FUNGAL ECOLOGY
(sometimes with special regard to macromycetes)
Fungi and their environment • Life strategies and interactions of fungi • Ecological groups of
fungi, saprotrophs (terrestrial fungi, litter and plant debris, wood substrate, etc.) • Fungal
symbioses (ectomycorrhiza, endomycorrhiza, endophytism, lichenism, bacteria, animal relationships)
• Parasitism (parasites of animals and fungi, phytopathogenic fungi, types of parasitic relations)
• Fungi in various habitats (coniferous forests, broadleaf forests, birch stands and non-forest
habitats, fungal communities)
• Fungal dispersal and distribution • Threat and protection of fungi
(the study material has not been corrected by native speaker)
PF_72_100_grey_tr ubz_cz_black_transparent
MASARYK UNIVERSITY, FACULTY OF SCIENCE
DEPARTMENT OF BOTANY AND ZOOLOGY

SYMBIOTIC RELATIONSHIPS WITH ANIMALS
Fungal symbionts of animals can grow on the surface or inside animal bodies. Growth on the surface
means colonization of fur, skin, feathers, exoskeleton; the fungus is often limited to dead tissue
and does not cause defense reaction of the body, but is exposed to the external environment and
there is often low availability of water and nutrients (keratin is very resistant to
decomposition).
In contrast, there is usually a stable environment inside the body, plenty of water and freely
available nutrients, but fungi have to deal with abundant bacteria, low oxygen content, low pH and
strong peristalsis (digestive system) or a strong immune response (blood circulatory system).
A common characteristic of fungi, which can be described as symbiotic (obligatory symbioses or
facultative relationships), is not harming the animal partner – seen from a human point of view,
the fungus tries to keep its „substrate“ alive and not cause its disease and death. Otherwise there
is a risk of loss of this „substrate“ and subsequent competition with necrotrophs.

At first we can mention cases of endosymbiosis, where the fungus spends its entire life inside the
animal’s body – for example, fungi have been found in the cells of amoebae or in the body cavities
of annelids.
The most common endosymbionts are yeasts or fungi
forming yeast-like stages, living in the digestive tract of
various animals (e.g. Spermophthoraceae are fixed on
animals).
The role of Candida albicans has not yet been fully
elucidated; this fungus is present in humans on the body
surface or in the digestive system, where it is a natural
inhabitant (cells attached to the intestinal wall). In the
case of excessive reproduction it becomes a pathogen
that can even cause the death of its host (see also
Parasitism, pathogenic fungi).
candida
http://medinfo.ufl.edu/year2/mmid/bms5300/images/semyeast.jpg

Fungi also play an important role as part of the microbiota in the rumen of ruminants or the
intestines of non-ruminant herbivores. With the exception of molluscs, animals do not produce
cellulases, so they need to „pre-chew“ plant food – especially the obligately anaerobic
Chytridiomycota (sensu lato), exactly Neocallimastigomycota are involved here (carbon dioxide and
methane occur in the digestive tract, traces of oxygen are immediately utilised by facultative
anaerobes).
Although the question is whether it is a mutalistic relationship or commensalism, it is probably a
beneficial interaction of fungi with other microbes, which results in the decomposition of
nutrients (these fungi are able to ferment cellulose, xylans, hemicellulose, starch to formic,
lactic and acetic acids), the release of vitamins and amino acids (plant food is quite poor of
them) and in some cases the detoxi-fication of plant toxins. They are effectively supplemented by
rumen bacteria – chytridia mechanically disturb the substrate, bacteria increase the activity of
chytrid enzymes and the efficiency of decomposition by producing methane.
C:\Documents and Settings\Hrouda\Dokumenty\S_Vyuka\stazeno\ekolhub_symbiot\81_neocallimastix.jpg
http://cgdc3.igmors.u-psud.fr/microbiologie/partie1/chap3_02_eumycota.htm
http://www.bsu.edu/classes/ruch/msa/wubah.html (2x)
Piromyces neocallimastix2
Left and centre: Neocalli-mastix frontalis; right: Piromyces communis

