Crocodilia
Introduction. Crocodilia (alligators, caimans, crocodiles and gharials), birds, dinosaurs (extinct) and pterosaurs (extinct) all trace their ancestry back to archosaurs (Green & al, 2014). Crocodilians first appeared 95Ma and diverged from birds 240Ma. Compared with birds, crocodilia have changed little and there are only 22 extant species compared with 10,000 species of birds.
Present study (Morris and Parsons 2023). Videos were made of 15 species of Crocodilia from 3 families. Nictitating membrane blinks were seen in 15 species, 3 with visible globe retraction, 4 with no evident globe retraction) and 11 associated with globe retraction and elevation of the lower lid. In five species, there was lower lid elevation and globe retraction without visible movement of the nictitating membrane. In no case was there upper lid blinking, though in some cases the upper lid sank a little into the orbit as the globe retracted.
Table summarising findings. Blink types in 15 species of Crocodile: NMBl: nictitating membrane blink; GlR: Globe retraction; LLBl: Lower lid blink
No blinks
Examples
Family: Crocodylidae
Species: Fresh water crocodile (Crocodylus johnsoni)
Blink type: Nictitating membrane and lower lid with 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
Nictitating membrane blink. The thickened leading edge is seen at 160ms and the cornea is covered by 400ms. Vessels are visible in the transparent nictitating membrane.
a) Pre-blink. Vertically elongated pupil. b) Nictitating membrane starts to emerge from inner canthus. Slight narrowing of palpebral fissure as globe retracts. c) Nictitating membrane with thickened marginal rim, travels diagonally across the pupil. d) Maximal blink. Transparent nictitating membrane.
Lower lid blink with globe retraction in the right eye. 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.
Stills from the video above. 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.
As the head submerges, the lower lid elevates.
Stills from video above. At 370ms, the lower eyelid has risen to almost cover the eye as the crocodile begins to submerge.
As the head submerges, the nictitating membrane crosses, the lower lid elevates and the globe retracts.
Stills from video above: 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.
Submerging. a) Pre-submerging. b) Water covers left lower eyelid and palpebral fissure narrows as globe retracts. c) Left lower lid elevates
a) Pre-submerging. b) Lower lid elevates. Upper lid sinks with globe into orbit. d) Lower lid rises further. e) Lower lid drops a little. e) Now nearly submerged. Nictitating membrane covers eye which is almost closed.
Submerging: lower lid rises and nictitating membrane crosses as the head slowly sinks into the water
Family: Crocodylidae
Species: Cuban crocodile (Crocodylus rhombifer)
Blink type: Nictitating membrane and lower lid.
The nictitating membrane moves across the left eye from the inner canthus then the lower lid rises slowly and stays shut for 24 seconds before springing open. Is this a blink or a brief nap albeit only involving one eye.
Family: Crocodylidae
Species: Siamese crocodile (Crocodylus siamesisk)
Blink type: Nictitating membrane and lower lid.
The globe retracts causing the eyelids to sink and come together. The nictitating membrane can be seen between the two. The lower lid pushes up against the upper lid, then the nictitating and lower lid spring back to their resting position.
Family: Crocodylidae
Species: West African slender snouted crocodile (Mecistops cataphractus)
Blink type: Lower lid elevated with sleep,
Family: Crocodylidae
Species: African dwarf crocodile (Osteolamus tetraspis)
Blink type: Nictitating membrane, partial lower lid and globe retraction.
The globe retracts causing the lids to come together (lower more than upper), though not meet, and the nictitating membrane crosses the eye from the inner canthus. The upper lid has multiple grooves giving an appearance like eye lashes. After 28 seconds the nictitating membrane and lower lid spring back into their resting position.
Family: Crocodylidae
Species: Saltwater crocodile (Crocodylus porosus)
Blink type: Nictitating membrane alone; nictitating membrane with globe retraction; nictitating membrane, globe retraction and lower lid elevation.
Elevated position of eyes, laterally placed bit capable of binocular vision and with horny protection above them
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.
Nictitating membrane blink with narrowing of palpebral fissure due to globe retraction
In sunlight. a) Pre-blink. Vertically aligned pupil. b) Nictitating membrane moves obliquely across the eye from the inner canthus. c) Maximal blink.
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.
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.
Juvenile saltwater crocodile. The lower eyelid slowly rises during what appears to be a state of drowsiness.
Juvenile saltwater crocodile. The lower eyelid slowly rises during what appears to be a state of drowsiness.
Nictitating membrane blink with narrowing of palpebral fissure due to globe retraction (or elevation of lower lid – hard to tell
Juvenile. a) Pre-blink. Pupil fully dilated and almost circular (has vertically elongated slit pupils in light). b) Nictitating membrane rises obliquely from inner canthus. c) Maximal blink. Eye covered by semi-translucent nictitating membrane. Narrowed palpebral fissure due to globe retraction.
