Joseph T. Eastman

Antarctic fish biology: evolution in a unique environment

The Antarctic Environment. Past and Present: Physical and Biological Characteristics of the Antarctic Marine Environment. Geologic and Climatic History of Antarctica. The Fossil Fish Faunas. The Modern Fauna: Biology and Relationships: The Modern Fauna: Zoogeography. The Modern Fauna: Taxonomic Composition. The Modern Fauna: Notothenioids. Systematic Relationships of Notothenioids. Zoogeographic Origins and Evolution of the Modern Fauna. Organ System Adaptation in Notothenioids: Biochemistry and Metabolism. Evolutionary Modification of Buoyancy. Anti-Freeze Glycopeptides. Muscular System and Swimming. Cardiovascular and Respiratory Systems. Nervous System and Special Senses. Final Remarks and Outlook. References. Index.

The nature of the diversity of Antarctic fishes

The species diversity of the Antarctic fish fauna changed notably during the ≈40 million years from the Eocene to the present. A taxonomically restricted and endemic modern fauna succeeded a taxonomically diverse and cosmopolitan Eocene fauna. Although the Southern Ocean is 10% of the world’s ocean, its current fish fauna consists of only 322 species, small considering the global diversity of ≈25,000–28,000 species. The fauna is “reasonably well-known” from a taxonomic perspective. This intermediate designation between “poorly known” and “well-known” indicates that new species are regularly being described. A conservative estimate of the number of undescribed species is ≈30–60; many of these may be liparids. On the Antarctic continental shelf and upper slope the fauna includes 222 species from 19 families of benthic fishes. The most speciose taxa are notothenioids, liparids and zoarcids, accounting for 88% of species diversity. Endemism for Antarctic species is also, coincidentally, 88%, at least threefold higher than in faunas from other isolated marine localities. Eight notothenioid families, including five that are primarily Antarctic, encompass a total of 44 genera and 129 species, 101 Antarctic and 28 non-Antarctic. The 101 Antarctic species make up 45% of the benthic species diversity in the Antarctic region. However, at the highest latitudes, notothenioids contribute 77% of the species diversity, 92% of the abundance and 91% of the biomass. Although species diversity is low compared to other shelf habitats, the nature of the adaptive radiation in organismal diversity among notothenioids is noteworthy in the marine realm. In some notothenioid clades phyletic diversification was accompanied by considerable morphological and ecological diversification. The exemplar is the benthic family Nototheniidae that underwent a habitat or depth related diversification centred on the alteration of buoyancy. They occupy an array of pelagic and benthopelagic habitats at various depths on the shelf and upper slope. Diversification in buoyancy is the hallmark of the nototheniid radiation and, in the absence of swim bladders, was accomplished by a combination of reduced skeletal mineralisation and lipid deposition. Although neutral buoyancy is found in only five species of nototheniids some, like Pleuragramma antarcticum, are abundant and ecologically important. Much work remains to be done in order to frame and to use phylogenetically based statistical methods to test hypotheses relating to the key features of the notothenioid radiation. To reach this analytical phase more completely resolved cladograms that include phyletically basal and non-Antarctic species are essential.

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.

Buoyancy Studies of Notothenioid Fishes in McMurdo Sound, Antarctica

composition in Crocodylus porosus caught along a salinity gradient. J. Comp. Physiol. 144:261-270. , L. E. TAPLIN, P. HARLOW AND J. WRIGHT. 1980. Survival and growth of hatchling Crocodylus porosus in saltwater without access to fresh drinking water. Oecologia 47:264-266. JOHNSON, I. M. 1969. Salt and water balance, and nitrogen excretion of the red-tailed hawk, Buteojamaicensis. Unpubl. PhD thesis in Zoology, Univ. of Montana.

Pleuragramma antarcticum (Pisces, Nototheniidae) as food for other fishes in McMurdo Sound, Antarctica

SummaryNine spcies of notothenioid fishes were captured near the southern limit of their range in ice covered McMurdo Sound, Antarctica. Stomach contents were examined using an occurrence method. Fishes were present in the diets of 8 of 9 species;Dissostichus mawsoni andGymnodraco acuticeps were predominantly piscivorous.Pleuragramma antarcticum was the most common prey fish consumed, being present in stomachs of 4 of 8 species.Pleuragramma was also partially piscivorous (22%) as well as cannibalistic (13%). As evidenced by their presence in the stomach contents of other fishes, all life history stages from 20 mm SL postlarvae to 160 mm SL adultPleuragramma were represented under the ice of the Sound.Pleuragramma was also a major food item for Weddell seals, birds and possibly invertebrates. As a widely distributed species in the pelagic zone,Pleuragramma may be an ecological substitute for euphausiids in the food web of the Sound.

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.

