Not far from the boundaries of our own morsel of Chiltern woodland a footpath runs alongside a large open field underneath a line of mature oak trees. Between the path and the field an untidy border with big patches of nettles has occasionally yielded Giant Puffballs – one of the few species that enjoys nitrogen-rich soil. Towards the end of October 2012, Jackie and I were enjoying a stroll along the path to see ‘what was about’, which is mycological shorthand for grubbing around under bushes and turning over logs. Extending from the trees towards the field and into the nettle patch a huge fairy ring of Clouded Funnel (Clitocybe nebularis) comprised dozens of large, pale-grey toadstools.
This is one of the commonest of autumnal saprotrophic species, easily recognised by its pallid, solid and stout fruit bodies with the margin of the cap at first rolled downwards, and having yellowish-tinted, rather crowded gills sloping on to a relatively short, sturdy stipe. It is distinguished from typical funnels in having a thick-fleshed cap that is hardly depressed in the centre, and has a distinctive fruity odour that may have encouraged over-confidence in its edibility in the past (it is best avoided). Typically, the middle of the cap carries a whitish ‘cloud’ of mycelium, looking as if a cobweb-thin sliver of tissue paper had been applied there. A forayer may pass by a circle of Clouded Funnels with little more than a nod of recognition, happy enough to see them but no further investigation required. Jackie’s years of rubbing along with a mycologist has honed her instinct for discovery, and something prompted her to wade into the nettle patch, following the fairy ring. There she discovered a fungus I had been trying to find for more than fifty years.
When I first began my long love affair with fungi in my childhood the only identification book that was widely available was The Observer’s Book of Common Fungi by Elsie M. Wakefield. This is where I first learned to recognise the Clouded Funnel (or Clouded Agaric, as it was then known). A few years later, in John Ramsbottom’s New Naturalist Mushrooms and Toadstools, a novel mushroom was introduced – in a footnote – appended to his mention of the Clouded Funnel; it was, he said, ‘the host of the rare Volvaria Loveiana [sic] which grows in clusters on the cap’. What a wonderful fact to learn! There could be mushrooms that grew on mushrooms – and, what is more, this was a special species that grew only on one particular host. It seemed to me to be the ultimate tribute to the wiles of evolution. When I was a schoolboy, mushrooms were already exotic enough, but here was curiousness piled upon exoticism.
Somehow, the current common name Piggyback Rosegill for what is now called Volvariella surrecta is hardly adequate to encapsulate the extraordinary idea of the fruit body of one species growing on top of another. The additional remark about its rarity only added to its allure, and ever since I first learned of its existence I had wanted to find it in the wild. The Collins Guide published in 1963 upped the stakes by describing it as ‘extremely rare’, with a good illustration showing a few pretty, white mushrooms arising from neat white cups (volvas) atop a decaying funnel, as if they had been modelled in porcelain. Thus began decades of hopefully scanning fairy rings of Clouded Funnels; and no year passed without many sightings of this common fungus dotted over the woodland floor. I never found an example of the ‘piggybacking’ toadstool, until I believe my inspection of funnels became a perfunctory ritual rather than a gesture of hope. I was probably becoming resigned to the idea of never seeing the perching parasite, but here it was, at last, hidden away among the nettles. Jackie had finally discovered it. If I got stung I didn’t notice. Remarkably, there was not just one of the funnels carrying the alien toadstools aloft. It seemed as if every other fruit body in the fairy ring had been instructed to burst forth its rare passenger at the same time. They hatched from white ‘eggs’ made from the volva, but most had already pushed out to open their caps and spread their spores. When this happened the gills became a pleasing shade of pink. The small boy interred somewhere deep inside my old body clapped his hands with delight. A clumsy attempt was made to immortalise the moment with a photograph on my mobile. I still automatically rake my glance over any group of Clouded Funnels, but it is now just an old habit that is hard to break, a mycological tic.
I later discovered that I had already seen the elusive Piggyback Rosegill, only I did not know it. The nebula-like ‘cloud’ in the specific name of the Funnel (Clitocybe nebularis) refers to the faint white patch that decorates the centre of the cap. Sometimes it looks slightly fluffy. This is actually the mycelium of the piggybacking parasite. I must have noticed it a hundred times without making the connection. Whatever its potential, most mycelium tends to look like other mycelium, so perhaps this unspectacular dusting does not really count as a sighting. Only once in a rare while does the superficial passenger ‘decide’ to produce a mushroom, and eventually I was privileged to see that moment at the edge of a wood in Oxfordshire. That does invite some intriguing questions. The obvious mystery is what triggers that rare fruiting, and why it does not happen more frequently.
