Studying the metabolism of living brachiopods like these collected from San Juan Island, Washington, allowed Stanford researchers to understand how the physiology of the modern fauna and Paleozoic fauna may have differed and how these groups would have been differentially impacted by oxygen and temperature changes during the Permian–Triassic mass extinction.
Image credit: Erik Sperling.
This is not the picture of a planet engineered to remain permanently benign or perfectly “fine-tuned” for life — still less for human life in the United States. Earth is habitable, but its habitability is contingent and sometimes precarious. The same interacting atmospheric, oceanic, geological and biological processes that sustain life can, when pushed beyond critical thresholds, drive abrupt environmental change, ecological collapse and mass extinction.
At several points in Earth's history, reinforcing feedbacks have transformed relatively small initial disturbances into rapid and profound environmental changes. Organisms adapted to the previous conditions were then confronted with combinations of heat, cold, acidification, oxygen loss or other stresses occurring too quickly for most populations to adapt. The result was widespread extinction.
What has been less well understood is why some groups were devastated while others living in the same changing environment survived. This is an important question for us because every organism alive today is descended from lineages that somehow survived every previous mass extinction.
Research by a Stanford University-led team, recently published in the Proceedings of the National Academy of Sciences of the United States of America (PNAS), now offers an experimentally supported explanation for one of the most striking patterns associated with the end-Permian mass extinction — the “Great Dying” of about 252 million years ago.
The catastrophe eliminated an estimated 96 per cent of marine species and roughly 70 per cent of terrestrial vertebrate species. It followed the immense Siberian Traps volcanic eruptions, which released enormous quantities of greenhouse gases and drove global temperatures sharply upwards. The warming oceans then presented marine animals with two simultaneous problems: warm water holds less dissolved oxygen, while higher temperatures accelerate biochemical reactions and increase an animal's need for oxygen.
The effects were not distributed evenly across the animal kingdom. Brachiopods — superficially resembling clams — and crinoids, or sea lilies, had dominated many seafloor communities for hundreds of millions of years, yet they were devastated. Molluscs such as bivalves and gastropods also suffered heavy losses, but a much larger proportion survived. This ancient ecological turnover helps explain why beachcombers today are far more likely to find the shells of clams and snails than those of brachiopods.
The Stanford-led researchers sought to explain this selectivity by studying living representatives of the animal groups that dominated before and after the extinction. They measured how much oxygen the animals consumed and how their oxygen requirements changed as the surrounding water became warmer.
At lower temperatures, the predominantly sedentary, slow-metabolising representatives of the older “Palaeozoic fauna” could survive at oxygen concentrations that would asphyxiate some of the more active animals. Their low-energy lifestyles required little oxygen. That apparent advantage disappeared, however, when the water warmed. Their oxygen requirements rose steeply, while their comparatively limited respiratory and circulatory systems could not increase the supply of oxygen sufficiently to meet the growing demand.
The more mobile animals, including many molluscs, already required more oxygen because they possessed muscular bodies, moved about, burrowed or actively pumped water across their respiratory surfaces. Supporting that activity had favoured the evolution of more effective oxygen uptake, ventilation and circulation, together with a greater capacity to increase oxygen delivery when necessary.
It was therefore not the higher metabolic rate itself that protected these animals. On its own, a high metabolic rate would have increased their vulnerability to oxygen shortage. The advantage was the more powerful oxygen-supply system that had evolved to support that metabolism. It provided a physiological reserve that could be called upon when warming simultaneously increased oxygen demand and reduced the amount of oxygen available in the water.
The animals most severely affected by the Great Dying were consequently those least able to tolerate the lethal combination of rising temperature and falling oxygen availability. The pattern revealed by the experiments closely matches the pattern of survival and extinction preserved in the fossil record.
The Warming–Oxygen Squeeze. Marine animals faced two related problems during the end-Permian mass extinction: the oceans became warmer and, at the same time, contained less oxygen.The paper in PNAS was accompanied by a news release from Stanford University:
This happens because warm water cannot hold as much dissolved oxygen as cold water. At the same time, increasing temperature accelerates many biochemical reactions, causing an animal’s metabolism — and therefore its demand for oxygen — to rise.
Animals were consequently caught in a physiological squeeze: they needed more oxygen precisely when less was available.
Why did more active animals fare better?
At first sight, animals with higher metabolic rates might be expected to suffer most severely because they normally consume more oxygen. The advantage, however, was not the high metabolic rate itself. It was the respiratory and circulatory capacity that had evolved to support an active lifestyle.
Mobile animals need efficient gills or other respiratory surfaces, effective circulation and the ability to increase oxygen uptake during activity. Under normal conditions, this extra capacity allows them to move, burrow, swim or pump water across their respiratory surfaces. During a warming crisis, it also provides an aerobic reserve — spare capacity that can be used to meet the rising demand for oxygen.
