Turtles
(Order Testudines)
Turtles are reptiles with a bony carapace. They are of the order Testudines, also known as Chelonia. DNA phylogentic studies place turtles close to Archosaurs (birds, crocodiles and dinosaurs) (Crawford, Parham, & al, 2014). The clade which includes Testudines and Archosaurs is called Archelosauria. Turtles are further subdivided into Cryptodira which can retract the head directly into the shell, and Pleurodira which fold their necks to the side to protect their heads.
Turtles have diversified little since ancestors of the 348 extant species first appeared 220mya, except for a period when continental coastal margins appeared 30mya increasing the size of their potential habitat (Thomson & Spinks, 2021). No taxonomic distinction is made between turtles, tortoises and terrapins. Turtles have round pupils. As with mudskippers, turtles which are primarily aquatic have had to deal with changes in the focussing properties of the cornea depending on whether they are looking through water or air. This problem has been dealt with in sea turtles by evolving flat corneas which do not refract light (Figure 1).
Figure 1. Refraction with a flat cornea in sea turtles (left water; right air)
Blinks are shown in a number of turtles. Two types of nictitating membrane blink were observed. The first, like a frog's, involved unfolding of the lower lid - a 'lower lid nictitating membrane blink'. Videos of a number of these are shown as they have not, to the author's knowledge, been described before. The second involved horizontal passage of the nictitating membrane from the inner canthus across the cornea, as occurs in lizards, crocodiles and birds.
Freshwater turtle
Family Chelidae
Saw shelled turtle (Myuchelys latisternum)
Blink type: Globe retraction with elevation of ‘lower lid nictitating membrane’
Wink then blink played at 10% speed
a) Pre-blink. b) Both eyes are retracted and the right covered. The left eye is still visible. The inferior part of the right lower lid (white arrow) is thicker than the superior part (the 'lower lid nictitating membrane') which covers the eye. c) Both eyes are covered by the nictiating membranes. d) and e) The left eye opens. f) Post-blink.
Wink in the same specimen at higher magnification: a) Pre-blink. b), c) and d) Left eye is retracted and both upper (orange arrow) and lower lids (white arrow) are prominent as they sink into the orbit. The thinner superior part of the lower lid (the 'lower lid nictitating membrane' has covered the left eye. e) The nictiating membrane is descending. f) Post-blink.
Freshwater turtle
Family Chelidae
Red-bellied short-necked turtle (Emydura subglobosa)
Blink: Globe retraction with elevation of ‘lower lid nictitating membrane’
Swimming underwater. a) Pre-blink. b) 'Lower lid nictitating membrane' elevated during a blink.
Freshwater turtle
Family Chelidae
Murray River turtle (Emydura macquarii)
Blink: Globe retraction with elevation of ‘lower lid nictitating membrane’
Eye movement and blink played at 10% speed
a) Pre-blink. b) Maximal blink. The upper lid has lowered slightly due to globe retraction. The eye is covered by the lower lid which comprises two parts: a semi-translucent upper section (grey arrow), the 'lower lid nictitating membrane', and an opaque lower section (white arrow), the lower lid. c) Post-blink.
Upward eye movement and 'lower lid nictitating membrane' blink with globe retraction, underwater, played back at 20% speed
Murray River turtle underwater: a) Pre-blink. b) Upper lid sinks as globe retracts. Eye covered by semi-translucent upper section of the lower lid (grey arrow), 'lower lid nictitating membrane', and opaque lower section (white arrow), the lower lid. c) Maximal blink. d) and e) 'Lower lid nictitating membrane' and lower lid descend. f) Post-blink
Freshwater turtle
Family Chelidae
Eastern long-necked turtle (Chelodina longicollis)
Blink type: Globe retraction with elevation of ‘lower lid nictitating membrane’
Blink played at 10% speed.
a) Pre-blink. b) Globes retract and right palpebral fissure narrows. c) and d) Lower lid, comprising thin upper section ('lower lid nictitating membrane') and thicker lower section (lower lid), covers the eye. e) 'Lower lid nictitating membrane' descends, tucking behind lower lid. e) Post-blink.
