Are Trees Socialists?

Plants are a lot like icebergs. There's the aboveground portion that's leafy, pretty, or tasty that everyone knows and appreciates. But then there's the hidden half: beneath the earth's surface, roots invisibly wend their way through the soil, patiently mining the recalcitrant earth for the nutrients it needs to survive and grasping hold to support the shoot's upward climb toward the sun. These roots create a shadow forest, one that's often bigger than the one we see. The competition is more intense, the community more diverse, and the seasonal changes more dramatic. But until recently, research into this upside-down world beneath our feet has been out of the public eye because it just doesn't seem as interesting as the things we can see and feel.

This trend has recently begun to change, however, especially in mycorrhizae, my specialty. For those who haven't read my introductory article, mycorrhizae are fungi that help give plants an edge in the competitive belowground environment. Mycorrhizae are smaller and nimbler than plant roots and can mine for nutrients in inaccessible areas. And, as we're beginning to learn, these fungi may play an even bigger role in how plants interact with each other. As mycorrhizal fungi explore the soil, they'll establish partnerships with many different plants, sometimes of different species. It's possible that these connections can allow plants to send materials, such as nutrients, sugars, and potentially even chemical signals for communication. The concept of common mycorrhizal networks, or the “wood wide web,” as it's been called, is gaining traction among mycorrhizal ecologists as more and more studies are published to support their existence, and some of that interest is reaching the popular press. It's certainly a great story: plants have their own internet? No way!

Pine seedlings with a mycorrhizal network forming between them. Photo by David Read for Nature.

Pine seedlings with a mycorrhizal network forming between them. Photo by David Read for Nature.

However, it’s possible for an imaginative story to get a little too imaginative.  Recently, I encountered a blog post for Scientific American that describes common mycorrhizal networks in what might be described charitably as an excessively colorful way. For context, you can read the article here. Otherwise, this post will discuss the article’s central claim, that:

Forest trees and their root fungi are more or less a commune in which they share resources in a fashion so unabashedly socialist that I hesitate to describe it in detail lest conservatives reading this go out and immediately set light to the nearest copse.

The evidence for this apparent socialistic behavior is a set of fantastically interesting experiments done by research group headed by Suzanne Simard. These experiments had three findings: first, individual mycorrhizal fungi will establish partnerships with multiple species of plants. Second, there is an apparent transfer of sugars from one plant in this partnership to another via these mycorrhizal connections – in the fall, birch will send sugar to Douglas fir, and in the spring, Douglas fir will apparently repay the favor and send sugar back to the birch. Third, individual plants that have been stressed, by, for example, an insect attack, it can send its resources to its neighbors.

All of this research is absolutely fascinating and deserves its own set of posts, but for now, let’s stick with the important question: does this set of behaviors mean that forests are a hotbed of subversive activity that must be cleansed with flame if they don’t agree with your personal politics? In short, no. This perspective is a major misapprehension of our best understanding for how the mycorrhizal symbiosis actually works. It takes two truths and uses it to make a lie. The first truth is that a mycorrhizal relationship is (usually) beneficial for both partners and (sometimes) benefits third parties. The lie is that this somehow makes a forest a “commune” where trees and fungi gather together, intertwine their respective tendrils, and creak out a round of “Kumbaya.” I wouldn’t object were this actually the case, but there’s a simpler and likely more accurate explanation for what’s going on.

The problem, as FTDM has discussed before, is that there isn't really such a thing as altruism in nature. While it's hyperbolic to describe interactions between different species as a knock-down, drag-out brawl or “red in tooth and claw,” it's equally silly to imply that individual organisms are out for anything other than their own reproductive benefit. The central premise of evolutionary theory is that organisms that are more reproductively successful (in terms of viable offspring) will eventually outnumber and outcompete those that aren't.

But if this is the case, why are trees apparently giving up nontrivial amounts of their hard-won sugar to individuals that may not be related and may even be a different species if it doesn't receive any benefits? To answer this question, we need to take a look at what happens when a mycorrhizal fungus colonizes a root. Under ordinary circumstances, a plant is alarmed by a fungus entering its roots and has two sets of defenses: the first set is triggered when the fungus is still outside the cells, and the second if the fungus penetrates the cell. The first response is like a burglar alarm – it'll go off, and the cells around the plant will reinforce their walls and make nasty chemicals to attack the intruder. If our burglar manages to break down the door of a particular cell, the cell in question will release a flood of toxins that hopefully kills or at least discourages the intruder and kills the plant cell in the process. It's a bit like responding to a home invasion by burning your own house down (assuming you keep a bunch of jet fuel in the basement), but it seems to work out all right for plants, at least most of the time.

When a mycorrhizal fungus invades, however, something very strange happens. It'll work its way into the roots, being very careful not to invade any cells and trigger the scorched-earth defenses, and then it'll cut the wires to the burglar alarm with some strategic bits of RNA. The plant, however, seems to be anticipating this strategy, because it'll respond with some RNA of its own designed to change the fungus's behavior. These exchanges result in a no-man's-land being established in the spaces between the plant's root cells where a fungus will give up mineral nutrients for the plant to absorb and sugar for the fungus to absorb. It's important to note that the plant and the fungus don't have complete control over this process – in order for the nutrient exchange to happen, both the plant and the fungus become a little “leaky,” meaning nutrients will passively flow from where they're in high concentrations to where they're in low concentrations. Physiologists refer to this as a “source-sink” dynamic. While both plants and fungi do have some ability to control this process – we’ve found that nitrogen-starved plants will up their contributions to their fungi and well-fertilized plants can ditch their partners altogether, when the relationship is stable there tends to be a steady flow of nutrients along their respective source-sink gradients. Sugar flows from the leaves where it’s made into the roots and then to the mycorrhizae, and minerals from the soils where they’re extracted into the plant’s roots and up the stem to leaves.

