18.

Dung stories

While the world was shut into lockdown as COVID-19 was spreading out of control, I spent much time contemplating dung of various kinds. There were probably not many people who took up this pastime to help with their mental health and wellbeing during a period of pestilence, but droppings, pellets and manure quite quickly developed into a minor obsession for me – from a fungal perspective, of course. My home laboratory is a small room at the top of the house, well away from the usual living quarters, so that my experiments did not impinge greatly on Jackie, or anyone of a nervous disposition. During that difficult time we were permitted to take exercise in local areas, and since we live very near open countryside it was pleasant to take a stroll in the open air. I always took a lidded box or two with me in case I encountered anything of interest along the way. I should say that my collections were confined to the excreta of herbivores – even for a mycologist, there are limits.

Rabbits oblige by neatly depositing their droppings on anthills. Our chalk meadows are favoured habitats for both ants and rabbits. Although it is possible to find rabbit pellets that are not on anthills, it is unusual to find a living anthill without its covering of neat, round pellets the size of garden peas. Many of the same anthills also have a close covering of fragrant wild thyme, but it is doubtless fanciful to imagine that the anthill is the bunny equivalent of the perfumed bathroom. However, when an anthill dies – as many of them seem to do when their tireless hosts move elsewhere – it is very quickly recolonised by grasses, and then it is not nearly so popular as a latrine. Old pellets become almost white, and it is better to discover darker, moister and more recent deposits for what happens next.

My wife and I also walked through many of our fine local beech woods. Deer have greatly increased in abundance over the last thirty years. This has not been to the benefit of the trees, as the seedlings are browsed relentlessly, preventing regeneration. Roe and fallow deer herds are shy: they are most often observed bounding off to get somewhere else fast. By contrast, tiny muntjac deer are solitary, creeping discreetly through cover; they specialise in nipping off orchids in the bud, which is probably why the early purple orchid has become rare in the Chiltern Hills. All deer leave their droppings in dark clusters among the leaf litter, and they are obviously larger than rabbit donations; they, too, are candidates for the little box. I believe I can distinguish small and pointed muntjac excreta from the larger deposits of other deer, but I am not confident to recognise fallow or roe deer droppings to species. Both deer and rabbits are properly wild, which means that they feed on natural vegetation and do not ingest the kind of chemicals that are often fed to domesticated animals – including antibiotics and supplementary nutrients. Such drug-free animals have the potential to yield a natural fungal biota from what they excrete.

The fungi are brought on by incubation. I do not mean that they are heated to speed things up. Rather, the pellets are placed in plastic vessels with slightly loosely fitting lids; I usually put the specimens a few together on damp pieces of blotting paper, as they should be moist but not sodden. It is important that the relative humidity remains very high – hence the lid. In nature you tend to find fungi appearing on dung only under very damp conditions, and often the fruiting bodies do not have time to develop fully if the sun returns too soon. The laboratory allows optimum conditions to be maintained for as long as it takes for several successive species to appear. Rabbit pellets are particularly easy subjects as they are the right size to be grasped in a pair of forceps. Mike Richardson, one of the high priests of coprophilous (dung-loving) fungi, refers to rabbit pellets as ‘pearls’, and indeed they are the size of larger examples of that precious gem, even if in this case beauty is in the eye of the beholder. When the fungi start to appear, the ‘pearl’ can be readily lifted out of the pot and placed on a small tray to examine under the low-power binocular microscope. If some tiny species requires higher magnification a specimen can be detached from the side of the pellet with a scalpel, placed on a microscope slide and protected with a glass cover slip. A drop of water placed next to the cover slip gets sucked under it by capillary action, and then if it is tapped with the blunt end of a pencil this usually splays out the tiny specimen in such a way that it can be examined under the higher-powered light microscope. It is a simple enough technique, but it takes a while to master.

