Optic-nerve-transmitted eyeshine, a new type of light emission from fish eyes

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RESEARCH

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Optic-nerve-transmitted eyeshine, a new type of light emission from fish eyes Roland Fritsch1* , Jeremy F. P. Ullmann2,3, Pierre-Paul Bitton1, Shaun P. Collin4† and Nico K. Michiels1*†

Abstract Background: Most animal eyes feature an opaque pigmented eyecup to assure that light can enter from one direction only. We challenge this dogma by describing a previously unknown form of eyeshine resulting from light that enters the eye through the top of the head and optic nerve, eventually emanating through the pupil as a narrow beam: the Optic-Nerve-Transmitted (ONT) eyeshine. We characterize ONT eyeshine in the triplefin blenny Tripterygion delaisi (Tripterygiidae) in comparison to three other teleost species, using behavioural and anatomical observations, spectrophotometry, histology, and magnetic resonance imaging. The study’s aim is to identify the factors that determine ONT eyeshine occurrence and intensity, and whether these are specifically adapted for that purpose. Results: ONT eyeshine intensity benefits from locally reduced head pigmentation, a thin skull, the gap between eyes and forebrain, the potential light-guiding properties of the optic nerve, and, most importantly, a short distance between the head surface and the optic nerves. Conclusions: The generality of these factors and the lack of specifically adapted features implies that ONT eyeshine is widespread among small fish species. Nevertheless, its intensity varies considerably, depending on the specific combination and varying expression of common anatomical features. We discuss whether ONT eyeshine might affect visual performance, and speculate about possible functions such as predator detection, camouflage, and intraspecific communication. Keywords: Marine visual ecology, Eye anatomy, Eyeshine, Optic nerve, Light guidance, Tripterygiidae, Tripterygion delaisi

Background Vision implies the presence of photoreceptors that absorb and transform light energy into a neural signal that can be interpreted by the brain. Advanced visual abilities as in vertebrates, however, also depend on the presence of the melanin containing retinal pigment epithelium (RPE) behind the photoreceptors. It absorbs excess light to prevent scattering within the eye and shields the photoreceptors against light coming from behind the eye, improving image contrast and resolution. This explains why the pupils of camera-type eyes are typically black. Some eyes, however, do not function strictly unidirectionally and may show stunningly bright pupils, from which light appears to be emitted by the eye, a phenomenon called eyeshine. Figure 1 provides an overview of previously described * Correspondence: [email protected]; [email protected]; [email protected] † Equal contributors 1 Institute of Evolution and Ecology, University of Tübingen, 72076 Tübingen, Baden-Württemberg, Germany Full list of author information is available at the end of the article

types of eyeshine [1, 2] and the new type described in this study. Based