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JAPAN SOCIETY LECTURE Ocean islands and mass extinctions: the fossil record of Japan - Oriental Club, London Lecture by Richard J. Twitchett University of Plymouth, Plymouth, PL4 8AA, UK. rtwitchett@plymouth.ac.uk Different periods of time in the planet's history were characterised by different groups of organisms, and the only evidence we have of their existence are their fragile fossil remains. Classifying fossils and documenting the history of life is a complex and ongoing process involving the efforts of many palaeontologists worldwide. These studies have resulted in two broad conclusions; firstly, that animal life today is more diverse than at any time in the geological past, and secondly that this overall increase in biodiversity through time has been punctuated by five major mass extinction events - relatively brief crises during which a significant proportion of the world's biota vanished forever. The most severe of these events was the Late Permian event that occurred some 250 million years ago. Currently this event is attracting an unprecedented level of scientific interest. Reasons for this include the fact that the event was apparently rapid (in geological terms), was caused by earthbound processes such as climate and sea-level change, and is intimately associated with an episode of global warming. Temperature rise during the Late Permian event is thought to have been between 4 and 6°C, which is a similar temperature rise as some scientists predict will occur by the end of the 21st century. Scientists are even beginning to describe the extinction of present-day species as the "6th Mass Extinction Event". Although the Late Permian event happened so long ago, its influence can still be seen in marine ecosystems of the present day. For example, all modern sea urchins (including the edible ones!) have a 5-fold symmetry (five rows of tube feet alternating with five rows of spines), whereas prior to the end-Permian event sea urchin morphology was much more variable. During the extinction event all this variety was lost. The one or two surviving species happened, by chance, to have a five-fold symmetry and this basic morphology has been passed down to all subsequent forms. The importance of Japan The rock and fossil records of Japan are proving crucial to understanding the Late Permian event. Japan's importance is due to two factors; its geological structure and geographic location. Presently Japan sits at the western edge of the Pacific Ocean, and 250 million years ago was in a similar position at the edge of an even greater ocean called Panthalassa. One of the planet's great tectonic plates, upon which the Pacific Ocean lies, is gradually being subducted beneath Japan. This downward movement triggers earthquakes and as the plate descends the rocks heat up and melt, and this molten material rises back to the surface forming the volcanoes that comprise the central spine of the country. Although most of the tectonic plate is melted and lost forever, every now and then parts of the Pacific Ocean floor, including oceanic islands and seamounts (submerged islands), are scraped off and end up being incorporated into the mass of Japan. This process has been going on for a long time, and these scraped off fragments of ancient seamounts and ocean floor from Panthalassa and the proto-Pacific provide unique windows back in time. They are also of economic importance too: the limestone that is quarried extensively at Tsukumi, in Oita-ken, Kyushu, being one example. The ancient ocean floor The rocks that line the Kiso river at Inuyama comprise scraped off fragments of ancient ocean floor. These rocks are cherts and are built of the skeletons of microscopic marine plankton called radiolaria. Differences in colour reveal environmental changes that took place in the deep ocean at the time of the Late Permian extinction event. Cherts of the Permian Period, before the extinction event, are a rich red colour, due to the presence of iron oxides at the time these rocks were being formed (in effect these deep ocean sediments "rusted" as they were laid down, just as an iron nail will rust if exposed to water and air). Iron oxides, and thus red-coloured rocks, indicate that plenty of oxygen was reaching the deep ocean floor. However, as we approach the extinction event in the Late Permian, the deep ocean cherts turn first grey and then black. The iron in these rocks is in the form of iron sulphide (not iron oxide), which indicates that the rocks were deposited in waters that lacked oxygen. The conclusion reached by Prof. Yukio Isozaki, of Tokyo University, who studied the Kiso river cherts in the early 1990s, was that the well-oxygenated oceans of the Permian, mixed by vigorously circulating currents, gradually stagnated. As the ocean currents slowed to near-standstill, there was no way of replenishing the oxygen content of the deep ocean waters, and as the oxygen was used up the animals died out. The extinction event coincided with the peak period of stagnation, and the darkest black rocks. As one continues on past the extinction event and through the recovery interval, a mirror-image change occurs as the rocks turn first grey and then to a lovely red colour once more. The deep ocean ecosystem returned to normal 10 million years after the extinction event. What caused the ocean currents to stop circulating in the Late Permian? The most likely answer is global warming. Computer simulations tell us that when the planet warms up, the currents that circulate through the deep oceans will slow down. This effect, coupled with the fact that warmer water holds less dissolved oxygen than cool water, means that the deep ocean becomes stagnant and unable to sustain diverse animal life. After millions of years of stagnation, the climate changed again, and the ocean currents returned to ventilate the depths and make them suitable, once more, for diverse animal life. Similar changes as those recorded along the banks of the Kiso river are recorded several times in the planet's history at locations worldwide. The sequence of global warming leading to ocean stagnation and extinction is always the same in each of these events - a worrying thought, perhaps, given the concerns of present day climatologists. The ancient seamounts Seamounts, also called guyots, are submerged ocean islands - peaks of biodiversity below the ocean waves but far above the ocean floor. Fragments of ancient seamounts from around the time of the Late Permian extinction event are accessible in a few locations in southwest Japan, most notably at Tahokamigumi (Ehime Prefecture, Shikoku) and Kamura (Miyazaki Prefecture, Kyushu). Both locations are forested and overgrown, and it's very difficult to observe the