He Cries Crocodile Tears
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Br J Ophthalmol 2002;86:23 23 Br J Ophthalmol: first published as 10.1136/bjo.86.1.23 on 1 January 2002. Downloaded from Coverillustration......................................................................... He cries crocodile tears... The saurian triumph which occurred dur- although there may be an appendix-like ing the Mesozoic era probably ended with remnant of a conus on the disc. But there a cosmic bomb slamming into the Yuca- is no demonstrable inner retinal nutritive tan 65 million years ago annihilating the support for the alligator eye. Perhaps the dinosaurs. Somewhere in the dark ooze closest analogous structure is the choroi- that remained after that catastrophic dal gland of some fish, but the alligator explosion, some opportunistic creatures does not seem to have even this seething were able to survive by capturing live prey, vascular knot found in the choroid, be they fish or terrestrial animals, feeding usually in the posterior pole. Inner retinal exclusively on carrion, or even going for nutrition remains a mystery especially long periods without eating anything since oxygen can diffuse only 143 µm in whatsoever. These grisly veterans are tissue. old—very old, as they can trace their line- The retina has other interesting adap- age to at least the Middle Triassic epoch tations. The retinal pigment epithelium is about 240 million years ago, and they modified in the superior half of the poste- were not about to let a comet interfere the eye from flying debris or kicking limbs rior pole to be a guanine containing non- with their longevity. From those tough during predatory attacks. The lacrimal occludable tapetum lucidum creating the and resistant predecessors come our gland is found under the dorsal orbital eerie primeval blood red glow seen at the modern day crocodilians, with surpris- roof but, in addition, the crocodilians also water’s edge at night in any swamp ingly few, and mostly conservative, mor- have a series of glands lining the under- inhabited by these predators. The tape- phological changes in their skeletal struc- surface of the leading edge of the tum allows the animal to maximise ture. nictitans. These are called Harderian nocturnal photons by reflecting light back The American alligator (Alligator missis- glands, and are seen in many birds and to the photoreceptors after these photons sippiensis) is one of the 23 species of croco- other reptiles. They are ancillary tear have passed through the retina unab- dilians. Living in the southeastern United glands and may produce specialised tears. sorbed. The retina contains cones but is States in swamps and bayous with a In the case of the crocodilians, the predominantly a rod retina, as might be maximum length of 5-6 metres and Harderian glands produce oily tears that expected. Even the cones could be de- weighing as much as two Sumo wrestlers presumably protect what was evolution- scribed as “rod-like” in their histological (between 800–1000 lb (364–455 kg)), this arily a terrestrial eye that returned to appearance, and may be an evolutionary species is important to the biodiversity water and had to readapt to the chronic intermediary as the cones “become” rods and ecology of the area, but may also offer osmotic effects of water on the cornea. So, or are simply lost. The photograph in the us an unintended glimpse into our evolu- the proverbial crocodile tears do exist, and lower right hand portion of the cover tionary past by looking through their in two forms, at that. reveals the fundus and the tapetum. http://bjo.bmj.com/ eyes. The iris is thick and darkly pigmented Although we are taught that these The crocodilians, represented here by and acts as a shade, preventing any stray lethargic appearing predators are closely the American alligator (including an light from entering the globe. The ante- related to other reptiles, they are not. albino shown in the upper left portion of rior layer of the iris is filled with Birds are perhaps their closest relatives, the cover), have several amphibious adap- lipophores giving a light brown or cream and these diapsid cousins probably split tations which are interesting and shed coloration to the iris. Sporting the vertical from the crocodiles during the Middle light on ocular evolution. The eyes are set slit pupil of many terrestrial predators, as Triassic epoch as the ancestral thecodonts above the principal dorsal surface axis of can be seen in the lower left portion of the split into Crocodilia and Aves. This conclu- on September 24, 2021 by guest. Protected copyright. the body so that only the eyes and nostrils cover, alligators have a surprisingly large sion is supported by homologous neuro- remain out of the water for camouflage, eye similar in structure to other verte- logical design as well as genomics (Janke leaving a shadowy outline of the rest of brate tetrapods and, surprisingly, similar A, et al, Mol biol Evol 1997;14:1266–72), but the body. The eye is large, often reaching to birds. Alligators even have the horizon- may be deduced from other evidence as 20 mm in diameter in the alligator and tal strip of concentrated photoreceptors well. larger in other crocodilians. The cornea is that resembles the infula of certain bird The eye should not be overlooked as a flatter than ours and this might be species, such as the flamingo, (see August site for biological data to understand expected as an aquatic adaptation. Conse- 2000 BJO cover). This horizontal strip of phylogenetic relationships. Recently, in- quently, to compensate for the loss of the concentrated photoreceptors can be seen vestigators, discovered that the photopig- refractive power of the cornea, the lens is above the optic disc in the posterior pole ments of A mississippiensis are more closely quite large and round or ellipsoidal much of the alligator eye (lower right portion of related to chickens, and presumably other like a piscine lens. The nocturnal nature the cover). But there are some differences, birds, than to reptiles or mammals (Smith of the species and the participation of and at least one difference asks startling WC, et al, Exp Eye Res 1995;61:569–78). other senses for prey capture probably questions. While many of the ocular The eye proves to be a window to the have put little emphasis on, or need for, structures are homologous, and even evolutionary soul. accommodation. For support, cartilage analogous to humans, the difference in lines much of the sclera, again in piscine retinal nutrition is perplexing. Many ver- Ivan R Schwab fashion. The upper lid contains a bony or tebrates have a direct retinal vascular Dennis E Brooks very tough cartilaginous tarsus with a supply such as our central retinal artery. University of California, Davis, 4860 Y St, Suite cartilaginous plate in the translucent nic- Birds have a pecten to serve inner retinal 2400, Sacramento, CA 95817, USA titans (or third eyelid). The retractor bulbi metabolism; many fish have a falciform ([email protected]; Brooks [email protected]) muscles are able to pull the eye beneath process for the same purpose; turtles and the horizontal plane of the skull, and with other reptiles have a conus papillaris, and Thanks to Judy Gire for assistance and to Bern the bony plate in the upper lid, cover the these intraocular structures are homolo- Levine, DVM of the Parrot Jungle and Gardens eyeball with a fortress-like lid to protect gous. Alligators have none of these, in Miami, Florida. www.bjophthalmol.com.