I trust that artist Rhim Lee is a visionary and all around great person, but I was a bit surprised when her TED talk had almost 1.5 million views. She is a talented speaker, funny and full of energy; her “Great Idea Worth Spreading” is a “mushroom suit” that would help nature extract our nutrients after we die. She has recently launched a company that would use her proprietary fungus that she selected for being the best at breaking down her hair, fingernail clippings, etc.
Lee should get credit for her original thinking in terms of accelerating nutrient recycling and detoxification, and for drawing attention to the process. It is an issue some of us in conservation burial have been thinking about for a couple of decades, but we have never had any where near the media coverage (My local TEDx talk on conservation burial had less than .2% of the views as Ms. Lee’s TED talk). I would love to be on a team with Lee.
So I hate to be a buzz-kill. The technology she proposes is not very well grounded in the science associated with decay of buried bodies in general nor the ecological role of soil fungi in particular.
This from an interview a few years ago for the New Scientist:
What kind of mushrooms are you using?
Right now I’m working with shiitake and oyster mushrooms.
Have you got a lab to do this in?
I have my own little DIY lab. I made a glovebox out of plastic storage boxes, and it all kind of works. You don’t need thousands of dollars worth of equipment to do this. My lab is a white tarp tent, it’s just a simple space, and it’s in my home.”
Sorry, but a plastic box containing keratin (hair and nails) in no way emulates the complex and changing environment of a buried body. A road-killed possum in a barrel would be a better experimental model, but maybe she rents and the landlord would not approve.
However, If Lee has coaxed shitake and oyster mushrooms into breaking down keratin, it would be quite an accomplishment. Keratin is extremely hard to degrade, requiring very specific proteases (keratinases) that until now have not been associated with basidiomycetes (which includes most mushrooms, stinkhorns, puffballs and earthstars-among other varieties). Keratin-eating toenail fungus, as we are all too often reminded about in disturbing TV ads (Ok, the talking mucus blobs are worse), are slow-growing and do not, thank God, have mushroom fruiting bodies.
Breaking down keratin-in chicken feathers, hair and other animal parts-has serious applications. The US chicken industry alone produces 2-3 billion pounds of waste chicken feathers each year. GEEK ALERT!! The next part is technical and feel free to skip it. It is why Lee’s interpretation of her plastic box experiment is almost certainly wrong.
A recent review of fungal enzymes that break down keratin (“Microbial Decomposition of Keratin in Nature—a New Hypothesis of Industrial Relevance”, Lange, et. al., Applied Microbiology and Biotechnology, March 2016, Volume 100, issue 5, pp 2083-2096 ) specifically notes that basidiomycetes (“mushrooms”) ,unlike some other very distant fungal relatives, are not known to produce the three enzymes required to break down keratin. Another review from 2002 in Letters in Applied Microbiology (“Screening Fungi for Keratinolytic Enzymes”, Freidrich, et. al. ) looked at some 300 species of fungi, and found no activity in basidiomycetes. Finally, a survey of proteases in wood rot fungi (which includes both oyster and shitake mushrooms) found no significant keratinase activity in these organisms (“Proteases of Wood Rot Fungi with Emphasis on the Genus Pleurotus”, Fabiola, ett. Al, p 65-66 in Biomed Research International, 2015).
Both the biology of subterranean decay and fungal/mycorrhiizal ecology are far more complex than Lee (or even we) imagined. To design a system that efficiently recycles the body’s nutrients, we must consider the major role of bacteria and nematodes, fungal utilization of organic (and later inorganic) nitrogen, including the succession of different fungal species adapted to various stages of decay, the issue of depth and soil aereation, and symbiotic relationships between different ectomycorrhzal species and vascular plants
A Couple of Definitions.
Mycorrhizal fungi are those fungi that have formed a symbiosis with the roots of vascular plants (ferns, grasses, wild flowers, shrubs, trees, etc.). A square meter of healthy forest soil contains several miles of mycorrhizaol filaments. These come in a number of varieties, including those that do NOT form mushrooms (most importantly arbuscular mycorrhiza-that actually penetrate and dwell partially in the root cells of the host plant) and those that do (most importantly etcomycorrhizal species that connect to plant rootlets). The mycorrhiza get carbon from the host plant(s) and provide the plant with greater access to water, nitrogen, trace minerals and (most importantly) phosphorous. Almost all of the mushrooms we eat are ectomycorrhizal, with the exception of the saprophytes.