Most endosymbiotic fungi are associated with insects (yeasts, hyphomycetes); they occur in the
digestive tract, Malpighian tubules or live in special tissues – mycetomes – or directly in special
cells – mycetocytes (bacteria are involved here in addition to fungi). The fungi supply the insects
with some amino acids and vitamins, they also help to degrade nitrogenous products of metabolism
(urea, uric acid). In order to transfer the fungus to other individuals, it usually passes from the
mycetome to the digestive tract, from where it is excreted => then it comes into contact with laid
eggs or offspring.
General rule: the more specific structures are evolved, the older (meaning evolutionarily) a given
symbiotic relationship usually is.
PM_B_bartosi_Kral_Sn_ceroteg_stred prodorsa_10mi
Springtails and mites are common among the organisms which frequently spread spores of fungi (both
saprotrophic and mycorrhizal) in the digestive tract and on the body surface,
Surface cerotegument on the dorsal side of the body of the soil oribatid mite Belba bartosii with
fungal spores (arrows).
Photo Jan Mourek, http://www.rozhlas.cz/leonardo
/veda/_galerie/449587?type=image&pozice=1

However, the mutually beneficial effects of these organisms have a broader scope – the hyphae serve
as food and the springtails in turn mobilise nutrients in the substrate (urea), maintain the
diversity of fungi in the soil and stimulate growth by biting when removing old hyphae (=>
compensatory growth). Some ectomycorrhizal fungi are even able to hunt for springtails (of which,
however, the „preys“ are probably not very happy...).
Both groups of invertebrates are an important part of edaphon (they feed on strongly decomposed
litter, algae, fungi, detritus or are predators).
There are still contradictory opinions, how strong the preferences for the substrate are
(phytophagous, mycophagous, herbivorous); probably they are „choosy generalists“ (i.e. they choose
what is possible), but we can suppose:
– if the utilise plant debris, it is strongly decomposed (low C:N ratio), i.e. already colonised by
fungi;
– if fungi, they prefer dematiaceous (however, the question remains why they feed on them, when
melanin is difficult to degrade), not chitinolytic (to avoid the fungus to eat them – but not
absolutely, the most common species associated with oribatid mites is chitinolytic (!) Beauveria
bassiana) and not toxinogenic (except the case of Aspergillus flavus on stored grain).

Other cases are symbiotic fungi living
outside the animal bodies or on their
surface.
Woodpeckers probably help the spread
of lignicolous fungi, whose action in wood,
on the contrary, they use in nest formation.
Nesting of red-cockaded woodpecker
(Picoides borealis) is reported in cavities,
which it creates in trees with heartwood
softened by Phellinus pini – the woodpecker
does not have to carve so much and at the same
time the nest is still protected by hard sapwood.
The use of various habitats created by vertebrates can be described as „free symbiosis“ – bird
nests have already been mentioned as a source of nutrients for keratinophilic species, or Hebeloma
radicosum drawing nutrients from mole „toilets“. Other cases may be crocodile nests with eggs,
where thermophilic species occur, or nests where the animals accumulate stocks – e.g. seed stocks
of the rodent Dipodomys spectabilis (photo), which are colonised by non-toxinogenic species of the
genus Penicillium.
http://en.wikipedia.org/wiki/Red-cockaded_woodpecker
Picoides_boreal
http://www.forestryimages.org
/browse/detail.cfm?imgnum=2250085
Phell_pini
http://www.mnh.si.edu
/mna/image_info.cfm?species_id=69
Diposomys

Coexistence of fungi with bark beetles
(Scolytidae) is known – beetle corridors
are grown through by Ophiostoma spp.,
which degrade cellulose and lignin, and
serve as food for hatched larvae.
Adult beetles then spread the fungus to
other trees – not „randomly glued“ fungi
(Ophiostoma or Ceratocystis spores are released from perithecia in sticky mass), but females have
„pockets“ on the body surface, below the surface or between the abdominal segments, in which they
transfer the mycelium or conidia, so-called mycetangia (mycangia) => when laying eggs, they also
„lay“ fungal diaspores. Weevils form similar symbiosis (transfer of fungal cells in mycetangia)
with some yeast species.
84_ophiostoma_koremie+perithecium+chodby_www-biology-ed-ac-uk_research_groups_jdeacon_FungalBiology
_dutchelm-htm 83_pit_mycangia_of_ambrosia_beetle 83_invaginated_mycangia_of_ambrosia_beetle
Top: Ophiostoma sp., (a) coremium, (b) perithecium with sticky drop at its top.
Centre: Surface mycangia on the head of Treptolatypus solidus (left), Scolytodes unipunctatus
(right; arrow shows a spore).
Bottom: Internal mycangia of Xyleborus affinis (left) and Xylosandrus germanus (right).
www.biology.ed.ac.uk/research/groups
/jdeacon/FungalBiology/dutchelm.htm
http://www.antmacroecology.org/~ambrosiasymbiosis/mycangia.html
Photo Jiří Hulcr
Photo Jiří Hulcr
Photo Mirek Kolařík
Photo J. Hulcr & K. Miller

