Fungi and invertebrates
There are numerous fungus-invertebrate associations, many of which are discussed in the reference given in the button and this link [http://www.botany.hawaii.edu/faculty/wong/BOT135/lect24.htm] discusses a few examples of fungus-insect symbioses.
The aptly named Stinkhorn fungi rely on carrion-loving insects for spore-dispersal. One thing common to all Stinkhorns is the production of spores in a foul-smelling, khaki to brownish slime. You can see this spore-bearing slime at the top of this Dictyophora multicolor . The smell is a powerful attractant of various flies and midges. In some other Stinkhorns, such as Anthurus archeri and Aseroë rubra , there is an additional colour cue. The red in these Stinkhorns looks much like freshly exposed meat.
In tropical America stingless bees in the genus Trigona have been seen collecting the exudates (and possibly spores) from stinkhorns in the genera Dictyophora and Phallus. Entomologists studying these examples found no exudate or spores on the bodies of the bees, strongly suggesting that the bees swallowed the exudate and spores. Presumably the bees include spores in their diet. It is also possible that at least some spores will pass, undigested, through the bees - in which case the bees would act as dispersal agents for the fungi.
The butterfly Prosotas dubiosa
on fungus Dictyophora multicolor
In late March 2006 the Australian National Botanic Gardens received an enquiry about a fungus found growing in a garden at Moore Park Beach, 25 km north of Bundaberg, Queensland. The fungus was Dictyophora multicolor and that very specimen is shown here . What was particularly interesting was that the photo showed a butterfly on the upper-right of the Stinkhorn. From a closer look, at an enlargement of the photo, it was clear that the butterfly's proboscis, though a little fuzzy, was uncoiled and with its further end either in contact with, or very close to, the fungal surface. The angle makes it hard to tell. There's an enlargement of the butterfly here (right). This was an interesting photo because there appeared to be no other reports of any butterfly visiting a Stinkhorn. The photo was taken by Sandra Sullivan, who has very kindly allowed its reproduction on this website. She also noted that she had noticed a couple of small butterflies on the fungus. This suggests that the visitation could be more than just a chance event.
For a definitive identification of the butterfly a specimen or at least a view of the upper wing surfaces would be necessary. The photograph shows only the underside, since the wings are folded. On the basis of this limited evidence, CSIRO Entomology in Canberra noted that the closest match is with the genus Prosotas, of the family Lycaenidae. The wing details most closely match the species Prosotas dubiosa. This butterfly is known from Sri Lanka and India, through to northern and eastern Australia and the Solomon Islands. It is a species of humid, tropical or sub-tropical areas, but has also been found once at Yunta, in arid South Australia, in 1999.
The South Australian record of Prosotas dubiosa is noted at: http://users.chariot.net.au/~rbg/dubiosa_ds.htm
The adult or juvenile stages of various flies, mites, gnats, beetles, springtails and nematodes eat fungal fruiting bodies, spores or mycelia. To give just one specific example, flies of the genus Tapeigaster are commonly seen on a variety of Australian mushrooms and boletes. Typically, a highly territorial male will patrol the cap of a mushroom or bolete while the female lays her eggs on the gills or pores below. Australian Tapeigaster species have been reared on a number of mushroom and bolete species.
If you take a medium to large mushroom cap and shake it gently (gills facing down) over a sheet of paper you are likely to end up with a collection of varied invertebrates on the paper. Amongst them will be a mixture of juvenile and adult forms with various feeding strategies. Some will be generalist feeders on any fungal tissue while others will be specialists, perhaps just feeding on the spores, for example. Then there will be those feeding on other invertebrates. The corky to woody bracket fungi are also often good harbours of invertebrates.
Various invertebrates have evolved associations with specific fungi. For example, in Central America the leafcutter ants farm fungi on digested leaf fragments. A very informative site is: http://www.zi.ku.dk/personal/drnash/atta/Pages/Leafcut.html
While many termites from Africa through to Asia also grow fungi but use the termite faeces as a base. The guts of these termites lack the wood-digesting microbes found in other termites and so the African-Asian species rely on the fungi for food.
