GUT-INHABITING FUNGI OF AUSTRALIAN HERBIVORES Athol V.Klievet
Introduction
Herbivores are extremely important to humans throughout the world both biologically and economically, as they undertake the primary conversion of plant biomass into animal protein. Being at the base of the animal food chain, it is the herbivores that underpin the complexity and biological diversity of the animals in natural ecosystems throughout the world. In addition, herbivores, and in particular ruminants, supply much of the world's requirements of protein for human consumption, fibre for garments and, in less industrialised countries, they provide power for transport and agriculture.
It would appear paradoxical that while herbivores convert plant biomass into animal protein, they are not physiologically capable of utilising a feedstuff largely consisting of plant structural polysaccharides. In order to achieve this outcome many herbivores have developed an enlarged portion of the gastrointestinal tract that acts as a fermentation chamber. This is most highly developed in ruminants, where the forestomach has enlarged to form the rumen. In the rumen, plant material is fermented by a complex microbial ecosystem to yield volatile fatty acids and microbial cells which satisfy the majority of the animal's energy and protein requirements respectively. This ecosystem comprises protozoans, bacteria, viruses and fungi. It is the fungi that inhabit the gastro-intestinal tract of herbivorous mammals that are the subject of this chapter.
While ruminants predominate in the herbivorous macrofauna of much of the world, this has not been the case in Australia until comparatively recent times. The geographic isolation of Australia has meant that large eutherian herbivores were not present on the continent until the arrival of Europeans about 200 years ago. Marsupials filled the niche occupied predominantly by ruminants elsewhere, and, like the ruminants, the macropod marsupials developed an enlarged complex forestomach for the fermentation of cellulosic and other complex plant materials before digestion (Hume, 1982). Also in common with ruminants, the microbes present in the microbial ecosystem of the forestomach include protozoans, bacteria, viruses and fungi (Dellow et al., 1988; Klieve, 1991). However, unlike our knowledge of the rumen ecosystem, the microbes and their interrelationships in marsupials are poorly understood.
Four distinct groups of fungi have been isolated from, or observed in, gut contents.
Soil and aerobic saprotrophic fungi are commonly ingested with food (Bauchop, 1989; Clarke, 1977; Lund, 1974), but are regarded as being passively present in the gastrointestinal tract, apparently neither able to grow nor reproduce in the anaerobic environment. These organisms and their associations with the host are generally of little interest when considering domestic herbivores, but a range of small mammals, including native marsupials, seek out and consume fungal fruit-bodies as a major part of their diet. Mycophagy appears to be of considerable importance in some Australian ecosystems where marsupials are involved.
Gut-inhabiting fungi
the anaerobic rumen chytridiomycetes
N. variabilis (buffalo) N. variabilis (cattle) Neocallimastix sp. C 148 P. communis (goat)
P. communis (sheep) P. minutus (goat) P. minutus (sheep) P. minutus (deer) Caecomycessp. (buffalo) O. bovis 8 48 O. intercalaris C 70 P. spiralis (goat)
and the aerobic chytridiomycetes
S. plurigibbosus BR 33 R. rosea BR 60 S. punctatus BR 117 S. acuminatus 131 162 R. rosea BR 186 Chy. confervae BR 97 Cat. anguillulae BR 105
The upper group of twelve organisms are anaerobic rumen chytrids, while the lower group of seven organisms are aerobic chytrids.
Chytridiomycetous fungi
Host animals and their distribution
Anaerobic gut chytridiomycetes inhabit a wide range of herbivores throughout the world. They are found in both the rumen of domestic and wild ruminants and in the intestines of non-ruminant herbivores. include the following non-marsupial hosts are as follows: cattle, sheep, deer, impala, llama, goat, reindeer, musk ox, camel, horse, elephant and rhinoceros. The organisms isolated were from ruminal contents, hindgut contents, from the oesophagus and from faeces. Teunissen et al. (1991) isolated monocentric fungi from faeces of zoo animals which included African and Indian Elephants, Black and Indian Rhinoceros, and Mara (a South American rodent). In the latter study, the species of fungi isolated were all Piromyces, with the exception of one species of Neocallimastix isolated from a sheep, the only ruminant in the study. Bauchop (1989) also noted that species of Neocallimastix were absent from hindgut fermenters in his work.
Bauchop (1989) did not detect fungi in faeces of rabbits or humans, while Teunissen et al. ,1991) were unable to isolate fungi from faecal samples from the African Wood Elephant, White Rhinoceros, Hippopotamus, or Pygmy Hippopotamus. Orpin & Joblin (1988) were unable to isolate fungi from the faeces of the Giant Panda.
Polycentric fungi have been isolated from cattle and water buffalo (Chen et al., 1994; Ho & Bauchop, 1991; Ho et al., 1990, 1994; Phillips, I989).
Chytrids have also been isolated from a range of Australian native marsupials, in particular the macropods. Bauchop (1989) reported the presence of fungi in the Eastern Grey Kangaroo, Red-necked Wallaby, Common Wallaroo , and Swamp Wallaby, but not in the Common Brushtail Possum. In addition to these species, Dellow et al. (1988) found fungi present in the foregut of the Tammar Wallaby but not the Red-necked Pademelon. Orpin, Theodorou & Bates (unpubl.) found fungi in high numbers in the forestomachs of Red Kangaroos, Eastern Grey Kangaroos and Common Wallaroos. The fungi were present in all sections of the alimentary tract, including unvoided faeces, in the Red Kangaroo and Common Wallaroo, but in the Eastern Grey Kangaroos some animals lacked fungi beyond the forestomach. The reason for this anomaly is yet to be determined.
Role in degradation of fibrous plant material
The role of the anaerobic chytrids in the breakdown of cellulosie plant materials is thought to be of major importance to herbivores. Dense populations of anaerobic fungi occur in animals fed fibrous diets. These fungi rapidly colonise plant fragments and degrade them by both physical disruption and enzymic digestion. The extensive rhizoidal development of the anaerobic fungi allows them to physically disrupt and weaken structural plant tissues. Species of the genus Caecomyces, which do not possess a fibrous rhizoidal system, disrupt plant fragments by the expansion of a bulbous rhizoid within the plant tissue (Joblin, 1989). These mechanisms also effectively increase the surface area available for colonisation by the fibrolytic bacteria of the gut.
Physical degradation is complemented by chemical digestion, and the gut fungi secrete an array of enzymes to digest plant fibre. Using a wide variety of substrates, Pearce & Bauchop (1985) demonstrated a range of glycanase activities including exoglucanase, endoglucanase, amylase, xylanase, P-galactosidase, (3-glucosidase, and (3-xylosidase. This array of enzymes enables fungi to degrade a considerable proportion of plant tissues.
A highly active fibrolytic rumen bacterium, Ruminococcus albus Hungate, degraded only 80% of the barley straw (Hungate, 1457).
From the fermentation of plant material, the fungi typically produce acetate, lactate, ethanol, formate, carbon dioxide and hydrogen as fermentation end products (Bauchop, 1989; Li & Heath, 1943; Orpin & Munn, 1486). These fermentation products are then available to the host animal or for the growth of other microorganisms in the ecosystem.
This entire article is a partial Extract from “Fungi of Australia Vol 1”( P 203-209)