Fungal connections (3.1)

articles

At the present time I'm not sure whether I'll ever get round to producing a collections album for fungi in the same way as the comprehensive section I managed to put together on lichens, whereas in this series of articles I'm able to narrow the coverage as I'm only focusing on fungal relationships in connection with woodland habitats.

In these situations fungi can be described and grouped by their ecological role and how they obtain nutrients. The following articles, which are now spread across three pages, provide a reasonably detailed overview of the two primary groups; the mycorrhizal fungi as covered here, and then saprotrophic fungi on the following page. By comparison the final page is a bit of a mixed bag where I take a brief look at some of the other groups like parasitic and lichenised fungi, as well as a few of the more unusual species such as pin-moulds and any other topics of interest. However, before looking at individual species it makes sense to begin with the different types of mycelia.

3.1: Fungal mycelium

3.1a: Mycorrhizal fungi - specifically the ectomycorrhizal 'mushrooms' and their symbiotic relationship with trees

> Mycorrhizal fungi - diversity in a genus (Amanita)

3.2: Saprotrophic fungi

> Brackets and Polypores > Cauliflower fungus > Corticoid (crust) fungi > Pleurotoid agarics

> Saprotrophic agarics > Bonnets > Clavaroid (coral) fungi > Jelly fungi > Cup fungi > Flask fungi

3.3: Fungal guttation

3.3a: Mucorales - pin mould

3.3b: Dendrostibella smaragdina

3.3c: Cystofilobasidium macerans - Sap Yeast

3.3d: Lichenised fungi

3.3e: Pucciniomycetes - rust fungi

Associated information:

Appendix 3A: Ectomycorrhizal fungi partnerships

Fungal mycelium

3.1 (v.1)

Before I started taking more interest in the ecological role of woodland fungi as discussed in the following articles, I hadn't given much consideration to the fact that the different types and formations of mycelium that I often find clinging to the underside of deadwood, or occasionally on the forest floor running across leaf-litter and humus, related to any particular type of fungus.

Fortunately that situation has changed, as I'm now trying to better understand the vital role that fungi undertake in keeping our woodlands healthy, hence this series of articles that I've collectively named 'fungal connections'. Whilst my photographic interests obviously lay with the fruiting bodies, it would be good to know a little bit about what's going on behind the scenes. I'm always going to be a generalist by nature of the subjects that I photograph, but I do like to spend the time trying to learn as much as I can when a subject graps my attention.

In respect of mycelium, I guess that a mycologist would instinctively be able to determine whether it was mycorrhizal or saprotrophic from experience and, although I don't expect to gain anything like that level of knowledge, it would be useful to have an insight regarding the structure and form of the various types of mycelia associated with each fungal group, namely Mycorrhizae, Saprotrophic and Parasitic (Pathogenic).

The following is my understanding from everything I've read, which has been pieced together from many different sources including a couple of open-access scientific papers - Boddy et al. (2006) 'Mycelial Foraging Strategies of Saprotrophic

Cord-Forming Basidiomycetes' and Yafetto (2018) 'The structure of mycelial cords and rhizomorphs of fungi: a mini review'. Not surprisingly these articles go into great detail way beyond the level of information that I'm attempting to cover here, which is purely for personal reference and understanding and, consequently, should not be quoted or used without verification.

Most articles about fungal mycelium in woodlands refer to the underground mycelial network that produces mushrooms. This is mycorrhizal mycelium that you're not likely to encounter unless you go looking for it as the hyphae that make up the body of the organism are very fine, individually microscopic thread-like filaments, that unless bound or matted, would be impossible to see with the naked eye. You'd also have to dig a fair way down as this form of mycelium is usually quite deep in the soil.

There are different types of mycorrhizal fungi as confirmed in the following article. The most common and widespread form is arbuscular mycorrhizal (AM) fungi which is the type associated with herbaceous understory shrubs and plants as well as some trees and has mycelia that can only be seen under a microscope. The mycelial network typically relates to the ectomycorrhizal (EM) type that forms symbiotic relationships with tree roots. It has a different method of connection where the hyphae become clustered into a mycelial sheath around the roots and, as such, could be visible to the naked eye if the tips of the roots were carefully unearthed. The only other time you're likely to find evidence of mycorrhizal fungi is in places where mushrooms have sprouted up from the ground in some abundance as the mycelial network would be more extensive and possibly visible if you had the desire to carefully work through the organic layer into the soil to locate entwined patches. It's not something I've tried to do, so I reserve judgement as to how practical it would be without the correct equipment, but in theory it's a possibility.

