The Fifth Kingdom - Chapter 11
Hotlinks to: the dung succession - amphibious
fungi in streams
aero-aquatic fungi in ponds - pine needle succession
fire fungi - macrofungal ecology - fairy rings - the humungous fungus -
ATBI (All Taxa Biodiversity Inventory)
|Ecology is the study of organisms as they relate to each other and their environment. It must be apparent that even in the taxonomic chapters I gave a lot of ecological information. Think of the effects that fungi have had on people: the potato famine, the downy mildew of the French grape vines, the blue mould of Canadian tobacco, the way chestnut blight removed an important species from the forests of eastern North America, and the more recent loss of the beautiful American elm trees to Dutch elm disease. Fungi may alter the ecology of our gardens, as their depredations persuade some people to give up growing roses (because of the prevalence of black spot disease, powdery mildew and rust) or phlox (because of its susceptibility to powdery mildew). The early leaf drop inflicted on horse chestnut trees by Guignardia blight (at least in Eastern North America) may persuade us to plant other shade trees. But in this chapter I want to explore some other areas of fungal ecology: some of the ways in which fungi influence the course of events in a variety of natural, as opposed to Man-made habitats. I will explore their roles in four natural habitats I and my undergraduate or graduate students have personally examined in some detail, and then give a few more general comments.|
The first habitat is dung (which is also known by many other names). We may turn up our noses, but to some other organisms, dung is a considerable resource, which is constantly being produced in large quantities by billions of animals all over the world. You may think that because it has passed through an animal's digestive tract, every bit of nutritional value will have been extracted from it. This is a false impression. There may not be a lot of high quality protein left, but there is a great deal of microbial biomass, as well as many food components, for example, cellulose, that neither the animal nor its gut flora managed to digest. There are also excretory products which, though they are of no further value to the animal, are high in nitrogen: herbivore dung may contain 4% nitrogen -- more, in fact, than the plant material originally eaten by the animal. So, at frequent intervals throughout its life, every mammal evacuates from its gut a mass of first class fungal substrate, simply asking to be exploited.
Are there fungi which specialize in exploiting dung? And if there are, how do they gain access to this substrate when it becomes available? The answers may surprise you. About 175 genera of ascomycetes are largely or exclusively found on dung. The extremely advanced and successful agaric genus Coprinus has many species that occur exclusively on dung. There are also many specialized dung-inhabiting zygomycetes, among which Pilobolus and some of the elaborate anamorphs in the order Kickxellales are perhaps the most spectacular. So there is no doubt that a specialized mycota of dung-inhabiting (coprophilous) fungi exists.
But how do they compete successfully for this substrate? The answer here may be a little unexpected, but it is nevertheless perfectly logical. These fungi contrive to be first to exploit the dung by the simple expedient of being in it when it is deposited.
The only way to achieve that is to be eaten by the animal.
Coprophilous fungi manage this trick in several ingenious ways. These processes must
take into account some immutable logic. 1) The fungi are growing in the dung and will
therefore have to fruit on it. 2) Animals do not, in general, eat their own dung (though
rabbits do, raising interesting questions about the coprophilous fungi associated with
them). 3) Therefore, the spores must be somehow distanced from the dung in such a way as
to increase their likelihood of being eaten by herbivorous mammals.
|(photo above by W.R.West)||
|How the ascus tips of the apothecial ascomycete, Ascobolus, protrude from the hymenium and bend toward the light before shooting their spores.|
|How the necks of the perithecial ascomata of Podospora and Sordaria bend toward the light before their ascospores are expelled.|
|Each of these independently evolved phototropic
mechanisms is obviously designed to direct the spores away from any other adjacent dung,
and to increase the efficiency with which spores are deposited on nearby vegetation that
has a good chance of being eaten by the animal.
Many other dung-inhabiting fungi are less specialized than those I have just mentioned, or have specializations so subtle that we have not yet detected them. Nevertheless, the fact remains that with patient and repeated examination, we can find a large number of fungi representing most of the major fungal groups on the dung of many herbivorous mammals.
Repeated observations will show that the various fungi tend to sporulate in a reasonably definite sequence. First the Zygomycetes will appear...Pilobolus [above], and other saprobic genera such as Mucor, Phycomyces, Thamnidium, Helicostylum and others . Then the dichotomously branched sporangiophores of Piptocephalis [below] which is parasitic on some of the zygomycetes just mentioned...as are Chaetocladium and Syncephalis [below].
|the tall sporangiophores of Syncephalis [below] with their swollen apices and linear merosporangia...|
|the graceful multiple recurved sporangia of Circinella minor (the three pictures below show a developmental sequence...note the columellas in the third picture.|
|Rhopalomyces elegans [left], which parasitizes nematode eggs...|
|Cunninghamella with its apical vesicle and unispored sporangia...|
|Then the Ascomycetes..apothecial fungi like Ascobolus...zooming in from left to right...|
|Saccobolus...again zooming in from left to right|
|Thecotheus...here with 32-spored asci|
|and the perithecial Podospora and Sordaria,
accompanied by a variety of conidial anamorphs (Hyphomycetes) such as the blastic-sympodial Basifimbria...
|...the nematode-trapping Arthrobotrys with its clustered didymosporous (2-celled) conidia and its various ways of snaring nematodes, including the 3-dimensional net shown here [below, right]...|
|the synnematal, slimy-spored (arthropod-dispersed) Graphium, here shown in a zoom sequence of four pictures...|
|the synnematal, dry-spored Cephalotrichum (below)...|
|...and Trichurus, a synnematal hyphomycete with twisted, hair-like setae arising all over the fertile head, which give it a 'big hair' look (below)...|
|and finally the Basidiomycetes, mainly small (but profuse) species of Coprinus...|
|It has been suggested that this is a true ecological succession, albeit a miniature
and condensed one. Initially it was postulated that the sequence was a nutritional one.
