Brain and sense organ anatomy and histology in hemoglobinless Antarctic icefishes (Perciformes: Notothenioidei: Channichthyidae)

Abstract

The Channichthyidae, one of five Antarctic notothenioid families, includes 16 species and 11 genera. Most live at depths of 200-800 m and are a major component of fish biomass in many shelf areas. Channichthyids are unique among adult fishes in possessing pale white blood containing a few vestigal erythrocytes and no hemoglobin. Here we describe the brains of seven species and special sense organs of eight species of channichthyids. We emphasize Chionodraco hamatus and C. myersi, compare these species to other channichthyids, and relate our findings to what is known about brains and sense organs of red-blooded notothenioids living sympatrically on the Antarctic shelf. Brains of channichthyids generally resemble those of their bathydraconid sister group. Among channichthyids the telencephalon is slightly regressed, resulting in a stalked appearance, but the tectum, corpus cerebellum, and mechanoreceptive areas are well developed. Interspecific variation is present but slight. The most interesting features of channichthyid brains are not in the nervous tissue but in support structures: the vasculature and the subependymal expansions show considerable elaboration. Channichthyids have large accessory nasal sacs and olfactory lamellae are more numerous than in other notothenioids. The eyes are relatively large and laterally oriented with similar duplex (cone and rod) retinae in all eight species. Twin cones are the qualitatively dominant photoreceptor in histological sections and, unlike bathydraconids, there are no species with rod-dominated retinae. Eyes possess the most extensive system of hyaloid arteries known in teleosts. Unlike the radial pattern seen in red-blooded notothenioids and most other teleosts, channichthyid hyaloid arteries arise from four or five main branches and form a closely spaced anastomosing series of parallel channels. Cephalic lateral line canals are membranous and some exhibit extensions (canaliculi), but canals are more ossified than those of deeper-living bathydraconids. We conclude that, with respect to the anatomy and histology of the neural structures, the brain and sensory systems show little that is remarkable compared to other fishes, and exhibit little diversification within the family. Thus, the unusual habitat and a potentially deleterious mutation resulting in a hemoglobinless phenotype are reflected primarily in expansion of the vasculature in the brain and eye partially compensating for the absence of respiratory pigments. Neural morphology gives the impression that channichthyids are a homogeneous and little diversified group.

Morphometry of retinal vasculature in Antarctic fishes is dependent upon the level of hemoglobin in circulation

“…Veins do not accompany the hyaloid arteries in teleosts that have lost the ocular vascular structures mentioned above (Copeland, 1980;Nicol, 1989). This has been documented in histological studies of the retinae of various notothenioids (Eastman, 1988;Eastman and Lannoo, 2003), including channichthyids (Eastman and Lannoo, 2004). The hyaloid arteries drain to an annular vein located in the vicinity of the ora serrata at the retinal periphery (Fig.·3B).…”

“…Because of this aerobic character, maintenance of adequate oxygen tensions is likely to be an acute challenge in eyes of many Antarctic notothenioid fishes, particularly for species of this group in which hemoglobin is expressed at low levels or is completely absent. Previous reports have indicated that dramatic differences exist in geometries of ocular blood vessels when comparing hemoglobinless and red-blooded Antarctic fishes (Eastman, 1988;Eastman and Lannoo, 2004). Those studies qualitatively described substantially higher vascular densities on the vitrad surface of the retina in -Hb species than in +Hb notothenioids but, with the exception of measuring vessel diameters, did not quantify any other morphometric parameter of retinal vascular anatomy.…”

“…In retrospect, this conclusion is somewhat axiomatic, given that the additional blood volume must be accommodated somewhere within the vascular tree. Vasculature associated with the retina of the eye provides an excellent example and is exceptionally dense in Hb-lacking icefishes compared to Hb-expressing notothenioid species (Eastman, 1988;Eastman and Lannoo, 2004;Sidell and O'Brien, 2006). The vasculature of the teleost retina, especially in the case of channichthyids, differs in a number of respects from that of mammals and other fishes.…”

“…There are also three vascular structures not present in mammals: the choroid rete mirabile, the lentiform body (also a rete), and the falciform process (Walls, 1942;Nicol, 1989). Although present in phyletically basal notothenioids (Eastman and Lannoo, in press), channichthyids have lost the latter three structures and the ophthalmic artery may be vestigal or lost as well (Eastman and Lannoo, 2004). Thus the channichthyid retina is supplied by an optic artery that branches at the optic disk into an extensive series of hyaloid arteries at the vitreoretinal interface (Fig.·1A).…”

“…Thus the channichthyid retina is supplied by an optic artery that branches at the optic disk into an extensive series of hyaloid arteries at the vitreoretinal interface (Fig.·1A). These arteries are thin-walled (Eastman and Lannoo, 2004) and serve as large bore arterial capillaries. Veins do not accompany the hyaloid arteries in teleosts that have lost the ocular vascular structures mentioned above (Copeland, 1980;Nicol, 1989).…”