Identification of the notothenioid sister lineage illuminates the biogeographic history of an Antarctic adaptive radiation.

BACKGROUND: Antarctic notothenioids are an impressive adaptive radiation. While they share recent common ancestry with several species-depauperate lineages that exhibit a relictual distribution in areas peripheral to the Southern Ocean, an understanding of their evolutionary origins and biogeographic history is limited as the sister lineage of notothenioids remains unidentified. The phylogenetic placement of notothenioids among major lineages of perciform fishes, which include sculpins, rockfishes, sticklebacks, eelpouts, scorpionfishes, perches, groupers and soapfishes, remains unresolved. We investigate the phylogenetic position of notothenioids using DNA sequences of 10 protein coding nuclear genes sampled from more than 650 percomorph species. The biogeographic history of notothenioids is reconstructed using a maximum likelihood method that integrates phylogenetic relationships, estimated divergence times, geographic distributions and paleogeographic history. RESULTS: Percophis brasiliensis is resolved, with strong node support, as the notothenioid sister lineage. The species is endemic to the subtropical and temperate Atlantic coast of southern South America. Biogeographic reconstructions imply the initial diversification of notothenioids involved the western portion of the East Gondwanan Weddellian Province. The geographic disjunctions among the major lineages of notothenioids show biogeographic and temporal correspondence with the fragmentation of East Gondwana. CONCLUSIONS: The phylogenetic resolution of Percophis requires a change in the classification of percomorph fishes and provides evidence for a western Weddellian origin of notothenioids. The biogeographic reconstruction highlights the importance of the geographic and climatic isolation of Antarctica in driving the radiation of cold-adapted notothenioids.

Divergence in skeletal mass and bone morphology in antarctic notothenioid fishes.

Cover illustration. Notothenioid fishes lack swim bladders, but species live temporarily or permanently in the water column. Without swim bladder, skeletal mass becomes a key determinant of buoyancy. In this issue of the Journal of Morphology, Joseph Eastman and coauthors (pp. 841-861 10.1002/jmor.20258) quantify the degree of skeletal ossification in notothenioid fish and discuss it in phylogenetic context. The cover image shows a volume rendered micro-CT image showing extensive bone in the adult skeleton of the non-Antarctic notothenioid Bovichtus diacanthus from Tristan da Cunha. Tissue density is mapped in false color on a spectrum ranging from less dense (cool colors) to more dense (warm colors). Bone is considerably more extensive in B. diacanthus than in Antarctic notothenioids.

Divergence in skeletal mass and bone morphology in antarctic notothenioid fishes.

Although notothenioid fishes lack swim bladders, some species live temporarily or permanently in the water column. Given its relatively high density, skeletal mass is a key determinant of buoyancy. Notothenioids have reduced skeletal ossification, but there is little quantitative data on the phylogenetic distribution of this trait. We obtained dry skeletal masses for 54 specimens representing 20 species from six notothenioid families. Although comparative data are sparse, notothenioid skeletons comprise a smaller percentage of body mass, <3.5%, than those of three non-notothenioid perciforms. With relatively high skeletal mass, the non-Antarctic Bovichtus diacanthus is similar in skeletal mass to some non-notothenioids. Eleginops maclovinus, the non-Antarctic sister group of the Antarctic clade, has a relatively light skeleton (<2% of body mass) similar to many species in the Antarctic clade. Low skeletal mass is therefore a synapomorphy shared by Eleginops plus the Antarctic clade. We provide gross, histological, and micro-CT documentation of the structure and location of bone and cartilage in skulls, pectoral girdles, and vertebrae, with emphasis on the bovichtid B. diacanthus, the eleginopsid E. maclovinus, and the channichthyid Chaenodraco wilsoni. In Eleginops and the Antarctic clade, most bone is spongy and most species have persisting cartilage in the skull and appendicular skeleton. We also measured the relative size of the notochordal canal in adult vertebral centra of 38 species representing all eight families. There is considerable interspecific variation in this pedomorphic trait and all species show an ontogenetic reduction in the relative size of the canal. However, large persisting canals are present in adults of the Antarctic clade, especially in the nototheniids Pleuragramma and Aethotaxis and in a number of bathydraconid and channichthyid genera.

Ancient climate change, antifreeze, and the evolutionary diversification of Antarctic fishes.