Zygomycetes can generally assimilate only fairly accessible carbon sources, such as
sugars. Their fast growth was assumed to give them an advantage in finding these, and
their early disappearance was thought to be due to the exhaustion of this substrate. The
ascomycetes and conidial anamorphs that appeared next were assumed to be able to
assimilate more complex carbon sources such as hemicellulose and cellulose; while the
basidiomycetes, appearing last and persisting longest, were able to exploit both cellulose
But when this hypothesis was scrutinized more carefully and tested by
experiment and further observation, it did not hold up. The growth rates of the various
fungi were found to be relatively similar, and the various carbon sources were not
exhausted as quickly as had been assumed. So a second hypothesis was advanced. This one
was based on the time it took for each kind of fungus to accumulate enough food reserves
to permit it to fruit. It was argued that the simple sporangiophores of the zygomycetes
could be developed after only a short period, while the more elaborate fruit bodies of the
ascomycetes would require a longer build-up, and the even larger basidiomata of the
coprini would need the longest preparation of all. This is a more reasonable hypothesis,
because if we grow some of the dung fungi on laboratory media, we find that it takes Mucor
hiemalis 2-3 days to sporulate, while Sordaria fimicola needs 9-10 days, and
Coprinus heptemerus 7-13 days.
|Some of the Kickxellales, zygomycetes often found on the dung of sedentary mammals
(those with a defined home base, a small territory, and habitually used paths) produce
extremely complex and convoluted anamorphs.
Spirodactylon, possibly the most
complex of all, produces tall, branched sporangiophores that bear tiny coils within which
develop innumerable one-spored sporangia. The whole structure must be designed to catch on
the hairs of the rat or mouse as it passes by. This is made possible by the habits of the
animal which, although it doesn't eat its own dung, at least deposits it somewhere along
one of the trails it follows every day in its journeys to and from its den or burrow. The
final step, the ingestion of the spores, is presumably taken when the animal grooms
itself, as mammals (other than human children) habitually do. Some coprophilous
hyphomycetes (e.g. Graphium) produce slimy droplets of conidia at the top of tall
conidiophores or synnematal conidiomata. These spores are presumably dispersed by
arthropods which may themselves specialize in seeking out dung, and may thus act as
specific, and very efficient, vectors for the slimy-spored fungi.
|Many other dung-inhabiting fungi are less specialized than those I have just mentioned, or have specializations so subtle that we have not yet detected them. Nevertheless, the fact remains that with patient and repeated examination, we can find a large number of fungi representing most of the major fungal groups on the dung of many herbivorous mammals. Repeated observations will show that the various fungi tend to sporulate in a sequence. First, zygomycetes will appear; then ascomycetes and conidial fungi, and finally basidiomycetes.|
So we can assume that an assortment of spores of coprophilous fungi will be present in dung when it is deposited, and that these will all have been triggered to germinate by some aspect of passage through the mammalian gut. While Pilobolus is producing its miniature artillery extravaganza, the other fungi are growing and assimilating steadily within the dung, preparing for their own appearance at the surface. The new hypothesis had neglected only one important factor: antagonism. After a few weeks, almost the only fungi still sporulating on the dung will be species of Coprinus. These can go on producing a sequence of ephemeral basidiomata for months. We now know that the various components of the substrate are far from exhausted after the initial flushes of growth and sporulation. What has really happened is that Coprinus has seized control by suppressing most of the other fungi. Hyphae of Coprinus are actually extremely antagonistic to those of many other coprophilous fungi. If a Coprinus hypha touches one belonging to Ascobolus, the Ascobolus hypha collapses within minutes. We don't understand exactly how this trick is done, but it is extremely effective, and turns out to be a fairly common stratagem among the fungi, whose main competitors for many substrates are other fungi
Another interesting and important gambit used by Coprinus involves repeated anastomoses. Spores are more or less evenly dispersed throughout the dung when it is deposited, and they all germinate more or less simultaneously, producing small mycelia within the dung. When compatible mycelia meet, they will anastomose, and soon the entire dung deposit is permeated by what is now essentially a single mycelium, which can then pool its resources and produce more and larger basidiomata. Cooperation pays off for Coprinus.
There are also some interesting subplots that run concurrently with the main story. Several of the zygomycetes that usually appear (e.g. Piptocephalis) are actually parasitic on other zygomycetes. One common zygomycete, Rhopalomyces elegans, parasitizes nematode eggs. Nematode-trapping fungi such as Arthrobotrys often sporulate, and develop their characteristic rings and nets (see Chapter 15). Keratinolytic hyphomycetes such as Microsporum (below) may appear on hair that the animal has accidentally eaten during grooming.
|Occasionally, an undescribed species of fungus may be seen. For many years the third
year mycology class at Waterloo followed the dung succession as a laboratory exercise.
These undergraduates saw the zygomycete Stylopage anomala on horse dung several
years before it was formally described in 1983. They also found an undescribed species of Podospora
(Ascomycetes), which is perhaps the 102nd species of this genus. They also found the rare
zygomycete, Helicocephalum, which I had never seen before.
Horse dung is easy to obtain in most areas, comes in discrete units, and can be handled and observed without creating much personal distress. As many as 40 species of fungi representing most major groups of eumycotan fungi are commonly recorded from a single collection of horse dung. Most of them can be identified fairly easily with the help of the specialized taxonomic literature that is now readily available, though I admit that some of the zygomycetes are not easily recognized as such by beginners. Most of them could be identified to genus with the help of the illustrations on this CD-ROM. Many of the fungi can be isolated in pure culture without too much difficulty, and with a little imagination, interesting experiments can be devised to investigate various aspects of their behaviour. Perhaps now you can understand why I and many other teaching mycologists ask our classes to put their culturally determined attitudes on hold, adopt an objective scientific approach, and study the succession of fungi on horse dung, then think about the biological mechanisms and manoeuvring that lie behind the visible manifestations. It's a truly thought-provoking mycological experience.
Before we leave this topic I should warn you that you should not collect and examine the dung of carnivores, because it might support fungi that could also grow on you. However, in the interests of science, your humble scribe checked out the dog do-do shown below, which had taken on a transmogrified appearance in cool, humid weather. I found that the principal fungus fruiting here is a species of Mucor (Zygomycetes). I was probably quite safe, because the animal was eating kibble, not cats. But my advice is still the same: stick to herbivores...their droppings don't smell nearly so bad...
|If you want to know more about the coprophilous fungi, I recommend
that you read a recent paper: Richardson, M.J. (2001) Diversity and
occurrence of coprophilous fungi. Mycol. Res. 105:
I cannot close this section without mentioning a magnificent new book from an Italian physician, Dr. Francesco Doveri (see references). It has 1104 pages, 158 colour photographs and 300 other illustrations. It is undoubtedly the most extensive coverage yet afforded to coprophilous fungi, and took the author 15 years to bring this project to fruition. Definitely worth a look, if you can find a copy.
