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.     

Mitochondrial DNA,morphology, and the phylogenetic relationships of Antarctic icefishes (Notothenioidei: Channichthyidae)

The Channichthyidae is a lineage of 16 species in the Notothenioidei, a clade of fishes that dominate Antarctic near-shore marine ecosystems with respect to both diversity and biomass. Among four published studies investigating channichthyid phylogeny, no two have produced the same tree topology, and no published study has investigated the degree of phylogenetic incongruence between existing molecular and morphological datasets. In this investigation we present an analysis of channichthyid phylogeny using complete gene sequences from two mitochondrial genes (ND2 and 16S) sampled from all recognized species in the clade. In addition, we have scored all 58 unique morphological characters used in three previous analyses of channichthyid phylogenetic relationships. Data partitions were analyzed separately to assess the amount of phylogenetic resolution provided by each dataset, and phylogenetic incongruence among data partitions was investigated using incongruence length difference (ILD) tests. We utilized a parsimony-based version of the Shimodaira-Hasegawa test to determine if alternative tree topologies are significantly different from trees resulting from maximum parsimony analysis of the combined partition dataset. Our results demonstrate that the greatest phylogenetic resolution is achieved when all molecular and morphological data partitions are combined into a single maximum parsimony analysis. Also, marginal to insignificant incongruence was detected among data partitions using the ILD. Maximum parsimony analysis of all data partitions combined results in a single tree, and is a unique hypothesis of phylogenetic relationships in the Channichthyidae. In particular, this hypothesis resolves the phylogenetic relationships of at least two species (Channichthys rhinoceratus and Chaenocephalus aceratus), for which there was no consensus among the previous phylogenetic hypotheses. The combined data partition dataset provides substantial statistical power to discriminate among alternative hypotheses of channichthyid relationships. These findings suggest the optimal strategy for investigating the phylogenetic relationships of channichthyids is one that uses all available phylogenetic data in analyses of combined data partitions.     

Antarctic icefishes (Channichthyidae): a unique family of fishes. A review, Part I

Icefish or white-blooded fish are a family of species, unique among vertebrates in that they possess no haemoglobin. With the exception of one species which occurs on the southern Patagonian shelf, icefish live only in the cold-stable and oxygen-rich environment of the Southern Ocean. It is still questionable how old icefish are in evolutionary terms: they may not be older than 6 Ma, i.e. they evolved well after the Southern Ocean started to cool down or they are 15–20 Ma old and started to evolve some time after the formation of the Antarctic Circumpolar Current. Individuals of most icefish species with the exception of species of the genus Champsocephalus have been found down to 700–800 m depth, a few even down to more than 1,500 m. Icefish have been shown to present organ-level adaptations on different levels to compensate for the ‘disadvantages’ of lacking respiratory pigments. These include a low metabolic rate, well perfused gills, increased blood volume, increased cardiac output, cutaneous uptake of oxygen, increased blood flow with low viscosity, enlarged capillaries, large heart, and increased skin vascularity. Biological features, such as reproduction and growth, are not unique and are comparable to other notothenioids living in the same environment. Icefish produce large yolky eggs which have a diameter of more than 4 mm in most species. Consequently, the number of eggs produced is comparatively small and exceeds 10,000–20,000 eggs in only a few cases. With the exception of species of the genus Champsocephalus which mature at an age of 3 to 4 years, icefish do not attain maturity before they are 5–8 years old. Spawning period of most icefish species is autumn-winter. The incubation period spans from 2 to 3 months in the north of the Southern Ocean to more than 6 months close to the continent. Growth in icefish to the extent it is known is fairly rapid. They grow 6–10 cm in length per annum before they reach spawning maturity. Icefish feed primarily on krill and fish. Some icefish species were abundant enough to be exploited by commercial fisheries, primarily in the 1970s and 1980s with Champsocephalus gunnari as the main target species. Most stocks of this species had been overexploited by the beginning of the 1990s, some had further declined due to natural causes. Other species taken as by-catch species in fisheries were Chaenocephalus aceratus, Pseudochaenichthys georgianus, and Chionodraco rastrospinosus. Chaenodraco wilsoni was the only species exploited on a commercial scale in the high-Antarctic. Part II will be published in the following issue. DOI 10.1007/s00300-005-0020-6.     