Similarly, the sawflies have mycetangia next to the ovipositor – they spread some stereoid fungi
(Stereum sanguinolentum, Amylostereum spp.) or polypores (Cerrena unicolor). Their larvae do not
have to feed directly on the fungus, but wood with degraded lignin and cellulose is better
digestible for them. The irony of fate is that the sawfly can carry an unwelcome „companion“ – a
nematode that feeds on the same fungi, which can attack the wasp larva, settle in it and in
adulthood spread further with laid eggs.
In general, fungi growing through and spread through insect corridors are referred to as ambrosia
fungi (ambrosia are thin-walled cells forming a continuous layer lining the inner walls of the
corridors in the wood).
The narrower concept is that true ambrosia fungi are only those that are carried by insects in
specialised organs (mycetomes, mycetangia).
A certain form of the fungus-animal relationship, although it is not an obligatory symbiosis, is
also endozoochory or epizoochory, which is common in many animal groups (more in the chapter Fungal
spread and distribution).
C:\Documents and
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C:\Documents and
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jpg C:\Documents and
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Amylostereum areolatum, Cerrena unicolor
Stereum sanguino- lentum

The „mushroom growing“ by animals has been found in ants (genera Atta and Acromyrmex from Latin
America), which create „mushroom gardens“ in their ant-hills (up to several hundreds, 20–30 cm in
size): they bring leaves and twigs to the anthill and they bite them on the pulp
C:\Documents and
Settings\Hrouda\Dokumenty\S_Vyuka\stazeno\ekolhub_symbiot\89_acromyrmex_houbova_zahradka.jpg
C:\Documents and Settings\Hrouda\Dokumenty\S_Vyuka\stazeno\ekolhub_symbiot\88_leaf-cutter-ants.jpg
=> they inoculate individual fragments by the fungi (Agaricaceae, specifically tribus
Leucocoprinae; there is a close connection, individual species of ants have „their own“ species of
fungi ) => the „gardens“ contain chewed pieces of leaves covered with dense mycelium (in species
forming underground nests they fill the chambers in the substrate) => hyphae then serve as food for
ants, which are obligately mycophagous – workers harvest inflated ends of hyphae and distribute
them in bowels to larvae and other adults (larvae are probably fully dependent on this food, in
adults it is
not such an essential
component of nutrition).
http://blog.fortumo.com/wp-content/uploads/2009/07/leaf-cutter-ants.jpg
C:\Documents and
Settings\Hrouda\Dokumenty\S_Vyuka\stazeno\ekolhub_symbiot\89_cyphomyrmex_costatus_in_fungal_garden_
in_panama.jpg
Left: „farming“ males of Cyphomyrmex costatus, Right: „mushroom garden“ of Acromyrmex sp.
Photo Alex Wild, http://www.alexanderwild.com/Ants/Taxonomic-List-of-Ant-Genera/Cyphomyrmex
Fisher et al. 1994;
http://www.mycolog.com/chapter16.htm

The ants not only „grow their mushrooms“, but also remove other species that contaminate „their
culture“ (the mechanism of recognition is still unknown, probably the ants recognise the smell of
various species), directly physically, they „weed their gardens“, i.e. they select „the other“
spores from the brought material and take them out of the colony in special pockets (for this
purpose, the workers use a separate exit, to minimise the possibility of contamination).
In addition, ants have symbiotic bacteria (genera Streptomyces or Pseudonocardia) in the holes in
the body, which they „feed“ by secretions. In return, the bacteria produce antibiotics to suppress
the growth of „unwanted“ fungi (shape of the holes is species-specific, as well as the symbiont
species).
C:\Documents and
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Inflated terminal cells of hyphae are called gongylidia; they do not grow individually in the
„gardens“, but form compact clusters of tangled hyphae called bromatia. No sporulation was found in
these fungi and the spread is likely realised through the transfer of mycelium with the queen when
a new colony is established.
Clémençon: Cytology & Plectology ..., 2004.