Right eye of another individual from side. a) Pre-blink. b) Lower half of the eye covered by the lower lid, more opaque in the lower region than the upper ('lower lid nictitating membrane'). c) Full blink. d) Lower lid and 'lower lid nictitating membrane' start to descend. e) Lower lid now looks brown, perhaps due to its upper part folding behind the lower part. f) Post-blink
Freshwater turtle
Family Pelomedusidae
Cape terrapin or African helmeted turtle (Pelomedusa subrufus nigra)
Blink type: Globe retraction with elevation of ‘lower lid nictitating membrane’
Blink played back at 10% speed. Globes retract causing upper lids to sink into orbits. 'Lower lid nictitating membrane cover globes and then descend, folding under lower lids.
Freshwater turtle
Family Geoemydidae
Spiny turtle or spiny terrapin (Heosemys spinosa)
Blink type: Globe retraction with elevation of ‘lower lid nictitating membrane’
Blink played at 10% speed.
a) Pre-blink. b) Eye covered with a paler upper section ('lower lid nictitating membrane') and a more opaque lower section (lower lid). c) and d) 'Lower lid nictitating membrane' (grey arrow) and lower lid (white arrow) descending. e) Membrane has now disappeared behind lower lid. f) Post-blink.
Freshwater turtle
Family Emydidae
River cooter (Pseudemys concinna)
Blink type: Globe retraction with elevation of ‘lower lid nictitating membrane’
Played at 50% speed
a) Pre-blink. b) Eye begins to retract and lower lid rises. c) Eye covered by lower lid, semi-translucent in the upper part, opaque and thicker in the lower part. d) Lower lid starts to fall. e) Upper section of lower lid tucks behind lower section revealing eye. f) Post-blink
Freshwater turtle
Family Podocnemididae
Madagascan big-headed turtle (Erymnochelys madagascariensis)
Blink type: Globe retraction, elevation of lower lid and horizontal movement of ‘inner canthus nictitating membrane’
Played at 10% speed
a) Pre-blink. b) Globe retracts and lower lid elevates. c) Lower lid descends but eye remains covered by semi-translucent nictitating membrane. d) Nictitating membrane can be seen half-way across the pupil withdrawing towards the inner canthus. e) More of the pupil is exposed as the membrane withdraws. f) Post-blink. The key observation here is that the nictitating membrane appears to move independently of globe retraction and lower lid movement.
d) and e) at higher magnification
Terrestrial tortoise
Family Testudinidae
Galápagos tortoise (Chelonoidis niger)
Blink type: Globe retraction, elevation of lower lid and horizontal movement of ‘inner canthus nictitating membrane’
Played at 10% speed
a) Pre-blink. b) Globe retraction begins. c) Full globe retraction causing lids to sink into the orbit. Lower lid elevation, closing the eye. d) Edge of nictitating membrane (grey arrow) visible as eye starts to open. e) Nictitating membrane moves back towards the inner fornix. f) Post-blink, membrane still visible.
Terrestrial tortoise
Family Testudinidae
Elongated tortoise (Indotestudo elongata)
Blink type: Globe retraction, elevation of lower lid and horizontal movement of ‘inner canthus nictitating membrane’
Played at 10% speed
Video 1. Blink in an elongated turtle video-ed at 25fps, played back at 30% speed.
At 80ms, the eyeball has retracted and the lower eyelid has elevated, covering the eye. By 400ms, the lower eyelid has descended revealing a nictitating membrane which half covers the eye. Its free edge is at right angles to the palpebral fissure.
Terrestrial tortoise
Family Testudinidae
Aldabra giant tortoise (Geochelone gigantea)
Blink type: Globe retraction, elevation of lower lid and horizontal movement of ‘inner canthus nictitating membrane’
Played at 10% speed
a) Pre-blink. b) Opaque nictitating membrane moves across the eye from the inner canthus. Palpebral fissure narrows probably due to retraction of the globe. Lower lid elevates slightly. c) Maximal excursion of nictitating membrane and lower lid. d) and e) Nictitating membrane withdraws. f) Post-blink.
