Rust Fungi: Femme Fatales, Gorgons, and a Surprising Honeybee Connection

The first important thing you need to know is that we make wild black raspberry wine. The second thing you need to know is that it's amazingly delicious. The third thing is that, this year, it's unlikely we'll harvest even a handful of berries, let alone the eight pounds we need for a batch of wine.







Tragedy has struck! Mind you, it's an uncommonly beautiful tragedy: a parasitic rust has attacked every one of our black raspberry patches. The colour of this fungus, unlike any iron rust I've ever seen, is a fluorescent 1969-blacklight-poster orange, a don't-hit-this-on-a-dark-road-in-the-middle-of-the-night orange, a ridiculously blinding, especially-when-placed-against-new-green-raspberry-leaf orange. So pretty! So deadly!

Black raspberry rust on underside of leaf.

There are more than 7,000 species of rust fungi out there, obligate parasites that cause varying degrees of destruction to their hosts, some of which are major food sources for our species. 

Arthuriomyces peckianus

The rust on my black raspberries is Arthuriomyces peckianus, which is extremely similar to Gymnoconia nitens, a species that prefers blackberries. Both are autoecious, meaning they require only a single host to complete their life cycle. Most other rusts are heteroecious, alternating between two completely unrelated hosts. Some of these dual-host species have such a complicated reproduction strategy that they produce what I think is a plethora of spore types, covering all the bases with not just one or two, but up to five different kinds of spores (for more info go here). 

Arthuriomyces peckianus aeciospores

Puccinia coronata

Members of the genus Puccinia for instance, some of which are pathogens of cereal grains, all produce five spore types. The one my friend Tony and I found growing on buckthorn leaves while collecting for Ontario's 2014 Bioblitz, Puccinia coronata, causes oat and barley crown rust. First found in North America in Nebraska in 1992, here it is in Toronto less than twenty-five years later. Its affect on oat and barley yields is not yet known. But look how pretty it is!

Puccinia coronata forms tiny erupting bumps on the underside of buckthorn leaves.

Buckthorn rust aeciospores

Cronartium ribicola

Cronartium ribicola attacks five-needle pines.

Another rust that has five spore stages is Cronartium ribicola, that creates very cool-looking yellow-orange hieroglyphic blisters on the trunks and branches of white pine. These blisters swell and eventually burst open spreading millions of spores far and wide. White pine blister rust's unlikely alternate hosts are wild and domesticated currants and gooseberries, as well as Indian paint brush and, of all things, snapdragons. Though it was introduced to North America more than a hundred years ago, our five-needle pines still have little resistance to it and suffer high mortality when infected.  

Gymnosporangium juniperi-virginianae

Despite its less intense colour, my favourite rust, if one can have a favourite, is cedar-apple rust. Known by the Latin mouthful, Gymnosporangium juniperi-virginianae, this species jumps back and forth between eastern red cedar (and other junipers) and apple or crabapple trees. It overwinters in the form of a gall on cedar branches. When spring rains arrive, horn-like structures, or telia, are extruded from the galls. The telia absorb moisture and swell, producing a mop of jelly-like orange snakes, the Gorgon of my title. They can shrink and swell numerous times in a single season, producing thousands of teliospores (a spore type) that, in turn, produce basidia, from which basidiospores (another spore type!) are expelled. Wind carries the basidiospores to apple trees, where the disease cycle continues. 


Infected apple trees can suffer major defoliation that can increase winter damage, affect fruit size and quality, and deform apples. Apple growers are sometimes advised to destroy all cedar trees growing within a mile of their orchards, which is perhaps an unrealistic way to deal with the problem. Of course, the other way to stop infection is to spray with fungicides. Or eat gnarly apples, which, incidentally, make another great wine.

The jelly-like telia of cedar-apple rust appear in
the spring on eastern red cedar.