The wood wasp Sirex noctilio was accidentally introduced to Australia in the 1950s and has caused considerable economic loss in Australian pine plantations. The larvae develop in trees that have been infected with a fungus in the genus Amylostereum. The fungus may regulate the water content in wood, to a level optimum for egg or larval development, or the larvae may eat the fungus. When an adult female emerges from her pupal case she picks up fungal cells in a pouch located near the base of her ovipositor. When she lays her eggs in another tree she simultaneously squeezes out fungal cells from the pouch, thereby initiating a new fungal infection. The fungus is carried to new host trees and seems to do so well out of this arrangement that it does not produce fruiting bodies in Australia. It has not lost the ability to do so, for fruiting bodies can be artificially induced in the laboratory. However, in the wild the fungus saves a considerable expenditure of resources by relying on the wasp for dispersal. There are also a number of beetles which have similar associations with fungi.
Numerous fungi are parasitic on invertebrates, though many of them are microfungi and so outside the scope of this website. However, Cordyceps is a widespread macrofungal genus, with the bulk of the species being parasitic on invertebrates. The adults or larvae of numerous moths, beetles, ants, wasps or spiders are the victims, with the fungi killing their hosts. This link shows exquisite paintings of various species of Cordyceps and a couple of other genera.
Cordyceps gunnii , is a fairly common Australian species. One photo shows the above-ground fruiting body of the fungus and the other shows the excavated larva and fungal fruiting body. The mycelium is ordinarily out of sight, in a below-ground larva of Ghost Moths in the genus Oxycanus. In this photo there are some examples of another Cordyceps species. By the time the club-like fruiting body is produced, the invertebrate has been dead for some time, its body filled with mycelium, hence the common name of Vegetable Caterpillar given to the genus Cordyceps.
Other names given to members of the genus are vegetable wasps and plant worms, also the title of a book by the 19th century English mycologist MC Cooke. The cover of the book, shown here, bears a drawing of Cordyceps taylori. This is an Australian species, discovered in 1837 on the banks of the Murrumbidgee River, 10 miles from Yass in NSW. In his book, Cooke called this the Murrumbidgee Vegetable Caterpillar. It parasitizes the larvae of moths in the genus Trictena. The smooth, antler-like areas are the above-ground fruiting bodies, while the knobbly sections are the below-ground, parasitized larvae. Here is an extract from Cooke's book in which he discusses four Cordyceps species found in Australia. Three of the four had been discovered first in Australia whereas the first record of Cordyceps robertsii was from New Zealand.
Theodor Holmskjold's Beata ruris otia Fungis Danici has been said to contain the finest fungal illustrations published in pre-modern times. The illustrations were printed as engraved outlines and were then hand-coloured and one of the species illustrated was named Clavaria militaris by Holmskjold. He was the first to observe that the fruiting bodies grew on dead insects. The general belief had been that the dead insect somehow was transformed into the fungus. The species is now known as Cordyceps militaris and here is a link to a PDF of the Beata ruris plate for this fungus.
Fungus sucks sap-suckers
The species in the genus Septobasidium form relationships with scale insects. These photos show a couple of examples of the flattish Septobasidium fruiting bodies , , collected from plants in the Australian National Botanic Gardens. Septobasidium is a worldwide genus, with about 200 species, and is fairly common in Australia.
The photos show nothing unusual. However, if you look beneath that brown surface you will find a number of scale insects. These insects are plant parasites and suck plant sap through long tubes that the insect inserts into the plant. In turn, Septobasidium grows over the insects, fungal hyphae penetrate the insects and absorb nutrients from them. The scale insects are immobile and it would seem that this is simply a case of parasitism with the fungus getting all the benefits, but there are benefits to the embedded scale insects. They are sheltered from the environment and protected from predators, allowing them to live longer than their free-living brethren. It has been shown that, in at least some cases, the fungal covering over the scale insects is deeper than the reach of the ovipositors of parasitic wasps that seek out scale insects.
The accompanying stylized diagram shows the basic features in a scale-Septobasidium association. The scale insect is the centrally positioned khaki coloured object and its sitting on the outside of a branch (coloured light brown). The scales sucking tube (blue) penetrates deep into the plant. You can see the numerous dark brown hyphae that make up the bulk of the Septobasidium. Inside the scale are numerous coiled hyphae (in red), which are the haustoria through which the fungus absorbs nutrients from the scale. In this case, the fungus has entered the scale from just one point, to the left.
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