Terrestrial tortoise
Family Testudinidae
Leopard tortoise (Stigmochelys pardalis)
Blink type: Globe retraction, elevation of lower lid and horizontal movement of ‘inner canthus nictitating membrane’
Played at 10% speed
Blink on head turn. a) Pre-blink. b) Retraction of globe, elevation of lower lid, appearance of white nictitating membrane at inner canthus. c) Maximal blink with full retraction of globe. d) Lower lid starting to fall revealing nictitating membrane covering the eye. e) Lower lid down, globe unretracted, nictitating membrane halfway across the eye. f) Post-blink
Sea turtle
Family Cheloniidae
Loggerhead sea turtle (Caretta caretta)
Blink type: Globe retraction, elevation of lower lid and horizontal movement of ‘inner canthus nictitating membrane’
Still photographs from National Geographic documentary on Youtube: a) Pre-blink. Yellow upper lid. b) Globe retraction causing upper lid to sink into orbit. c) Glimpse of nictitating membrane (grey arrow) withdrawing into inner canthus as globe unretracts. d) Post-blink.
Comments
In the freshwater aquatic species studied, with the exception of the Madagascan big-headed turtle, blinking involved retraction of the globe and elevation of the lower lid, which appeared to have an upper and lower part, the upper part folding under the lower part when the blink ended like the nictitating membrane does in frogs. This type of nictitating membrane is labelled here as a ‘lower lid nictitating membrane’. In all the terrestrial species and the Madagascan big-headed turtle and loggerhead sea turtle, an opaque nictitating membrane moved across the eye from the inner canthus during a blink. This type of nictitating membrane is labelled here as an ‘inner canthus nictitating membrane’. There was also retraction of the globe and elevation of the lower lid. I had no access to marine turtles but found two videos on Youtube. The first was of an olive ridley sea turtle (Lepidochelys olivacea) with a straw stuck in its nostril, the second a loggerhead. Unlike other turtles, marine turtles are said to have mobile upper as well as lower eyelids. The upper lids were certainly prominent but it was hard to say whether they were drawn over the eye actively or sank passively into the orbit as the globe retracted. It looked more like the latter. The loggerhead had a clearly visible inner canthus nictitating membrane.
According to Walls (Walls, 1943), the [inner canthus] nictitating membrane in turtles is drawn across the eye by the pyramidalis muscle (Figure 1). As the pyramidalis muscle pulls on both the nictitating membrane tendon and lower lid tendon, the nictitating membrane and lower lid cannot operate independently.
The palpebral fissure is canted at an angle as freshwater and marine turtles float in a slanted position at the water surface (Figure 2).
Lubrication of the cornea is provided by a lacrimal gland and an Harderian gland with a single duct. There is no nasolacrimal duct (Walls, 1943). In marine turtles, the lacrimal gland is enormously enlarged and excretes a salty solution which can be seen trickling out of the eye when the turtle is on land. The Harderian gland lubricates the eye (Wyneken, 2001).
Figure 1
Medial view of a turtle eyeball showing the pyramidalis muscle (Pyr) which sends tendons to the nictitating membrane (n) and lower eyelid (p.i). Also seen is the retractor bulbi muscle (R.b). ‘Retraction of the globe will also pull on these tendons causing the lower lid to rise and the nictitating membrane to cross, though the latter seems to vary with different species’ (Walls, 1963).
Figure 2. Angle of the palpebral fissure in a western painted turtle (Chrysemys picta). The line is drawn through the canthi.
References
Crawford, N., Parham, J., & al, e. (2014). A phylogenomic analysis of turtles. Molecular Phylogenetics and Evolution, 83: 250-257.
Ecker, A (Translated by Haslam, G). 1889. The anatomy of the frog. Oxford: OUP.
Thomson, T., & Spinks, P. a. (2021). A global phylogeny of turtles reveals a burst of climate-associated diversification on continental margins. PNAS, 118 (7) e2012215118; https://doi.org/10.1073/pnas.2012215118.
Walls, G. (1943). The vertebrate eye and its adaptive radiation. Bloomfield Hills, Mich.: Cranbrook Institute of Science. Cranbrook Press. Bulletin no 19.
Wyneken, J. (2001). The Anatomy of Sea Turtles.