The Honeybee Connection

But here's where rusts get really cool. For more than a century, people have been observing honeybees collecting spore "pollen" from various species of rusts. This happens often enough that rust spores are regularly found in hives as well as in the guts of honeybees (I have to say I was thrilled to hear that beekeepers inspect their bees' gut contents!). So what's going on?

First off, many individual rust spores are similar in size to the pollens bees collect, so it's easy for them to pack them into their pollen baskets. Honeybees are more likely to collect rust spores when there is a dearth of pollen. Rust spores aren't high in protein, but there may be enough to supplement the bees' diet when pollen sources are low. Though some spore-collecting bee colonies seem fine, others show clear signs of decline. Is this a sign that the spores are toxic, or does it simply point to poor nutrition in the hives? More study is obviously needed.

The dispersal of spores by honeybees and other insects is certainly advantageous for rust fungi and they have clearly evolved to tap into this transport system. Their day-glo orange colours, high in yellows, are very visible to honeybees and other insects. Some rusts also produce a sweet pycnidial secretion, mimicking flower nectar, while others go so far as to produce floral scents. Some rusts use all three of these strategies.

So, basically, the orange spots or blisters produced by many rusts are "pseudoflowers," and their purpose, using colour, and sometimes sugar and scent, is to attract insects to help carry their spores closer to their alternate hosts, or, in the case of the Arthuriomyces peckianus on my black raspberries that has no alternate host, to attract insects that will then carry spores to an uninfected berry patch where the insects might visit real flowers that are, conveniently, blossoming at the same time that the rust is producing spores. Sadly, I have a feeling our run of black raspberry wine is over.

More Information:

Black raspberry rust
Oat and barley crown rust
White pine blister rust
Cedar apple rust

Bees & Rust Spore References

Raguso, R.A., and Roy, B.A. (1998) ‘Floral’ scent production by Puccinia rust fungi that mimic flowers. Molecular Ecology 7, 1127-1136

DANIEL McALPINE MEMORIAL LECTURE 1999 

Bees and fungi, with special reference to certain plant pathogens

D.E. Shaw 

Shaw, D.E., and Robertson, D.F. (1980) Collection of neurospora by honeybees.  Trans. British Mycol Soc. 74 (3): 459-464.   

Bee/Fungi related: Interesting article about polypore extracts being tested on honeybees to fight viruses spread by Varroa destructor mites.

Gyromitra esculenta and Gyromitra gigas: Two False Morels

Gyromitra esculenta contains large amounts of the toxin, gyromitrin.

When we first moved to east-central Ontario, old timers on our road told us they'd seen people coming out of our woods every spring with garbage bags filled with morels. Green garbage bags! So every spring we've battled black flies and mosquitoes, and poison ivy so fresh you just have to look at it to get a half-body rash, in search of this mythical motherlode, and every year we've fallen short. A few morels, yes. Garbage-bagsful, absolutely not.

What was going on? Where were these famous mushrooms? I finally figured it out when, one May day, I bumped into a stranger in the woods. A stranger with a big bag full of...not delectably edible morels, but false morels—Gyromitra esculenta, to be precise. He'd been eating them for years, he told me. 

"Maybe not for many more," I suggested, a less confrontational reply, I decided, than starting a discourse about trespassing.

Unlike real morels, false morels, like Gyromitra esculenta, are not hollow.

Though we could, indeed, easily fill garbage bags with the crop of G. esculenta that pops up in our local woods every spring, we won't be eating any of them, because they, and several other Gyromitra species, contain varying amounts of gyromitrin, a toxin and probable human carcinogen that metabolizes in the body into—believe it or not—rocket fuel (monomethylhydrazine). 

Though people claim that by using specific cooking methods they can render various Gyromitra species edible ("esculenta" actually means "edible"), there may be long-term cumulative effects of the toxin, and 2 to 4 percent of all fungal fatalities are associated with them. Before anyone convinces you to try eating one, please read Tom Volk's excellent page on their toxicity.  

