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.     

Ultrastructural observations and pH-measurements on red and white muscle from Antarctic fish

Summary Red and white muscle in the two Antarctic notothenioid fishes Dissostichus mawsoni and Pagothenia borchgrevinki show a rate of postmortem fall of 0.2 pH units per hour, which is close to the rate reported for mammalian muscle at 30°C, but the plateau value is reached several hours earlier in the Antarctic fish, indicating significantly lower stores of initial glycogen. A few particles, most likely representing glycogen, were seen in P. borchgrevinki white muscle and D. mawsoni red muscle, whereas predictably fewer glycogen still was evident in D. mawsoni white muscle. When large numbers of mitochondria and lipid stores were encountered in combination with a small amount of glycogen, we concluded that aerobic metabolism is dominant and that the two species examined would not use white trunk muscle for sustained or slow swimming. Rapid contractions of white trunk muscle as in prey capture or predator evasion are more likely.     

Underwater video observation of the Antarctic toothfish Dissostichus mawsoni (Perciformes: Nototheniidae) in the Ross Sea, Antarctica

A towed benthic camera system captured images of a ca. 66-cm-long Antarctic toothfish partially under a boulder at 76°30'S, 174°59'E (depth 454 m) in the southern Ross Sea. This is noteworthy because, excluding McMurdo Sound, there are only two published records for this species in the Ross Sea and none in an offshore locality. Adult Dissostichus mawsoni are neutrally buoyant and live and feed in the lower reaches of the water column. Benthic perching is unexpected, suggesting that this subadult is not neutrally buoyant.     

Buoyancy of sub-Antarctic notothenioids including the sister lineage of all other notothenioids (Bovichtidae)

The radiation of notothenioid fishes (Perciformes) in Antarctic waters was likely the result of an absence of competition in the isolated Antarctic waters and key traits such as the production of antifreeze glycoprotein and buoyancy modifications. Although notothenioids lack a swim bladder, the buoyancy of Antarctic species, ranging from neutrally buoyant to relatively heavy, corresponds to diverse life styles. The buoyancy of South American notothenioids has not been studied. Static buoyancy was measured in adult notothenioids (n = 263, from six species of the sub-order Notothenioidei, families Bovichtidae, Eleginopidae, Nototheniidae, and Harpagiferidae) from the Beagle Channel. Measurements were expressed as percentage buoyancy (%B). Buoyancy ranged from 3.88 to 6.96% (median, 4.0–6.7%), and therefore, all species could be considered benthic consistent with previous studies that found that neutral buoyancy in notothenioids is rare. Harpagifer bispinis, Patagonotothen cornucola, and Cottoperca gobio were significantly less buoyant than Paranotothenia magellanica. The buoyancy values of most species were concordant with known habitat preferences. These data, especially the data of C. gobio (sister lineage of all other nototehnioids) and E. maclovinus (sister lineage of the Antarctic clade of notothenioids), could be useful for understanding the diversification of this feature during the notothenioid radiation.     

Buoyancy Range, Gas Bladder Volume, and Lipid Content of Adult Bloater, Coregonus hoyi Gill, in the Laurentian Great Lakes

We analyzed buoyancy characteristics (buoyancy range, gas bladder volume, and lipid content) of adult bloater, Coregonus hoyi Gill, in the Laurentian Great Lakes. Buoyancy was measured directly in individual bloater and compared with the hydrostatic pressures at the depths of capture. The results of the buoyancy comparisons suggest that C. hoyi has a buoyancy range comparable to the 'free vertical range' of movement that has been described for other fishes. The buoyancy range of bloater does not support the argument that they undergo diel vertical migrations, as suggested in earlier studies. Rather, the buoyancy range for bloater reflects the depths of neutral buoyancy and the distance above these depths at which they can maintain vertical position in the water column. The available data suggest that adult bloater are neutrally buoyant near the lake bottom, and C. hoyi with 50% positive buoyancy are at the top of their depth range. Large bloater have relatively small gas bladder volumes and a high lipid content. Based on the observed vertical distribution of large and small C. hoyi and our results, we deduced that large fish are more adept than small fish at regulating their buoyancy for prolonged stays at higher hydrostatic pressures. Lipid content for bloater was not significantly different with respect to sex or origin (wild vs. captive-raised).     