Many sedentary animals, such as brachiopods and crinoids, normally required relatively little oxygen. Their respiratory systems were adequate in cool, well-oxygenated seas, but they had less capacity to increase oxygen delivery when temperatures rose. Their oxygen requirements increased, but their ability to supply that oxygen did not increase sufficiently.
The more active animals did not survive because they used less oxygen. They survived more often because evolution had already equipped them with better machinery for obtaining and distributing it.
Sedentary, low-metabolism animals More active animals Low oxygen demand under normal conditions Higher routine oxygen demand Limited ventilation and circulation More effective oxygen uptake and circulation Little spare oxygen-delivery capacity Greater aerobic reserve Demand could outstrip supply rapidly as water warmed Better able to increase oxygen delivery as demand rose
Researchers confirm cause of Earth’s biggest mass extinction
Through experiments comparing living representatives of animal groups that dominated Paleozoic oceans with those that thrive today, Stanford scientists have directly linked the disappearance of once-dominant marine groups to intolerable heat and diminished oxygen in ancient oceans.
In briefA new Stanford-led study offers the clearest picture yet of how some ocean life survived our planet’s biggest mass extinction while most animals did not.
- The Permian–Triassic extinction event, which killed off most life on Earth, did not impact all animal groups equally
- In the oceans, groups of animals collectively called the Paleozoic fauna that had long dominated marine environments were almost completely wiped out, but the so-called modern fauna experienced far fewer extinctions and have dominated since
New research reveals that the warmer, poorly oxygenated oceans of the Permian–Triassic transition strongly favored the modern fauna’s faster metabolisms, while the Paleozoic fauna’s slow metabolisms could not keep up with increased oxygen demand triggered by the warming waters
About 252 million years ago, 96% of marine species and 70% of land animals died off during the Permian–Triassic extinction event, known as the “Great Dying.” Not all branches of the evolutionary tree were affected evenly, however.
In the ancient oceans, the extinction wiped out nearly all brachiopods, which resemble clams, and certain types of seafloor-dwellers like sea lilies (crinoids). These were the animals that dominated seafloors for roughly the first 280 million years of animal life on Earth. However, only about half of the mollusks, like clams and snails, died out. Ever since, Earth’s oceans have been dominated by mollusks, fish, and echinoderms such as starfish and sea urchins that survived.
The new study, published July 6 in Proceedings of the National Academy of Sciences, for the first time incorporates biological responses of the animal groups that were decimated in the extinction and those that fared better. The groups hit hardest were those whose metabolisms could least tolerate warm, poorly oxygenated water. Such conditions prevailed throughout much of the world’s oceans as the Great Dying unfolded, caused by a surge of volcanic activity that released gargantuan amounts of planet-warming gases like carbon dioxide and methane into the atmosphere.
With this study, we essentially wanted to solve the mystery of why, when you go to the beach, you collect the shells of clams and snails rather than those of brachiopods. Our findings show that, across different organism groups, extinctions happened at much higher rates for those more vulnerable to increases in water temperature and decreases in oxygen availability.
Jose Andres Marquez, lead author
Department of Earth & Planetary Sciences
Doerr School of Sustainability
Stanford University
Stanford, CA. USA.
Representative samples of the modern fauna (left three samples) and the Paleozoic fauna (right four samples).
Image credit: Sarah Leibovitz.
The findings serve as a warning of sorts. Conditions preceding the extinction event are very similar to the climate of the past tens of millions of years, which is being altered by emissions from burning fossil fuels and other human activities.
This study is really the final nail in the coffin for what caused the Permian–Triassic mass extinction. The biggest mass extinction of all time started from a world that is very similar to today in having a relatively cool, relatively well-oxygenated ocean, and then there was a giant injection of carbon dioxide into the Earth system. Understanding how Earth and Earth’s biota responded back then could inform us of what’s to come.
Erik A. Sperling, senior author.
Department of Earth & Planetary Sciences
Doerr School of Sustainability
Stanford University
Stanford, CA. USA.
Ancient vs. modern metabolisms
Metabolism refers to all the chemical processes happening inside an organism’s body to obtain energy and sustain life. During the Paleozoic period, which ended with the Great Dying, much of the oceanic life consisted of slow-metabolizing, bottom-dwelling, mostly immobile, filter-feeding animals such as brachiopods, crinoids (sea lilies, related to starfish), and certain corals and sea anemones.
In contrast, animal groups that persisted after the Paleozoic display greater mobility and predatory behavior, requiring faster metabolisms. These more modern ocean creatures include fish – obvious frequent, fast movers – as well as slow but mobile snails, sea urchins, and bivalves, such as clams, oysters, and mussels.