Antarctic icefishes (Channichthyidae): a unique family of fishes. A review, Part II

Icefish or white- blooded fish are a family of species unique among vertebrates in that they possess no haemoglobin. With the exception of one species which occurs on the southern Patagonian shelf, icefish live only in the cold-stable and oxygen-rich environment of the Southern Ocean. It is still questionable how old icefish are in evolutionary terms: they may not be older than 6 Ma, i.e. they evolved well after the Southern Ocean started to cool down or they are 15–20 Ma old and started to evolve some time after the formation of the Antarctic Circumpolar Current. Individuals of most icefish species with the exception of species of the genus Champsocephalus have been found down to 700–800 m depth, a few even down to more than 1,500 m. Icefish have been shown to present organ-level adaptations on different levels to compensate for the ‘disadvantages’ of lacking respiratory pigments. These include a low metabolic rate, well perfused gills, increased blood volume, increased cardiac output, cutaneous uptake of oxygen, increased blood flow with low viscosity, enlarged capillaries, large heart, and increased skin vascularity. Biological features, such as reproduction and growth, are not unique and are comparable to other notothenioids living in the same environment. Icefish produce large yolky eggs which have a diameter of more than 4 mm in most species. Consequently, the number of eggs produced is comparatively small and exceeds 10,000–20,000 eggs in only a few cases. With the exception of species of the genus Champsocephalus which mature at an age of 3 to 4 years, icefish do not attain maturity before they are 5–8 years old. Spawning period of most icefish species is autumn–winter. The incubation period spans from 2 to 3 months in the north of the Southern Ocean to more than 6 months close to the continent. Growth in icefish to the extent it is known is fairly rapid. They grow 6–10 cm in length per annum before they reach spawning maturity. Icefish feed primarily on krill and fish. Some icefish species were abundant enough to be exploited by commercial fisheries, primarily in the 1970s and 1980s with Champsocephalus gunnari as the main target species. Most stocks of this species had been overexploited by the beginning of the 1990s, some had further declined due to natural causes. Other species taken as by-catch species in fisheries were Chaenocephalus aceratus, Pseudochaenichthys georgianus, and Chionodraco rastrospinosus. Chaenodraco wilsoni was the only species exploited on a commercial scale in the high-Antarctic. Part I was published in the preceding issue of Polar Biology. DOI 10.1007/s00300-005-0019-z.     

Morphological Characteristics of Sailfish Pike Channichthys velifer (Channichthyidae) from the Kerguelen Islands (Southern Ocean)

Journal of Ichthyology - Based on a representative sample set (41 specimens), features of external morphology, seismosensory system, and axial skeleton of the sailfish pike Channichthys velifer...     

Nitric oxide synthase type I (nNOS), vascular endothelial growth factor (VEGF) and myoglobin-like expression in skeletal muscle of Antarctic icefishes (Notothenioidei: Channichthyidae)

The Antarctic icefishes Channichthyidae lack haemoglobin and are thought to lack myoglobin (Mb) in their skeletal muscle as well. Due to the absence of both respiratory pigments, icefishes may present a variety of physiological adaptations in their skeletal muscles. In mammals, molecular responses to limiting oxygen availability in the skeletal muscle include, among others, the over expression of nitric oxide synthases (NOS), such as type I (neuronal nNOS) and type III (endothelial eNOS), as well as the vascular endothelial growth factor (VEGF). In this paper, we evaluated by western blot analysis whether the skeletal muscle of haemoglobin-less icefishes expresses in a constitutive manner higher levels of the type I and type III NOS isoforms and VEGF. Our results demonstrate that haemoglobin-less icefish of the family Channichthyidae do indeed present higher expression of the type I NOS isoform compared with red-blooded Antarctic fish species of other families of the same suborder Notothenioidei. In contrast, VEGF was not over-expressed. Moreover, we show that some icefish species, thought previously to lack Mb in oxidative muscles, actually present Mb-like immunoreactivity in their skeletal muscle.     

