Busting the “No Known Poisonous Polypores” Myth: Hapalopilus nidulans

The cap of Hapalopilus nidulans starts out finely tomentose
but becomes glabrous with age.

I don’t know how many times I’ve read this phrase over the past couple of years: “There are no known poisonous polypores.” I see it mostly on internet forums, and mostly on threads about edible or medicinal fungi. Someone will excitedly post a photo of their first “chicken of the woods” (Laetiporus sp.) or “reishi” (Ganoderma sp.), photos that regularly, and clearly, show that the poster has got the wrong ID. This happens unbelievably frequently with the fad medicinal, “chaga” (Inonotus obliquus). A photo of a burl or gall, growing on the trunk of a tree that is obviously not a Betulina of any sort, will be posted as “chaga” and everyone will chime in their congratulations and suggest that the finder immediately race back to hack away at a living tree with a hatchet to claim his or her "prize." When someone sensible suggests that one of the above IDs may be flawed, another poster will jump in with the claim that a misidentification doesn’t matter anyway since “there are no known poisonous polypores.”

Well, it’s not true. There is at least one seriously toxic polypore, Hapalopilus nidulans (H. rutilans).  

Hapalopilus nidulans can be overlooked since it's often
quite small and frequently grows alone.

H. nidulans is an unassuming, cinnamon-coloured polypore that can grow up to 10 cm wide, though it's usually considerably smaller. It has a rough or smooth cap and small angular pores, 2-4 per millimetre. When fresh, its flesh is soft and watery; when dry it's tough and hard and can be quite brittle. A white rot agent, it prefers a wide variety of deciduous trees, but can occasionally be found on conifers. Though it's widely distributed east of the Rockies, it's not particularly common. 

The small, angular pores of Hapalopilus nidulans

An Impressive Chemical Reaction

Basically, it's an easily overlooked, unexciting fungus—unless you happen to have some KOH handy, or a bottle of ammonia tucked under your kitchen sink. Personally, I loathe the smell of ammonia, probably because I once had a 19-year-old cat that could no longer find its box. Though that cat is long dead, I still put up with the stink of ammonia since this inexpensive cleaning solution is a wonderful tool for any fungiphile as many species of bolete undergo specific colour changes when hit with a drop of it—as does H. nidulans.

When this otherwise boring fungus comes into contact with either ammonia or KOH, it immediately turns a psychedelic fuchsia (or cherry red in other parts of the world), a reaction that's so magical and so spectacular it's hard not to play with the effect over and over again. At least it is for me. It's also a fabulous part of anyone's arsenal of ultra-cool things to get kids interested in mycology, along with reconstituting jelly fungi and locking children in dark closets with bioluminescent mushrooms. H. nidulans is also much sought after as a natural dyeing agent that—again with the help of ammonia—produces purples that are both more vivid and more fast than those produced by other fungi.

A drop of KOH or ammonia on Hapalopilus turns it a crazy purple/fuchsia
—though not as crazy as these web colours are making it look.

Toxicity

And apparently there's also nothing boring about eating this humble little character, though, from the sound of it, there's nothing pleasant about it either. The few cases of poisonings on record, including one adult and two children in the late Eighties, and a father and daughter a couple of years ago, (the latter incident involving the consumption of H. nidulans after misidentifying it as the "beefsteak fungus," Fistulina hepatica), have all been similar in their descriptions of signs and symptoms that happen after a delay of at least 12 hours, the results of dysregulation of central nervous system functions and liver and kidney dysfunction:

• abdominal pain
• nausea and vomiting
• headache
• visual disturbances, including double vision, blurred vision, hallucinations
• multidirectional involuntary eye movements
• balance disorders 
• general weakness
• loss of appetite
• signs of liver and kidney failure
• and violet-coloured urine

The culprit is likely polyporic acid, which can make up an astonishing 40% of H. nidulans by weight. In a lab study, rats given straight polyporic acid via probang developed "strongly reduced locomotor activity, depressed visual placing response and impaired wire manoeuvre," as well as hepatorenal failure and low blood potassium and calcium levels, symptoms that closely parallel those of the people who ate the fungus. I am not sure if the urine of these poisoned rats turned purple or not—but I bet a cat's would! 

Hapalopilus nidulans is watery and soft when fresh and often feasted
on by slugs that are, presumably, unaffected by polyporic acid.

As noted above, the father and daughter poisoned by H. nidulans mistook it for Fistulina hepatica, which is a well-known edible. I have to assume they were not experienced foragers since there are very clear differences between Hapalopilus and Fistulina. Unlike the soft, fibrous flesh of H. nidulans, the flesh of F. hepatica is strangey meat-like, streaky whitish and reddish, and "bleeds" a reddish liquid when squeezed. The surface texture of both cap and stem is finely, and peculiarly pebbly. The tubes on the undersurface are also completely different—easily separable because they are not fused together as they are in most polypores (see my Cyphelloid Wannabes post for more info). 

