The Ross Sea: A Cold Evolutionary Hot Spot

Dr. Joseph Eastman writes about the incredible and unique evolution of Antarctic fishes in the Ross Sea

Trematomus bernacchi, one of many Notothenioid fishes (photo credit: John B. Weller)

Recently the home page of my web browser highlighted the discovery of 123 new species of vertebrates and invertebrates in the remote tropical forests of Borneo, an area in Indonesia now protected by the World Wildlife Fund due to its tremendous biodiversity.  Even Darwin called the island “one great luxuriant hothouse made by nature for herself.”

Why would I mention this at the beginning of a piece focused on Antarctic fish and the Ross Sea?  While the Ross Sea may not match the unrivaled taxonomic biodiversity of the tropics, the waters of the Antarctic shelf – exemplified by the Ross Sea, contain spectacular radiations of large marine animals. As used here, radiation means the divergence of members of a single evolutionary line into different niches. These include three species of killer whales, four species of seals, an enormous biomass of two penguin species and about 100 species of fish, including the two-meter long 100 kg Antarctic Toothfish. Numbers of species aside, the high latitude waters of Antarctica, especially the Ross Sea, are a world-class evolutionary site.

Joe Eastman with Icefish (photo courtesy of Joe Eastman)

Evolution in Antarctic waters

Though I am an Ichthyologist, I first went to the Ross Sea in 1971 to study Weddell seal anatomy at McMurdo Station on a National Science Foundation grant. During the trip I met Art DeVries, a physiologist who had been studying Antarctic fishes since the early 1960s. While dissecting seals was my daytime activity at McMurdo, at night Art took me fishing and introduced me to the fish fauna, including the Antarctic Toothfish – the largest fish predator in the Southern Ocean.

I didn’t know much about the ecology of the notothenioid fish (the dominant family of Antarctic fish) but I was aware of Art’s work because that summer I read his paper in Science on the discovery of antifreeze proteins in notothenioid fish.  Art’s paper described how these antifreeze proteins cause a depression in the freezing point of blood that allows notothenioids to survive in subzero water.  Today we call these antifreezes a “key innovation” because they permitted notothenioids to radiate (expand evolutionarily) in these cold waters.  If they were not first protected from freezing, this could not have happened; I would not have devoted decades of my career to studying their evolution and I would have nothing to write about here.

After Art sparked my interest in notothenioids, I received my own National Science Foundation grant to work on the anatomy of a variety of different body systems that had changed over time from their ancestral condition.  Notothenioids lack swim bladders (the mechanism by which most fish stay aloft in the water column) and are therefore supposed to be bottom dwellers. Yet we caught some of them, like the Antarctic Toothfish, on hooks set a couple hundred meters above the sea floor.  As Art and I collaborated, we soon discovered that indeed a few notothenioids, like the toothfish and the silverfish, were neutrally buoyant and permanent inhabitants of the water column.

Over the next two decades I worked on various aspects of the buoyancy and morphology of notothenioids, with periodic trips to McMurdo to replenish my supply of fish.  To expand the diversity of my catch, I participated on research cruises out in the Ross Sea on the Nathaniel B. Palmer.  By the late 1990s I had encountered dozens of species, a few of them new to science, and gained a greater appreciation of the diversity and dominance of notothenioids in the high shelf Antarctic ecosystem.  Over the last decade or so, an average of one new Antarctic fish species has been discovered every year.

A new species Pogonophryne stewarti that Richard Eakin, Tom Near and Joe Eastman described in 2009. It was taken at 1,700 m as bycatch on a toothfish longlining vessel (figure courtesy: Joe Eastman).

Antarctica has 327 fish species, a small number considering the global diversity of fishes (about 31,000 species total) and the large size of the Southern Ocean (about ten percent of the world’s ocean). But this relatively low species diversity does not indicate the fauna is uninteresting in comparison to the species-rich faunas of tropical lakes, rivers and coral reefs.

Biodiversity is not just about numbers. It has three levels or dimensions: genetic, taxonomic and functional.  Genetic biodiversity refers to the information in various DNA molecules, while taxonomic biodiversity refers to the number or quantity of different species, and functional biodiversity includes all aspects of ecosystem function, such as the importance of organisms in the food web.

In the case of the Ross Sea ecosystem, which harbors 95 different fish species, the functional biodiversity of these fishes is paramount. The isolated waters of the Ross Sea shelf form a unique evolutionary site where the abundance, biomass, and functional biodiversity of the notothenioid fishes confer uniqueness on the structure of the Ross Sea ecosystem.  By this I mean that instead of having a variety of unrelated fishes filling the various niches, as is the case in all other shelf areas of the world, notothenioids fill nearly all the niches in the Ross Sea.  Furthermore, notothenioids eat each other and in turn are eaten by the large vertebrates (birds, seals, and whales).  In short, they are the linchpin of the ecosystem and it could not function without them.