Population divergences despite long pelagic larval stages: lessons from crocodile icefishes (Channichthyidae)

Dispersal via pelagic larval stages plays a key role in population connectivity of many marine species. The degree of connectivity is often correlated with the time that larvae spend in the water column. The Antarctic notothenioid fishes develop through an unusually long pelagic larval phase often exceeding 1 year. Notothenioids thus represent a prime model system for studying the influence of prolonged larval phases on population structure in otherwise demersal species. Here, we compare the population genetic structure and demographic history of two sub‐Antarctic crocodile icefish species (Chaenocephalus aceratus and Champsocephalus gunnari) from the Scotia Arc and Bouvet Island in the Atlantic sector of the Southern Ocean to delineate the relative importance of species‐specific, oceanographic and paleoclimatic factors to gene flow. Based on 7 (C. aceratus) and 8 (C. gunnari) microsatellites, as well as two mitochondrial DNA markers (cytochrome b, D‐loop), we detect pronounced population genetic structure in both species (amova FSTs range from 0.04 to 0.53). High genetic similarities were found concordantly in the populations sampled at the Southern Scotia Arc between Elephant Island and South Orkney Islands, whereas the populations from Bouvet Island, which is located far to the east of the Scotia Arc, are substantially differentiated from those of the Scotia Arc region. Nonetheless, haplotype genealogies and Bayesian cluster analyses suggest occasional gene flow over thousands of kilometres. Higher divergences between populations of C. gunnari as compared to C. aceratus are probably caused by lower dispersal capabilities and demographic effects. Bayesian skyline plots reveal population size reductions during past glacial events in both species with an estimated onset of population expansions about 25 000 years ago.     

Decrease in stomach contents in the Antarctic minke whale (Balaenoptera bonaerensis) in the Southern Ocean

The Antarctic minke whale (Balaenoptera bonaerensis) is one of the major krill predators in Antarctic waters. A reported decline in energy storage over almost two decades indicates that food availability for the whales may also have declined recently. To test this hypothesis, catch data from 20 survey years in the Japanese Whale Research Program in the Antarctic (JARPA) and its second phase (JARPA II) (1990/91–2009/10), which covered the longitudinal sector between 35°E and 145°W south of 58°S, were used to investigate whether there was any annual trend in the stomach contents weight of Antarctic minke whales. A linear mixed-effects analysis showed a 31 % (95 % CI 12.6–45.3 %) decrease in the weight of stomach contents over the 20 years since 1990/1991. A similar pattern of decrease was found in both males and females, except in the case of females sampled at higher latitude in the Ross Sea. These results suggest a decrease in the availability of krill for Antarctic minke whales in the lower latitudinal range of the research area. The results are consistent with the decline in energy storage reported previously. The decrease in krill availability could be due to environmental changes or to an increase in the abundance of other krill-feeding predators. The latter appears somewhat more likely, given the recent rapid recovery of humpback whale. Furthermore, humpback whales are not found in the Ross Sea, where both Antarctic krill and ice krill (Euphausia crystallorophias) are available, and where no change in prey availability for Antarctic minke whales is indicated.     

Diet of the Antarctic starry skate Amblyraja georgiana (Rajidae, Chondrichthyes) at South Georgia (Southern Ocean)

Stomach contents were identified from 206 Antarctic starry skate (Amblyraja georgiana) that were collected during three groundfish surveys (September 2007, April 2008 and January 2009) at South Georgia, Southern Ocean. The diet of A. georgiana varied with skate size and between years. Preferred prey included fish (particularly for larger individuals) and Antarctic krill, Euphausia superba, as well as amphipods, polychaetes and other benthic fauna. The skate A. georgiana appears to be an opportunistic predator, and the clear presence of Antarctic krill in this demersal predator’s diet may indicate a benthic habit of this euphausiid species, which has hitherto mainly been considered as occupying a purely pelagic niche.     

Molecular analysis of Southern Ocean skates (Bathyraja) reveals a new species of Antarctic skate

Two regions of mtDNA, cytochrome b and cytochrome c oxidase subunit 1, were sequenced in nine species of Bathyraja from the Southern Ocean and New Zealand. Based on sequence divergence, the species that has been referred to as Bathyraja eatonii from the Antarctic continental shelf and slope is a species distinct from B. eatonii from the Kerguelen Plateau (the type locality) and is a new and undescribed species Bathyraja sp. (cf. eatonii). There was no sequence divergence among samples of Bathyraja sp. (dwarf) from the Ross Sea and the South Atlantic. However, for both Bathyraja sp. (cf. eatonii) and Bathyraja maccaini in the Ross Sea and the South Atlantic Ocean, the DNA sequence divergences indicate differentiation among ocean basins and within Bathyraja sp. (cf. eatonii) divergences are similar to those among recognized species of Bathyraja in the North Pacific Ocean.     

