Can our bacteria and virus friends save us? The rise of psychobiotic therapies for the human holobiont

 

The effect of the gut microbiota on the brain in the human holobiont is an incredibly complex story. It is described in a review appeared in 2019 on the "Physiological Reviews" journal. Not so much a review as a whole treatise, it is huge, with 1694 references in the bibliography!!! You can find a more readable summari on the blog "gut microbiota for health"

Before going on, a note of caution: as it is the rule nowadays, most of what appears in the medical literature is biased or simply false as the result of the widespread corruption of the medical research system. This review has been partly sponsored by the pharmaceutical industry, nevertheless it seems reasonably free of hype for specific treatments or wonder drugs. Its approach is correctly evolutionary, for instance when they say:

"Given that there has never been a time when mammals existed without microbes (apart from under highly restrictive laboratory conditions), there has also never been a time when the brain has been without signals from the gut, and it is important to consider the relationship between the host and its microbiota from an evolutionary perspective"

And they have it perfectly right when they use the magic word "holobiont"!!!

"The hologenome theory may even account for complex biological phenomena such as certain behaviors. For instance, behavior that facilitates social interaction among holobionts might be considered evolutionarily adaptive/advantageous as it gives rise to greater transmission of microbiota, thereby enhancing genetic variation (1285, 1286, 1689). In light of these inextricable links between the microbiota and the brain throughout evolutionary history, it is imperative for the study of our own biology (and that of the entire animal kingdom) to understand how microbial symbionts influence brain physiology and behavior."

The main point of the paper is that the human brain is strongly influenced by the gut, that our behavior, to the point that modifying the gut composition can be seen as a form of "psychobiotic therapy" that improves plenty of pathological situations and improves also the quality of life, for instance helping against depression. 

Seeing how the world is behaving nowadays, it would seem that the human microbiome is in bad conditions, indeed. Especially the gut of our leaders seems to have been invaded by micro-monsters instead of the beneficial gut flora that's normal for humans. And, surely, the various habits of hyper-cleaning, distancing, and self-suffocation that became fashionable during the past two years didn't help in improving the situation. Maybe, at this point, only our bacterial and viral friends can help us (with a little support also from our friendly archaea and fungi). Go, friends, go! We need you badly! 

The epidemic of obesity keeps getting worse. What's a good holobiont supposed to do?

 

The obesity epidemic keeps expanding. The above are, I believe, the most recent data available for the US. The COVID-19 lockdowns and isolation measures are reported having made things even worse. This trend is simply horrendous: what the heck is happening to humankind? (Disclaimer: I am not a nutritionist, I am just someone who is fascinated by data and trends. And, of course, we are all interested in our health! Here, I report some data I found, hoping you may find them useful. Don't take them as the last word on the subject. As always, before acting on things that affect your health, do your own search and use your judgement about what works for you.)

The obesity epidemics had a considerable boost by the lockdowns during the Covid-19 pandemic. Coupled with the opposite effect, that obesity is a risk factor for people who contract Covid, you have a remarkable disaster in the making. With several Western countries having percentages of obese people close to or higher than 50%, one wonders what's going to happen in the future. Why are the human holobionts in such a poor shape?

The story is complicated, and I don't pretend to say anything new. I just want to attract your attention to some recent studies that I think shed some light on the mechanism of human obesity (but even our fellow dog holobionts are suffering from obesity). 

First, the work by Raubenheimer and Simpson on the food preference of various animals, summarized in a recent book titled, "Eat like the Animals." (Mariner Books, 2021). Their discovery is easy to summarize: it seems that most living beings have a specific set point in their needs for the main nutrients. They seek for a specific balance among proteins, fats, and carbohydrates. In particular, they aim at a minimum intake of protein. If animals are fed an unbalanced diet, for instance, poor in protein, they will tend to eat more food until they reach the right level. Raubenheimer and Simpson call this the "protein leverage hypothesis:" 

"In a protein-poor but energy-rich food environment, humans will overeat carbs and fats to try to reach their protein target. However, when the only available diet is rich in protein, human will underconsume carbs and fats"

Since excess carbohydrates are stored in the body as fat, we can say that one of the causes of the obesity pandemic is that the human diet in Western countries is overstocked in carbohydrates. 

Here comes Robert Lustig and his book "Metabolical" (Yellow Kite 2021) where he minces no words on how this is not only true but also a profitable strategy for the food industry. They discovered long ago that if they put more and more carbohydrates (sugars) in the food they sell, then people will get fat, they will eat more, and that will increase their profits. Just like sick people are a boon for medical doctors, obese people are a boon for food producers. 

You don't believe that? Let me show you a picture I took a few days ago in an Italian supermarket:

There are four kinds of regular mayonnaise on sale, plus a fancy one with no eggs. Can you guess which is the only one that does not contain added carbohydrates? Let me tell you, it is the most expensive one among the regular ones. All the others contain sugar. Maybe it is not the same for all mayonnaise brands on the market, but I think it is significant. Food companies do add sugar everywhere, even when it is not called for by the traditional recipes. They deny that, but it is written on the list of the ingredients (I have pictures, if you don't believe me!)

Now, it may well be that there is much more to obesity than just carbohydrates, but I think that these results point at an important cause of the problem. There are data showing that what we are seeing may be a delayed effect of "peak sugar" that occurred around the year 2000. From then on, the amount of sugar consumed in the U.S. has been going slightly down. But it remains high. 

The beauty of this is that, if it is true, with obesity we don't have such a wicked problem as others, say, global warming. We know that to avoid global warming, we should stop burning hydrocarbons, but it is also true that we can't just stop: billions of people would die. But we could stop, or at least strongly reduce, the extra carbohydrates added to processed food, and we could do it today. Nobody would die, but the problem would be eased and many people would be healthier! But this is the way things are in the world: no problem can ever be solved when there is somebody making money if it remains unsolved. 

