Sunday, 24 August 2014

Read It and Weep: Fungal Guttation

Guttation on Fomitopsis pinicola bracket fungus
Young Fomitopsis pinicola with guttation drops (click to see bigger)
Some fungi are prone to exhibiting a curious phenomenon—they exude beads of moisture, called guttation. In several polypores, such as Fomitopsis pinicola, the liquid produced can look so much like tears that you'd swear the fungus was weeping. Or maybe sweating. Other species produce pigmented drops that can look like milk, or tar, or even blood.

Guttation is more well-known in some vascular plants. During the night, when the plant's transpiration system is shut down, pressure from excess moisture in the roots can force beads of sap out of special structures on leaf edges. 

strawberry leaf guttation noah erhardt
Guttation droplets on strawberry leaves (Noah Erhardt/Wikipedia)
In fungi, the guttation mechanism is not so well understood. In many species, however, it's so often observed, particularly during times of rapid growth when temperature and humidity are favourable, that these beads of liquid can be a reliable macroscopic characteristic. Hydnellum peckii, for instance, so frequently "bleeds" pigmented drops in its early stages of growth that it's been given gruesome nicknames, including "Bleeding Tooth Fungus" and "Devil's Tooth." Coincidentally, a 1965 study found a compound in the fruiting body of  H. peckii that has anticoagulant properties similar to those of heparin, too much of which can make one bleed to death internally.   

bleeding mushroom guttation lisa neighbour
Producing blood-like guttation droplets during periods of rapid growth is 
well-known characteristic of Hydnellum peckii(Lisa Neighbour)
polypore shelf fungus baby weeping guttation droplets
Young fruit bodies of Fomitopsis pinicola commonly produce copious guttation.
A few weeks ago, I came across a crop of Inonotus glomeratus on a maple log. I've found this amazing polypore a few times, once right after it had showered itself, and everything else around it, with what I assumed were millions of sulphur-yellow spores. The one I found this summer, though, was very young, and instead of spewing spores, it was weeping globules of "tar" in copious enough amounts that shiny black pools were accumulating on the forest floor. Unlike most guttation drops, which are watery, these exudations were thick and sticky and stained my finger and thumb a deep auburn brown. And kind of glued them together. Oddly, though this unusual guttation has been noted by others, there seems to be no mention of it in the literature. I. glomeratus is so unusual in so many ways, I've written a whole post about it.

Inonotus glomeratus fungus dripping black tar guttation
Fast-growing Inonotus glomeratus produces tarry guttation.
yellow spores of polypore Inonotus glomeratus
This Inonotus glomeratus continued to drip its viscous black exudate
even after it began releasing its yellow spores.
holes made guttation Inonotus glomeratus
The guttation drops on this Inonotus glomeratus were so thick that the fungus grew
around them, producing a pitted appearance after rain washed them away.
Polypores and Hydnoids are not the only fungi to produce guttation. In moist conditions, young Suillus americanus stipes can be heavy with yellow-tinted drops. Guttation is also common enough in the uncommon Rhodotus palmatus that this characteristic is often included in descriptions. 


Suillus americanus liquid drops stem
Suillus americanus (above) and Rhodotus palmatus (below) 
guttation of young Rhodotus palmatus

Guttation can happen in incredibly small ways, too. During the Toronto Bioblitz this past spring, we found some Lachnum subvirgineum that, despite what seemed like dry conditions, were covered in minute guttation droplets, as were most other Lachnum I've since come across. 



Lachnum subvirgineum with guttation water droplets
The largest of these Lachnum subvirgineum was less than .5 mm. in 
diameter, which makes the guttation droplets impressively small.
Just yesterday I found another ascomycete sporting the same clear drops—this time Incrucipulum ciliare, whose hair-rimmed discs are even smaller than L. subvirgineum, hence, so, too, were its guttation droplets.


ascomycete oak Incrucipulum ciliare
The guttation droplets on these Incrucipulum ciliare were almost too small for 
my camera to capture. The "stick" in the lower right corner is an oak leaf vein. 
Another minute character is so characteristically bejewelled in guttation droplets, it's named for it: Pilobolus crystallinus, which is one of the "Cannon" or "Hat Thrower" fungi found on herbivore dung.


Pilobilus crystallinus cannon fungus
Pilobilus crystallinus is named for its sparkling
guttation droplets. (
Keisotya/Wikipedia)
Though little is known about guttation in wild fruiting bodies of fungi, it's a common phenomenon of fungal mycelia and hyphae in the lab, and a number of studies have been done to determine what the exudates contain. Penicillin has been found in the guttation droplets produced by Penicillium species in similar concentrations to that found in the culture broth, while gliotoxin, which has immunosuppressive qualities, has been found in guttation droplets of Aspergillus fumigatusDo these fungi use guttation droplets as reservoirs for metabolic byproducts, or do they simply use them for water storage

Or have different species evolved to produce guttation droplets for different purposes? The edible bolete, Suillus bovinus, for instance, has been shown in the lab to reabsorb nutrients from its guttation droplets, while leaving behind less useful byproducts, such as oxalic acid. So perhaps guttation has evolved as an efficient method of expelling waste for some fungi. 