The Southern Ocean around Antarctica is among the most rapidly warming regions on Earth, but has experienced episodic climate change during the past 40 million years. It remains unclear how ancient periods of climate change have shaped Antarctic biodiversity. The origin of antifreeze glycoproteins (AFGPs) in Antarctic notothenioid fishes has become a classic example of how the evolution of a key innovation in response to climate change can drive adaptive radiation. By using a time-calibrated molecular phylogeny of notothenioids and reconstructed paleoclimate, we demonstrate that the origin of AFGP occurred between 42 and 22 Ma, which includes a period of global cooling approximately 35 Ma. However, the most species-rich lineages diversified and evolved significant ecological differences at least 10 million years after the origin of AFGPs, during a second cooling event in the Late Miocene (11.6-5.3 Ma). This pattern indicates that AFGP was not the sole trigger of the notothenioid adaptive radiation. Instead, the bulk of the species richness and ecological diversity originated during the Late Miocene and into the Early Pliocene, a time coincident with the origin of polar conditions and increased ice activity in the Southern Ocean. Our results challenge the current understanding of the evolution of Antarctic notothenioids suggesting that the ecological opportunity that underlies this adaptive radiation is not linked to a single trait, but rather to a combination of freeze avoidance offered by AFGPs and subsequent exploitation of new habitats and open niches created by increased glacial and ice sheet activity.

Divergence of brain and retinal anatomy and histology in pelagic antarctic notothenioid fishes of the sister taxa Dissostichus and Pleuragramma.

The neutrally buoyant Antarctic fishes of the sister taxa Dissostichus (D. eleginoides and D. mawsoni) and Pleuragramma antarcticum diverged early in the notothenioid radiation and filled different niches in the pelagic realm of the developing Southern Ocean. To assess the influence of phylogenetic and ecological factors in shaping neural morphology in these taxa, we studied the anatomy and histology of the brains and retinae, and determined the proportional weights of brain regions. With the brain of the non-Antarctic sister taxon Eleginops maclovinus as plesiomorphic, statistically significant departures in the brains of the two Antarctic taxa include reduction of the corpus cerebelli and expansion of the mesencephalon and medulla. Compared to Eleginops, both species also have a relatively smaller telencephalon, although this is significant only in Dissostichus. There are a number of apomorphic features in the brain of Pleuragramma including reduced olfactory nerves and bulbs, an extremely small corpus cerebelli and an expanded mesencephalon. Although there is not a significant difference in the relative weights of the medulla in the two taxa, the prominence of the eminentia granularis and bulging cap-like appearance of the crista cerebellaris are distinctive in Pleuragramma. Brain histology of Dissostichus and Pleuragramma reflects typical perciform patterns and the two species of Dissostichus are histologically identical. Lateral compression in Pleuragramma and notable lobation in Dissostichus also contribute to differences between the taxa. Compression in Pleuragramma is attributable to convergence on an anchovy/herring body shape and to the relatively large brain in this small fish. The less prominent pattern of lobation of the telencephalon, inferior lobes and corpus cerebelli in Pleuragramma probably reflects underlying histology, specifically a reduction in cellularity of the neuropil in the nuclei and lobes. The retinal histology of Dissostichus and Pleuragramma encompasses the extremes seen in Antarctic notothenioids. Dissostichus has a thin scotopic retina with few cones and a high degree of summation. The retina of Pleuragramma is thick and cellular with many small single cones and rods and resembles that of Eleginops. Pedomorphy has not influenced brain morphology in these species but Pleuragramma has superficial neuromasts that are pedomorphic. Although Dissostichus and Pleuragramma are sympatric in the water column, their brains and retinae are highly divergent and reflect the influences of both phylogeny and ecological partitioning of the pelagic realm. Compared to Eleginops, the relatively smaller corpus cerebelli but relatively larger medulla probably indicates, respectively, reduced activity levels of notothenioids in subzero temperatures and expansion of the mechanosensory lateral line system as a supplement to vision under conditions of reduced light. Compared to Dissostichus, Pleuragramma has reduced olfactory bulbs and corpus cerebelli and an expanded mesencephalon. The reduction of the corpus to a small round knob is consistent with physiological parameters and video observations suggesting that, although pelagic, it is relatively inactive. Because mesencephalic weights also include the valvula cerebelli, the relatively large value for Pleuragramma may be attributable to its role in integration and sensorimotor coordination of information from the highly cellular duplex retina and to integration of signals from thewell-developed octavolateralis system. The brain of Dissostichus displays considerable persistent morphology in its overall resemblance to that of Eleginops, especially the large olfactory bulbs and the relatively large caudally projecting corpus, and Dissostichus exhibits olfactory tracking ability and migratory behavior in common with Eleginops.