To make you happier, let me show you some data that tell us that a little excess weight (a little!) is not necessarily bad for your organism. Here are some data from Malcolm Kendrick's wonderful book "The Clot Thickens" (Columbus 2021). 

BMI stands for "Body Mass Index" and the overall lowest risk of death is for a BMI of 25-30 that's normally classified as "overweight" (if you want to know, I am at BMI=27). Being underweight is a larger risk than being obese! But obesity has many other problems, not least in terms of self-esteem. 

In the end, remember that you are a holobiont and that for hundreds of millions of years your holobiont ancestors never ate anything that was processed in an industrial plant. You are a fine-tuned machine that includes trillions of friendly viruses and bacteria living in your guts. They want a balanced diet of fats, protein, fiber, and not too much in terms of carbohydrates (but you need them, too!). Try to make them happy, and you'll be happier, too!

Gaia's One Billion Years Task: Colonizing the Land

 

Gaia as the sea Goddess Grammamare according to Hayao Miyazaki's interpretation in the film "Ponyo"

Imagine a time machine that brings you back to the Earth of one billion years ago, right in the middle of the eon called the "Proterozoic." First of all, you need an oxygen respirator, otherwise you'll die of suffocation in a few minutes. You also need a wide-brimmed hat and an outfit that covers your limbs in such a way as to protect your skin from the ultraviolet radiation. It is your planet, but in this period it is not especially friendly to a metazoan as you are.

You walk a few cautious steps onward. In front of you, the blue sea. You turn around: an expanse of dry rocks that continues all the way to the horizon. No traces of anything green that you can see: no plants, no insects, no birds, nothing like that. Above you, the sun is bright in the blue sky. You notice that it is a little less bright than you are used to seeing it, in your time. No traces of clouds: it is what you expected: no trees means no evapotranspiration of water vapor, no volatile organic compounds to function as nucleation sites for the water droplets that form clouds. 

You walk toward the sea. There are mainly rocks, but also some sandy places: small patches of beach. If there is a beach, there has to be a river, somewhere, that created it. You see it, not far away. It is completely dry, its bed going straight through the rocky landscape from the hills in the distance. Rains, when they arrive, must be torrential downpours that come and go quickly. 

You kneel on the beach, in front of the sea, lifting some water with your cupped hands. You know that it should be less salty than the seawater you are used to in your time, and you are tempted to taste it to confirm. But that is not a good idea. That water is brimming with microorganisms, most of them unlike anything your immune system is used to. You drop the water on the surface of a rock, where it forms a dark spot that rapidly evaporates and disappears. 

Standing up in front of that alien sea, you look at the gentle waves coming and going. You know that there are no fish in there. No crabs, no seashells, no seaweed, nothing like that. But there are enormous numbers of microorganisms. They are photosynthesizing, eating each other, reproducing by splitting themselves in two. They can live only in water. Is there life on the dry rocks on the shore? Maybe some of those microscopic creatures survive there, maybe even thrive, perhaps algae or even ancestors of modern lichens. But they are just eking out a precarious existence. They are invisible to the naked eye, and their time has not come yet.

On the horizon, an enormous orange moon rises as the sun slowly fades on the opposite side. You keep looking at the dark waters in front of you. Just under the surface, you glimpse something that looks like a pair of large eyes. You think you see her just for a moment, Gaia in her form of sea goddess, languidly swimming in the calm sea. 

____________________________________________________

Back to your time machine. You dial 350 million years before your time, the start of the Carboniferous Period. You press the button. 

You emerge out of the machine, breathing the fresh air, smelling something you had never smelled before. Whatever it is, the air is humid, rich in oxygen. You are in a small clearing, in front of you, there is a pond surrounded by a lush forest. Trees, tall trees, forming a full canopy under the low clouds, swept by a gentle wind. The place is eerily silent: no birds, no insects, nothing like that. Yet, you recognize the place: this is your planet, Earth, not yet the way it will be in the future that is your time, but a familiar world. 

As you stand, a noise comes to you: a buzz. You see something flying away, an insect of some kind. It starts raining. It is a warm, gentle downpour that wets you rapidly, but ends quickly. It has been enough to disturb the creatures living under the low bushes. You have a glimpse of them scuttling away: tetrapods, early amphibians. They jump into the water of the pond and then disappear. They are your ancestors, the ancestors of all the metazoans that will move on land in the future that's your time. 

As you walk, splashing your boots on the mud, you wonder how Gaia pulled this incredible trick: transforming the bare rock of entire continents into lush forests. While you think that, you have a glimpse of a pair of bright eyes staring at you from the canopy. You look up, and they disappear, leaving only a Cheshire-cat smile of the Goddess of the Forests, then she vanishes among the branches.

Images of the Goddess courtesy of "Mon Seul Desir"

Good Advice for Holobionts

 

h/t Ilargi Meyer

The Great Cycle of Earth's Forests

 

 Forests appeared on Earth some 400 million years ago, and they have been thriving over that long period. But, during the past 150 million years, they started to show signs of distress, reacting to the decline in atmospheric CO2 concentrations and to the competition with grasslands. As Earth changes, will forests be able to cope and survive? It is an extremely slow trend, but we cannot rule out that forests will conclude their cycle and disappear in a geologically short time. This text is an attempt to reconstruct the story of forests and to imagine what their future could be in deep time. (image courtesy of Chuck Pezeshky) 

A forest is a magnificent, structured, and functional entity where the individual elements -- trees -- work together to ensure the survival of the ensemble. Each tree pumps water and nutrients all the way to the crown by the mechanism called evapotranspiration. The condensation of the evaporated water triggers the phenomenon called the "biotic pump" that benefits all the trees by pumping water from the sea. Each tree pumps down the carbohydrates it manufactures using photosynthesis to its mycorrhizal space, the underground system of roots and fungi that extracts mineral nutrients for the tree. The whole "rhizosphere" -- the root space -- forms a giant brain-like network that connects the trees to each other, sometimes termed "the Wood Wide Web." It is an optimized environment where almost everything is recycled. We can see it as similar to the concept of "just in time manufacturing" in the human economy. 

