Juliana T. Hauser
Microbiology Department, Carolina Biological Supply Company
Although many people shun dung as a subject fit for study, it is a
marvelous resource that is constantly being produced and deposited in
large quantities at convenient locations. Even though it has passed
through an animal's digestive tract, dung retains many
nutrients. Thus, it attracts its own fauna and flora consisting of
bacteria, fungi, protozoa, platyhelminths, nematodes, annelids, and
arthropods.
Coprophilous (dung-loving) fungi are uniquely adapted to herbivore
dung. They are deposited with dung, and they grow and reproduce
there. They disperse their spores from the heap to a location from
which they will be consumed by a herbivore, pass through its gut, and
again be deposited with the dung heap (Fig. 1).
Dung as a Home
Dung consists of the macerated and undigested remains of plant food
plus vast quantities of bacteria (mostly dead) as well as animal waste
products, such as broken-down red blood cells and bile pigments. The
nature of herbivore dung depends on the efficiency of the digestive
tract, which, in turn, depends on the animal's digestive anatomy and
its microflora. Ruminants produce a fine-textured dung of fibrous
plant material whereas horses, with a less efficient system, produce
much coarser dung. Dung decomposes rapidly because the macerated
material has a high nitrogen content, available aeration, and a high
water content that is protected from fluctuations.
Although there is little available protein in dung, many other
undigested food components are present. Dung is rich in water-soluble
vitamins, growth factors, and mineral ions, some of which are
metabolic by-products of the microbes in a herbivore's gut. For
example, coprogen, an organo-iron compound found in dung, is necessary
for the growth and reproduction of the fungus Pilobolus
crystallinus. Dung also contains a large amount of readily available
carbohydrates.
Fungal Dung Inhabitants
Considering the great variation in the feeding habits, habitats, and
digestive systems of herbivores, it is surprising how universal
coprophilous fungi are. All classes of the Kingdom Fungi are found on
dung, with the Zygomycetes usually appearing first, followed by the
Ascomycetes, and finally the Basidiomycetes. Their distribution is
influenced locally by the number of herbivores in an area. Some
species are restricted to a particular herbivore; for example,
Lasiobolus cainii is found only on porcupine dung. However, many
coprophilous fungi grow indiscriminately on any herbivore dung. The
greatest variety of fungi have been reported on cow, rabbit, and horse
dung, but this could be because the majority of research has focused
on these animals.
Adaptations of Fungi to Dung
Coprophilous fungi are highly specialized for growth on dung, and some
never occur elsewhere. While some dung fungi show few modifications
peculiar to their habitat, most do have some unique features. Many
exhibit some very specialized structures to ensure survival in their
unique habitat.
Herbivores do not graze near their own dung; therefore, the spores
must be propelled beyond this "zone of repugnance." Thus, the spores
or spore masses are relatively large and heavy. In the Zygomycete
Pilobolus, for instance, the entire sporangium is discharged as a unit
(Fig. 2). In the bird's nest fungus, Cyathus stercoreus, the
peridioles (the "eggs") containing many spores are violently
discharged when a raindrop hits the peridium (the "nest"). The
spores/masses, because of their weight, do not remain in the air long,
but follow a parabolic trajectory landing on nearby grass without the
aid of air currents. The sporangium and sporangiophore of Pilobolus
measure about 0.5-1.0 cm, yet the sporangium has been propelled as
much as 1.8 m vertically and 2.1 m horizontally.
Some coprophilous fungi exhibit a phototropic response that
determines the direction the spore mass will be projected and ensures
that the spores clear the substrate. Spore discharge is always during
the day. The entire sporangium of Pilobolus, for example, grows toward
the light source (Fig. 3). To demonstrate this phototropic response,
place the mature culture of Pilobolus inside a container with a hole
punched into one side of the container top. Wrap the container inside
aluminum foil and punch another hole in the foil aligned over the
container hole. Place transparent tape over the hole, and set the
container in a window. The following day, remove the foil and
container. The majority of the ejected sporangia will be found stuck
to the tape or around the light source in the container top (Fig. 4).
