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.

Keywords: Percomorpha; evolution; fishes; histology.

FIGURE 1

Head of Pegusa lascaris with superficial head musculature exposed. (a) ocular side and (b) blind side. Arrow indicating the facial chamber of the recessus orbitalis of both sides.

FIGURE 2

Internal anatomy of the facial chamber of the recessus orbitalis of the blind side of Bothus ocellatus showing the smooth muscle fibers in dark red. (a) longitudinal section, (b) zoom in of (a).

FIGURE 3

Sagittal section of the head of Poecilopsetta albomarginata. (a) Broad view of the section showing the sessile eye and its surrounding tissues. (b) Detail of the facial chamber of the recessus orbitalis and its internal smooth muscle fibers. (c) Detail of the margin of the eye showing the elastic nature of the rippled texture when the eye is retracted and the scleral chamber of the recessus orbitalis. am, facial segment of the adductor mandibulae; ln, lens; ro.fc, recessus orbitalis, facial chamber; ro.sc, recessus orbitalis, scleral chamber; rt., retina; sc, Sclera; se, Sessile eye; so, Sclerotic ossicle.

FIGURE 4

Longitudinal section of the ocular side of the head of Bothus ocellatus. (a) Broad view of the section showing the sessile eye and its surrounding tissues. Dashed‐line rectangle indicates the region of which (b) image zooms in. Continuous rectangle indicates the region of which (c) image zooms in. (b) Region in which facial chamber of the recessus orbitalis communicates with the scleral chamber of the recessus orbitalis. (c) Facial chamber of the recessus orbitalis and its internal smooth muscle fibers in red. am, facial segment of the adductor mandibulae; ic, interchamber constriction; ln, lens; nc, neurocranium; ob, obliqui muscles; on, optic nerve; re, recti muscles; ro.fc, recessus orbitalis, facial chamber; ro.sc, recessus orbitalis, scleral chamber; rt., retina; sc, sclera; se, sessile eye.

FIGURE 5

Longitudinal section of the ocular side of the head of Symphurus melanurus. (a) Broad view of the section showing the sessile eye and its surrounding tissues. (b) Detail of the facial chamber of the recessus orbitalis. (c) Detail of the sessile eye surrounded by the scleral chamber of the recessus orbitalis. am, Facial segment of the adductor mandibulae; ic, interchamber constriction; ln, lens; me, migrated eye; nc, neurocranium; ob, obliqui muscles; rc, Retraction chamber; re: Recti muscles; ro.fc: Recessus orbitalis, facial chamber; ro.sc: Recessus orbitalis, scleral chamber; rt.: Retina; sc: Sclera; se: Sessile eye.

FIGURE 6

X‐ray microcomputed tomographies of the mandibular jaw of the ocular side of Psettodes erumei showing the facial segment of the adductor mandibulae and the sessile eye with its associated muscles and recessus orbitalis. (a) Lateral view, (b) transversal section of the head showing the position of the blind side recessus orbitalis, sandwiched in between the facial segment of the adductor mandibulae and adductor hyomandibulae, (c) medial view, (d) Posterior view. ah, adductor hyomandibulae; am, facial segment of the adductor mandibulae; (b) blind side; me, Migrated eye; (o) ocular side; ro.fc, recessus orbitalis, facial chamber; ro.sc, recessus orbitalis, scleral chamber; se, sessile eye.

FIGURE 7

X‐ray microcomputed tomographies of the head of Psettodes erumei showing the position of the recessus orbitalis of both the ocular and blind sides. (a) Ocular side of the head, (b) ocular side of the eyes and their recessus orbitales, (c) frontal view, (d) posterior view. (b) blind side; (o) ocular side; ro.fc, recessus orbitalis, facial chamber; ro.sc, recessus orbitalis, scleral chamber.

FIGURE 8

Ocular side of the head of Rhombosolea tapirina showing the position of the recessus orbitalis serving both the sessile and migrated eyes. (b) blind side; me, migrated eye; (o) ocular side; ro.fc, rrecessus orbitalis, facial chamber; ro.sc, rrecessus orbitalis, scleral chamber; se, ssessile eye.

FIGURE 9

X‐ray microcomputed tomographies of the head of Psettodes erumei showing the position of the eyes and their associated musculature. (a) Ocular side of the head. (b) Blind side of the head. (c) Ocular side of the eyes and their corresponding muscles. (d) Blind side of the eyes and their corresponding muscles. (e) Frontal view of the eyes and their corresponding muscles. (f) Frontal view of the head. ObI, obliquus inferioris; ObS, obliquus superioris; Re, recti muscles; ReEx, rectus externus; ReI, rectus inferioris.

FIGURE 10

Dorsal view of the sessile (right) eye. (a) Psettodes erumei, X‐ray microcomputed tomography. (b) Hippoglossus hippoglossus, photography and corresponding schematic view. ObS, obliquus superioris; RS, rotatory slip.

FIGURE 11

X‐ray microcomputed tomographies of the frontal view of the head of Psettodes erumei. Schematic representation of how the double‐pump mechanism of the two chambers of the recessus orbitalis work. fc, facial chamber; sc, Scleral chamber.