Forests are wonderful biological machines, but they are also easily destroyed by fires and attacks by parasites. And forests have a competitor: grass, a plant that tends to replace them whenever it has a chance to. Areas called savannas are mainly grass, although they host some trees. But they don't have a closed canopy, they don't evapotranspirate so much as forests, and they tend to exist in much drier climate conditions. Forests and grasslands are engaged in a struggle that may have started about 150 million years ago when grass appeared for the first time. During the past few million years, grasses seem to have gained an edge in the competition, in large part exploiting their higher efficiency in photosynthesis (the "C4" pathway) in a system where plants are starved for CO2.

Another competitor of forests is a primate that left its ancestral forest home just a couple of million years ago to become a savanna dweller -- we may call it the "savanna monkey," although it is also known as "Homo," or "Homo sapiens." These monkeys are clever creatures that seem to be engaged mainly in razing forests to the ground. Yet, in the long run, they may be doing forests a favor by returning the atmospheric CO2 concentration to values more congenial to the old "C3" photosynthetic mechanism still used by trees. 

Seen along the eons, we have an extremely complex and fascinating story. If forests have dominated Earth's landscape for hundreds of millions of years, one day they may disappear as Gaia gets old. In this post, I am describing this story from a "systemic" viewpoint -- that is, emphasizing the interactions of the elements of the system in a long-term view (it is called also "deep time"). The post is written in a light mood, as I hope to be able to convey the fascination of the story also to people who are not scientists. I tried to do my best to interpret the current knowledge, I apologize in advance for the unavoidable omissions and mistakes in such a complex matter, and I hope you'll enjoy this post. 

The Origin of Forests: 400 million years ago

Life on Earth may be almost 4 billion years old but, since we are multicellular animals, we pay special attention to multicellular life. So, we tend to focus on the Cambrian period (542-488 million years ago), when multicellular creatures became common. But that spectacular explosion of life was all about marine animals. Plants started colonizing the land only during the period that followed the Cambrian, the Ordovician, (485 - 443 million years ago). 

To be sure, the Ordovician flora on land was far from impressive. As far as we know, it was formed only by moss (perhaps lichens, too, but it is not certain). Mosses are humble plants: they are not vascularized, they don't grow tall, and they surely can't compare with trees. Nevertheless, mosses could change the planetary albedo and perhaps contribute to the fertilization of the marine biota -- something that may be related to the spectacular ice ages of the Ordovician. It is a characteristic of the Earth system that the temperature of the atmosphere is related to the abundance of life. More life draws down atmospheric CO2, and that cools the planet. The Ordovician saw one of these periodic episodes of cooling with the start of the colonization of the land. (image from Wikipedia)

There followed another long period called the "Silurian" (444 – 419 My ago) when plants kept evolving but still remained of the size of small shrubs at most. Then, during the Devonian (419 -359 million years ago) we have evidence of the existence of wood. And not only that, the fossil record shows the kind of channels called "Xylem" that connect the roots to the leaves in a tree. These plants were already tall and had a crown, a trunk, and roots. By the following geological period, the Carboniferous (359 - 299 My ago), forests seem to have been widespread.  

A major feature of these ancient trees was the development of an association with fungi. Their roots formed what we call a "mycorrhizal" symbiotic system. The fungi receive carbohydrates that the tree manufactures using photosynthesis, while the tree receives from the fungi essential minerals, including nitrogen and phosphorous. We don't know the details of how this symbiotic relationship evolved over hundreds of millions of years but, below, you can see a hypothesis of how it could have happened. (Source) (in the figure, "AM" stands for "arbuscular mycorrhiza" - the oldest form of symbiotic fungi).

Another major evolutionary innovation that may have been already operating in the Paleozoic forests is the "biotic pump." As an effect of the pressure drop created by the condensation of evapotranspirated water, forests can create pump water vapor from the ocean and create the "atmospheric rivers" that bring water inland. That, in turn, creates the land rivers that bring that water back to the sea. As forests create their own climate, they can expand nearly everywhere. The image shows clouds created by condensation over the modern Amazon rainforest (source).  

If we could walk in one of those ancient forests, we would find the place familiar, but also a little dreary. No birds and not even flying insects, they evolved only tens of million years later. No tree-climbing animals: no monkeys, no squirrels, nothing like that. Even in terms of herbivores, we have no evidence of the kind of creatures we are used to, nowadays. Grass didn't exist, so grazers couldn't exist either. Herbivores were browsers surviving on leaves or on decaying plant matter. Lots of greenery but no flowers, they had not evolved yet. You see in the image (source) an impression of what an ancient forest of Cladoxylopsida could have looked like during the Paleozoic era.

The Paleozoic forests already had one of the characteristics of modern forests: fires. There had never been fires on Earth before for at least two good reasons: one was that there was not enough oxygen, and the other was that there was nothing flammable. But now, with the oxygen concentration increasing and plants colonizing the land, fires appeared, lighting up the night. They would remain a characteristic of the land biosphere for hundreds of millions of years.

Image Source. The "fire window" is the region of concentrations in atmospheric oxygen in which fires can occur. Note how during the Paleozoic, the concentration could be considerably larger than it is now. Fireworks aplenty, probably. Note also how there exist traces of fires even before the development of full-fledge trees, in the Devonian. Wood didn't exist at that time, but the concentration of oxygen may have been high enough to set other kinds of dry organic matter on fire. 

Wildfires are a classic case of a self-regulating system. The oxygen stock in the atmosphere is replenished by plant photosynthesis but is removed by burning wood. So, fires tend to reduce the oxygen concentration and that makes fires more difficult. But the story is more complicated than that. Fires also tend to create "recalcitrant" carbon compounds, charcoal for instance, that are not recycled by the biosphere and tend to remain buried for long times -- almost forever. So, over very long periods, fires tend to increase the oxygen concentration in the atmosphere by removing CO2 from it. The conclusion is that fires both decrease and increase the oxygen concentration. How about that for a taste of how complicated the biosphere processes are? 