Ontogenetic shift in buoyancy and habitat in the Antarctic toothfish, <Emphasis Type="Italic">Dissostichus mawsoni</Emphasis> (Perciformes: Nototheniidae)

Buoyancy measurements and depth of capture were taken on 70 individuals of Dissostichus mawsoni collected from the Southern Scotia Arc and McMurdo Sound, Antarctica, to examine the effect of age on buoyancy and habitat use. Standard lengths (SL) ranged from 10.4 to 138.0 cm. Juveniles were not buoyant (heavy in water), whereas adults were neutrally buoyant. The slope of the relationship between buoyancy and SL was significantly negative for juveniles (individuals less than 81 cm SL), but there was no significant relationship for adults (individuals greater than 81 cm SL). These results demonstrate an ontogenetic shift in buoyancy. For juveniles, depth of capture and SL had a significantly positive relationship. As individuals reach adulthood they achieve neutral buoyancy and appear to use deeper water habitats. This interpretation is supported by a significant positive correlation between buoyancy and depth of capture for juveniles. Changes in buoyancy with maturation of juveniles may also be associated with a shift in habitat use. Juveniles appear to exploit benthic habitats, whereas adults use the entire water column over deeper water. Given the differences in prey species available in these habitats and based on our results, we predict that diets of juveniles and adults should differ significantly. We also hypothesize that accumulation of lipid deposits from the diet during maturation of juveniles may account for the ontogenetic shift in buoyancy and allow neutral buoyancy to be achieved in adulthood.     

Measurements of buoyancy for some Antarctic notothenioid fishes from the South Shetland Islands

Buoyancy was measured for 258 specimens representing 13 species of adult and sub-adult nototheniids, bathydraconids, and channichthyids from the South Shetland Islands. Measurements were expressed as percentage buoyancy (%B)=W_water/W_air᎒². There were no neutrally buoyant species and mean values for %B were 3.07-6.11%, with channichthyids at the low end and benthic nototheniids and bathydraconids at the high end. All species showed an ontogenetic decrease in %B with increasing body weight. With the exception of Champsocephalus gunnari, there was no sexual dimorphism in %B within this sample. With some exceptions, values for %B were consistent with life-history information. Sub-adult Dissostichus mawsoni were not neutrally buoyant, as are large adults. Notothenia rossii had a significantly lower %B than closely related N. coriiceps. Benthic Gobionotothen gibberifrons had a lower %B than semipelagic Lepidonotothen larseni. Although they exhibit some diversification in life history, the four channichthyids in the sample were similar in %B. Neutral buoyancy is rare in notothenioids and may be confined to a single nototheniid clade.     

Observations of neutral buoyancy in diapausing copepods Calanoides acutus during Antarctic winter

The herbivorous Antarctic copepod Calanoides acutus overwinters inactively in a resting stage (diapause) at depths below 500 m. It is assumed that during diapause C. acutus is neutrally buoyant in order to retain energy reserves otherwise depleted by swimming activities. However, so far, no experimental observations on its buoyancy have been reported and our knowledge of buoyancy regulation mechanisms is incomplete. In the present study, species-specific differences in buoyancy were assessed visually. Observations were made of specimens from the diapausing cohort of C. acutus and compared to another herbivorous copepod Calanus propinquus, which overwinters actively feeding in the upper water layers. Freshly caught copepods were anaesthetized in a 3-amino-benzoic acid ethyl ester (MS222) in seawater solution in order to exclude the influence of swimming movements on buoyancy control. It was shown that C. propinquus was negatively buoyant, whereas diapausing C. acutus remained neutrally buoyant. This is the first record that neutral buoyancy in diapausing copepods is maintained by the biochemical body composition without the additional need of swimming movements.     

Hepatic ultrastructural specialization in Antarctic fishes

Summary Compared with those of other vertebrate animals, the livers of Antarctic fishes have a unique type of perisinusoidal (Ito) cell. These cells were studied in 9 species with emphasis on Dissostichus mawsoni. Perisinusoidal cells are found in large numbers throughout the liver, have long cytoplasmic arms and, in Dissostichus, contain numerous lipid droplets. The extensive rough endoplasmic reticulum and prominent nucleolus are ultrastructural characteristics indicating that these cells are engaged in protein synthesis. An evolutionary specialization, perisinusoidal cells may be partially responsible for the elevated levels of protein synthesis characteristic of fishes in the Antarctic marine environment.     

