THE ARCTIC AZOLLA EVENT

he Cenozoic was characterised glaciation and succession of glacial- Jonathan Bujak by enormous changes in the interglacial cycles, is highly Earth’s climate that affected the unusual and possibly unique in the and Alexandra entire biosphere, including the Earth’s history. T evolution of our own species. The asteroid impact at Chicxulub on Bujak* reveal how These changes resulted from a the Yucatán coast, which marked the combination of factors that end of the Mesozoic 66 million years a unique plant progressively sequestered the ago, combined with other factors may greenhouse gas carbon dioxide from have had a devastating effect on marine changed our the atmosphere, resulting in cooler and terrestrial biotas, but it did not global temperatures, particularly at the affect long-term climate. The early part planet’s climate poles with their year-round cover of ice of the Cenozoic therefore inherited the and snow. Mesozoic greenhouse world, which Our modern bipolar icehouse world continued through the Paleocene. contrasts strongly with the earlier Extensive volcanism associated with the greenhouse climate of the Mesozoic, Greenland mantle plume injected which had lower latitudinal thermal enormous quantities of gases, including gradients and poles that were much carbon dioxide, into the atmosphere, warmer than those of today. raising temperatures and triggering the The Cenozoic greenhouse-to-icehouse release of methane clathrates. shift is even more striking because the This potent combination resulted in geological record indicates that our high levels of greenhouse gases 55 Above: Azolla from North America present climate, with its bipolar million years ago during the Paleocene-

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THE ARCTIC AZOLLA EVENT LASTED FOR ABOUT A MILLION YEARS, BEGINNING IN THE LATEST EARLY EOCENE (YPRESIAN) AND ENDING JUST AFTER THE ONSET OF THE MIDDLE EOCENE (LUTETIAN) ❞ Courtesy of Dr Ron Blakey, Professor Emeritus NAU Geology

The greenhouse world at the end of the Cretaceous 66 million years ago compared to the modern icehouse world with its bipolar glaciation

Part of the ACEX core dominated by thin brown The ACEX scientific drillship, Vidar Viking beds of Azolla

Eocene Thermal Maximum (PETM, icebreakers Oden and Sovetskyi Soyuz, to Lomonosov aka. the Early Eocene Thermal undertake a unique voyage to the North Vidar Viking reached its drilling location Maximum, EETM). Pole. This was Leg 302 of the Integrated on August 13, but was forced to move to Ocean Drilling Project (IODP), also a nearby site due to deteriorating ice Trigger known as the Arctic Coring Expedition conditions. Drilling began on August 18 Although temperatures fell after EETM, (ACEX). Over the past five decades, in 1209 metres of water, but soon they remained high during the early IODP and its predecessor, the Deep Sea encountered more problems, this time Eocene and averaged 12oC to 15oC in the Drilling Project (DSDP), had due to a shattered core liner, forcing Arctic, where the remains of lush forests systematically drilled sediments beneath Vidar Viking to move to a third location on are preserved in sediments on Ellesmere the world’s oceans, but extensive ice August 27. This time it was successful Island. It is therefore surprising that cover had prevented an expedition to and cored into the Lomonosov Ridge as initiation of the greenhouse to icehouse the Arctic Ocean. the two ice-breakers protected it from the shift occurred at the end of the early The expedition’s objective was to core drifting sea ice. Eocene which, apart from the EETM, Upper Cretaceous and Cenozoic Finally, on September 8, ACEX experienced the highest temperatures of sediments of the Lomonosov Ridge, recovered cores from sediments the Cenozoic. What could have which extends for 1800km across the deposited during the initial greenhouse triggered this remarkable climatic Arctic Ocean and rises three and a half to icehouse shift, revealing thousands of change which eventually led to our kilometres above the surrounding organic-rich layers filled with beautifully present bipolar icehouse world? seafloor. Would the expedition preserved remains of the floating The answer came in 2004, when accomplish its mission to core more than freshwater fern Azolla. Later analyses reduced ice conditions allowed the 300 metres, while maintaining its confirmed that the ‘Arctic Azolla Event’ scientific drillship, Vidar Viking, drilling location in constantly moving lasted for about a million years, supported by the Swedish and Russian sea ice? beginning in the latest Early Eocene ▼