 The Mesozoic: Forests and Dinosaurs

At the end of the Paleozoic, some 252 million years ago, there came the great destruction. A gigantic volcanic eruption of the kind we call "large igneous province" (sometimes affectionately "LIP") took place in the region we call Siberia today. It was huge beyond imagination: think of an area as large as modern Europe becoming a lake of molten lava. (image source)

It spewed enormous amounts of carbon into the atmosphere in the form of greenhouse gases. That warmed the planet, so much that it almost sterilized the biosphere. It was not the first, but it was the largest mass extinction of the Phanerozoic age. Gaia is normally busy keeping Earth's climate stable, but sometimes she seems to be sleeping at the wheel -- or maybe she gets drunk or stoned. The result is one of these disasters.  

Yet, the ecosystem survived the great extinction and rebounded. It was now the turn of the Mesozoic era, with forests re-colonizing the land. Over time, the angiosperms ("flowering plants") become dominant over the earlier conifers. With flowers, forests may have been much noisier than before, with bees and all kinds of insects. Avian dinosaurs also appeared. They seem to have been living mostly on trees, just like modern birds. 

For a long period during the Mesozoic, the landscape must have been mainly forested. No evidence of grass being common, although smaller plants, ferns, for instance, were abundant. Nevertheless, the great evolution machine kept moving. During the Jurassic, a new kind of mycorrhiza system evolved, the "Ectomycorrhizae" which allowed better control of the mineral nutrients in the rhizosphere, avoiding losses when the plants were not active. This mechanism was typical of conifers that could colonize cold regions of the supercontinent of the time, the "Pangea."  

During the Mesozoic, the dinosaurs appeared and diffused all over the planet. You surely noted how the Jurassic dinosaurs were often bipedal (See the illustration showing an early form of Iguanodon). They are also called "ornithopods," it is a body plan that allows herbivorous creatures to browse on leaves on the high branches of trees. A bipedal stance makes the creature able to stand up, balancing on its tail, reaching higher heights. Some dinosaurs chose a different strategy, developing very long necks for the same purpose: the brontosaurus is iconic in this sense even though, traditionally, it was shown half-submerged in swamps (the illustration is from the New York Tribune of 1919). The idea that brontosaurs lived mainly in swamps is not so bright, if you think about that. Why should a semiaquatic creature need a long neck? Think of a hippo with the neck of a giraffe: it wouldn't work so well. 

A much better representation of long-necked dinosaurs came with the first episode of the "Jurassic Park" (1993) movie series when a gigantic diplodocus eats leaves. At some moment, the beast rises on its hind legs, using the tail as further support. 

If you are a dinosaur lover (and you probably are if you are reading this post) seeing this scene must have been a special moment in your life. And, after having seen it maybe a hundred times, it still moves me. But note how the diplodocus is shown in a grassy environment with sparse trees: a Savanna. That's not realistic because grass didn't exist yet when the creature went extinct at the end of the Jurassic period, about 145 million years ago. 

To see grass and grazers, animals specialized in eating it, we need to wait for the Cretaceous (145-66 million years ago). Evidence that some dinosaurs had started eating grass comes from the poop of long-necked dinosaurs. That's a little strange because, if you are a grazer, the last thing you need is a long neck. But new body plants rapidly evolved. The Ceratopsia were the first true grazers, also called "mega-herbivores". Heavy, four-legged beasts that lived their life keeping their head close to the ground. The Triceratopses gained a space in human fantasy as prototypical dinosaurs, and they are often shown in movies while fighting tyrannosauruses. You see that scene in Walt Disney's movie "Fantasia" (1940). It may have happened for real.

Note the heavy bone shield over the head. With so much weight on board, Trixie couldn't possibly rise on its hind legs to munch on leaves on tree branches. Note also the beak, it looks perfectly adapted for collecting grass. It means that the Cretaceous landscape was probably similar to our world. We don't know if there existed the kind of biome we call today "savanna" -- a mix of grass and trees, but surely the land was shared by forests and grass, each biome with its typical fauna. 

The Great Cooling and the Rise of C4 Grass

At the end of the Cretaceous period, 66 million years ago, a new large igneous province appeared in the Deccan region, in India. It generated another climate disaster with the associated mass extinction. Most dinosaurs were wiped out, except those we call "birds" today. A large meteorite also hit Earth at that time. It caused only minor damage but, millions of years later, it gave human filmmakers a subject to explore in many dramatic movies. 

In time, the Deccan LIP faded away, and the era that followed is called the "Cenozoic." The ecosystem recovered, forests re-colonized the land, and mammals and birds (the only survivors of the Dinosauria clade) fought to occupy the ecological niches left free by their old masters. The early Cenozoic was a warm period of lush forests that offered refuge to a variety of animals: birds made their nests in branches, while squirrels and other small mammals jumped from branch to branch, or lived at the bottom. It is during this period that primates evolved: the huge forests of those times offered refuge for a variety of species that had probably already developed sophisticated social behaviors.  

Grass also survived the end-Cretaceous catastrophe. As a result, some mammals evolved into new "megaherbivores" or "megafauna" that occupied the same ecological niche that the triceratopsides had colonized long before.  Here is a brontotherium, a large herbivorous mammal that lived some 37-35 million years ago, during the late Eocene period (image from BBC).

The megabeasts of the Cenozoic do not have the same fascination of the giant dinosaurs, but this creature has a nice-sounding name, and it looks a little like Shrek, the ogre of Spielberg's movie. Note how the beast is correctly shown walking on a grassy plain. The Eocene is supposed to have been mostly forested, but grass existed, too. The brontotherium was an opportunistic grazer, apparently able to subsist on various kinds of food, not just grass. 