Compared to brachiopods, bivalves possess much faster metabolisms and greater energy needs because they often have bulkier bodies and muscular “foot” extensions to dig and crawl.
This is why we eat clam chowder and we don’t eat brachiopod chowder. Brachiopods have almost no meat.
Erik A. Sperling.
Prior to the Great Dying, brachiopods outnumbered bivalves. Nowadays, only around 400 brachiopod species still exist, compared to about 10,000-15,000 bivalve species. Sperling said:[ …this dramatic turnover compares to the extinction of the non-avian dinosaurs 65 million years ago during what is probably the most famous mass extinction,] where mammals essentially took over and never gave up that niche to reptiles again.
Erik A. Sperling.
Worldwide patterns of extinction
The new research builds on a 2018 study led by researchers at Princeton and Stanford – including Sperling and Jon Payne, also a co-author of the new study – that found evidence indicating oxygen loss and warming in Earth’s oceans were the primary cause for the Great Dying. However, the physiological data in that study came only from modern ocean species measured by other scientists, skewing the results toward economically important fish and crustaceans versus the kinds of animals that went extinct at higher rates during the mass die-off.
In our new study, we filled in this gap about the physiology of the Paleozoic fauna to see if we could explain not only the biogeography of the extinction but the taxonomic selectivity of the extinction.
Erik A. Sperling.
Fieldwork to gather information on impacted organismal groups took place over the years since the earlier study, including in the San Juan Islands of Washington state, where brachiopods are still common. The researchers collected a diverse set of ocean animal groups representative of those that dominated oceans before and after the Great Dying. They performed experiments at field stations and in Sperling’s lab at Stanford to monitor organisms’ oxygen use in a chamber and how that usage changed with water temperature. As temperature rises, animals’ metabolic rates increase as the extra energy makes reactions occur faster, and they require more oxygen.
The lab work showed that the Paleozoic fauna can live in water with less oxygen, under conditions that would asphyxiate ocean animals from the modern groups. But when the temperature increases, the Paleozoic fauna’s slow metabolisms cannot keep pace and their oxygen needs increase much faster than modern fauna’s. This outcome is ultimately related to their different body plans – the more active and athletic modern fauna require more oxygen at a minimum, but when oxygen requirements rise (as during warming), they have the muscles and gills to match.
Sea urchins in respirometry chambers, which monitor oxygen use (changes in metabolism) as water temperature increases.Image credit: Murray Duncan.
Warming and oxygen loss are the key drivers.
Erik A. Sperling.
Other research has strongly implicated ocean acidification as well, whereby reactions with atmospheric carbon dioxide render ocean water more acidic, making it tougher for organisms to grow their shells. However, while the new findings suggest acidification may have contributed to the extinction, it was nowhere near the most devastating factor, Sperling added.
Warming today
The Stanford researchers plan to examine more marine animal groups to further understand the intertwined impacts of the three stressors of warming, lack of oxygen, and acidification, which are growing in severity today.
The researchers emphasize that history could well repeat itself, as changing ocean conditions threaten modern species that are vulnerable to warmer, oxygen-depleted waters.The bad news is, we are on track for Permian-Triassic levels of warming in worst-case scenario projections. But the good news is, we’re still at the point where we can change things and do something about it.”
Erik A. Sperling.
Temperatures increased 8-12° Celsius over thousands of years to cause the Great Dying, and today, over just 100-200 years, temperatures are projected to be 1.5-4° Celsius warmer than pre-industrial times by 2100.
Publication:
The lesson from the Great Dying is not that life was protected by some benevolent force, but that survival depended on accidents of evolutionary history. The molluscs that endured were not designed in advance for a catastrophe 252 million years in the future. They survived because adaptations that had evolved for movement and active feeding happened also to provide greater capacity to obtain and distribute oxygen when the oceans became warmer and increasingly depleted of it.
Brachiopods and crinoids, by contrast, had flourished for hundreds of millions of years in the conditions to which they were adapted. Their extinction was not evidence of inferiority, still less of divine judgement. When the environment changed beyond their physiological limits, the very traits that had served them well became liabilities. Evolution does not plan for future disasters; it modifies what already exists in response to the conditions prevailing at the time.
Nor does this history support the creationist fantasy of a planet carefully fine-tuned for life. Earth’s systems can sustain rich and diverse ecosystems, but they can also be driven into states in which much of that life becomes impossible. The end-Permian extinction was not a minor adjustment to a perfect world. It was a planetary catastrophe in which most marine species vanished because the physical environment changed faster than their populations could adapt.
The survivors did not inherit the Earth because they had been specially favoured. They inherited it because, by chance, their evolutionary legacy gave them a little more physiological room for manoeuvre when the crisis came. The fossil record reveals no guiding intelligence, only evolution without foresight on a dangerously unstable planet — exactly what creationism cannot explain and science can.
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