fossils in the field. In order to study these important rocks, one has to collect many kilograms of rock and transport them back to the laboratory for detailed analysis. Microscopic fossils contained in these rocks have been studied for many years by Professor Toshio Koike (Yokohama). His research has shown that these limestones provide a continuous record through the Late Permian mass extinction event and the subsequent recovery of the Triassic Period. The ecological changes that are recorded in these limestones have, until recently, been little studied. Rocks collected from both localities reveal that the diverse, complex marine ecosystem of the Late Permian period rapidly disappeared and was replaced by an exceedingly low diversity community of rare, small-sized animals. The rocks change from pleasant, pale coloured limestones, to very dark limestones with a strange, "clotted" texture. This is very unusual. The clotted texture informs us that the seafloor, where these limestones formed, was carpeted by a thick microbial mat. Little oxygen penetrated the mat, and in the sediment underneath iron sulphides could form, which give the limestones their dark black colour (just as we saw in the deep ocean cherts from Inuyama). The few organisms that could live in such an environment included very small snails, and thin-shelled bivalves that lived on the seafloor and were adapted to such an unpleasant environment. Marine environments that are dominated by microbial mats are exceedingly rare on the Earth today. One example is Shark Bay, in Western Australia. In most places, large-sized grazing and burrowing animals keep the seafloor churned up and prevent the microbes from forming extensive mats. Only where such large animals are rare, because of locally harsh environmental conditions, can microbial mats grow. In Shark Bay, the waters in the shallow lagoons have too much salt in them for most marine animals to tolerate, and so the microbial communities can thrive. In the aftermath of the Late Permian extinction event, the large-sized animals that normally hold the mats at bay became extinct and the mats took over. Similar clotted, dark limestones with evidence of extensive mats are observed at many localities worldwide, not just in Japan. Gradually, as conditions improved after the Late Permian event, the larger-sized organisms returned and the mats disappeared once more. The Triassic seamount limestones become, once again, light grey or cream in colour and the abundance and size of animal remains (of bivalve shellfish, sea urchins, snails, brittle stars etc.) slowly increase. The ecosystem gradually returned to its former complexity too, as new species appeared to fill the vacant niches left in the wake of the extinction event. The process by which animals and plants recolonise an area that has been wiped clean by some disaster (such as a volcanic eruption) is called ecological succession. On land, the ecological succession of plant communities follows a fairly fixed pattern as ferns, grasses and herbs are first to appear, followed by shrubs, then immature woodland, and culminating in a mature forest ecosystem. After small-scale events at the present day, this process takes a couple of centuries. After the global-scale devastation during the Late Permian event, this process took much, much longer (several million years). What about ecological succession in the oceans? My recent work, on the rocks of Japan and elsewhere, is beginning to show that similar patterns of community change may be observed in ancient marine ecosystems too. Animals in marine ecosystems are adapted to live at different heights above and below the seafloor. For example, some shellfish burrow deeply, while others are cemented on the seafloor, and some animals such as sponges may reach far up into the water column. These different levels above and below the seafloor are called tiers. In the immediate aftermath of the Late Permian extinction event, the rare animals that comprise the seafloor communities, such as very small snails, occupy only the lowest and shallowest tiers. Deep burrowers are absent, as are those organisms that reach up into the overlying water column. In the next stage of succession, animals that burrow a bit deeper begin to return. These are followed by animals that reach up into the water column for food. In the Triassic recovery, the group that comprises this stage (analogous to the immature woodland stage of plant succession on land) are the crinoids. Crinoids are related to the sea urchins and starfish, but have a long stalk for attachment to the seafloor. On top of this stalk sits the body of the animal, which has a number of long, frond-like arms that are used to catch particles of food. In the modern oceans, crinoids are confined to water greater than 100m in depth, and are usually rare animals (although they happen to be particularly common off the Pacific coasts of Japan). Crinoids require plenty of floating food particles, and their re-appearance is an indicator that the ecosystem is beginning to function normally again. Finally, the marine community returns to its previously complex and normal state. The appearance of crinoids is an important marker during the Triassic recovery, indicating that the ecosystem is returning to normal. In most tropical, shallow seas of the Triassic, crinoids do not appear for 3-4 million years after the Late Permian extinction event. In oceanic seamount settings, however, crinoids appear much quicker. In the Japanese seamounts of Kamura and Tahokamigumi crinoid fossils may be found within a million years after the event. Still a long time, but a significantly quicker reappearance than elsewhere! Seamounts in Oman show a similar pattern. Thus it appears that the oceanic seamount ecosystem recovered more rapidly than other tropical ecosystems, although the deep ocean floor remained uninhabitable for much longer. Acknowledgments I wish to thank the Japan Society for the Promotion of Science for funding my research in Japan; Dr. Tatsuo Oji (Tokyo) for being my host professor and for introducing me to the Permian and Triassic rocks of Japan; the other members of the research group in Tokyo for discussions, field assistance and for making my stay so enjoyable, especially Prof. Tanabe, S. Fujiwara, Y. Kashiyama, Y. Yoshioka and H. Yamagishi; Prof. Yukio Isozaki (Tokyo) for many years of help and discussions; David Casenove, for undertaking a preliminary study of the seamount limestones; Prof. Toshio Koike (Yokohama) for useful discussion; the EJEF language school for their patience in trying to teach me Japanese; and finally, thankyou to all those friends and colleagues in Tokyo who made my stay such an enjoyable and fruitful one.

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