on earth can do: Hafiz (1315–1390), in Ladinsky (2010).
specimens that remain undiscovered: Ferguson et al. (2003). There are numerous other reports of enormous networks of Armillaria. A study published by Anderson et al. (2018) investigated a mycelial network in Michigan with an estimated age of 2,500 years and a weight of at least 400 metric tons, sprawling over an area of 75 hectares. The researchers found that the fungus had an extremely low rate of genetic mutation, suggesting that it has a way of protecting itself against damage to its DNA. How exactly the fungus is able to maintain such a stable genome is not known, but this probably helps to account for its ability to live to such a great age. Apart from Armillaria, some of the largest organisms are clonal sea grasses (Arnaud-Haond et al. [2012]).
genus Homo has existed: Moore et al. (2011), ch. 2.7; Honegger et al. (2018). The fossilized remains of Prototaxites have been found in North America, Europe, Africa, Asia, and Australia. Biologists have puzzled over what Prototaxites was since the mid-nineteenth century. It was first thought to be a rotted tree. Shortly afterward, it was promoted to the status of giant marine alga despite overwhelming evidence that it grew on land. In 2001, after decades of debate, it was argued that Prototaxites were in fact the fruiting bodies of a fungus. It is a persuasive argument: Prototaxites were formed from thickly woven filaments that look more like fungal hyphae than anything else. Analysis of the carbon isotopes indicate that it survived by consuming its surroundings rather than by photosynthesis. More recently, Selosse (2002) has argued that it is more plausible that Prototaxites were giant lichen-like structures, made up of a union of fungi with photosynthetic algae. He argues that Prototaxites were too large to support themselves by decomposing plants. If Prototaxites were partly photosynthetic, they would have been able to supplement their diet of dead plants with energy from photosynthesis. They would have both the means and the incentive to grow into structures taller than anything else around. What’s more, Prototaxites contained tough polymers found in algae of the time, suggesting that algal cells lived interwoven with the fungal hyphae. The lichen hypothesis also helps to explain why they went extinct. After forty million years of global dominance, Prototaxites mysteriously died out just as plants were evolving into trees and shrubs. This observation fits with Prototaxites being lichen-like organisms, because more plants mean less light.
as leaves or roots: For a broad discussion of fungal diversity and distribution see Peay (2016); for marine fungi see Bass et al. (2007); for fungal endophytes see Mejía et al. (2014), Arnold et al. (2003), and Rodriguez et al. (2009). For an account of specialist fungi found in distilleries where they thrive on the alcohol fumes that evaporate from whiskey barrels as they age see Alpert (2011).
the energy in sunlight: For rock-digesting fungi see Burford et al. (2003) and Quirk et al. (2014); for plastics and TNT see Peay et al. (2016), Harms et al. (2011), Stamets (2011), and Khan et al. (2017); for radiation-resistant fungi see Tkavc et al. (2018); for radiographic fungi see Dadachova and Casadevall (2008) and Casadevall et al. (2017).
snow, sleet, and hail: For spore ejection see Money (1998), Money (2016), and Dressaire et al. (2016). For spore mass and influence on weather see Fröhlich-Nowoisky et al. (2009). For a review of the many colorful solutions fungi have evolved in response to the problems of spore dispersal see Roper et al. (2010) and Roper and Seminara (2017).
in animal nerve cells: For flow see Roper and Seminara (2017); for electrical impulses see Harold et al. (1985) and Olsson and Hansson (1995). Yeasts make up about one percent of the fungal kingdom and multiply by “budding” or splitting in two. Some yeasts can form hyphal structures under certain conditions (Sudbery et al. [2004]).
drawn with Coprinus ink: For accounts of fungi pushing through asphalt and lifting paving stones see Moore (2013b), ch. 3.
with fragments of leaf: Leaf-cutter ants don’t just feed and house their fungi, they medicate them as well. Leaf-cutter ants’ fungal gardens are monocultures, consisting of a single type of fungus. Like human monocultures, the fungi are vulnerable. Particularly threatening is a type of specialist parasitic fungus that can destroy a fungal garden. Leaf-cutters harbor bacteria in elaborate chambers in their cuticles, fed by specialized glands. Each nest cultures its own specific strain of bacteria, recognized and favored by the ants above other strains, even closely related ones. These domesticated bacteria produce antibiotics that powerfully inhibit the parasitic fungus and boost the growth of the cultivated one. Without these fungi, leaf-cutter ant colonies wouldn’t be able to grow to such a large size. See Currie et al. (1999), Currie et al. (2006), and Zhang et al. (2007).
in the coming decades: For the Roman god Robigus see Money (2007), ch. 6, and Kavaler (1967), ch. 1. For fungal superbugs see Fisher et al. (2012, 2018), Casadevall et al. (2019), and Engelthaler et al. (2019); for fungal disease of amphibians see Yong (2019); for banana disease see Maxman (2019). Among animals, diseases caused by bacteria pose more of a threat than those caused by fungi. By contrast, among plants, diseases caused by fungi pose a greater threat than those caused by bacteria. It is a pattern that holds through sickness and through health: Animal microbiomes tend to be dominated by bacteria, while plant microbiomes tend to be dominated by fungi. This is not to say that animals don’t suffer from fungal diseases at all. Casadevall (2012) hypothesizes that the rise of mammals and decline of reptiles following the extinction event that wiped out the dinosaurs—the Cretaceous-Tertiary (K-T) extinction—was due to the ability of mammals to fight fungal diseases. Compared with reptiles, mammals have a number of handicaps: It is energetically costly to be warm-blooded, and even more so to produce milk and deliver intensive parental care. But it may be that mammals’ elevated body temperatures were exactly what made it possible to replace reptiles as the dominant land-dwelling animals. Mammals’ elevated body temperatures help to deter the growth of fungal pathogens that are hypothesized to have proliferated in the “global compost heap” that followed the widespread dieback of forests during the K-T extinction. To this day, mammals are more resistant to common fungal diseases than reptiles or amphibians.
as a medicine: For a study of Neanderthals see Weyrich et al. (2017); for Iceman see Peintner et al. (1998). How the Iceman used the birch polypore (Fomitopsis betulina) can’t be known for certain, but they are bitter and indigestibly corky, so clearly not “nutritional” in any conventional sense. The Iceman’s careful preparation of these fungi—which were mounted like key rings on leather thongs—indicates a well-developed knowledge of their value and application.
the Second World War: For mold cures see Wainwright (1989a and 1989b). Human remains from archaeological sites in Egypt, Sudan, and Jordan dating from around the year AD 400 have been found to have high levels of the antibiotic tetracycline in their bones, indicating a long-term sustained intake, most likely in a therapeutic context. Tetracycline is produced by a bacterium, not a fungus, but its likely source was moldy grains, likely used to make a medicinal beer (Bassett et al. [1980] and Nelson et al. [2010]). The journey from Fleming’s first observation to penicillin’s emergence onto the world stage was not a straightforward one and required a great deal of human effort: experiments, industrial know-how, investment, and political support. For a start, it was difficult for Fleming to persuade anyone to take an interest in his discovery. In the words of Milton Wainwright, a microbiologist and historian of science, Fleming was eccentric, a “messer abouter.” “He had a reputation for being a nutter and doing daft things, like creating pictures of the Queen on a petri dish using different bacteria cultures.” Dramatic proof of penicillin’s therapeutic value didn’t come until twelve years after Fleming’s first observations. In the 1930s, a research group in Oxford developed a method to extract and purify penicillin and, in 1940, conducted trials that demonstrated its astonishing ability to fight infections. Nonetheless, penicillin remained difficult to produce. In the absence of a widely available product, instructions on how to grow the mold were published in the medical press. Crude “kitchen sink” extracts, along with chopped mycelium on surgical gauze—“mycelial pads”—were used by some doctors to treat infections, treatments observed to be remarkably effective (Wainwright [1989a and 1989b]). It was in the United States that penicillin production was industrialized. This was partly due to the well-developed American methods to cultivate fungi in industrial fermenters, and partly due to the discovery of higher yielding strains of Penicillium mold, strains that were further enhanced by rounds of mutation. The industrialization of penicillin led to a massive effort to search for new antibiotics, and thousands of fungi and bacteria were screened.
mushrooms are increasing yearly: For drugs see Linnakoski et al. (2018), Aly et al. (2011), and Gond et al. (2014). For psilocybin see Carhart-Harris et al. (2016a), Griffiths et al. (2016), and Ross et al. (2016). For vaccines and citric acid see the State of the World’s Fungi (2018). For the market in edible and medicinal mushrooms see www.knowledge-sourcing.com/report/global-edible-mushrooms-market [accessed October 29, 2019]. In 1993, a study published in Science reported that paclitaxel (sold under the brand name Taxol) was produced by an endophytic fungus isolated from the bark of the Pacific yew (Stierle et al. [1993]). It has subsequently emerged that paclitaxel is produced far more widely by fungi than by plants—by around two hundred endophytic fungi, spread across several fungal families (Kusari et al. [2014]). A potent antifungal, it plays an important defensive role: Fungi that are able to produce paclitaxel are able to deter other fungi. It acts against fungi in the same way it acts against cancer, by interrupting cell division. Paclitaxel-producing fungi are immune to its effects, as are other fungal endophytes of yew (Soliman et al. [2015]). A number of other fungal anticancer drugs have made their way into mainstream pharmaceutical practice. Lentinan, a polysaccharide from the shiitake mushroom, has been found to stimulate the immune system’s ability to fight cancers and is medically approved in Japan for the treatment of gastric and breast cancers (Rogers [2012]). PSK, a compound isolated from turkey tail mushrooms, extends the survival time of patients suffering from a range of cancers and is used alongside conventional cancer treatments in China and Japan (Powell [2014]).
radiation-resistant biomaterials: For fungal melanins see Cordero (2017).
sophistications of fungal lives: For estimates of the number of fungal species see Hawksworth (2001) and Hawksworth and Lücking (2017).
when we actually look: Among neuroscientists, the involvement of our expectations in perception is known as top-down influence, or sometimes as Bayesian inference (after Thomas Bayes, a mathematician who made a founding contribution to the mathematics of probability, or “the doctrine of chances”). See Gilbert and Sigman (2007), and Mazzucato et al. (2019).
“they’re cleverer than me”: Adamatzky (2016), Latty and Beekman (2011), Nakagaki et al. (2000), Bonifaci et al. (2012), Tero et al. (2010), and Oettmeier et al. (2017). In Advances in Physarum Machines (Adamatzky [2016]), researchers detail many surprising properties of slime molds. Some use slime molds to make decision gates and oscillators, some simulate historical human migrations and model possible future patterns of human migrations on the moon. Mathematical models inspired by slime molds include a non-quantum implementation of Shor’s factorization, calculation of shortest paths, and the design of supply-chain networks. Oettmeier et al. (2017) note that Hirohito, the emperor of Japan between 1926 and 1989, was fascinated by slime molds and in 1935 published a book on the subject. Slime molds have been a high-prestige subject of research in Japan ever since.
may start to change: The system of classification devised by Linnaeus and published in his Systema Naturae in 1735, a modified version of which is used today, extended this hierarchy to human races. At the top of the human league tables were Europeans: “Very smart, inventive. Covered by tight clothing. Ruled by law.” Americans followed: “Ruled by custom.” Then Asians: “Ruled by opinion.” Then Africans: “sluggish, lazy…[c]rafty, slow, careless. Covered by grease. Ruled by caprice” (Kendi [2017]). The way that hierarchal classification systems order different species can be seen, by extension, as species racism.
stars in our galaxy: For different microbial communities in different parts of the body see Costello et al. (2009) and Ross et al. (2018). For comparison with stars in the galaxy see Yong (2016), ch. 1. W. H. Auden, in his “New Year Greeting,” offers up the ecosystems of his body to his microbial inhabitants. “For creatures your size I offer / a free choice of habitat, / so settle yourselves in the zone / that suits you best, in the pools / of my pores or the tropical / forests of arm-pit and crotch, / in the deserts of my fore-arms, / or the cool woods of my scalp.”
ubiquitous feature of life: For organ transplants and human cell cultures see Ball (2019). For an estimate of the size of our microbiome see Bordenstein and Theis. (2015). For viruses within viruses see Stough et al. (2019). For a general introduction to the microbiome see Yong (2016) and a special issue of Nature on the human microbiome (May 2019): www.nature.com/collections/fiabfcjbfj [accessed October 29, 2019].
dark matter, or dark life: In a sense, all biologists are now ecologists—but disciplinary ecologists have a head start and their methods are starting to seep into new fields: A number of biologists are starting to call for the application of ecological methods to historically non-ecological fields of biology. See Gilbert and Lynch (2019) and Venner et al. (2009). There are a number of examples of the knock-on effects of the microbes that live within fungi. A study published by Márquez et al. (2007) in Science in 2007 described “a virus in a fungus in a plant.” The plant—a tropical grass—grows naturally in high soil temperatures. But without a fungal associate that grows in its leaves, the grass can’t survive at high temperatures. When grown alone, without the plant, the fungus fares little better and is unable to survive. However, it turns out not to be the fungus that confers the ability to survive high temperatures after all. Rather, it is a virus that lives within the fungus that confers heat tolerance. When grown without the virus, neither fungus nor plant can survive high temperatures. The microbiome of the fungus, in other words, determines the role that the fungus plays in the microbiome of the plant. The outcome is clear: life or death. One of the most dramatic examples of microbes that live within microbes comes from the notorious rice blast fungus: Rhizopus microsporus. The key toxins used by Rhizopus are actually produced by a bacterium living within its hyphae. In a dramatic indication of how entwined the fates of fungi and their bacterial associates can be, Rhizopus requires the bacteria not only to cause the disease but also to reproduce. Experimentally “curing” Rhizopus of its bacterial residents impedes the fungus’s ability to produce spores. The bacterium is responsible for the most important features of Rhizopus’s lifestyle, from its diet to its sexual habits. See Araldi-Brondolo et al. (2017), Mondo et al. (2017), and Deveau et al. (2018).
only now becoming known: For remarks about loss of self-identity see Relman (2008). The questions of whether human beings are singular or plural is not a new one. In nineteenth-century physiology, the bodies of multicellular organisms were thought of as being made up of a community of cells with each cell an individual in its own right, by analogy to the individual human member of a nation-state. These questions are complicated by developments in the microbial sciences because the multitude of cells in your body aren’t strictly related to each other, as, for example, an average liver cell would be related to an average kidney cell. See Ball (2019), ch. 1.
Who’s pimping who?: Prince, “Illusion, Coma, Pimp & Circumstance,” Musicology (2004).
to the eyes of animals: Psychoactive “truffles” sold in Amsterdam are not, as their name suggests, fruiting bodies. They are storage organs known as “sclerotia,” which are called truffles because of their superficial resemblance.
to have olfactory flashbacks: For trillion odors see Bushdid et al. (2014); for olfactory navigation see Jacobs et al. (2015); for olfactory flashbacks and a general discussion of human olfactory abilities see McGann (2017). Some humans are classed as “super smellers,” or hyperosmic individuals. A study published by Trivedi et al. (2019) reported that a super smeller was able to detect Parkinson’s disease using their sense of smell alone.
smell metallic and oily: For a discussion of the smell of different chemical bonds see Burr (2012), ch. 2.
Olympic swimming pools: These receptors belong to a large family called G-protein coupled receptors, or GPCRs. For a study of human olfactory sensitivity see Sarrafchi et al. (2013), who report that humans can detect some odors at concentrations of 0.001 parts per trillion.
“visual and emotional memories”: For turmas de tierra see Ott (2002). Truffles, according to Aristotle, were “a fruit consecrated to Aphrodite.” They are reputed to have been used as aphrodisiacs by Napoleon and the Marquis de Sade, and George Sand described them as the “black magic apple of love.” The French gastronome Jean Anthelme Brillat-Savarin documented that “truffles are conducive to erotic pleasure.” In the 1820s, he set out to investigate this commonly held belief, and embarked on a series of consultations with ladies (“all the replies I received were ironical or evasive”) and men (“who by their profession are invested with special trust”). He concluded that “the truffle is not a true aphrodisiac but in certain circumstances it can make women more affectionate and men more attentive” (Hall et al. [2007], p. 33).
“it’s perishable and mercurial”: For Laurent Rambaud see Chrisafis (2010). The reporter Ryan Jacobs documents the foul play that occurs all the way along truffle supply lines. Some poisoners use meatballs laced with strychnine, others poison pools of water in the forest so that dogs with muzzles can still be poisoned, some deploy meat spiked with shards of glass, others use rat poison or antifreeze. Based on vets’ reports, hundreds of poisoned dogs receive treatment each truffle season. The authorities have taken to using poison-sniffing dogs to patrol certain woods (Jacobs [2019], pp. 130–34). In 2003, The Guardian reported that Michel Tournayre, a French truffle expert, had his truffle dog stolen. Tournayre suspected that the thieves had not sold the dog but rather were using her to steal truffles from other people’s land (Hall et al. [2007], p. 209). What better way to steal truffles than with a stolen dog?
that break down wood: For elk with bloodied noses see Tsing (2015), “Interlude. Smelling”; for fly-pollinated orchids see Policha et al. (2016); for orchid bees collecting complex aromatic compounds see Vetter and Roberts (2007); for similarity with compounds produced by fungi see de Jong et al. (1994). Orchid bees secrete a fatty substance that they apply to the scented object. Once the scent has been absorbed, they scrape the fat back up and store it in pockets on their hind legs. This approach is identical in principle to enfleurage, the method used by humans for hundreds of years to capture fragrances like jasmine that are too delicate to extract using heat (Eltz et al. [2007]).
extinction in the wild: Naef (2011).
ghosts at a disco: For Bordeu see Corbin (1986), p. 35.
nonlinearly with their size: For record-breaking truffle see news.bbc.co.uk/1/hi/world/europe/7123414.stm [accessed October 29, 2019].
than a single organism: For a discussion of the role of truffle microbiome in odor production see Vahdatzadeh et al. (2015). When I was out with Daniele and Paride I noticed that a truffle excavated from the silty soil near a river smelled quite different from one found in the more clay-heavy soil farther up the valley. These differences are unlikely to make much difference to a hungry shrew. But a white truffle found in Alba will sell for four times as much as a white truffle found near Bologna (although the fact that some truffle dealers regularly pass off Bolognese truffles as being from Alba would suggest that not everyone is able to tell the difference). Regional differences in truffles’ volatile profiles have been confirmed in formal studies (Vita et al. [2015]).
