Abstract

The extrinsic ocular or extraocular muscles are those associated with the eye either directly (extraocular muscles attached to the globe) or indirectly (muscles associated with the eyelids). Those that are directly associated with the eye (musculi bulbi) and assist in directing the eye's gaze comprise seven muscles in most mammals: the inferior, superior, medial and lateral recti muscles, the inferior and superior oblique muscles and the retractor bulbi muscle. Those associated with the eyelids (musculi palpebrae) consist of those that control the opening and closing of the palpebral fissure. To date, a complete description of this musculature in the Florida manatee (Trichechus manatus latirostris) is lacking. The present study examines anatomically, by gross and histological observations, the organization of the extrinsic ocular muscles in this species and relates these findings to observed ocular movement and previously described visual behavior.

For this study, complete orbital specimens of four animals (one juvenile and three adults) that had died from natural causes were collected at the Marine Mammal Pathobiology Laboratory in St. Petersburg, Florida. The specimens were placed in 10% buffered formalin and further dissected and photographed. Selected portions were embedded in paraffin, and sectioned at 5 μm. Sections of the selected portions were stained using either hematoxylin and eosin, Masson's trichrome or elastic stain.

Orbital dissections of all specimens consistently revealed the absence of a true set of musculi bulbi, i.e., the muscles that are directly connected to the globe, in the manner typically found in mammalian species (Figure 1). Instead, four muscles have been observed in the orbit and their associations appear to be primarily with the palpebrae. The most prominent of these muscles ends at the base of the upper eyelid, and a similar one attaches to the base of the lower eyelid, both originating from the area of the optic foramen (Figure 2). There are two other muscles that are both attached to the third eyelid (membrana nictitans), one inferiorly and the other medially. All musculature has been verified to be skeletal. Their nerve and vascular associations remain to be ascertained. The upper and lower eyelids have a confluent set of orbicularis oculi muscles that are uninterrupted by any appreciable amounts of connective tissue including areas that would constitute the medial and lateral canthi of most species. Specific levator muscles for expanding the palpebral fissure were not encountered.

The extrinsic ocular muscles of the Florida manatee form a unique design not previously encountered in the animal kingdom. The absence of a true set of musculi bulbi is quite remarkable, especially in the face of a variety of reports including those that have stated that this animal has a highly developed retractor bulbi muscle.^2-4 The present findings reveal that the retractor bulbi muscle appears to have been replaced by adipose tissue with its own fascial lining that encapsulates the optic nerve, and when observed grossly its presence may be misconstrued to be a retractor bulbi muscle. Movement of the third eyelid is direct in this species, having two separate muscles that undoubtedly facilitate the blinking and sweeping activity of this structure. The prominent superiorly located muscle may be the levator superioris muscle, but here does not extend into the upper eyelid. On the other hand, the inferiorly located muscle may be the inferior rectus that now attaches to the base of the lower eyelid. They are both well developed and together could assist in pushing the eye forward.

The upper and lower eyelids are designed for squinting rather than blinking as they essentially possess one muscle, the orbicularis oculi, which when contracted brings the palpebral fissure to a small rounded point, much like that in miosis of rounded iridal pupils. The actual blinking and concomitant sweeping of tears over the surface of the cornea is performed by the third eyelid.

The collective changes and differences of the extrinsic ocular muscles of the Florida manatee that we have observed most likely reflect adaptations needed for their survival in an immensely divergent aquatic environment. The requirements for adequate vision have unquestionably been altered, having resulted in eyes that have become greatly reduced in size in relation to their body size. It is quite possible that the small eyes have then resulted in remarkable changes of their supportive musculature, which in turn affects their physical behavior. As manatees visually perceive objects, they have a tendency to move from right to left in a serpentine manner as they approach the objects.¹ In that way, both eyes can become engaged for binocular vision.

Click on the image to see a larger view.

Figure 1. Manatee EOM (extraocular muscles) up eyelid & orbit. Note the absence of any EOM directly attached to the eye. NM - Nictitating membrane (third eyelid).

Figure 2. Manatee EOM (extraocular muscles) up eyelid & orbit. Note the presence of the extensive muscle lying superiorly. E - eye; NM - Nictitating membrane (third eyelid); OO - orbicularis oculi muscle.

Acknowledgements

This work was supported by a grant from the Florida Fish and Wildlife Commission.

References

1.  Bauer G.B., D.B. Colber, J.C. Gaspard III, B. Littefield, and W. Fellner. 2003. Underwater visual acuity of Florida manatees (Trichechus manatus latirostris). Int J Comp Psychol 16: 130.

2.  Duke-Elder S. 1958. The Eye in Evolution. Vol I. London: Henry Kimpton.

3.  Prince J.H. Comparative anatomy of the eye. 1956. Springfield, IL: Charles C. Thomas.

4.  Walls L.G. 1967. The Vertebrate Eye and Its Adaptive Radiation. New York: Hafner.