The secret in their eyes: A review of the recessus orbitalis, a unique structure of flatfishes.

Abstract

Flatfishes (Pleuronectiformes) are famous for having one of the most peculiar anatomical transformations in the animal kingdom, the ontogenetic migration of one eye from one side of the head to the other. But the eyes of flatfishes also carry a much lesser known but equally unique modification: an organ called the recessus orbitalis, which is responsible for projecting the eyeball above the level of the head, thus expanding their fields of vision. However, the morphology and distribution of the organ have never been thoroughly investigated. Previous studies reported only part of the recessus orbitalis and mistakenly suggested that it opened into the orbital cavity. We show that the organ forms a fully enclosed system consisting of two interconnected chambers: the facial chamber, which corresponds to the organ previously reported in the literature, and the scleral chamber, which encases the inner portions of the eyeball and is more challenging to detect through manual dissection. The organ is filled with interstitial fluid, and the walls of both chambers-especially the facial one-contain smooth, not skeletal and muscle fibers. These findings combined with field observations allowed us to propose a new functional model for the recessus orbitalis. The organ seems to operate as a dual-pump system, dynamically shifting interstitial fluid between the facial and scleral chambers. Inflation of the facial chamber results in eye retraction, whereas inflation of the scleral chamber causes eye protrusion. The presence of smooth muscle fibers, which can sustain contractions with minimal energy expenditure, supports this inferred mechanism, allowing the eye to remain fully protruded or retracted for extended periods. The recessus orbitalis has never been confirmed in several flatfish families, and the organ was recently considered absent in Psettodidae, the sister group to all other flatfishes. However, we positively identified this organ in all 74 species examined representing all 16 currently recognized flatfish families, including Psettodidae. This indicates that the presence of the recessus orbitalis is an evolutionary novelty (synapomorphy) for the entire Pleuronectiformes.