Now on to a very different habitat...
Amphibious Fungi in Streams
The second area of fungal ecology I want to examine is a stream flowing through a woodland, somewhere in the temperate zone. We already know that the tiny chytrids and oomycetes live here, but we might not expect to find many of the typically terrestrial dikaryan fungi. However, if you collect some stream foam and examine it under the microscope, you will see that the bubbles have trapped a rather unusual kind of spore (this is simply a physical phenomenon -- a surface tension effect -- and there is no other relationship between the bubbles and the spores).
|I collected foam in winter from this stream near where I live...|
|If you pass a litre of this stream water through a filter, then stain the filter in cotton blue and examine it through the microscope, you will see many large and strikingly shaped fungal spores. Many, perhaps most, will be tetraradiate.|
|These two sets of drawings are from a booklet published by Ingold (who discovered these strange fungi) in 1975.|
|You can see tha there is a wide
range of different morphologies, almost all of which share one feature -
they have arms or appendages sticking out in various directions.
We will see how these evolved...
|dark field picture of Lemonniera conidia|
|phase contrast photomicrograph of a
|Tetracladium marchalianum (interference contrast)|
|Culicidospora gravida (phase contrast)|
|Others will be unbranched, long, thin and arc-shaped, sinuate or sigmoid (s-shaped).|
|Anguillospora, a common sigmoid form (phase contrast)|
|They are all produced by conidial anamorphs that are specially adapted for living in streams.|
|There are even yeasts with a tetraradiate arrangement of their cells, presumably for the same reason this shape has been adopted by the other spores. This photomicrograph is of Candida aquatica.|
|Where do these spores come from, and how do the fungi that produce them make a
living? The first clue came when limnologists (biologists specializing in freshwater
systems) began to examine the energy budgets of streams. Because some streams flow through
forests, they are heavily shaded during the growing season. This means that few green
plants (primary producers) can grow in them. It was found that more than half, and
sometimes nearly all, of the energy supporting organisms that live in streams comes from
autumn-shed leaves. This source of energy is described as 'allochthonous' (which means
'coming from somewhere else' just in case you wanted to know).
When they first fall into the water, these leaves are extremely unpalatable to stream invertebrates, but as they are colonized and 'conditioned' by microorganisms, they apparently become tastier. Experiments in which batches of leaves were treated with either antifungal or antibacterial antibiotics showed that the fungi were chiefly instrumental in making leaves palatable to animals such as Gammarus pseudolimnaeus, a numerous amphipod crustacean living in the stream (another amphipod lives on the beach below my house in millions, eating decaying tidal jetsam, mostly seaweeds and, no doubt, the fungi growing on and in them).
|Gammarus, a detritivorous and mycophagous amphipod crustacean|
|In a feeding experiment, Gammarus (the dark, comma-like objects) choose to eat fungal mycelium (the greyish stuff at lower right) rather than unconditioned leaf discs (dark circles).|
|Later experiments with leaves conditioned by individual stream fungi showed that not
only were some of the fungi that produce tetraradiate or sigmoid conidia most active in
conditioning leaves, but their mycelia and sporulating structures were also highly
nutritious food for detritivorous stream animals such as Gammarus
(Amphipoda, Crustacea). An important
ecological role had been established for these fungi.
|But many questions remained. Were those fungi with tetraradiate spores related to one
another? Did they have teleomorphs? (which would help to answer the first question). Since
streams always flow the same way, and have a natural tendency to carry small things like
spores downstream, where did the inoculum for the upper reaches come from? What were the
advantages of the tetraradiate and sigmoid spore shapes? The information we needed was
gradually accumulated over several years of experiments, until eventually we were in a
position to give some answers.
Many of the tetraradiate (4-armed) spores, though similar in configuration at maturity, developed in rather different ways. I will describe just two of these. In some, three arms grew upward and outward from the top of the first-formed arm. In others, one arm grew upward, the other three or four outward and downward at the same time from a central cell. Some of these conidia were thallic, some blastic. A few had clamp connections, like Taeniospora gracilis, shown here, and were clearly basidiomycetous...
didn't. This impression of diversity was confirmed when some of the teleomorphs were
discovered. Some were unitunicate ascomycetes, both operculate and inoperculate, producing
apothecial and perithecial ascomata. Some were bitunicate ascomycetes. Some were
For some recent conclusions based on molecular research, click here.
It became clear that the morphologically similar anamorphs were
actually a mixed bunch: fungi of very different origins that had undergone convergent
evolution, molded by selection pressure into similar shapes. The teleomorphs also provided
one answer to the question of how these fungi got upstream: ascomata and basidiomata,
unlike the anamorphs, were not submerged in streams, and they liberated airborne
ascospores or basidiospores. The group has been christened the amphibious fungi,
because of its immersed anamorphs and emergent teleomorphs.
Much of the early work on stream fungi was done by Terence Ingold, who published many papers on the strange fungi to be found on leaves in water, starting as long ago as 1943.
|The reason for the sigmoid shape has not yet been fully
established, but Webster and Davey (1984) published a paper: 'Sigmoid
conidial shape in aquatic fungi' in Transactions of the British
Mycological Society 83: 43-52. They observed that most such conidia
tended to roll along in flowing water with their long axes at right angles
to the current, though some vaulted end over end when they touched a
surface. Both kinds of movement bring the ends of the spore into
contact with the substrate. If the flow slows down (and it is almost
zero at the boundary layer next to the substrate), this gives the end of
the conidium a chance to stick to the surface. After attachment, the
conidia swing around and lie with their long axis parallel to the current,
and rarely become detached again. They then produce sticky appressoria,
and germinate quite quickly, apparently stimulated by the
Sigmoid conidia may represent an evolutionary compromise. Although not as efficient at attachment as tetraradiate spores, they represent a more efficient allocation of resources. As usual in the living world, there is more than one answer to a particular problem
After colonizing the leaves, the amphibious fungi sporulate again, and it was found that they would do this only in highly oxygenated conditions, and with the physical stimulus provided by flowing water. It is clear that amphibious fungi incorporate many special adaptations, both morphological and physiological, to their environment.