Taxonomic studies of the Antarctic icefish genus Cryodraco Dollo, 1900 (Notothenioidei: Channichthyidae)

Based on a meristic and morphometric study of 101 specimens, we recognise 2 valid species in the Antarctic channichthyid genus Cryodraco: Cryodraco antarcticus Dollo, 1900 and C. atkinsoni Regan, 1914. Although the species overlap in most meristic and morphometric characters, we have distinguished several reliable characters for diagnosis and identification. Multidimensional scaling, a nonparametric multivariate technique, clearly separates the two species on the basis of pelvic fin length, head length, number of second dorsal fin rays and origin of the lower lateral line relative to the anal fin rays. We provide a revised identification key to the species of Cryodraco. From a zoogeographical point of view, C. antarcticus has a circum-Antarctic distribution whereas C. atkinsoni is largely confined to the East Antarctic Zoogeographic Province.     

Distribution of surface zooplankton and seabirds across the Southern Ocean

Surface zooplankton and seabird densities and community composition in the Atlantic (between Cape Town and Sanae) and Pacific (between New Zealand and the Ross Sea) sectors of the Southern Ocean are described and related to oceanographic features. Samples were collected during two return voyages aboard the MV Benjamin Bowring as part of the Transglobe Expedition (1979–1981). High abundances of surface zooplankton and seabirds were consistently observed within the main frontal systems of the Southern Ocean. Generally, on a mesoscale significant correlations between surface temperature and the distribution of zooplankton or seabirds were observed. On a macroscale, the geographical positions of the zooplankton and seabird communities coincided with specific water masses. The results of this study suggest that appropriate food availability rather than water temperature is important for the determination of seabird distribution. The ecological importance of the recently described frontal zone associated with the northern boundary of the maximum winter expansion of sea ice is confirmed by biological data obtained in this study.     

Trophodynamics of Protomyctophum (Myctophidae) in the Scotia Sea (Southern Ocean)

This study investigated spatial and temporal patterns in distribution, population structure and diet of Bolin's lanternfish Protomyctophum bolini, Tenison's lanternfish Protomyctophum tenisoni and gaptooth lanternfish Protomyctophum choriodon in the Scotia Sea using data collected by midwater trawl during spring, summer and autumn. Protomyctophum bolini was the most abundant species of the genus encountered throughout the Scotia Sea with the greatest concentrations occurring around the Antarctic Polar Front (APF). This species had a life cycle of 2+ years, but spatial differences in population structure were apparent as the I‐group was absent from all regions south of the APF, suggesting that the species does not recruit in the Scotia Sea. Protomyctophum tenisoni occurred mostly in waters characteristic of the APF and was absent from the southern Scotia Sea. It had a limited size range, but there was clear size‐related sexual dimorphism with males significantly larger than females. The species had a life cycle of c. 2 years, but the I‐group (c. 1 year old, 1 November to 31 October the next year) occurred only in regions close to the APF suggesting that recruitment is restricted to these waters. A seasonal southward migration for P. choriodon is likely as the species occurred mostly to the south‐west of South Georgia in summer, but extended to the sea‐ice sectors in autumn. Protomyctophum choriodon had a life cycle of 4+ years in the Scotia Sea and the population was dominated by age classes >3 years old. Larval stages were absent during the surveys for all species. Diurnal variations in vertical distribution were apparent for all three species. Interspecific variations in diet were evident, but all species were primarily copepod feeders, with Metridia spp., Rhincalanus gigas and Calanus simillimus generally dominating their diet. Small euphausiids, principally Thysanoessa spp., were also an important component of their diets, particularly for P. choriodon which had the largest body size. The spatial and temporal variations in diet for both P. bolini and P. tenisoni were broadly consistent with underlying abundance patterns within the mesozooplankton community.     

