Penguins are easily recognizable by their many adaptations to an aquatic lifestyle, including wings that have modified into paddles and feathers that have been modified to retain body heat when exposed to wet and cold conditions. One important feature that may not immediately jump to mind is vision. In order to hunt for food, penguins must have sufficient underwater vision. Many anatomical structures in the eye contribute to vision, but the function of accessory eye structures is often less clear. One example of such an accessory structure is the nictitating membrane. Often called a “third eyelid”, the nictitating membrane is a thin film that can be closed and opened to cover the eye. While humans don’t have a nictitating membrane, many reptiles, birds, amphibians, and mammals do, and it helps keeps the eye lubricated, clear away debris, and provide physical protection. In penguins, the nictitating membrane may play another role. A recent study by Shaun Collin and Barry Collin (2020) published in Integrative Organismal Biology examined the morphology of the nictitating membrane in the little penguin, Eudyptula minor, and found several structures that suggest the membrane may be modified to play a role in underwater vision.
The nictitating membrane consists of three layers: two sheets of tissue, an outer (conjunctival) epithelium and an inner (bulbar) epithelium, and a connective tissue matrix (stroma) that holds them together. The little penguin has modifications to all three layers of the nictitating membrane.
Figure 1 from Collins and Collins (2020). A) An adult little penguin, B) The little penguin eye (beak is to the right), C) A cross section through the nictitating membrane, c= outer (conjunctival) membrane and b=inner (bulbar) membrane, D) A close-up of the rectangle in C, cep= outer membrane, st=connective tissue stroma, bep=inner (bulbar) membrane. Scale bars: (A) 25 micrometers; (B) 40 micrometers; (C) 50 micrometers; and (D) 50 micrometers.
The first noteworthy structure on the little penguin nictitating membrane is found on the outer surface. The peripheral edge of the outer surface is covered in small finger-like projections and ridges, which have not been found in other aquatic birds. Many marine animals have similar ridges covering the cornea, and so the authors hypothesize that the ridges on the nictitating membrane of the little penguin may indicate that the membrane covers the eye when feeding at sea.
Figure 2 from Collins and Collins (2020). Surface of the outer (conjunctival) surface of the nictitating membrane. A-D move from the leading edge of the membrane to the periphery. A) Microvilli, B) Microplicae, C) and D) Microridges.
The second interesting find is on the inner tissue layer of the nictitating membrane. The inner layer lacks a feathered surface, which has been found in other birds. The feathered surface is caused by the cells in the inner tissue layer producing small finger-like extensions of their cytoplasm (the fluid inside cells). This feathered surface is thought to be useful in distributing lubricating fluid across the eye when the nictitating membrane is closing and opening. This function may not be necessary in an aquatic bird, as the eyes are regularly submerged in water. Supporting this idea is the fact that other aquatic birds, namely the rockhopper penguin and mallard duck, also lack this feathering on the inner membrane.
The final finding is in the structure of the connective tissue matrix (stroma) that holds the inner and outer epithelium of the nictitating membrane together. At the leading edge of the membrane the collagen fibrils of the stroma are randomly arranged, but in the region of the membrane that covers the pupil when the membrane is closed, the fibrils are aligned parallel to the leading edge. The importance of the collagen fibril arrangement stems from a theory called the lattice theory of transparency for the cornea. Under this theory, in order for tissue to be transparent the internal collagen fibrils must all be parallel. The organization of collagen fibrils over the pupillary region of the nictitating membrane thus suggests that there is increased transparency and improved visibility in this region, creating a “transparent window”. A similar window has been found in several other aquatic birds (e.g., hooded merganser, rock hopper penguin, mallard duck). This window would allow for improved visibility while the nictitating membrane is closed over the eye, which could occur during important underwater activities like hunting.
Figure 4 from Collins and Collins (2020). Cross sections through the stroma of the nictitating membrane. A) Stroma at the leading edge where collagen fibrils are randomly arranged. B) Stroma away from the leading edge where collagen fibrils are arranged parallel to each other. In A and B, cf=collagen fibril.
By Amanda Hewes
Amanda Hewes is a PhD student in the Department of Biology at the University of Washington, Seattle. Her interests include the evolution of form-function relationships and functional morphology, focusing on avian pollinators and bird-plant coevolution.