Nathaniel B. Palmer in pack ice (photo credit: Joe Eastman)

The importance of notothenioid functional biodiversity was truly brought home to me while bottom trawling from the Nathaniel B. Palmer near Beaufort Island, just north of McMurdo Sound.  Here notothenioids made up 77 percent of the species, 92 percent of the individuals and 91 percent of the biomass of our catch.  No other shelf area in the world has such lopsided figures.

Not only were notothenioids dominant on the bottom, but they also made up most of the fish we found throughout water column – a mark to their incredible diversification.  As I mentioned above, all notothenioids lack swim bladders and the original stock was confined to the seafloor.  However in the shelf waters some species have undergone morphological and ecological diversification during their evolution to confer neutral buoyancy, which allows them to occupy pelagic niches at various depths on the shelf and slope. Diversification in buoyancy is the ecological hallmark of the notothenioid radiation and was accomplished by a combination of reduced skeletal mineral content and deposition of low density fat.  They also have a tendency to retain larval features (the technical term is pedomorphy), like cartilage, that makes them less dense than if they were bony.

The toothfishes, Dissostichus mawsoni and D. eleginoides, and the Antarctic Silverfish, Pleuragramma antarcticum, are the prime examples of neutrally buoyant species.  Both D. mawsoni and Pleuragramma are abundant and ecologically important in the Ross Sea as the top piscine predator and the primary forage fish, respectively.  A net towed through the upper few hundred meters of the Ross Sea shelf comes up with nothing but silverfish (Pleuragramma) – their sheer abundance helps sustain whales, seals, and penguin populations in the Ross Sea.  Bottom line here: in the Ross Sea a single group of fishes, the notothenioids, fills most of the ecological niches and their functional biodiversity is unrivaled In comparison with any other marine shelf area of the world.

Filling a frozen niche

How did notothenioids alone become the dominant fish group on the Antarctic shelf?  Mostly they were in the right place at the right time. Tectonic, oceanographic and climatic events associated with Antarctica moving south and breaking off from the supercontinent Gondwana caused a severe decline of the cosmopolitan taxonomically diverse fish fauna from the Late Eocene 34–40 million years ago.  With little competition from other fish groups, the notothenioids (which were an innocuous benthic group at that time) took advantage of the newly opened niches and radiated opportunistically.  In doing so, they expanded from a single lineage into five families and 104 species – all found only in Antarctica.

Because they evolved in isolation in this remote locality, 97 percent of the notothenioids (along with some of the other Antarctic shelf vertebrates and invertebrates) are endemic, meaning they are found nowhere else on earth. As a result the waters around Antarctica contain, in the words of the well-known biogeographer John C. Briggs, “the world’s most distinctive marine biota.”

Antarctic Toothfish, also known as "Chilean sea bass" (photo credit: Rob Robbins)

Fish are not the only organisms that make the high Antarctic shelf and the Ross Sea a noteworthy evolutionary site.  With the breakup of Gondwana, invertebrates were also experiencing bursts of diversification, including some lineages of bryozoans (moss animals), pycnogonids (sea spiders), echinoderms (sea stars) as well as shrimp-like amphipods and isopod crustaceans.  Four species of seals (Weddell, crabeater, Ross and leopard) and two species of penguins (Emperors and the Adélies) also took advantage of this new cold and open environment.  Finally, the Ross Sea has three species of killer whales.  Type A preys on minke whales, type B feeds on seals, and type C (considerably smaller that the other two) lives in dense pack ice and eats primarily Antarctic Toothfish.  The Ross Sea has quite an impressive array of conspicuous and inconspicuous marine life.

Pagothenia borchgrevinki, Notothenioid family (photo credit: John B. Weller)

Let’s wind this up.  In the mid 1980s I was surprised to see Chilean sea bass (D. eleginoides) in my local Kroger’s for $7.00 a pound.  An obscure fish from a long way off, but I didn’t connect the dots.  The contemporary Chilean sea bass (now comprised of both D. eleginoides and D. mawsoni) is now $24.99 a pound, too pricey for Kroger’s, but found sporting an “MSC” certification label in the local yuppie fish market.

We did not spot any toothfish longlining vessels during a 1998 cruise in the Ross Sea, as they were not yet out in force.  Now there are multiple toothfishing vessels within site of McMurdo Station at nearly 78 degrees south in the Ross Sea – as far south as a ship can sail.

Who saw it coming?  I didn’t and I don’t know what the future holds.  I wish I could say that the eyes of the world were turning towards the Ross Sea and its fauna, closely monitoring the health and welfare of the ecosystem as intently as the latest sports scores or episode of “Dancing with the Stars.”  But we know this is not the case.  Evolution knows no geographic or thermal bounds and, unfortunately, neither does commerce.  The Ross Sea deserves protection for its status as an unparalleled marine habitat—currently underappreciated by the general public, but equivalent in its biological significance to World Heritage Sites such as Lake Baikal, the African Great Lakes, the Galápagos and portions of the Hawaiian Islands and Madagascar.  Hopefully my two cents worth here will at least serve to bring a slightly higher level of appreciation to this area and its fauna, and will hasten the day for a broad recognition of the Ross Sea as a fascinating cold evolutionary hot spot.

The Ross Sea, Antarctica (photo credit: John B. Weller)

 

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