During the warm phase of the Cenozoic, Earth reached a maximum temperature around 55 million years ago, some 8-12 deg C higher than today. The concentration of CO2, too, was large. That is called the "early Eocene climatic optimum". It doesn't mean that this period was better than other periods in terms of climate, but it seems that Earth was mainly covered with lush forests and that the biosphere thrived.  

Then, the atmosphere started cooling. It was a descent that culminated at the Eocene-Oligocene boundary, about 34 million years ago, with a new mass extinction. It was a relatively small event in comparison to other, more famous, mass extinctions, but still noticeable enough that the Swiss paleontologist Hans Georg Stehlin gave it the name of the "Grande Coupure" (the big break) in 1910. One of the victims was the Brontotherium -- too bad, it was a nice-looking beast. 

Unlike other cases, the extinction at the Grande Coupure was not correlated to the warming created by a LIP, but to rapid cooling. You see the "step" in temperature decline in the figure. 

Why the big cooling? The answer is not completely known. Surely, cooling was correlated to a decline in the CO2 content in the atmosphere and that, in turn, may have been generated by the collision of the Indian plate with Eurasia. It was a gigantic geological event that generated the Himalayan mountain belt. It exposed huge amounts of fresh rock to the atmosphere, and the result was the removal of CO2 because of silicate erosion and weathering. 

The Himalaya hypothesis is one of those explanations that seem to make a lot of sense, but it has big problems. Another possible explanation is that Earth just outgassed less CO2 than before. The CO2 that plants need for their photosynthesis is generated mainly at the mid-oceanic ridges where the hot mantle (the molten rock layer below Earth's crust) outgasses it, as it has been doing for billions of years. It may well be that the mantle is getting a little colder over the eons, so it outgasses less CO2 than before. It may be true, but it seems to be a weak effect -- not enough to explain the CO2 decline of the Cenozoic.

In my opinion, the most likely hypothesis is that the CO2 concentration declined because of higher biological productivity not just on land, but also in the sea (as seems to be implied in a recent study )

In other words, the early Cenozoic may have been so booming with life of all kinds that it absorbed more CO2 from the atmosphere than the mantle could replace by outgassing. The result was the cooling phase. The abrupt step at the "Grande Coupure" may be related to the evolution of a specific life form: baleen whales, which changed the equilibria of the whole marine ecosystem, drawing down even more CO2 from the atmosphere.

This interpretation agrees with the fact that ice ages are often observed after LIPs. It may be one of the many cycles of the ecosphere. When a major LIP appears, the rise of CO2 is disastrous at the beginning but, in the long run, it gives the biosphere a chance to rebound and expand in a CO2 rich system.  Then, the rebound generates its own doom: the abundant biological productivity draws down CO2 from the atmosphere, cools the planet, and the system finds itself CO2-starved again. In this interpretation, the Eocene cooling and the Grande Coupure were long-term consequences of the Deccan LIP that had destroyed the dinosaurs, millions of years before. I hasten to note that this is just one of the several possible interpretations but, in my opinion, it makes a lot of sense.    

The Eocene cooling had profound effects on forests. First, the CO2 decline gave an advantage to those plants which utilized a more efficient photosynthesis mechanism called the "C4" pathway. Earlier on, the standard photosynthesis mechanism (called "C3") had evolved in an atmosphere rich in CO2. The C3 mechanism is efficient in processing carbon dioxide, but it is hampered by the opposite process called "photorespiration," which becomes important when the CO2 concentration is low. Using the C4 mechanism, plants can concentrate CO2 in the cells where photosynthesis occurs and avoid the losses by photorespiration. 

C4 plants appeared shortly after the Grande Coupure and diffused mainly in grasses, Trees, instead, didn't adopt the new mechanism. The explanation is subtle: photosynthesis needs water, and the process that goes on in leaves is strongly connected to the evapotranspiration mechanism. The C4 mechanism needs less water than the C3 one, so evapotranspiration is hampered. The result is that C4 trees -- if they exist -- cannot be as tall as the ordinary C3 ones, and so they are not favored by natural selection in forests. In an atmosphere of very low CO2, forests are disadvantaged because of the higher photosynthesis efficiency of grasses. 

During the period that followed the Grande Coupure, temperatures and CO2 concentrations remained stable, but at relatively low levels. The result was that many forests disappeared, replaced by grasslands and savannas. Herbivorous species evolved teeth more specialized for grazing and became "mega-herbivorous" species. The landscape must have become similar to the modern one, with patches of forests alternating with savannas. 

A typical savanna ecosystem: the Tarangire national park in Tanzania. (Image From Wikipedia). Compare with the forest image at the beginning of this post. 

Despite the expansion of savannas, rainforests continued to exist in the tropical regions. Conifer forests kept a foothold in the Northern regions, helped by their Ectomycorrhiza system that avoided the runoff of nutrients in winter. The boreal forest is also called "Taiga." 

Then, a new cooling phase started, apparently a continuation of the previous trend: cooling begets more cooling. It was the beginning of the "Pleistocene," a period of unstable climate with ice ages and interglacials following each other, triggered by small oscillations in solar irradiation caused by the characteristics of Earth's orbit. These oscillations are called "Milankovich Cycles" -- they are not the cause of the ice ages, just triggers. (Image Source).

The oscillations are caused by ice having a built-in albedo feedback so that the more ice expands, the more sunlight is directly reflected into space. That causes the temperature to decline and ice to expand even more. Taken to its extreme consequences, this mechanism may lead to the "Snowball Earth" condition, with ice covering the whole planet's surface. It may have happened for real during the "Cryogenian" period, some 600 million years ago. Fortunately, there were mechanisms able to re-heat Earth and return it to the conditions we consider "normal." 

During the Pleistocene, the CO2 concentration in Earth's atmosphere plunged to very low levels, especially during the glacial periods, when it reached levels as low as around 150 parts per million (ppm). Earth may have inched close to a new snowball Earth but, fortunately, that didn't happen. In part, it may be because the sun, today, is about 5% hotter than it was during the Cryogenian. But we will never know how close Gaia got to freeze to death. 