Although mycorrhizal mycelium exists deep in the soil, the thread-like hyphae may still be found on organic matter near the surface and may also be seen as a cotton-like mass. The difference with saprotrophic (SA) fungi is that their mycelium is primarily found in the upper layer of the soil where organic matter accumulates or at the soil/litter interface. In these ground level situations there are bound to be times where mycorrhizal and saprotrophic mycelium are in close contact, but they work in different ways with different ecological roles even if they occasionally appear to be competing for resources.

Two examples of different forms of mycelium photographed on leaf-litter and humus under deadwood

(in the photo on the left it looks as though the mycelium has recently emerged and is now starting to fan out in search

of suitable material, whereas the shot on the right shows cotton-like patches clearly joined by mycelial cords)

Saprotrophic fungi are the decomposers, so you'd expect to find the mycelium on dead organic material like leaf-litter, twigs, branches and fallen trees where the fruiting bodies grow. However, there are essentially two types of saprotrophic wood-decay mycelia that adopt different foraging strategies. One forms a network across the forest floor where it effectively waits for woody debris or leaves to fall from the trees, and the other is the type that I believe you're more likely to encounter when turning logs or rummaging around in leaf-litter looking for invertebrates.

The secondary form that I believe is represented in most of these photos actively searches for new resources, adapting and changing form as the need requires. I haven't seen the term used elsewhere, but I refer to this type of mycelia as a 'shapeshifter' given that they're able to change their structure such that over time you can track movement and physical appearance. The hyphae can weave themselves into a loosely interlaced strand, known as a mycelial cord or rhizomorph.

The above examples show mycelial cord and leading hyphae moving across deadwood in search of a new food source

These thicker, stronger, and indeed far more visible, cords are better suited to the tougher role of clinging on to deadwood and surviving underfoot on the forest floor rather than worming their way through the soil. They are formed in different ways, but the primary role of a central cord is to facilitate the progress of the mycelium locating new nutrient resources. Tendril hyphae from the older regions of the mycelia interlace to produce either a thicker, but thin-walled strand as shown above, or a thick-walled fibrous hyphal cord that may resemble a plant root, but they're not rhizomorphs in the true sense.

I presume that the straw-coloured strands in these photos are 'thick-walled fibrous cords'

The mycelial cords are linear organs of massed interlaced threads of parallel hyphae that are working as one to help feed the leading, fanned-out head that is searching for the next suitable resource. The mycelium grows by the hyphae increasing in length, not in thickness as in plant roots. The flow of compounds and sugars that are needed to add new material to the cell walls of the leading hyphae are produced by the release of enzymes that are broken down and converted and the reabsorbed. With new hyphae being added to the front, any branching occurs some distance back so that mycelium always comprises a fanned-out head of unbranched filaments.

In both of the above examples, it appears that the mycelium is still in the process of colonising these

pieces of deadwood as the leading hyphae are still fanned out and exploring

In situations where separate competing saprotrophic basidiomycete mycelia meet, there's often gridlock as neither party will yield to allow the other to move forward which, in addition to the requirement for needing a fresh resource, is probably why the hyphae team up. When the leading hyphae find suitable material, they will start to spread out to colonise and effectively stake a claim and, once established, the cohesive growth of the central cord will slowly unravel.

Unfortunately I don't have any photos at the moment in order to compare the visual appearance of a rhizomorph with a fibrous cord. Rhizomorphs are definitely more root-like, often dark-coloured with a strengthened melanised wall and can be either cylindrical or flat in shape. They are also structurally different, as rhizomorphs have a much more complex multicellular construction with a central cavity that feeds water and dissolved nutrients through to a front-growing tip, all surrounded by a protective, waterproof sheath rather than the far more simple, loosely woven hyphal cord described above. At maturity, these true rhizomorphs can be up to 5mm in diameter and can range from 0.5m to 2m or more in length. The best examples are the parasitic Armillaria spp., notably in Britain the Honey Fungus [Armillaria mellea], but there are a couple of other members of genus that are only weakly parasitic, and then saprobic. In these species the rhizomorphs are well-formed, like old bootlaces, round in section if unearthed from the ground at the base of trees, but usually flattened where the rhizomorphs are pushing up the tree behind the bark. There are a few other fungi that have true rhizomorphs but, as far as I'm aware, none of those species are going to be encountered in British woodlands.

There are of course many aspects to the way that fungal mycelium is formed and how it grows, survives and interacts, or how it differs from one fungal species to another, or indeed how it physically connects with its fungal partner and/or substrate on which it feeds, but those subjects are outside the scope of this article.