Is that what's going on with Inonotus glomeratus? Is that viscous, black ooze just a collection of rejected metabolic byproducts? If anyone would like to analyze it and has the means, I have some dehydrated exudate that I'd love to send you!  


slime mold Stemonitis flavogenita guttation drops
Even some slime moulds, like this immature Stemonitis 
flavogenita, produce guttation droplets. (Ulrike Kullik) 
pink polypore Fomitopsis rose
Pink-pored Fomitopsis rosea are even prettier when 
decorated with shimmering beads of moisture. I think the 
pattern on rim was made by the teeth of a grazing slug.

young Punctularia strigosozonata bleeding
Punctularia strigosozonata "bleeds" rust-tinted droplets.
Early nubbins of an unidentified polypore exude milky drops.
teardrop shaped indentations left by guttation on bracket fungus
This Fomitopsis pinicola produced guttation droplets for three
months this summer. When it finally stopped, trompe l'oeil
teardrop-shaped indentations were left behind.
Wet weather makes Xylaria hypoxylon produce beads of moisture.
Weeping Pleurotus dryinus
This large Pleurotus dryinus was weeping copiously
despite there having been no rain  for a week.
Many parasitic Hypomyces, such as this H. chrysospermus, are prolific weepers. 
Inonotus dryadeus is a lumpy polypore known for its ample
 production of amber guttation droplets. (Wikipedia)


Selected References:


Erast Parmasto, Andrus Voitk, (2010). Why Do Mushrooms Weep? Fungi, Vol. 3:4
N.B. In my original post, relying on the above article, I had repeated that Fomitopsis pinicola does not produce guttation drops in Newfoundland. Andrus Voitk has since kindly informed me that, in fact, they regularly do, as he notes in Omphalina Vol. III, No. 3. 

Hutwimmer, S., Wang, H., Strasser, H., Burgstaller, W. (2010) Formation of exudate droplets by Metarhizium anisopliae and the presence of destruxins. Mycologia, Vol. 102 no. 1, 1-10

Gerhard Saueracker. On the Exudates of Polypore Fungi. Fungimap Newsletter 48, Jan. 2013

Monday, 11 August 2014

Ascomycete Wannabes: Cyphelloid Fungi—Part II

The first cyphelloid fungus I found was Henningsomyces candidus. These are tiny, usually snow white, hairy tubules that cluster on the undersides of rotting logs. Though they occasionally reach an astonishing length of three millimetres, their diameter maxes out at only a sixth of that. Tiny, as I said. They can, however, grow in large enough communities that the white patches are easily seen. You just can't tell how startlingly odd they are until you look at them under magnification.
Henningsomyces candidus - Boleslaw Kuznik
Henningsomyces candidus (Boleslaw Kuznik, Mushroom Observer)

Nia vibrissa

In my first post about cyphelloids I promised a weirder link between not-very-similar-looking fungi. This is where we bring in Nia vibrissa, another minute guy. N. vibrissa has a couple of very interesting things going for it. First off, it's a marine fungus. Yes, that's right, it's an underwater saprophyte that can be found all over the world on different types of submerged wood, including mangroves and sunken ship timber. Secondly, it's not a cyphelloid fungus, it's a gasteroid: like puffballs, it produces its spores inside its fruiting body instead of on the surface. The third thing (if I have this right) is that there's phylogenetic evidence that shows a sister group relationship between the Henningsomyces candidus I found and Nia vibrissa. Which means that N. vibrissa is likely a reduced form of a reduced form (see Part I). 

What goes around, comes around: the earliest ancestors of our contemporary terrestrial fungi are thought to have evolved from simple, flagellated aquatic forms.
cyphelloid Henningsomyces candidus young
Some Henningsomyces candidus are barely tubular.

A Fistulina Connection

There is also evidence, though weakly supported, that the Nia/
Henningsomyces clade is sister to the non-cyphelloid Schizophyllum/
Fistulina clade.
Fistulina hepatica Beefsteak polypore growing on ground
Fistulina hepatica, the Beefsteak Polypore.
If you look closely at some of the hairy cyphelloids in the Nia clade, i.e. Henningsomyces and Merismodes species, and compare them to the spore-producing tubes of Fistulina hepatica, it's hard not to see a resemblance, a resemblance that was noted long before DNA analysis was possible. 