None detected the androstenol: For the original report that truffles produce androstenol see Claus et al. (1981); for the follow-up study from nine years later see Talou et al. (1990).
even for taxonomic purposes: The number of volatiles produced by a single species of truffle has steadily increased over the years as the sensitivity of detection methods has improved. These methods are still less sensitive than the human nose, and the number of truffle volatiles is likely to increase yet further in the future. For white truffle volatiles see Pennazza et al. (2013) and Vita et al. (2015); for other species see Splivallo et al. (2011). There are a number of reasons why it is risky to pin all of truffles’ allure on a single compound. In the study by Talou et al. (1990), a small sample of animals was used and only a single species of truffle was tested, at a single shallow depth, at a single site. Different subsets of the profile of volatile compounds might be more prominent at different depths or in different places. Moreover, in the wild, a range of animals are attracted to truffles, from wild pigs to voles to insects. It might be that different elements of the cocktail of volatile compounds that truffles produce attract different animals. It may be that androstenol acts on animals in more subtle ways. It might not be effective on its own, as tested in the study, but only in conjunction with other compounds. Alternatively, it may be less important in finding the truffles and more important in the animals’ experience of eating them. For more on poisonous truffles see Hall et al. (2007). Besides Gautieria, the truffle species Choiromyces meandriformis is reported to smell “overpowering and nauseous” and is considered toxic in Italy (although it is popular in northern Europe). Balsamia vulgaris is another species considered to be mildly toxic, although dogs appear to enjoy its aroma of “rancid fat.”
them with such urgency: For truffle export and packaging see Hall et al. (2007), pp. 219, 227.
attract itself to itself: In areas of exploring mycelium, hyphae usually grow away from other hyphae without ever touching. In more mature parts of the mycelium, hyphal inclinations pivot. Growing tips instead become attracted to each other and start to “home” (Hickey et al. [2002]). How hyphae attract and repel each other remains poorly understood. Work on the model organism, the bread mold Neurospora crassa, is starting to provide some clues. Each hyphal tip takes it in turn to release a pheromone that attracts and “excites” the other. Through this back-and-forthing—“as if throwing a ball,” write the authors of one study—hyphae are able to entrain and home in on each other by falling into rhythm. It is this oscillation—a chemical rally—that allows them to lure the other without stimulating themselves. When they are serving, they aren’t able to detect the pheromone. When the other serves, they are stimulated (Read et al. [2009] and Goryachev et al. [2012]).
off into otherness gradually: For a discussion of mating types of Schizophyllum commune see McCoy (2016), p. 13; for fusion between sexually incompatible hyphae see Saupe (2000) and Moore et al. (2011), ch. 7.5. The ability of hyphae to fuse with each other is determined by their “vegetative compatibility.” Once hyphal fusion has taken place, a separate system of mating types determines which nuclei can undergo sexual recombination. These two systems are regulated differently, although sexual recombination cannot take place unless hyphae have fused with each other and shared genetic material. The outcome of vegetative fusions between different mycelial networks can be complex and unpredictable (Rayner et al. [1995] and Roper et al. [2013]).
pheromone for this purpose: For details of truffle sex see Selosse et al. (2017), Rubini et al. (2007), and Taschen et al. (2016); for examples of intersexuality in the animal world see Roughgarden (2013). If truffle cultivators really want to understand how to crack truffle cultivation, they must understand truffle sex. The problem is that they don’t. Truffle fungi have never been caught in the act of fertilization. Perhaps this isn’t so surprising given their inaccessible lifestyles. More peculiar is that no one has ever found a paternal hypha. Despite searching, researchers have only found maternal hyphae growing on tree roots and in soil, whether “+” or “-.” Paternal truffles seem to be short-lived and vanish after fertilization: “birth, then a drop of sex, then nothing” (Dance [2018]).
microbes course and engage: The hyphae of some types of mycorrhizal fungi can withdraw themselves back into their spores and resprout at a later date (Wipf et al. [2019]).
physiology of their associates: For fungal influence on plant roots see Ditengou et al. (2015), Li et al. (2016), Splivallo et al. (2009), Schenkel et al. (2018), and Moisan et al. (2019).
another in real time: For a discussion of the evolution of communication in mycorrhizal symbioses, including suspension of immune response, see Martin et al. (2017); for a discussion of plant-fungus signaling and its genetic basis see Bonfante (2018); for plant-fungus communication in other types of mycorrhizal association see Lanfranco et al. (2018). The chemical propositions released by fungi are nuanced and have a wide dynamic range. The volatiles used to communicate with a plant might also be used to communicate with the surrounding bacterial populations (Li et al. [2016] and Deveau et al. [2018]). Fungi use volatile compounds to deter rival fungi; plants use volatile compounds to deter unwanted fungi (Li et al. [2016] and Quintana-Rodriguez et al. [2018]). The same volatile can have different effects on plants depending on its concentration. The plant hormones produced by some truffles to manipulate their hosts’ physiology can kill plants at higher concentrations and may serve as competitive weapons to deter plants that might compete with their own plant partners (Splivallo et al. [2007 and 2011]). Some species of truffle fungus are parasitized by other fungi, probably attracted by their chemical announcements. The truffle parasite, Tolypocladium capitata, is a cousin of the Ophiocordyceps fungi that parasitize insects and is known to parasitize certain species of truffle such as the deer truffle, Elaphomyces (Rayner et al. [1995]; for photos see mushroaming.com/cordyceps-blog [accessed October 29, 2019]).
hasn’t yet caught up: For the first report of fruiting Tuber melanosporum in the British Isles—thought to be due to climate change—see Thomas and Büntgen (2017). The “modern” method used to cultivate Tuber melanosporum wasn’t developed until 1969 and resulted in the first batch of artificially inoculated truffles in 1974. Seedling roots are incubated with the mycelium of Tuber melanosporum and planted out when the roots are thoroughly inhabited by the fungus. After several years, given the right conditions, the fungus will start to produce truffles. There is an increasingly large area of land in truffle cultivation (more than 40,000 hectares worldwide), and Périgord truffle orchards are successfully fruiting in countries from the United States to New Zealand (Büntgen et al. [2015]). Lefevre explained that even if he wrote his method down point by point, it would be difficult for someone else to replicate. There is so much intuitive knowledge that is hard to communicate and keep track of. The tiniest details—from the vagaries of the season to the conditions in the nursery—make a huge difference. Secrecy is part of the problem. Truffle cultivators spend much of their time in a fog of uncertainty, picking their way around jealously tended “proprietary insight.” “It is a tradition with old roots in mushroom picking,” Büntgen told me. “Many people go out to pick mushrooms in the woods, but they never tell you anything. If you ask someone how their day was and they say, ‘Oh I found a huge crop!’ they probably found nothing. It is an attitude that persists over generations and makes research very slow.” Undeterred, Lefevre still grows a number of trees with the mycelium of the elusive Tuber magnatum every year in the hope that something, somehow, might just prompt them to fruit. Armed with the same optimism, he continues to experiment in pairing European truffle species with American trees (Tuber magnatum turns out to develop a healthy—though fruitless—partnership with aspens). Other cultivators isolate bacteria from truffles in the hope that they will encourage the growth of Tuber mycelium (some groups of bacteria do seem to be helpful). I asked if many people bought his Tuber magnatum trees for their truffle orchards. “Not many,” he replied, “but we sell the trees in the spirit that if no one tries, no one will succeed.”
eavesdrop on their prey: For a discussion of chemical eavesdropping see Hsueh et al. (2013).
known as “gun cells”: Nordbring-Hertz (2004) and Nordbring-Hertz et al. (2011).
many options remains unknown: Nordbring-Hertz (2004).
or forget to notice: Today, the field of biology most inflamed by debates about anthropomorphism is the study of plants and the ways they sense and respond to their environment. In 2007, thirty-six prominent plant scientists signed a letter that dismissed the nascent field of “plant neurobiology” (Alpi et al. [2007]). Those who put forward the term argued that plants have electrical and chemical signaling systems equivalent to those found in humans and other animals. The thirty-six authors of the letter argued that these were “superficial analogies and questionable extrapolations.” A spirited debate ensued (Trewavas [2007]). From an anthropological perspective, these controversies are fascinating. Natasha Myers, an anthropologist at York University in Canada, interviewed a number of plant scientists about how they understood plants to behave (Myers [2014]). She describes the troubled politics of anthropomorphism and the different ways that researchers dealt with the issue.
different kind of trap: Kimmerer (2013), “Learning the Grammar of Animacy.”
on which they depend: “Its relationship with its host trees is very poorly understood,” Lefevre explained, “even in places where truffle productivity is high, the proportion of tree roots colonized by the fungus is often extremely low. This means that productivity can’t be explained in terms of the amount of energy that the fungus receives from the host tree.”
talk about other organisms: For smells and their likenesses see Burr (2012), ch. 2. The anthropologist Anna Tsing writes that in the Edo period in Japan (1603–1868) the smell of matsutake mushrooms became a popular subject for poetry. Trips to pick matsutake grew into the autumn equivalent of cherry-blossom parties in the spring, and references to “the autumn aroma” or the “aroma of the mushroom” became familiar poetic moods (Tsing [2015]).
there is no thread: Cixous (1991).
somehow, improbably, both: For the fungal navigation of mazes see Hanson et al. (2006), Held et al. (2009, 2010, 2011, 2019). For excellent videos see supplementary information of Held et al. (2011) at www.sciencedirect.com/science/article/pii/S1878614611000249 [accessed October 29, 2019] and Held et al. (2019) at www.pnas.org/content/116/27/13543/tab-figures-data [accessed October 29, 2019].
challenges our animal imaginations: For marine fungi see Hyde et al. (1998), Sergeeva and Kopytina (2014), and Peay (2016); for fungi in dust see Tanney et al. (2017); for an estimate of the length of fungal hyphae in soils see Ritz and Young (2004).
completely remodeled itself: This is a commonly reported phenomenon. See Boddy et al. (2009) and Fukusawa et al. (2019).
this memory remains unclear: Fukusawa et al. (2019). Did the new block of wood cause changes in chemical concentrations or gene expression across the network? Or did the mycelium rapidly redistribute itself within the original block of wood, making regrowth in one direction more likely? Boddy and her colleagues aren’t sure. The researchers who challenge fungi with microscopic mazes have observed that structures within fungal growing tips behave like internal gyroscopes and provide hyphae with a directional memory that allows them to recover the original direction of growth after being diverted around an obstacle (Held et al. [2019]). However, it is unlikely that this mechanism is responsible for the effect Boddy and her colleagues observed because all the hyphae—including their tips—were removed from the original block of wood before it was placed in the fresh dish.
mycelium is a multitude: Fungal hyphae are unlike cells in animal or plant bodies, which (usually) have clear boundaries. In fact, strictly speaking, hyphae shouldn’t be described as cells at all. Many fungi have hyphae with divisions along their length, known as “septa,” but these can be opened or closed. When open, hyphal contents can flow between the “cells,” and the mycelial networks are referred to as being in a “supracellular” state (Read [2018]). One mycelial network can fuse with many others to make sprawling “guilds,” in which the contents of one network may be shared with others. Where does one cell start and stop? Where does one network start and stop? These questions are often unanswerable. For a recent study on swarms see Bain and Bartolo (2019) and commentary by Ouellette (2019). This study treats swarms as entities in themselves, rather than a collection of individual agents behaving according to local rules. By treating the swarm as a pattern of fluid flow, its behavior can be more effectively modeled. It’s possible that these top-down “hydrodynamic” models could be used to model the growth of hyphal tips more effectively than swarm models based on local rules of interaction.
or to program robots: For slime molds see Tero et al. (2010), Watanabe et al. (2011), and Adamatzky (2016); for fungi see Asenova et al. (2016) and Held et al. (2019).
in search of food: For a discussion of mycelial trade-offs see Bebber et al. (2007).
without a body plan: For a discussion of natural selection of links in mycelial networks see Bebber et al. (2007).
“My kids loved it”: For discussion of the role of fungal bioluminescence and insect spore dispersal see Oliveira et al. (2015); for foxfire and the Turtle see www.cia.gov/library/publications/intelligence-history/intelligence/intelltech.html [accessed October 29, 2019] and Diamant (2004), p. 27. In a guidebook to fungi published in 1875, Mordecai Cooke wrote that bioluminescent fungi were commonly found on the timber props used in coal mines. Miners “are well acquainted with phosphorescent fungi, and the men state that sufficient light is given ‘to see their hands by.’ The specimens of Polyporus were so luminous that they could be seen in the dark at a distance of twenty yards.”
a different physiological state: Olsson’s videos are available online at doi.org/10.6084/m9.figshare.c.4560923.v1 [accessed October 29, 2019].
over such short timescales: A study published by Oliveira et al. (2015) found that the bioluminescent mycelium of Neonothopanus gardneri was regulated by a temperature-regulated circadian clock. The authors hypothesize that by increasing bioluminescence at night, fungi are better able to attract insects that disperse their spores. The phenomena that Olsson observed can’t be explained on the basis of a circadian rhythm because it took place only once over the course of several weeks.
bodies in the food: For hyphal diameter see Fricker et al. (2017). The ecologist Robert Whittaker observed that animal evolution is a story of “change and extinction,” whereas fungal evolution is one of “conservatism and continuity.” The great diversity of animal body plans in the fossil record illustrates the many ways animals have found to ingest features of their worlds. The same can’t be said about fungi. Mycelial fungi have had much longer to evolve than many organisms, but ancient fossilized fungi are remarkably similar to those alive today. It appears that there are only so many ways to make a life as a network. See Whittaker (1969).
to catch falling leaves: For mycelial nets that catch falling leaves see Hedger (1990).
eight-ton school bus: For measurement of the pressure exerted by the rice blast pathogen see Howard et al. (1991); for the eight-ton school bus figure and for a general discussion of invasive fungal growth see Money (2004a). To exert such high pressures, the penetrative hyphae must glue themselves to the plant to prevent themselves from pushing away from the surface. They do this by producing an adhesive that can resist pressures of more than 10 megapascals—superglue can resist pressures of 15 to 25 megapascals, though probably not on the waxy surface of a plant leaf (Roper and Seminara [2017]).
six hundred a second: The cellular “bladders” are known as “vesicles.” Fungal tip growth is managed by a cellular structure, or “organelle,” called the “Spitzenkörper,” or tip body. Unlike most organelles, the Spitzenkörper does not have a clearly defined boundary. It is not a singular structure like a nucleus, although it appears to move as one. The Spitzenkörper is thought of as a “vesicle supply center,” receiving and sorting vesicles from inside the hyphae and distributing them to the hyphal tip. The Spitzenkörper pilots both itself and its hypha. Hyphal branching is triggered when Spitzenkörpers divide. When growth stops, the Spitzenkörper disappears. If one changes the position of the Spitzenkörper within the growing tip, one can steer the hypha in a different direction. What the Spitzenkörper makes, it can also unmake, dissolving hyphal walls to allow fusion between different parts of a mycelial network. For an introduction to the Spitzenkörper and “six hundred vesicles per second” see Moore (2013a), ch. 2; for a further discussion of the Spitzenkörper see Steinberg (2007); for the observation that the hyphae of some species can extend in real time see Roper and Seminara (2017).
in its continual development: The French philosopher Henri Bergson described the passage of time in terms reminiscent of a fungal hypha: “Duration is the continuous progress of the past which gnaws into the future and which swells as it advances” (Bergson [1911], p. 7). For the biologist J.B.S. Haldane, life was not populated with things but with stabilized processes. Haldane went as far as to deem “the conception of a ‘thing,’ or material unit,” to be “useless” in biological thinking (Dupré and Nicholson [2018]). For a general introduction to processual biology see Dupré and Nicholson (2018); for the Bateson quote see Bateson (1928), p. 209.
