Frogs

(Order Anura)


Most living frogs arose from lineages originating at the time of the Cretaceous-Paleogene mass extinction 66mya (Feng, 2017). Their closest relatives are salamanders. Frogs are an order within the class of amphibia comprising over 7,000 species. Despite the name, only a minority of frogs are truly amphibious after they cease to be tadpoles. The majority are wholly terrestrial, and a few are wholly aquatic. Wholly aquatic anurans such as aglossal toads, never develop eyelids (Walls, 1943). No taxonomic distinction is made between frogs and toads. Tadpoles, the larval stage of frogs, have no eyelids. Frogs have slit-shaped pupils elongated in the horizontal axis.


Examples of blinking in adult frogs follow: 
 

Family Pelodryadidae
White-lipped tree frog (Nyctimystes nitrogenates) 
Blink: Globe retraction with elevation of ‘lower lid nictitating membrane’ 

Blink played at 30% speed.

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Blink during a slight head turn: a) Pre-blink b) Globe retraction, slight elevation of lower lid (white arrow) and elevation of nictitating membrane arising as a fold from inside the lower lid (grey arrow) c) Maximal blink d) Eyeballs start to unretract e) Nictitating membranes descend f) Post-blink

Family Pelodryadidae
Green and golden bell frog (Litoria aurea) 
Blink type: Globe retraction with elevation of ‘lower lid nictitating membrane’ 

Blink played at 20% speed

Litoria area.png

Blink seen from the left side. a) At rest. Horizontally elongated pupils. b) Eyeballs start to retract. At this time the left palpebral fissure narrows and the ‘rims’ around its edge become more prominent. c) The pale green semi-translucent left lower lid rises to partially cover the pupil (arrow). What is harder to see is that a translucent nictitating membrane has covered the eye d) The top edge of the left nictitating membrane, marked by arrows, here and in e) and f), is seen descending down the cornea. 

Family Pelodryadidae
Magnificent or splendid tree frog (Ranoidea splendida)
Blink: Persistent elevation of lower lid and ‘lower lid nictitating membrane’ in sleep

The edge of the lower lid has reached the pupil and the nictitating membrane has fully covered the cornea.

Family Pelodryadidae
Yellow spotted tree frog (Litoria castanea)
Blink type: Globe retraction with elevation of ‘lower lid nictitating membrane’

 

Yellow spotted.png

a) Pre-blink b) Elevation of lower lid (white arrow) and 'lower lid nictitating membrane (grey arrow) c) Lower lid has descended leaving just the nictitating membrane (arrow)

Family Phyllomedusidae
Red-eyed tree frog (Litoria chloris)
Blink type: Globe retraction with elevation of ‘lower lid nictitating membrane’

 

Blink played at 20% speed.

Red eyed tree frog.png

a) Pre-blink. Horizontally elongated pupils. b) Both globes retract causing narrowing of the palpebral fissures. c) The eyes retract further. d) and e) A semi-translucent lower lid (white arrow) is seen rising in the right eye and the edge (grey arrow) of a translucent nictitating membrane is seen rising in the left eye. f) Post-blink. 

Comments


As with mudskippers, frog’s eyes sit on the dorsum of the skull and in some species are elevated above the skull allowing aerial vision for the detection of prey and predators, while the rest of the animal remains submerged in water. And, as with mudskippers, blinking involves retraction of the globes into the skull. Frogs have upper and lower eyelids, although the upper one appears to have no movement independent of the eyeball – sinking a little as the eyeball retracts. The lower lid rises a little on globe retraction but the nictitating membrane, which is a fold arising from the inner surface of the lower lid (Figure 1), rises to fully cover the cornea in a full blink and during sleep. The membrane is usually semi-transparent, preventing complete loss of vision during a blink, an advantage in the presence of predators or prey. Winking has a similar benefit. The nictitating membrane moistens the surface of the cornea by spreading oily secretions from a gland present in all vertebrates with a nictitating membrane, the Harderian gland, which fills most of the orbit (while also providing cushioning behind the eye). There is a circulation of secretions from the gland into the conjunctival space and then into the nasal cavity via the naso-lacrimal duct (Figure 2). The nictitating membrane probably also protects the cornea from floating debris when the eye is open.  Retraction of the globe into the skull protects the eye from mechanical injury from pressure or from a blow, an important function as frogs lack a neck and can jump but cannot turn their heads to avoid injury. Uniquely, blinking in frogs also aids in swallowing as the retracted eyes project into the throat.

