Introduction

My field and laboratory work deals with a group of Antarctic teleost fishes called notothenioids, the dominant and most diverse fish group in the shelf and upper slope waters of Southern Ocean.  My objectives are to gain insight into the evolution and diversification of this group, and to understand the role of notothenioids in the Antarctic marine ecosystem.  I study the biology of these fishes in a historical and phylogenetic context.  Like much evolutionary research, this work is frequently retrospective, investigating the modern results of historical processes.  I am attempting to decipher the results of a series of evolutionary events that have proceeded for 40–50 million years under the unusual conditions found in Antarctic waters.  I am interested in a series of questions pertaining to the nature of Antarctic fish diversity.  Why did the fish fauna evolve the way it did?  Why is the modern fauna unlike the preceding fossil faunas as well as the shelf faunas of other southern continents?  Why do notothenioids contribute so heavily to Antarctic fish diversity at the organismal and level?  When did the fauna become "modern" in taxonomic composition?  How did neutrally buoyant fish evolve from ancestors who were heavy bottom dwellers?  What morphological and ecological changes accompanied the notothenioid radiation?  Is novel morphology required for notothenioids to live in subzero waters?  Are examples of species flocks contained within the notothenioids?  Obviously, some of these questions are unanswerable or will have no clear answers.  The sections below provide some background information.

Antarctica and the Southern Ocean

Antarctica is a continental-sized island, twice the size of Australia, with the dominant fauna inhabiting the water rather than the ice-covered landmass.  The sea is the largest living space on earth and the Southern Ocean surrounding Antarctica is 10% of the world's ocean.  Antarctica and its fish fauna are commanding increased attention in a world attuned to loss of biological diversity, depletion of marine fisheries and the encroachment of human activities into isolated and incompletely studied ecosystems.  Unfortunately, Antarctica is no longer pristine and unmarred by human activities.  As detailed below, the popular gourmet delicacy marketed as “Chilean sea bass” is actually two heavily exploited notothenioid species.

Antarctica as an evolutionary site

The waters of the high latitude Antarctic shelf—exemplified by the Ross Sea—contain spectacular radiations of large marine animals that have not yet been decimated as is the case elsewhere in the world.  These isolated subzero waters are a fascinating but underappreciated evolutionary locale—a cold evolutionary hotspot (Eastman 1993, 2005).  Here radiations of vertebrates include four species of lobodontine seals (Deméré et al. 2003; Fyler et al. 2005) and three recently diverged species of killer whales including one that preys on minke whales, another on seals, and a smaller form that inhabits dense pack ice and eats primarily fish (LeDuc et al. 2008).  Although not a radiation, there is an enormous biomass of the two species of high Antarctic penguins, the Emperor and Adélie.  Some lineages of invertebrates have also radiated including bryozoans, pycnogonids, echinoderms, amphipods and isopods (Brandt 2000; Brandt et al. 2007).  I study the radiation of notothenioid fishes that includes species ranging from a small herring-like fish to a large 100+ kg predator that is ecologically equivalent to sharks, a group absent from high latitude waters.

Until recently most Antarctic biological research had focused on adaptations to the “extreme” environment rather than on macroevolutionary similarities between the Antarctic fauna and faunas in other isolated habitats such as islands and ancient rift lakes.  Unlike other large marine ecosystems, the waters of the continental shelf around Antarctica resemble a closed basin, isolated from other areas in the Southern Hemisphere by distance, current patterns, deep bathymetry and subzero water temperatures.  The attention of evolutionary biologists is drawn to these isolated habitats because of the unusual faunas that tend to appeared there.  Thus research on Antarctic fishes provides insight into macroevolutionary processes and events in the marine realm where they are not as well known as in freshwater and terrestrial habitats.

Trematomus nicolai, a typical benthic notothenioid fish of the family Nototheniidae.

The emergence of the modern Antarctic fish fauna

Over the past 40–50 million years there has been a nearly complete replacement of the fish fauna of Antarctica.  A diverse, cosmopolitan, temperate to cold temperate Eocene fauna was succeeded by the highly endemic, cold adapted modern fauna. The modern fauna is dominated by the 100+ species of notothenioids that evolved in situ.  Notothenioids are monophyletic group of eight families and about 130 species of teleost fishes confined to the Southern Ocean around Antarctica, its peripheral islands, and the southern extremities of South America, Australia and New Zealand.  As can be seen from the cladogrm below, the phyletically basal notothenioid families have a non-Antarctic distribution and have experienced little phyletic diversification compared to the Antarctic families.

