Armored eyes of the whale shark.

Taketeru Tomita,Masakatsu Kino,Minoru Toda,Kiyomi Murakumo,Shinya Komoto,Alistair Dove,Kei Miyamoto,Luis Lucifora

doi:10.1371/journal.pone.0235342

Abstract

This report elaborates on adaptations of the eyes of the whale shark Rhincodon typus (Elasmobranchii, Rhincodontidae), including the discovery that they are covered with dermal denticles, which is a novel mechanism of eye protection in vertebrates. The eye denticle differs in morphology from that of the dermal denticles distributed over the rest of the body, consistent with a different function (abrasion resistance). We also demonstrate that the whale shark has a strong ability to retract the eyeball into the eye socket. The retraction distance was calculated to be approximately half the diameter of the eye, which is comparable to those of other vertebrates that are known to have highly retractable eyes. These highly protective features of the whale shark eye seem to emphasize the importance of vision for environmental perception, which contradicts the general, though poorly established, notion of low reliance on vision in this species.

Highlights

The eye, which is the organ that obtains optical information from the external environment, must be located on or near the surface of the body
Numerous dermal denticles are distributed on the eye surface around the iris
The general morphology of each eye denticle is characterized by a central ridge running through the longitudinal axis of the denticle and several sub-ridges branching laterally from the central ridge (Fig 3A–3D and S1 Video)

Summary

Introduction

The eye, which is the organ that obtains optical information from the external environment, must be located on or near the surface of the body. Many terrestrial and aquatic vertebrates prevent this risk by the coverage of eye surfaces with eyelids [1]. Carcharhinid and sphyrnid sharks have nictitating membranes or “third eyelids”, which cover their eyes completely during their feeding activities [2]. The outer surface of this membrane is covered with dermal denticles, which likely increases its protective ability [3]. Many other elasmobranchs that are not equipped with nictitating membranes have to protect their eyes in different ways, such as retracting the eyeballs into the head (e.g., electric ray [4]; guitarfish [5]), or rotating the eyeballs back into the orbit (e.g., white shark [6]). The eye-protection mechanism in many elasmobranch species remains largely uninvestigated

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Conclusion