Unexpected Positive Buoyancy in Deep Sea Sharks,Hexanchus griseus,and a Echinorhinus cookei

We do not expect non air-breathing aquatic animals to exhibit positive buoyancy. Sharks, for example, rely on oil-filled livers instead of gas-filled swim bladders to increase their buoyancy, but are nonetheless ubiquitously regarded as either negatively or neutrally buoyant. Deep-sea sharks have particularly large, oil-filled livers, and are believed to be neutrally buoyant in their natural habitat, but this has never been confirmed. To empirically determine the buoyancy status of two species of deep-sea sharks (bluntnose sixgill sharks, Hexanchus griseus, and a prickly shark, Echinorhinus cookei) in their natural habitat, we used accelerometer-magnetometer data loggers to measure their swimming performance. Both species of deep-sea sharks showed similar diel vertical migrations: they swam at depths of 200–300 m at night and deeper than 500 m during the day. Ambient water temperature was around 15°C at 200–300 m but below 7°C at depths greater than 500 m. During vertical movements, all deep-sea sharks showed higher swimming efforts during descent than ascent to maintain a given swimming speed, and were able to glide uphill for extended periods (several minutes), indicating that these deep-sea sharks are in fact positively buoyant in their natural habitats. This positive buoyancy may adaptive for stealthy hunting (i.e. upward gliding to surprise prey from underneath) or may facilitate evening upward migrations when muscle temperatures are coolest, and swimming most sluggish, after spending the day in deep, cold water. Positive buoyancy could potentially be widespread in fish conducting daily vertical migration in deep-sea habitats.     

Proximate composition and energy density of nototheniid and myctophid fish in McMurdo Sound and the Ross Sea,Antarctica

Nototheniid and myctophid fish are primary prey for marine piscivores, yet little is known about their nutritional value. In this study, we characterized the proximate composition [PC: water, fat (neutral lipids), crude protein (CP) and ash] and energy density (ED; kJ g⁻¹) of fifteen fish species from McMurdo Sound and the Ross Sea, Antarctica. We assayed the entire fish for all species except for the large Antarctic toothfish, Dissostichus mawsoni (muscle tissue only). On a wet mass basis (WM), fish were variable in composition: moisture content ranged from 64.9 to 87.3% WM, fat from 0.5 to 17.4% WM, CP from 7.7 to 16.7% WM, ash from 11.2 to 21.0% FFDM (fat-free dry mass), and ED from 2.9 to 10.3 kJ g⁻¹. Myctophids and pelagic nototheniids such as Pleuragramma antarcticum and D. mawsoni were high in fat content (7–17% WM), while a bathylagid and benthic nototheniids including most Trematomus spp. and Lepidonotothen squamifrons were low in fat (0.5–4% WM). The epibenthic Trematomus species (T. eulepidotus and T. lepidorhinus) were intermediate. Energy density tracked fat content, with highest values in myctophids and pelagic nototheniids. The variation in nutrient and energy density confirms that prey composition must be taken into account when modelling energy and nutrient fluxes within the Antarctic ecosystem. Further analyses of prey collected over a number of different locations and seasons are needed in order to determine how the nutritional value of certain species might affect annual or decadal variation in reproductive success or population size of top predators.     

Occurrence of Pseudoterranova decipiens (Nematoda) in fish from the Southeastern Weddell Sea (Antarctic)

Eleven fish species from the Weddell Sea (Antarctic) were examined for infestation with anisakid nematodes. Two species of the genus Contracaecum and the sealworm Pseudoterranova decipiens were isolated from the liver and the body cavity of fish affected. Only two specimens of P. decipiens (1.4%) partly invaded the belly flaps. The following fish species were infested by P. decipiens at the given prevalences: Cygnodraco mawsoni (74.4%), Trematomus scotti (23.2%), Pagetopsis maculatus (10.0%), Cryodraco antarcticus (7.1%), Trematomus lepidorhinus (3.0%), and Dolloidraco longedorsalis (2.7%). All of these, except Trematomus scotti, are new host records. Chaenodraco wilsoni, Chionodraco myersi, Gerlachea australis, Racovitzia glacialis and T. eulepidotus were not infested. The reasons for low prevalence and intensity of infestation are seen in the difficulties of P. decipiens in completing its benthic life cycle in the Weddell Sea environment, in the absence of shallow coastal waters due to the floating shelf-ice. Cygnodraco mawsoni is a crucial intermediate host, without which completion of the parasite life cycle might not be possible. In order to clarify the taxonomical position of Antarctic Pseudoterranova, morphological comparisons with specimens of P. decipiens from the German and Norwegian coast were made using scanning electron microscopy. Results revealed no differences; hence, all specimens studied belong to the same species P. decipiens.     