|If the spore numbers are charted over the entire year, it will be seen that their numbers peak in Fall and Spring. In the first place, the massive new input of autumn-shed leaves provides the necessary substrate. In the second case, spring run-off will also carry plant debris into the stream. The entire process is diagrammatically summarized below, showing that the fungi are vital intermediaries of energy flow in streams, providing a link between dead leaves and trout.|
|Nikolcheva et al. (2005) have used molecular techniques to explore diversity of fungi in the early stages of colonization of leaves in streams (see references), and showed that after initially high diversity, numbers of taxa fell as terrestrial fungi were outcompeted by aquatic species, and aquatic species established their own pecking order.|
Aero-Aquatic Fungi in Ponds
One good aquatic habitat deserves another, so after sorting out the role of fungi in streams, we switched our attention to woodland ponds (our third habitat). The pond in question lay in the heart of the woods behind my house in Waterloo.
|Again, primary production within the pond was limited by the forest canopy. Again, there was a specialized group of fungi living in the pond, though no-one knew if these fungi played an important role in the ecology of the pond. In this case the fungal propagules commonly found were hollow, and floated. Again, this end was achieved in several different ways, of which I will describe only two. The pond has almost dried out in summer (1) A conidiophore emerges from a dead leaf just below the surface of the the water, and branches like a tree. Eventually, the ends of the fine branches all swell up and fuse with their neighbours to form an air-filled, watertight structure. This is the propagule of Beverwykella.|
|(2) Another conidiophore grows from a dead leaf, emerges through the water surface, and its tip begins to grow in circles. Coiling repeatedly on itself in wider and wider, then narrower and narrower gyres, it eventually builds a barrel-shaped, air-filled, watertight structure. This is the propagule of Helicoon.|
|Here is another apparently rare pond fungus, the tiny floating
gasteromycete, Limnoperdon. It has been recorded only from our pond in
Ontario and somewhere near Seattle, Washington, though it surely occurs at many places
between those widely separated localities -- people just haven't looked carefully.
fruit bodies (magnified X 10 in the top left picture, and X 50 in the top right picture)
are hollow, and are lined with non-shooting basidia (bottom right X
1500). Note the symmetrical mounting of the spores and the lack of a pointed
sterigma (see discussion in Chapter 5b).
Because these fungi live and grow under water, but produce their spores only above the surface, they are called the aero-aquatic fungi. It's obvious that the structures of the two kinds of conidia described above, though functionally equivalent, are not closely related. Again, convergent evolution has been at work, the selection pressure applied by some ecological imperative.
We finally discovered what this was. It was the need to be first on the scene when new substrate appears. When a dead leaf falls into a pond, it does not sink immediately.
|It may actually fall on top of some of the floating propagules just illustrated, or the propagules may be drawn to the floating leaves by surface tension. In either case, these fungi will be the first pond-adapted species to enter this new substrate. The leaves soon sink to the bottom of the pond, carrying their new colonizers - hyphomycete or gasteromycete - with them|
|These fungi also have the ability to grow at low oxygen levels, and to survive the virtually anaerobic conditions that prevail at the bottom of a pond for extended periods during the winter.|
|Sporulation will happen again when the pond begins to dry out during the following summer, and the water level subsides until the colonized leaves are once more just below the surface. We found that these aero-aquatic hyphomycetes play an ecological role parallel to that of the amphibious fungi in streams: conditioning the dead leaves, and making them palatable to the detritus-eating invertebrates such as snails, and vertebrates such as frogs, whose larval stages live in the pond.|
|Frog spawn [left]|
|produces tadpoles which skeletonize leaves after the fungi have 'conditioned' them...|
|...and eventually metamorphose into tree frogs [left] which represent the apex of the pyramid of life in the pond.|
|There are quite a few marine fungi, including many ascomycetes, some hyphomycetes and a small number of basidiomycetes, but all the evidence, both morphological and molecular, points to terrestrial origins for these fungi.|
The biosphere has myriads of other habitats, each unique in various ways, and each making special demands of the organisms that live in it. The roots of plants create special conditions around themselves, and have established especially intimate relations with hundreds of endotrophic and thousands of ectotrophic mycorrhizal fungi (which have Chapter 17 to themselves). Other rather less specialized saprobic and parasitic fungi also abound on and near roots. The surface of living leaves is inhabited by a specialized mycota, while dead and decaying leaves are substrates for a succession of other species. The soil, into which most leaf remains are incorporated, is itself a mass of microhabitats, and is the richest reservoir of fungal diversity. And of course the leaves of different plants, and the various soil types, will have different subsets of the total mycota. Juliet Frankland, in her Presidential address to the British Mycological Society (reference below), gives a nice overview of the problems and progress in our study of fungal succession, exemplifying them with an autecological study of the agaric, Mycena galopus.
Not all fungi can be parceled out neatly into successive steps of a succession. Often, fungi compete for access to a substrate. Sometimes a natural phenomenon will give us an unexpected insight into this struggle. Here is a picture of a block of wood which has been colonized by many different mycelia. The boundaries between the 'territories' of different mycelia can be clearly seen as black lines or zones, and the wood is described as 'spalted.' The black material is melanin-like, oxidized and polymerized phenolics deposited by wood-rotting fungi, and although the biological function of the zones isn't entirely clear, melanins are the precursors of the humic acids, which are long-lived and important determinants of soil fertility.
|This kind of partition can even occur in much smaller substrates, such as individual leaves, as in this one of Oregon grape (Mahonia) from John Dean Provincial Park near where I live. The colonies and black fruit bodies shown are of Coccomyces (Rhytismataceae, Ascomycetes). The lower pictures are close-ups, which show the unusual polygonal outline and stellate opening of the ascomata. Note that while the colonies in the second picture have produced only one ascoma each, that in the third picture has a larger territory, and has been able to develop multiple ascomata, now open to expose the hymenium.|
|Another fungus exploiting leaves of
Mahonia is Cumminsiella (Pucciniaceae, Teliomycetes).