WWW.GEOLSOC.ORG.UK/GEOSCIENTIST | JUNE 2014 | 11 Eocene palaeogeograp hy of the Arctic Ocean before (Turgay Strait open) and during (Turgay Strait closed) the Azolla event

▼ (Ypresian) and ending just after the onset of the Middle Eocene (Lutetian). Specimens of Azolla is a floating freshwater fern that Azolla from Ecuador where can only tolerate slight amounts of Dr Mariano salinity. What were millions upon Montaño is millions of Azolla plants doing in the developing its use as a rice middle of the Arctic Ocean, and why biofertilizer were they there precisely when the Earth experienced one of the most dramatic climatic changes in its history? Was there a connection between the two events? Fossil Azolla Following ACEX, a model answering dated between 50.5 and 55.5 these questions was proposed and Ma (million repeatedly tested during the next decade years) from the when scientists from all over the world Green River Formation of analyzed the ACEX cores, confirming its Garfield County, validity and refining its details. It was Colorado, which subsequently published in a series of are similar in age to Azolla in papers, and featured in the New York the ACEX core. Times on 30 November 2004 (‘Under all The floating leaves and that ice, maybe oil’), National Geographic tendrils are in May 2005 (‘Was the icy Arctic once a identical to warm soup of life?’) and Nature in June those of modern Azolla 2006 (‘From greenhouse to icehouse in 55 million years’). Turgay Following the EETM, the Arctic Ocean was largely land-locked and centered on the North Pole, as it is today, so that it experienced Arctic summers with 24 hours of daylight and winters with 24 hours of darkness, but with much warmer temperatures than those seen today. Its only significant marine connection was through a long narrow seaway called the Turgay Strait, which extended southwards across western Siberia to the equatorial Tethyan Ocean. Then, 49 million years ago, the shallow Turgay Strait became blocked, and the Arctic Ocean became isolated from the other oceans, similar to today’s Henk Brinkhuis Black Sea, which only has a single very at the North Pole narrow connection to the Mediterranean GEOSCIENTIST FEATURE

through the Bosporus. Like the Black were supplied by rocks exposed on the Sea, the Arctic Ocean became ‘stratified’, land surrounding the Arctic, rocks that with little vertical mixing of its water, so may have eventually been eroded away, that its bottom waters became anoxic and ending the Azolla Event. all bottom-dwelling benthic organisms died out. High greenhouse temperatures Impact also caused more energetic weather than Calculations of Azolla’s volume during today and increased the amount of the event show that it had a huge impact rainfall. Rivers discharged large on the world’s climate. The billions of volumes of freshwater, resulting in layers tiny plants drew down the carbon of surface freshwater extending out into dioxide needed for their growth directly the ocean. Satellite images show similar from the atmosphere, reducing freshwater layers spreading out from greenhouse gases, and ending the today’s Amazon River for hundreds of greenhouse climate that had prevailed for kilometres into the Atlantic Ocean. hundreds of millions of years. Levels of

