Lizards
(Orders squamata and rhyncocephalia)
Introduction. The order squamata (scaled reptiles) includes snakes and lizards and has over 10,000 species. Very similar in appearance to squamata lizards is the tuatara, the sole species within the order of rhyncocephalia. Classifications based on morphology alone have been modified as DNA based genomic information has become available (Wiens & al, 2012) (Pyron, 2013). The lineage of crown group squamates (those which have extant species) can be traced back to the period immediately after the Triassic-Jurassic extinction event 201Mya.​​
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Present study. 27 turtles from the order of squamata and one from the order of rhyncocephalea were studied. Blinks included those involving:
1) just the nictitating membrane
2) the nictitating membrane and globe retraction (shown by the eyelids closing slightly as the eye beneath them sank into the orbit)
3) nictitating membrane, globe retraction and elevation of the lower eyelid
4) elevation of the lower lid alone
5) globe retraction alone.
In one case, the nictitating membrane blink was accompanied by an upper lid blink. In general, nictitating membrane blinks were brief, while lower lid blinks were slow and prolonged, sometimes blending into sleep. As with turtles, the lower lids were segmented.
The table below summarises the findings.
Examples
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Class Reptilia
Order Squamata
Family Varanidae
Species Komodo dragon (Varanus komodoensis)
Blink a: Globe retraction with no blink
Video of globe retraction at original speed.
The palpebral fissure narrows as the eyeball retracts and the eyelids sink into the orbit.
Blink b: Retraction of the eyeball followed by lower lid blink
a) Pre-blink. b) and c) Palpebral fissure narrows as globe retracts. d) Lower lid elevates. e) Globe unretracts and lower lid falls. f) Post- blink.
Lower lid blink with globe retraction.
Blink c: Lower lid elevation with no globe retraction
Blink d: Nictitating membrane blink with slight globe retraction
a) Pre-blink. b) Slight globe retraction. Nictitating membrane emerges from inner canthus. Note line of pigment parallel to the edge of the membrane. c) Nictitating membrane almost covers the eye. d) Maximal blink. e) Nictitating membrane starts to withdraw. f) Post-blink.
Stills from video showing minimal eyelid movement. The slight narrowing of the palpebral fissure is due to the eyelids sinking into the orbit as the globe retracts.
At 120ms, the eyeball has retracted causing the upper and lower eyelids to sink into the orbit and the nictitating membrane has covered the cornea.
Lower lid blink: a) Pre-blink showing three segments of the lower lid (orange) separated by creases. b) Blink involving elevation of all three segments of the lower lid with a further crease in the upmost segment covering the pupil. The upper lid has been pushed up a little. c) Sagittal plane of the eye showing the three segments of the lower eyelid. d) As for c), the lower lid covers the cornea​​
Order Squamata
Family Varanidae
Species Merten's water monitor (Varanus mertensi)
Blink type: Globe retraction with nictitating membrane blink
Globe retraction and nictitating membrane blink played at 30% speed
Semi-submerged in water. a) Pre-blink. Note overhanging upper lid. b) Slight narrowing of palpebral fissure as eye retracts. d) Semi-translucent nictitating membrane appears from inner canthus. d) and e) Eye covered by nictitating membrane. f) Post-blink
Order Squamata
Family Varanidae
Species Lace monitor (Varanus varius)
Blink a: Nictitating membrane blink
Blink b: Lower lid blink
Lower lid blink and globe retraction. Then globe unretraction pushing upper lid up. Played at original recording speed.
Order Squamata
Family Varanidae
Species crocodile monitor (Varanus salvadorii)
Blink: Globe retraction with nictitating membrane blink
Played at 30% speed
a) Pre-blink. b) Globe retracts drawing upper lid beneath the brow. Opaque nictitating membrane covers eye. c) Globe un-retracts. d) Post- blink
Order Squamata
Family Varanidae
Species Perentie (Varanus giganteus)
Blink a: Nictitating membrane blink on head movement
Nictitating membrane blink with slight elevation of the upper lid, on head turn. Played back at 10% speed.
a) Pre-blink. Note overhanging upper lid which shelters the eye from the sun. b) Upper lid rises a little as nictitating membrane appears out of inner canthus. c) Full blink with semi-transparent nictitating membrane. d) Post-blink.
Blink b: Globe retraction and elevation of lower lid
Lower lid elevation following a meal in a drowsy perentie (Varanus giganteus).
a) Pre-blink. b) Lower lid elevates a little. c) Maximal blink with globe retraction causing depression of the lower lid. No movement of the upper lid associated with globe retraction.
Order Squamata
Family Agamidae
Species Inland bearded dragon (Pogona viticeps)
Blink a: Lower lid elevated in sleep. Upper lid depressed with downward gaze.
Played at 30% speed
a) Asleep with eye closed. b) Lower lid falls as it wakes up. c) Eye fully open with upper eyelid pushed up as it looks up
Order Squamata
Family Agamidae
Species Frilled lizard (Chlamydosaurus kingii)
Blink type: Nictitating membrane blink on eye movement
Order Squamata
Family Agamidae
Species Philippine sailfin lizard (Hydrosaurus postulates)
Blink type: Lower lid and nictitating membrane blink with globe retraction (10% playback speed)
Order Squamata
Family Teiidae
Species Northern Caiman lizard (Dracaena guianensis)
Blink type: Lower lid blink
Asleep with white lower lid elevated. Lower lid then descends
Blink type: Nictitating membrane blink (10% playback speed)
Order Squamata
Family Iguanidae
Species Fijian crested iguana (Brachylophus vitiensis)
Blink type: Lower lid elevation after eye movement
Note red sclera. a) Looking forward. b) Looking to the side. c) Lower lid has elevated.