“weighed eighty-three pounds”: For stinkhorns growing through asphalt see Niksic et al. (2004); for Cooke see Moore (2013b), ch. 3. Tip growth occurs in other organisms besides fungi, but it is an exception not the rule. Animal neurons grow by elongating at the tip, as do some types of plant cell, like pollen tubes. But neither can prolong themselves indefinitely, as fungal hyphae can under the right conditions (Riquelme [2012]).
and beside one another: Frank Dugan describes the “herb wives” or “wise women” of Reformation Europe as “midwives” to the field of modern mycology (Dugan [2011]). Many lines of evidence suggest that women were primary holders of fungal lore. Such women were the source of much of the information about mushrooms that were formally described by male scholars of the time, including Carolus Clusius (1526–1609) and Francis van Sterbeeck (1630–1693). A number of paintings—from The Mushroom Seller (Felice Boselli, 1650–1732), to Women Gathering Mushrooms (Camille Pissarro, 1830–1903), to The Mushroom Gatherers (Felix Schlesinger, 1833–1910)—portray women working with mushrooms. Numerous European travelers’ accounts from the nineteenth and twentieth centuries describe women selling or gathering mushrooms.
would sing something different: For a discussion and broad definition of polyphony see Bringhurst (2009), ch. 2, “Singing with the frogs: the theory and practice of literary polyphony.”
structures remains a mystery: For estimates of flow rates through cords and rhizomorphs see Fricker et al. (2017). It is generally thought that fungi use chemicals to regulate their development, but little is known about these growth-regulating substances (Moore et al. [2011], ch. 12.5, and Moore [2005]). How can such well-defined forms arise from a uniform mass of hyphal strands? An animal’s finger is an elaborate form. But it is made up of an elaborate combination of different sorts of cells, with its blood cells, bone cells, nerve cells, and all the rest. Mushrooms are elaborate forms too, but they are sculpted tufts of one type of cell: hyphae. How fungi make mushrooms has long proved a mystery. In 1921, the Russian developmental biologist Alexander Gurwitsch puzzled over the development of mushrooms. A mushroom’s stalk, the ring around its stalk, and its cap are all made of hyphae, tousled like “shaggy uncombed hair.” This is what baffled him. Building a mushroom from nothing but hyphae is like trying to build a face from nothing but muscle cells. For Gurwitsch, the way hyphae grew together to make complex forms was one of the central riddles in all of developmental biology. An animal’s organization is specified at the earliest point in their development. Animal form arises from highly organized parts; regularity gives rise to further regularity. But the form of mushrooms arises from less organized parts. A regular form arises from an irregular material (von Bertalanffy [1933], pp. 112–17). Inspired in part by mushroom growth, Gurwitsch hypothesized that the development of organisms was guided by fields. Iron filings can be rearranged using a magnetic field. In an analogous way, Gurwitsch advanced, the arrangement of cells and tissues within an organism could be shaped by form-giving biological fields. Gurwitsch’s field theory of development has been picked up by a number of contemporary biologists. Michael Levin, a researcher at Tufts University in Boston, describes how all cells are bathed in a “rich field of information,” whether made up of physical, chemical, or electrical cues. These fields of information help to explain the way that complex forms can arise (Levin [2011] and [2012]). A study published in 2004 built a mathematical model that simulated fungal mycelial growth—a “cyberfungus” (Meskkauskas et al. [2004], Money [2004b], and Moore [2005]). In the model, each hyphal tip is able to influence the behavior of other hyphal tips. The study reports that mushroom-like forms can emerge when all the hyphal tips follow exactly the same rules of growth. These findings imply that mushrooms’ forms can emerge from the “crowd behavior” of hyphae without the need for the sort of top-down developmental coordination found in animals and plants. But for this to work, tens of thousands of hyphal tips must obey the same sets of rules at the same time, and switch to different sets of rules at the same time—a modern reframing of Gurwitsch’s riddle. The researchers who created the cyberfungus hypothesize that developmental changes might be coordinated using a cellular “clock,” but no such mechanism has yet been identified, and the means by which living fungi coordinate their development remains a mystery.
was where it fruited: For microtubule motors see Fricker et al. (2017); for Serpula in Haddon Hall see Moore (2013b), ch. 3; for a discussion of the role of flow in fungal development see Alberti (2015) and Fricker et al. (2017). Flow rates in fungal hyphae range from 3 to 70 micrometers per second, sometimes more than a hundred times faster than passive diffusion alone (Abadeh and Lew [2013]). Alan Rayner is keen on the river analogy because rivers are “systems that both shape, and are shaped by their landscape.” A river flows between its banks. In the process, it shapes the banks that it flows within. Rayner understands hyphae to be blunt-ended rivers that flow within banks that they build for themselves. As in any flow system, pressure is everything. Hyphae absorb water from their surroundings. The inward flow of water increases the pressure in the network. But pressure itself doesn’t lead to flow. For material to flow through mycelium, hyphae have to make space for it to flow into. This is hyphal growth. Hyphal contents flow toward hyphal growing tips. Water flows through a mycelial network toward a rapidly inflating mushroom. If one reverses the pressure gradients, one reverses the flow (Roper et al. [2013]). Hyphae appear to be able to regulate flow in more precise ways, however. A study published in 2019 traced the movement of nutrients and signaling compounds through hyphae in real time. In certain large hyphae, the flow of cellular fluid changed direction every few hours, allowing signaling compounds and nutrients to flow along the network in both directions. For around three hours, flow occurred in one direction. For the next three hours, flow occurred in the other direction. How hyphae are able to control the flow of material inside them isn’t known, but by rhythmically changing the direction of cellular flow, substances are distributed more efficiently through the network. The authors speculate that coordinated opening and closing of hyphal pores are a “major factor” in the coordination of bidirectional flow along transport hyphae (Schmieder et al. [2019], see also commentary by Roper and Dressaire [2019]). “Contractile vacuoles” are another way that fungi might direct flow through themselves. These are tubes within hyphae along which waves of contraction are able to pass, and which have been reported to play a part in transport through mycelial networks (Shepherd et al. [1993], Rees et al. [1994], Allaway and Ashford [2001], and Ashford and Allaway [2002]).
the researchers wryly observed: Roper et al. (2013), Hickey et al. (2016), and Roper and Dressaire (2019). Videos available on YouTube: “Nuclear dynamics in a fungal chimera,” www.youtube.com/watch?v=_FSuUQP_BBc [accessed October 29, 2019]; “Nuclear traffic in a filamentous fungus,” www.youtube.com/watch?v=AtXKcro5o30 [accessed October 29, 2019].
hundreds of times higher: Cerdá-Olmedo (2001) and Ensminger (2001), ch. 9.
is far from proven: For “the most intelligent” see Cerdá-Olmedo (2001); for avoidance response see Johnson and Gamow (1971) and Cohen et al. (1975).
different kinds of “other”: Many aspects of mycelial life are influenced by light, from mushroom development to relationship-building with other organisms—the dreaded rice blast fungus only infects its plant hosts at night (Deng et al. [2015]). For light sensing in fungi see Purschwitz et al. (2006), Rodriguez-Romero et al. (2010), and Corrochano and Galland (2016); for sensing surface topography see Hoch et al. (1987) and Brand and Gow (2009); for sensitivity to gravity see Moore (1996), Moore et al. (1996), Kern (1999), Bahn et al. (2007), and Galland (2014).
even like a brain: Darwin and Darwin (1880), p. 573. For arguments in favor of “root-brains” see Trewavas (2016) and Calvo Garzón and Keijzer (2011); for arguments against brain analogies see Taiz et al. (2019); for an introduction to the “plant intelligence” debate see Pollan, “The Intelligent Plant” (2013).
a massively parallel basis: For behavior of hyphal tips see Held et al. (2019).
mycelial networks so quickly: For fairy rings see Gregory (1982).
options that remained: electricity: Some researchers have reported sudden hyphal contractions, or twitches, that might be used to transmit information. But they aren’t regular enough to be useful on a moment-to-moment basis. See McKerracher and Heath (1986a and 1986b), Jackson and Heath (1992), and Reynaga-Peña and Bartnicki-García (2005). Some propose that information can be transmitted across mycelial networks by changing the patterns of flow within the network, in some cases changing the direction of flow in rhythmic oscillations (Schmieder et al. [2019] and Roper and Dressaire [2019]). This is a promising line of research, and it may be helpful to think of mycelial networks as a type of “liquid computer,” many versions of which have been built and deployed in systems from fighter jets to nuclear reactor control systems (Adamatzky [2019]). However, changes in mycelial flow are still too slow to explain many phenomena. The regular pulses of metabolic activity that pass across mycelial networks are a plausible way for mycelial networks to coordinate their behavior but are also too slow to explain many phenomena (Tlalka et al. [2003, 2007], Fricker et al. [2007a and 2007b, and 2008]). The poster organism for network living is the puzzle-solving slime mold. Although they’re not fungi, slime molds have evolved ways to coordinate their sprawling, shape-shifting bodies and provide a helpful model for thinking about the challenges and opportunities faced by mycelial fungi. They grow more quickly than fungal mycelium, which makes them easier to study. Slime molds communicate between different parts of themselves using rhythmic pulses that ripple down the branches of their networks in rolling waves of contraction. Branches that have found food produce a signaling molecule that increases the strength of contraction. Stronger contractions cause a greater volume of cellular contents to flow along that branch of the network. For a given contraction, more material will pass along a shorter route than a longer route. The more material passes along a route, the more it is strengthened. It is a feedback loop that allows the organism to redirect itself along “successful” routes at the expense of less “successful” ones. Pulses from the different parts of its network combine, interfere, and reinforce one another. In this way, slime molds can integrate information from its various branches and solve complex routing problems without needing a special place to do so (Zhu et al. [2013], Alim et al. [2017], and Alim [2018]).
important role in fungal lives: One researcher observed in the mid-1980s that “fungal electrobiology is about as far as one can get from the present mainstream of biological research” (Harold et al. 1985). Nevertheless, fungi have since been found to respond to electrical stimulation in potentially surprising ways. Treating mycelium with bursts of electrical current can substantially increase mushroom crops (Takaki et al. [2014]). Crops of the highly prized matsutake mushroom—a mycorrhizal species that has so far resisted cultivation—can be nearly doubled by jolting the ground around its partner trees with a 50-kilovolt pulse of electricity. Researchers conducted the study following reports from matsutake pickers that bumper crops of mushrooms could be found in the area around a lightning strike several days after it hit (Islam and Ohga [2012]). For action potentials in plants see Brunet and Arendt (2015); for early reports of action potentials in fungi see Slayman et al. (1976); for a general discussion of fungal electrophysiology see Gow and Morris (2009); for “cable bacteria” see Pfeffer et al. (2012); for action potential–like waves of activity in bacterial colonies see Prindle et al. (2015), Liu et al. (2017), Martinez-Corral et al. (2019), and a summary in Popkin (2017).
food for this species: Olsson measured the speed of travel by timing the gap between stimulation and measuring a response. This estimated speed thus includes the time taken for the fungus to sense the stimulus, for the stimulus to travel from A to B, and for the response to register with the microelectrodes. The actual speed of travel of the impulse could thus be considerably faster than this estimate. The fastest rate of bulk flow measured in fungal mycelium is around 180 millimeters per hour (Whiteside et al. [2019]). The action potential–like impulses that Olsson measured traveled at 1,800 millimeters per hour.
“other individuals around it”: Olsson and Hansson (1995) and Olsson (2009). For Olsson’s recording of the change in action potential–like activity see doi.org/10.6084/m9.figshare.c.4560923.v1 [accessed October 29, 2019].
metaphor was in play: Oné Pagán points out that there is no generally accepted definition of a brain. He argues that it makes more sense to define brains in terms of what they do, rather than based on specific details of their anatomy (Pagán [2019]). For regulation of pores in fungal networks see Jedd and Pieuchot (2012) and Lai et al. (2012).
into the fungal computer: Adamatzky (2018a and 2018b).
network-based organism: For examples of network computing see van Delft et al. (2018) and Adamatzky (2016).
they are sensitive to: Adamatzky (2018a and 2018b).
“turns out to be right”: I asked Olsson why no one had followed up his studies from the 1990s. “When I presented the work at conferences people were really, really interested,” Olsson said, “but they thought it was weird.” All of the researchers I have asked about his study are fascinated and want to know more. The study has since been cited many times. But he was unable to get funding for further work into the subject. It was considered too likely to come to nothing—“too risky” in technical parlance.
before recognizable brains arose: For “archaic myth” see Pollan (2013); for ancient cellular processes underlying brain behavior see Manicka and Levin (2019). The “moving hypothesis” posits that brains evolved as a cause and a consequence of the need for animals to move around. Organisms that don’t move around aren’t faced with the same type of challenge and have evolved different types of networks to deal with the problems they face (Solé et al. [2019]).
is all that’s needed: Darwin (1871), quoted in Trewavas (2014), ch. 2. For “minimal cognition” see Calvo Garzón and Keijzer (2011); for “biologically embodied cognition” see Keijzer (2017); for plant cognition see Trewavas (2016); for “basal” cognition and degrees of cognition see Manicka and Levin (2019); for a discussion of microbial intelligence see Westerhoff et al. (2014); for a discussion of different types of “brain” see Solé et al. (2019).
flexibly remodeling themselves: For “network neuroscience” see Bassett and Sporns (2017) and Barbey (2018). Scientific advances that make it possible to grow cultures of human brain tissue in a dish—known as brain “organoids”—complicate our understanding of intelligence yet further. The philosophical and ethical questions raised by these techniques—and the absence of clear answers—are a reminder of how the limits of our own biological selves remain far from clear. In 2018, several leading neuroscientists and bioethicists published an article in Nature in which they raised some of these questions (Farahany et al. [2018]). Over the coming decades, advances in brain-tissue culturing will make it possible to grow artificial “mini-brains” that more closely mimic the functioning of human brains. The authors write that “as brain surrogates become larger and more sophisticated, the possibility of them having capabilities akin to human sentience might become less remote. Such capacities could include being able to feel (to some degree) pleasure, pain, or distress; being able to store and retrieve memories; or perhaps even having some perception of agency or awareness of self.” Some are concerned that brain organoids might one day outsmart us (Thierry [2019]).
to reach and grasp: For flatworm experiment see Shomrat and Levin (2013); for nervous systems of octopuses see Hague et al. (2013) and Godfrey-Smith (2017), ch. 3.
catastrophic global transformations: Bengtson et al. (2017) and Donoghue and Antcliffe (2010). With studied caution, Bengtson and colleagues point out that their specimens might not be actual fungi but might belong to a separate lineage of organisms resembling modern fungi in every observable way. One can understand their hesitance. The authors point out that if these mycelial fossils were true fungi, they would “overturn” our current understanding of where and how fungi first evolved. Fungi do not fossilize well, and exactly when fungi first branched off the tree of life is disputed. DNA-based methods—using the so-called “molecular clock”—suggest that the earliest fungi diverged around a billion years ago. In 2019, researchers reported fossilized mycelium found in Arctic shale that dates from around a billion years ago (Loron et al. [2019] and Ledford [2019]). Prior to this finding, the earliest undisputed fungal fossils date from around 450 million years ago (Taylor et al. [2007]). The earliest fossilized gilled mushroom dates from around 120 million years ago (Heads et al. [2017]).
ceaselessly remodel themselves: For Barbara McClintock see Keller (1984).
to make sense of: Ibid.
oldest of life’s labyrinths: Humboldt (1849), vol. 1, p. 20.
when we said “we”: Rich (1994).
“have our samples back”: BIOMEX is one of several astrobiological projects. For BIOMEX see de Vera et al. (2019); for the EXPOSE facility see Rabbow et al. (2009).
“limitations of terrestrial life”: For “limits and limitations” quote see Sancho et al. (2008); for a review of organisms sent into space, including lichens, see Cottin et al. (2017); for lichens as models for astrobiological research see Meeßen et al. (2017) and de la Torre Noetzel et al. (2018).
be understood in isolation: Wulf (2015), ch. 22.
neither could survive alone: For a discussion of Schwendener and the dual hypothesis see Sapp (1994), ch. 1.
“believe in Schwendener’s theory”: Sapp (1994), ch. 1; for “sensational romance” see Ainsworth (1976), ch. 4. Some of Beatrix Potter’s biographers have suggested that she was a proponent of Schwendener’s dual hypothesis, and it is possible she changed her mind over the course of her life. Nonetheless, in 1897, in a letter to Charles MacIntosh, a rural postman and amateur naturalist, she appeared to take a clear stance on the question: “You see we do not believe in Schwendener’s theory, and the older books say that the lichens pass gradually into hepaticas, through the foliaceous species. I should like very much to grow the spore of one of those large flat lichens, and also the spore of a real hepatica in order to compare the two ways of sprouting. The names do not matter as I can dry them. If you could get me any more spores of the lichen and the hepatica when the weather changes I should be very much obliged” (Kroken [2007]).
entirely unexpected: converging: The tree is one of the founding images in modern theories of evolution, and famously the only illustration in Darwin’s On the Origin of Species. Darwin was by no means the first to deploy the image. For centuries, the branching form of trees has provided a framework for human thought in fields from theology to mathematics. Perhaps most familiar are genealogical trees, which have their roots in the Old Testament (the Tree of Jesse).
relationships at the other: For a debate about Schwendener’s portrayal of lichens see Sapp (1994), ch. 1, and Honegger (2000); for Albert Frank and “symbiosis” see Sapp (1994), ch. 1, Honegger (2000), and Sapp (2004). Frank first used the word “symbiotismus” (which translates literally as “symbiotism”).
described them as “microlichens”: Ancestors of green sea slugs—Elysia viridis—ingested algae that continued to live within their tissues. Green sea slugs obtain their energy from sunlight, as a plant would. For new symbiotic discoveries see Honegger (2000); for “animal lichens” see Sapp (1994), ch. 1; for “microlichens” see Sapp (2016).
of inter-kingdom collaboration: For Huxley quote see Sapp (1994), p. 21.