Two people poisoned by Hapalopilus nidulans mistook it
for an edible Fistulina hepatica, like this one.

Fistulina hepatica has separate, unfused tubes and the
flesh is much more meat-like than Hapalopilus nidulans.

References & Resources:

Michael W. Beug, Polyporic Acid in Fungi: A Brief Note, McIlvainea, Vol. 21

Kraft, J., S. Bauer, G. Keihoff, J. Mieersch, D. Wend, D Riemann, R. Hirschelmann, H-J Holzhausen, J. Langer. 1998. Biological effects of the dihydroorotate dehydrogenase inhibitor polyporic acid, a toxic constituent of the mushroom, Hapalopilus rutilans, in rats and humans. Arch Toxicol 72:711-721.

Villa AF, Saviuc P, Langrand J, Favre G, Chataignerl D, Garnier R: Tender Nesting Polypore (Hapalopilus rutilans) poisoning: report of two cases. Clin Toxicol (Phila); 2013 Sep-Oct;51(8):798-800

Dyeing with Hapalopilus: http://www.allfiberarts.com/library/mushrooms/hap-rutilans.htm

The only other known cause of purple urine

Species descriptions of Hapalopilus nidulans: 

Mycoquebec (as Hapalopilus rutilans)

Mushroom Expert

"Eyelash Cups" on Moose and Deer Dung: Cheilymenia stercorea

Okay, go ahead, call me weird, but ever since I found Pseudombrophila porcina polka-dotting my dog's poop last spring I've been getting down on my hands and knees in the woods to closely inspect the dung of other animals. If I see something that could be something, I bring it close to my eye so I can magnify it with my loupe.

Handling dung isn't really a stretch for me. I'm an organic gardener, so I've been intimately familiar with livestock manure for going on thirty years. Black gold, we call it. We top-dress perennials with it in the fall, dig it into the vegetable garden in the spring, and brew hundred-gallon vats of manure tea throughout the summer to use for watering. 

A small cluster of Cheilymenia stercorea apothecia on a moose pellet...

...and on deer dung.

Since there's a healthy population of deer where we live, there are also plenty of piles of deer droppings in my foray woods, so these have been my primary sources for finding all kinds of mini coprophilous ascomycetes. I also stray a couple of hours further north a few times each season into moose habitat, and it was on one of these forays that I found my first Cheilymenia stercorea that were large enough (2 mm diam.!) to spot without the assistance of magnification. Since then I've found three more fruitings of these eyelash-rimmed orange disks on local deer droppings. Apparently they also commonly colonize horse and cow manure, though I haven't yet found any on my garden supply.

An illustration of Cheilymenia stercorea (Fig. II) from 1790, back when its name was Peziza ciliata. (Bulliard)

My favourite thing about these little guys is what their hairs look like under the microscope. Compared to their cylindrical asci, which, at about 200 µ, aren't exactly short (at least for asci), their hairs are gigantic—and spectacularly graphic. Some are multi-septate, others have barely any divisions at all, while a third type found lower on the apothecia are diagnostically stellate with two to five septate arms projecting from swollen basal cells. 

Cheilymenia stercorea hairs and asci 

Cheilymenia stercorea hairs dwarf the asci.

Two three-pronged stellate hairs

A four-armed stellate hair

Cheilymenia stercorea is considered to be an obligate dung decomposer—it never shows up anywhere else. There are several other outwardly similar Cheilymenia speciesthat also grow on dung, such as C. fimicola and C. raripila, but these lack the basal stellate hairs. 

The spores of all Cheilymenia have an outer layer that loosens into a floating sheath around the spore "when heated in lactic acid." I haven't tried this treatment yet, as I'm not sure how one would go about doing it. It sounds so wonderfully arcane that I would like to try it. Could I just do a mount with a drop of my fermented dill pickle brine and hold a match underneath? Would that work? Perhaps someone with more experience could give me some tips.

Cheilymenia stercorea has smooth, ellipsoid spores, slightly
 clavate paraphyses and long, slender, cylindrical asci.

References & Resources:

Denison, William C., The Genus Cheilymenia in North America, Mycologia, Vol. 56, No. 5 (Sep. - Oct., 1964), pp. 718-737

Ascomycete Fungi of North America: A Mushroom Reference Guide, Michael Beug, Alan E. Bessette, Arleen R. Bessette, University of Texas Press, 2014

Diabolical Parasites: Ophiocordyceps variabilis and Relatives

My fungi friend Ulli and I were crashing through the bush on our way back to the car after a day of searching for oddities near Dorset, Ontario, when she pointed out these little beauties on a large rotting log. "Good eye," I said, since whatever they were, they were barely a centimetre tall. 