Though there's a fall species in my area, G. infula—that's usually saddle-shaped and grows on rotting logs—the only spring one I've found around here is G. esculenta. Last weekend, though, on a Mycological Society of Toronto foray northeast of the city, we found a different one.

Gyromitra gigas looks less "brainy" than G. esculenta.

I have no photographs of it in place because, before I plucked one for display, it fooled me into thinking it was G. esculenta. Its fertile surface was a warm brown, and it was somewhat contorted. I didn't look at it closely until I got back to the parking lot and saw that it was less "brainy" looking than usual, had an abnormally stout stipe, and, when I cut it in half, had cottony white material in its convoluted interior. It wasn't  an abnormal G. esculenta, it was G. gigas, (often split into G. korfii in the east, and G. montana in the west).

Gyromitra gigas has a convoluted interior.

Cottony interior of Gyromitra gigas

Gyromitra esculenta and G. gigas differ even more different under the microscope. The spores of G. esculenta are kind of nice in their smooth, fusiform to elliptic clarity, usually containing two oil droplets at either end, while those of G. gigas are slightly roughened and fusiform, with several small oil droplets orbiting a larger central one. Most notably, though, the spores of G. gigas have two knob-like apiculi at either end.

Gyromitra esculenta spores have two oil droplets.

Gyromitra gigas asci, spores, and colored paraphyses.

Gyromitra gigas spores have knoblike apiculi on either end.

Gyromitra gigas apparently contains much less gyromitrin than G. esculenta, and is thus generally considered to be a safe edible, but since this G. gigas appears to be a species complex that may vary considerably from place to place I think I'll wait until more study is done before eating it.  



References:

Gyromitra gigas on Mycoquebec
Gyromitra esculenta on Tom Volk's Mushroom of the Month




Tom Volk's excellent page about Gyromitra toxicity.

Chlorociboria and Patinellaria sanguinea: Colourful Wood Spalting Fungi

Patinellaria sanguinea stains wood coral red. 

It’s easy to forget while collecting fungi that the ones we find growing on wood and elsewhere are only their fruiting bodies—the actual organism is usually hidden, its mycelium buried deep in wood or soil. But the microscopic mycelium of some wood-loving fungi make it very clear just how large an area they’ve taken over by staining the wood they’ve colonized. This staining, which can sometimes be dark lines, other times extensive areas of colour, is called spalting.

Wood stained blue-green by the fungus Chlorociboria.

The fairly common Chlorociboria aeruginascens and its sister C. aeruginosa, which can only be differentiated microscopically, stain the wood they’ve colonized a stunning blue-green with the pigment xylindein. This beautiful blue wood has been used by woodworkers since at least the 15^th century, primarily in inlays (see examples here). It’s such a striking colour that studies are underway to find a way to inoculate various forest trees with Chlorociboria to enhance the value of the lumber. Personally, I’m impressed that anyone has ever found a piece of this blue wood in good enough shape to use for anything other than as a conversation piece. In my experience, whenever I find it, the wood is already so decomposed I can easily pull it apart with my fingers.

Chlorociboria produces gorgeous blue-green fruit bodies.

Serendipitously, I recently came across a much more uncommon Helotiales that also stains wood.

Slightly dried Patinellaria sanguinea discs and subiculum.

A month or so ago, I brought in a branch I’d left outside for the winter that had had the beginnings of a mystery purple crust growing on it in the fall. I hoped that by giving it a little warmth and moisture it might revive and offer me some spores to help in its identification. But nothing happened. Well, actually something happened—the purple corticioid started decaying. I was about to relegate the branch to the kindling pile when I noticed that in a couple of places its surface was oddly coloured with reddish-pink spiderwebby fuzz. I assumed this was just an unusual mold, but when I got out my loupe to inspect it I was surprised to see a multitude of minute blackish discs embedded in it. Helotiales type discs. Hmm.

