Science

Toxic Slime Contributed to Earth’s Worst Mass Extinction—And It’s Making a Comeback

At sunrise on a summer day in Australia, about an hour’s drive from Sydney, we clambered northward along the base of a cliff on a mission. We were searching for rocks that we hoped would contain clues to the darkest chapter in our planet’s history.

Life on Earth has experienced some terrifyingly close calls in the past four billion years—cataclysmic events in which the species driven to extinction outnumbered the survivors. The worst crisis occurred 252 million years ago, at the end of the Permian Period. Conditions back then were the bleakest that animals ever faced. Wildfires and drought scoured the land; oceans became intolerably hot and suffocating.

Very few creatures could survive in this hellscape. Ultimately more than 70 percent of land species and upward of 80 percent of ocean species went extinct, leading some paleontologists to call this dismal episode the Great Dying.

This calamity has been etched in stone across the globe but perhaps nowhere as clearly as on the rocky coasts of eastern Australia. By midmorning we had found our target: an outcrop of coal within the cliff face. Sedimentologist Christopher Fielding of the University of Connecticut, one of our longtime colleagues, had recently identified these rocks as river and lake sediments deposited during the end-Permian event. Following his lead, we had come to sift through the sediments for fossil remains from the few survivors of the arch extinction.

From our vantage point on the outcrop, we could see our first hint of ancient devastation: the absence of coal beds in the towering sandstone cliffs above us. During our dawn scramble across the rocks, we had spotted numerous coal beds sandwiched between the sandstones and mudstones in the lower rock levels. These coals date to the late Permian (around 259 million to 252 million years ago). They represent the compacted remains of the swamp forests that existed across a vast belt of the southern supercontinent Gondwana. In contrast, the younger, overlying rocks that span the early part of the subsequent Triassic Period, some 252 million to 247 million years ago, are devoid of coal. In fact, not a single coal seam has been found in rocks of this vintage anywhere in the world. Instead these strata reflect the peaceful deposition of sand and mud by rivers and lakes, seemingly undisturbed by life.

Historically ignored because of its paucity of fossil fuels for humans to exploit, this so-called coal gap has recently emerged as a key to understanding the history of life on Earth. We now know it was a symptom of a sick world. At the end of the Permian, not only did terrestrial and marine ecosystems collapse, but so, too, did freshwater ones. Recent studies by our team have shown that as global temperatures surged at the close of the Permian, blooms of bacteria and algae choked rivers and lakes, rendering them largely uninhabitable. Our findings help to explain why the ensuing mass extinction was so devastating—and raise concerns about the future of biodiversity in our warming world.

Scorched Earth

As the sun rose higher in the sky, its heat beat down on us relentlessly. We managed to pack in a few productive hours of fossil and rock collection before the outcrop became unbearably hot. At that time, in the early summer of 2018, it seemed warmer than the previous field season. Maybe it really was warmer, or maybe it was just because we had recently arrived from chilly Stockholm, where we work at the Swedish Museum of Natural History. Regardless, by midmorning we retreated to the shade for a couple of hours to cool down and ponder what we had seen.

LAST COAL DEPOSIT of the Permian Period, which appears as a black band in the exposed rock layers, is overlain by cliffs of fossil-barren Early Triassic sandstone. Credit: Chris Mays

We found the coals to consist almost entirely of compacted leaves, roots and wood belonging to trees in the genus Glossopteris. Glossopteris trees flourished in wetlands and readily formed peat, a precursor to coal. Directly above the coals we saw no fossils at first. All the outcrops of similar age around Sydney seemed to contain a fossil dead zone. There were no leaves or roots and scarcely a fossil of any kind, with one critical exception: simple, curved sand-filled burrows up to two meters long. Based on the sizes and shapes of these burrows, we concluded that they were most likely excavated by small mammal-like reptiles roughly the size of modern gophers or mole rats. The busy burrowers had made their homes in the muddy dead zone, implying that these animals had survived the end-Permian catastrophe. Moreover, their burrowing strategy was probably key to their success: it provided a refuge from the scorching surface.