Brain and sense organ anatomy and histology of the Falkland Islands mullet, Eleginops maclovinus (Eleginopidae), the sister group of the Antarctic notothenioid fishes (Perciformes: Notothenioidei).

The perciform notothenioid fish Eleginops maclovinus, representing the monotypic family Eleginopidae, has a non-Antarctic distribution in the Falkland Islands and southern South America. It is the sister group of the five families and 103 species of Antarctic notothenioids that dominate the cold shelf waters of Antarctica. Eleginops is the ideal subject for documenting the ancestral morphology of nervous and sensory systems that have not had historical exposure to the unusual Antarctic thermal and light regimes, and for comparing these systems with those of the phyletically derived Antarctic species. We present a detailed description of the brain and cranial nerves of Eleginops and ask how does the neural and sensory morphology of this non-Antarctic notothenioid differ from that seen in the phyletically derived Antarctic notothenioids? The brain of Eleginops is similar to those of visually oriented temperate and tropical perciforms. The tectum is smaller but it has well-developed olfactory and mechanoreceptive lateral line areas and a large, caudally projecting corpus cerebellum. Eye diameter is about twofold smaller in Eleginops than in many Antarctic species. Eleginops has a duplex (rod and cone) retina with single and occasional twin cones conspicuous centrally. Ocular vascular structures include a large choroid rete mirabile and a small lentiform body; a falciform process and hyaloid arteries are absent. The olfactory rosette is oval with 50-55 lamellae, a large number for notothenioids. The inconspicuous bony canals of the cephalic lateral line system are simple with membranous secondary branches that lack neuromasts. In Antarctic species, the corpus cerebellum is the most variable brain region, ranging in size from large and caudally projecting to small and round. "Stalked" brains showing reduction in the size of the telencephalon, tectum, and corpus cerebellum are present in the deep-living artedidraconid Dolloidraco longedorsalis and in most of the deep-living members of the Bathydraconini. Eye diameter is generally larger in Antarctic species but there is a phylogenetic loss of cellularity in the retina, including cone photoreceptors. Some deep-living Antarctic species have lost most of their cones. Mechanosensation is expanded in some species, most notably the nototheniid Pleuragramma antarcticum, the artedidraconid genera Dolloidraco and Pogonophryne, and the deep living members of the bathydraconid tribe Bathydraconini. Reduction in retinal cellularity, expansion of mechanoreception, and stalking are the most noteworthy departures from the morphology seen in Eleginops. These features reflect a modest depth or deep-sea effect, and they are not uniquely "Antarctic" attributes. Thus, at the level of organ system morphology, perciform brain and sensory systems are suitable for conditions on the Antarctic shelf, with only minor alterations in structure in directions exhibited by other fish groups inhabiting deep water. Notothenioids retain a relative balance among their array of senses that reflects their heritage as inshore perciforms.

Biogeography and adaptation of Notothenioid fish: hemoglobin function and globin-gene evolution.

The recognition of the important role of the polar habitats in global climate changes has awakened great interest in the evolutionary biology of polar organisms. They are exposed to strong environmental constraints, and it is important to understand how they have adapted to cope with these challenges and to what extent adaptations may be upset by current climate changes. We present an introductory overview of the evolution of the Antarctic fish fauna with emphasis on the dominant perciform sub-order Notothenioidei, as well as some specific comments on the biogeography of the three phyletically basal notothenioid families. The wealth of information on the ecology and biodiversity of the species inhabiting high-Antarctic and sub-Antarctic regions provides a necessary framework for better understanding the origin, evolution and adaptation of this unique group of fish. Notothenioidei offer opportunities for identification of the biochemical characters or the physiological traits responsible for thermal adaptation. The availability of phylogenetically related taxa in a wide range of latitudes has allowed to look into the molecular bases of environmentally driven phenotypic gain and loss of function. In the process of cold adaptation, the evolutionary trend of notothenioids has produced unique specialisations, including modification of hematological characteristics, e.g. decreased amounts and multiplicity of hemoglobins. The Antarctic family Channichthyidae (the notothenioid crown group) is devoid of hemoglobin. This loss is related to a single deletional event removing all globin genes with the exception of the inactive 3' end of adult alpha-globin. In reviewing hemoglobin structure, function and phylogeny, the evolution of the fish Root effect is analysed in detail. Adaptation of the oxygen-transport system in notothenioids seems to be based on evolutionary changes involving levels of biological organisation higher than the structure of hemoglobin.