Amazing colour of "black" Patinellaria sanguinea fruit bodies under the microscope.

When I put a sample under the microscope I immediately saw that the pink fuzz was not a mold, but a hyphal mat, or subiculum, that clearly belonged to the blackish discs. Not only that, but, when sectioned, the “black” discs were actually quite strikingly coloured. There were even some asci and spores.

Wonky ellipsoid to clavate spores of Patinellaria.

I didn’t have a clue what it was, or even how to start looking to find a name since nothing like it was in either Fungi of Switzerland or the brand new Ascomycete Fungi of North America. I got my knife out and carved a few chunks off the branch to dry for later study. It was only then that I realized my little ascomycete had another interesting characteristic: it had stained the wood a gorgeous coral red. Surely, I thought, this would make finding its identity easier. But still no luck on Google or Ascofrance or anywhere else.

Days passed. I was doing an unrelated image search for another minute black disc, Patellaria atrata, this one sans color, when halfway down the page a picture jumped out at me. It clearly showed exactly what I had accidentally grown—mini blackish discs with a pinkish red subiculum. And they had a name. Panitellaria sanguinea.

I have not been able to find out much about this little curiosity, which has also been known as Durella sanguinea and Peziza sanguinea, other than that it’s rare, grows in North America and Europe, and apparently prefers hardwoods. If anyone can add anything else, I’d be grateful.

More Info:

Tom Volk’s Chlorociboria page

Panitellaria sanguinea on Mycoquebec

Panitellaria sanguinea on Mycokey
Robinson, S.C., Tudor, D., Snider, H., Cooper, P.A. 2012. Stimulating growth and xylindein production of Chlorociboria aeruginascens in agar-based systems. AMB Express 2(15).
More about spalting: Northern Spalting

George Grant Hedgcock. "Studies Upon Some Chromogenic Fungi which Discolor Wood." St. Louis, 1906

A Poop & Scoop Ascomycete: Pseudombrophila porcina

Our puppy Ruby—now almost a year old—developed an interesting habit after the first snow last fall: she used her snout as a shovel to meticulously bury every one of her droppings. Okay with us. Out of sight, out of mind, as far as we were concerned. But when the big thaw happened a couple of weeks ago we ended up with a major yard and garden clean-up that had nothing to do with last year's plant matter. 

As happens, we missed a couple, and a few days ago I came across one of these strays. I was about to scoop it up with a shovel and toss it into the woods when I noticed something peculiar about it. It was polka-dotted. 

Sigh. 

I knew what I had to do—get out my loupe so I could closely inspect, yes, my dog's doodoo. This is the life of an ascomycetes freak. And here's what I saw, which, precisely because I've turned into an ascomycetes freak, was exciting:

Immature Pseudombrophila porcina on dog feces.

I'd obviously found a coprophilic fungus. A dung lover. But which one? There are lots to choose from, especially from the ascomycetes clan. "Lots" is a good thing—I don't know about everybody else but I like the idea of animal dung being broken down and returned to the earth as quickly as possible, and fungi are perfect for the job.

Immature Pseudombrophila look like tiny beads.

My find was clearly immature, so I got a couple of pieces of toilet paper and a pair of tweezers and brought a sample into the warm house where I dampened the paper. With this simple coaxing, two days later the tiny brown beads had turned into pale beige discs with furry exteriors. The biggest was about 2 mm across.

Mature Pseudombrophila porcina are still tiny.

A bit of digging got me to two very similar species in the genus Pseudombrophila that are both known to colonize herbivore and carnivore dung, P. porcina and P. merdaria. After reading an illuminating discussion about these two on Mycofrance, I went to the microscope. 

Pseudombrophila porcina spores.

The spores were smooth and the tips of the paraphyses were not inflated, so it looks like mine are Pseudombrophila porcina. 

I hate to say it, but as unpleasant as animal dung might be, for people like me it's still worth taking a closer look. 

References:

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