I will however end this lengthy opening article about woodland fungal connections with a more generalised brief note regarding the way that mycelium feeds as references to this matter may have been vague. Whilst the actual feeding strategies differ, the hyphae release various enzymes into the substrate, which will break down polymers into soluble elements that are then reabsorbed. The mycorrhizal fungi do this by effectively exchanging soil nutrients and water for nutrients via their symbiotic connection with tree roots, whereas the decomposing saprotrophic fungi produce a similar return by breaking down dead organic material, and the parasitic fungi that haven't really been mentioned here, absorb their nutrients from a living source.

Mycorrhizal fungi

3.1a (v.1)

In broadleaved woodlands particularly, mycorrhizal fungi are all around us, but we only get to appreciate their presence during certain times of the year when the fruiting bodies we most commonly refer to as mushrooms start appearing. For most species this would be in the autumn, but there are some, such as the Common Earthball [Scleroderma citrium] for example that are more likely to seen in July or August. Unlike saprotrophic fungi that grow on decaying organic matter, mycorrhizal fungi grow up from the ground. There are many different species of varying sizes and colours, which is what makes them so popular, but what we see on the surface is just the result of what's happening beneath our feet.

These species form symbiotic relationships living in the soil in connection with tree roots. The thread-like hyphae that form the body of the fungus spreads out in search of nutrients which are exchanged with a compatible tree or possibly various trees. Once the connection is made the hyphae, which are a lot thinner than the tree roots, can extend further, finding the important minerals such as nitrogen and phosphorous that plants need to grow, and tapping into water reserves in the soil that the tree roots wouldn't be able to reach. In return, the fungus receives important elements in the way of sugars and vitamins necessary for its growth and reproduction.

The mycelial network, commonly referred to as the 'woodwide web', never stops spreading as the sugars promote growth, and as the mycelium works its way through the forest soil it detects molecules from other trees, which invariably leads to a new association and explains why most mycorrhizal fungi are connected with multiple trees. And, of course, the same applies to the trees, which may well be connected to more than one fungal partner. It's a sensible strategy, along the lines of 'not having all your eggs in one basket', as neither the fungus or the tree is totally dependent on each other. However, most species cannot survive without a specific host partner. In fact, about 85% of vascular plants form symbiotic relationships with mycorrhizal fungi.

The following photo of three Brittlegills [likely Russula sardonia] were part of a scattered patch of a dozen or more individuals growing alongside a path close to some Scots Pine, probably connected to the same fungal source, but not necessarily to the same tree, as each separated patch could be connected to different trees.

Research shows that whilst some of these mycelial networks may only grow over a few square metres and are relatively short-lived, others can spread over much larger areas and be able to survive for decades if suitable conditions prevail.

Primrose Brittlegill [Russula sardonia]

(occurs in coniferous woodlands typically in association with pines)

Brown Birch Bolete [Leccinum scabrum]

(this particular bolete is only mycorrhizal with birch trees)

Another interesting fact worth knowing is that certain trees such as Oaks, Beech and Birch particularly have many known fungal associations, whereas others like Holly and Hazel may only have two or three. Similarly with conifers, where Scots Pine, and to a lesser extent Spruce, have various relationships, but Fir and most of the other conifer species have very few. Having knowledge of these tree-fungal partnerships is really useful when trying to distinguish between similar species, such as some of the Boletes, Milkcaps and Brittlegills so, in that respect, I'm going to start compiling a reference list - Appendix 3A.

Beech or Slimy Milkcap [Lactarius blennius]

(nearly always found in association with beech, rarely oak)

Red Cracking Bolete [Xerocomellus chrysenteron]

(mainly with conifers, but occasionally with beech trees as here )

Ochre Brittlegill [Russula ochroleuca]

(favours damp woodland and is commonly linked with birch trees)

Mild Milkcap [Lactarius sudulcis]

(typically associated with beech trees)

Of course some of these trees could be colonised by a number of different species of mycorrhizal fungi, which would produce a complex tangled web of hyphae with root connections spreading and intermingling across the whole forest floor all trying to find new partners that can provide the resources they require whilst, at the same time, having to acquire the nutrients that the tree needs to survive. The quest is endless, but the relationship between fungus and tree goes further as research shows that each partner gains information through the exchange, such that a Beech for example can determine and regulate the direction of flow in order to provide extra nutrients to certain seedlings that may be growing in less favourable conditions. With each species of fungus, and indeed with each individual fungus, having its own network there are bound to be some that provide a better service - much like a shorter and more reliable underground train route - and it's these stronger networks that the trees want to connect with as they obviously provide the most mutually beneficial partnership. And, in that respect there's also an added benefit for the tree in finding the right partner as the presence of mycorrhiza can prevent fungal pathogens from attacking its roots.