It is particularly curious that the trigger for fruit body production – whatever the cause – simultaneously affects the whole fairy ring of Clouded Funnels. There is apparently no connection between the Volvariella on one funnel mushroom and that of its neighbours, yet it is as if a clarion call was sounded to produce their spores at the same time, to awaken their hidden mushroom. It might be plausible to invoke some concatenation of external events – a combination of rainfall, nutrition and season perhaps. However, another ring of Clouded Funnels not far away was apparently not obliged to allow its mycelial passengers to announce themselves, and if it were just down to meteorological conditions there should surely have been more piggybackers nearby. Maybe some strains of V. surrecta differ from others in a propensity to produce fruit bodies, or possibly the necessary ‘mating types’ to make a fruit body rarely come into contact. How typical of the fungi to leave behind two questions for every one answer.
Although the Piggyback Rosegill is the most glamorous hitchhiker, it is not unique. Some other agarics have developed a similar trick, and they are commoner. The most frequent member of the mycorrhizal genus Russula in our woodland is the Blackening Brittlegill (Russula nigricans), a chunky toadstool, typified by very widely spaced gills, that begins almost white and finishes up completely black, in which state old fruit bodies can hang around on the forest floor for many weeks. By then, most of the fungi that came up alongside this durable species will have decayed away. If October is wet – and it often is – some small powdery lumps may appear on the old wrecks of the Blackening Brittlegill. In a few days these will have assumed a mushroom shape, usually in a cluster, with caps no larger than a small coin, looking as if they are covered with pale yellow-brown dust. Then they are quite conspicuous (if you know what to look for) emerging from the dead corpse of their host.
Discovering them on a foray is always exciting. This Powdery Piggyback[1] (Asterophora lycoperdoides) – a long name for a small toadstool – is as curious in its way as the Piggyback Rosegill. The superficial powder that covers its cap is a mass of spores, but not the usual kind that are born on the gills. Instead these are tiny bits of fungal hyphae derived from the parent fruit body. Blown by the least puff of wind these can be carried to another blackened wreck rapidly to produce a clone of the parent. I have noticed that if you find one Powdery Piggyback you will often find others nearby, and this easy form of propagation may be the reason. The gills of this toadstool are rather poorly developed, and may not be as important in reproduction as in most agarics, thanks to its special fairy dust. A related, white-coloured species (Silky Piggyback, A. parasitica) found on the same host has more normally developed gills and lacks the exterior dusting. In my experience it is less frequently encountered than its powdered cousin.
All these piggybacking agarics are using the host mushroom to provide them with a source of food, in order to further their own reproductive ends. None of them affect the host’s ability to grow to maturity and shed its own spores. Nor is the parasitic habit confined to agarics. A few boletes have developed a similar trick. I had a close encounter with one of these specialists near the village of Walberswick in Suffolk, which lies about as far to the east as it is possible to go in the British Isles. The ground nearby is sandy and relatively infertile – good for encouraging heathland, with a scattering of oaks, sweet chestnuts and birches. From late summer, often the only fungus that is seen in profusion along the path sides is the Common Earthball, the yellow, scaly spheres of which emerge from even the most compacted ground, looking as if some careless customer had allowed potatoes to drop at random from their shopping bag.
It is one of those fungi that the walker tends to ignore after a while, because it is so abundant. In 2015, during one of my familiar strolls to the sea, one cluster of earthballs on a bank looked a little unusual – too crowded together perhaps. A large specimen appeared to be surrounded by a group of three other smaller fruit bodies. To my surprise and delight these proved to be diminutive boletes, almost the same colour as the earthball, but with an obvious stem and cap and the yellow pores typical of their kind. The texture was clearly softer than that of their host, and it would have been easy to walk on by without noticing the Parasitic Boletes (Pseudoboletus parasiticus), but once alerted to their presence it was clear that several other earthballs had similar smaller companions. The attentions of these freeloaders did not obviously stunt their hosts, so these may not have been particularly demanding as parasites go. Further along the same path, one of the curious boletes was itself looking sickly. It had been almost completely colonised by a white or yellow velvety covering that served to obscure the pores. The covering made the Pseudoboletus cap more conspicuous by the wayside. It was obviously a mycelium blanket. So here was a fungal parasite on a fungal parasite! The Bolete Eater (the asco Hypomyces chrysospermus) changes from white to golden yellow as it matures. It commonly ‘mummifies’ boletes from head to foot, to the disappointment of humans who like to eat the same fruit bodies before a fungus beats them to it.
