"Supersonic" Dung Cannons: Pilobolus oedipus

(N.B. This post was originally published with the erroneous ID of Pilobolus lentiger. Thanks to Malcolm Graves for catching my error and pointing out that, because of its double-walled spores, this is actually Pilobolus oedipus.)

 

My friend Ulli handed me a large Tupperware container. "A present," she said.  

A peak under the lid revealed a large pile of horse manure—always a nice gift for an organic gardener. But this wasn't just any horse manure, this was special horse manure: it had sprouted a massive colony of a dung-loving fungus called Pilobolus, also known as the Dung Cannon or Hat Thrower. 

Golden clusters of Pilobolus lentiger on horse dung.

Pilobolus species, (which, like the Spinellus and Syzygites I wrote about in my last post, belong to the order Mucorales), are impressive little coprophiles that, despite their smelly choice of substrate, are not only well-studied, but have even managed to hit the news as the "Fastest Living Thing on the Planet." 

Pilobolus species are usually the first coprophilous
fungi to produce fruit on herbivore dung.

Copriphilous fungi evolved to produce fruiting bodies in animal waste, and the way the spores that produce these fruiting bodies get into that waste is usually via the gut, which means the spores first need to be ingested. There's a problem with this scenario, though: herbivores shun their own, and others' excrement when they're grazing. Each animal, in fact, has its own well-defined "zone of repugnance." So how to get the spores far enough away from the dung to be eaten? Build a squirt gun, that's how—at least that's how Pilobolus species do it. And impressive squirt guns they are. Some are capable of expelling spores more than six feet (2 m) away, which, in human terms, would be like having a kid's water pistol that could hit a target 500 ft. (150 m) away.   

The spore capsules launched by Pilobolus species are coated
with a sticky material that glues them to nearby blades of
grass or, in this case, the wall of a plastic container.

Using only the normal, osmosis-generated pressure levels of fungi cells, Pilobolus spores are launched so fast that, until recent advancements in high-speed photography, the action was invisible to the human eye. Though the spore packets only reach maximum speeds of 25 meters per second, which isn't exactly shabby for something less than a millimetre in diameter, their acceleration is stupendous—up to 180,000 G! I witnessed this spectacular feat, or more accurately was its target, while trying to take close-ups of these tiny fungi. I felt a distinct ping! on my cheek, then another on my forehead, then another on my lip. It felt strange to be under attack by tiny missiles, stranger still to know that these missiles were probably being aimed at sunlight reflecting off my face.

Pilobolus oedipus

Structurally, a single Pilobolus consists of a long, thin sporangiophore that is expanded at the end into the subsporangial vesicle. The fluid-filled vesicle is capped by a black sporangium, or spore packet, with resistant walls. Orange pigments inside the sporangiophore act as light sensors which, in conjunction with the subsporongial vesicle that functions as a lens, allow the fungus to track light and angle towards it. In essence, Pilobolus have "eyes," eyes that aim for the brightest light around, the sun. Their aim is pretty amazing, too. You can place them in a dark box with a single pinhole of light and after a few hours you will find their spore capsules glued in a tight cluster around the pinhole. 

Some Pilobolus species, like my P. lentiger, also have rhythm. Not that they're dancers, (though maybe with time-lapse photography and a moving light source it might appear as if they're dancing—anybody?), but there's rhythm to their sporulation. When researchers placed them in either continuous light or continuous dark, sporangia were discharged almost continuously. But in a half-day-of-light/half-day-of-dark cycle, they consistently discharged sporangia most vigorously 6 hours after the light period began. 

Pilobolus oedipus spores are globose double-walled.

 The black sporangium with its load of spores—the missile part of 
Pilobolus—sits like a hat on top of the subsporangial vesicle.

The spore capsule easily ruptures under the weight of a cover slide.

The columellae that the sporangium sits on
before discharge are mammiform. 

I didn't realize until it was too late that my Pilobolus specimens had
been aiming sporangia missiles at the lens of my camera as well
as my face while I was photographing them outside, hence the
dark smudges on all my micro pics.

Reference & Resources:

Key and descriptions of Pilobolus species found in Brazil

Key and photos of British Pilobolus species
Mycoquebec's key to Pilobolus species 
Spores of a few Pilobolus species
Bruce, V. G., F. Weight, and C. S. Pittendrigh. 1960. Resetting the sporulation rhythm in Pilobolus with short light flashes of high intensity. Science 131:728–30.
"Spore Ballistics" with a nice little video of spores discharging set to music

Cornell Mushroom Blog post on the connection between Pilobolus and lungworm

Fun videos

The Fastest Living Thing on the Planet

18 hour time lapse of Pilobolus crystallinus (if only they'd moved the light around they would have been dancing!)

claimtoken-543f9098dd30f

When Mushrooms Grow Hair: Spinellus and Syzygites megalocarpus

Spinellus fusiger parasitizes Mycena species, like this M. haematopus.

