyelid blinks are usually accompanied by globe retraction causing sinking of the upper eyelid and brow into the orbit. This is best seen in profile.
Opening then closing of the right eye in a freshwater crocodile. The eye moves out of the orbit from its retracted position, raising the upper lid and brow. At the same time, the lower lid descends. The reverse then occurs.
At 0ms, the right upper eyelid and brow are seen in profile above the eye. At 920ms, they have sunk (arrow), the lower eyelid has elevated and the eye is no longer visible. The left eye remains open.
Sinking of the horny brow above the left upper eyelid as the globe retracts in an American alligator.
The lines mark the upper and lower positions of the brow at 355ms after the onset of the blink.
In the Nile crocodile (Crocodylus niloticus), globe retraction is so marked that, as both eyelids come together, they sink momentarily into the orbit).
Nile crocodile. At the onset of the blink, the upper and lower lids approach each other and the nictitating membrane crosses. The globe then retracts causing the eyelids to briefly sink into the orbit.
At 4840ms, the eyelids lie in a depression in the orbit.
In the saltwater crocodile, the upper eyelid almost covers the eye in the drowsy state.
Saltwater crocodile. In the drowsy state at 0ms, the upper eyelid has almost covered the eye. At 7360ms, the lower lid has risen to meet it as the crocodile falls asleep.
Freshwater crocodile. As the head submerges, the lower lid elevates.
Played back at 30% speed.
At 370ms, the lower eyelid has risen to almost cover the eye as the crocodile begins to submerge.
Freshwater crocodile. As the head submerges, the nictitating membrane crosses, the lower lid elevates and the globe retracts.
At 1400ms after the onset of the blink, the globe has retracted, the lower lid has elevated and the cornea is covered by the nictitating membrane.
Juvenile saltwater crocodile. The lower eyelid slowly rises during what appears to be a state of drowsiness.
The muscles involved in blinking in crocodilia are shown in the figures below.
Medial view of the eyeball in a crocodilian. The nictitating membrane is drawn across the eye by contraction of the pyramidalis muscle (Pyr) pulling on the tendon of the membrane (n). Retraction of the eye is done by the retractor bulbi muscle (R.b). (Walls 1963).
Medial view of the eyeball of the Alligator mississippiensis. The pyramidalis muscle is here labelled Retr. membr. nict. (retractor membranae nictitantis). Of note is the muscle labelled Retr. palp. sup (retractor palpebrae superioris), which is attached to the upper eyelid. There is also a depressor palpebrae inferioris (Wedin 1953) (Underwood 1970).
In summary, in crocodilia, the nictitating membrane is able to move independently of globe retraction or lower eyelid elevation. This action is performed by the pyramidalis muscle. Nictitating membrane blinks presumably cleanse and lubricate the cornea with the oily secretions of the Harderian gland and the watery secretions of the lacrimal gland when the crocodile is out of water. The nictitating membrane may also have a protective function when the crocodile is swimming underwater, covering the cornea while allowing some light to enter the pupil.
Eyelid blinking begins with passage of the nictitating membrane. Then the eyeball retracts and as it does so, the upper eyelid and the ‘brow’ to which it fixed, sink into the orbit on their hinge. It probably does this passively initially, drawn in as the eyeball retracts beneath it, but the movement is also reinforced by contraction of the retractor bulbae superioris muscle which presumably holds the lid down tightly. This would be important in the face of a large flailing prey. While retraction of the upper eyelid is the most visible movement in this type of blink, the full closure of the eye is performed by the lower eyelid which slides up over the cornea as the eyeball retracts. The lower eyelid can also rise independently from any movement of the upper eyelid. Reflex lower eyelid closure in response to submergence has been described (Garrick 1974). The depressor palpebrae inferioris draws the lower eyelid down at the end of a blink
Innervation of the muscles involved in blinking:
Retractor bulbi: Abducens nerve (VIth cranial nerve)
Pyramidalis: Abducens nerve
Retractor palpebrae superioris: --
Depressor palpebrae inferiors: --
Comment
The upper lid has evolved to provide protection from pressure and blows, the lower lid helps protect the eye from surface debris when it is half submerged. Retraction protects the eyeball from injurious blows. The nictitating membrane lubricates and cleans the cornea and protects it during underwater travel. In sleep, the eye retracts and both lids close.
References
Garrick, L.D. and Saiff, E.I. 1974. "Observations on submergence reflexes of Caiman sclerops." Journal of Herpetology 8(3):231-236.
Underwood, G. 1970. "The eye." In The Biology of Reptilia Vol 2, by C and Parsons, T.S (Eds) Gans, 1-97. New York: Academic Press.
Walls, GL. 1963. The vertebrate eye and its adaptive radiation. New York and London: Hafner.
Wedin, Bertil. 1953. "The origin and development of the extrinsic ocular muscles in the alligator." Journal of Morphology 303-335.