Having no reading glasses with me, nor time to inspect them with my loupe, and thinking the orange blurs were simply shrivelled jelly or coral fungi (it hadn't rained in a while), I roughly carved them out of the log and stuck them in a container in my basket.  

Ophiocordyceps variabilis with larval host (visible at right)

It wasn't until I had a chance to look at them more closely the next day that I realized they were something good, something really good—a Cordyceps of some kind, an ascomycete that parasitizes insects. Not only that, but by collecting them along with a chunk of the rotting log, which I confess I'd done for no other reason than to not lose them among other small finds of the day, I'd conveniently also gathered the larval host, a larva that, because of its bright orange-brown colour, I assumed was a youthful Coleoptera, or beetle.

Xylophagus fly larva mimicking a beetle larva—host of Ophiocrodyceps variabilis

Silly me. 

After a bit of micro work and some research, I got a name, Ophiocordyceps variabilis, a species that actually only attacks wood-inhabiting Diptera, or fly, larvae. The hosts of mine have been identified by Ziggy, an entomologist friend (Ulli's daughter, in fact!), as belonging to the genus Xylophagus—which is exactly the genus cited in a paper about O. variabilis Ziggy fished up for me. It helps to have friends in buggy places! 

The fertile portion of Ophiocordyceps variabilis stromata are

strongly textured by protruding perithecial ostioles.

Though O. variabilis, like many Ophiocordycipitaceae, is not well studied, it probably invades an unsuspecting host in a similar way to more studied species: after adhering to the exoskeleton of a larva, a spore germinates, grows a specialized structure that, in combination with pressure and the secretion of lipase and protease enzymes, allows it to penetrate the exoskeleton. Once past this barrier, the fungus grows and divides and, in some species at least, causes aberrant behaviour in the host before the host dies. Post death, the fungus consumes the innards, filling the intact exoskeleton with tightly packed, often peanut-shaped, hyphal bodies. During this process, the larval victim of O. variabilis changes colour, darkening from cream to burnt sienna, which makes it easy to mistake it for the larva of a beetle, so easy, in fact, that beetle larvae have regularly been erroneously named as the hosts of O. variabilis in the original description and elsewhere. 

A second, surprise, Ophiocordyceps variabilis I unknowingly collected
the same day as the ones pictured above that I found in a
container in the fridge a month later.

Eventually, when conditions are appropriate, O. variabilis sprouts its usually single fruiting body—a cylindrical yellowish orange stroma, ranging from 2-24 mm tall, with a terminus that is ornamented with variably shaped cushions holding orange-tipped perithecia. These perithecia contain characteristically thick-capped asci with multiseptate filiform ascospores that, once released, fragment into part-spores. 

And the life cycle goes on. 

Which is all fine and good, but I have a question. If the spores are dispersed by air current, as is assumed, how do they get inside the rotting logs where the eggs that produce these Diptera larvae are deposited? Ziggy has watched another wood-inhabiting Diptera, a cranefly, inserting its ovipositor deep into a rotting log and suggests it is perhaps via this apparatus that spores could be introduced into the wood. But she says, too, that since Xylophagidae larvae prey on other wood-inhabiting larvae, these other larvae could be carrying spores on their cuticles or inside their guts, thus infecting their assassins as a kind of post-mortem revenge.  

The asci of Ophiocordyceps variabilis wear "hats" and their multiseptate
filiform spores fragment into "part-spores" when they're released.

Almost all Ophiocordyceps and their close relatives, Cordyceps, are entomopathogenic: they  parasitize insects, and usually kill them as well. Though there are a number of temperate-zone species, the greatest diversity is distributed throughout the tropics, where several hundred have been identified. Though most of these fungi are restricted to a single host species, or closely related ones, as a group they are known to victimize a wide range of arthropods from at least ten different orders, ranging from flies to Lepidoptera to grasshoppers to spiders. Some species specifically attack adults, while others infect larval, nymph, or pupal stages. 

Cordyceps locustiphila (Susanne Sourell, Mushroom Observer)

The morphology of their spore-producing structures is as varied as the host species they attack. Some form clusters of stromata, while others sprout one or two long, serpentine appendages with mace-like tips. Some of these erupt willy-nilly from their victims, while others always grow from a specific part of the anatomy, such as between the head and the thorax. There is a fabulous book out there, by Japanese mycologists D. Shimizu and K. Kobayasi, featuring exquisite illustrations, a book I'd love to get my hands on if I ever have a few hundred dollars to spare. You can also click here to see Daniel Winkler's spectacular photos of numerous species. 