Fistulina hepatica cross-section and close-up of tubes
Cross-section and close-up of Fistulina hepatica tubes.
merismodes confusa growing on Diatrypella betulina
When tiny, hairy Merismodes cups are not fully open, there are similarities
to Fistulina hepatica's spore producing structures.

Merismodes

I found several Merismodes species last winter on dead branches fallen from trees (one of which I wrote about here)Merismodes spend a lot of their time looking like hairy little nubbins—until they're offered some moisture and open up into hairy little cups. They're not the only cyphelloids that go into dormancy in drought and revive when moisture returns.  


Calathella eruciformis

Wading through deep snow in March, I investigated some pale dots on a dead Populus branch, dots that turned into down-hanging goblets with pinched "stems" when I looked at them through my hand lens after waking them up in the house with a bit of warmth and moisture. Under the microscope, strands of their shaggy, bi-coloured hair were encrusted with minute, glimmering granules. Overnight, they conveniently produced some spores. It took awhile, and some dead ends, but eventually I found their name—Calathella eruciformis (thanks, Mycoquebec!). I'm not sure where this particular species fits into the cyphelloid phylogenetic tree since members of its genus appear to be all over the place (see phylogenetic diagrams in Bodensteiner paper cited below).
Calathella eruciformis on populus
Calathella eruciformis often grow on dead poplars in loose groups. 
Spores and encrusted hairs of Calathella eruciformis
Spores and encrusted hairs of Calathella eruciformis.

Stigmatolemma/Resupinatus

I collected another cyphelloid, a Stigmatolemma/Resupinatus speciesduring the Alderville Black Oak Savannah Bioblitz. Its cups were so incredibly tiny I wouldn't have noticed them if I hadn't already been magnifying some nearby, relatively gigantic, Orbilia on a rotting logMolecular evidence supports the suggestion that these cyphelloids are closely related to gilled members of the genus Resupinatus. The immature "cups" growing in-between more mature fruiting bodies of the gilled Resupinatus below certainly look a lot like the tiny characters I found.

cyphelloid basidiomycete Stigmatolemma Resupinatus cup fungus
The biggest of these Stigmatolemma/Resupinatus cups was .2 millimetres wide.

resupinatus stigmatolemma
Before their gills develop, immature Resupinatus sp.
look similar to Stigmatolemma cups.

Flagelloscypha minutissima

Conveniently, since I was already writing this post, I found yet another cyphelloid a few days ago. As usual, when I first looked at it, I was tricked once again into thinking that I'd found an ascomycete—a cluster of immature Lachnum virgineum to be specific, which I've come across several times this season. 

Like Lachnum virgineum, these were tiny, hairy white cups, but since they seemed a tad too small, and there was no sign of a stem on any of them, I stuck a couple under the microscope. Instead of the asci and ascospores I expected to see, there were basidia and basidiospores. There were also elaborately encrusted hairs with delicate, naked whips on the ends, characteristic of Flagelloscypha minutissima, a cyphelloid in the Nia clade.        
tiny basidiomycete cup Flagelloscypha minutissima
The cyphelloid basidiomycete, Flagelloscypha minutissima,
produces minute, stemless, hairy white cups.
Lachnum virgineum ascomycete white hairy cup
Lachnum virgineum, an ascomycete, looks similar to 
F. minutissima, but is considerably larger. 
Flagelloscypha minutisimma encrusted hairs whip tip spores basidia
The encrusted exterior hairs of Flagelloscypha minutisimma
have slender whip-like tips.

Cyphelloid Fungi: What to Look For 

  • Hair – a lot of cyphelloids have hairy, often shaggy exteriors
  • Size – most cyphelloid fungi are really tiny—less than half a millimetre
  • Orientation – cyphelloids are usually down-hanging so their spores, which are not ejected in the same way that ascospores are, can fall out of the cup, tube or goblet
  • Microscopy – among other anatomical differences, cyphelloid fungi have basidia instead of asci


References: 

Manfred Binder, et al. (2001) Phylogenetic relationships of the marine gasteromycete Nia vibrissa, Mycologia, 93 (4), pp. 679-688


Bodensteiner P. et al. (2004). Phylogenetic relationships of cyphelloid homobasidiomycetes. Molecular Phylogenetics and Evolution 33 (2): 501-15.

Moncalvo, J. M., et al. (2002). One hundred and seventeen clades of euagaricsMolecular Phylogenetics and Evolution 23: 357–400
J. Breitenbach, F. Kr√§nzlin, Fungi of Switzerland, Vol. 2: Non-gilled Fungi, Vertag Mykologia, 1986 (which conveniently showcases a crew of ascomycetes-like cyphelloid fungi in a group)

Cyphelloid fungi