As we have seen, most fungi avoid nitrogen-rich habitats, and indeed, many kinds of toadstools are killed by nitrogenous compounds – these fungi could be described as ‘coprophobes’. It is not surprising that coprophilous fungi are specialists, and are hardly ever found elsewhere. They relish their special role. For them, the compass of a single rabbit pellet can be their own entire small world. It is surprising how many individuals of several species are supported by such a tiny ball of nutrients. Fungal mycelium must move fast once a spore has germinated, feeding on the rich broth that other fungi eschew. The next generation will be released as spores from some kind of fruit body, which must, of course, release them into the atmosphere to be carried to the next ‘pearl’ on the adjacent anthill. A fully occupied pellet might be covered in tiny mouths ejecting spores into that special microhabitat close to the ground where ants and beetles ply their various trades. Sometimes during my experiments I have been surprised to see a fly in the same sample box with a dropping or two; it wasn’t there before. Its maggot must have fed on the dung alongside the diminutive fungi – maybe even nourished by the mycelium that secretes enzymes to make excreta more digestible. It pupated within the pellet, but when it emerges it may yet repay its fungal host by carrying spores to another site, where they can germinate in fresh offerings. To understand this world one has to think small.

Ecological succession is a theory that recognises that in many habitats particular species (sometimes several species) follow one another more or less in order during colonisation. In our local nature reserve, for example, grassland left untended soon gets birch seedlings all over, joined quickly by hawthorn and willow, followed in due course by longer-lived trees like beech and oak, when the woodland gradually attains its mature structure. It is not an invariable law, and has been criticised as a concept lacking in rigour, but in general it appeals to commonsense and experience. A version of this notion is an important part of ‘rewilding’, although it is not often acknowledged. A sequence of trees takes years to follow through; but a rabbit pellet can show ecological succession in fast frame. A parade of fungus species takes just a few weeks to complete the cycle in a specimen box. Mike Richardson showed me that it is an exemplary demonstration of the principles involved: it costs nothing, and can be set up in even the most modest laboratory. The order of species is not invariable, but some of the actors merit investigation as they make their entrance one by one.

On the cultivated ‘pearl’ the earliest activity is enigmatic. Tiny, glassy bodies appear on the surface: under a lens they look like rocket launchers drenched in dewdrops. Over the course of a day the tops of these minute transparent threads thicken and puff up. Many of them lean in the same direction as if propelled by some inner urge. Their translucent stems grow; they now resemble minuscule, un-pigmented tulips. By now they can be readily seen with the naked eye. Within a day or two each stalk is topped with a black dot. This fungus is Pilobolus – the Spore Shooter – one of the advance guard on excreta of many kinds. Sometimes it is so abundant that the original poo cannot be seen for a festoon of threads not much longer than a fingernail, all seeking the light. The black dot is a package of spores, the basis of the next generation of Pilobolus.

Although it is so delicate, the Spore Shooter is able to propel the little package for considerable distances – anything from a centimetre or two to three metres. In a laboratory dish the whole of the lid is rapidly covered on the inside with a spattering of tiny black dots – rather like the dots at the end of every sentence in this book. A shoot-out. The analogy of a human athlete lobbing a tennis ball over the Eiffel Tower seems appropriately dramatic. Compared to the size of the fungus, it is a prodigious throw. In nature, the spore capsules are catapulted far enough to attach to a neighbouring herb or blade of grass. They even carry a dab of adhesive to help the process. When a herbivore eats the grass the capsule is carried happily into its digestive tract. When the nourishment has been extracted from the grass within the animal, the capsule is carried inevitably towards the anus of its host, but the spores will not germinate until they arrive on the ground embedded in pellet or cowpat, and then the mycelium gets to work apace to produce the next generation. It is an extraordinary and finely tuned mode of life.

The mechanism of the ‘gun’ that shoots the spore package has been investigated in detail. The force necessary to fire the ‘gun’ is developed in the inflated part of the stem – it builds to a pressure of 7 atmospheres, or even more. When the spore package is released, it accelerates in a mere two microseconds to 20 kilometres an hour, which, of course, slows rapidly in air, but is sufficient to help the parcel to be delivered to the right place. The inflated sac below the spore package also acts as a lens, and contains chemicals sensitive to light which prompt the orientation of the tiny threads, and guarantees that the spores will be propelled into the clearest space to help them on their way. Even the capsule itself has a dusting of chemicals that react with the smallest dewdrop to turn the spore package towards the blade of grass so that the sticky side adheres. This tiny species is as marvellous in its way as the most glamorous mushroom – and far commoner, as any field or footpath will harbour its secrets.