This fungus attacks living leaves, and thus preempts the saprobic Coccomyces.
|This time a single infection
occupies a whole leaf. The uredinial sori open on the lower surface of the
There's more information on this fungus, including a photomicrograph of urediniospores and a teliospore, in Chapter 5d.
|This senescent salal (Gaultheria shallom) leaf has also become divided up, but in this case two or three different fungi are involved.|
|Even if a leaf isn't subdivided into territories, after it dies you are
likely to see fungal colonies develop, as is happening in the Hosta
leaf (above, left) from our garden. The fungi in this case are mainly Cladosporium
and Epicoccum, two common saprobic hyphomycetes. The picture
on the right shows a part of another Hosta leaf, clearly
demonstrating that the areas covered by the fungal colonies, marked X, are
the first to be eaten by animals. We may compare the fungi to peanut
butter, and the leaf to the bread which it renders palatable.
Which brings me to the subject of my own PhD thesis -- the succession of fungi involved in the long, slow decomposition of another kind of leaves -- Scots pine needles (our fourth habitat).
I was presented with a problem which, briefly stated, was as follows. "When we isolate fungi from the soil, the majority of cultures will be of light-coloured fungi, while a majority of the hyphae seen in the soil are darkly pigmented. Figure out what's going on."
I chose to work in a pure stand of Scots pine (Pinus sylvestris)
|I looked at the various soil horizons in the forest, and tried innumerable times to grow the dark hyphae, picking them out with a micromanipulator and giving them a variety of delicious media. But they refised to grow, so I eventually decided that most of them must be dead, and that they had perhaps grown at some other time and in some other place. I looked in the organic horizon above the mineral soil, and found there a thriving community of litter decomposing fungi, which I proceeded to investigate (I did not realize it at the timer, but this is fairly typical of PhD projects, which are often changed in mid-course by some unforeseen event(s).|
|I embedded a small chunk of the Scots pine forest floor in cold-setting resin, then cut it into vertical slices, one of which I drew for this illustration, which shows the spatial distribution of needles, and their gradual transition from L > F1 > F2 > H layers. I then decided to examine as many needles from each layer and sub-layer as I could process each month (the number turned out to be 300 needles).|
|The left-hand vial contains living needles from the tree, which represented stage one in fungal colonization. Vial 2 = L layer (pale brown), vial 3 = upper F1(much darker, but still tough), vial 4 = lower F1 (blackish and softer), vial 5 = F2 (greyish and fragmenting). By the time litter material entered the H layer, it was no longer recognizable as individual needles.|
|Needles were treated in various ways. (1) Some were washed repeatedly to remove loose surface spores and plated out in segments to isolate fungi on and in the needles. (2) Some were surface sterilized before plating out, to select for internal colonizers. (3) Some were wax embedded and sectioned. (4) Some were observed directly over a period of incubation in damp chambers.|
|This is a reference point -- a transverse section of a healthy, living needle. Changes can be measured against this.|
|And here is one of the first dramatic changes, the development of numerous ascomata of Lophodermium pinastri, which apparently often colonizes the interior of living needles without producing overt symptoms. The death and fall of the needle stimulates the fungus to fruit.|
|The large number of lenticular black ascomata of Lophodermium that can occur in a single needle indicates a dominant colonizer. Here two ascomata are seen in section.|
|Other fungi fruit in other needles -- note the several paths along which individual needles may travel. In this picture, the fruit bodies are pycnidial conidiomata of a coelomycetous anamorph, Fusicoccum (holomorph probably Botryosphaeria). The interior of the needle can be seen to be breaking down under the attacks of the fungus.|
|Meanwhile, on the surface of the needle, networks of dark hyphae (remember them?) develop. But what fungi do they represent? Mycelium without sporulating structures is not very helpful unless one has access to molecular techniques.|
|Fortunately, several of these fungi fruited either in nature or in the damp chambers. The first of these is Slimacomyces monospora (which I mistakenly described as a species of Helicoma in 1958!)|
|A second major surface colonizer is Sympodiella acicola which I described as the type species of a new genus (It still stands). Again, note that the conidiophores are in an almost pure stand.|
|Here is a drawing of Sympodiella acicola, showing that its unique characteristics are that while its conidiophore extends sympodially, the conidia are thallic-arthric (for those of you who are fans of conidium development -- otherwise look back to Chapter 4).|
|Another fungus that is obviously at least partly internal develops sclerotia and conidiophores. This was Thysanophora penicillioides...|
|And here is part of a Thysanophora conidiophore with a penicillus (the brush-like conidiogenous apparatus - the numerous cells at the top are phialides, which can each produce many conidia in a dry chain).|
|Another pure stand of external conidiophores of an internal fungus, Verticicladium trifidum (an anamorph connected to an apothecial fungus, Desmazierella acicola, which I never saw). The conidiogenous cells of this fungus extend sympodially during conidiogenesis.|
|Finally, we have arrived at the partitioning of needles among fungi. It is particularly obvious here, where a darkly pigmented fungus squares off against an apparently unpigmented fungus.|
|Section of a partitioned needle, showing the melanin barrier between species. The fungus at upper left is Verticicladium; its neighbour is not fruiting so cannot be identified. Compare this partition with the black lines shown earlier in wood and leaf.|
|Now a new participant bursts onto the scene (well, it's aleady left, but it has left its trademark - frass). Now the needles have been softened up by the fungi, arthropods can eat the needle material. The frass identifies the intruder as an oribatid mite.|
|And here it is, a miniature armoured tank that eats fungi and needle.|
|Now in the lower F1, the interior of the needle has collapsed or been eaten, and the upper surface is coated with a deposit of frass, which contains many fragments of fungal hyphae and spores.|
|This diagram plots the overall picture, following the needles through 9 years of mainly fungal decay. The width of each bar represents the relative importance of the fungus at each stage. Darker bands show fruiting periods. At far left the fungi are those that grow on or in living needles. As we move to the right, the fungi involved in later stages of decay are traced.|
|Read this table carefully -- it will amaze you, and it shows just how important fungi are in the forest ecosystem. Not merely important, but producing greater biomass than any group other than the plants.|
A recent paper by Paulus et al. (2003 - see references) gives further insight into what is going on in decaying plant litter. Using a particle filtration technique, these authors isolated no fewer than 1365 isolates, representing 112-141 morphotaxa, from 8 leaves of Neolitsea delabata in the tropical forests of Queensland.