During the Pleistocene, the advancing ice sheets swept away all plants, but even in non-glaciated areas, forests suffered badly.  Tropical rainforests didn't disappear, but they were much reduced in extension. In the North, most of the Eurasian boreal forests were replaced by the "mammoth steppe," a huge area that went from Spain to Kamchatka. where mammoths and other mega-herbivores roamed. 

It is not impossible that an ice age colder than the Pleistocene average could have led to the eventual extinction of the forests, completely replaced by grasses. But that didn't happen, and things were going to change again with the appearance of the Savanna Monkeys -- a completely new species that came to dominate the ecosystem. 

The rise of the Savanna Monkeys

Primates are arboreal creatures that evolved in the warm environment of the Eocene forests. They used tree branches as a refuge, and they could adapt to various kinds of food. Modern primates do not shy from hunting other species, maybe even ancient primates did the same. From the viewpoint of these ancient primates, the shrinking of the area occupied by tropical forests that started with the "Grande Coupure," some 30 million years ago, was a disaster. They were not equipped to live in savannas: they were slow on the ground: an easy lunch for the powerful predators of the time. Primates also never colonized the northern taiga. Most likely, it was not because they couldn't live in cold environments (some modern monkeys can do that), but because they couldn't cross the "mammoth steppe" that separated tropical forests from the Northern forests. If some of them tried, the local carnivores made sure that they didn't succeed. So, "boreal monkeys" do not exist (actually, there is one, shown in the picture, but it is not exactly a monkey!). 

Nevertheless, eventually, monkeys were forced to move into the savanna. During the Pleistocene, about 4 million years ago, the Australopithecines appeared in Africa, (image source). We may call them the first "savanna monkeys." In parallel, perhaps some time later, another kind of savanna monkey, the baboon, also evolved in Africa. In the beginning, australopithecines and baboons were probably practicing similar living techniques, but in time they developed into very different species. The baboons still exist today as a rugged and adaptable species that, however, never developed the special characteristics of australopithecines that turned them into a very different kind of animals. The first creatures that we classify as belonging to the genus Homo, the homo habilis, appeared some 2.8 million years ago. They were also savanna dwellers.

This branch of savanna monkeys won the game of survival by means of a series of evolutionary innovations. They increased their body size for better defense, they developed an erect stance to have a longer field of view, they super-charged their metabolism by getting rid of their body hair and using profuse sweating for cooling, they developed complex languages to create social groups for defense against predators, and they learned how to make stone tools adaptable to different situations. Finally, they developed a tool that no animal on Earth had mastered before: fire. Over a few hundred thousand years, they spread all over the world from their initial base in a small area of Central Africa. The savanna monkeys, now called "Homo sapiens," were a stunning evolutionary success. The consequences on the ecosystem were enormous.

First, the savanna monkeys exterminated most of the megafauna. The only large mammals that survived the onslaught were those living in Africa, where they had the time to adapt to the new predator. For instance, the large ears of the African elephant are a cooling system destined to make elephants able to cope with the incredible stamina of human hunters. But in Eurasia, North America, and Australia, the arrival of the newcomers was so fast and so unexpected that most of the large animals were wiped out. 

By eliminating the megaherbivores, the monkeys had, theoretically, given a hand to the competitors of grass, forests, which now had an easier time encroaching on grassland without seeing their saplings trampled. But the savanna monkeys had also taken the role of megaherbivores. They used fires with great efficiency to clear forests to make space for the game they hunted. In the book "1491" Charles Mann reports (. p 286) how "rather than domesticating animals for meat, Indians retooled ecosystems to encourage elk, deer, and bear. Constant burning of undergrowth increased the number of herbivores, the predators that fed on them, and the people who ate them both"  

Later, as they developed metallurgy, the monkeys were able to cut down entire forests to make space for the cultivation of the grass species that they had domesticated meanwhile: wheat, rice, maize, oath, and many others. 

But the savanna monkeys were not necessarily enemies of the forests. In parallel to agriculture, they also managed entire forests as food sources. The story of the chestnut forests of North America is nearly forgotten today but, about one century ago, the forests of the region were largely formed of chestnut trees planted by Native Americans as a source of food (image source). By the start of the 20th century, the chestnut forest was devastated by the "chestnut blight," a fungal disease that came from China. It is said that some 3-4 billion chestnut trees were destroyed and, now, the chestnut forest doesn't exist anymore. The American chestnut forest is not the only example of a forest managed, or even created, by humans. Even the Amazon rainforest, sometimes considered an example of a "natural" forest, shows evidence of having been managed by the Amazonian Natives in the past as a source of food and other products. 

The action of the savanna monkeys was always massive and, in most cases, it ended in disaster. Even the oceans were not safe from the monkeys: they nearly managed to exterminate the baleen whales, turning large areas of the oceans into deserts. On land, entire forests were razed to the ground. Desertification ensued, brought upon by "megadroughts" when the rain cycle was no more controlled by the forests. Even when the monkeys spared a forest, they often turned it into a monoculture, subjected to be destroyed by pests, as the case of the American chestnuts shows. Yet, in a certain sense, the monkeys were making a favor to forests. Despite the huge losses to saws and hatchets, they never succeeded in completely exterminating a tree species, although some are critically endangered nowadays. 

The most important action of the monkeys was their habit of burning sedimented carbon species that had been removed from the ecosphere long before. The monkeys call these carbon species "fossil fuels" and they have been going on an incredible burning bonanza using the energy stored in this ancient carbon without the need of going through the need of the slow and laborious photosynthesis process. In so doing, they raised the concentration of CO2 in the atmosphere to levels that had not been seen for tens of millions of years before. That was welcome food for the trees, which are now rebounding from their former distress during the Pleistocene and reconquering the lands they had lost to grass. In the North of Eurasia, the Taiga is expanding and gradually eliminating the old mammoth steppe. Areas that today are deserts are likely to become green. We are already seeing the trend in the Sahara desert. 