Brain and sense organ anatomy and histology of two species of phyletically basal non-Antarctic thornfishes of the Antarctic suborder Notothenioidei (Perciformes: Bovichtidae).

The predominantly non-Antarctic family Bovichtidae is phyletically basal within the perciform suborder Notothenioidei, the dominant component of the Antarctic fish fauna. In this article we focus on the South Atlantic bovichtids Bovichtus diacanthus, the klipfish from tide pools at Tristan da Cunha, and Cottoperca gobio, the frogmouth from the Patagonian shelf and Falkland Islands. We document the anatomy and histology of the brains, olfactory apparatus, retina, and cephalic lateral line system. We also use the microvascular casting agent Microfil to examine ocular vascular structures. We provide detailed drawings of the brains and cranial nerves of both species. Typical of perciforms, the brains of both species have a well-developed tectum and telencephalon and robust thalamic nuclei. The telencephalon of C. gobio is prominently lobed, with the dorsomedial nucleus more conspicuous than in any other notothenioid. The corpus cerebelli is relatively small and upright and, unlike other notothenioids, has prominent transverse sulci on the dorsal and caudal surfaces. Areas for lateral line mechanoreception (eminentia granularis and crista cerebellaris) are also conspicuous but olfactory, gustatory, and somatosensory areas are less prominent. The anterior lateral line nerve complex is larger than the posterior lateral line nerve in B. diacanthus, and in their cephalic lateral line systems both species possess branched membranous tubules (which do not contain neuromasts) with small pores. These are especially complex in B. diacanthus where they become increasingly branched and more highly pored in progressively larger specimens. Superficial neuromasts are sparse. Both species have duplex (cone and rod) retinae that are 1.25-fold thicker and have nearly 5-fold more photoreceptors and than those of most Antarctic notothenioids. Convergence ratios are also high for bovichtids. Bovichtus diacanthus has a yellow intraocular filter in the dorsal aspect of the cornea. Both species are unique among notothenioids in possessing all three vascular structures present in the generalized teleostean eye: the choroid rete mirabile, the lentiform body (also a rete), and the falciform process. When comparing the phyletically derived Antarctic clade exemplified by the families Artedidraconidae, Bathydraconidae, and Channichthyidae to the phyletically basal bovichtids, we observe phyletic regression and reduction in some regions of the brain and in some sensory modalities that are well displayed in bovichtids. In the phyletically derived families the brain is less cellular and nuclei are smaller and less prominent. In some species reduction in the size of the telencephalon, tectum, and corpus cerebelli imparts a "stalked" appearance to the brain with the neural axis visible between the reduced lobes. There is also a phyletic reduction in the number of ocular vascular structures from three in bovichtids to one or none in artedidraconids, bathydraconids, and channichthyids. There are no morphological features of bovichtid brains and sense organs that presage the divergence of the phyletically derived members of the clade in the Antarctic marine environment with its cold and deep continental shelves. We conclude that this environment does not require sensory or neural morphology or capabilities beyond those provided by the basic perciform body plan.