The two giant sister species of the Southern Ocean, <Emphasis Type="Italic">Dissostichus eleginoides</Emphasis> and <Emphasis Type="Italic">Dissostichus mawsoni</Emphasis>, differ in karyotype and chromosomal pattern of ribosomal RNA genes

The two giant notothenioid species, the Patagonian toothfish Dissostichus eleginoides and the Antarctic toothfish D. mawsoni, are important components of the Antarctic ichthyofauna and heavily exploited commercially. They have similar appearance and size, both are piscivorous and bentho-pelagic, but differ in their geographic distribution and absence/presence of the antifreeze trait. We karyotyped these two sister species by analyzing specimens collected from multiple Antarctic and sub-Antarctic sites. Both species have a diploid number of 48, but differ in karyotypic formula, (2m + 2sm + 44a) for D. eleginoides and (2m + 4sm + 42a) for D. mawsoni, due to an extra pair of submetacentric chromosomes in the latter. Chromosomal fluorescence in situ hybridization with rDNA probes revealed unexpected species-specific organization of rRNA genes; D. mawsoni possesses two rDNA loci (versus one locus in D. eleginoides), with the second locus mapping to its additional submetacentric chromosome. The additional rRNA genes in D. mawsoni may be a cold-adaptive compensatory mechanism for growth and development of this large species in freezing seawater.     

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.     

Thermostability of haemoglobins from Antarctic fish

Summary Proteins from Antarctic fish are less stable at high temperatures than those from fish from lower latitudes. Investigations into the thermostability of haemoglobins from a range of Antarctic teleosts have been carried out for comparison with data from temperate species. Haemoglobin concentrations following periods of heating at 50°C were analysed spectrophotometrically and the time taken for 50% denaturation (t_50%) determined. The effects of pH and salt concentrations were also examined. With the exception of that of Rhigophila dearborni, the haemoglobins were found to be relatively unstable with t_50% values ranging from 7.7 to 29.9 min at pH 7. All haemoglobins became less stable on addition of KCl but the effect of pH was variable. Freezing had no effect on the stability of haemoglobin from Dissostichus mawsoni. The thermostability of haemoglobin from a temperate nototheniid, Notothenia angustata, was within the range displayed by its antarctic relatives and it would seem that in general the differences between genera are as great as those between Antarctic and temperate species as a whole.     

Confirmation of neutral buoyancy in <Emphasis Type="Italic">Aethotaxis mitopteryx</Emphasis> DeWitt (Notothenioidei: Nototheniidae)

Aethotaxis mitopteryx is a nototheniid species with a circum-Antarctic distribution in the Southern Ocean. We present new locality records, buoyancy measurements, and morphometric data on five A. mitopteryx specimens collected from the Bransfield Strait. Our analyses demonstrate that A. mitopteryx is neutrally buoyant. This result lends additional support to the hypothesis that neutral buoyancy has a single evolutionary origin in Notothenioidei. Food items in these specimens consisted entirely of krill (Euphausia sp.), and all specimens were sexually immature. We present morphometric data from these five specimens and compare to the holotype specimen, which is the only A. mitopteryx specimen collected in the Ross Sea.     

Exercise challenge in Antarctic fishes: do haematology and muscle metabolite levels limit swimming performance?

 Burst swimming increased haematocrit (partly from erythrocyte swelling) in the cryopelagic nototheniid Pagothenia borchgrevinki, but not in the benthic species Trematomus bernacchii. Erythrocyte nucleotides, which regulate haemoglobin-oxygen affinity, remained constant. Plasma cortisol was high in all captive fish and raised questions about the effects of chronic stress on metabolic measurements from Antarctic fish held in captivity. Glycogen was reduced in white trunk muscle, but not in the red pectoral muscle of exercised P. borchgrevinki. Red pectoral muscle glycogen was nearly 3 times higher in T. bernacchii than in P. borchgrevinki but post-exercise lactate rises were modest. Lactate values were, however, higher in exercised P. borchgrevinki white muscle than in T. bernacchii, and correlated with muscle-buffering capacity. Resting adenylate energy charge (AEC) was unexpectedly low in both species and reduced with exercise only for white muscle in P. borchgrevinki. While it appears that the capacity for burst swimming is limited by endogenous metabolic fuels, confirmation of low resting values of ATP and AEC in Antarctic fishes requires the development of methods that maintain high phosphocreatine levels in the muscle. Received: 12 February 1996/Accepted:1 May 1996     