According to Walls (Walls, 1943): ‘The thickened rim of the lower eyelid continues round the posterior part of the globe as a cord (tendon to nictitans) and passes through retractor bulbi (Figure 3). When this muscle contracts, the eyeball is pulled into the head and the transparent fold of the lower eyelid is pulled up over the cornea to meet the upper eyelid which is motionless. A broad hammock-like muscle, the levator bulbi, raises the globe to its normal elevated position and the lower lid slips back into its folded position. The eye can close without complete retraction. The tendon of the nictitating membrane (n) is pulled by the globe when the retractor bulbi muscle (Rb) contracts.’ 

According to Ecker (Ecker, 1889): ‘The pigmented free border of the nictitating membrane passes, at the inner and outer angles of the eye, into a tendon which passes for some distance to fibrous tissue then descends to the under surface of the eyeball and joins that the opposite side, so that the free border of the eyelid, together with this tendon form a complete ring (Figure 4). The tendinous part of the ring, which is thin and threadlike, is found on the under surface of the eyeball and lies under the m. retractor bulbi and is bound to this muscle. The m. retractor pulls the eyeball into the cavity backwards and downwards, while the levator raises it. There is less agreement about the movements of the eyelids, or rather of the lower eyelid, for the upper has no independent movements. Duges says that the two muscles which he considers to be levatores palpebrae inferiores, and which according to him are connected with the m. retractor bulbi, draw up the lid as it is being drawn backwards and downwards by the latter muscle. The depression of the lid on the relaxation of the retractor and projection of the eyeball is due simply to elasticity. Manz on the contrary has shown that the sinking of the eyeball by the contraction of the retractor must necessarily cause a rising of the nictitating membrane as its tendons are attached to that muscle and so must follow its movements. Depression of the lower lid occurs simultaneously with the raising of the eyeball by means of m. levator bulbi, through the contraction of the m. depressor palpebrae inferioris, which proceeds from that muscle; this is easily understood, as they are but parts of the same muscle’.

In summary, frogs have the following features of blinking which are additional to those seen in mudskippers: a mobile lower lid, a semi-transparent nictitating membrane and a gland which lubricates the cornea. Blinking in frogs is initiated by retraction of the globe by the retractor bulbi muscle. This causes elevation of the nictitating membrane by pulling on its tendon, which circles the globe. The nictitating membrane is an extension of the lower eyelid. There is no muscle pulling on the nictitating membrane tendon other than the

retractor bulbi muscle to which it is attached, so movement of the nictitating membrane/lower eyelid and retraction of the globe cannot occur independently of each other. The upper eyelid has no muscles or tendons attached to it. Any movement of the upper eyelid which occurs is therefore passive, caused by the eyeball on which it rests, retracting into the skull and then protruding at the end of the blink. Depression of the lower lid at the end of the blink is done by contraction of depressor palpebrae inferioris, a branch of the levator bulbi muscle which raises the globe. In frogs, all blinks involve the same structures.

Innervation of the muscles involved in blinking is as follows:
     Retractor bulbi:  Abducens nerve (VIth cranial nerve)
     Levator bulbi: Trigeminal nerve (Vth cranial nerve)
     Depressor bulbi inferioris: Trigeminal nerve

Amphibia have only ten pairs of cranial nerves; mammals have twelve pairs. 
 

Figure 5.png

Figure 1

Drawing of a section of the lower eyelid based on Rana pipiens. The nictitating membrane (nm) is shown to be attached to and folded under the lower eyelid (ll), (Walls 1943).

Frog nasolacrimal system.png

Figure 2

Nasolacrimal duct (nld) connecting the conjunctival space with the nasal cavity (Hillenius, Watrobski, & Rehorek, 2001)

Figure 6.jpg

Figure 3

In the Figure above, the muscles which move the nictitating membrane in various vertebrates are shown. Diagram 'a' shows the posterior aspect of a frog’s eye with the tendon of the nictitating membrane (n) circling the globe and overlying the retractor bulbi muscle (R.b).

Figure 7.png

Figure 4

Coronal view of the tendon of the nictitating membrane (n) of the frog (Ecker 1889).

References

Ecker, A (Translated by Haslam, G). 1889. The anatomy of the frog. Oxford: OUP.

Feng, Y.-J. e. (2017). Phylogenomics reveals rapid, simultaneous diversification of three major clades of Gondwanan frogs at the Cretaceous–Paleogene boundary. PNAS, 114 (29) E5864-E5870.

Walls, G. (1943). The vertebrate eye and its adaptive radiation. Bloomfield Hills, Mich.: Cranbrook Institute of Science. Cranbrook Press. Bulletin no 19. 

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