This explained Azolla’s presence far atmospheric carbon dioxide that had from the ancient Arctic Ocean shoreline. been as high as 2500 to 3500ppm before Above: ACEX coring locations close to the North Pole In the Arctic spring and summer, the the Azolla Event were reduced by up to a ❞ free-floating freshwater plant spread and half by the Azolla Event. Below: ACEX scientists at the North Pole multiplied on surface freshwater layers Atmospheric carbon dioxide continued that extended from rivers discharging to fall over the next 49 million years due into the ocean. Each bed of Azolla in the to mountain uplift and changing oceanic WHAT WERE ACEX cores represents a single mat or currents that sequestered even more succession of mats of floating Azolla that carbon dioxide. As atmospheric carbon MILLIONS UPON MILLIONS extended away from shore towards the dioxide fell below 1000ppm about 40 OF AZOLLA PLANTS DOING centre of the Arctic Ocean. As the million years ago, permanent ice and IN THE MIDDLE OF THE floating mats became waterlogged or as snow increased in Antarctica. Then, as it storms fragmented them, the plants died fell even lower to 600ppm just 2.6 million ARCTIC OCEAN, AND WHY and sank to the sea floor and lay years ago, widespread glaciation began in WERE THEY THERE undisturbed, due to the absence of the Arctic, initiating the succession of benthic organisms. The remains of Azolla glacial-interglacial cycles that characterise PRECISELY WHEN THE were then gradually buried by fine today’s icehouse world. Present values EARTH EXPERIENCED ONE sediments or the remains of plankton are just above 400ppm, having risen from OF THE MOST DRAMATIC and other organisms living in the surface pre-industrial values in the mid 18th water, which formed the thin beds Century of about 280ppm. CLIMATIC CHANGES IN separating the Azolla layers. The atmospheric carbon dioxide ITS HISTORY? This process was repeated again and sequestered by Azolla was incorporated again, gradually forming the thousands into the plant biomass, which is ❞ of Azolla beds seen in ACEX cores. preserved in sediments beneath the Some of them may have been deposited Arctic, but a crucial question still needed annually, some every few years or longer, answering. Nitrogen is essential for the others in clusters that were related to growth of all plants and almost all of climatic cycles that affected temperature them obtain this nutrient from nitrogen- and the amount of rainfall and runoff. based compounds present in the soil or These details would be gradually teased underwater substrate. How was Azolla from the core samples, and many still able to grow so rapidly, free-floating in wait to be refined as increasingly the middle of an ocean without this sophisticated techniques become source of nitrogen? ▼ available. However, the general model has stood the test of time. The Arctic Azolla Event lasted for about a million years and scientists are still unsure why it ended. Perhaps the Turgay Strait re-opened and the Arctic Ocean resumed its earlier configuration, or maybe the nutrients needed for Azolla’s growth were finally depleted – nutrients such as phosphates that

WWW.GEOLSOC.ORG.UK/GEOSCIENTIST | JUNE 2014 | 13 GEOSCIENTIST FEATURE

▼ Nine months after ACEX, Henk symbiotic cyanobacterium called fixing organelle in Azolla, and in 2010 Brinkhuis, the expedition’s palynologist, Anabaena azollae. Francisco Carrapiço published his arranged the first meeting of the ‘Darwin Although a few other plants have landmark paper: ‘Azolla as a Azolla Group’ at Utrecht University in cyanobacterial symbionts, the Superorganism’, proposing that Azolla and the Netherlands for geologists with relationship is lost when the plant dies A. azollae are so closely interconnected expertise relevant to the Azolla Event. and has to be renewed each generation. that they represent a single Also invited was biologist Francisco Azolla is unique because it is the only superorganism. This was the missing Carrapiço, Assistant Professor at the known plant in which a cyanobacterial part of the puzzle needed to explain the University of Lisbon’s Department of symbiont is passed to successive Arctic Azolla Event. It showed how Plant Biology, and the world’s leading generations during the plant’s Azolla was able to repeatedly spread expert on modern Azolla. He was to reproduction. The fossil record indicates across freshwater surface layers in the provide information that would answer that the relationship between Azolla and Arctic Ocean, sequestering large the question. A. azollae was established in the mid quantities of atmospheric carbon dioxide, Cretaceous, so that the two organisms to trigger the initial change from a Superorganism have been co-evolving for about 100 greenhouse to icehouse climate. Azolla is a fern that floats freely on the million years. This has resulted in their surface of quiescent freshwater bodies, developing highly efficient and Perfect storm such as ponds, lakes and gently flowing complementary biochemistry, enabling We humans are threatened by a perfect rivers, and it is one of the fastest growing Azolla’s phenomenal growth rate. storm as our population passes seven plants on the planet, doubling its It is a perfect marriage: Azolla billion thanks to shortages of land, food biomass in as little as two days. provides a home for A. azollae, which and energy. Increased emissions of We know that Azolla is a fern because of sequesters nitrogen fertilizer for Azolla greenhouse gases are also reversing its internal structure and the way that it directly from the atmosphere. climatic changes that occurred over reproduces, but it looks nothing like a Their relationship is now so intimate that millions of years. The greenhouse-to- fern. Its leaves are composed of small many of A. azollae’s genes have been lost icehouse shift was caused by a spongy lobes, just a few millimetres long, or transferred to the nucleus in Azolla’s succession of processes that took 49 which float on the water with hair-like cells, so that A. azollae can no longer million years, but mankind’s emission of tendrils dangling in the water below. survive independently outside Azolla. greenhouse gases could reverse this Its larger dorsal leaves are buoyant All of the genetic evidence indicates that process in just a few decades, changing and contain cavities enclosing a A. azollae is evolving towards a nitrogen- the climate back to a greenhouse world Photograph kindly provided by Dr Ian Miller of the Denver Museum of Science