“look like fairy tales”: For the eight percent estimate see Ahmadjian (1995); for a greater area than tropical forests see Moore (2013a), ch. 1; for “hung in hashtags” see Hillman (2018); for the diversity of lichen habitats, including erratics and lichens that live on insects, see Seaward (2008); for the interview with Knudsen see aeon.co/videos/how-lsd-helped-a-scientist-find-beauty-in-a-peculiar-and-overlooked-form-of-life [accessed October 29, 2019].
a “clay-like” consistency: For “every monument” quote see twitter.com/GlamFuzz [accessed October 29, 2019]; for Mount Rushmore see Perrottet (2006); for Easter Island heads see www.theguardian.com/world/2019/mar/01/easter-island-statues-leprosy [accessed October 29, 2019].
been able to form: For lichens’ approach to weathering see Chen et al. (2000), Seaward (2008), and Porada et al. (2014); for lichens and soil formation see Burford et al. (2003).
to make a life: For the history of panspermia and related ideas see Temple (2007) and Steele et al. (2018).
now known as astrobiology: In response to Lederberg’s concerns about interplanetary infection, NASA developed ways to sterilize spacecraft before departure from Earth. These have not been entirely successful: There is a thriving volunteer population of bacteria and fungi aboard the International Space Station (Novikova et al. [2006]). When the Apollo 11 mission returned from the first trip to the moon in 1969, the astronauts were isolated in stringent quarantine in a converted Airstream trailer for three weeks (Scharf [2016]).
several hours a day: It had been known that bacteria are capable of acquiring DNA from their surroundings since the work of Frederick Griffith in the 1920s, later confirmed by Oswald Avery and his colleagues in the early 1940s. What Lederberg showed was that bacteria could actively exchange genetic material with each other—a process known as “conjugation.” For a discussion of Lederberg’s findings see Lederberg (1952), Sapp (2009), ch. 10, and Gontier (2015b). Viral DNA has had a profound influence on the history of animal life: It is thought that viral genes played key roles in the evolution of placental mammals from their egg-laying ancestors (Gontier [2015b] and Sapp [2016]).
the domains of life: Bacterial DNA is found in the genomes of animals (for a general discussion see Yong [2016], ch. 8). Bacterial and fungal DNA is found in plant and algal genomes (Pennisi [2019a]). Fungal DNA is found in lichen-forming algae (Beck et al. [2015]). Horizontal gene transfer is pervasive in fungi (Gluck-Thaler and Slot [2015], Richards et al. [2011], and Milner et al. [2019]). At least eight percent of the human genome started off in viruses (Horie et al. [2010]).
potentially catastrophic consequences: For foreign DNA “short-circuiting” evolution on Earth see Lederberg and Cowie (1958).
within twenty-four hours: For hostile conditions in space see de la Torre Noetzel et al. (2018).
“degree of biological activity”: Sancho et al. (2008).
with no apparent problems: Even at 18 kilograys of gamma irradiation, samples of Circinaria gyrosa only suffered a seventy percent reduction in photosynthetic activity. At 24 kilograys, photosynthetic activity was reduced by ninety-five percent but wasn’t eliminated entirely (Meeßen et al. [2017]). To put these results in context, one of the most radiotolerant organisms ever documented, an archaea isolated from deep-sea hydrothermal vents (appropriately named Thermococcus gammatolerans), can withstand levels of gamma irradiation up to 30 kilograys (Jolivet et al. [2003]). For a summary of lichen space studies see Cottin et al. (2017), Sancho et al. (2008), and Brandt et al. (2015); for effects of high-dose irradiation on lichens see Meeßen et al. (2017), Brandt et al. (2017), and de la Torre et al. (2017); for tardigrades in space see Jönsson et al. (2008).
“They inform us”: Some disciplines are routinely “informed” by lichens. Lichens are so sensitive to some forms of industrial pollution that they are used as reliable indicators of air quality—“lichen deserts” extend downwind of urban areas and can be used to map the zone affected by industrial pollution. In some cases, lichens serve as indicators in a more literal sense. They are used by geologists to determine the age of rock formations (a discipline known as lichenometry). And litmus, the pH-sensitive dye used to make the indicator paper found in all school science departments, comes from a lichen.
where photosynthesis happens: Recent work by Thijs Ettema and his group at Uppsala University suggest that eukaryotes arose within archaea. The exact sequence of events remains much debated (Eme et al. [2017]). Bacteria have long been thought of as having no internal cellular structures, known as “organelles.” This view is changing. Many bacteria appear to have organelle-like structures that perform specialized functions. For a discussion see Cepelewicz (2019).
“intimacy of strangers”: Margulis (1999); Mazur (2009), “Intimacy of Strangers and Natural Selection.”
that themselves contain bacteria: For “fusion and merger” see Margulis (1996); for origins of endosymbiosis see Sapp (1994), chs. 4 and 11; for Stanier quote see Sapp (1994), p. 179; for “serial endosymbiosis theory” see Sapp (1994), p. 174; for bacteria within bacteria within insects see Bublitz et al. (2019); for Margulis’s original paper (under the name Sagan) see Sagan (1967).
“sum of its parts”: For “quite analogous” quote see Sagan (1967); for “remarkable examples” quote see Margulis (1981), p. 167. For de Bary, in 1879, the most significant implication of symbiosis was that it could result in evolutionary novelty (Sapp [1994], p. 9). “Symbiogenesis” (“becoming by living together”) was the term given to the process by which symbiosis could give rise to new species by its earliest Russian proponents, Konstantin Mereschkowsky (1855–1921) and Boris Mikhaylovich Kozo-Polyansky (1890–1957) (Sapp [1994], pp. 47–48). Kozo-Polyansky included several references to lichens in his work. “One should not think that lichens are just a simple sum of certain algae and fungi. Rather, they have many specific features found neither in algae nor in fungi…everywhere—in its chemistry, its shape, its structure, its life, its distribution—the composite lichen exhibits new features not characteristic of its separated components” (Kozo-Polyansky trans. [2010], pp. 55–56).
“twentieth-century biology”: For Dawkins and Dennett quotes, among others, see Margulis (1996).
as fungal hyphae do: “The evolutionary ‘tree of life’ seems like the wrong metaphor,” the geneticist Richard Lewontin remarked. “Perhaps we should think of it as an elaborate bit of macramé” (Lewontin [2001]). It’s not entirely fair on trees. The branches of some species can fuse with each other. It is a process known as “inosculation,” from the Latin osculare, which means “to kiss.” But look at the tree nearest to you. The chances are that it forks more than it fuses. The branches of most trees are not like fungal hyphae, which meld with each other as part of their daily practice. Whether the tree is an appropriate metaphor for evolution has been debated for decades. Darwin himself worried about whether the “coral of life” would make a better image, though he decided in the end that it would make things “excessively complicated” (Gontier [2015a]). In 2009, in one of the most acrimonious upwellings of the tree question, New Scientist published an issue that proclaimed on its cover that “Darwin was wrong.” “Uprooting Darwin’s tree,” shrieked the editorial. Predictably, it inflamed a furious response (Gontier [2015a]). Amid the storm of reaction a letter sent by Daniel Dennett stands out: “What on earth were you thinking when you produced a garish cover proclaiming that ‘Darwin was wrong’…?” You can understand why Dennett was cross. Darwin wasn’t wrong. It is just that he came up with his theory of evolution before DNA, genes, symbiotic mergers, and horizontal gene transfer were known to exist. Our understanding of the history of life has been transformed by these discoveries. But Darwin’s central thesis that evolution proceeds by natural selection is not contested—though the extent to which it is the primary driving force in evolution is debated (O’Malley [2015]). Symbiosis and horizontal gene transfer provide new ways that novelty can be generated; they are new co-authors of evolution. But natural selection remains the editor. Nonetheless, in the light of symbiotic mergers and horizontal gene transfer, many biologists have begun to reimagine the tree of life as a reticulate meshwork formed as lineages branch, fuse, and entangle one another: a “network,” or a “web,” a “net,” a “rhizome,” or a “cobweb” (Gontier [2015a] and Sapp [2009], ch. 21). The lines on these diagrams knot and melt into each other, connecting different species, kingdoms, and even domains of life. Links loop in and out of the world of viruses, genetic entities not even considered to be alive. If anyone wanted a new poster organism for evolution they needn’t look far. This is a vision of life that resembles fungal mycelium more than anything else.
form their relationship afresh: In some lichens, specialized dispersal structures called “soredia” form, which consist of fungal and algal cells. In some cases, a newly germinated lichen fungus might team up with a photobiont that doesn’t quite satisfy its needs and survive as a small “photosynthetic smudge” known as a “prethallus” until the real thing comes along (Goward [2009c]). Some lichens can disassemble and reassemble without producing spores. If certain lichens are placed in a petri dish with the right kind of nutrients, the partners disentangle and creep apart. Once separated, they can re-form their relationship (though usually imperfectly). In this sense, lichens are reversible. At least in some cases, the honey can be stirred out of the porridge. However, to date only in the case of a single lichen—Endocarpon pusillum—have the partners been separated from each other, grown apart, and then recombined to form all the stages of the lichen, including functional spores—known as a “spore-to-spore” resynthesis (Ahmadjian and Heikkilä [1970]).
“see the lichen itself”: The symbiotic nature of lichens presents some interesting technical problems. Lichens have long been small nightmares for taxonomists. As the situation stands, lichens are referred to by the name of the fungal partner. For example, the lichen that arises through the interaction of the fungus Xanthoria parietina and the alga Trebouxia irregularis is known as Xanthoria parietina. Similarly, the combination of the fungus Xanthoria parietina and the alga Trebouxia arboricola is known as Xanthoria parietina. Lichen names are a synecdoche, in that they refer to a whole by reference to a part (Spribille [2018]). The current system implies that the fungal component of the lichen is the lichen. But this isn’t true. Lichens emerge out of a negotiation between several partners. “To see lichens as fungi,” Goward bemoans, “is to miss seeing lichens altogether” (Goward [2009c]). It is as if chemists called any compound that contained carbon—from diamond to methane to methamphetamine—carbon. You’d be forced to admit that they might be missing something. This is more than semantic grumbling. To name something is to acknowledge that it exists. When any new species is found, it is “described” and given a name. And lichens do have names, plenty of them. Lichenologists aren’t taxonomically ascetic. It’s just that the only names they can give glance off the phenomenon they aim to describe. It is a structural issue. Biology is built around a taxonomic system that has no way to recognize the symbiotic status of lichens. They are literally unnameable.
worlds writ small: Sancho et al. (2008).
rehydrated thirty days later: de la Torre Noetzel et al. (2018).
legacies of the relationship: For unique lichen compounds and human uses see Shukla et al. (2010) and State of the World’s Fungi (2018); for metabolic legacies of lichen relationships see Lutzoni et al. (2001).
thousands of years old: For a report from the Deep Carbon Observatory see Watts (2018).
nine thousand years old: For lichens in deserts see Lalley and Viles (2005) and State of the World’s Fungi (2018); for lichens within rocks see de los Ríos et al. (2005) and Burford et al. (2003); for Antarctic Dry Valleys see Sancho et al. (2008); for liquid nitrogen see Oukarroum et al. (2017); for lichen longevity see Goward (1995).
to make interplanetary journeys: Sancho et al. (2008).
any living cell whatsoever: For the shock of ejection see Sancho et al. (2008) and Cockell (2008). In a number of studies, bacteria have proved to be more resistant to high temperatures and shock pressures than lichens. For reentry see Sancho et al. (2008).
the question remains open: Sancho et al. (2008) and Lee et al. (2017).
depending on their circumstances: For origins of lichens see Lutzoni et al. (2018) and Honegger et al. (2012). There is a lot of debate about the identity of ancient lichen-like fossils and their relationship to extant lineages. Marine lichen-like organisms have been found dating from 600 million years ago (Yuan et al. [2005]) and some argue that these marine lichens played a role in the movement of lichens’ ancestors onto the land (Lipnicki [2015]). For multiple evolution of lichens and re-lichenization see Goward (2009c); for de-lichenization see Goward (2010); for optional lichenization see Selosse et al. (2018).
in each other’s company: Hom and Murray (2014).
symbiotic way of life: For “the song, not the singer” see Doolittle and Booth (2017).
well be other planets: Hydropunctaria maura used to be known as Verrucaria maura (or “warty midnight”). For a long-term study of the arrival of lichens on a newly born island see the case of Surtsey at www.anbg.gov.au/lichen/case-studies/surtsey.html [accessed October 29, 2019].
as well as nouns: For “wholes” and “collections of parts” see Goward (2009a).
centuries of painstaking scrutiny: Spribille et al. (2016).
“one fungus and one alga”: For a discussion of diversity of fungi within lichens see Arnold et al. (2009); for additional partners in wolf lichens see Tuovinen et al. (2019) and Jenkins and Richards (2019).
what living organisms are: For “It doesn’t matter what you call it” see Hillman (2018). Goward has formulated a definition of lichens that takes account of these recent findings: “The enduring physical byproduct of lichenization defined as a process whereby a nonlinear system comprising an unspecified number of fungal, algal and bacterial taxa give rise to a thallus [the shared body of the lichen] viewed as an emergent property of its constituent parts” (Goward 2009b).
“blob on a dish”: For lichens as microbial reservoirs see Grube et al. (2015), Aschenbrenner et al. (2016), and Cernava et al. (2019).
“it hard to relate”: For queer theory for lichens see Griffiths (2015).
Or perhaps y’all: See Gilbert et al. (2012) for a more detailed breakdown of how microbes confuse different definitions of biological individuality. For more on microbes and immunity see McFall-Ngai (2007) and Lee and Mazmanian (2010). Some propose alternative definitions of biological individuals based on the “common fate” of the living system. For instance, Frédéric Bouchard proposes that “A biological individual is a functionally integrated entity whose integration is linked to the common fate of the system when faced with selective pressures from the environment” (Bouchard 2018).
that they actually exist: Gordon et al. (2013) and Bordenstein and Theis (2015).
be fraught with tension: For infections caused by gut bacteria see Van Tyne et al. (2019).
“We are all lichens”: Gilbert et al. (2012).
and they answer me: Sabina, from a recording by Gordon Wasson, quoted in Schultes et al. (2001), p. 156.
bounded sense of self: For a brief summary of clinical studies into psychedelics see Winkelman (2017); for an extended discussion see Pollan (2018).
act like trip wires: Hughes et al. (2016).
onto a major vein: For the timing and height of ants’ death grips see Hughes et al. (2011) and Hughes (2013); for orientation see Chung et al. (2017). There are many different species of Ophiocordyceps fungi, and many different species of carpenter ant, but each ant is host to only one species of fungus, and each species of fungus can only control one species of ant (de Bekker et al. [2014]). Different fungus-ant pairings are particular about their choice of death site. Some fungi cause their insect avatars to bite onto twigs, some onto bark, and some onto leaves (Andersen et al. [2009] and Chung et al. [2017]).
over the ants’ behavior: For fungal proportion of ant biomass see Mangold et al. (2019); for visualization of fungal network within ant bodies see Fredericksen et al. (2017).
manipulation of ant behavior: For the hypothesis that fungal manipulation takes place by chemical means see Fredericksen et al. (2017); for chemicals produced by Ophiocordyceps see de Bekker et al. (2014); for a discussion of Ophiocordyceps and ergot alkaloids see Mangold et al. (2019).
minds to manipulate: For fossilized leaf scars see Hughes et al. (2011).
or less equal measure: For McKenna quote see Letcher (2006), p. 258.
cultures and spiritual practices: Schultes et al. (2001), p. 9. For wide-ranging if sometimes uncritical discussions of intoxication in the animal world see Siegel (2005) and Samorini (2002).
caused by convulsive ergotism: For a discussion of Amanita muscaria see Letcher (2006), chs. 7–9. Some hypothesize that the accusers in the Salem witch trials were afflicted by convulsive ergotism (Caporael, 1976 and Matossian, 1982) although their arguments have been robustly countered by Spanos and Gottleib (1976). Known in the Middle Ages and Renaissance as Saint Anthony’s fire, ergot-induced visions and psycho-spiritual anguish are thought to have inspired contemporary visions of hell. For Bosch see Dixon (1984). Livestock, too, are vulnerable to ergot poisoning. “Sleepy grass,” “drunk grass,” and the “ryegrass staggers” are all named after their effects on cattle, horses, and sheep (Clay [1988]). Ergot fungi also have powerful medicinal effects and have been used for hundreds of years by midwives to stop postpartum bleeding. Henry Wellcome, the entrepreneur whose endowment founded the Wellcome Trust, researched reports into the medicinal effects of ergot, the grain fungus. He recorded that ergot was regarded by midwives in sixteenth-century Scotland, Germany, and France “to be of remarkable and certain efficacy” in inducing uterine contractions and controlling bleeding after childbirth. It was from these herbwives or midwives that male physicians learned of the therapeutic properties of ergot, which forms the basis of the drug ergometrine, still used today to treat heavy bleeding following childbirth (Dugan [2011], pp. 20–21). It was for their reputation as obstetric drugs that Albert Hofmann began investigating them at Sandoz Laboratories in the 1930s, a research program that led to the synthesis of LSD in 1938. For a discussion of ergot alkaloids, their history and uses, see Wasson et al. (2009), “A Challenging Question and My Answer.”
accounts of mushroom use: For a discussion of the history of psilocybin mushroom use in Mexico see Letcher (2006), ch. 5; Schultes (1940); and Schultes et al. (2001), “Little Flowers of the Gods.” For the Sahagún quote see Schultes (1940).
aloft by feathered deities: Letcher (2006), p. 76.