Effect of dietary lipid level on fatty acid beta-oxidation and lipid composition in various tissues of haddock,Melanogrammus aeglefinus L

Haddock (Melanogrammus aeglefinus) is a gadoid fish species that deposits dietary lipid mainly in the liver. The fatty acid (FA) beta-oxidation activity of various tissues was evaluated in juvenile haddock fed graded levels of lipid. The catabolism of a radiolabelled FA, [1-(14)C]palmitoyl-CoA, through peroxisomal and mitochondrial beta-oxidation was determined in the liver, red and white muscle of juvenile haddock fed 12, 18 and 24% lipid in the diet. There was no significant increase in the mitochondrial or peroxisomal beta-oxidation activity in the tissues tested as the dietary lipid level increased from 12 to 24%. Peroxisomes accounted for 100% of the beta-oxidation observed in the liver, whereas mitochondrial beta-oxidation dominated in the red (91%) and white muscle (97%) of juvenile haddock. Of the tissues tested, red muscle possessed the highest specific activity for beta-oxidation expressed on a per mg protein or per g wet weight basis. However, white muscle, which forms over 50% of the body mass in gadoid fish was the most important tissue in juvenile haddock for overall FA catabolism. The total lipid and FA composition of these tissues were also determined. This study confirmed that the liver was the major lipid storage organ in haddock. The hepatosomatic index (HSI; 10.0-15.2%) and lipid (73.8-79.3% wet wt.) in the liver increased significantly as dietary lipid was increased from 12 to 24% lipid. There was no significant increase in the lipid composition of the white muscle (0.8% wet wt.), red muscle (1.9% wet wt.) or heart (2.5% wet wt.).     

The lipid compositions of high-Antarctic notothenioid fish species with different life strategies

Lipid and fatty acid compositions of five notothenioid fishes from the Antarctic Weddell and Lazarev Seas were investigated in detail with regard to their different modes of life. The pelagic Aethotaxis mitopteryx was the lipid-richest species (mean of 61.4% of dry mass, DM) followed by Pleuragramma antarcticum (37.7%DM). The benthopelagic Trematomus lepidorhinus had an intermediate lipid content of 23.2%DM. The benthic Bathydraco marri (20.8%DM) and Dolloidraco longedorsalis (14.5%DM) belonged to the lipid-poorer species. Triacylglycerols were the major lipid class in all species. Important fatty acids were 16:0, 16:1(n-7), 18:1(n-9), 18:1(n-7), 20:5(n-3) and 22:6(n-3). The enhanced proportions of the long-chain monounsaturated fatty acids, 20:1 and 22:1, in the lipid-rich pelagic fishes clearly reflected the ingestion of the two copepod species, Calanoides acutus and Calanus propinquus, which are the only known Antarctic zooplankters rich in these fatty acids. Although wax esters are the major storage lipid in many prey species, they were absent in all notothenioid fishes studied. Thus, wax esters ingested with prey are probably converted to triacylglycerols via fatty acids or metabolised by the fishes. The enhanced lipid accumulation with increasingly pelagic lifestyle has energetic advantages, especially with regard to improved buoyancy. It is still unknown to what extent these lipids are utilised as energy reserves, since it has been suggested that not only the benthic but also the pelagic Antarctic fishes are rather sluggish, with a low scope for activity and hence low metabolic requirements. Accepted: 14 May 2000     

Buoyancy and its constraints on the underwater foraging behaviour of Reed Cormorants Phalacrocorax africanus and Darters Anhinga melanogaster

The effects of changing buoyancy on the diving and feeding behaviour of Reed Cormorants Phalacrocorax africanus and Darters Anhinga melanogaster was investigated at Lake Kariba, Zimbabwe. A qualitative model of the energetic constraints caused by buoyancy changes on the diving behaviour of these two birds is presented and the predictions from the model are tested. The buoyancy of both species declined exponentially at different rates with water depth. Reed Cormorants were neutrally buoyant at 5–6 m while Darters were neutrally buoyant at 2–4 m depth. Buoyancy changes affect underwater swimming speed, which for Reed Cormorants is twice as fast on the bottom than when commuting, and for the Darter is significantly slower when diving than at any other time. Cormorants feeding in water deeper then 6 m spent less time on the bottom and fed less successfully than those birds feeding in shallower water. This is because their bottom times were significantly reduced as a result of the energetic constraints caused by changes in their buoyancy.