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

We quantitatively assessed ocular vascular patterns of six Antarctic notothenioid fishes that vary in their expression of the circulating oxygen-binding protein, hemoglobin (Hb). Digital image analyses revealed marked differences in vessel morphometries among notothenioid species. Hemoglobinless (-Hb) icefishes display mean vessel length densities that are greater (Chaenocephalus aceratus, 5.51+/-0.32 mm mm(-2); Champsocephalus gunnari, 5.15+/-0.50 mm mm(-2)) than those observed in red-blooded (+Hb) species (Gymnodraco acuticeps, 5.20+/-0.46 mm mm(-2); Parachaenichthyes charcoti, 4.40+/-0.30 mm mm(-2); Trematomus hansoni, 3.94+/-0.08 mm mm(-2); Notothenia coriiceps, 2.48+/-0.21 mm mm(-2)). -Hb fishes also have mean vessel diameters that are approximately 1.5 times greater than vessel diameters of +Hb species (-Hb, 0.193+/-0.006 mm; +Hb, 0.125+/-0.005 mm). Vascular density index (VDI), a stereological index that is affected by both vessel number and length, is greatest in -Hb C. aceratus (3.51+/-0.20) and lowest in +Hb N. coriiceps (1.58+/-0.14). Among four +Hb species, there is a direct relationship between red blood cell content and retinal vasculature. Hematocrit (Hct) is inversely correlated to vascular density (r(2)=0.934) and positively correlated to intervessel distance (r(2)= 0.898) over a >2.3-fold range of Hct. These results indicate that anatomical capacity to supply blood to the retina increases to compensate for decreases in oxygen-carrying capacity of the blood.

Brain and sensory organ morphology in Antarctic eelpouts (Perciformes: Zoarcidae: Lycodinae).

Eelpouts of the family Zoarcidae comprise a monophyletic group of marine fishes with a worldwide distribution. Centers of high zoarcid diversity occur in the North Atlantic and North Pacific, with important radiations into the Arctic, along southern South America, and into the Southern Ocean around Antarctica. Along with snailfishes (Liparidae), zoarcids form an important component of the non-notothenioid fauna in the subzero shelf waters of Antarctica. We document the anatomy and histology of the brains, cranial nerves, olfactory apparatus, cephalic lateral lines, taste buds, and retinas of three Antarctic zoarcid species, living at depths of 310-939 m, representing three of the nine genera from this region. The primary emphasis is on Ophthalmolycus amberensis, and we provide a detailed drawing of the brain and cranial nerves of this species. Although this brain reflects general perciform neural morphology, it exhibits a reduction of the (optic) tecta and the eminentia granulares and crista cerebellares of the lateral line system. Interspecific differences among the three species are slight. The olfactory rosette consists of three to four lamellae and the nasal sac, contrary to the claim of Fanta et al. ([2001] Antarct Rec, Natl Inst Polar Res, Tokyo 45:27-42), is not in communication with the cephalic lateral line system. Primary olfactory neurons are abundant and converge on branches of the olfactory nerve. Numerous taste buds are located in the lips. All three species lack an ocular choroid rete and have relatively thin retinas with a low cell density and a single bank of rods as the only type of photoreceptor. Neural diversification among Antarctic zoarcids has not involved the evolution of sensory specialists; brain and sensory organ morphologies do not approach the condition seen in primary deep-sea fishes, or even that of some sympatric non-perciform secondary deep-sea fishes, including liparids and muraenolepidids (eel cods). There may be phylogenetic constraints on brain morphology in perciforms such that we do not see extreme specialization in sensory and neural systems for deep habitats. We suggest that the brains and sensory organs of Antarctic zoarcids reflect habitation of 500-2,000-m depths and likely reflect morphologies seen in zoarcids living on continental slopes elsewhere in the world. This balance among the sensory modalities makes zoarcids relatively generalized among secondary deep-sea fishes and may be one of the reasons this opportunistic and adaptable group has been successful in colonizing a variety of emergent and ephemeral habitats.

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

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.

Diversification of brain and sense organ morphology in Antarctic dragonfishes (Perciformes: Notothenioidei: Bathydraconidae).