There are also, however, important contributions to fish biodiversity from the Zoarcidae (eelpouts) and Liparidae (snailfishes), two families of North Pacific origin that have also radiated in the Antarctic.  They are not ecologically and morphologically diverse compared to notothenioids but, with the recent discovery of many new species, especially of liparids, they are certainly phyletically diverse.  Their role in the ecosystem is unknown.  Although notothenioids and zoarcids have traditionally been considered perciforms and liparids scorpaeniforms, several recent molecular phylogenetic studies have cast doubt on these relationships and have suggested major taxonomic realignments (Smith and Wheeler, 2004; Smith and Craig, 2007; Li et al., 2009).

Filling ecological niches on the Antarctic shelf

Why are notothenioids the dominant fish group on the Antarctic shelf?  This is probably the result of contingency event—they just happened to be in the right place at the right time.  Tectonic, oceanographic and climatic events associated with the breakup of Gondwana isolated Antarctica, lowered the water temperature and changed the trophic structure of the ecosystem.  The Late Eocene and post Eocene faunas declined and largely disappeared.  With little competition from other fish groups, the notothenioids, an innocuous benthic group at the time, filled newly opened niches and radiated opportunistically over a period of a few tens of millions of years.  During this time, especially during the past 10 million years, there were repeated groundings of the ice sheet on the continental shelf.  These large scale disturbances contributed to the habitat instability that is so important in promoting evolutionary change.  Under these conditions, notothenioids expanded from a single lineage into five families and 100+ species, as well as into many different morphological and ecological types including some that live in the water column in spite of the absence of a swim bladder. Notothenioids underwent a depth-related diversification directed away from the ancestral benthic habitat toward pelagic or partially pelagic zooplanktivory and piscivory.  Notothenioids were able to fill these niches as well as remaining the dominant benthic group.   The figure below provides an example of the range of morphological diversity within the Nototheniidae.  Because they evolved in isolation in this remote locality, 97% of notothenioid species are endemic.  As a result the waters around Antarctica contain, in the words of the well-known biogeographer John Briggs (2003), “the world’s most distinctive marine biota”.

A variety of interesting physiological specializations also distinguish the Antarctic notothenioids.  Noteworthy among these are antifreeze glycoprotein compounds (AFGPs), blood plasma osmolarities about 70% higher than most marine fishes, and extreme stenothermia that allows survival only in the range of –2.5 to +6.0°C (DeVries and Cheng 2005).  Appearing coincident with the initiation of glacial and sea ice conditions, the AFGPs are essential for survival in ice-laden waters (Chen et al., 1997).  Although they are sometimes considered a “key innovation”, there is no correlation between the appearance of AFGPS and the ecological diversification of the majority of notothenioids.  Another way to view AFGPs is as a “constituitive adaptation”, meaning that they are vital, continuously synthesized compounds that are absolutely necessary for survival in subzero, ice laden seawater.  As an analogy, they operate in the background, similar to the autonomic nervous system, as an essential system but one that is not directly coupled to ecological diversification.  The protection they afforded notothenioids allowed subsequent diversification into cold icy habitats when such became available.  Divergence times inferred from nucleotide sequence data suggest this was relatively recent, about 10 million to 1 million years ago, about 10 million years after the initial inferred appearance of AFGPs (Near et al., 2012).

The Antarctic fish fauna lacks the higher taxonomic diversity typical of all other inshore marine habitats.  On the Antarctic shelf notothenioids dominate the fauna in terms of species diversity, abundance and biomass, the latter two at levels of 90%.  The diversification of notothenioids centered on the evolutionary alteration of buoyancy and the morphology associated with swimming and feeding in the water column.  Although they lack swim bladders, in some species density reduction to neutral buoyancy has been achieved through a combination of reduced skeletal mineralization and lipid deposition.  Pedomorphic changes in the skeleton are also associated with reduced density.  In the dominant family Nototheniidae, about 50% of the Antarctic species temporarily or permanently inhabit the water column rather than the ancestral benthic habitat.  This evolutionary tailoring of morphology for life in the water column is the hallmark of the notothenioid radiation and arose repeatedly in different notothenioid clades. 