Forest fires, slash burns, camp fires and even volcanic eruptions will all trigger the fruiting of a rather specialized group of macrofungi. We are all becoming familiar with the massive fruitings of morels, particularly the black morels, Morchella elata and allies, which appear in the spring on areas burned the previous year. Foresters may be familiar with the ascomycete, Rhizina undulata, which resembles, quite literally, a pile of dung, because this species attacks conifer seedlings on burn sites. Less familiar are the many other species in the genera Pholiota, Myxomphalia, Omphalina, Tephrocybe, Psathyrella, Coprinus, and the cup fungi Pyronema, Lamprospora, Octospora, and Peziza that appear in similar situations. While some of the cup fungi and Pholiotas are brightly coloured and conspicuous, others are black, dark grey or brown, and therefore are hard to see among charred wood and soil. If you want to find these fungi, squat down and slowly scan small areas, particularly those showing some regeneration of mosses. Many of the ‘fire fungi’ are in fact bryophilous species associated with the mosses and liverworts that also characterize old burns. Fire fungi may be induced almost anywhere, by controlled burning (and a little patience), or in the laboratory by various heat shock treatments of soil samples.
Many of the food webs illustrated in ecology textbooks miss out more than half of the organisms involved in the transfer of energy and nutrients. They often stress macroscopic organisms, while omitting microscopic organisms such as the saprobic and mycorrhizal fungi. This neglect is unfortunate, especially since we now appreciate that microorganisms, being at the base of food webs, provide nutrients and mutualistic symbionts for almost all plants and animals. The basic links in terrestrial food webs lie in the soil which is, of course, where a huge number of fungi still live. Every attempt to understand trophic systems must start and finish with soil organisms. And surely the fungi are among the most important of those.
Most of the situations I have described in this chapter are small or localized. If we consider the macroscopic fungi, and their roles in such extensive ecosystems as forests, we find that the state of fungal ecology is relatively primitive, meaning that we simply don't know very much about how those fungi act and interact under natural conditions. If you doubt this, you could explore the mycological literature for information on where to find morels (in my opinion, the best of all edible fungi). You will be led a merry dance, from old apple orchards and dead elms to recently burned forests. Until relatively recently, no-one even seemed to know whether morels were mycorrhizal or not (my understanding is that they are opportunistic saprobes, exploiting new substrates then fading away, only to appear somewhere else when new food sources present themselves).
As for the ubiquitous agarics, which are undoubtedly the most widely collected and studied of all fungi, I have to report that things aren't much better. Only Europe holds out a candle in the darkness. Since europeans have been collecting and recording macrofungi for centuries, they have the kind of database that allows the present generation of mycologists to draw comparisons with the past. This is why several European countries have 'Red Lists' compilations of macrofungi which seem to have undergone serious declines in recent years -- or even to have disappeared altogether. It is impossible to produce such red lists for anywhere in North America because records do not go back far enough and are, in any case, still fragmentary. Although we may suspect that certain species are declining or disappearing, we have no well-documented historical reason for saying so. You can find out more about red lists by going to a good search engine such as 'google' ( www.google.com ) or 'Yahoo' or 'alltheweb' and entering 'red list endangered fungi'.
We understand that about half of the known agarics are mycorrhizal -- they have an intimate, mutually beneficial relationship with many of our forest trees, and ecological research has recently begun to focus on the effects on such fungi of various forest practices, and especially the clear-cutting of old-growth forests which still (regrettably) goes on in many jurisdictions, and most blatantly in British Columbia where I live. One of my own graduate students has recently established that many of the fungi associated with old growth forests do not re-colonize clear-cut habitats for 40-50 years. And his suspicion is that the recolonization happens by means of airborne basidiospores which originate in nearby old growth. What if there is no longer any nearby old growth to provide this inoculum? But International logging companies carry on in blissful ignorance of any such concerns.
Just when we think we have established a few principles based on the occurrence of fruiting bodies of the mycorrhizal fungi, it is demonstrated by molecular techniques that in many cases the fungi producing the fungal sheaths around the roots of the trees are not those whose basidiomata are appearing above ground. Are we back to square one? No one seems sure at present. But I mention this to demonstrate how little we actually know about macrofungal ecology. Some recent studies (2005) claim that the apparent disconnect is at least partly because many of the mycorrhizal fungi develop small, inconspicuous, cryptic or seasonally limited fruit bodies, rather than the large and conspicuous ones detected by most collectors.
fascinating study by Tofts and Orton (1998) points out that although they
have been collecting agarics regularly in a particular woodland in
Scotland for 21 years, and have recorded 502 species in that time, each
year they still find species they have never seen before. Over twenty
years of collecting, and they still cannot say that they have a proper handle on agaric biodiversity in that woodland. They suggest that
least 25 to 30 years of collecting, and possibly more, will be necessary
before that goal can be attained.
A group of west-coast mycologists (including Paul Kroeger, Christine Roberts, Oluna and Adolf Ceska, and me), supported by the Mellon Foundation, has been doing a macrofungal inventory of Clayoquot Sound on the west coast of Vancouver Island. Over 5 years, visiting once in spring and twice in fall, we have collected 660 species. Two of the most interesting features of our study have been: (1) that only 38 species were found every year and 407 were found only once, and (2) that a large number of fungi new to the study cropped up each year. After year one, we have found about 100 additional species each year.
In Fall 2004 the Cascade Mycological Society held its 16th successive mushroom fair at the Mount Pisgah Arboretum just outside Eugene, Oregon. As a guest speaker for the Society I was fortunate enough to be invited to participate in the collecting trips leading up to the fair. The fair is an exciting introduction to the larger fungi because over 300 species are usually on display - speaking to a huge effort on the part of the members. I was also fortunate enough to get my hands on the statistics for all sixteen years. Over those years just over 700 species have been recorded from the area. When we arranged the data according to the number of years in which each species had been collected, an interesting picture emerged.
To begin with the extremes. I was rather surprised to discover that only 37 species (just over 5% of the total number) had been found in all sixteen years. It was equally thought-provoking to learn that no fewer than 190 species (almost a third of the total) had been recorded only once in those 16 years. Here is the list of species versus years.
of years recorded
There are possible flaws in the data set. For example, species may have been misidentified. But the general trend is obvious. A relatively small number of taxa will show up every year, or almost every year, while a much larger number of taxa will be found much less often, and a very large number will be encountered only once every decade or so.
How many more taxa will show up in the years to come? What is the full number of species that the Cascade group can expect to find if they keep at it long enough? If we may be allowed to take a quick look in the crystal ball, might we not find that after 50 years they will have found 1,000 species?