When a tree seed germinates the roots may end up becoming attached to the same mycorrhizal network that's connected to the parent tree or a completely different network, which may explain why saplings grow at different rates. One would think that seedlings closest to the mother tree would be better provided, whereas research shows that's generally not the case as the larger seedlings tend to be further way. All in all it's an extremely complex arrangement that will never be fully understood apart from the fact that the symbiotic relationship and connection between mycorrhizal fungi and trees is probably the most important aspect of woodland ecology in respect of the health and continued growth of forests.

Mycorrhiza - the correct scientific name of these fungi - are categorised in one of two ways depending on how the connection is made to the plant roots, either being endomycorrhizal where the hyphae physically penetrate the root cells and, therefore, can't be seen on the exterior surface of the root, or ectomycorrhizal where the fungi form a tight mat-like network of visible hyphae around the roots with tendrils that feed into the soil and back into the roots.

Without getting into detail that doesn't really apply to the relationships discussed here, endomycorrhizal fungi are further subdivided into three specific types; arbuscular, which is the most common type, that form structures within the cell roots of a wide variety of plants including ferns and mosses, but can't grow independently so are known as obligate symbionts - these species belong to the Glomeromycota (briefly covered in a later article); ericoid, which as the name suggests form relationships with plants in the Ericaceae family including heathers and rhododendron that typically grow in acid soils; and orchidaceous that have a specific and essential bond with orchids.

As noted above, ectomycorrhizal fungi operate in a completely different way to the endomycorrhizal fungi as the hyphae do not penetrate the root cells. This type of mycorrhiza is primarily associated with woody plants, particularly trees. They're the dominate fungus in coniferous forests and are prevalent in broadleaved woodlands with particular connection with Oaks, Beech and Birch as previously highlighted. Once the connection between the hyphae and the tree roots is made, the hyphae begin to fan out to form a covering known as the 'Hartig net' (after the scientist Robert Hartig who pioneered the early research of these species) where the tendrils work into the root system, extending between the cells, but only so far as to form a good connection. The net-like structure that envelops the roots is called the sheath or mantle.

Most ectomycorrhizal species, or at least most of the fungi that produce visible epigeous (above-ground) fruiting bodies are Basiodiomycete macro-fungi, but there are also quite a few that belong to the Ascomycetes although the majority of these, such as truffles, are hypogeous as they fruit underground.

Mycorrhizal fungi - diversity in a genus

3.1b (v.1)

In theory, the Amanita genus includes a dozen or more species that could potentially be found locally, but when you start looking at the distribution data it's disappointing to find that only five are recorded on a regular basis. They're a bit of a mixed bunch with very individual common names, but they all live in mycorrhizal relationships with various trees in both broadleaved and coniferous woodland, and seeing that I've actually photographed all five, I thought it would be useful to feature them here in a separate article.

The most photographed, although not necessarily the most common species locally, is Amanita muscaria - a rather variable agaric shown here in three stages of growth, two colour forms and both with and without the little white warts that invariably become dislodged with time and wear; it can be found in various habitats, but is primarily associated with conifers or Birch trees. Amanita citrina is probably the most frequently observed member of the genus in the New Forest as it has strong connections with the Beech woodlands, whereas Amanita fulva, which is also featured below at three different growth stages, is more likely to be found in coniferous or mixed woodlands. The least frequently observed is Amanita excelsa, which is probably far more common elsewhere as it's primarily associated with spruce forests, but it also occurs under Beech. And, last but not least, Amanita rubescens which is possibly the most frequently recorded Amanita from local woodlands where it has mycorrhizal connections with various broadleaved and coniferous trees.

Fly Agaric [Amanita muscaria]

(new growth sprouting alongside a path in mixed woodland)

Fly Agaric [Amanita muscaria]

(at its best - a pristine example growing under birch trees)

Fly Agaric [Amanita muscaria]

(a fine example of the less common 'orange form' amongst conifers)

False Deathcap [Amanita citrina]

(mainly associated with beech trees on neutral to slightly acidic soil)

False Deathcap [Amanita citrina]

(frequent in New Forest beech woodlands)

Tawny Grisette [Amanita fulva]

(fresh growth in coniferous mixed woodland)

Tawny Grisette [Amanita fulva]

(the only one of these featured species without a stem ring)

Tawny Grisette [Amanita fulva]

(a smaller species where the expanded cap rarely exceeds 9cm)

Grey Spotted Amanita [Amanita excelsa]

(alongside deadwood in beech woodland)

Blusher [Amanita rubescens]

(particularly frequent locally in coniferous woodland)

Beyond those five species, records are sparse, but there's always a chance of finding Amanita phalloides (Deathcap), Amanita pantherina (Panthacap) or Amanita virosa (Destroying Angel).

Ectomycorrhizal associations

Appendix: 3A (v.1)

A future article