“of the hominid mind”: For McKenna and the Tassili painting and quote see McKenna (1992), ch. 6; for a discussion of McKenna and the Tassili painting see Metzner (2005), pp. 42–43; for a more critical discussion see Letcher (2006), pp. 37–38.
a master of the art: A paper published in 2019 analyzed the residues inside a pouch made from a fox snout found in a ritual bundle excavated in Bolivia, dating from more than a thousand years ago. The researchers found traces of multiple psychoactive compounds—including cocaine (from coca), DMT, harmine, and bufotenine. The analysis provided tentative evidence of psilocin—a psychoactive breakdown product of psilocybin—which, if true, would suggest that psilocybin mushrooms had been present in the ritual bundle (Miller et al. [2019]). The Eleusinian Mysteries—a celebration of Demeter, the goddess of grain and harvest, and her daughter Persephone—were one of the major religious festivals in ancient Greece. As part of the celebrations, initiates drank a cup of a liquid known as “kykeon.” Following the drink, initiates experienced ghostly apparitions and awe-inspiring ecstatic and visionary states. Many described being permanently changed by their experience (Wasson et al. [2009], ch. 3). Although the identity of kykeon remained a carefully guarded secret, it is very likely to have been a mind-altering brew—a notorious scandal erupted when it was found that Athenian aristocrats had been drinking kykeon at home with their guests at dinner parties (Wasson et al. [1986], p. 155). There were no registration lists for the rites of Eleusis, and so there is some uncertainty about exactly who attended. However, most Athenian citizens were initiates, and many notable figures are thought to have attended, including Euripides, Sophocles, Pindar, and Aeschylus. Plato wrote about the experience of mystery initiations in some detail in his Symposium and in Phaedrus, using language that refers clearly to the rites at Eleusis (Burkett [1987], pp. 91–93). Aristotle did not refer explicitly to the mysteries at Eleusis but did refer to mystery initiations—a reference that is probably compatible with the Eleusinian Mysteries given the preeminence of the Eleusinian rites by the mid-fourth century BC. Hofmann, along with Gordon Wasson and Carl Ruck, hypothesized that kykeon was made from ergot fungi growing on grain, somehow purified to avoid the dreadful symptoms associated with its accidental consumption (Wasson et al. [2009]). McKenna speculated that the priests at Eleusis distributed psilocybin mushrooms (McKenna [1992], ch. 8). Others have suggested a preparation made from opium poppies. There are other examples of possible use of mushrooms in ancient religious contexts. In central Asia a religious cult sprang up around the use of a mind-altering preparation called “soma.” Soma induced ecstatic states, and devotional hymns to soma are recorded in the Rigveda, an ancient text dating from around 1500 BCE. Like kykeon, the identity of the drink remains unknown. Some—most notably Wasson—have argued that it was the red-and-white-spotted mushroom Amanita muscaria (for a discussion see Letcher [2008], ch. 8). McKenna—true to form—suggested that psilocybin mushrooms are more likely candidates. Others have suggested cannabis. There is no unequivocal evidence either way.
minds of their hosts: For the reference to the fictional monsters see Yong (2017). In 2018, researchers at the University of Ryukyus in Japan discovered that several species of cicada had domesticated Ophiocordyceps fungi that lived within their body (Matsuura et al. [2018]). Like many insects that live mostly on sap, cicadas depend on symbiotic bacteria to produce several essential nutrients and vitamins, without whom they can’t survive. But in a number of Japanese species of cicada, the bacteria have been replaced by a species of Ophiocordyceps. It is the last thing one would expect. Ophiocordyceps are brutally effective killers that have honed their abilities over tens of millions of years. Yet somehow, over the course of their long history together, Ophiocordyceps have become essential life partners of the cicadas. What’s more, it has happened at least three times in three separate lineages of cicada. Domesticated Ophiocordyceps are a reminder that the distinctions between “beneficial” and “parasitic” microbes are not always clear-cut.
nostrum for eternal youth: For immunosuppressant drugs see State of the World’s Fungi (2018), “Useful Fungi”; for nostrum for eternal youth see Adachi and Chiba (2007).
of its insect host: Coyle et al. (2018); for “whacky” discovery see twitter.com/mbeisen/status/1019655132940627969 [accessed October 29, 2019].
nervous systems remain intact: For a description of the behavior of infected flies see Hughes et al. (2016) and Cooley et al. (2018); for “flying saltshakers of death” see Yong (2018).
a very different story: For the Kasson study see Boyce et al. (2019) and the discussion in Yong (2018). It isn’t the first report that insect-manipulating fungi might control their hosts using chemicals that can also alter human minds; cousins of Ophiocordyceps fungi are eaten alongside psilocybin mushrooms in some indigenous ceremonies in Mexico (Guzmán et al. [1998]).
how, exactly, isn’t known: Cathinone has been reported to increase aggression in ants, and it might be responsible for the hyperactive behaviors observed in infected cicadas (Boyce et al. [2019]).
when they hunt elk: See Ovid (1958), p. 186; for Amazonian shamanism see Viveiros de Castro (2004); for Yukaghir people see Willerslev (2007).
“fungus in ant’s clothing”: See Hughes et al. (2016). Neuromicrobiology is a relatively new field and understanding of gut microbes’ influence on animal behaviors, cognition, and psychological states remains patchy (Hooks et al. [2018]). Nonetheless, some patterns are starting to emerge. Mice, for example, require a healthy gut microflora to develop a functional nervous system in the first place (Bruce-Keller et al. [2018]). If one knocks out the microbiome of adolescent mice before they have had the chance to develop a functional nervous system, they develop cognitive defects. These include memory problems and difficulty identifying objects (de la Fuente-Nunez et al. [2017]). The most dramatic demonstrations come from studies that swap the microbiota between different mouse lines. When “timid” mouse strains are given fecal transplants from “normal” strains, they lose their caution. Likewise, if “normal” strains are inoculated with the microbes of the “timid” strains, they acquire “exaggerated caution and hesitancy” (Bruce-Keller et al. [2018]). Differences in gut microbiota in mice affect the ability of mice to forget the experience of pain (Pennisi [2019b] and Chu et al. [2019]). Many gut microbes produce chemicals which influence the activity of the nervous system, including neurotransmitters and short chain fatty acids (SCFAs). More than 90 percent of the serotonin in our bodies—the neurotransmitter that when abundant makes us feel happy, and when depleted makes us feel depressed—is produced in our guts, and gut microbes play a major role in regulating its production (Yano et al. 2015). Two studies have investigated the effect of transplanting the fecal microbiota of depressed human patients into germ-free mice and rats. The animals developed symptoms of depression, including anxiety and a loss of interest in pleasurable behaviors. These studies suggest that not only can imbalances in the gut microbiota result in depression but that the same imbalances may be responsible for depressed behavior in mice and in humans (Zheng et al. [2016] and Kelly et al. [2016]). Further studies on humans have shown that certain probiotic treatments can reduce symptoms of depression, anxiety, and the occurrence of negative thoughts (Mohajeri et al. [2018] and Valles-Colomer et al. [2019]). However, a multibillion-dollar probiotics industry hovers around the field of neuromicrobiology, and a number of researchers have pointed out the tendency to overhype findings. Gut communities are complex, and manipulating them is a challenge. There are so many variables involved that few studies are able to identify causal links between the action of specific microbes and specific behaviors (Hooks et al. [2018]).
in the pond, and…: For a full exposition of the “extended phenotype” see Dawkins (1982); for “tightly limited speculation” see Dawkins (2004); for a discussion of fungal manipulation of insect behavior in terms of extended phenotypes see Andersen et al. (2009), Hughes (2013 and 2014), and Cooley et al. (2018).
is simply catching up: For a discussion of the “first wave” of psychedelic research in the 1950s and ’60s see Dyke (2008) and Pollan (2018), ch. 3.
history of modern medicine: For the Johns Hopkins study see Griffiths et al. (2016); for the NYU study see Ross et al. (2016); for the interview with Griffiths see Fantastic Fungi: The Magic Beneath Us, directed by Louis Schwartzberg; for a general discussion, including the record “treatment effect” sizes, see Pollan (2018), ch. 1.
defined sense of self: For a study on psilocybin-occasioned mystical experience see Griffiths et al. (2008); for the role of awe in psychedelic-assisted psychotherapy see Hendricks (2018).
with the natural world: For the role of psilocybin in treating tobacco addiction see Johnson et al. (2014 and 2015); for psilocybin-induced “openness” and life satisfaction see MacLean et al. (2011); for a general discussion of the role of psychedelics in treating addiction see Pollan (2018), ch. 6, pt. 2; for sense of connection with the natural world see Lyons and Carhart-Harris (2018) and Studerus et al. (2011). There is a long tradition of Native American communities using the psychedelic cactus peyote as a treatment for alcoholism. Between the 1950s and the 1970s, a number of studies investigated the possibility that psilocybin and LSD could be used to treat drug addiction. Several reported positive effects. In 2012, a meta-analysis pooled the data from the most rigorously controlled trials. It reported that a single dose of LSD had a beneficial effect on alcohol misuse that lasted up to six months (Krebs and Johansen [2012]). In an online survey designed to investigate the “natural ecology” of the phenomenon, Matthew Johnson and his colleagues analyzed accounts from more than three hundred people who reported that they had reduced their tobacco intake or stopped entirely following an experience with psilocybin or LSD (Johnson et al. [2017]).
of religious belief—exists: For “started out stone-cold” see Pollan (2018), ch. 4; for nonmaterial reality as basis for religious belief see Pollan (2018), ch. 2. Even sitters who guide and observe the sessions at Johns Hopkins have reported unexpected changes in their worldviews. One guide who had sat through dozens of psilocybin sessions described the experience: “I started out on the atheist side, but I began seeing things every day in my work that were at odds with this belief. My world became more and more mysterious as I sat with people on psilocybin” (Pollan [2018], ch. 1).
and structure of neurons: For the influence of psychedelics on the growth and architecture of neurons see Ly et al. (2018).
states of cerebral flux: For psilocybin and the DMN see Carhart-Harris et al. (2012) and Petri et al. (2012); for the effects of LSD on brain connectivity see Carhart-Harris et al. (2016b).
a change in symptoms: For the Hoffer quote see Pollan (2018), ch. 3.
new cognitive possibilities: For the Johnson quote see Pollan (2018), ch. 6; for the role of psilocybin in treating the “rigid pessimism” of depression see Carhart-Harris et al. (2012).
relationship to the world: For a discussion of ego-dissolution and “merging” see Pollan (2018), prologue and ch. 5.
humans or fungi alone: For “cool night of the mind” and “baroque” see McKenna and McKenna (1976), pp. 8–9.
continent of possible opinion: For the Whitehead quote see Russell (1956), p. 39; for “tightly limited” speculation see Dawkins (2004).
so for very long: It isn’t straightforward to estimate when exactly the first mushrooms became “magic.” The simplest approach is to assume that the ability to make psilocybin originated in the most recent common ancestor of all the fungi that make psilocybin. However, this doesn’t work because 1) psilocybin has been horizontally transferred between fungal lineages (Reynolds et al. [2018]), and 2) psilocybin biosynthesis has evolved more than once (Awan et al. [2018]). Jason Slot, a researcher at Ohio State University, made the estimate of seventy-five million years based on a hypothesis that the genes needed to make psilocybin first clustered in an ancestor of the genera Gymnopilus and Psilocybe. Slot suspects this to be the case because the other occurrences of the psilocybin gene cluster have been shown to have arisen through horizontal gene transfer.
would have quickly degenerated: For horizontal gene transfer of psilocybin gene cluster see Reynolds et al. (2018); for multiple origins of psilocybin biosynthesis see Awan et al. (2018).
which makes matters worse: Some relationships between insects and fungi involve more ambiguous manipulation, like “cuckoo fungi,” which capitalize on the social behavior of termites by producing small balls that look like termite eggs, and produce a pheromone found in real termite eggs. Termites carry the fake eggs into their nest, where they tend to them. When they fail to germinate, the fungal “eggs” are thrown into waste piles. Surrounded with a nutrient-rich compost, the cuckoo fungi sprout and are able to live free from competition with other fungi (Matsuura et al. [2009]).
that benefited the fungus: For leaf-cutter ants foraging for psilocybin mushrooms see Masiulionis et al. (2013); for gnats and other insects that eat psilocybin mushrooms and the “lure” hypothesis of psilocybin see Awan et al. (2018). Pure crystalline psilocybin is expensive, and heavy regulation makes research hard. There is some evidence that psilocybin impedes the behavior of insects and other invertebrates. In a well-known series of experiments in the 1960s, researchers gave a range of drugs to spiders to study the webs that they spun. High doses of psilocybin prevented web-building altogether. Spiders on lower doses spun looser webs, behaving “as if they were heavier.” By contrast, LSD caused the spiders to produce “unusually regular” webs (Witt [1971]). More recently, studies have found that fruit flies given metitepine, a chemical that blocks the serotonin receptors that psilocybin stimulates, lost their appetites. This has led some to suggest that psilocybin may serve to increase the appetite of flies—possibly serving to disperse fungal spores (Awan et al. [2018]). Michael Beug, a biochemist and mycologist at Evergreen State College, is among the researchers who argue against the psilocybin-as-deterrent hypothesis. Mushrooms are a fruit. Just as an apple tree makes its fruit conspicuous to facilitate the dispersal of its seeds, so fungi produce mushrooms to facilitate the dispersal of their spores. Psilocybin, as Beug points out, is found in high concentrations in mushrooms of psilocybin-producing species but in negligible quantities in the mycelium of most psilocybin-producing species (though not all: Psilocybe caerulescens and Psilocybe hoogshagenii/semperviva are reported to contain significant concentrations of psilocybin in their mycelium). Yet it is the mycelium, not the mushrooms, that is in most need of defense. Why would psilocybin mushrooms go to the trouble to defend their fruit while leaving their mycelium unprotected (Pollan [2018], ch. 2)?
human relationships with fungi: Other mammals, too, are known to eat species of psilocybin mushroom with no ill effects. Beug, the biochemist and mycologist in charge of the poisoning reports filed with the North American Mycological Association, has received many such accounts. “With horses or cows, it may or may not be accidental,” Beug told me. In some cases, however, animals do seem to seek them out. “Some dogs will see their owners picking psilocybin mushrooms and take an interest—and then will eat the mushrooms again and again with effects that appear familiar to the human observer.” Only once has he dealt with reports of a cat “who ate mushrooms repeatedly, and appeared to become quite ‘bemushroomed.’ ”
“visions in brilliant colors”: Schultes (1940).
“Growths that Produce Visions”: For a discussion of Wasson’s article in Life and its reach see Pollan (2018), ch. 2, and Davis (1996), ch. 4.
“had nothing to add”: For “trailing our mother” see McKenna (2012). Possibly the first account of a trip in a widely read organ was written by the journalist Sidney Katz, who published an article in the popular Canadian magazine Maclean’s entitled “My Twelve Hours as a Madman.” For a discussion see Pollan (2018), ch. 3.
“these strange deep realms”: For a discussion of Leary’s “visionary voyage” and the Harvard Psilocybin Project see Letcher (2006), pp. 198–201, and Pollan (2018), ch. 3. For Leary quote, see Leary (2005).
or driven underground: Letcher (2006), pp. 201 and 254–55; Pollan (2018), ch. 3.
“in alchemical gold”: For a discussion of the growing interest in magic mushrooms see Letcher (2006), “Underground, Overground”; for a discussion of the development of cultivation techniques see Letcher (2006), “Muck and Brass”; for the grower’s guide see McKenna and McKenna (1976).
with subtly different effects: For a discussion of The Mushroom Cultivator and the Dutch and English magic mushroom scenes see Letcher (2006), “Muck and Brass.”
inhospitable temperate climates: In Central American pastures mushrooms grow readily, and there is nothing to suggest that people actively cultivated them.
“state courthouses and jails”: For psilocybin-containing lichen see Schmull et al. (2014); for global distribution of psilocybin mushrooms see Stamets (1996 and 2005); for “occur in abundance” see Allen and Arthur (2005); for an account of the discovery of psilocybin mushrooms around the world see Letcher (2006), pp. 221–25; for “parks, housing developments” see Stamets (2005).
“the mushrooms themselves”: Schultes et al. (2001), p. 23.
James concluded: See James (2002), p. 300.
Describe the sky to me: Tom Waits/Kathleen Brennan, “Green Grass,” on Real Gone (2004).
nearly all terrestrial organisms: For the evolution of land plants see Lutzoni et al. (2018), Delwiche and Cooper (2015), and Pirozynski and Malloch (1975); for biomass of plants see Bar-On et al. (2018).
Mollusks thrived: For early biocrusts see Beerling (2019), p. 15, and Wellman and Strother (2015); for Ordovician life see web.archive.org/web/20071221094614/http://www.palaeos.com/Paleozoic/Ordovician/Ordovician.htm#Life [accessed October 29, 2019].
make it onto land: For incentives of life on land for the ancestors of plants see Beerling (2019), p. 155. Perhaps unsurprisingly, there has not always been consensus on this topic. The idea was first proposed by Kris Pirozynski and David Malloch in their 1975 paper “The origin of land plants: a matter of mycotropism.” In it they made the claim that “land plants never had any independence [from fungi], for if they had, they could never have colonised the land.” It was a radical idea at the time because it posited that symbiosis had been a major force in one of the most significant evolutionary developments in the history of life. Lynn Margulis ran with the idea and described symbiosis as “the moon that pulled the tide of life from its oceanic depths to dry land and up into the air” (Beerling [2019], pp. 126–27). For a discussion of fungi and their role in the evolution of land plants see Lutzoni et al. (2018), Hoysted et al. (2018), Selosse et al. (2015), and Strullu-Derrien et al. (2018).
can’t afford to sustain: For the proportion of plant species that form mycorrhizal associations see Brundrett and Tedersoo (2018). The seven percent of land plant species that don’t form mycorrhizal associations have evolved alternative strategies, like parasitism or carnivory. This figure may be even less than seven percent: Recent studies have found that plants that are traditionally thought of as “non-mycorrhizal”—those in the cabbage family for example—form relationships with non-mycorrhizal fungi that provide benefit to the plant as mycorrhizal associations do (van der Heijden et al. [2017], Cosme et al. [2018], and Hiruma et al. [2018]).
an evolutionary refrain: For fungi in seaweeds—“mycophycobiosis”—see Selosse and Tacon (1998); for “soft green balls” see Hom and Murray (2014).