This data set (for which I am indebted to the hardworking collectors and record-keepers of the Cascade Mycological Society) points up the necessity for very long-term studies wherever the diversity of fungi is to be fully explored, and calls for the accumulation of much concurrent data on weather conditions and other ecological factors if we are to understand why some fungi are so notably shy.
These reports are not intended to put you off, to deter you from getting involved in fungal ecology. Rather the reverse. It is clear that the need for research in this area is critical. We need good ecological studies just as much as we need molecular research on fungi. Some groundwork has been done in Britain, where the macrofungal assemblages characteristic of many habitats have been broadly outlined. But this is still far from an understanding of the full role played by those fungi in the habitats being considered. The need for seminal research has never been greater. The next section discusses some of that.
Fairy rings are one of the few fungal phenomena that most people have seen. To the superstitious mind the arrangement of the fruit bodies in a circle might seem very strange. On top of that, the grass often doesn’t grow just inside the fruiting zone, so it looks really weird, and it isn’t too surprising that in the past, people ascribed such rings to supernatural events (fairies or witches dancing).
The real explanation is simple enough, once you know that mushrooms start life as microscopic spores that germinate, develop branching hyphae, and soon grow outward from their point of origin as a mycelium that tends to spread equally in all directions (see Chapter 3a), and thus forms a colony that describes an ever-widening circle in the soil. When the mycelium has accumulated enough food, and conditions are right, mushrooms develop at the periphery of the circle, finally bringing the previously invisible colony to our attention.
Fairy rings become larger every year, as the mycelium grows outward, always looking for food. It can’t turn back because it has used up the food resources behind it. Growth of the grass is inhibited because the dense fungal mycelium prevents water from penetrating the soil, and possibly because the fungus has released metabolites inimical to the plants. The grass inside the rings sometimes grows more lush, because the fungus has liberated nitrogen by its activities. Some rings, on places such as Salisbury Plain in England, that have been under grass for many centuries, are estimated to be at least 400 years old. It is quite possible that much larger and therefore even older ones could be found. You might keep your eyes open.
Many species of agarics (perhaps as many as 60) produce fairy rings. The most obvious are those which occur in pasture, and are often generated by species of Agaricus (see Chapter 5b), or by Marasmius oreades, which is actually called the 'fairy ring mushroom' (see photograph below). Sometimes another kind of fairy ring develops around trees, as mycorrhizal fungi grow outward from the roots.
Some years ago, mycologists were working on a forest in Michigan where three species of Armillaria, well known pathogens, had been causing trouble. They found that one of these species, Armillaria gallica, seemed to be monopolizing a large area of the forest - 15 hectares. When molecular biologists checked samples from within this area, they found that all belonged to a single genet (a product of sexual reproduction). So here was a single species of mushroom that had spread through the soil and covered an amazing 15 hectares (35 acres). How was this achieved?
Armillaria gallica apparently had a secret weapon. It soon became apparent that this was its rhizomorphs, well-organized hyphal strands with conducting hyphae in the centre, and a dark protective rind on the outside, which help this fungus spread through the soil protected from the hostile influences so common in this medium. Armillaria gallica sends out rhizomorphs through the soil in search of new food substrates. It isn't a particularly pathogenic species, so its rhizomorphs wait patiently until a tree is weakened or dead before invading. Having established its new base, it sends out more rhizomorphs...
Sampling established that there were about 10 tonnes of rhizomorphs in the genet. If the fine assimilative hyphae and other structures were factored in, the total mass of the colony/genet added up to 100 tonnes - about the size of a blue whale. It was also calculated that the colony was at least 1500 years old.
No sooner had the credentials of this fungus been established than a larger genet was discovered in Washington State. This one belonged to Armillaria ostoyae, the common west coast species of Armillaria, and it covered an almost incredible 600 hectares (1500 acres). Even more recently, an even larger genet of Armillaria ostoyae has been identified in the Blue Mountains of north-eastern Oregon: this one covers 2200 acres (about 900 hectares) and is estimated to be between 2,400 and 8,500 years old. This is among the largest and most extensive organisms on earth. Who said fungi were insignificant?
article by Tom Volk, which can also be found at: http://botit.botany.wisc.edu/toms_fungi/apr2002.html
Of course, you can't do fungal ecology unless you know what fungi are present. There is almost certainly no habitat in the world whose fungi have been fully enumerated. A group of 22 mycologists gathered in Costa Rica in 1995 and came up with a strategy for isolating and identifying all of the fungi (an estimated 50,000) in a particular habitat (the Guanacaste Conservation Area) -- an All-Taxa Biodiversity Inventory for fungi (Rossman et al. [eds.] 1998 -- see reference below)This ambitious plan called for a staff of 100, $1 million worth of agar media, 1.8 million slants to isolate the endophytic fungi alone... Unfortunately all this would have cost about US$25 million, so it hasn't been done. But the need remains, and the general lack of knowledge about fungi means that they are not usually considered when conservation issues are raised. Perhaps you can help to change that.
A less ambitious ATBI is now under
way in Great Smoky Mountains National Park, but it is a long-term
endeavour -- visit the web site at http://www.discoverlife.org/
A well-known and
scientifically ambitious couple, Oluna and Adolf Ceska, living in
Victoria, BC, began in 2004 to compile an inventory of the fungi of
Observatory Hill, a largely forested area, 71.4 ha in area and 224m
high, just north of Victoria. After several years, and by dint of making
almost 200 trips to the hill, they have as of late 2012 collected more
than 1,100 species, and the study continues... They have found a number of
extremely rare species, and some undescribed taxa. Theirs is now
probably the most intensive and species-rich study for such a small area
in the history of mycology. An account of the study can be accessed at:
During the same years the Ceskas also participated in a multi-year study of Clayoquot Sound, including Pacific Rim National Park, other team members being Christine Roberts, Paul Kroeger and Bryce Kendrick (Roberts et al. 2004). They found 551 species, only 28 being collected in all years, and 308 species being found in only one year.
A similar study in the Haida Gwaii archipelago, with the same 5 mycologists, visiting the islands 2 or 3 times per year, found over 600 taxa, and led to the publication of a book 'The Outer Spores - Mushrooms of Haida Gwaii' (Kroeger et al. 2012).