The Spore Shooter is a pin mould (Mucorales), a member of one of the most primitive and ancient fungal groups, for all its sophisticated adaptations. Next to emerge from the rabbit dropping is a regular toadstool, if a very diminutive one. Several tiny, shining white finger-like projections emerge from the side of the pellet and within a day they can be recognised as having a cap and a stem, though at this stage the cap is folded down like an unfurled umbrella, so the whole fruit body looks something like a tiny chicken drumstick. It is covered with a glistening powdery cover as white as snow. Under the microscope the cover is revealed to be a mass of minute spheres, mixed with threads, loosely piled together to form a veil. The toadstool is rather beautiful at this stage. Within a matter of hours the stem extends, growing upwards to lift the toadstool well above the pellet that gave it succour. At the same time the cap opens out, exactly like a miniature Chinese parasol, with radial ribs supporting a thin membrane between them. The remains of the snowy veil dust the surface. Now you can see the gills, the same number as the ‘struts’ on the surface of the parasol. Almost as soon as the cap has unfolded and expanded, the spores dust the surface of the gills and the spores are obviously dark in colour – a striking contrast to what went before. It is easy to imagine the spores being released into the breeze to travel to the next rabbit dropping. Before long, the tiny cap has blackened completely, the gills melting away to nothing. Soon, just the stem remains. This dissolution reveals the tiny white toadstool as an inkcap, one of several small species specifically adapted to dung.

The life of a single toadstool is brief, but if conditions are right, new examples will emerge and go through the same short cycle. When I came to look at deer pellets, this Dung Inkcap, Coprinopsis stercorea, turned up regularly, but it was soon joined by other inkcaps like the delicate C. radiata and smooth brown Parasola misera. Deer dung supported a greater range of species than rabbit. Some of the tiny inkcaps I discovered carried a thicket of tiny, spine-like projections on cap and stem, and were identified as Tulosesus pellucidus and Coprinellus pusillulus. Clearly, this ecological niche was ideal for the transient inkcaps, some so delicate that they could be destroyed inadvertently just by breathing a little too hard. It intrigues me that these fragile, evanescent productions of nature were recognised by early mycologists, even though they grew on what most people instinctively avoid. Elias Magnus Fries had discriminated ‘Coprinus’ stercoreus by 1838, taking the species name from a still earlier publication. The curiosity of the dedicated naturalist evidently has always trumped squeamishness.

Some bowl or disc-shaped ‘spore shooters’ appear early in the parade of species on dung. Most walkers will know at least one of them. In damp fields with herds of cows the cowpats are often coloured orange, and this is noticeable even from some distance. If you get down on your hands and knees and gingerly approach the object in question, you will see that they are covered in small, bright orange discs just a couple of millimetres across. This is often one of the first fungi to appear on a fresh deposit as soon as a crust has formed, and has, somewhat optimistically, been dubbed the Cowpat Gem (Cheilymenia granulata). It often appears as early as Pilobolus. The spores are carried on the waxy-looking outward-facing orange surfaces; they are located inside little sacs (asci) in lines of eight. When mature they are expelled from the asci and get carried on the air currents to nearby cowpats, or on to grasses where they will wait until a cow decides to munch that particular bunch, when they will enter the cow’s digestive system.

A great variety of other ‘discos’ colonise all types of dung. Most really belong to the microscopic realm, since they all require careful examination at high magnification to identify, but I cannot resist visiting one or two of them. Their identification kept me engaged while the COVID pandemic was at its peak. Such fungi usually appeared as tiny gelatinous discs, drums or lumps on the surface of my rabbit pellets, and can be almost any colour except green and blue. Their spores are very small, so they are usually completely invisible to the naked eye unless seen en masse. However, those on Ascobolus are visible even under a magnifying glass. That is because the tiny top-shaped disc of this fungus is often semi-transparent, and a hand lens reveals scattered minuscule black dots on the surface. These are the asci that contain relatively large spores, which are darkly pigmented and often show up purple-brown under a microscope. They carry an interesting surface sculpture of darker ridges, which are important in identifying species. Now they are displayed inside transparent asci on the pallid, spore-bearing surface, like minute chocolate cakes laid out on a platter.