I will use the two nototheniid species shown in the photos below to illustrate their great functional biodiversity and the fact that their interactions within the ecosystem are particularly important.  The Antarctic toothfish, Dissostichus mawsoni and the Antarctic silverfish, Pleuragramma antarcticum, are the prime examples of neutrally buoyant species that exhibit substantial morphological and ecological diversification in spite of being sister taxa.  Both D. mawsoni and Pleuragramma are abundant and ecologically important in the shelf waters as the top piscine predator and the primary forage fish, respectively.  A net towed through the waters of the Ross Sea shelf comes up with almost nothing but Pleuragramma.  Because both species live in the water column, they are available as prey to whales, seals and penguins and to each other.  Thus their sheer abundance helps sustain these populations of top predators (La Mesa and Eastman, 2012).  In the absence of sharks, D. mawsoni is the top fish predator, with the largest documented specimen measuring 2.36 m (7.74 ft) and weighing 150.6 kg (331 lbs).  They attain a maximum age of nearly 40 years.  The bottom line: notothenioids fill most of the ecological niches and their functional biodiversity is unrivaled—nowhere else in the marine shelves of the world is a single fish clade is so dominant.

There may be multiple species flocks among notothenioids

The notothenioid diversification has produced different life history or ecological types similar in magnitude to those displayed by taxonomically unrelated shelf fishes elsewhere in the world.  This is unusual in the marine realm and raises the possibility that notothenioids may include examples of species flocks.  A species flock is an assemblage of a disproportionately high number of closely related species which evolved rapidly within a circumscribed area where most species are endemic.  Classic examples include Darwin’s finches in the Galápagos, Drosophila fruit flies in Hawaii, cichlid fishes in the East African Great Lakes and sculpin fishes in Siberian Lake Baikal.  Notothenioids on the high Antarctic shelf possess many of the characteristics of a species flock—disproportionate speciosity, morphological and ecological diversification, habitat dominance, high endemicity and monophyly.  However, the notothenioid “flock” may actually a group of flocks that appeared sporadically over a protracted period, but especially during the cold icy climatic downturns during last 10 million years (Near et al., 2012).

Commercial fishing for D. mawsoni in the Ross Sea—the last intact large marine ecosystem

In the mid-1980s “Chilean sea bass” (Patagonian toothfish, Dissostichus eleginoides) began appearing in American fish and supermarkets for about $7.00/pound.  As an obscure fish from distant oceans, it didn’t raise many eyebrows at the time.  By the mid 1990s, a market for Chilean sea bass (consisting of D. eleginoides as well as D. mawsoni) had been created (Knecht, 2006), and by 1996 fishing had expanded into the high latitude waters of the Ross Sea, nearly 2,000 miles south of New Zealand.  With a current retail price of $25-$30/pound, toothfish has became too pricey for all but the most upscale clientel, nevertheless the demand persists.  During the Antarctic summers there are now numerous longlining vessels in the Ross Sea, nearly as far south as a ship can sail.  The commercial fishery has impacted the D. mawsoni population to the extent that, in McMurdo Sound, it is now difficult to catch the few specimens of D. mawsoni needed for scientific research (Ainley et al., 2012).

The implications of all this are sobering—toothfishes are probably the last large marketable fish left in the ocean.  What does the future hold?  The Ross Sea deserves protection for its status as an unparalleled marine habitat—a fascinating cold evolutionary hot spot and the last intact large marine ecosystem on the planet.  The Ross Sea and its fauna are currently underappreciated by the general public, even though their biological significance is equivalent to World Heritage Sites such as Lake Baikal, the African Great Lakes, the Galápagos and portions of the Hawaiian Islands and Madagascar.  A group of Antarctic scientists (FORSE: Friends of the Ross Sea Ecosystem) have united under the leadership of David Ainley to call attention to the commercial fishing, to elevate the public appreciation of the Ross Sea and its fauna, and to advocate for the establishment of a marine protected area encompassing most of the Ross Sea.

If these issues are of interest to you, please visit The Last Ocean web site (http://www.lastocean.org) to learn more about the Ross Sea and how you can help preserve this spectacular marine ecosystem.  Also watch for the appearance of the “The Last Ocean” film by Peter Young of Fisheye Films Limited in New Zealand. The film reveals the beauty of High Antarctic and its fauna, and explores the ecological and human implications of harvesting the last large fish in the ocean. The film/DVD will be probably be released in the US in 2013.  You can view the official trailer here:

References