Antarctic notothenioid fishes as subjects for research in evolutionary biology

Antarctica is a continental island and the waters of its shelf and upper slope are an insular evolutionary site. The shelf waters resemble a closed basin in the Southern Ocean, separated from other continents by distance, current patterns and subzero temperatures. The benthic fish fauna of the shelf and upper slope of the Antarctic Region includes 213 species with higher taxonomic diversity confined to 18 families. Ninety-six notothenioids, 67 liparids and 23 zoarcids comprise 45%, 32% and 11% of the fauna, a combined total of 88%. In high latitude (71–78°S) shelf areas notothenioids dominate abundance and biomass at levels of 90–95%. Notothenioids are also morphologically and ecologically diverse. Although they lack a swim bladder, the hallmark of the notothenioid radiation has been repeated diversification into water column habitats. There are pelagic, semipelagic, cryopelagic and epibenthic species. Notothenioids exhibit the disproportionate speciosity and high endemism characteristic of fish species flock. Antifreeze glycopeptides originating from a transformed trypsinogen gene are a key innovation. It is not known when the modern Antarctic shelf fauna assumed its current taxonomic composition. A late Eocene fossil fauna was taxonomically diverse and cosmopolitan. There was a subsequent faunal replacement with little carryover of families into the modern fauna. Basal notothenioid clades probably diverged in Gondwanan shelf locations during the early Tertiary. Dates inferred from molecular sequences suggest that phyletically derived Antarctic clades arose 15–5 m.y.a.

Lipid sacs as a buoyancy adaptation in an Antarctic fish

THE Notothenioidei, the dominant perciform suborder of Antarctic fishes, is a predominantly benthic group of about 75 species1. They lack a swim bladder, a feature consistent with their mode of life on the bottom of the sea1. Therefore few of them have been able to exploit the enormous biomass of planktonic crustaceans (krill) indigenous to the mid-waters of the Antarctic Ocean2,3. One notable exception, however, is the nototheniid Pleuragramma antarcticum Boulenger which has invaded this highly productive habitat. Unlike other members of this family, Pleuragramma spends its life swimming in the water2,4, at times beneath a cover of sea ice. Although Pleuragramma lacks a swim bladder, it has been observed to remain nearly motionless in the water when placed in an aquarium. Furthermore, its slow swimming speed and general body morphology (Fig. 1) appear to preclude the use of forward motion and associated hydrodynamic lift as a mechanism for maintaining position in the water column. In—1.8 °C seawater, specimens of Pleuragramma weighed between 0.5 and 1 % of their weight in air indicating they were almost neutrally buoyant. We report here that this reduction in density results from the accumulation of lipid in intermuscular and subcutaneous sacs, and from a reduction in skeletal ossification.

The fish fauna of the Ross Sea, Antarctica

The RV Nathaniel B. Palmer was used for bottom trawling at depths of 100–1200 m during two recent cruises in the south-western Ross Sea. Although only 10 of 20 trawls were completely successful, a diverse collection of 979 specimens was obtained representing 47 species (36 notothenioids and 11 nonnotothenioids) and eight families. The collection included four new species, a new colour morph of a known species and eight rare species. The collection also established four new locality records, three second occurrences, three most southerly records and eleven new depth records for fish in the Ross Sea. Good taxonomic coverage for some groups was indicated by collection of all four species of Artedidraco , nine of ten bathydraconids and seven of eight channichthyids occurring in East Antarctica. The most abundant species were Trematomus scotti (29.7%), Bathydraco marri (10.4%), Trematomus eulepidotus (8.7%) and Dolloidraco longedorsalis (6.1%). Fish biomass was determined at two stations. The fish fauna of the Ross Sea south of the 1000-m isobath includes at least 80 species – 54 notothenioids and 26 non-notothenioids, approximately the same number as the Weddell Sea. Species diversity ( H ′ = 1.88) was higher than both the Weddell Sea and boreal regions. This collection indicates that, even in relatively shallow water, knowledge of specific and intraspecific diversity in the Ross Sea fauna is incomplete.

A Comparison of Adaptive Radiations of Antarctic Fish with those of NonAntarctic Fish

Antarctic biologists frequently emphasize the differences between the modern Antarctic environment and its fauna, and aquatic habitats and faunas elsewhere in the world. While it is valid to portray Antarctica as remote and its fauna as endemic and cold adapted, this approach tends to obscure broad scale similarities between Antarctic and non-Antarctic faunas. For example, the Antarctic fish fauna shares an evolutionary response to its habitat with fish in some tropical, temperate and boreal lakes. In this review we compare some well studied lacustrine radiations of fish with the two radiations of marine fish in the Antarctic Region of the Southern Ocean, notothenioids and liparids. We shall first make the case that, unlike other marine habitats, the Antarctic Region fulfills most of the essential parameters of lakes containing radiations of fish and that this large component of the world ocean is equivalent to a closed basin. Therefore in spite of its vastness, the Antarctic Region provides a comparable opportunity for studying evolutionary biology within a confined area. It is likely that notothenioids, and possibly liparids, are the first known examples of species flocks or radiations of marine fish. Thus the high Antarctic shelf and upper slope is an insular evolutionary site, with endemic faunas equally as interesting, but less well known, as those in ancient lakes throughout the world.