Nictitating membrane blink with narrowing of palpebral fissure due to globe retraction
Juvenile a) Pre-blink. Vertically elongated pupils almost fully dilated. b) Palpebral fissure narrows as globe retracts. c) Nictitating membrane reaches pupil from inner canthus. d) Semi-translucent nictitating membrane covers eye. e) Maximal blink. f) Post-blink.
Nictitating membrane blink with elevation of lower lid
Juvenile a) Pre-blink. Vertically elongated pupils almost fully dilated. b) Palpebral fissure narrows as globe retracts. c) Nictitating membrane reaches pupil from inner canthus. d) Semi-translucent nictitating membrane covers eye. e) Maximal blink. f) Post-blink.
Juvenile a) Pre-blink. b) Palpebral fissure narrows as globe retracts. Nictitating membrane reaches pupil from inner canthus. c) Lower lid rises. Maximal blink
Family: Crocodylidae
Species: Philippine crocodile (Crocodylus mindorensis)
Blink type: Nictitating membrane, globe retraction and lower lid elevation.
Nictitating membrane blink with globe retraction in a Phillipine crocodile (Crocodylus mindorensis). From this angle, the membrane appears to be arising from inside the lower lid. Played back at 30% speed.
Family: Crocodylidae
Species: Nile crocodile (Crocodylus niloticus)
Blink type: Nictitating membrane, globe retraction and lower lid elevation.
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.
Family: Gavialidae
Species: Gharial (Gavials gangeticus)
Blink type: Nictitating membrane, globe retraction and lower lid elevation.
The lower lid rises and the nictitating membranes crosses the eye from the inner canthus. After 21 seconds they both spring back to their resting positions,
Nictitating membrane blink (with no globe retraction)
Family: Alligatoridae
Species: American alligator (Alligator mississippiensis)
Blink type: Nictitating membrane alone; nictitating membrane with globe retraction; nictitating membrane, globe retraction and lower lid elevation.
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.
Nictitating membrane and lower lid blink in the left eye: At 240ms, the nictitating membrane has partially covered the eye. At 1880ms the lower lid has risen to close the eye. The lines show that the upper lid has fallen a little, sinking into the orbit as the globe retracts.
a) Pre blink. Note heavy brow and visible nictitating membrane in the inner canthus. b) Opaque nictitating membrane with thickened marginal rim rises obliquely. c) Maximal blink. Hardly any change in the size of the palpebral fissure suggesting no globe retraction.
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.
Nictitating membrane blink with minimal eyelid movement (due to globe retraction) in a hatchling American alligator (Alligator mississippiensis).
Nictitating membrane (blue), left eye at 0, 80 and 120ms.
A pair of hatchling American alligators. a) Pre-blink. Note prominence of globe in the hatchling on the right showing that the globe of the left-hand hatchling is a little retracted. b) Nictitating membrane arising from the inner canthus of the right-hand hatchling half covers the globe. c) Maximal blink. The eye is covered by a transparent nictitating membrane and the lower lid is slightly elevated. The upper lid has not moved showing that the lower lid has been elevated and there has been no globe retraction.
Hatchling. Showing that the position of the eyes would allow binocular vision
The mechanism of blinking in crocodilia
The schematic figure above and the drawing from a dissection below shows the back of an alligator eye: a) Retractor bulbi muscle. b) Quadratus muscle c) Nictitating membrane tendon. Adapted from Walls (Walls, 1943).
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The lower lid and nictitating membrane are able to move independently as is globe retraction. The membrane has a cartilage (Gans, 1970). The retractor bulbi and quadratus muscles are supplied by the VIth cranial nerve. Other muscles involved in blinking include: depressor palpebralis inferior and levator palpebralis superioris. (Gans, 1970). Hardner’s gland discharges on the inner face of the nictitating membrane. Drainage of tear fluid is through 3-8 canaliculi on the margin of the lower lid which join the lachrymal duct.
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).
Summary. Two main types of blink were observed. The nictitating membrane blink was often accompanied by mild globe retraction shown by slight narrowing of the palpebral fissure. The membrane rose obliquely from the inner canthus except in the Phillippines crocodile where it appeared to rise from behind the lower lid. The lower lid blink was accompanied by movement of the nictitating membrane and marked globe retraction. In some species, a bony moveable ‘brow’ covered in horny scales (scutes), closed like a trapdoor on a hinge over the orbit as the eyeball retracted, providing extra protection from the flailing limbs of preys.​
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, initially passively but then by contraction of the branch of retractor bulbae superioris muscle which inserts into the upper lid. 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.
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The retractor bulbi and pyramidalis muscles are supplied by the abducens nerve (VIth cranial nerve)​​
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References
Garrick, L.D. and Saiff, E.I. 1974. "Observations on submergence reflexes of Caiman sclerops." Journal of Herpetology 8(3):231-236.
Morris, J.G.L. and Parsons, J.J. The Various Ways in Which Birds Blink. Animals 2023, 13, 3656. https://doi.org/10.3390/ani13233656
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.