In the subzero shelf waters of Antarctica, fishes of the perciform suborder Notothenioidei dominate the fish fauna and constitute an adaptive radiation and a species flock. The 16 species of dragonfishes of the family Bathydraconidae live from surface waters to nearly 3,000 m and have the greatest overall depth range among notothenioid families. We examined the anatomy and histology of the brain, retina, and cephalic lateral line system of nine bathydraconid species representing 8 of the 11 known genera. We evaluate these data against a cladogram identifying three clades in the family. We provide a detailed drawing of the brain and cranial nerves of Gymnodraco acuticeps and Akarotaxis nudiceps. Bathydraconid brain morphology falls into two categories. Brains of most species are similar to those of generalized perciforms and some basal notothenioids (Class I). However, brains of deep-living bathydraconids (members of the tribe Bathydraconini minus Prionodraco) have a reduced telencephalon and tectum that renders the neural axis visible - the stalked brain morphology (Class II). All bathydraconids have duplex (rod and cone) retinae but there is considerable interspecific variation in the ratio of cones:rods and in the number of cells in the internal nuclear layer. Retinal histology reflects habitat depth but is not tightly coupled to phylogeny. Although the deep-living species of Bathydraconini have rod-dominated retinae, the retinae of some sister species are photopic. An expanded cephalic lateral line system is also characteristic of all members of the Bathydraconini as exemplified by Akarotaxis. This morphology includes large lateral line pores, wide membranous canals, hypertrophied canal neuromasts, and large anterodorsal lateral line nerves, eminentia granulares, and crista cerebellares. The saccular otoliths are also enlarged in members of this tribe. Neural diversification among bathydraconids on the Antarctic shelf has not involved the evolution of sensory specialists. Brain and sense organ morphologies do not approach the specialized condition seen in primary deep-sea fishes or even that of some secondary deep-sea fishes including sympatric non-notothenioids such as liparids (snailfishes) and muraenolepidids (eel cods). The brains and sense organs of bathydraconids, including the deep-living species, reflect their heritage as perciform shorefishes.

Anatomy and histology of the brain and sense organs of the antarctic plunderfish Dolloidraco longedorsalis (Perciformes: Notothenioidei: Artedidraconidae), with comments on the brain morphology of other artedidraconids and closely related harpagiferids.

In the high-latitude shelf waters of Antarctica, fishes in the perciform suborder Notothenioidei dominate the fish fauna and constitute an adaptive radiation and a species flock. The 25 species of notothenioid plunderfishes, comprising four genera of the family Artedidraconidae, contribute substantially to fish species diversity on the high Antarctic shelf. A mental barbel is an autapomorphy for the family. Dolloidraco longedorsalis is the most abundant artedidraconid at depths over 400 m in these waters. In this article we present the anatomy and histology of the brain and special sense organs of Dolloidraco and compare it to the brains of other artedidraconids, closely related harpagiferids, and more generally to other notothenioids. We provide a detailed drawing of the brain and cranial nerves. The brain of Dolloidraco is simple, without external hypertrophy of sensory or motor regions, but contains several unusual features associated with the ventricular system and CSF, including well-developed circumventricular organs, subependymal expansions, and subarachnoid cisterns; and a ventricle in the corpus cerebellum. The brain of Dolloidraco also contains a lobed chief sensory nucleus of the trigeminal nerve that is correlated across species with barbel length. The eyes are large and contain a small choroid rete, a structure previously thought to be absent from members of this family. We document the histology of the duplex retina, olfactory apparatus, cutaneous taste buds, and barbel musculature and innervation. We discuss the role of pedomorphy in producing simplified brain morphologies. We consider the possibility that Dolloidraco is a somatosensory specialist-an unusual feature among vertebrates-and decide that this is unlikely.

Buoyancy studies and microscopy of skin and subdermal extracellular matrix of the antarctic snailfish, Paraliparis devriesi.

The Antarctic snailfish Paraliparis devriesi (Liparididae) occupies an epibenthic habitat at a depth of 500-650 m in the subzero waters of McMurdo Sound, Antarctica. Although lacking a swim bladder, this species is neutrally buoyant through the combined effects of reduced skeletal ossification and expansion of a watery gelatinous subdermal extracellular matrix (SECM). The SECM serves as a low density buoyancy agent. It comprises a mean of 33.8% of the body weight, the largest known proportion of any adult fish. The SECM is loose connective tissue dominated by ground substance consisting of glycosaminoglycans, especially hyaluronic acid, and immobilized water. Although the SECM is 97% water, elevated levels of NaCl provide an osmotic strength greater than that of other body fluids. Only small amounts of antifreeze compounds have been identified in P. devriesi; therefore, freezing avoidance may result from the combined effects of antifreezes and the elevated osmolality of body fluids. The skin overlying the SECM is thin (85-200 µm) and loose, and unlike most other fishes, the epidermis is several times thicker than the dermis. The midepidermis, has a distinctive layer of vacuolated club cells of unknown function. Light and electron microscopy indicate that the skin is unspecialized for protection against entry of ice. © 1994 Wiley-Liss, Inc.