What the savanna monkeys could do was probably a surprise for Gaia herself, who must be now scratching her head and wondering what has happened to her beloved Earth. And what's going to happen, now?  

The New Large Igneous Province made by Monkeys

The giant volcanic eruptions called LIPs tend to appear with periodicities of the order of tens or hundreds of million years. But nobody can predict a LIP and, instead, the savanna monkeys engaged in the remarkable feat of creating a LIP-equivalent by burning huge amounts of organic ("fossil") carbon that had sedimented underground over tens or hundreds of millions of years of biological activity. 

It is remarkable how rapid the monkey LIP (MLIP) has been. Geological LIPS typically span millions of years. The MLIP went through its cycle in a few hundreds of years. It will be over when the concentration of fossil carbon stored in the crust will become too low to self-sustain the combustion with atmospheric oxygen. Just like all fires, the great fire of fossil carbon will end when it runs out of fuel, probably in less than a century from now. Even in such a short time, the concentration of CO2 is likely to reach, and perhaps exceed, levels never seen after the Eocene, some 50 million years ago. It is not impossible that it could reach more than 1000 parts per million. 

There is always the possibility that such a high carbon concentration in the atmosphere will push Earth over the edge of stability and kill Gaia by overheating the planet. But that's not a very interesting scenario, so let's examine the possibility that the biosphere will survive the carbon pulse. What's going to happen to the ecosphere?

The Savanna Monkeys are likely to be the first victims of the CO2 pulse that they themselves generated. Without the fossil fuels they had come to rely on, their numbers are going to decline very rapidly. From the incredible number of 8 billion individuals, they are going to return to levels typical of their early savanna ancestors: maybe just a few tens of thousands, quite possibly they'll go extinct. In any case, they will hardly be able to keep their habit of razing down entire forests. Without monkeys engaged in the cutting business and with high concentrations of CO2, forests are advantaged over savannas, and they are likely to recolonize the land, and we are going to see again a lush, forested planet (arboreal monkeys will probably survive and thrive). Nevertheless, savannas will not disappear. They are part of the ecosystem, and new megaherbivores will evolve in a few hundreds of thousands of years. 

Over deep time, the great cycle of warming and cooling may restart after the monkey LIP, just as it does for geological LIPs. In a few million years, Earth may be seeing a new cooling cycle that will lead again to a Pleistocene-like series of ice ages. At that point, new savanna monkeys may evolve. They may restart their habit of exterminating the megafauna, burning forests, and building things in stone. But they won't have the same abundance of fossil fuel that the monkeys called "Homo sapiens" found when they emerged into the savannas. So, their impact on the ecosystem will be smaller, and they won't be able to create a new monkey-LIP. 

And then what? In deep time, the destiny of Earth is determined by the slowly increasing solar irradiation that is going, eventually, to eliminate the oxygen from the atmosphere and sterilize the biosphere, maybe in less than a billion years from now. So, we may be seeing more cycles of warming and cooling before Earth's ecosystem collapses. At that point, there will be no more forests, no more animals, and only single-celled life may persist. It has to be. Gaia, poor lady, is doing what she can to keep the biosphere alive, but she is not all-powerful. And not immortal, either. 

Nevertheless, the future is always full of surprises, and you should never underestimate how clever and resourceful Gaia is. Think of how she reacted to the CO2 starvation of the past few tens of millions of years. She came up with not just one, but two brand-new photosynthesis mechanisms designed to operate at low CO2 concentrations: the C4 mechanism typical of grasses, and another one called crassulacean acid metabolism (CAM). To say nothing about how the fungal-plant symbiosis in the rhizosphere has been evolving with new tricks and new mechanisms. You can't imagine what the old lady may concoct in her garage together with her Elf scientists (those who also work part-time for Santa Claus). 

Now, what if Gaia invents something even more radical in terms of photosynthesis? One possibility would be for trees to adopt the C4 mechanism and create new forests that would be more resilient against low CO2 concentrations. But we may think of even more radical innovations. How about a light fixation pathway that doesn't just work with less CO2, but that doesn't even need CO2? That would be nearly miraculous but, remarkably, that pathway exists. And it has been developed exactly by those savanna monkeys who have been tinkering -- and mainly ruining -- the ecosphere. 

The new photosynthetic pathway doesn't even use carbon molecules but does the trick with solid silicon (the monkeys call it "photovoltaics"). It stores solar energy as excited electrons that can be kept for a long time in the form of reduced metals or other chemical species. The creatures using this mechanism don't need carbon dioxide in the atmosphere, don't need water, they may get along even without oxygen. What the new creatures can do is hard to imagine for us (although we may try). In any case, Gaia is a tough lady, and she may survive much longer than we may imagine, even to a sun hot enough to torch the biosphere to cinders. Forests, too, are Gaia's creatures, and she is benevolent and merciful (not always, though), so she may keep them with her for a long, long time. (and, who knows, she may even spare the Savanna Monkeys from her wrath!). 

We may be savanna monkeys, but we remain awed by the majesty of forests. The image of a fantasy forest from Hayao Miyazaki's movie, "Mononoke no Hime" resonates a lot with us. But can you see the mistake in this image? What makes this forest not a real forest? 

__________________________

Note: You always write what you would like to read, and that's why I wrote this post. But, of course, this is a work in progress. I am tackling a subject so vast that I can't possibly hope to be sufficiently expert in all its facets to avoid errors, omissions, and wrong interpretations. Corrections from readers who are more expert than me are welcome! I would also like to thank Anastassia Makarieva for all she taught me about the biotic pump and about forests in general, and Mihail Voytehov for his comments about the rhizosphere. Of course, all mistakes in this text here are mine, not theirs.

Gaia in Red Tooth and Claw: do Ants Sacrifice Themselves to the Fungus God?