Termitomyces titanicus
http://panacea.med.uoa.gr/topic.aspx?id=263
C:\Documents and
Settings\Hrouda\Dokumenty\S_Vyuka\stazeno\ekolhub_symbiot\91_substrate-for-termitomyces.jpg
Heinz Clémençon: Cytology and Plectology of the Hymenomycetes.
C:\Documents and
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A specific symbiosis is formed by termites with fungi of the genus Termitomyces (Basidiomycota,
Tricholomataceae, weighing up to 2.5 kg and a pileus diameter of 60 cm) and some xylariaceous
fungi: termites in the nests roll „balls“ of wood, herbs, mycelia and fungal conidia, which then
they eat together with the wood – the fungal exoenzymes probably allow them to digest the wood =>
conidia of the fungi are then spread with their droppings.
Various species of termites also form macroscopic formations of sponge-like consistency (using
plant remnants and their exudates), containing chambers, which are grown through (and their walls
covered) by fungal hyphae.

Instead of fruitbodies, termitospheres are formed on their surface – tiny structures (analogous to
sporodochia), ...
C:\Documents and
Settings\Hrouda\Dokumenty\S_Vyuka\stazeno\ekolhub_symbiot\92_young-termitospheres.jpg
Heinz Clémençon: Cytology and Plectology of the Hymenomycetes. Bibliotheca Mycologica 199. J.
Cramer, Berlin-Stuttgart, 2004.
C:\Documents and
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jh
C:\Documents and
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jpg
... on the surface of which aleurio-spores (thick-walled conidia) are formed => termitospheres are
eaten by termites and aleuriospores spread by faeces (similar to the case of „balls“).
If the termitospheres are not eaten, they can later develop into fruitbodies.
„Mushroom growing“ (described for 210 ant species and 330 termite species!) is known only from
tropical regions (forests, savannas).
C:\Documents and
Settings\Hrouda\Dokumenty\S_Vyuka\stazeno\ekolhub_symbiot\95_termitomyces-aleuria.jpg
Clémençon: Cytology and Plectology ..., 2004.

The „triple relationship“ is formed by fungi of the order Septobasidiales with plants and scale
insects. Wingless insect females live appressed at the leaf from which they suck nutrients
(basically it is parasitism) => they are overgrown with fungal hyphae until the fungi form a
continuous cover over the insect colony => they immobilise the insects, penetrate haustoria into
the blood cavity and suck nutrients from there – in principle the fungus parasitises on parasitic
insects (Septobasidiales are probably not able to exist independently for a long time).
C:\Documents and Settings\Hrouda\Dokumenty\S_Vyuka\stazeno\ekolhub_symbiot\99_scale-insect.jpg
C:\Documents and Settings\Hrouda\Dokumenty\S_Vyuka\stazeno\ekolhub_symbiot\99_septobasidium.jpg
The relationship is established using chemical attractant secreted by the fungus => insects form a
colony in which only some individuals are directly attacked, while others use protection of the
fungal cover together with them.
Top: still free individuals of scale insects.
Bottom: Septobasidium, which has already covered the colony of these insects.
http://www.morning-earth.org/Graphic-E/SymbiosisCrossKingFungi.html

Individuals of scale insects, into which the haustoria of fungi have penetrated, do not reproduce;
reproduction of the species is ensured by other females in the colony, which are not directly
attacked by the fungus (insects also ensure spread of the fungus, they transfer basidiospores on
their bodies).
To summarise the plus and minus of the relationship, the fungus parasitises on the insects, but on
the other hand provides them protection (against predators and pathogens) and a stable environment
(limited evaporation) – this is an example of relativity of the meaning of the word symbiosis.
It is therefore appropriate to make a general conclusion at the end of this chapter: there are no
sharp boundaries between mutualistic symbiosis, saprotrophy and parasitism.