All organisms must bend to the forces of nature. Like our ancestors that survived the end-Permian event, we sought a reprieve from the punishing temperatures during our fieldwork. Fortunately, we had to hide for just a few hours before we could emerge. But what if the insufferable heat had lasted months— or millennia?

Before long the sun crept westward, casting us in the cliff’s shadow, and we concluded the day’s work by collecting more rock samples to analyze back in the laboratory. For most paleontologists, the absence of observable fossils, as occurs within the dead zone of a mass extinction, makes for a short expedition. But we suspected that the full story lay hidden in fossils that couldn’t be seen with the naked eye.

We combined the day’s samples with those we had collected from other rocks of the same age around Sydney, then split them into three batches. We sent one batch off to Jim Crowley of Boise State University and Bob Nicoll of Geoscience Australia to obtain precise age estimates for the extinction event. The second batch went to our colleague Tracy Frank of the University of Connecticut so she could calculate the temperatures that prevailed during the late Permian. We took the third batch with us to the Swedish Museum of Natural History, where we sifted through the samples for microscopic fossils of plant spores and pollen, as well as microbial algae and bacteria, to build a blow-by-blow account of the ecological collapse and recovery.

As expected, our analyses of the microfossils showed that abundances of plant spores and pollen dropped off precisely at the top of the last Permian coal deposit, reflecting near-total deforestation of the landscape. To our surprise, however, we also found that algae and bacteria had proliferated soon after the extinction, infesting freshwater ecosystems with noxious slime. In fact, they reached concentrations typical of modern microbial blooms, such as the record-breaking blooms in Lake Erie in 2011 and 2014. Because explosive microbial growth leads to poorly oxygenated waters, and many microbes produce metabolic by-products that are toxic, these events can cause animals to die en masse. In the wake of the end-Permian devastation, the humblest of organisms had inherited the lakes and rivers and established a new freshwater regime. We wondered how these microbes came to flourish to such a great extent and what the consequences of their burgeoning were. To answer these questions, we needed more context.

Insights came from analyses of the other two samples. The age estimates revealed that the ecosystem collapse coincided with the first rumblings of tremendous volcanic eruptions in a “large igneous province” known as the Siberian Traps, in what is now Russia. The term “volcanic” seems inadequate in this context; the volume of magma in the Siberian Traps was a whopping several million cubic kilometers. Thus, the Siberian Traps province is to a volcano as a tsunami is to a ripple in your bathtub. Studies have consistently implicated the Siberian Traps igneous event as the ultimate instigator of the end-Permian mass extinction, in large part because of the composition of the rocks in the area. Prior to this event, the rocks underneath Siberia were rich in coal, oil and gas. When the Siberian Traps erupted, the heat of the intrusive magma vaporized these hydrocarbons into greenhouse gases, which were then emitted into the atmosphere. Atmospheric carbon dioxide levels increased sixfold as a result.

The timing lined up with Tracy’s new geochemical temperature estimates, which revealed an increase of 10 to 14 degrees Celsius in the Sydney region. The age estimates also nailed down the duration of the observed changes in the Sydney area: the temperature spike and ecosystem collapse had occurred within tens of thousands of years. This geologically rapid change in conditions drove animals from temperate zones to extinction or compelled them to live part-time in the cooler temperatures underground. It also triggered the widespread microbial blooms we detected in our microfossil studies: the slime revolution had begun.

The ancient recipe for this toxic soup relied on three main ingredients: high carbon dioxide, high temperatures and high nutrients. During the end-Permian event, the Siberian Traps provided the first two ingredients. Sudden deforestation created the third: when the trees were wiped out, the soils they once anchored bled freely into the rivers and lakes, providing all the nutrients that the aquatic microbes needed to multiply. In the absence of “scum-sucking” animals such as fish and invertebrates that would otherwise keep their numbers down, these microbes proliferated in fits and starts over the following 300 millennia. Once this new slime dynasty had established its reign, microbe concentrations at times became so high that they made the water toxic, preventing animals from recovering their preextinction diversity for perhaps millions of years. We had just discovered that freshwater, the last possible refuge during that apocalyptic time, was no refuge at all.

