The Deep-Sea Teleost Cornea: a Comparative Study of Gadiform Fishes
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Histol Histopathol (1998) 13: 325-336 Histology and 001: 10.14670/HH-13.325 Histopathology http://www.hh.um.es From Cell Biology to Tissue Engineering The deep-sea teleost cornea: a comparative study of gadiform fishes S.P. Collin1 and H.B. Collin2 1Marine Neurobiology Laboratory, Department of Zoology, University of Western Australia, Nedlands, Western Australia and 2Department of Optometry and Visual Sciences, The University of Melbourrne, Parkville, Victoria, Australia Summary. The corneal structure of three deep-sea spectacles (Hein, 1913; Walls, 1942), corneal filters species of teleosts (Gadiformes, Teleostei) from different (Moreland and Lythgoe, 1968; Appleby and Muntz, depths (250-4000 m) and photic zones are examined at 1979; Heinermann, 1984; Kondrashev et aI., 1986), the level of the light and electron microscopes. Each iridescent layers (Locket, 1972; Lythgoe, 1975, 1976), species shows a similar but complex arrangement of annular ligaments (Tripathi, 1974; Collin and Collin, layers with a cornea split into dermal and scleral 1996), autochthonous layers (Walls, 1942; Collin and components. The dermal cornea comprises an epithelium Collin, 1988), sutural fibres (Smelser, 1962; Fisher and overlying a basement membrane and a dermal stroma Zudunaisky, 1977), mucoid laye rs (Walls, 1942; with sutures and occasional keratocytes. N ezumia Tripathi, 1974) and epithelial goblet cells (Collin and aequalis is the only species to possess a Bowman's Collin, 1996) are features of a range of shallow-water layer, although it is not well-developed. The scleral species from a diverse range of habitats. cornea is separated from the dermal cornea by a mucoid In contrast, the deep-sea teleost cornea has received layer and, in contrast to shallow-water species, is divided relatively little attention. Although primarily thought to into three main layers; an anterior scleral stroma, a act as a protective goggle, the cornea of deep-sea teleosts middle or iridescent layer and a posterior scleral stroma. mus t also overcome the physical constraints of The iridescent layer of collagen and intercalated cells or temperature and pressure, while maintaining a clear cellular processes is bounded by a layer of cells and the optical pathway for the transmission of both low levels posterior scleral stroma overlies a Des<;emet's membrane of sunlight and bioluminescent emissions. Most deep-sea and an endothelium. In the relatively shallow-water teleosts survive between 2 and 5 DC at depths where the Microgadus proximus, the keratocytes of the dermal pressure may attain over 400 atmospheres. Although stroma, the ce lls of the iridescent layer and the light levels are high in the upper euphotic zone, levels endothelial cells all contain aligned endoplasmic fall markedly to a depth of 1000 m, beyond which not reticulum, which may elicit an iridescent reflex. No even single quanta of sunlight penetrate (Denton, 1990). alignment of the endoplasmic reticulum was found in N. Previous studies on the eyes of deep-sea fishes have aequalis or Coryphanoides (Nematonurus) armatus. The identified a number of corneal specialisations. These relative differences between shallow-water and deep-sea include corneal projections (Pearcy et aI., 1965) or corneas are discussed in relation to the constraints of pearly accessory corneal bodies (Whitehead et aI., 1989) light, depth and temperature. adjacent to the secondary globe in the eye of Bathylychnops exilis (Opisthoproctidae), which may Key words: Cornea, Ultrastructure, Deep-sea, Iridescent increase the monocular visual field. Similarly, the lens layer, Spectacle, Fishes pad in the scopelarchid, Scopelarchus guntheri, and the optical fold in the evermannelid, Evermannella indica, are both thought to extend the monocular visual field, Introduction allowing light to strike the ventro-Iateral aspect of the lens and a specialised region of the accessory retina by The cornea of shallow-water teleosts has undergone light guiding and geometrical optics, respectively extensive selection incorporating a number of unique (Locket, 1971, 1977; Collin et aI., 1997). structural adaptations setting them apart from almost all With the exception of the few species mentioned other vertebrate corneas. Specialisations such as above, little is known of the basic arrangement of layers in the corneas of deep-sea teleosts, although the Offprint requests to: Dr. Shaun P. Collin, Marine Neurobiology tendency for a split cornea has been noted by a few Laboratory, Department of Zoology, University of Western Australia, authors. In the tripod fish, Bathypterois longipes Nedlands, 6907, Western Australia, Australia (Bathypteroidae) and the sea snail , Careproctus 326 The