The spores are dark to protect them from ultraviolet light until
they are consumed by a herbivore. In some fungi, melanin is present in
the spore walls; in others, a dark membrane covers the spore
mass. Coprinus comatus, a mushroom that fruits on dung, exhibits these
dark spores.
The spores/mass are often mucilagenous so that they stick to
vegetation upon impact, and the mucilage, when dry, cements firmly. In
Cyathus, the peridiole has a sticky piece of hypha, the funiculus,
which attaches to vegetation upon impact and wraps the peridiole
firmly around it. Other coprophilous fungi, such as Mucor hiemalis,
form a sticky droplet around their spores. When an insect visits the
dung, the spores stick to the insect's body. If the insect rests again
on other vegetation or another dung heap, the spores rub off and
adhere to the new environment.
Many of the coprophilous fungal spores will not germinate until
after passing through an herbivore's digestive tract: They must be
heated inside the gut, digested by the gut enzymes and/or bacteria, or
stimulated by the higher pH of dung.
Fungal Dung Succession
Some observers have noted a true ecological succession on dung in that
first the Zygomycetes, then the Ascomycetes, and finally the
Basidiomycetes appear. Early researchers suggested that this
succession was a nutritional one. They postulated that the
Zygomycetes, or sugar fungi, appear first, because their spores
germinate quickly and their mycelium grows rapidly, exploiting the
fresh substrate; that is, they utilize the simple sugars and
hemicelluloses present in dung. The Zygomycetes are not capable of
utilizing the cellulose and lignin found in dung. When the simpler
carbon sources are metabolized, the Zygomycetes disappear and are
replaced by the Ascomycetes, which can utilize cellulose. These are
then replaced by the Basidiomycetes, which can utilize both the
cellulose and the lignin.
Although this nutritional hypothesis of dung succession was an
attractive one that seemed to fit the observations, it ignored some
important ecological and physiological facts. For example, some spores
had already germinated or had their dormancy broken in the herbivore
gut. Also, no scientist had yet considered the
interference/competition/enhancement effects of the various dung
inhabitants on each other.
The nutritional hypothesis was based solely on the order of appearance
of fruiting structures. Mycelial development and growth may not have
been proceeding at the same rate, so a second hypothesis, the
reproduction hypothesis of dung succession, was developed. This
hypothesis was based on the time it takes each kind of fungus to
fruit. The simple sporangia of the Zygomycetes could develop much more
quickly and require much less energy than the more complex Ascomycete
fruiting body. The even larger Basidiomycete fruitification would
require the largest amount of energy expenditure and would, therefore,
take the longest amount of time to appear. This hypothesis still
neglects the interrelationships between fungi themselves and between
fungi and other dung inhabitants.
The dung heap is not inhabited exclusively by fungi. As mentioned
previously, vast populations of bacteria, protozoa, platyhelminths,
nematodes, annelids, and arthropods coexist with the fungi. These
compete for resources, and some parasitize or consume the fungi while
others provide substrates for them. Also, these organisms can deplete
the dung of nutritionally necessary compounds, such as nitrogenous
ones, and can produce waste products that enhance or retard the growth
and reproduction of some fungi. For instance, ammonia, a waste product
of the bacterial degradation of proteins, stimulates sporangial
production of Pilobolus, which grows better in the presence of other
microbes.
Coprophilous bacteria enhance the growth of some of the coprophilous
fungi, but retard the growth of others. Also, the number of fly
larvae, Lycoriella mali (Diptera: Sciaridae) that survive to pupate
increases as fungal competition increases. It could be that as fungal
growth is inhibited, more resources are available to the fly larvae,
or that larvae may be favored by the enzymes produced by fungi to
inhibit other fungi!