The mycorrhizal fungi form a dense "Hartig net" under the outermost layer of cells of a plant. Left - an SEM micrograph of a plant root cross-section with the larger plant cells on the right and the smaller fungal cells on the left. Right - a light microscrope showing fungal cells from the Hartig net surrounding plant root cells (arrowheads). Source.

The mycorrhizal fungi form a dense "Hartig net" under the outermost layer of cells of a plant. Left - an SEM micrograph of a plant root cross-section with the larger plant cells on the right and the smaller fungal cells on the left. Right - a light microscrope showing fungal cells from the Hartig net surrounding plant root cells (arrowheads). Source.

So let’s see how this explanation can result in the sort of relationship Simard and her colleagues found in their research. Suppose that a mature tree has a mycorrhizal partner and the relationship is going well for the both of them; the fungus is gathering nitrogen, the plant is making sugar, everyone’s happy.  Then, one day, the fungus encounters a tree seedling. The fungus acts according to its nature and colonizes a root, but the seedling's behavior is much different than that of a mature plant. In a well-established plant, a healthy canopy is producing way more sugar than the leaves or the stem need, and so the excess is sent to the roots to keep them alive (since they don't photosynthesize) and to store the rest for winter or in case something bad happens topside and the plant needs to resprout immediately. The mycorrhizal fungus acts as an additional sink – it has less sugar than the roots and is also using it for its own metabolism. Then the fungus forms an association with a plant that's essentially all sink. It's drawing nutrients from the seed to grow as quickly as possible both down and up. The root and the stem are both consuming more sugar than the seedling's canopy is producing, and along comes a fungus who's got a lot of sugar courtesy of its host plant. Recall, the fungus is a bit leaky, so some of the sugar it’s carrying will wind up in the seedling because the concentration gradient is pushing it in that direction.

So why would the fungus even bother colonizing a seedling to begin with? We can, and the author of the Scientific American post does, speculate that it's to the fungus's benefit to maintain partners that will come back to help it out later once they're living on their own and so will float it a start-up loan. However, this explanation ignores several simpler possibilities. First, it's possible that the fungus simply can't tell between mature plant roots and baby plant roots, and ending up on the hook for the occasional lemon is simply a cost of doing business. A second possibility is that the fungus may cover its losses by becoming a stronger sink, in effect demanding more from the trees that are paying for its services, and the tree may not notice what to it may be a trivial uptick in its expenses. This is an unexplored possibility given that it still difficult to quantify how much sugar seedlings get from mycorrhizae.

The source-sink dynamic can also explain the other situations tested by Simard’s group. Sugar flow between plants can occur as a result of seasonal variation – if a deciduous tree (like a birch) and an evergreen (like Douglas fir) are hooked up via a mycorrhizal connection, the birch becomes a particularly strong source in the fall, when it’s retrieving nutrients from its leaves and reducing its consumption in order to prepare for dormancy, and a particularly strong sink in the spring, when it’s mobilizing large amounts of stored energy in order to produce new leaves. A dying tree is probably unable to maintain the complex process that keeps the mycorrhizal relationship going, and there’s some evidence that mycorrhizal fungi will switch roles from a partner to a decomposer when its partner starts to fail, meaning that a dying tree doesn’t flood a mycorrhizal network with sugar so much as a result of a last will that its fellow trees live on, but because a mycorrhizal is able to break into its roots and loot the place before competition arrives.

This explanation doesn't have any more direct evidence for it than the Scientific American's explanation, but it does do something important: it satisfies Occam's Razor, which says that the simplest explanation that accounts for all the evidence is usually the correct one. This explanation doesn't have to come up with a reason why a fungus or a tree would behave altruistically – that is, doing something that isn't to its advantage (giving up a scarce resource) with little to no impact on its reproductive output. Altruism is great when we're talking about individuals of a very social species, such as ours, but not so much in the world of plant ecology, where competition between even individuals of the same species can be extremely intense, much less individuals of another species. This puts us at a rather dissatisfying tautology – that this apparent relationship between multiple trees and a shared fungus has persisted because it hasn't been too unfavorable to either member for it to cease – but it avoids ascribing intentions to the plants that simply aren't there. And it's a conclusion the author reaches too, at the end of her article:

It’s possible that it is only passive effect of a source-sink scenario, where the douglas-fir [sic] dumped food into its mycorrhizae for safe-keeping in light of severe stress, and the excess resources simply moved from an area of high concentration to an area of low concentration.

How we describe the nature of any natural association is always going to be tinged with human morality and philosophy that aren't truly applicable, but it's a sacrifice we need to make in order to successfully communicate with each other – science isn't completely objective because its observers aren't, either. How scientists have approached mycorrhizae has spurred a lot of arguments that aren’t going to stop any time soon. It may seem like only so much counting angels on pinheads, but these perspectives matter when it comes time to make decisions that affect mycorrhizal networks. Can we expect mycorrhizal networks to function the same way when forests are disturbed by humans? When climate change alters the composition of plant communities? These are important questions this research raises, and how we think about mycorrhizae when we approach them will definitely be crucial to how we continue to build our understanding of mycorrhizal ecology.