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
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
Why do notothenioids contribute so heavily to
Antarctic fish diversity at the organismal and
When did the fauna become "modern" in taxonomic
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
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
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,
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
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.
a typical benthic notothenioid fish of the family
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
A diverse, cosmopolitan, temperate to cold
temperate Eocene fauna was succeeded by the highly
endemic, cold adapted modern fauna.
fauna is dominated by the 100+ species of
notothenioids that evolved
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
Cladogram of notothenioid relationships, with colors
showing showing geographic distributions and wedges
proportional to species diversity in each of the
This cladogram is simplified from one based
on nucleotide sequence data in Near et al. (2004).
A more recent cladogram, based on more gene
sequences and more species, suggests that some of
the families in the Antarctic clade may not be
monophyletic (Near et al., 2012).
The red dot indicates that all the Antarctic
notothenioids possess antifreeze glycopeptides.
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
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
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
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
Because they evolved in isolation in this
remote locality, 97% of notothenioid species are
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
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
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
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
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.
dominant family Nototheniidae, about 50% of the
Antarctic species temporarily or permanently inhabit
the water column rather than the ancestral benthic
evolutionary tailoring of morphology for life in the
water column is the hallmark of the notothenioid
radiation and arose repeatedly in different
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
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
In the absence of sharks,
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
The Antarctic toothfish,
mawsoni, is a large benthopelagic, migratory
The fish in the photo appears docile but is
just recovering from anesthesia prior to being
Its head has been scarred by the wire set
line used to capture it in McMurdo Sound.
(Photo credit: Rob Robbins)
The Antarctic silverfish,
antarcticum is a small, pelagic (but inactive)
This one is about 115 mm TL and is 3–4 years
reach a maximum size of 250–260 mm TL and live to be
12–14 years old.
There may be multiple species flocks among
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
fruit flies in Hawaii, cichlid fishes in the East
African Great Lakes and sculpin fishes in Siberian
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).
A recently discovered artedidraconid species (Pogonophryne
stewarti), taken at 1,700 m as bycatch from a
toothfish longlining vessel.
with 19 species is less than one million years old,
and may be one of the examples of a species flock
within the notothenioids.
Ilustration by Danette Pratt (from Near et
Commercial fishing for
in the Ross Sea—the last intact large marine
In the mid-1980s “Chilean sea bass” (Patagonian
Dissostichus eleginoides) began appearing in
American fish and supermarkets for about
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
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
population to the extent that, in McMurdo Sound, it
is now difficult to catch the few specimens of
needed for scientific research (Ainley et al.,
The implications of all this are sobering—toothfishes
are probably the last large marketable fish left in
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.
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
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