Azolla fertilizing a rice paddy in Ecuador Inset: Azolla usually floats freely on the Bread made from Azolla by Erik Sjödin at Wysing surface of freshwater, but tendrils that dangle freely beneath the plant can also Arts Centre, England. Erik also has recipes for root in wet muddy substrate to provide additional nitrogen fertilizer for the plant pancakes, soup, burgers, and more... GEOSCIENTIST FEATURE

with dizzying speed. Could Azolla help nitrogen-enriched water used to grow their people, rather than dealing with us combat man-made climate change and Azolla is an ideal biofertiliser for problems of climate change. The billions also provide local renewable food, hydroponics to grow fruit and of pledged ‘climate change dollars’ can livestock feed, biofertilizer and biofuel? vegetables, providing local renewable therefore help developing countries using Azolla has been used for thousands of food. And because Azolla can be grown Azolla’s synergy, thus turning Perfect years in India and the Far East as a indoors, anywhere in the world under Storm into Perfect Opportunity. biofertilizer and livestock feed, and its carefully controlled conditions, it has Geologists are fortunate in having a potential as a biofuel is indicated by the potential to provide these products unique perspective grounded in deep- (unpublished) studies on modern Azolla. globally, promoting urban agriculture in time. We have traditionally used the It has also been taken on space missions our growing cities and megacities, and present as a key to the past, but we can to confirm its use as a food, water helping to provide a permanent also use the past to understand the purifier and oxygen provider for space solution to regions with repeated present and shape the future in a positive travel because of its ability to rapidly famines such as East Africa. way. Perhaps the remarkable events that grow in stacked trays of shallow water occurred 49 million years ago in the less than three centimetres deep. Azolla Global potential Arctic can help us do that. ◆ can therefore help us tackle the threat of This flexibility is the key to Azolla’s man-made climate change and shortages global potential. The complex * Dr Jonathan Bujak is a palaeontologist who of land, food and energy. Its potential biotechnology has already been has spent the past 40 years studying Arctic can be increased because the water in developed by Azolla and A. azollae’s palaeoclimate and the greenhouse to icehouse which Azolla grows is enriched in co-evolution, so all we need to do is shift. His daughter, Alexandra Bujak, is an nitrogen sequestered by A. azollae from work with nature instead of destroying environmental scientist specializing in modern the atmosphere. it. And because Azolla’s biosystem Azolla’s multiple uses. Their book ‘The Azolla For example, Azolla’s growth can be addresses the problems of energy and Story’ will be published in 2014. Author contact: integrated with the production of algal food as well as climate change, it is E: [email protected] oil (‘algoil’), with the nitrogen-enriched not necessary to prioritise them. Azolla water from fertilizing algal growth This resolves the main problem that ➤ FURTHER INFORMATION and increasing the sequestration of plagued the 2009 and 2013 Copenhagen You can read more about this carbon dioxide to produce a range of and Doha Summits on Climate Change remarkable plant at: biofuels precisely where they are needed. when many developing countries http://theAzollafoundation.org Or, to take another example, the argued that their priority was to feed Image: Nikita Tiunov / Shutterstock.com

Above (upper): Azolla and inset Azolla’s cyanobacterial symbiont, A. azollae Above (lower): Azolla’s leaves and a magnified image of A. azollae living inside Azolla’s leaf cavities