Order Squamata
Family Iguanidae
Species Green iguana (Iguana iguana)
Blink type On upward eye movement, the globe retracts and the nictitating membrane moves across the eye from the inner acanthus
The figure above shows stills from the video. a) Pre-blink showing partial descent of the upper lid with downward gaze (as occurs in humans). b) The eye and upper lid rise. and the nictitating membrane partially cover the pupil. c) The nictitating membrane covers the eye. The palpebral fissure has narrowed as the globe retracts. d) Post- blink
Order Squamata
Family Egerniidae
Species Soloman Island skink (Corsica zebra)
Blink type: Globe retraction with no blink
Order Squamata
Family Shinisaurisdea
Species Chinese crocodile lizard (Shinisaurus crocodilurus)
Blink type: Upper lid and nictitating membrane
The figure above shows a nictitating membrane with upper lid blink in the left eye: a) Pre-blink showing a sliver of nictitating membrane (blue) in the medial canthus. b) The upper lid (orange) descends and the nictitating membrane partially covers the pupil. c) The upper lid has returned to its resting position and the nictitating membrane is starting to return to its resting position.
Mechanism by which the nictitating membrane is drawn across the eye in Squamata
The figure above shows the back of the lizard eye. a) Retractor of the quadratus muscle b) Nictitating membrane tendon c) Quadratus muscle; d) Retractor bulbi muscle. Adapted from Walls (Walls, 1943). By having two muscles, quadratus and its retractor effectively in series, pulling on the nictitating membrane tendon, the membrane can be made to move a greater distance.
The figure above compares the width of the iris when it is constricted (left) and dilated (right). This shows that the dilator muscles of the iris are able to approximately halve their length to achieve maximal pupillary dilatation. Assuming it has similar contractile properties, the quadratus muscle would have to be double the width of the visible part of the eye in order to cover it with the nictitating membrane
The nictitating membrane is able to move independently from the upper and lower eyelids. The retractor of quadratus muscle, the quadratus muscle and the retractor bulbi muscle are all supplied by the VIth cranial nerve.
Order Squamata
Family Chamaeleonidae
Species Common chameleon (Chameleon chameleon)
Blink type: No blinks. Eyelids are fused together to form a turret which can move around. Independent eye movements can also be seen.
The eyes of chameleons lie outside the bony protection of the orbits. This prominent position gives them a much wider potential field of vision than any other creature though this depends on the eyes also having a wide range of movements for the visual field of each eye is narrow. In order to scan the landscape around them they move their eyes jerkily as we would move our heads if we were looking through a rolled-up newspaper. The 'turret' in which the eye lies evolved from the upper and lower eyelids, now fused together except for a narrow aperture, through which the eye peers. Protection of the eye comes from the horny skin of the eyelids below which there is a layer of muscle and a bony plate. The eyes move independently ('uncoupled') until the chameleon fixates upon an object whereupon the eyes come together providing stereoscopic vision. So chameleons cannot blink.
Order Squamata
Family Chamaeleonidae
Species Veiled chameleon (Chamaeleo calyptratus)
Blink type: No blinks. Wide amplitude of movements in the left eye
Order Squamata
Family Eublepharidae
Species Leopard gecko (Eublepharis macularius)
Blink type: Upper and lower eyelid. No visible nictitating membrane. Many geckos have fused transparent eyelids which they clean with their tongues.
Order Rhyncocephalia
Species Tuatara (Sphenodon punctatus)
Blink type: Nictitating membrane blink
Nictitating membrane, right eye: a) Pre-blink, showing a vertically elongated pupil and resting nictitating membrane (blue). b) The nictitating membrane reaches the pupil. The lower lid has not moved. c) The nictitating membrane has covered the eye. There is no movement of the eyelids.
Mechanism by which the nictitating membrane is drawn across the eye in a tuatara
The figure above shows the back of the tuatara eye: (a) The retractor bulbi muscle; (b) The tendon of the nictitating membrane, running through the retractor bulbi muscle and inserting onto the dorsal wall of the orbit (c). Adapted from Walls (Walls, 1943). The nictitating membrane is pulled across the eye when the retractor bulbi muscle contracts. The lower lid moves independently, by the action of the orbicularis oculi muscle. The retractor bulbi muscle (which evolved from the lateral rectus muscle) is supplied by the VIth cranial nerve.
In summary, in lizards the globe can retract without involving the lower eyelid. The nictitating membrane is also able to move independently from the lower lid, unlike turtles. But movement of the nictitating membrane is always accompanied by globe retraction. In lizards, some blinks primarily involve globe retraction with movement of the nictitating membrane. In other blinks, the lower eyelid elevates with or without retraction of the globe. Walls (1963) refers to a muscle akin to but not homologous with orbicularis oculi in mammals, which elevates the lower eyelid.
​The retractor bulbi and bursalis muscles are supplied by the abducens nerve (VIth cranial nerve).
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Reference
Walls, GL. 1963. The vertebrate eye and its adaptive radiation. New York and London: Hafner.
