In The Kingdom of Decay: How a Motley Team of Subterranean Dwellers Ransacks the Dead and Liberates Nutrients for the Living

by Liam Heneghan


The recently dead rot much like money accumulates in banks (until recently, at least), only, of course, in reverse. A sage great-great-ancestor who had, for instance, set aside a few shillings for a distant descendant would, through the plausible alchemy of compound interest, have made that great-great-offspring a wealthy person indeed. In contrast, after death a body-heft of matter accumulated over the course of a lifetime is hustled away, rapidly at first, but leaving increasingly minute scraps of the carcass to linger on nature’s banquet table. It is as if Zeno had not shot an arrow but instead had ghoulishly slobbered down upon the departed, progressively diminishing the cadavers but never quite finishing his noisome meal. The soils of the world contain in tiny form, scraps of formerly living things going back many thousands of years. Perhaps these are the ghosts we sense when we are alone in the woods.

Before you rake away the final leaves of the autumn season, hold one up to the early winter light. Those patches where you see sky rather than leaf are the parts that had been consumed live, nibbled away by insects or occasionally browsed by mammals. But you may have to pick up several leaves to see any consumption at all! The eating of live plant material is rarer than one might suspect. It is almost as if most creatures, unlike us of course, have the decency to wait for other beings to die before they consume them. Ecologists have wondered why this is the case, asking in one formulation of the problem “why is the world green?” At the peak of the summer season the world is mysteriously like a large bowl of uneaten salad. The world it turns out is green for many reasons but a compelling one is that plants generally defend themselves quite resourcefully. The thorn upon the rose provides more than a pretty metaphor – this shrub knows exactly what to do with its aggressive pricks. And if one can neither run nor hide nor protrude a thorn, you might manufacture chemical weapons. Crush a cherry laurel leaf in your hand, wait a moment or so, and then inhale that aroma like toasted almond. It’s hydrogen cyanide, of course. “Don’t fuck with me” is one of the shrubbery’s less lovely messages.

Gravity tugs upon the dead. Those things not already in the soil when death arrests them tend soilwards upon their demise. If this were a world where the dead remained unconsumed an unwholesome detrital pile would have accumulated upon the bottom of ancient seas until the world’s usable matter had been exhausted and life on earth would have faltered. The dead must be moved along for the living to keep moving at all. Why this must be so is pretty obvious but precisely how post-mortem remains get disarticulated and converted into forms usable for the living is still being investigated. Professionally, I am a student of death and decay, which is an accurate way of saying that I am a student of life. The world is as brown as it is green.MOLAMay1708Wormin2008-05-17_11-31-09

From this point on I will primarily consider the decay of plant material since this comprises the bulk of terrestrial biomass. Concentrating on the breakdown of leaves rather than bodies makes the story less gruesome but the processes are much the same. The consumption of the formerly living and the transmutation of organic into inorganic constituents is the ecological business of a diverse community of saprophytic organisms (etymologically derived from sapro = putrid, and phyte = plant) and of an accompanying host of small animals that feed directly upon the decay or that nibble on the saprophytic microbes involved in decomposition. The outcome of all this caliginous toil is the liberation of carbon, nitrogen, phosphorus, and elements otherwise trapped in the death’s charmless chambers. The carbon burbles through the soil and back into the atmosphere, the nutrients spill into the soil and are scrambled over by microbes and plants all obeying life’s blind will to amplify.

Earthworms, millipedes, woodlice and so forth fragment dead leaves, breaking them into smaller pieces and exposing fresh surfaces to colonization by microorganisms. Earthworms, like mobile and mucousy tubes of toothpaste open on both ends, squirt their way through the world’s putrefaction. What they squeeze out may not be minty fresh but it has its own charisma. An earthworm’s body surface, its internal workings, and its copious soil-full egesta glisten with a snotty discharge that microbes simply die for. Or rather live for since these easily degraded substances prime the decomposer microbes whose micro-feeding frenzy continues the assault on dead organic matter. Earthworms inside and out are maestros of putrescence. In their poetic moments earthwormologists (a freshly coined term) have referred to their beast of interest as “Prince Charming”, its mucus as a “Kiss”, and those microbes that get whipped up into a digestive frenzy as “sleeping beauties”.

Fungi and bacteria are royalty in the kingdom of decay. They satisfy their nutritional needs by regally exuding extracellular enzymes upon their putrescent foodstuff and absorbing the rot. The soil is a trickle down economy of the most literal form. The bulk of global decomposition is performed in this macerating way. A bacterium, from the perspective of putrescence, is a single-celled sack of carnage constrained within a robust peptidoglycan wall. Not only can they break down some extraordinarily robust materials (including cement) some produce powerful fungicides and thus dispatch and then consume the competition. If it was not for one small design limitation this world of ours would host little other than bacteria consuming bacteria. A scientific madman indeed would be he who genetically engineered tiny legs for bacteria. For this is their structural drawback – bacteria are relatively immobile, and like sea anemones or corals they wait for their food to come to them or for some biddable creature to transport them to their comestibles. For this reason a majority of bacteria cells in the soil are physiologically inactive, waiting, waiting, waiting for some moist dead thing to enliven them and unleash a digestive maelstrom.

