Entomopathogenic Fungi'ed Fluffy Flies

Spring in Canberra this year has had an abundance of wet weather and variably cool mornings. Conditions which are ideal for a pathogenic fungus which infects a range of insects, but is particularly noticeable to us humans when it affects flies. Entomophthora is also sometimes known as the puppeteer fungus and causes infected flies to have distended abdomens, with spread legs, and outstretched, often forward-pointing, wings.

Entomophthora comes from the Greek roots entomo (entomo), meaning insect, and   jqora (phthora), meaning deterioration/damage/destruction/decay – so a very apt construction. It belongs to a group (Phylum) of fungi called Zygomycota, and is very far removed from the various fungi, such as mushrooms, bracket fungi, and even yeast, that we are more familiar with.

The reason for the name puppeteer fungus is the concept that some of these fungi effectively hijack the insect’s brain, turning them into ‘zombies’ with behaviours that enhance the further success of the fungal infection.

Entomophthora fungus is not uncommon, provided the right conditions prevail, but infected flies, apart from being small, tend to cling to the undersides of leaves or are otherwise unobvious and not noticed by the vast majority of people. I found a dozen or so infected and very dead flies early one dewy morning in mid-September when I was inspecting our nectarine tree to see how much fruit set there might be this year. Later, I found more on a range of other plants, including azaleas and on the undersides of the leaves of the olive tree. These provided opportunities for what I think are some beautiful, if rather gruesome, photos.

Several links to further information are provided at the end of this post.

https://en.wikipedia.org/wiki/Entomophthora_muscae

https://botit.botany.wisc.edu/toms_fungi/mar2000.html

https://biocontrol.entomology.cornell.edu/pathogens/entomophagamuscae.php

https://www.inverse.com/article/47656-mind-control-fungus-in-flies

Emu Dung Fungus

There is a genus of puffball fungus called Pisolithus which includes a number of closely related species. In Europe it is gastronomically known as the Bohemian truffle, and in the US it is prosaically called the dyemaker's puffball. But in call-it-like-it-is Australia it is known colloquially as the horse dung fungus – because that’s pretty much what it looks like. In the central Australian Pitjantjatjara language it’s apparently called ayinkura, but I don’t know if or what that might translate to.

This is a pile of horse dung. It is not a group of puffballs (stock photo)

Pisolithus is a type of puffball or earth ball fungus, from the family Sclerodermataceae. The name Pisolithus means “pea-stone” (pisum is Latin for pea, and lithos is Greek for stone). It is not a kind name to those afflicted with a lisp, and is rather difficult to say more than a few times in quick succession (though I can’t see any reason why you might want to do so!).

There are a number of species of Pisolithus around the world, and it appears there are several in Australia, with some only being recently discovered / described. And I’m not certain which species I’m dealing with in this post, but it may be Pisolithus arrhizus, or Pisolithus albus, or Pisolithus marmoratus, or Pisolithus tinctorius, or some similar species…

There is another type of fungus called ‘horse dung fungus’ but it is a very different type of fungus and it gets the name because it grows in horse dung rather than looking like horse dung. It is the common inky cap mushroom Coprinopsis cinerea, and it looks instead like a fairly typical small pixie-capped type of mushroom. But it has recently been in the limelight because it produces a novel antibiotic compound with much potential in the fight against the growing prevalence of antibiotic resistant bacteria as a result of the overuse of antibiotics (see for example http://www.natureworldnews.com/articles/10189/20141110/horse-dung-fungus-bizarre-help-vs-antibiotic-resistance.htm).

But I digress.

On a recent bird-banding trip to the Weddin Mountains in central NSW, we came across a dried out emu turd. It was fairly weathered, starting to crumble, and exposing a mass of barely digested seeds.

Old, dried and weathered emu dropping at Weddin Mountain National Park, NSW.

Other emu dung I have seen, in the wet mountain ranges near Canberra, have been wetter, greener and distinctly peaked from cloacal constrictive forces. 

Fresh, soft and moist emu droppings at Tidbinbilla Nature Reserve, ACT.

So there can be some variability in the appearance of emu dung, and I figure I can be excused for initially mistaking a large round Pisolithus for another emu dropping when I first rushed past it.

But it was sufficiently different for me to do a double-take and when I turned back for a closer look, realised it was a firm immature fungus with a rather spotted golden brown surface. 

Large, firm, immature Pisolithus puffball fungus at Weddin Mountain National Park, NSW.

I whipped out my baby Swiss army knife and sliced it cleanly in half (or nearly so) and was amazed by the incredible structure and pattern that was revealed.

The inside of an immature Pisolithus puffball presents an unexpected display of colour and pattern.

The pea-sized spore bundles or locuoles supposedly resemble peas!