There is evidence that some fungi excrete products that inhibit fungal
competitors. A few weeks after dung is deposited, the Zygomycetes and
Ascomycetes disappear, but the Basidiomycetes continue fruiting for
months. Obviously, the substrate has not been depleted. Some
Basidiomycetes suppress some of the Zygomycetes and Ascomycetes by
hyphal interference. Within minutes of contact, the sensitive species'
hyphae undergo vacuolization and lose turgor. This is followed by a
drastic alteration of cell membrane permeability and subsequent death
of the hyphae.
qIn the classroom, dung succession is easy to observe and is sure to
promote the interest of students. Fresh or weathered dung can be
placed in empty containers. If the dung is dry, add a small amount of
distilled water. Plastic wrap secured with a rubber band will allow
observation and prevent evaporation of the necessary moisture. The
dung culture should be observed over a period of three to four weeks
to study fungal succession.
The success of coprophilous fungi, as measured by their ability to
produce and maintain a fruiting body, is not simply a matter of
competing against other fungi. Instead, it is a complex web of
interactions, some combative, some inhibitive, some mutually or
exclusively beneficial between and among the bacteria, fungi,
protozoans, platyhelminths, nematodes, annelids, and arthropods. It's
a jungle in there!
Further Reading
Francis, S. M. 1988. Fungus guns 2. The Mycologist 2:78-79.
Ing, B. 1989. Why not look at the dung fungi? The Mycologist 3:33.
Kendrick, B. K. 1985. The Fifth Kingdom. Mycologue Publications,
Waterloo, Ontario.
Safar, H. M., and R. E. Cooke. 1988. Interactions between bacteria and
coprophilous ascomycotina and a Coprinus species on agar and in
copromes. Transactions of the British Mycological Society 91:73-80.
Stanley. A. 1992. Fun with fungi. Address to the North Carolina
Science Teachers' Meeting, Charlotte, NC. Ms. Stanley is curator of
the Fungal Herbarium Collection, UNC-Charlotte.
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Fungi Cultures and Supplies
from Carolina Kits and Sets
Pilobolus Kit
This popular "shotgun" fungus is used for studying phototropic
responses. The kit includes one plate culture Pilobolus crystallinus,
foil sheets, 6 plates rabbit dung agar, containers for experiment,
sterile scalpel, autoclavable disposal bag, and instructions.
R1-155800 Per kit . . $24.50
Student Independent Study Kit: Fungi
Consists of a microscope slide of the specimen; a cardboard holder for
the slide; card with labeled drawings, text, and photomicrograph; and
a culture of your choice of four fungi listed below.
Consists of a box culture (ready to fruit) of Coprinus cinereus and a
pad of 30 "Gill Fungus Life Cycle Bioreview" Sheets. Includes
culturing instructions.
R1-155792 Per set . . $17.95
Culturing Supplies
Rabbit Dung Agar
R1-156381 Per 10 plates . . $16.18
Rabbit Dung
Sterile. For culturing Pilobolus and other coprophilous organisms. 4-oz cup.
R1-156382 Per cup . . $5.00
8"-Diameter Culture Dish
Molded specially for us of crystal-clear
soda-lime glass. The glass gives off minute traces of salts which are
beneficial to microorganisms. Good for stock cultures and for use as
terraria or aquaria.
R1-741006 Each . . . . $8.50
12 (case) . . $91.80
Single-Culture Fungi
Cyathus stercoreus
Basidiomycete. A bird's nest fungus. Vase-shaped fruiting body. Large
culture ready to fruit. Cultured on nutrient straw/dirt.
R1-155986B Each . . $12.25
Pilobolus crystallinus
Zygomycete. Shotgun fungus found on dung; phototropic. Cultured on
rabbit dung agar.
R1-156207 Each . . $8.45
Coprinus cinereus
Basidiomycete. Inky cap mushroom. Cultured on rabbit dung agar.
R1-155979 Each . . $6.95
Coprinus cinereus
Large culture ready to fruit. Cultured on rabbit dung agar.
R1-155979B Each . . $12.25
All prices are f.o.b. shipping point and are subject to change without notice.