One should not be deceived by the daintiness of an intermittently protruding mushroom or toadstool. These are merely wardrobe malfunctions in the great show of mouldering – unseemly exposed tips of a grand underground organism whose digestively capable filaments (called hyphae) can extend as a network over many miles… yes, miles. Fungi, in fact, are celebrated among the world’s largest organisms. The strategy is that the organism can glean a portion of the nutritional requirement in one place and other portions elsewhere and in theory can distribute the ambrosial broth across the entire cytoplasmic web. Their sheer size has led to debate about what precisely constitutes an individual organism (genetic identity is clearly not enough) but for our purposes the significant point is that more or less everywhere below us a fungus toils, relieving the dead of the elements they have little use for anymore.

The community of soil animals supported by decay is profligately diverse – enigmatically diverse in fact since many occupy themselves with the consumption of similar morsels. The application of one of ecology’s few implacable laws, competitive exclusion, should dictate that this richness be diminished. There are predators down there of course – monstrous feeders, some of Fungus2006-05-28_08-51-48which are sheathed in chitin and furnished with pincers beyond the extravagance of ordinary phantasms. On predators’ menus: nematodes, protozoa, rotifers, mites, springtails, diplurans, termites, woodlice, and amphipods. All with their distinct gustatory charms one supposes; no-one is sharing recipes. The cupboards of non-predatory soil animals are rarely bare and you’d not go hungry down there as long as your appetite is whetted for fungus or bacteria for all your days. And this is the enigma of soil diversity therefore: so many animals live on the same diet with little specialization of feeding habits. How can this be so?

Energetically, soil animals, other than worms, directly contribute little to the decay of the dead. Functionally, however, they are tremendously important. The problem with the unrefracted dead, as you will recall, is that the dead harbor essential matter required by the living; the problem with microbes is that as quickly as they liberate these essential ingredients they immobilize them again in their own burgeoning biomass. Soil animals disrupt and facilitate in equal measure. They help things along by champing down upon microbes liberating their nourishing juices in a form available to plants. Now, one may wonder why consumption by the animals doesn’t simply lead to their accumulation in the biomass of those microbivores. If this were the case it might make it difficult for plants to get the elements necessary for their growth – all in all an unfortunate thing since it is primarily dead plant material keeping the whole thing going. Here’s what happens then. The composition of microbial cytoplasm is different from that of soil animals in one important respect. There is more nitrogen relative to the concentrations of carbon in microorganisms. Animals feed upon microbes to get at get their carbon fix and in doing so take in more nitrogen that they can process. To deal with this animals excrete that excess. The bottom line: the piss of armies of small animals sustains this green earth. Nitrogen gets into soils in other ways, of course, and soil critters perform other functions, but it is hard to overestimate the influence of tiny soil animals – mites and springtails (primitive wingless insect-like critters) – in orchestrating rot. Microarthropods0004

The nitrogen and all the other essential soil nutrients liberated during the decomposition of the dead ensures that plants can respond to the sun’s energy and live for a while, to sustain the living of others, such as us, for a while, to animate matter for a while, and all that while preparing matter for its lengthy sojourn in the kingdom of decay.

In its broad strokes the story of decay has been known for some time. Darwin famously contributed to that understanding. His book The Formation of Vegetable Mould through the Action of Worms, with Observations on their Habits (1881) culminated a lifelong interest in worms. Nothing escaped his attention: the density of worms in soil, their taste preferences, and even their unusual sexual habits (their “passion” he said, “is strong enough to overcome for a time their dread of light.”) In particular though he meticulously quantified the rate at which worms convert leaves into soil, thereby increasing the fertility of the soil. In the intervening century and a third the details have been worked out. The critical role of tiny soil animals in determining the rates of decay and in liberating soil nutrients emerged from the work of the last generation of researchers. I have contributed in a very modest way to this research literature in the last couple of decades.

Big questions remain unanswered. What might the significance be of the loss of below-ground diversity for the functioning of ecosystems? Can soil communities be restored if they are damaged? Can individual plant species manipulate soil decomposers to ensure a rate of decay that favors their own growth? What are the implications of global change for decomposition? If decomposition rates increase in bogs or in the tundra as they are expected to in most models of climate change, will the additional carbon released into the atmosphere in turn exacerbate global temperature increases (some folks speculate that soil carbon release will contribute to the breaching of a critical transition).

Perhaps it is just “cowards who die many times before their deaths”, but the matter that constitutes each and every one of us has experienced death so often that we should all be able to face our end languidly. We are all shuffling along the waiting line into the Kingdom of Decay. The workings of the upper five centimeters of the Earth’s surface may repay the considerable effort it takes to learn about it. The payoff may be felt not only in contemplating our collective environmental future but in contemplating our personal demise.

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All photos by Liam Heneghan except photo of soil mite (Oppiella nova) by Claire Gilmore and Liam Heneghan.