Field marveled: A group of living plants called “liverworts” are thought to be the earliest-diverging lineage of land plants and may stretch back more than four hundred million years. Liverworts in the genera Treubia and Haplomitrium may provide us with the best glimpse at early plant life (Beerling [2019], p. 25). There are a number of lines of evidence besides fossils. The genetic apparatus responsible for the chemical signals, used by plants to communicate with mycorrhizal fungi, is identical in all living plant groups, implying that it was present in the common ancestor of all plants (Wang et al. [2010], Bonfante and Selosse [2010], and Delaux et al. [2015]). The surviving ancestors of the earliest land plants—the liverworts—form relationships with the most ancient lineages of mycorrhizal fungi (Pressel et al. [2010]). Furthermore, the most recent estimates of the timings suggest that fungi made the transition to land earlier than the ancestors of modern land plants, indicating that it would have been nearly impossible for early plants not to have encountered fungi (Lutzoni et al. [2018]).
fungi (mykes) into being: For evolution of roots see Brundrett (2002) and Brundrett and Tedersoo (2018).
“fungus-roots, myco-rhizas”: For the evolution of thinner, more opportunistic roots see Ma et al. (2018). The diameter of fine roots varies but is typically between 100 and 500 micrometers. Among one of the most ancient lineages of mycorrhizal fungi—the arbuscular mycorrhizal fungi—transport hyphae are around 20 to 30 micrometers in diameter, and their fine absorptive hyphae are as thin as 2 to 7 micrometers (Leake et al. [2004]).
figures are certainly underestimates: For a third to a half of soil biomass see Johnson et al. (2013); for estimates of lengths of mycorrhizal fungi in top ten centimeters of soil see Leake and Read (2017). These estimates are based on the lengths of mycorrhizal mycelium found in different ecosystems and take into account mycorrhizal type and land-use type (Leake et al. [2004]).
“tree from the soil”: For Frank’s work on mycorrhizal fungi see Frank (2005); for a discussion of Frank’s work see Trappe (2005).
grown in sterile conditions: For a description of Frank’s experiments see Beerling (2019), p. 129. One of Frank’s most vocal critics was the botanist and later the dean of Harvard Law School Roscoe Pound, who denounced his propositions as “decidedly fishy.” Pound took the side of more “sober” authors who maintained that mycorrhizal fungi were “probably injurious by taking nourishment properly belonging to the tree.” “In all cases,” Pound thundered, symbiosis “results advantageously to one of the parties, and we can never be sure that the other would not have been nearly as well off, if left to itself” (Sapp [2004]).
The Lord of the Rings: Tolkien (2014), “For you little gardener” see vol. II, “Farewell to Lórien”; for “Sam Gamgee planted” see vol. III, “The Grey Havens.”
think it’s probable: For rapid evolution in the Devonian see Beerling (2019), pp. 152 and 155; for the drop in carbon dioxide see Johnson et al. (2013) and Mills et al. (2017). There are alternative hypotheses regarding the triggers for the drop in atmospheric carbon dioxide. For example, carbon dioxide and other greenhouse gases are emitted by volcanism and other tectonic activity. If levels of volcanic carbon dioxide emissions fell, then levels of atmospheric carbon dioxide would also fall, potentially triggering a period of global cooling (McKenzie et al. [2016]).
climates start to change: For mycorrhizal assistance to the plant boom in the Devonian see Beerling (2019), p. 162; for a discussion of weathering in light of mycorrhizal activity see Taylor et al. (2009).
composition of the atmosphere: Mills used the COPSE model (Carbon, Oxygen, Phosphorus, Sulphur, and Evolution), which examines the cycling of all these elements over long periods of evolutionary time in relation to a “simplified representation of the land biota, atmosphere, oceans and sediments” (Mills et al. [2017]).
“of life on Earth”: Mills et al. (2017); for Field’s experiments on mycorrhizal responses to ancient climates see Field et al. (2012).
upon a winning strategy: For a general discussion of mycorrhizal evolution see Brundrett and Tedersoo (2018). The group of fungi that helped plants onto land, and which thrive in grasslands and tropical forests—arbuscular mycorrhizal fungi—are thought to have evolved only once. Arbuscular mycorrhizal fungi are the ones that grow into feathery lobes within plant cells. The type that dominates in temperate forests—ectomycorrhizal fungi—has arisen on more than sixty separate occasions (Hibbett et al. [2000]). These fungi—which include truffles—weave themselves into mycelial sleeves around plant root tips, as Frank observed in the late nineteenth century. Orchids have their own type of mycorrhizal relationship, with its own evolutionary history. So do plants in the blueberry family, or Ericaceae (Martin et al. [2017]). Field and her colleagues are studying a completely different group of mycorrhizal fungus that was only discovered in the late 2000s, known as the Mucoromycotina. It occurs across the plant kingdom and is thought to be as old as the earliest land plants, but had gone entirely unnoticed despite decades of study. There may well be more hiding in plain sight (van der Heijden et al.[ 2017], Cosme et al. [2018], Hiruma et al. [2018], and Selosse et al. [2018]).
some less so: For strawberry experiments see Orrell (2018); for a further study on the influence of mycorrhizal fungi on plant-pollinator interactions see Davis et al. (2019).
I often wonder: For basil see Copetta et al. (2006); for tomatoes see Copetta et al. (2011) and Rouphael et al. (2015); for mint see Gupta et al. (2002); for lettuce see Baslam et al. (2011); for artichokes see Ceccarelli et al. (2010); for Saint-John’s-wort and echinacea see Rouphael et al. (2015); for bread see Torri et al. (2013).
plants and mycorrhizal fungi: Rayner (1945).
demanding flurry of interaction: For the “social function of intellect” see Humphrey (1976).
their own exclusive benefit: For “reciprocal rewards” see Kiers et al. (2011). Kiers and her colleagues were able to be so precise because she used an artificial system. The plants weren’t normal plants but root “organ cultures”—disembodied roots that grow without shoots or leaves. Nonetheless, the ability of plants and fungi to preferentially transfer nutrients or carbon to more favorable partners has been demonstrated with whole plants growing in soil (Bever et al. [2009], Fellbaum et al. [2014], and Zheng et al. [2015]). Exactly how plants and fungi are able to regulate these fluxes is not well understood, but it appears to be a general feature of the relationship (Werner and Kiers [2015]).
or anything in between: Not all plant and fungal species are able to control their exchange to the same degree. Some species of plant inherit an ability to preferentially supply carbon to favorable fungal partners. Some species just don’t have this talent (Grman [2012]). Some plants depend more on their fungal partners than others. Some species, like those that produce dust seeds, won’t germinate without a fungus present; many plants will. Some plants don’t give anything back to the fungus when they’re young but start to reward the fungus when they get older, a lifestyle that Field calls the “take now, pay later” approach (Field et al. [2015]).
of supply and demand: For a study on resource inequality see Whiteside et al. (2019).
of carbon in return: Kiers and her colleagues measured the speed of transport through the network, observing maximum speeds of more than fifty micrometers per second—roughly a hundred times faster than passive diffusion—as well as regular changes, or oscillations, in the direction of flow through the network (Whiteside et al. [2019]).
different outcome: For the role of context in mycorrhizal associations see Hoeksema et al. (2010) and Alzarhani et al. (2019); for the impact of phosphorus on plant “pickiness” see Ji and Bever (2016). Even within plant and fungal species, there is a large amount of variation between the behavior of individual plants and fungi (Mateus et al. [2019]).
small and back again: For the estimate of number of trees on Earth see Crowther et al. (2015).
what they’re actually doing: For a discussion of knowledge gaps in mycorrhizal research see Lekberg and Helgason (2018).
of excitement and frustration: For a discussion of plant and fungal exchange and how it is controlled see Wipf et al. (2019). In one study, a single fungus connected to two different species of plant at the same time—flax and sorghum—supplied more nutrients to flax, even though sorghum supplied the fungus with more carbon. Based on a cost-benefit analysis, one would expect the fungus to supply more nutrients to sorghum (Walder et al. [2012] and Hortal et al. [2017]). Some species of plant are even more extreme and don’t provide any carbon to their mycorrhizal partners at all. In these instances, exchange between partners appears not to be based on reciprocal rewards exchanged tit for tat. Of course, there may be many other benefits and costs that aren’t being taken into account, but it’s hard to measure so many variables at once. For this reason, most studies focus on a small number of easily manipulated parameters, like carbon and phosphorus. This provides fine detail but makes it difficult to extend the findings to complex real-world scenarios (Walder and van der Heijden [2015] and van der Heijden and Walder [2016]).
ten meters per year: For the influence of mycorrhizal fungi on forest dynamics on a continental scale see Phillips et al. (2013), Bennett et al. (2017), Averill et al. (2018), Zhu et al. (2018), Steidinger et al. (2019), and Chen et al. (2019); for the migration of trees following the retreat of the Laurentide Ice Sheet see Pither et al. (2018).
arrived somewhere new: For the study at the University of British Columbia see Pither et al. (2018) and commentary by Zobel (2018); for a study on mycorrhiza-mediated encroachment of plants onto heathlands see Collier and Bidartondo (2009); for co-migration of plants and their mycorrhizal partners see Peay (2016).
the salty coastal soils: Rodriguez et al. (2009).
one species became two: Osborne et al. (2018), with commentary by Geml and Wagner (2018).
beyond their prior limits: For involution see Hustak and Myers (2012).
than in agriculture: For a discussion of the role of plant-fungal relations in adaptation to climate change see Pickles et al. (2012), Giauque and Hawkes (2013), Kivlin et al. (2013), Mohan et al. (2014), Fernandez et al. (2017), and Terrer et al. (2016); for “alarming deterioration” see Sapsford et al. (2017) and van der Linde et al. (2018). Mycorrhizal relationships can pattern the aboveground world in a number of ways, for example through their influence on soil nutrient cycles. One can think of soil nutrient cycles as chemical weather systems. The chemical “climate” set up by different types of fungi helps to determine what kind of plants grow where. The influence of different plants, in turn, feeds back on the behavior of mycorrhizal fungi. Arbuscular mycorrhizal (AM) fungi—the ancient lineage that grows inside plant cells—steer chemical weather systems in a completely different direction than ectomycorrhizal (EM) fungi—the type that has evolved multiple times, and grows around plant roots in a mycelial sleeve. Unlike AM fungi, EM fungi descended from free-living decomposer fungi. As a result, they are better at decomposing organic matter than arbuscular mycorrhizal fungi. On an ecosystem scale, this makes a big difference. EM fungi thrive in colder climates where decomposition is slower. AM fungi thrive in warmer, wetter climates where decomposition is faster. EM fungi tend to compete with free-living decomposers and reduce the rate at which carbon cycles. AM fungi tend to promote the activity of free-living decomposers and increase the rate at which carbon cycles. EM fungi cause more carbon to become immobilized in the upper soil layers. AM fungi cause more carbon to trickle down into lower soil layers and become immobilized there (Phillips et al. [2013], Craig et al. [2018], Zhu et al. [2018], and Steidinger et al. [2019]). Mycorrhizal relationships can also influence the ways that plants interact with each other. In some situations, mycorrhizal fungi increase the diversity of plant life by easing competitive interactions between plants, allowing less dominant plant species to establish themselves (van der Heijden et al. [2008], Bennett and Cahill [2016], Bachelot et al. [2017], and Chen et al. [2019]). In others, they reduce diversity by allowing plants to exclude competitors. In some cases, plant feedbacks with mycorrhizal communities span generations, sometimes known as “legacy effects” (Mueller et al. [2019]). A study into the effects of the deadly pine beetle on the West Coast of North America found that the survival of young pine seedlings varied depending on where their mycorrhizal communities came from. If grown with mycorrhizal fungi taken from areas where adult pines had been killed by pine beetles, seedlings had higher rates of mortality. Mycorrhizal communities allowed the effects of pine beetles to cascade through generations of trees (Karst et al. [2015]).
“future of civilization depends”: Howard (1945), chs. 1 and 2.
urgency of the crisis: For the doubling of crop production see Tilman et al. (2002); for agricultural emissions and plateau of crop yields see Foley et al. (2005) and Godfray et al. (2010); for the dysfunction using phosphorus fertilizer see Elser and Bennett (2011); for loss of crops see King et al. (2017); for thirty football fields see Arsenault (2014); for projections of global food demand see Tilman et al.
plants, too, will suffer: For a study of traditional agricultural practices in China see King (1911); for Howard’s concern about the “life of the soil” see Howard (1940); for damage to soil microbial communities by agriculture see Wagg et al. (2014), de Vries et al. (2013), and Toju et al. (2018).
mycelium in the soil: For the Agroscope study see Banerjee et al. (2019); for the impact of plowing on mycorrhizal communities see Helgason et al. (1998); for a comparison of organic and inorganic practices on mycorrhizal communities see Verbruggen et al. (2010), Manoharan et al. (2017), and Rillig et al. (2019).
ever lived on Earth: For “ecosystem engineers” see Banerjee et al. (2018); for the role of mycorrhizal fungi in soil stability see Leifheit et al. (2014), Mardhiah et al. (2016), Delavaux et al. (2017), Lehmann et al. (2017), Powell and Rillig (2018), and Chen et al. (2018); for the impact of mycorrhizal fungi on soil water absorption see Martínez-García et al. (2017); for carbon stored in soil see Swift (2001) and Scharlemann et al. (2014); for an analysis of soil carbon bound up in fungi see Clemmensen et al. (2013) and Lehmann et al. (2017); for estimates of the number of organisms in the soil see Berendsen et al. (2012); and for the estimate of the number of people who have ever lived see www.prb.org/howmanypeoplehaveeverlivedonearth/ [accessed October 29, 2019].
can even reduce them: For the impact of mycorrhizal fungi on plant resistance to stress see Zabinski and Bunn (2014), Delavaux et al. (2017), Brito et al. (2018), Rillig et al. (2018), and Chialva et al. (2018). Other studies have found that by inoculating crops with the endophytic fungi that live in plants’ shoots, they can dramatically increase crops’ tolerance to drought and heat stress (Redman and Rodriguez [2017]).
Field pointed out: For unpredictable outcomes of mycorrhizal associations on crop yields see Ryan and Graham (2018), but see Rillig et al. (2019) and Zhang et al. (2019); for Field’s studies on crop responses to mycorrhizal fungi see Thirkell et al. (2017); for variability of mycorrhizal response between crop varieties see Thirkell et al. (2019).
to damaged gut flora: For a discussion of the effectiveness of commercial mycorrhizal products see Hart et al. (2018) and Kaminsky et al. (2018). There are a growing number of products that use fungal endophytes of plants to protect crops. In 2019 the US Environmental Protection Agency gave approval to a fungal pesticide designed to be delivered to plants by bees (Fritts [2019]).
needs of plants above their own: See Kiers and Denison (2014).
better cultivate one another: See Howard (1940), ch. 11.
very same fungal network: Bateson (1987), ch. 4.94; Merleau-Ponty (2002), pt. 1, “The Spatiality of One’s Own Body and Motility.”
net-like, entangled fabric: Humboldt (1845), vol. 1, p. 33. Translation here by Anna Westermeier. The sentence containing the phrase “net-like, entangled fabric” (Eine allgemeine Verkettung, nicht in einfacher linearer Richtung, sondern in netzartig verschlugenem Gewebe, […], stellt sich allmählich dem forschenden Natursinn dar) does not occur in the published English translation of 1849.
via a fungal pathway: The Russian botanist was F. Kamienski, who published his speculation about Monotropa in 1882 (Trappe [2015]); for a study with radioactive glucose see Björkman (1960).
net and fabric real: For a discussion of Humboldt’s “net-like, entangled fabric” see Wulf (2015), ch. 18.
in a natural environment: For Read’s study with radioactive carbon dioxide see Francis and Read (1984). In 1988, Edward I. Newman, the author of a classic review on the subject of shared mycorrhizal networks, commented that “if this phenomenon is widespread, it could have profound implications for the functioning of ecosystems.” Newman identified five routes by which shared mycorrhizal networks might make an impact: 1) seedlings may quickly become linked into a large hyphal network and begin to benefit from it at an early stage; 2) one plant may receive organic materials (such as energy-rich carbon compounds) from another via hyphal links, perhaps sufficient to increase the “receiver’s” growth and chance of survival; 3) the balance of competition between plants may be altered if they are obtaining mineral nutrients from a common mycelial network, rather than separately taking them up from the soil; 4) mineral nutrients may pass from one plant to another, thus perhaps reducing competitive dominance; and 5) nutrients released from dying roots may pass directly via hyphal links to living roots without ever entering the soil solution (Newman [1988)].
from plenty to scarcity: Simard et al. (1997). Simard grew seedlings of three species of tree in a forest in British Columbia. Two of the species—paper birch and Douglas fir—form relationships with the same type of mycorrhizal fungus. The third species—western red cedar—forms relationships with a quite unrelated type of mycorrhizal fungus. This meant that she could be fairly sure that the birch and fir shared a network, while the cedar just shared root space with no direct fungal connections (although this approach does not show beyond doubt that the plants remain unconnected—a point for which her study was later criticized). In an important twist on Read’s previous studies, Simard exposed pairs of tree seedlings to carbon dioxide labeled with two different radioactive isotopes of carbon. With only a single isotope, it’s impossible to follow the bidirectional movement of carbon between plants. One might well find that a receiver plant has taken up labeled carbon from a donor plant. But the donor plant might have taken up just as much carbon from the receiver and one would have no way of knowing. Simard’s approach allowed her to calculate the net movement between plants.
“The Wood Wide Web”: Read (1997).
“resources within the community”: For root grafts see Bader and Leuzinger (2019); for “we should place” see Read (1997). Root grafts have received comparatively little attention in the last few decades, yet account for a number of interesting phenomena, such as “living stumps,” which continue to survive long after they have been cut. Root grafts can occur between roots of a single individual, individuals of the same species, and even individuals of different species.