The pattern results from the variable stages of development of the spore bundles, or locuoles - it is the appearance of these locuoles that prompted the name “pea-stone”.

It was pleasing to find that when we next returned to Weddin Mountains a month or so later, the half of the puffball that was still rooted (hyphaed?) to the ground had continued to grow and the cut surface had healed over – so it still had its chance to puff its spores into the wind when it ripened.

The scarred-over cut surface and continued growth of this Pisolithus puffball made me feel less guilty about having inflicted the damage on it in the first place.

And just to round out this post, below is a photo of another small clump of Pisolithus that I came across at the wetlands in West Wyalong, showing the more typical appearance that elicited the horse dung fungus appellation.

A small cluster of Pisolithus puffballs starting to resemble horse dung.

But to me, these things will now always be emu dung fungus.

Some references:

https://en.wikipedia.org/wiki/Pisolithus_arrhizus

https://en.wiktionary.org/wiki/ayinku%E1%B9%9Fa

http://blogs.scientificamerican.com/artful-amoeba/wonderful-things-the-hidden-beauty-of-the-horse-dung-fungus/

Canberra Autumn Mushroom Soup

It seems that for most people who live in Canberra, autumn is a favourite season. A time of cooler temperatures; a reprieve from the often unrelenting heat of a long dry summer, and a change to clear, crisp, sunny days. A time of softer light, and of course, the turning of the leaves from summer green through an almost surreal palette of vibrant yellows, reds, and oranges.

Autumn in Weston Park, Canberra, 18 April 2015.

Manchurian Pear leaves, 13 April 2015.

Japanese Maple leaf, 8 May 2015.

Fallen oak leaves, 18 April 2015.

But for me, while all of this is true, it is also underlain with the inevitability that the brief tapestry of brilliant autumn colours will all too soon be replaced with a drear treescape of gaunt grey and brown skeletons, and more depressingly, the foreboding knowledge of the imminent onset of Canberra’s cold winter months. I dread the slow dying of summer. And look keenly to the onset of spring’s re-birth as soon as the winter solstice passes - somewhat prematurely given the coldest months are still to come.

I just prefer heat to cold!

*  *  *

Another less obvious feature of a Canberra autumn is the sudden appearance of a variety of mushrooms, a flush of fungal exuberance in the wake of recent rains, in a landscape otherwise in seasonal decline. They might appear almost anywhere: in the parklands, woodlands and forests, in patches of lawn, along roadside verges, and almost anywhere garden mulch has been applied.

Tiny unidentified mushrooms pushing through eucalypt mulch in our front garden, 26 April 2015. 

While I’m interested in mushrooms, I really am not very good at identifying them. There are a small number of edible ones that I am sufficiently comfortable not only to identify but even to eat, however these tend to be non-native species that have been introduced, generally from Europe, and are well known both historically and gastronomically. These include the standard field mushroom Agaricus campestris (and a couple of close relatives), the shaggy cap Coprinus comatus, the saffron milk cap or red pine mushroom Lactarius deliciosus (the name says it all), and a small caramel-coloured mushroom that springs up in fairy rings in lawns, Marasmius oreades.

One of the first I noticed this year was definitely not one to eat though - a small cluster of classic ‘toadstools’, the red and white speckled fly agaric or Amanita muscaria.  These were in a small garden area beside the footpath along Marcus Clark Street, beside Ian Potter House (once Beauchamp House) in the middle of Canberra City. And, not surprisingly, they were in the mulch beneath an oak tree. While not as poisonous as the death cap Amanita phalloides, this mushroom contains several pharmacological and psychoactive compounds which are definitely not worth messing around with.

The fly agaric Amanita muscaria - the classic red & white 'toadstool' that occurs under oak trees. 17 April 2015.

The fly agaric has bright white gills underneath.

Despite being poisonous (to humans), this fly agaric is apparently being enjoyed by a slug.

During a walk through Weston Park, on the other side of the lake, I came across a few other types of mushroom. The first was possibly some type of agaric but I’m really not sure. Although I wouldn’t eat them, they were certainly of great appeal to a range of invertebrates, including several millipedes, and at least four different types of fly. In fact they were looking pretty fly-blown and ratty.

A quiet corner of Lake Burley Griffin in autumn from Weston Park, 18 April 2015.

Some type of agaric? Certainly enjoyed by many small critters, 18 April 2015.

Millipedes were seen on several of the mushrooms.

One type of fly, of which there were at least half a dozen individuals, would settle on the cap of the mushroom for a while, then fly a short distance away and trace out a rapid erratic triangular path on the flat exposed blade a fallen eucalypt leaf. Only the palest (brightest in the weak sunlight) leaves seemed to be selected. It was quite bizarre to see several of these flies, in reasonable proximity to the mushrooms and to each other, darting about on their chosen leaves like some sort of animated Spirograph doodle bugs (remember Spirograph?).