An unusual hermaphrodite reproductive trait in the Antarctic brooding bivalve Lissarca miliaris (Philobryidae) from the Scotia Sea, Southern Ocean

The Antarctic marine environment is extreme in its low temperatures and short periods of primary productivity. Invertebrates must therefore adapt to maximise reproductive output where low temperature and limited food slow larval development. Brooding is a common reproductive trait in Antarctic marine bivalves; larval development occurs within the mantle cavity, and larvae are released as fully developed young. Lissarca miliaris is a small, short-lived, shallow-water brooding bivalve of circum-Antarctic distribution and found most abundant in the sub-Antarctic Magellan Region and islands of the Scotia Arc. Here, an unusual hermaphrodite reproductive trait is described for L. miliaris from King George Island (62°14′S, 58°38′W) and Signy Island (60°42′S, 45°36′W), Antarctica, using histological and dissection techniques. Specimens demonstrate simultaneous and sequential hermaphrodite traits; male and female gonads develop simultaneously, but the production of oocytes is reduced while testes are ripe. Functional females are more abundant in specimens above 3 mm shell length, although male reproductive tissue persists and functional males are found in all size classes. The number of previtellogenic oocytes produced by far exceeds the number of oocytes extruded and brooded, which may indicate an ancestral link to a planktotrophic past. Hermaphroditism in L. miliaris maximises reproductive efficiency in a short-lived species, in which the female’s capacity to brood its young is limited, and demonstrates a specialised adaptation to a cold stenothermal and food-limited environment prevailing in the Southern Ocean.     

Evidence of counter‐gradient growth in western pond turtles (Actinemys marmorata) across thermal gradients

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Macroscopic and histological analyses of gonads during the spawning season of Chionodraco hamatus (Pisces,Channichthyidae) off Terra Nova Bay,Ross Sea,Southern Ocean

A macroscopic and histological analysis of gonads was carried out during the spawning season of the high-Antarctic channichthyid Chionodraco hamatus in the western Ross Sea. Samples were collected between December and February during several years in the coastal waters of Terra Nova Bay. Gonad maturity stages were described for males and females according to macroscopic and histological scales. Using multi-year data, the estimated length at first spawning of females was about 35 cm TL, very similar to that obtained indirectly for males. Similar to many other high-Antarctic fish, C. hamatus is a summer spawner. The greater part of the stock was indeed in spawning condition between December and February, although a large proportion of females large enough to spawn probably did not spawn in that season. The present data confirm that C. hamatus, as is typical for Antarctic fish, probably spawns a single batch of oocytes once a year. In addition, vitellogenesis is a slow process that extends over at least 1 year. Discrepancies between the macroscopic and histological appearance of gonads were found. These were associated mainly with spent and resting females (maturity stages 5 and 2, respectively). This study demonstrates the importance of histological analysis of gonads in order to confirm the results of the macroscopic analyses routinely carried out in studies of reproductive biology. This is of particular importance in determining size at maturity and spawning stock biomass, for assessment purposes.     

Distribution and ecology of <Emphasis Type="Italic">Chaenocephalus aceratus</Emphasis> (Channichthyidae) around South Georgia and Shag Rocks (Southern Ocean)

Chaenocephalus aceratus (Family Channicthyidae) is one of the dominant species of demersal fish living on the South Georgia shelf where it is caught in low numbers as by-catch in the mackerel icefish and Antarctic krill commercial fisheries. Data collected during 14 demersal fish surveys, from 1986 to 2006, are analysed to investigate biomass, distribution, growth and diet. Biomass estimates from a swept area method ranged from 4,462 to 28,740 tonnes on the South Georgia and Shag Rock shelves although few fish were caught at Shag Rocks. Analysis of length frequency data indicated that growth was fast in the first five years with males and females attaining lengths at first spawning of 440 mm TL and 520 mm TL. The diet was comprised of fish and crustaceans, with an ontogenetic shift in diet from Euphausia superba and mysids to benthic fish and decapods observed to begin at 250 mm TL. In larger fish (>500 mm TL) the diet was dominated by fish. C. aceratus diet is sufficiently different from the other species of channichthyids around South Georgia to suggest that these species have undergone resource partitioning.