Spinellus fusiger

Though it's hot as stink outside right now, and dry, to boot, most of this summer has been unseasonably cool and moist—perfect growing conditions for all kinds of interesting fungal fruitings, including one I've wanted to see for years, Spinellus fusiger. The weather has, in fact, been so accommodating that I've found this spectacular bread-mould-related growth four separate times. It's hard to care about how crummy the weather is for swimming when hair-raising characters like this keep appearing in the woods.

The long, erect sporangiophores of Spinellus fusiger make the
mushrooms they attack look as if they've been electrocuted.

Spinellus species are parasites that attack your basic mushroom-looking mushroom, and are, in my humble opinion, wonderfully photogenic. The most common in these parts, S. fusiger, prefers Mycena species as its victims, often M. haematopus, which, even when its cap is sprouting a crazy new fungal hair-do, can still be identified by snapping its stem to look for its characteristic "blood."

Spinellus species grow long erect "sporangiophores" tipped by 

spherical spore-producing bodies that darken as spores mature.

Mucorales

Spinellus species belong to the order Mucorales, or "pin molds," in the phylum Zygomycota. The hyphae of these fungi, unlike those of ascomycetes or basidiomycetes, are rarely septate, which means they have no barriers to slow the movement of cytoplasm, allowing them to grow extremely quickly. If you've ever had a loaf of bread that's been colonized by the less spectacular, but much more common mucorale, Rhizopus stolonifer, or black bread mould, you will understand how quickly these fungi can grow.  

Hundreds of asexual Spinellus spores are produced by each sporangium. 

All mucorales produce spores in tiny globose sporangia held at the tips of sometimes very long specialized hyphae called sporangiophores. Though mucorales are capable of reproducing both sexually and asexually, the vast majority of spores are anamorphic, or asexual. 

The stalks of Spinellus, and all other mucorales, 
have a swelling at the tip called a columella.

The balloon-like columellae persist after spore dispersal.

Syzygites megalocarpes

Another woodland mycoparasitic mucorale, is Syzygites megalocarpus. The only species in its genus, S. megalocarpus is nowhere near as choosy about its victims as S. fusiger and has, so far, been found on 65 different genera. It's easily recognized by its multi-branched sporangiophores that make the fungi they parasitize look as if they've not only grown hair, but hair that desperately needs frizz-control. When they first start growing, these sporangiophores are deep yellow due to the carotenoid pigments they produce, but become paler as they stretch out, and eventually turn a more traditional mould colour—bluish gray. 

This Syzygites has made an Amanita flavoconia almost unrecognizable.

This Syzygites megalocarpus appeared overnight on a
Boletus subvelutipes left out on my dining-room table.

An ethereal veil of Syzygites megalocarpus hangs 
from the cap of a small Pluteus species.

Though I've found S. megalocarpus a number of times, they've always either been past their prime or I've been without camera, so I had no usable in situ photographs for this post. Ever the optimist, though, I went out in search of one a few days ago, before this heat wave hit, and—lucky me!—I found a beauty in full glory that had infested a Pluteus growing picturesquely on a log. 

The sporangiophores of Syzygites megalocarpus are 
dichotomously branched up to six times. 

Asexual spores of Syzygites megalocarpus are 
produced on the tips of branched sporangiophores.

So what does a cold summer have to do with finding Spinellus fusiger for the first time? Well, it turns out that Spinellus species, as well as S. megalocarpus, are temperature sensitive, with a distinct preference for cooler weather. Spinellus are the pickiest, requiring temperatures to be lower than 22ºC to grow. I don't know about where you live, but summers here in Ontario have become so consistently hot over the past twenty years that a high of 22ºC has come to be considered "cold." Is it coincidence that, though I'd never come across it before, I stumbled upon Spinellus four separate times this season? I doubt it. And because I doubt it, I'm adding the previous dearth of Spinellus to my growing list of local anecdotal evidence that fungi fructifications are being affected by climate change.   



References:

Syzygites megalocarpus on Mycoquebec
Spinellus fusiger on Mycoquebec
Zygomycota
Mucorales
McLaughlin, D. J., E. G. McLaughlin, and P. A. Lemke. 2001. The Mycota VIIA: Systematics and Evolution. Springer-Verlag, New York.  
Hoffmann, K., Pawlowska, J., Walther, G., Wrzosek, M., de Hoog, G. S., Benny, G. L., ... & Voigt, K. (2013) The family structure of the Mucorales: a synoptic revision based on comprehensive multigene-genealogies. Persoonia 30: 57-76.


Fun: 
Time-lapse video of Syzygites growing