One of the species I identified was Ascobolus hawaiiensis, which, as the name implies, was originally recognised in Hawaii. This is surely a case where the fungus was transported to Hawaii with the cows when the islands were colonised, rather than spreading from the remote archipelago back to Europe. Farm animals can carry their biota much as a traveller might carry his or her hand luggage. Saccobolus appears early on as dark humps on the surface of the ‘pearl’ – quite well disguised until you realise what they are. They include arrays of asci, within which the eight dark spores huddle together as a package rather than separating into individual spores. Maybe this is a similar strategy to that of Pilobolus to increase the chances of being picked up by a grazing animal. Some of the other early species that appear on rabbit and deer dung even break the rule in ascomycetes of eight spores in each spore-bearing ascus, which holds true for thousands of species. The inconspicuous bag-like asci of Thelobolus can contain hundreds of spores; prolonged cell division during their development continues to double and redouble their number. Counting them is almost impossible. It seems reasonable to suppose that this is a simple way of increasing the chances of any one spore reaching a suitable place for germination: safety in numbers.

After the early fungal species have had their way the rabbit pellet can look quite different. A mass of small dark flasks takes over. Most conspicuous are a few species that sit on the surface, but elsewhere the apertures – you want to say mouths – of the flasks protrude from the surface. It can occasionally look almost prickly. In these fungi the asci are concealed inside the flasks rather than exposed as in the ‘discos’. Their spores are lemon-shaped and very black in colour, but many have colourless gelatinous appendages at each end. When the spores are ripe the ascus holding them extends and pushes up into the ‘mouth’ (ostiole) of the flask and ejects them into the air. One of the first species I investigated broke the ‘eight spore rule’ but the other way round – Schizothecium tetrasporum only has four spores per ascus. There are examples in other dung-lovers of ‘spore killing’ where half the spores in an ascus that lack a particular gene are eliminated by the other four that have that gene. Many of the common flask fungi belong to the genus Podospora and have interesting arrangements of hairs on the surface or around the ‘mouth’; they, too, employ the numbers game with their spores … 8, 16, 32 … all the way to 256 in one ascus. It is intriguing why dung-loving fungi should play tricks with spore numbers; although more spores give a reproductive advantage, it cannot be all about that since some species have gone the other way – to fewer spores.

Perhaps durability has something to do with it. Sporormiella is another immersed fungus, with a brown cellular ‘bag’ occurring commonly within in all kinds of dung that house asci with eight very peculiar-looking spores – each one rather like a string of short sausages, four in a row. These distinctive spores (which can break into four pieces) are very durable and survive in many sediments, so they have an excellent fossil record. Because they are so common in herbivore dung, their relative frequency as fossils should be a sound proxy for the abundance of large herbivores: the more animals, the more excrement, and the more Sporormiella spores. In western North America it was discovered that the numbers of these spores had a precipitous decline in abundance 12,900 years ago, coinciding closely with the extinction of giant herbivores like mammoths, mastodons and sloths, and even horses and llamas. Since this also coincided rather closely with the arrival of modern humans into that continent across the Bering Strait, the inference was drawn that it was the hunting activities of our own species that so depleted the number of Sporormiella spores, not to mention removing some of the most impressive herbivores that have ever existed. I cannot think of a better example where the study of something that is apparently tiny and obscure to most people intersects with an issue of mammoth concern – and where the word ‘mammoth’ can be used literally rather than metaphorically.

My rabbit and deer (and a few sheep) excreta became exhausted after only a few weeks. I had also tried horse dung in the laboratory, but domestic issues involving flies (and threats) meant that it was politic to cut that study short. I did not even attempt to bring home a whole cowpat. It is perhaps not surprising to find that horse and cow droppings yield scaled-up versions of the tiny mushrooms and other fungi that made their home in my rabbit ‘pearls’. Near my home I know a piece of parkland where artificial fertilisers have been withheld, and the grazing animals are not so numerous as to add too much nitrogen to the habitat. When it has been damp and humid for some time – usually in spring and autumn – fungi are soon evident among the grass, either growing directly upon or next to the waste products of the grazing animals. The common Dung Roundhead (Protostropharia semiglobata) can be recognised from afar, with its perfectly hemispherical, yellow cap the size of a coin balanced on a slender stipe, and dark gills.