Unidentified fly, torn between mushroom and eucalypt leaf. 18 April 2015.

...and in blurry close-up.

There were also flies that looked like they were from the family Dolichopodidae, and possibly Sepsidae, as well as several Heleomyzid flies (I think) which were probably the most possessive of all about their mushrooms.

A Dolichopodid fly (?) on an agaric mushroom, 18 April 2015.

Possibly a Sepsid fly on an agaric, 18 April 2015.

A mushroom fly (Heleomyzidae) on an agaric. 18 April 2015.

These mushroom flies (Heleomyzidae) seemed quite possessive of their mushrooms. 18 April 2015.

They would battle it out if two of them happened to cross paths atop the mushroom cap. 18 April 2015.

Further along, I came across several clusters of a type of bright yellowish-brown mushroom that appeared only to grow on the cut stumps of pine trees (probably Pinus radiata, but there are several other Pinus species included in the plantings along the lake between Warrina Inlet and Nursery Bay). No idea what these are, but they’re cute.

Unidentified mushrooms on Pinus stump, 18 April 2015.

They always grew in tight clusters.

And had the typical gills possessed by most mushrooms.

Then, in some well kept lawns I came across a band of Boletus mushrooms, just one small arc at the circumference of a would-be fairy ring that must have had a diameter of about 30 metres or more. Fairy rings are produced as the underground mycelium (the fine thread-like hyphae) of the fungus grow and spread out radially from a central point, the fruiting bodies (the mushrooms) emerging around the circumference or part thereof, of the actively growing fungus while the inner parts progressively die off. The under-surface of the cap of Boletus mushrooms is characterised by having pores rather than the gills that most mushrooms have.

A species of Boletus, growing as part of a fairy ring in Weston Park, Canberra, 18 April 2015.

Boletus has pores rather than the more usual gills.

Pores of a Boletus mushroom in close-up, 18 April 2015.

A week or so later, while walking back to the car from work, I espied a clump of Agaricus mushrooms, possibly campestris, possibly something else closely related, from a footbridge over Parkes Way. I immediately back-tracked and picked them. They definitely weren’t Agaricus xanthodermis, the yellow stainer, which is similar-looking but slightly poisonous, so I felt comfortable eating them. That night, I prepared a simple mushroom soup using the remains of a roast chicken carcass for stock and adding the mushrooms, a few herbs from the garden, and a dash of cream. I get a real buzz out of making great food from simple wild produce.

Field mushrooms picked on the way home from work - the basis for a great mushroom soup - 30 April 2015.

Field mushrooms - chopped and ready for the pot.

Yum!

Another week later, in almost the exact same spot and under almost identical circumstances, I gathered a paper bag full of shaggy caps Coprinus comatus (also known as ink caps, shaggy mane or lawyer’s wig mushroom). These are undoubtedly my favourite wild mushroom, but you have to get onto processing them quickly because within a short time of picking, or if left in the field for that matter, they will essentially dissolve through a process called autolysis to a sticky black liquid mess.

Shaggy caps are absolutely delicious - they have an intense ‘mushroomy’ flavour and are perfect for adding to stews or (if not too advanced) simply sautéing briefly with butter and having as a side on toast with eggs and bacon for breakfast. I recall one time when we were on holiday, coming across some shaggy caps in Kingston SE in South Australia during an early morning walk. It took a little persuasion to get Karen to join me in having them for breakfast that morning, but she’s been a convert ever since. 

Shaggy caps, or lawyer's wigs, on the chopping block. 7 May 2015.

These shaggy caps are a little more advanced and on the verge of autolysing.

Shaggy caps sliced down the middle - the cap is only loosely attached to the top of the stalk.

On slicing the mushrooms I noticed what at first I thought were flecks of dirt - but they were moving! A closer look revealed that they were in fact tiny collembolans. Collembola is a class of arthropods, not quite insects but related to them, and referred to as entognathous hexapods (along with two other groups the Protura and Diplura). Even though they are extremely common in soil and vegetative matter, because they are so tiny (these were no more that a millimetre in length) this was the first time I'd ever knowingly noticed collembolans (though I had used similarly 'dirty' mushrooms in the past).

Tiny collembolans, only a mm or so in length, infested the inside of the hollow stalk of the shaggy caps.

But I wasn't about to let a little additional protein from the collembolans get in the way. On this occasion, with a bit of a mix of young and not so young specimens, I simply cooked them all up briefly in a frying pan with a little butter and a splash of water, then froze them in an ice cube tray, to be used as required through the encroaching cold dark Canberra winter evenings…



PS. If anyone knows the identity of any of the mushrooms or flies that I don't, or thinks I've misidentified others, please leave a comment. I hate the thought of wrong information being published and perpetuated on the web and will gladly correct any errors I may have made.