deep-sea teleost cornea kermadecensis (Liparididae), the dermal and scleral Corneas were post-fixed in 2% osmium tetroxide with corneas are split with the dermal cornea continuous with 1.5% potassium ferrocyanide in O.IM sodium cacodylate the skin and the scleral cornea continuous with the buffer (the reduced osmium method of Collin and scleral eyecup (Munk, 1964a). Munk (1966) also noted Allansmith, 1977, which is a slight modification of the that in the mesopelagic Nallsenia groenlandica, the inner osmium potassium ferrocyanide method of Dvorak et aI., surface of the scleral cornea is covered by Des~emet's 1972). Tissue was then dehydrated in acetone and membrane, a thin endothelium and a thick annular embedded in resin (Polybed/812, Polysciences Inc). ligament in the irido-corneal angle. Even where the eyes Thick (1 ,urn) sections were stained with Richardson's are thought to be degenerate (i.e. in the angler fishes stain and examined by light microscopy. Thin sections Cryptopsaras cousei and Ceratias holboelli, Ceratiidae), were stained with lead citrate and uranyl acetate and the cornea is well developed with dermal and scleral examined on a Siemens Elmiskop lA or an Hitachi components separated by loose connective tissue (Munk, H500 transmission electron microscope. 1964b), although the scleral stroma is thought to be thin. Measurements were taken from photographic In this study, we have examined three species of enlargements using a graticule and magnifying glass. gadiform fishes from three different photic zones; the Photographs were taken on either 35 mm Kodak Pacific tom cod, Microgadus proximus (Gadidae) from Technical Pan film (rated at 50 ASA, light microscopy) the well-lit waters of the euphotic zone, the rat-tail, or Kodak 4489 electron microscope film. Nezumia aequalis (Macrouridae) from the twilight or mesopelagic zone and the armoured grenadier, Results Coryphanoides (Nematonurus) armatus (Macrouridae) from the dark benthopelagic zone where sunlight fails to The general structure and arrangement of the penetrate. This detailed ultrastructural study, provides a corneas in the three species examined is shown in Fig.I. comparative analysis of the structure and arrangement of Detailed measurements of each layer and its component the cornea in response to the constraints of light, structures for each species are also provided (Table 1). temperature and pressure. The overall corneal structure of all three species is similar. The corneas of species from three photic zones Materials and methods (namely the euphotic, the mesopelagic and the benthopelagic zones) showed evidence of an epithelium. Four specimens of each of the Pacific tom cod, However, as a result of the method of collection, all Microgadus proximus (Gadidae, Gadiformes), the rattail, except one cornea (Microgadus proximus) were devoid Nezumia aequalis (Macrouridae, Gadiformes) and the of a complete epithelium. Hence, the thickness of only armoured grenadier, Coryphanoides (Nematonurus) one species could be estimated. armatus (Macrouridae, Gadiformes) were used in this All three species have a well-developed epithelial study. Specimens of M. proximus were collected in Puget basement membrane, although that of Coryphanoides Sound, San Juan Island, Washington (USA) and (Nematonurus) armatus is particularly thick (1.8 ,urn). specimens of N. aequalis and C. (N.) armatus were Anchoring fibrils are evident in all species and are collected on a scientific expedition on board the RRS particularly prominent in M. proximus and C. (N.) 'Challenger' in 1992 (Cruise No. 94) in the vicinity of armatus (Fig. 2A, B, D). Only Nezumia aequalis has a 49-51 ON (latitude) and 110-150 oW (longitude) over the thin Bowman's layer (0.2,um in thickness) of randomly Globan Spur and Porcupine Sea Bight. All specimens arranged collagen fibrils (Fig. 2C). were captured with semi-balloon otter trawling nets There are three separate collections of collagen fibril (OTSB 14) at depths between 100 and 4,000 m. lamellae forming three stromas (Fig. 1). The central For all specimens, sampling was carried out thickness of these strom as varies considerably (Table 1) according to the ethical guidelines of the National Health with the dermal stroma (or spectacle) being thickest (up and Medical Research Council of Australia. Most to 0.18 mm), followed by the anterior scleral stroma (30 animals were dead when the trawl was brought on deck to 53 ,um) and the posterior scleral stroma (2.7 to 6,um). but some animals were killed by immersion in an The central and peripheral stromal thickness is similar overdose of tricaine methane sulphonate (MS 222, for each species except for the anterior scleral stroma of 1:2,000) in seawater, after which the eyes were excised. M. proximus, which is approximately 30 ,um thick The eyes of all specimens were intact