“enter the public consciousness”: Barabási (2001).
phenomenon using a network model: For a study of the World Wide Web see Barabási and Albert (1999); for a general discussion of developments in network science in the mid-1990s see Barabási (2014); for “more in common” see Barabási (2001); for “cosmic web” and network structure of the universe see accessible summary by Ferreira (2019), also Gott (2016), ch. 9, Govoni et al. (2019), and Umehata et al. (2019), with commentary from Hamden (2019).
an important ecological role: For a summary of the studies that have found biologically meaningful transfer of resources between plants see Simard et al. (2015). For “two hundred eighty kilograms” see Klein et al. (2016) and commentary by van der Heijden (2016). The study by Klein et al. (2016) was unusual in measuring the transfer of carbon between mature trees in a forest. The trees were of similar age, meaning there were no obvious source–sink gradients between them.
mycorrhizal partner would: For studies that report little or variable benefit see van der Heijden et al. (2009) and Booth (2004). On the whole, experiments that have found clear benefits to plants have looked at species that form relationships with a group known as ectomycorrhizal fungi. Studies that have found more ambiguous effects have examined one of the oldest groups, the arbuscular mycorrhizal fungi.
space with one another: For a discussion of the variety of opinions within the research community and the differences in interpretation of the evidence see Hoeksema (2015). Part of the problem is that experimenting on shared mycorrhizal networks is complicated in controlled lab conditions, let alone in wild soils. To start with, it’s very difficult to show that two plants are connected by the very same fungus. Living systems are leaky. There are countless ways that a radioactive label applied to one plant could end up in another. What’s more, any experiment on networks must compare networked with non-networked plants. The problem is that networks are the default mode. Some researchers sever the fungal ties between plants by moving the position of fine mesh barriers between them. Others dig trenches to separate plants, but it’s hard to know whether these interventions are causing collateral damage.
do Simard’s fir seedlings: For multiple origins of mycoheterotrophy see Merckx (2013). Darwin was a great orchid enthusiast and spent time puzzling over how orchids could survive with such small seeds. In 1863, in a letter to Joseph Hooker, the director of Kew Gardens, Darwin wrote that although he had “not a fact to go on,” he had a “firm conviction” that germinating orchid seeds “are parasites in early youth on cryptogams [or fungi].” It was not until three decades later that fungi were shown to be crucial for the germination of orchid seeds (Beerling [2019], p. 141).
he reflected fondly: For the snow plant see Muir (1912), ch. 8; for the “thousand invisible cords” see Wulf (2015), ch. 23. This was a recurring theme for Muir, who also wrote of “innumerable unbreakable cords,” besides his more well-known line: “When we try to pick out anything by itself, we find it hitched to everything else in the universe.”
remain sinks forever: Source–sink dynamics regulate plant photosynthesis. When the products of photosynthesis accumulate, the rate of photosynthesis is reduced. Mycorrhizal fungal networks increase the rate of plant photosynthesis by acting as a carbon sink, thereby preventing the buildup of the products of photosynthesis, which would normally slow the process (Gavito et al. [2019]).
living plants were sinks: For Simard shading fir seedlings see Simard et al. (1997); for dying plants see Eason et al. (1991).
areas of scarcity: For the switching of direction of carbon flow see Simard et al. (2015).
soon be weeded out: For a discussion of the evolutionary puzzle see Wilkinson (1998) and Gorzelak et al. (2015).
in the shaded understory: For sharing of surplus resources as a “public good” see Walder and van der Heijden (2015). Another possibility is that the receiver plants harbor a multitude of different fungal species. Plant A might benefit from plant B’s community of fungi when conditions change. Diverse fungal communities offer insurance against environmental uncertainty (Moeller and Neubert [2016]).
to move between them: For kin selection mediated by shared mycorrhizal connections see Gorzelak et al. (2015), Pickles et al. (2017), and Simard (2018). A number of species of fern have employed a form of kin selection, or parental “care,” using shared mycorrhizal networks, and have probably done so for millions of years (Beerling [2019], pp. 138–40). These fern species (in the genera Lycopodium, Huperzia, Psilotum, Botrychium, and Ophioglossum) have two phases of their life cycle. Spores germinate into a structure called a “gametophyte.” Gametophytes are small underground structures that don’t photosynthesize. They are where fertilization takes place. Once a gametophyte has been fertilized, it develops into the aboveground adult phase called a “sporophyte.” The sporophyte is where photosynthesis takes place. Gametophytes are only able to survive underground because they are supplied with carbon via mycorrhizal networks, shared with the adult sporophytes. It is a case of “take now, pay later.”
between source and sink: For bidirectional transport see Lindahl et al. (2001) and Schmieder et al. (2019).
into a digital utopia: For studies showing benefits of plant participation in shared mycorrhizal networks see Booth (2004), McGuire (2007), Bingham and Simard (2011), and Simard et al. (2015).
are cut back: For a study showing no benefit of participation in a shared mycorrhizal network see Booth (2004); for amplification of competition by shared mycorrhizal networks see Weremijewicz et al. (2016) and Jakobsen and Hammer (2015).
reducing their growth: For “fungal fast lane” and fungal transport of poisons see Barto et al. (2011 and 2012), and Achatz and Rillig (2014).
have barely been explored: For hormones see Pozo et al. (2015); for nuclear transport through mycorrhizal fungal networks see Giovannetti et al. (2004 and 2006); for transport of RNA between a parasitic plant and its host see Kim et al. (2014); for RNA-mediated interaction between plants and fungal pathogens see Cai et al. (2018).
and some for consumption: For bacterial use of fungal networks see Otto et al. (2017), Berthold et al. (2016), and Zhang et al. (2018); for influence of “endohyphal” bacteria on fungal metabolism see Vannini et al. (2016), Bonfante and Desirò (2017), and Deveau et al. (2018); for bacterial farming in thick-footed morel see Pion et al. (2013) and Lohberger et al. (2019).
and their wasp allies: Babikova et al. (2013).
Johnson pondered: For plant-plant information transfer between tomato plants see Song and Zeng (2010); for stress-signaling between Douglas fir and pine seedlings see Song et al. (2015a); for transfer between Douglas fir and pine seedlings see Song et al. (2015b).
“is actually being sent”: For electrical signaling in plants see Mousavi et al. (2013), Toyota et al. (2018), and commentary by Muday and Brown-Harding (2018); for plant electrical response to herbivory see Salvador-Recatalà et al. (2014). Many questions remain about the chemical conversations that take place between plant roots and fungi that allow them to form their relationships in the first place. Read once tried to grow the mycoheterotrophic snow plant—Muir’s “glowing pillar of fire”—and made some progress before hitting “a brick wall.” “It was fascinating,” Read recalled, “the fungus grew toward the seed and showed huge excitement and interest—it fluffed up and said ‘hi.’ There’s clearly signaling going on. The sadness is that we never had plants big enough to let it go further. These signaling questions are questions that the next generation of researchers will have to work on.”
connected to each other: Beiler et al. (2009 and 2015). Other studies have looked at the architecture of shared mycorrhizal networks based on which species interact, but these have not been explicit about the spatial arrangement of trees within an ecosystem. These include Southworth et al. (2005), Toju et al. (2014 and 2016), and Toju and Sato (2018).
serious disruption will ensue: If one drew lines between the trees in Beiler’s forest plot randomly, each tree would end up with a similar number of links between them. Trees with an exceptionally high or exceptionally low number of links would be rare. One could calculate an average number of links per tree, and most trees would fall somewhere around this number. In network language this characteristic node would represent the network’s “scale.” In reality we see something different. In Beiler’s plots, Barabási’s map of the Web, or a network of airplane routes, a few highly connected hubs account for the vast majority of connections in the network. The nodes in this type of network differ from one another so greatly that there is no such thing as a characteristic node. The networks have no scale, and are described as “scale-free.” Barabási’s discovery of scale-free networks in the late 1990s helped to provide a framework to model the behavior of complex systems. For the difference between well-connected and poorly connected hubs see Barabási (2014), “The Sixth Link: The 80/20 Rule”; for vulnerability of scale-free networks see Albert et al. (2000) and Barabási (2001); for a discussion of scale-free networks in the natural world see Bascompte (2009).
range of fungal species: For a discussion of different types of shared mycorrhizal networks and their contrasting architectures see Simard et al. (2012); for a discussion of fusion between different arbuscular mycorrhizal networks see Giovannetti et al. (2015). Just because two trees are linked, it doesn’t mean that they are linked in the same way. Some types of alder tree, for instance, associate with a very low number of fungal species, which in turn tend not to associate with plants other than alders. This means that alders have an isolationist tendency and form closed, inward-facing networks with one another. In terms of the overall architecture of a patch of forest, an alder grove would be a “module”—well connected inside but only sparsely inter-linked (Kennedy et al. [2015]). We are used to this idea. Plot a network of your acquaintances on a piece of paper. Then consider that each link is a relationship. How many of your relationships are equivalent? What do you forfeit when you count your relationship with your sister, your third cousin, your friend from work, and your landlord as equivalent links in your social network? The network scientists Nicholas Christakis and James Fowler describe how influential a given link in a social network is in terms of its “contagion.” You may have a social link between your sister and your landlord, but the amount of influence, the contagion, each of these links carries will differ. Christakis and Fowler have a theory known as “three degrees of influence” to describe how social influence drops off after three degrees of separation (Christakis and Fowler [2009], ch. 1).
shimmering, unceasing turnover: Prigogine and Stengers (1984), ch. 1.
are sneezes, and orgasms: For ecosystems as complex adaptive systems see Levin (2005); for the dynamic nonlinear behavior of ecosystems see Hastings et al. (2018).
“who connects to whom”: For Simard’s parallels between shared mycorrhizal networks and neural networks see Simard (2018). Researchers in other fields share this view. Manicka and Levin (2019) argue that tools so far only used to study brain function should be transferred to other biological arenas to overcome the problem of “thematic silos” that segregate fields of biological inquiry. In neuroscience, a “connectome” is a map of neural connections within a brain. Would it be possible to plot the mycorrhizal connectome of an ecosystem? “If I had unlimited funding,” Beiler told me, “I would sample the hell out of a forest. Then you could get a very precise view of the network—who exactly is associating with whom and where—and also a broad view of the system as a whole.” For an example of a study in neuroscience that takes an analogous approach see Markram et al. (2015).
fungi at these junctions: Simard (2018).
have interacted with plants: “Many fungi interact with roots in a loose way,” Selosse explained to me. “Take truffles, for example. Of course, you can find truffle mycelium growing on the roots of its official ‘host’ trees. But you can also find it in the roots of surrounding plants which aren’t its normal hosts and don’t usually form mycorrhizal associations at all. These casual relationships aren’t strictly mycorrhizal, but they nonetheless exist.” For more on non-mycorrhizal fungi that link different plants see Toju and Sato (2018).
our being in it: Le Guin (2017).
climate-change-inducing pollutant: Many of these early plants—classed as lycophytes and pteridophytes—produced comparatively little “true” wood and are thought to have been made up mostly of a bark-like material known as “periderm” (Nelsen et al. [2016]).
gigatons of carbon: For three trillion trees see Crowther et al. (2015). The current best estimates of global biomass distributions put plants at around eighty percent of the total biomass on Earth. Around seventy percent of this plant fraction is estimated to be “woody” stem and trunk, making wood around sixty percent of global biomass (Bar-On et al. [2018]).
matrix of molecular rings: For the composition of wood and relative abundances of lignin and cellulose see Moore (2013a), ch. 1.
emitted around ten gigatons: For an introduction to wood decomposition and enzymatic combustion see Moore et al. (2011), ch. 10.7, and Watkinson et al. (2015), ch. 5; for eighty-five gigatons see Hawksworth (2009); for 2018 global carbon budget see Quéré et al. (2018). The other major group of decomposing fungi are brown rot fungi, so called because they cause wood to turn a brown color. Brown rot fungi largely digest the cellulose component of wood. But they are able, too, to use radical chemistry to accelerate the breakdown of lignin. Their approach is slightly different from white rot fungi. Rather than use free radicals to break apart lignin molecules, they produce radicals that react with lignin and make it vulnerable to bacterial decay (Tornberg and Olsson [2002]).
their apparatus of decay: How so much wood could go un-rotted for such a long time has been the subject of considerable discussion. In a paper published in Science in 2012, a team headed by David Hibbett argued that the evolution of lignin peroxidases in the white rot fungi approximately coincided with the “sharp decrease” in carbon burial at the end of the Carboniferous period, suggesting that the Carboniferous deposits may have arisen because fungi hadn’t yet evolved the ability to degrade lignin (Floudas et al. [2012], with commentary by Hittinger [2012]). This finding supported the hypothesis first proposed by Jennifer Robinson (1990). In 2016, Matthew Nelsen et al. published a paper refuting this hypothesis, on several grounds: 1) Many of the plants that formed the Carboniferous deposits responsible for large amounts of carbon burial were not major lignin producers. 2) Lignin-degrading fungi and bacteria may have been present before the Carboniferous period. 3) Significant coal seams have formed after the point at which white rot fungi are estimated to have evolved lignin-degrading enzymes. 4) If there had been no degradation of lignin before the Carboniferous period, all the carbon dioxide in the atmosphere would have been removed in less than a million years. See Nelsen et al. (2016), with commentary by Montañez (2016). The case isn’t clear-cut. The relative rates of decomposition versus carbon burial are difficult to measure, and it is hard to imagine that the ability of white rot fungi to degrade lignin and other tough components of wood, such as crystalline cellulose, would have no impact on the global levels of carbon burial (Hibbett et al. [2016]).
material escaped fungal attention: For fungal degradation of coal see Singh (2006), pp. 14–15; the “kerosene fungus” is a yeast, Candida keroseneae (Buddie et al. [2011]).
distinct field, even today: Hawksworth (2009). See also Rambold et al. (2013), who argue that “mycology should be recognized as a field in biology at eye level with other major disciplines.”
in the year 2000: For mycology in ancient China see Yun-Chang (1985); for the state of mycology in modern China and global production of mushrooms see State of the World’s Fungi (2018); for deaths by mushroom poisoning see Marley (2010).
outlet for fungal inquiry: State of the World’s Fungi (2018); Hawksworth (2009).
Or just amateurs: For a discussion of the recent history of citizen science and the “zooniverse”—a digital platform that allows people to participate in research projects across a wide number of fields—see Lintott (2019), reviewed by West (2019); for a classic discussion of “lay experts” with regard to the AIDS crisis see Epstein (1995); for a discussion of modern crowdsourced participation in science see Kelty (2010); for citizen science in ecology see Silvertown (2009); for a discussion of the history of experimental “thrifty” science as conducted at home see Werrett (2019). The work of Darwin is a notable example. For most of his life, he conducted almost all of his work at home. He bred orchids on the windowsills, apples in the orchard, racing pigeons, and earthworms on the terrace. Much of the evidence Darwin mobilized in support of his theory of evolution came from networks of amateur animal and plant breeders, and he maintained a large volume of correspondence with well-organized networks of hobbyist collectors and backyard enthusiasts (Boulter [2010]). Today, digital platforms open new possibilities. In late 2018, a low-frequency seismic hum traveled around the world, evading mainstream earthquake-detection systems. Its trajectory and identity were pieced together in an impromptu collaboration between academic and citizen seismologists interacting on Twitter (Sample [2018]).
or its “grassroots”: For a history of DIY mycology see Steinhardt (2018).
“that mycelium spreads”: McCoy (2016), p. xx.
air quality is improved: For figures on agricultural waste see Moore et al. (2011), ch. 11.6; for diapers in Mexico City see Espinosa-Valdemar et al. (2011)—when the plastic was left on, the mass loss was still an impressive seventy percent. For agricultural waste in India see Prasad (2018).
was a matsutake mushroom: For fungal proliferation at the Cretaceous-Tertiary extinction see Vajda and McLoughlin (2004); for matsutake mushrooms after Hiroshima see Tsing (2015), “Prologue.” Tsing writes in her notes that the source of this story is difficult to pin down.
out of the top: For a video of Pleurotus on cigarette butts see https://web.archive.org/web/20200429100059/https://www.youtube.com/watch?v=fCAX9P50SNU [accessed October 29, 2019].
a commonplace challenge: For a discussion of nonspecific fungal enzymes and the potential for breaking down toxins see Harms et al. (2011).
“What do we do”: In 2015, Stamets was given an award by the Mycological Society of America. In the official announcement, he was described as a “highly original, self-trained member of the mycological community who has had a huge and sustained impact on the field of Mycology” (fungi.com/blogs/articles/paul-receives-the-gordon-and-tina-wasson-award [accessed October 29, 2019]). In a 2018 interview with Tim Ferris, Stamets explained that he had been given the award for “bringing more students into mycology than anyone in history” (tim.blog/2018/10/15/the-tim-ferriss-show-transcripts-paul-stamets/ [accessed October 29, 2019]).
are white rot fungi: For DMMP see Stamets (2011), “Part II: Mycorestoration.” Note that Psilocybe azurescens is not mentioned here—Stamets told me about this in person.
antibiotics to synthetic hormones: For a summary of fungal ability to break down toxins see Harms et al. (2011); for a broader discussion of mycoremediation see McCoy (2016), ch. 10.
gold from electronic waste: For mycelial highways see Harms et al. (2011); for the mycofiltration of E. coli see Taylor et al. (2015); for the Finnish company reclaiming gold with mycelium see https://web.archive.org/web/20200429095819/https://phys.org/news/2014-04-filter-recover-gold-mobile-scrap.html [accessed October 29, 2019]. A number of studies reported mushrooms enriched in the radioactive heavy metal cesium following the nuclear fallout at Chernobyl (Oolbekkink and Kuyper [1989], Kammerer et al. [1994], and Nikolova et al. [1997]).
and we’re inside it: For a discussion of additional fungal needs see Harms et al. (2011); for challenges see McCoy (2016), ch. 10.