A Carpenter Ant attacked by Ophiocordyceps unilateralis. The fungus is reproducing by sprouting a fruiting body out of the ant's body. It is cruel and horrible, and yet fascinating. What's happening, exactly? Is this a sacrifice to the fungus God?

There are things in nature that are far from being the happy world of Disney's cartoons. I stumbled recently into the story of the "Zombie Fungus" and of how it captures ants, devouring them from inside. It is a story that has been known for a long time, discovered in 1859 by that Alfred Russel Wallace, who was the co-discoverer with Darwin of evolution by natural selection.

It is a classic example of Nature "in red tooth and claw" as Alfred Tennyson defined it in 1830. An exquisitely evil story:

"When the fungus infects a carpenter ant, it grows through the insect’s body, draining it of nutrients and hijacking its mind. Over the course of a week, it compels the ant to leave the safety of its nest and ascend a nearby plant stem. It stops the ant at a height of 25 centimeters—a zone with precisely the right temperature and humidity for the fungus to grow. It forces the ant to permanently lock its mandibles around a leaf. Eventually, it sends a long stalk through the ant’s head, growing into a bulbous capsule full of spores. And because the ant typically climbs a leaf that overhangs its colony’s foraging trails, the fungal spores rain down onto its sisters below, zombifying them in turn.

"So what we have here is a hostile takeover of a uniquely malevolent kind. Enemy forces invading a host’s body and using that body like a walkie-talkie to communicate with each other and influence the brain from afar. Hughes thinks the fungus might also exert more direct control over the ant’s muscles, literally controlling them “as a puppeteer controls as a marionette doll.”

Note, indeed, the cruelty of the procedure: the fungus does not touch the ant's brain. It only cuts all the communications the brain has with the muscles of the ant's body. We may imagine the poor creature watching in horror as its body is snatched away from its control and led to do things that no sane ant would ever do. The ultimate horror? Surely it has been the source of inspiration for many horror movies. So, is Gaia really such a bitch?

The answer, as usual, is nuanced. Gaia is not a Goddess -- she is a Daimona (Δαίμονα), a servant of the Almighty, just like all of us. She just happens to be the highest-ranking daimon ("holobiont," using a more modern term) on Earth. Holobionts are not necessarily cruel, but they are not necessarily benevolent and merciful, either.  

But by seeing the ant being devoured by the fungus as cruel, we are making the same mistake that Richard Dawkins made when he tried to explain in evolutionary terms why trees are as tall as they are. Trees, definitely, are not male primates -- as Dawkins is. And ants, despite much fictional characterization, are not minimalist versions of human factory workers. Of course, we shall never be able to know what an ant thinks, but we can say that it is not an "organism" in the same sense as a human being. An ant is not a creature for which we can define a genetic individuality. It is only an expression of the genotype of the ant colony it is part of. It is no more an individual than a red blood cell in our body is. For an ant colony, losing a few ants is nothing worse than for us losing a few drops of blood.  

If the ant is not an organism, then it has no obvious interest to develop a form of defense against fungal attacks. As is a sterile female and it wouldn't be able to pass this information to its descendants. It is the anthill that evolves, not single ants. Only the anthill can be seen as a full-fledged "organism" -- although it also has elements of the holobionts.

So, the term "zombification" is wrong in many respects. Mainly because what we are seeing is not a fungus-ant interaction. It is a fungus-anthill interaction. Only the anthill could develop forms of resistance against this kind of attack and pass them to its descendants. But, apparently, that was never a priority. Reports Merlin Sheldrake in his book "Entangled Life" that there are traces of this fungus affecting ants already more than 45 million years ago. If there had been an advantage for the anthill in evolving a defense against this fungus, there was plenty of time to do that.  

Indeed, when the zombie fungus attacks an ant, that's not an attack. It is a form of communication. In other words, it is not parasitism, it is symbiosis, probably of the mutualistic kind. The fungus and the anthill can be seen as a holobiont in themselves. The fungus communicates with the anthill by infecting a few ants and using them to reproduce itself. The anthill doesn't care about giving the fungus a few of its ants. It does that, surely, in exchange for useful information. The anthill-fungus interaction is much more complex and wide-ranging than the formation of the fruit body, the only thing we can observe from our macroscopic and remote viewpoint. We can only say that it is a conversation that must be significant for both organisms. Otherwise, they wouldn't have been engaged in it for 45 million years. Good holobionts form long-lasting relationships!

Yet, there remains a dark fascination in the event we can witness. A single ant moves away from the colony to reach a high place, from where she (a female worker), gives herself completely to the fungus in a sort of apotheosis that (excuse me for the blasphemy) reminds the Christian myth of the sacrifice on the cross. 

Think for a moment about that, a "sacrifice" means to separate something from the human sphere to transfer it to the divine sphere. It is a form of communication with the Gods, the only one that was left to humans once the Gods stopped speaking to them from inside their minds (at least according to Julian Jaynes). Do ants see this behavior as a sacrifice to the Fungus God? Who knows? As I said, we can't know what an ant thinks, but of one thing we can be sure: the macrocosm reflects the microcosm and the holobiont universe is fractal. So, we should not be surprised if we see a reflection of our own deep thoughts on such as small scale as an anthill. 

The ant sacrifice has a further element relevant for us. Unlike ants, we are organisms interacting on an individual basis with the microscopic world of fungi, bacteria, archaea, and viruses. We are not normally invaded by hordes of hungry creatures wanting to zombify us because of tens of millions of years of individual conversations that our ancestors engaged in with the creatures that surrounded them. Our body knows how to deal with them. That is, unless we chose to stop communicating with them by masking, disinfecting, and other useless rituals. Only if we continue with this unnatural behavior, do we risk seeing mushrooms sprouting from the back of our heads. (*)

And, in the end, Gaia knows best. 

 (*) which, by the way, may be exactly what we are facing with the current attack by the fungus called "Candida Auris." It is a battle that we cannot win as long as we don't recognize that the ecosystem is not our enemy.