The pinnacle of this parasite narrative has to be another, very rare bolete that was found in the same sandy ground a few years earlier. With a domed, warm yellow-brown cap that is usually markedly rolled under along its perimeter, and bright-yellow pores that bruise blue when touched, Buchwaldoboletus lignicola is an exciting find for any mycologist. My friend Stuart and I discovered two examples emerging from dry sandy ground near the base of an old pine tree along the Blyth estuary. The fungus is sometimes called the Wood Bolete, which is probably a literal translation from its Latin species name. This is mistaken, because the rare bolete does not grow on wood; it is another parasite – this time upon a common bracket fungus called Dyer’s Mazegill (Phaeolus schweinitzii). The latter is a large, often broadly fan-like fungus with a thick, meaty texture; it appears at the base of ageing pine trees. It is typically yellow when young, but becomes umber brown as it matures, and is perhaps best identified by its dark, finely porous, maze-like spore-bearing lower surface. We were gratified to be able to find an example of these unusually durable brackets near our discovery of Buchwaldoboletus. The apogee in this cascade of parasitism is that Phaeolus is itself a parasite of pine trees. So in the Wood Bolete, we have a parasite living off a parasite. It is not too fanciful to surmise that the very common Bolete Eater might in turn infect the Wood Bolete (perhaps sadly, ours wasn’t). Were that the case we would have a parasite depending upon a parasite parasitic on a parasite. To recall a famous rhyme by Augustus de Morgan: Great fleas have little fleas upon their backs to bite ’em, And little fleas have lesser fleas, and so ad infinitum.
There are much more malevolent parasitic fungi known to science than the relatively benign agarics and boletes,[2] which do at least allow their hosts to shed their spores, and in the case of Asterophora the host is already defunct. As an evolutionary strategy this would seem to make sense because the parasites depend on the continuation of their host for their own survival. There are other scenarios. An invading parasite could completely take over another fungus, hijacking it for its own reproduction. This is the technique of the stranglers.
I first learned of these fungi in the pages of a very dry book of keys to fungi by Professor Meinhard Moser, but the name of the genus Squamanita leaped off the page as something exotic, carrying with it a hint of the lethal glamour of the Death Cap Amanita, but mixed with the esoteric attraction of something rare and remarkable. All the species of Squamanita were very seldom encountered, said Professor Moser, so here was a challenge just as there was with the Piggyback Rosegill. The stranglers have specific hosts – they are choosy about their victims. They are body snatchers. They do not wait for their intended target to make a mushroom, but they take over – hijacking their unfortunate quarries to produce their own fruit bodies – and obliterating their fungus hosts in the process. The typical species of Squamanita is parasitic on Amanita (I suppose that is how it got its generic name) and makes the most extraordinary fruit body – with a massive base like a turnip from which arises a handsome agaric (sometimes more than one) with white gills and a fibrous-looking cap which is unlike that of any Amanita, though like that genus it does have a ring on the stipe and white gills. In the end, there is not much left of the host fungus.
The thickened base has been termed a gall (a recent scientific paper recognises its unique character with a different name – mycocecidium) and is where the parasite takes hold; DNA analysis suggests that both Amanita and Squamanita are present within it at this stage. Thereafter, the lethal intruder takes advantage of the fungal network of its host to reproduce its own kind. The Amanita is simply obliterated. It is hard to escape a grisly comparison with the horror film Alien. This particular fungus (Squamanita schreieri) has not yet been collected in Britain, despite some claims to the contrary. It is listed as endangered in Europe, and I think it is now improbable that I will ever see it in the flesh. It is sobering to know that some fungi are so uncommon that a lifetime is not long enough for site and season to intersect with exceptional good fortune.