Now we can approach this problem in a completely new way, as this article in PNAS describes:
traveled to 26 pine forests across North America and collected
10-cm-deep soil cores, more than 600 in all. Within hours of collection,
and with the assistance of local scientists and universities, they
preserved the samples to extract and isolate the fungal DNA. The
researchers then used modern genomic tools to sequence unique stretches
of the environmental DNA that can be used as barcodes to identify all of
the fungal species present in each sample.
sequencing revealed more than
10,000 species of fungi, which the
researchers then analyzed to determine biodiversity, distribution, and
function by geographical location and soil depth. Interestingly, author Peay said, there was very little overlap in the fungal species from
region to region; East Coast fungi didn't show up on the West Coast or
Midwest, and vice versa.
often assume that similar habitats in, say, North Carolina and
California would have similar fungi, but this is the opposite of what we
find," an author said. "What’s more interesting, despite the
fact that soil fungal communities in Florida and Alaska might have no
fungi in common, you find that many of the processes and the functional
rates are convergent. The same jobs exist, just different species are
team found this to be particularly true when comparing the functionality
of fungi at different strata of the core samples. Even though the
samples were collected thousands of miles apart, fungi near the top all
performed the same task; similarly, bottom fungi performed very similar
functions across the continent.
We need many more similar studies to establish baseline data for North American fungi, such as have existed for many years in Europe, which may give us warnings about decline and loss of species resulting from anthropogenic influences (habitat loss, climate change).
And having outlined that encouraging state of affairs, we must turn the page to another,
completely different aspect of mycology which came
to prominence in the middle of the 19th century, and has remained front
and centre ever since...
© Mycologue publications 2015
Baerlocher F (1992) (ed) The Ecology of Aquatic Hyphomycetes. Ecological Studies 94. Springer Verlag.
Baerlocher F, Kendrick B (1974) Dynamics of the fungal population on leaves in a stream. J. Ecology 62: 761-791.
Baerlocher F, Kendrick B (1981) The role of aquatic hyphomycetes in the trophic structure of streams. pp. 743-760 (in) The Fungal Community: its Organization and Role in the Ecosystem. (eds.) E.T. Wicklow ET, Carroll GC. Marcel Dekker, New York.
Bell A (1983) Dung Fungi: an illustrated guide to coprophilous fungi in New Zealand. Victoria University Press, Wellington.
Cannon PF (1995) An ATBI - How to find one and what to do with it. Inoculum 46: 1-4
Deighton J (2003) Fungi in Ecosystem Processes. Mycology Series No. 17. 424pp Marcel Dekker.
Doveri F (2004) Fungi Fimicoli Italici: A guide to the recognition of basidiomycetes and ascomycetes living on faecal material. 1104 pp. Assoc. Micol. Besadola
Frankland JC (1998) Fungal succession - unravelling the unpredictable. Mycol. Res. 102: 1-15
Hudson HJ (1980) Fungal Saprophytism. 2nd Edn. Arnold, London.
Ingold CT (1966) The tetraradiate aquatic fungal spore. Mycologia 58: 43-56.
Ingold CT (1975) Guide to Aquatic Hyphomycetes. Freshwater Biological Assoc. Publ. # 30. 96 pp. Ambleside.
Kendrick B (1958) Microfungi in pine litter. Nature
Kroeger P, Kendrick B, Ceska O, Roberts C (2012) The Outer Spores: Mushrooms of Haida Gwaii. Mycologue Publications, Sidney, BC. and Haida Gwaii Museum, Skidegate. http://www.mycolog.com/mycologueproducts.html
Michaelides J, Kendrick B (1982) The bubble-trap propagules of Beverwykella, Helicoon and other aero-aquatic fungi. Mycotaxon 14: 247-260.
Nikolcheva LG, Bourque T, Baerlocher F (2005) Fungal diversity during initial stages of leaf decomposition in a stream. Mycol. Res. 109: 246-253.
Paulus B, Gadek P, Hyde KD (2003) Estimation of fungal biodiversity in tropical rainforest leaf litter using particle filtration: the effects of leaf storage and surface treatment. Mycol. Res. 107: 748-756.
Peabody RB, Peabody DC, Sicard KM (2000) A genetic mosaic in the fruiting stage of Armillaria gallica. Fungal Genetics and Biology 29: 72-80.
Peabody RB, Peabody DC, Tyrrell MG, Edenburn-MacQueen E, Howdy RP, Semelrath KM (2005) Haploid vegetative mycelia of Armillaria gallica show among-cell-line variation for growth and phenotypic plasticity. Mycologia 97: 777-787.
Price PW (1988) An overview of organismal interactions in ecosystems in evolutionary and ecological time. Agriculture, Ecosystems and Environment 24: 369-377.
Richardson MJ, Watling R (1982) Keys to fungi on dung (Revised Edition). British Mycological Society, Cambridge.
Richardson MJ (2001) Diversity and occurrence of coprophilous fungi. Mycol. Res. 105: 387-402.
Roberts C, Ceska O, Kroeger P, Kendrick B (2004) Macrofungi from six habitats over five years in Clayoquot Sound, Vancouver Island. Can. J. Bot. 82: 1518-1538.
Rossman AY, Tulloss RE, O'Dell TE, Thorn RG, (eds) (1998). Protocols for an All Taxa Biodiversity Inventory in a Costa Rican Conservation Area. Parkway Publishers, Boone, North Carolina, U.S.A.
Seifert, K, Kendrick B, Murase G (1983) A Key to Hyphomycetes on Dung. University of Waterloo Biology Series, 27. Department of Biology, University of Waterloo, Waterloo.
Straatsma G, Ayer F, Egli
S (2001) Species richness, abundance and
phenology of fungal fruit bodies over 21 years in a Swiss forest plot.
Mycol. Res. 101: 515-523.
Tofts RJ, Orton PD (1998) The species accumulation curve for agarics and boleti from a Caledonian pinewood. Mycologist 12: 98-102.
Webster J (1970) Coprophilous fungi. Transactions of the British Mycological Society 54: 161-180.
Webster J, Descals E (1981) Morphology, distribution, and ecology of conidial fungi in freshwater habitats. pp. 295-355 (in) Biology of Conidial Fungi. Vol. 1 (eds.) Cole GT, Kendrick B. Academic Press, New York.