Frogs
(Order Anura)
Introduction. 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.
Present study. Videos were made of 7 species of frog: Lemur leaf-frog (Agalychnis lemur). Source: internet; Australian green tree frog (Ranoidea caerulea/Litoria caerulea); Red-eyed tree frog (Agalychnis callidryas). Source: internet; Green and golden bell frog (Ranoidea aurea); White-lipped tree frog (Nyctimystes infrafrenetus); Magnificent tree frog (Ranoidea splendida); Cane toad (Rhinella marina). Source: internet.
Blinking occurred infrequently and the following did not blink during the observation period: Amazon milk frog (Trachycephalus resinifictrix); mossy frog (Theloderma corticale); blue poison dart frog (Dendrobates azureus maculatus); Lake Oku clawed frog (Xenopus longipes).
Examples
​Family Pelodryadidae
Species White-lipped tree frog (Nyctimystes nitrogenates)
Blink: Globe retraction with elevation of lower lid nictitating membrane
Blink played at 30% speed.
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
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Lower lid nictitating membrane blink with globe retraction, right eye: a) Pre-blink showing a horizontally elongated oval pupil. b) Blink involving the nictitating membrane (blue), partly covering the pupil, with the pupil visible behind it, and the lower lid (orange). c) Maximum excursion of the lower lid - covering the pupil. The narrowing of the palpebral fissure is due to retraction of the globe.
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
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 nictitating membrane
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.
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.
Family Bufonidae
Species Cane toad (Rhinella marina). Source: internet
Nictitating membrane blink with globe retraction: a) Pre-blink, showing a horizontally elongated pupil and lower eyelid (orange). b) Blink involving nictitating membrane (blue) and lower lid (orange) rising and partly covering the pupil. c) Maximum excursion of the nictitating membrane and lower lid covering the cornea. The narrowing of the palpebral fissure is due to retraction of the globe.
Mechanism of elevation of the nictitating membrane and lower lid in frogs.
It is difficult to find current studies of the muscles involved in moving the nictitating membrane and lower lid in frogs. According to Ecker (Ecker, 1889) and Walls (Walls, 1943) the two upper ends of the nictitating membrane are connected to each other by a tendon.
The figure above, adapted from Ecker (Ecker, 1889), provides a view from below of the coronal plane of a frog’s head showing the bellies of the retractor bulbi muscle (brown) inserting onto the globe. The tendon of the nictitating membrane (blue) encircles the globe. According to Ecker (Ecker, 1889), the tendon of the nictitating membrane pulls the membrane up over the cornea when the globe is retracted into the orbit by the bellies of the retractor bulbi muscle. At the end of the blink, the globe pushes the membrane and lower lid aside as the retractor bulbi muscle relaxes and the levator bulbi muscle, which sits under the globe like a hammock, contracts. The lower lid is folded again by the action of a slip of the levator bulbi muscle (Duellman & Trueb, 1994).
The figure above shows a nictitating membrane blink with globe retraction (left eye from the side) in a magnificent tree frog (Ranoidea splendida) together with a drawing of the proposed mechanism of the blink: a) Pre-blink showing prominence of the globe and a horizontally elongated pupil. b) The globe retracts and the nictitating membrane (blue) and lower lid (orange) rise. c) Maximum excursion of the nictitating membrane and lower lid with marked retraction of the globe. d) Pre-blink, showing the nictitating membrane (blue) behind the lower lid (orange) and the tendon of the nictitating membrane (blue line) forming the medial part of the tendon circling the globe. It is attached to the lower surface of the retractor bulbi muscle behind the eye. e) Blink, showing the nictitating membrane and lower lid being drawn over the eye as the globe is pulled into the orbit by the retractor bulbi muscle. c) Maximum excursion of the nictitating membrane and lower lid.
The figure above shows a sagittal section of the eye and lower lid showing the nictitating membrane (blue) arising from the conjunctival membrane inside the lower lid (orange)
Discussion. 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, 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.
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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.
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The 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
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Amphibia have only ten pairs of cranial nerves; mammals have twelve pairs.
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​​​​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.
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References​
Ecker, A (Translated by Haslam, G). 1889. The anatomy of the frog. Oxford: OUP.
​Duellman, W., & Trueb, L. (1994). Biology of amphibians. Chicago: JHU press.
​Feng, Y.J. et al. (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.