Saprophytic fungi live on living, dead or waste material such as wood, toenails, feces or rarely, dead bodies, without a symbiotic relationship with living plants (and can be important disease pathogens). Notable saprophytic mushrooms include Ms. Lee’s magical keratin-eating oyster and shitake mushrooms, as well as psilocybin and the largest organism ever discovered, a 2400-8600 year old honey mushroom (Armillaria bulbosa) fungus in Oregon that weighs a at least a million pounds and covers 2,384 acres (most of it is underground, but it’s tasty fruiting bodies are all from the same organism). .
What Happens to Bodies Buried Underground?
The following is a sketch of the decay of the body underground. The squeamish might want to skip this section as well. Most of the information below is from Soil Analysis in Forensic Taphonomy, edited by Tibbett and Carter, CRC Press 2008, especially Chapter 4, p. 67-101, Sagara, Yamanaka and Tibbett “Soil Fungi Associated with Graves and Latrines: Toward a Forensic Mycology” (this is a real page turner); “Decomposition of Buried Corpses, with Special Reference to the Formation of Adipocere, Fiedler and Graw, Naturwissenschaften (2003) 90:291-300; and Mycorrhizal Symbiosis, Third Edition, Smith and Read, 2008, Academic Press .
In Europe, where cemeteries routinely disinter bodies and re-use graves after 15-25 years, researchers find that the entire process of decay takes about 3-12 years under favorable conditions.
After someone dies, cells soon begin to break down in a process called autolysis. Bacteria-mainly in the gut-begin to multiply given the available nutrients and loss of the protective immune system. This part of the process is anaerobic-meaning it goes on without oxygen, and is called putrification. Gasses produced in this phase eventually bloat the body; breaches in the cadaver allow what oxygen is around to come into the body, beginning active decay.
Early on, the body begins to lose much of the fluid is 60% of the mass of a cadaver; within 25 days the body weighs only 40% as much as it did at burial. The speed of this process is influenced by many factors including soil type, moisture, temperature, pH, burial container (if any), clothing (I hope the mushroom suit is fluid permeable, or it could very well delay decay), ecological setting including potential contact with soil organisms, condition of the body (including fat content, penetrating injuries, and time since death), and depth. Many of these factors influence oxygen availability.
Soil bacteria, nematodes and some insects also contribute to recycling the body, probably as much or more than fungi do. A square meter of soil may contain a million nematodes; some fungi depend on these tiny animals for their food supply.
To the extent that fungi could play a part in this process, it will be dominated early on by molds and other non-mushroom fungal species that can tolerate high pH and ammonia levels. Later, the pH becomes acidic as the ammonia degrades.
During above-the-ground decay and that occurring at very shallow depths, fungi have early phase-species that can tolerate and utilize ammonia and high pH (including some molds, cup fungi and later, small gilled fungi including Coprinus), and a late phase that is dominated by ectomycorrhizal basidomycetes (mushrooms that have a relationship with the roots of vascular plants), arbuscular mycorrhizal-actually the most common type-that live partially IN the host root, (and other mycorrhizal symbionts including a menagerie of fungal types) and some saprophytes ( those that can live on dead or decaying material) notably Hebeloma (A.K. A. “corpse finder”). Please note, mushroom suit fans, that wood loving saprophytes including oyster mushrooms and shittake are not playing a role here, unless it is in breaking down a wooden casket.
The late phase can go on for years, and the fungi involved depend on the species mix of the site (for example, prairie plant roots have a different set of mycorrhizal associates than those found in forests, although some species overlap). After initially repelling roots, the richness of the late phase burial site stimulates root growth (as does, perhaps, soil looseness, and water percolation). We have seen this in our meadow areas where we no longer re-vegetate the graves with big bluestem (Andropogon gerardii) because of the exuberant growth-over six feet. In non-grave prairie, it is no higher than 3 feet. S. Forbes documented that increased vegetative growth can assist in locating grave sites in a forensic setting (“Decomposition Chemistry in a Burial Environment”, in Tibbett and Carter, p. 207).
But note that I said that that fungi played a bigger role in above ground decay and decay in shallow graves. By “shallow” I mean less than 30 inches below the surface. In deeper graves, fungi are not all that involved until the roots go that deep, well into the process. Saprophytic Hebelaoma can go at least that 3 feet, but they are at early in the late-phase. I just don’t think oyster mushrooms are going to survive or thrive from even a couple of feet under. Any more shallow, and animals become a big concern.
Burial Suits and Bio-Remediation
Lee claims that one of the important tasks her mushroom suit addresses is bio-remediating the cadaver’s accumulated toxins that she apparently thinks are quite deadly.