I felt I must meet one of the British stranglers before I could write this book. The most well-known species (can I use ‘well-known’ for something so rare?) parasitises a common yellow grassland mushroom, the Earthy Powdercap (Cystoderma amianthinum), a familiar species favouring short turf, distinguished by a powdery covering of loose cells that often form tiny teeth around the edge of the cap, and similar bands of cells on the slender stipe below a small ring. After a lifetime of reducing the fertility of my garden lawn, I was rewarded with powdercaps – but not accompanied by their exotic parasites. I was obliged to look elsewhere. Recent work on the DNA of the stranglers has shown that British species, including the Powdercap Strangler, should now be placed in a different genus, Dissoderma, so with a tear in my eye I bade farewell to the exotic Squamanita, which I will now never meet face to face. Science has to move on. Professor Gareth Griffiths of Aberystwyth University, who has minutely studied the stranglers, kindly put me in touch with Torben Fogh, who lives deep in the Lake District. Torben knew where the stranglers hide.
It may seem a trifle eccentric to drive five hundred miles to see a mushroom the size of a ten pence piece, but in October 2023 a message from Torben propelled us northwards: Dissoderma paradoxum, the Powdercap Strangler, had arrived! The southern part of the Lake District is not as rugged, bare and bleak as the country beloved of fell walkers. Relatively gentle hillsides are clothed in broadleaved trees – birch, oaks and beech – and sheep farming predominates. We admired the stone walls that kept the Herdwick sheep confined; they were carefully constructed from grey grit and coarse slates in alternating layers, and capped by vertical slabs, serious walls, meant to last. Some of the fields on lower ground looked too lushly green to be rich in fungi – fertilisers had done their worst. The pastures we were looking for would have been grazed short, but not artificially fertilised. The open fells themselves occupying the high ground tended to be covered with bracken, which is generally bad news for fungi.
In the early morning, the mist hung low over Lake Coniston. Torben proved to be a tall, bearded, lifelong Lakesman and naturalist, with a gentle manner. He told us he had been determined to find stranglers once he had learned of their existence. On a perfect sunny autumn day he led us uphill across several fields, past quite a few of those admirable walls, to a farm he said had been run in the traditional way for generations. Sloping fields were wonderfully free of the nettles and brambles that soon disfigure ‘improved’ pasture. It was not long before we found brilliant yellow caps of the Golden Waxcap (Hygrocybe chlorophana) and the slimy green ones of the Parrot Waxcap (Gliophorus psittacinus). We knew that waxcap grassland is the preferred habitat for powdercaps. It was a perfect site. A small beck marked by scrubby hazels and alders tumbled across the fields, providing a tinkling accompaniment to our close scrutiny of the sward. While not exactly on hands and knees, this process involved slowly quartering the field peering at the ground. After a few minutes the first fairy ring of powdercaps was spotted, even though rain had stripped the caps of much of their typical dusting. Carefully plucking one from the grass, we could see the somewhat shaggy lower part of the stem. We soon discovered several such fairy rings, but none of them obviously ‘strangled’.
Torben had been here earlier, and I am not sure we would have found the strangler at all had he not done a reconnaissance – he had left a small cairn to mark the spot. And there they were, near the top of the field; in a ring of powdercaps, three had been taken over by the parasite. Close inspection showed that the lower part of the stem was still that of the Earthy Powdercap – but the upper part had been converted to that of a very different toadstool with a purplish cap. One species captured by another! You could even see the point on the stem where the crime had taken place. There were probably better specimens, and they would have grown further given another day or two, but I had at last seen this perplexing toadstool for myself. Torben then told me he had discovered a second, shaggier and even rarer strangler (Dissoderma pearsonii) on the same host, but growing in a different meadow. We had better come back to see that one.
The stranglers lead to so many questions. It is difficult to understand why the powdercap is particularly vulnerable – so much so that two parasites had evolved to take advantage of the same species. After all, the Lakeland field was full of other toadstools – not least waxcaps – that could have played host. Perhaps it is because stranglers are more closely related to the powdercaps than to the other fungi. They are like the ne’er-do-well cousins that sponge off His Lordship in the big house: only blood relatives could get away with it. Then we need to know why they are so excessively rare; if the parasitic lifestyle could succeed in one spot in a field, why not all over? Why not in my garden? If this parasitic lifestyle is viable on powdercaps, there seems to be no reason why it should not have arisen multiple times with other kinds of mushrooms – but that is not the case. There are no Milkcap Stranglers or Parasol Stranglers. And if stranglers need powdercaps to complete their life cycles, one has to wonder where they lurk for the rest of the time. The wonderful thing about mushrooms is that for every question answered there are a dozen posed.