Skin structure and vascularization in the Antarctic notothenioid fish Gymnodraco acuticeps.

The scaleless notothenioid Gymnodraco acuticeps is a bottom dweller beneath the sea ice of McMurdo Sound, Antarctica. Gymnodraco experience unusual environmental conditions, including highly oxygenated subzero water. Skin morphology is evaluated with reference to its potential as a barrier to ice propagation and as a surface for cutaneous respiration. Light and electron microscopy and histochemistry reveal skin structure that is generally similar to that of other teleosts. In the epidermis, epithelial cells are arranged in nine to fifteen layers, and two types of mucous cells are also present. Large mucous cells are most common on external epidermal surfaces, whereas small cells are more frequent on internal epithelial surfaces. Epithelial cell junctions have extensive areas of desmosomes as well as interdigitations of the cell membranes, especially in the basal and midepidermis. The dermis consists of an exceptionally dense stratum compactum. The skin is thicker than that of Bovichtus, a scaleless temperate notothenioid from New Zealand. Mean skin thicknesses at sites on the trunk are 371-711 µm. With the exception of fins that contact the substrate, epidermal thickness between rays of most fins is 70-118 µm. The epithelial surfaces of the oral and branchial cavities are 27-50 µm thick. An unusual type of connective tissue is present beneath the epidermis of the pelvic fin. It contains abundant ground substance and is similar to mucous connective tissue of the mammalian umbilical cord. Perfusions of a microvascular filling agent reveal a moderately developed cutaneous vasculature. These vessels have the dimensions of capillaries (mean external diameter 11 µm). They are confined to the dermis and are more prominent on the head than on the trunk. The skin is secondary to the gills as a respiratory surface in Gymnodraco.

Ocular morphology in antarctic notothenioid fishes.

Beneath the sea ice at McMurdo Sound, Antarctica, notothenioid fishes are subject to extreme seasonal variation in the annual light cycle including 4 months of continual darkness. Gross and microscopic anatomy of the eyes of 18 species revealed ocular morphology that was generally similar to that of coastal fishes elsewhere in the world, and unlike that of deep sea fishes living in perpetual darkness. The spectacle was well developed as were hyaloid arteries at the vitreoretinal interface. Fourteen species had a choroid body, and its presence was considered a primitive character state for notothenioids. The choroid body was absent in phyletically derived groups. The choroid body was especially large in Dissostichus mawsoni, the only species with a rod dominated retina. Retinae were 154-279 µm thick with layering and sublayering typical for teleosts. Although all species had both rods and cones, there was marked interspecific variation in the ratio of cones:rods and in the total number of visual cells. Non-Antarctic notothenioids from New Zealand had more visual cells than most species from McMurdo Sound. Retinae appeared balanced for vision under dim but seasonally variable light conditions and not specially adapted to the 4-month period of winter darkness. Retinal histology reflected the ecology and depth range of most species. Based on ecology and retinal histology, four groups of species were recognized: (1) Non-Antarctic, (2) cryopelagic (including two visually oriented benthic species), (3) pelagic and benthopelagic, and (4) benthic.

Buoyancy adaptations in a swim-bladderless Antarctic fish.

The endemic Antarctic teleosts of the suborder Notothenioidei are bottom dwellers. They lack swim bladders, are heavier than seawater, and feed on or near the bottom. The midwaters surrounding the Antarctic continent are productive and underutilized by fishes. There is an evolutionary trend toward pelagism in some notothenioids. We discovered that the largest Antarctic fish, Dissostichus mawsoni, was neutrally buoyant. Attainment of neutral buoyancy was associated with specializations of the skeletal, integumentary, muscular, and digestive systems. The skeleton had a low mineral content and contained considerable cartilage. Scales were also incompletely mineralized. Static lift was obtained from extensive lipid (mostly triglyceride) deposits. A 2-8 mm subcutaneous lipid layer accounted for 4.7% of the body weight. White muscle also contained much lipid-23% on a dry weight basis, or 4.8% of the body weight. Microscopic examination suggested that the liver was active in lipid metabolism, although it was not an organ of buoyancy. Stellate (perisinusoidal) cells with many lipid droplets were a very prominent cytological component of the liver. These specializations made Dissostichus neutrally buoyant and capable of inhabiting the food-rich Antarctic midwaters.