First of all, she overstates the case. I don’t know why a general public that is hyper-concerned about the last part per billion of this or that toxin yawns at habitat loss. I do not think we are all walking EPA superfund sites. Yes we have various toxins, but these are obviously not anywhere near lethal levels. Or we would all be dead.
Once buried, and the body dissipates, toxins would further dilute dramatically (especially in a conservation burial ground with low burial densities), and most would stay underground.
Secondly, I would trust the dozens if not hundreds of bacterial and fungi species in a diverse woodland to do just as well if not better than one “selected” species of wood fungus when it comes to bio-remediating toxins (Smith and Read address arbuscular and ectomycorhhizal bio-remediation in Myorrhizal Symbiosis). In fact, we have avoided introducing cultivars of native plants (instead of local biotypes) and would not be terribly interested in introducing a “selected” wood fungus to Ramsey Creek.
Toward a Green Burial Taphonomy (Part 1)
Lee is a great designer and spokesperson (to repeat: I wish we were on the same team), and her belief that fungi play an important role in recycling nutrients of a buried body to the living layer is correct. No, her suit will not work, but all of us doing natural burial need to understand the process better. Such understanding could lead to new region and site-specific techniques to help ensure that our bodies benefit other life.
Taphonomy is the study of the fossilization process, but more generally is the study of the process of decay of remains and those factors that promote longer term preservation. Forensic taphonomy is the study of the decay of human remains.
We need a conservation burial taphonomy: one that integrates landscape-level land protection and with burial services, while ensuring that the remains are recycled to nurture new life.
Slow Recycling can be a Problem for Buried Remains
Bodies that are not buried decay quickly-related to aerobic (oxygen dependent) processes, temperature and the action of animals (vertebrates and invertebrates). The Body Farm in Tennessee studies these processes to assist with forensic analysis of crime scenes, accidents, etc.
When bodies are buried quickly, the chance of long-term preservation of tissue goes up dramatically, and this is an outcome we want to avoid with conservation burial.
Hot and Dry, Cold and Wet, High and Dry, Bogs and Adipocere
Most of us are familiar with mummies high in the Andes, those in the coastal Atacama desert, the incredibly preserved bog-bodies from iron-age northern Europe and the 5000 year old “iceman”, Otzi.
These finds are remarkable and fascinating in part because of their rarity. However, shorter-term body preservation (decades or even a century or more) could be much more common than we think.
Fiedler and Graw (2003) reported that some 30-40 % of cemeteries in Germany (where they generally re-use graves after 25 years) have a problem with persistent preservation of remains. The chief culprit in dramatically slowing the recycling of buried human remains is adipocere.
Adipocere (or “grave wax”) forms from body fat. After death, fat liquefies and saturates the surrounding muscle and skin tissue. Bacteria change the liquefied fat to fats with much higher melting points, including palmitic acid ( 142 degrees f) and 10-hydroxysteric acid (178 degrees f). These waxy fats are very resistant to further degradation and can preserve parts of the body for decades (several studies documented adipocere lasting 130-140 years).
Factors that seem to promote adipocere include those specific to the body (a high percent of body fat, for example), certain soil conditions including heavy clay soils and high soil moisture, depth of burial, the type of clothing (burial suits?) and sealed caskets. My best guess is that most of these conditions have to do with slowing the decomposition of soft tissue other than fat, and many of them create anaerobic or near anaerobic conditions. In fact, adipocere translocated to or near the surface degrades relatively quickly. The degradation of 1 kg of steric acid requires almost 3 kg of oxygen (Schoenen, 2002, cited in Fiedler and Graw 2003).
What factors seemed to promote prompt recycling? Lighter soils, higher temperatures, less depth, “ventilated” caskets, delay between death and burial and vegetative bedding in the bottom of a coffin (or the bottom of a grave in shroud burial). Interestingly, the extra oxygen present in a casket can make decomposition go faster (Forbes, in Tibbett and Carter). The straw or other material could help recycling in a couple of ways. It can provide some insulation to hold onto some of the heat released as a body decays (it is an exothermic process in technical terms); it could provide additional micro-organism contact with the skin, and could absorb some of the fluid being purged from the body. “Ventilated caskets” means lighter unsealed materials, but also refers to a finding that accidentally perforating caskets with tomb-stone anchors prevented adipocere (in an area where adipocere is a major problem).
So how can we use this information to design site specific burial techniques to ensure that the body is recycled back to the living forest or grassland? That is the subject of the next post: graves as one-use composting machines part 2.