The inkcap tribe is represented by the wonderfully shining white Snowy Inkcap (Coprinopsis nivea), which is a scaled-up version of the tiny white species I had raised on rabbit ‘pearls’, covered in white powdery cells, and destined to turn from white to black as it matured. One year I found its beautiful pale-pink relative (C. pseudonivea) in great profusion, and never saw it again, which is what fungi do to wind you up. A variety of small brown toadstools are especially there to test the taxonomic abilities of the enthusiast. Rarely, there is even the Dung Bird’s Nest fungus (Cyathus stercoreus) vying with some larger orange ‘discos’ for attention. There are no Field Mushrooms on dung, even though tradition has it that they like fields with horses. What they like is the grassy spaces between the droppings. Even a single meadow can be a mix of several fungal habitats; fungi see the world in a discriminating way so that they pick and choose exactly where to appear.

In pursuit of a close encounter with a great rarity, Stuart and I went into the heart of the New Forest on a perfect autumn morning. We were looking for pony dung. The dew still painted up the spider’s webs, linking one clump of heather to another with threads almost as delicate as mycelium. Corvids croaked a welcome. Scattered birch trees were surrounded by Amanitas and milkcaps, but tempting though these toadstools were, our search was for something more extraordinary. Several piles of fresh dung were not sufficiently mature. Some scuffed-out patches were probably too old; their fungal days were over. Then we saw what we were looking for. Emerging from the top of a horse dropping the size of a small potato were what looked like half a dozen small white coins. The Nail Fungus (Poronia punctata)! There is a particular thrill in seeing in the flesh something that for years you have only seen in books. Some part of you believes that it doesn’t really exist – that it is something like a leprechaun, not to be taken too literally. But here it was, in the flesh, and just as odd as it is supposed to be. The white ‘coin’ was just the outermost part of the fungus; it was like the flat head of a longer nail, and the lower part of the nail was hammered into the dung. Of course, it was really the other way round: mycelium fed the fruit body, and a ‘stem’ grew upwards and outwards before opening out on top of the heap. On closer examination I saw that the white surface was dotted with black points, a dozen or more, which stood out clearly from the white background. These were the mouths of immersed flasks containing asci with brown spores, which would be expelled when ripe to spread the Nail across the forest. Extraordinarily, this very odd fungus is a relative of the Candlesnuff fungus that feeds on dead wood, a species familiar from every copse and forest. At some distant time an ancestral pioneer species ‘jumped’ from wood to dung. The versatility of fungi never ceases to astonish me.

The Nail Fungus is a very uncommon species now, and the New Forest is one of its few redoubts. At one time it was abundant. As long ago as 1753 it came to the attention of the great Linnaeus, who gave it the specific name we still employ. It was everywhere in the nineteenth century, when horses were used for all manner of tasks, from drawing carriages and barges to transporting commodities around cities. Disposing of tonnes of horse dung proved a major logistical problem. Trams, trains and petrol-powered vehicles helped to end that era and Poronia became less frequent. It did not respond well to agricultural chemicals like artificial fertilisers and pesticides, which fed into the grass that the horses ate, nor to the treatments developed to ‘worm’ the animals. The Nail Fungus began to go into full retreat across the whole of Europe. It survived only in places like the New Forest where there were still ‘wild’ ponies that fed upon natural vegetation in unimproved countryside. Fortunately, its very oddity attracted enough attention to give it protected status and it is now the subject of a Biodiversity Action Plan, and the New Forest population is monitored. Future mycologists should still be able to discover those Nails hidden among the heather on a bright September morning.

My most recent encounter with the Nail Fungus took place not on the wild slopes of the New Forest (Hampshire) but in a suburban garden in Henley-on-Thames (Oxfordshire). As I walked past the front of a Victorian house I noticed some horse manure on a flowerbed, and from deeply ingrained habit glanced to see if there were any mushrooms about. I was astonished to see a Poronia poking out from one piece of dung. I thought it might be the first record for the county, and was not unreasonably excited. After dithering for some time, I went up to the front door and rang the bell. I attempted to explain something about the Nail Fungus to a nice woman who answered the door, and I have to say she looked rather sceptical. Then I had a bright idea. ‘I don’t suppose that manure came from the New Forest?’ I enquired. ‘How did you know?’ she responded, with obvious astonishment. She told me she had brought back a bag of pony manure to treat the roses after a visit to Hampshire. While I was happy to feel my expertise had impressed, I could not record this occurrence as a first Nail for the county. It was just the dung taking a holiday.