None has reached maturity: For CoRenewal see corenewal.org [accessed October 29, 2019]; for fungal cleanup after California fires see newfoodeconomy.org/mycoremediation-radical-mycology-mushroom-natural-disaster-pollution-clean-up/ [accessed October 29, 2019]; for Pleurotus booms in the Danish harbor see www.sailing.org/news/87633.php#.XCkcIc9KiOE [accessed October 29, 2019].
degrade polyurethane plastic: For the polyurethane digesting fungus see Khan et al. (2017); for another example of a plastic-digesting fungus see Brunner et al. (2018). The mycologist Tradd Cotter at the organization Mushroom Mountain runs a crowdsourced initiative to collect strains of fungi from unusual places; see newfoodeconomy.org/mycoremediation-radical-mycology-mushroom-natural-disaster-pollution-clean-up/ [accessed October 29, 2019].
and remained largely unavailable: For Mary Hunt see Bennett and Chung (2001). The “crowd” need not always be “non-scientists.” In 2017, a study published by the Earth Microbiome Project in Nature attracted attention for its unusual methodology. Researchers put out a call to scientists around the world for well-preserved environmental samples for inclusion in the survey of global microbial diversity (Raes [2017]).
award of $1 million: Every year Darwin competed with his cousin, a vicar, as to who could grow the largest pears by crossing the latest varieties. It was a contest that became a source of much family entertainment. See Boulter (2010), p. 31.
about a decade old: For Wu San Kwung see McCoy (2016), p. 71; for “Paris” mushrooms see Monaco (2017); for a general history of cultivation in Europe see Ainsworth (1976), ch. 4. There is a modern twist in the story of underground mushroom growing in Paris. Car ownership in Paris is falling, and several underground car parks have been converted into successful edible mushroom farms; see www.bbc.co.uk/news/av/business-49928362/turning-paris-s-underground-car-parks-into-mushrooms-farms [accessed October 29, 2019].
precursors to radical mycology: The preparation of mushrooms is certainly not limited to humans. Several species of North American squirrels are known to dry mushrooms and cache them for later (O’Regan et al. [2016]).
by any insect group: For the age of Macrotermes mounds see Erens et al. (2015); for the complexity of Macrotermes societies see Aanen et al. (2002).
passes through Macrotermes mounds: For a discussion of Macrotermes digestion and prolific metabolisms see Aanen et al. (2002), Poulsen et al. (2014), and Yong (2014).
populations of malarial mosquitoes: For termites eating “private property” see Margonelli (2018), ch. 1; for termites eating banknotes see www.bbc.co.uk/news/world-south-asia-13194864 [accessed October 29, 2019]; for a discussion of Stamets’s insect-killing fungal products see Stamets (2011), “Mycopesticides.” A study published in Science in 2019 reported that a genetically modified strain of Metarhizium eliminated nearly all of the mosquitoes in an experimental “near-natural environment” in Burkina Faso. The authors propose the use of the modified strain of Metarhizium to fight the spread of malaria (Lovett et al. [2019]).
quickly abandoned their post: For “waking up” the soil see Fairhead and Scoones (2005); for the benefits of termite earths see Fairhead (2016); for the destruction of the French garrison see Fairhead and Leach (2003).
the largest possible scale: For spiritual hierarchies see Fairhead (2016). In parts of Guinea, people plaster the walls of houses with earth harvested from the inside of Macrotermes mounds (Fairhead [2016]).
materials out of mycelium: For a discussion of materials made from fungi see Haneef et al. (2017) and Jones et al. (2019); for portabello mushrooms and batteries see Campbell et al. (2015); for fungal skin substitutes see Suarato et al. (2018).
Stamets’s termite-killing fungi: For termite-resistant mycomaterials see phys.org/news/2018-06-scientists-material-fungus-rice-glass.html [accessed October 29, 2019]. Mycelial building materials have been used in a number of high-profile exhibits, including the 2014 PS1 gallery pavilion at the Museum of Modern Art in New York, and the Shell Mycelium Installation in Kochi, in India.
“at really low cost”: For NASA growing structures in space see www.nasa.gov/directorates/spacetech/niac/2018_Phase_I_Phase_II/Myco-architecture_off_planet/ [accessed October 29, 2019]; for “self-healing” concrete using fungi see Luo et al. (2018).
shaped like a lampshade: To make the wood-mycelium composite, sawdust and corn are mixed into a damp slurry. The mixture is inoculated with fungal mycelium and loaded into plastic molds. The mycelium “runs” through the substrate, forming a cast made of interlocked mass of mycelium and partially digested wood. It is a different story for the leather and soft foam. Rather than pack the inoculated substrate into molds, it is spread on flat sheets. By controlling the growth conditions, the mycelium is persuaded to grow upward into the air. In less than a week, the spongy layer can be harvested. When compressed and tanned, it produces a material that feels remarkably like leather. If dried as it is, it forms a foam.
their mycelium will make: Bayer’s longer-term goal is to understand the biophysics of how mycelium creates physical structures. “I think about fungi as nanotech assemblers that put molecules in place,” he explained. “We’re trying to understand how the 3-D orientation of the microfibers influence the properties of the materials; their strength, durability, and flexibility.” Bayer’s vision is to develop genetically programmable fungi. With this level of control, he explained, “we’ll be able to dial in a different material. You could even have it excrete a plasticizing compound like glycerin. Then you’d have something that’s naturally more flexible and water resistant. There’s so much you could do.” Could is the operative word. Fungal genetics are byzantine and poorly understood. To insert a gene and have the fungus express it is one thing. To insert a gene and have the fungus express it in a stable and predictable way is another. To program fungal behavior by issuing a stream of genetic commands is yet another.
with a mycelial alternative: There is no precedent for building with fungi, so a lot of the research has to be done from scratch. This is a bigger focus for Bayer than straightforward production. Over the last ten years, they have invested $30 million in research. To work with mycelium in these ways requires new methods, new ways to persuade the fungus to grow, to behave differently.
“millimeter of the building”: For FUNGAR see info.uwe.ac.uk/news/uwenews/news.aspx?id=3970 and www.theregister.co.uk/2019/09/17/like_computers_love_fungus/ [both accessed October 29, 2019].
range of deadly viruses: For the importance of pollinators and pollinator decline see Klein et al. (2007) and Potts et al. (2010); for problems caused by varroa mites see Stamets et al. (2018).
more recent brain wave: For a review of fungal antiviral compounds see Linnakoski et al. (2018); for a discussion of Project BioShield see Stamets (2011), ch. 4. Stamets told me that the fungi found to have the strongest antiviral activity were agarikon (Laricifomes officinalis), chaga (Inonotus obliquus), reishi (Ganoderma spp.), birch polypore (Fomitopsis betulina), and turkey tail (Trametes versicolor). The most richly documented histories of fungal cures come from China, where medicinal mushrooms have occupied a central place in the pharmacopeia for at least two thousand years. The classic herbal dating from around AD 200, the Shennong Ben Cao, thought to be a compilation of far older orally transmitted traditions, includes several fungi still in medicinal use today, including reishi (Ganoderma lucidum) and the umbrella polypore (Polyporus umbellatus). Reishi was one of the most venerated and can be found depicted in countless paintings, carvings, and embroidery (Powell [2014]).
bees to this extent: Stamets et al. (2018).
which systems systematize systems: Haraway (2016), ch. 4.
yeasts were discovered: For yeasts in the human microbiome see Huffnagle and Noverr (2013). For sequencing of the yeast genome see Goffeau et al. (1996); for Nobel Prizes on yeast see State of the World’s Fungi (2018), “Useful Fungi.”
brewing for far longer: For a discussion of evidence for early brewing practices see Money (2018), ch. 2.
of years before humans: Lévi-Strauss (1973), p. 473.
yeasts have domesticated us: For the domestication of yeast see Money (2018), ch. 1, and Legras et al. (2007); for bread-before-beer see Wadley and Hayden (2015) and Dunn (2012). The development of agriculture affected a number of human relationships with fungi. Many fungal pathogens of plants are considered to have evolved in parallel with domesticated crops. As is the case today, domestication and cultivation provide fungal pathogens of plants with new opportunities (Dugan [2008], p. 56).
filled up with bottles: I was inspired by the excellent book Sacred Herbal and Healing Beers (Buhner [1998]).
human cultural categories: For Sumerians and The Egyptian Book of the Dead see Katz (2003), ch. 2; for Ch’orti’ see Aasved (1988), p. 757; for Dionysus see Kerényi (1976) and Paglia (2001), ch. 3.
machine that is built: For a discussion of yeast in biotechnology see Money (2018), ch. 5; for Sc2.0 see syntheticyeast.org/sc2-0/introduction/ [accessed October 29, 2019].
have never stayed clear: For rhapsodic verse see Yun-Chang (1985); Yamaguchi Sodo quoted in Tsing (2015), “Prologue,”; Magnus quoted in Letcher (2006), p. 50; Gerard quoted in Letcher (2006), p. 49.
power in different ways: Wasson and Wasson (1957), vol. II, ch. 18. The Wassons divided up much of the world into their categories. The United States (Wasson was American) was mycophobic, along with Anglo-Saxons and Scandinavians. Russia (Valentina was Russian) was mycophilic, along with Slavs and Catalans. “The Greeks,” the Wassons observed disdainfully, “have always been mycophobes.” “From beginning to end in the writings of the ancient Greeks we find not one enthusiastic word for mushrooms.” Of course, things are rarely so straightforward. The Wassons confected a binary system and were the first to dissolve its hard edges. They observed that Finns were “by tradition mycophobes,” but in areas where the Russians used to go on vacation had learned to “know and love many species.” Where exactly the reformed Finns fell between the two poles of their system the Wassons neglected to say.
what fungi actually are: For reclassification of fungi and bacteria see Sapp (2009), p. 47; for a discussion of the history of fungal taxonomy see Ainsworth (1976), ch. 10.
“what is a Variety”: For Theophrastus see Ainsworth (1976), p. 35; for the association of fungi with lightning strikes and a general discussion of the European understanding of fungi see Ainsworth (1976), ch. 2; for “The order of Fungi” and a good general history of fungal taxonomy see Ramsbottom (1953), ch. 3.
be abandoned altogether: Money (2013).
morals of the maids: Raverat (1952), p. 136.
person doing the describing: One of the first recorded taxonomic attempts to order the fungi was made in 1601, and divided mushroom species into categories of “edible” and “poisonous,” that is, the potential relationship they would have with a human body (Ainsworth [1976], p. 183). These judgments are seldom meaningful. Brewer’s yeast can be used to make bread and alcohol, yet can cause a life-threatening infection if it gets into your blood.
conceptual and ideological tinderbox: The word “mutualism” was explicitly political for the first decades of its life, describing a school of early anarchist thought. The concept of the “organism,” too, was understood in explicitly political terms by German biologists of the late nineteenth century. Rudolf Virchow understood the organism to be made up of a community of cooperating cells, each working for the good of the whole, just as a population of interdependent cooperating citizens underpinned the operation of a healthy nation-state (Ball [2019], ch. 1).
to exist at all: For “close to the margins” see Sapp (2004). The relationship between Darwin’s theory of evolution by natural selection, Thomas Malthus’s analysis of food supply and human populations, and Adam Smith’s theory of the market has received considerable scholarly attention. See for example Young (1985).
“bodily, intellectual, and moral”: Sapp (1994), ch. 2.
“for this year’s Symposium”: Sapp (2004).
free of cultural bias: For Needham see Haraway (2004), p. 106; Lewontin (2000), p. 3.
and “market gains”: Toby Kiers, professor at Vrije University in the Netherlands, is one of the leading proponents of applying “biological market frameworks” to plant and fungal interactions. Biological markets are not themselves a new idea—they have been used to think about animal behavior for decades. But Kiers and her colleagues are the first to apply them to organisms that don’t have brains (see for example Werner et al. [2014], Wyatt et al. [2014], Kiers et al. [2016], and Noë and Kiers [2018]). For Kiers, economic metaphors underpin economic models, which are helpful investigative tools. “It’s not about trying to make analogies to human markets,” she told me. Instead, “it allows us to make more testable predictions.” Rather than sweep the dizzyingly variable world of plant and fungal exchange into vague notions of “complexity” or “context-dependency,” economic models make it possible to break down dense webs of interactions and test basic hypotheses. Kiers became interested in biological markets after she found that plants and mycorrhizal fungi use “reciprocal rewards” to regulate their exchange of carbon and phosphorus. Plants that receive more phosphorus from a fungus provide it with more carbon; fungi that receive more carbon provide the plant with more phosphorus (Kiers et al. [2011]). In Kiers’s view, market models provide a way to understand how these “strategic trading behaviors” might have evolved, and how they might change in different conditions. “So far it’s been a very useful tool, even in the way that it allows us to set up different experiments,” she explained. “We might say, ‘Theory suggests that as we increase the number of partners that the trade strategy is going to change in a certain way depending on those resources.’ That allows us to set up an experiment: Let’s try changing the number of partners and see if this strategy actually changes. It’s a sounding board rather than a strict protocol.” In this case, the market frameworks are a tool, a set of stories based on human interactions that help to formulate questions about the world, to generate new perspectives. It is not to say, as Kropotkin did, that humans should base their behavior on the behavior of nonhuman organisms. Nor is it to say that plants and fungi are actually capitalist individuals making rational decisions. Of course, even if they were it is unlikely that their behavior would fit perfectly within a given human economic model. As any economist will admit, human markets don’t behave like “ideal” markets in practice. The messy complexity of human economic life spills out of the models built to house it. And in fact, fungal lives don’t fit neatly into biological market theory either. For a start, biological markets depend—like the human capitalist markets from which they derive—on being able to identify individual “traders” that act in their own interest. The truth of the matter is that it is not clear what counts as an individual “trader” (Noë and Kiers [2018]). The mycelium of a “single” mycorrhizal fungus might fuse with another and end up with several different types of nucleus—several different genomes—traveling around its network. What counts as an individual? An individual nucleus? A single interconnected network? One tuft of a network? Kiers is straightforward about these challenges. “If biological market theory is not a useful way to study interactions between plants and fungi, then we’ll stop using it.” Market frameworks are tools whose utility is not known in advance. Nonetheless, biological markets are a problem for some researchers in the field. As Kiers remarked, “This debate can get emotional with no particular reason for it to get emotional.” Perhaps it is the fact that biological market frameworks touch a sociopolitical nerve? Human economic systems are many and diverse. Yet the body of theory known as biological market frameworks bears a striking resemblance to free-market capitalism. Would it help to compare the value of economic models drawn from different cultural systems? There are many ways to attribute value. There might be other currencies that haven’t been taken into account.
treat them as such: The Internet and World Wide Web are more of a self-organizing system than many human technologies (in Barabási’s words, the World Wide Web appears to have “more in common with a cell or an ecological system than with a Swiss watch”). Nonetheless, these networks are built from machines and protocols which are not self-organizing, and which would cease to function without constant human attention.
“to make artificial dichotomies”: Sapp told me a story that illustrates how easy it is for biologists’ metaphors to become a flash point. He noticed that many portrayed larger, more complex organisms, like animals and plants, as more “successful” than the bacteria or fungi that they partnered with. Sapp gave this argument short shrift. “By what definition of success? The last time I looked, the world was primarily microbial. This planet belongs to microbes. Microbes were at the beginning and they will be at the end, long after complex ‘higher’ animals are gone. They created the atmosphere and life as we know it, they make up most of our bodies.” Sapp explained how he had observed the evolutionary biologist John Maynard Smith playing down microbes by changing a metaphor. If a microbe was gaining from a relationship, Maynard Smith called it a “microbial parasite” and the large organism the “host.” However, if the large organism was manipulating the microbe, Maynard Smith didn’t call the big organism the parasite. He changed metaphors, and called the big organism the “master” and the microbe the “slave.” Sapp’s concern lay in the fact that the microbe was either a parasite or a slave, but for Maynard Smith it could never be understood as a dominant partner manipulating the host. The microbe could never be the one in control.
robust, root, sappy, radical: For puhpowee see Kimmerer (2013), “Learning the Grammar of Animacy” and “Allegiance to Gratitude.” The Dutch primatologist Frans de Waal, frustrated at people using the charge of “anthropomorphism” to defend human exceptionalism, complains of “anthropodenial”: “the a priori rejection of shared characteristics between humans and animals when in fact they may exist” (de Waal [1999]).
“beyond his left side”: Hustak and Myers (2012).
as “typical” life-forms: Ingold asks how human thought would look different if fungi, not animals, had been taken as the “paradigmatic instance of a life-form.” He explores the implications of adopting a “fungal model” of life, arguing that humans are no less embedded in networks, it is just that our “pathways of relationship” are more difficult to see than those of fungi (Ingold [2003]).
mycologists and bacteriologists: For “Sharing resources” see Waller et al. (2018).
these extraordinary creatures: Deleuze and Guattari (2005), p. 11.
metabolic sense of them: Carrigan et al. (2015). Alcohol dehydrogenase is different from acetaldehyde dehydrogenase, another enzyme responsible for alcohol metabolism that varies in between human populations and can cause people to have trouble metabolizing alcohol.
much more ancient fascination: For the drunken monkey hypothesis see Dudley (2014). Fungal infestations have been shown to boost fruit aroma and removal by animals and birds (Peris et al. [2017]).
negative effects of inebriation: Wiens et al. (2008) and Money (2018), ch. 2.
human agricultural transformation: For consequences of biofuel production in the United States see Money (2018), ch. 5; for land-use change and biofuels see Wright and Wimberly (2013); for subsidies and carbon release see Lu et al. (2018).
drawing power in matter: Stukeley (1752).
beautiful in this world: Ladinsky (2002).