A recurrent symptom

Author Terry Pratchett once wrote of revolutions: “They always come around again. That’s why they’re called revolutions.” Although the end-Permian was uniquely ruinous to life, it was probably just the end of a spectrum of warming-driven extinction events in Earth’s history. If the environmental conditions that led to the end-Permian microbial blooms are typical for mass extinctions, then other ecological disasters of the past should reveal similar uprisings. Indeed, almost all past mass extinctions have been linked to rapid and sustained CO2-driven warming. One might therefore expect to see similar, albeit less dramatic, microbial signatures for many other events.

From the precious little previously published data we found on freshwater systems during other mass extinctions, the pattern held up. So far, so good. But the best sign that we were onto something significant came when we placed the end-Permian event, along with the others, on a spectrum from least to most severe. The extinctions appeared to show a “dose- response relationship.” This term is often used to describe the reaction of an organism to an external stimulus, such as a drug or a virus. If the stimulus is really the cause of a reaction, then you would expect a higher dose of it to cause a stronger response. When we applied this reasoning, we saw that the global severity of these microbial “infections” of freshwater ecosystems really seemed to have increased with higher doses of climate warming. The relatively mild warming events barely elicited a microbial response at all, whereas the severe climate change of the end-Permian gave rise to a metaphorical pandemic of aquatic microbes.

We then compared this pattern with the most famous mass extinction of all: the end-Cretaceous event that took place 66 million years ago and led to the loss of most large-bodied vertebrate groups, including the nonbird dinosaurs. In a matter of days some of the most awesome animals to walk the land, swim the seas or fly the skies were snuffed out. Although massive volcanic eruptions are known to have occurred at this time, the majority of extinctions from this event are generally attributed to the impact of an asteroid at least 10 kilometers in diameter that struck an area off the coast of modern-day Mexico at a speed of up to 20 kilometers a second. The resultant global cloud of dust, soot and aerosols may have inhibited the proliferation of photosynthetic microbes in the immediate aftermath of the event. Once the sun broke through, some microbes did multiply, but their reign was short-lived and relatively restricted, probably because of the modest increases in global CO2 and temperature.

Source: “Lethal Microbial Blooms Delayed Freshwater Ecosystem Recovery following the End-Permian Extinction,” by Chris Mays et al., in Nature Communications, Vol. 12; September 17, 2021 (reference material).


Source: “Lethal Microbial Blooms Delayed Freshwater Ecosystem Recovery following the End-Permian Extinction,” by Chris Mays et al., in Nature Communications, Vol. 12; September 17, 2021 (reference material). Credit: Graphic by Jen Christiansen

Without a simmering Earth to prop them up, we found, a new world order for microbes quickly breaks down. The contrasting microbial responses to magma- and asteroid-driven extinction events highlight the importance of high CO2 and temperature for fueling harmful algal and bacterial blooms. This link between greenhouse gas–driven warming and toxic microbial blooms is both satisfying and alarming: an elegant theory of freshwater mass extinction is emerging, but it may be simpler than we thought to cause widespread biodiversity loss—and it all seems to start with rapid CO2 emissions.

On the Rise

Today humans are providing the ingredients for toxic microbial soup in generous amounts. The first two components—CO2 and warming—are by-products of powering our modern civilization for nearly 200 years. Our species has been industriously converting underground hydrocarbons into greenhouse gases with far more efficiency than any volcano. The third ingredient—nutrients—we have been feeding into our waterways in the form of fertilizer runoff from agriculture, eroded soil from logging, and human waste from sewage mismanagement. Toxic blooms have increased sharply as a result. Their annual costs to fisheries, ecosystem services such as drinking water, and health are measured in the billions of dollars and are set to rise.

Wildfires can exacerbate this problem. In a warming world, droughts intensify, and outbreaks of fire become more common even in moisture-rich environments, such as the peat forests of Indonesia and the Pantanal wetlands of South America. Wildfires not only increase nutrient levels in water by exposing the soil and enhancing nutrient runoff into the streams, but they also throw immense quantities of soot and micronutrients into the atmosphere, which then land in oceans and waterways. Recent studies have identified algal blooms in freshwater streams of the western U.S. in the wake of major fire events. Farther afield, in the aftermath of the 2019–2020 Australian Black Summer wildfires, a widespread bloom of marine algae was detected downwind of the continent in the Southern Ocean.