Cordyceps discoideocapitata from the Japanese book,  冬虫夏草図鑑―カラー版,
(Illustrated Vegetable Wasps and Plant Worms in Colour) ISBN-10: 4-259-53866-7.

Cordyceps sp. from the same book.

Beyond the aesthetics of their fabulously sculptural stromata, Ophiocordyceps and Cordyceps species are attracting attention from researchers worldwide for the abundance of biologically active compounds they produce. O. sinensis, an Asian species endemic to the Tibetan plateau, which has been used in traditional Asian medicine since at least the 15th century, and C. militaris, which occurs in North America, both produce a biometabolite, Cordycepin, which has been shown to be a broad-spectrum antibiotic and polyadenylation inhibitor, and is currently being investigated for tumour suppression properties. Anamorphs of several other species are already being used as insect biological control agents, or pesticides. 

But there's another really interesting "control" aspect of at least some species of Ophiocordyceps and Cordyceps: they brainwash their victims, causing them to behave in ways that are advantageous for the pathogen. 

(David Hughes)

In the case of Ophiocordyceps unilateralis and other closely related species that infect mostly tropical, tree-dwelling carpenter ants, the process works something like this: a spore that has adhered to the exoskeleton of an ant grows an appressorium that produces hypha that penetrate the ant's protective armour using a combination of mechanical pressure and enzymes. Once inside, the parasite grows as free-living yeast cells, eventually producing nerve toxins that alter the ant's behaviour. The ant staggers away from the colony, descending from the dry canopy to the humidity of the ground where, between convulsions, it ascends a small sapling at high noon. The ant clamps down on the main vein of a leaf with its mandibles at a height of about 25 cm. above the soil surface. The ant soon dies, but the life of the fungus continues. Hyphae emerge from orifices and joints, welding the ant to the leaf, while at the same time saprophytic mycelia run rampant through the corpse. Eventually, the fruiting stalk bursts forth from the rear of the head, its fertile surface knobbly with perithecia that produce the asci, which forcibly eject spores into the forest (watch BBC video here).     

Ophiocordyceps unilateralis growing from a carpenter ant. (David Hughes)

David Hughes of Penn State University is at the forefront of research into these fungi and the chemical mechanisms behind their creation of zombie ants. Controlling a host's behaviour is an example of an extended phenotype, or, as Hughes writes: "While the manipulated individual may look like an ant, it represents a fungal genome expressing fungal behaviour through the body of an ant." 

Ophiocordyceps camponoti-balzani, a recently discovered species,
growing out of a "zombie" ant's head. (David Hughes)

Hughes and his colleagues have shown that an infected ant's jaw muscles atrophy, keeping the mandibles locked in place long after the ant's demise, a "death grip" that is clearly advantageous to the fungus since it keeps the host in the optimum location long enough for spores to be produced. With the help of gene-sequencing and metabolomics (the analysis of bioactive chemicals produced by a particular genome), Hughes and his team have now identified the likely chemical compound that causes the atrophy. Other colleagues, working at Penn State's Genomics Institute, have found molecules that play a key role in the "mind control" of the so-called zombie ants.  

These compounds and others that will can expect to be isolated from various Ophiocordyceps and Cordyceps species will likely have wide-ranging uses in agriculture, pharmacology, and other fields—yet another reason to preserve, and fund studies in, our planet's diverse ecosystems.

But back to my O. variabilis: I was curious about whether or not this fungus is known to manipulate the behaviour of its fly larva hosts and posed the question to Hughes. His reply was that, though there are anecdotal suggestions of other insects (flies, crickets, moths) being manipulated, i.e. being found in unusual locations, no one has looked at any of these species in detail. At least not yet. 

Resources & References:

Codyceps.US - an Electronic Monograph of Cordyceps and Related Fungi

Daniel Winkler's Cordyceps blog

David Pacchioli’s article about David Hughes & his work, “Getting to the bottom of the zombie ant phenomenon” on Penn State news

Hughes, D.P., Andersen, S.* Hywel-Jones, N.L. , Himaman, W., Bilen, J and J.J. Boomsma. Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection BMC Ecology 2011, 11:13doi:10.1186/1472-6785-11-1

Hughes, D.P. Parasites and the Superogranism (2012). In Host Manipulation by Parasites Edited by David P. Hughes, Jacques Brodeur, and Frédéric Thomas 

Hodge, K.T.; Humber, R.A.; Wozniak, C.A. 1998. Cordyceps variabilis and the genus Syngliocladium. Mycologia. 90:743-753

Fantastic BBC video showing time-lapse of Cordyceps growing from ant's head!