Wildfire could have helped nourish aquatic microbes in the deep past, too. Our investigation of the sediments above the coal seams around Sydney revealed abundant charcoal, a clear sign of widespread burning in the last vestiges of the Permian coal swamps. As in the modern examples, a combination of surface runoff and wildfire ash may well have led to nutrient influx into late-Permian waterways and the proliferation of deadly bacteria and algae.

These ancient mass extinctions hold lessons for the present and the future. Consider the following two premises of Earth system science. First, the atmosphere, hydrosphere, geosphere and biosphere are linked. If one is significantly modified, the others will react in predictable ways. Second, this principle is as true today as it was throughout Earth’s past. The Intergovernmental Panel on Climate Change (IPCC) applied this logic in its latest assessment of the causes and impacts of global warming.

TOXIC BLOOMS of microbes in freshwater ecosystems such as Lake Erie (left) are on the rise as carbon dioxide, temperatures and nutrient runoff increase. Wildfires such as those in the Pantanal wetlands of Brazil (right) can worsen the problem. Credit: Andy Morrison/The Blade/AP Photo

Drawing on ice, rock and fossil records, this consortium of more than 200 scientists concluded that the world has not experienced the present levels of CO2 in more than two million years. In periods with such levels of CO2 in the past, how high were sea levels? How did these conditions affect soil-weathering rates? How were the forests distributed? In other words, how did this difference in the air affect the oceans, land and life? Our society should be desperate to answer such questions in relation to our modern CO2 levels of 415 parts per million (ppm), not to mention 800 or 900 ppm, which is where the IPCC estimates we’ll be by the year 2100 if the world continues to burn fossil fuels at the current rate. As CO2 keeps rising, we need to look further back in time for clues about what to expect. The records of past extreme warming events are only becoming more relevant.

The analogy between the end-Permian event and today breaks down in at least two important ways, yet these discrepancies may not be as comforting as we might hope. For one thing, the pace of warming was probably different. Life struggles to cope with large environmental changes on short timescales, so perhaps the end-Permian event, the worst struggle in history, occurred much more quickly than modern warming. It is more likely that modern warming is much faster, however. Our team and others have shown that the sixfold increase in CO2 during the end-Permian collapse happened over the course of perhaps tens of thousands of years. At business-as-usual rates, the IPCC projects the same increase in CO2 concentration within hundreds, not thousands, of years.

A second strike against the analogy is the human element. Humans are becoming a force of nature, like a magma plume or a rock from space, but the diversity of ecological stressors they exert is unique in Earth’s history. For this reason, we argue that extreme warming events from the past, such as the one that occurred at the end of the Permian, potentially provide a clear signal of the consequences of climate change. If we listen carefully enough, the fossils and rocks can tell us the results of warming alone, without additional, possibly confounding influences from humans such as nutrient influx from agriculture, deforestation via logging or extinctions from poaching.

Here is the message these past events are telling us with increasing clarity: one can cause the extinction of a large number of species simply by rapidly releasing a lot of greenhouse gas. It does not matter where the gases come from—whether the source is volcanoes, airplanes or coal-fired power plants, the results end up being the same. When we add to that mix the myriad other stressors generated by humans, the long-term forecast for biodiversity seems bleak.

There is, however, a third way in which our species could break the analogy, one that is far more hopeful. Unlike the species that suffered the mass extinctions of the past, we can prevent biodiversity loss through the intelligent application of our ideas and our technologies. Case in point: we can prevent a microbial takeover by keeping our waterways clean and curbing our greenhouse gas emissions.

It is increasingly clear that we are living through the sixth major mass extinction. Freshwater microbial blooms, wildfires, coral bleaching and spikes in ocean temperature are becoming more frequent and intense in our warming world. Where along the extinction-event spectrum the present warming will place us is, for the first time in Earth’s history, up to just one species.


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