Fungi are found in a wide diversity of environments. Some habitats are normally continuously disturbed. Aquatic ecosystems, especially the sea shore and streams are continually moving. The fungi found in these environments must have adaptations which enable them to tolerate ongoing disturbance. Some habitats are normally more stable. Disturbance in stable environments is normally localised, infrequent and unpredictable. Soil might be disturbed on a small scale by burrowing animals or locally by rapid flowing water, and at a larger scale by fire.
Humans now regularly disturb some of these previously stable ecosystems, and the disturbance is ongoing, widespread and on a large scale. Imposition of agriculture, especially cropping, has introduced a new stress on the biota in soil. This essay examines cropping as a regular, severe and widespread disturbance.
Cropping consists of a number of different types of disturbance. Apart from cultivation, the soil is subjected to fertilisation, planing, irrigation, growth of single plant species for short periods and periods where plants are absent. Once sown, the crop is of a single age and treatment of the crop is homogeneous. Weeds are suppressed often by chemicals, fertiliser is applied to the entire paddock to create even growth of the crop, and the crop matures and is harvested at the same time. As a consequence of cultivation, soil carbon is reduced. As a consequence of the limited number of crop species, soil organic matter is homogenised and simplified. Overall, the heterogeneity of the ecosystem is severely reduced and the fungal community is modified and probably simplified.
We might predict that the impact of disturbance would increase with greater frequency and intensity of the disturbance. Studies over a long period have shown that soils used for cropping have markedly different communities, reduced species richness, and total fungal biomass is reduced when compared to undisturbed sites. This overall pattern takes place within an annual framework of bacterial dominance early in the period of crop growth, followed by a change to fungal dominance as the crop matures. Data from eastern Australia indicate that in cropped soil, plant pathogens increase, some saprotrophs (eg Trichocomaceae) decline and, of course, ectomycorrhizal fungi dissapear.
Monoculture provides an ideal environment for the explosive expansion of fungi adapted to the new single source of food, that is pathogens adapted to the crop species. Reduced species richness might be associated with the reduced complexity and quantity of organic carbon. Reduced fungal biomass might be due to the reduced total organic energy in cropped soil. Interpretation of these data must be tempered with the knowledge that methods used for studying fungal populations influence the results obtained. As both culture-based and molecular studies have arrived at broadly similar results, the loss of fungal diversity and biomass in cropped soils is well supported and now well accepted. However, while diversity is reduced overall, the community found within arable systems appears well adapted to the conditions.
Much of what follows is speculation. It assumes that you have read the chapter on life history strategies. LINK The basic message is that ecosystems are dynamic, the populations found in the ecosystem are adapted to their environment, and that the responses of fungi to disturbance are predictable. We use the example of arbuscular mycorrhizal (AM) fungi to compare the strategies used by fungi in disturbed habitats. LINK
In relatively undisturbed woodlands in Australia, AM fungi associate with approximately 70% of the plant species. Other types of mycorrhizal fungi are also present in undisturbed habitats. LINK In undisturbed Australian soils, the community is dominated by fungi that form complex sporocarps, though infrequently and usually below ground. Single spores are uncommon. If you determine the molecular characteristics of the occupants of roots and soil, you will find more than 40 members of Gigasporaceae, Acaulosporaceae and Glomaceae, the latter dominating. If you place soil cores into a growth room and cultivate the plants that are normally found in that soil, a variety of species of Gigasporaceae and Acaulosporaceae will sporulate. Only if you leave the pot for more than about 4 months will you find spores of Glomaceae. These are invariably in complex structures called sporocarps, incorporating soil particles and found beneath the soil surface. Interestingly, if you examine the scats of small mammals from the woodland, such as bush rats and bandicoots, spores of many more of the sporocarpic Glomalean fungi will be seen. The small animals fossick through the litter and soil, extract and eat sporocarps. Clearly, the fungi fruit regularly.
With sufficient replicate cores, a typical woodland habitat in Australia will be found to include more than 40 species of AM fungi, and the species will probably include many that have not, as yet, been described. The larger the habitat, the greater the diversity of microsites, and the greater the diversity of AM fungi.
Glomalean AM fungi in woodland sites are intolerant of disturbance. Clearing the vegetation and disrupting the soil will kill a large proportion of the existing AM fungi. If the soil is stockpiled at one side and sown with plants to sustain the fungi, a small number of species of AM fungi will be maintained. However, even when this stored topsoil is spread back over the site, the population of AM fungi will be severely reduced and diversity comparatively limited.
Reductions in the fungal population by this type of soil manipulation has ramifications for revegetating cleared sites, as commonly follows mining. Usually many plant species will not survive outplanting because they depend on mycorrhizas for survival. LINK It is possible to reintroduce AM fungi to these sites during revegetation, but the practice is expensive and difficult.
Studies with AM fungi that are easy to culture suggest that establishment and maintenance of plant diversity in communities relies on the presence of a wide diversity of AM fungi. Further, plant productivity is greater when a large array of AM fungi are associated with the plants. Presumably, each of the fungi has a degree of specificity with hosts and environment, resulting in a complex interaction whereby the fungal population contributing to plant growth and development changes over time and space. It might be predicted that the response of AM fungi to the complex plant community is the same. The studies that indicate inter-relations between plant and fungal diversity, might be used to argue for diversity of both groups ensuring complexity of the chemical and physical environment in which they exist.
In terms of life history strategies, the fungi in woodlands are following a K strategy. The organisms are long lived, reproduce relatively slowly, contribute a considerable energy to the offspring and exist in stable communities.
AM fungi in soils used for cropping appear to have a very different life history strategy. The offspring (hyphal fragments and blastospores) are comparatively small, produced in abundance, commonly short lived, and they exist in an unstable environment.
|'K' selected||'r' selected|
|Number of offspring||few||huge|
|Rate of response||slow||fast|
|Length of life||long||short|
|Stability of community||stable||fluctuating|
|Tolerance of disturbance||intolerant||tolerant|
AM fungi found in cropping soils form single spores in large numbers. Up to 1000 blastospores per ml of soil have been counted, though these are not all likely to be viable and some may be dormant. Sporocarps have been recorded, though they rarely contain more than 3 spores. The fungi are adapted to disturbance, to a degree. An assessment of quantities of AM fungi, called MPN, mixes soil through a sterile diluent, prior to quantification. Quantification of AM fungi using MPN indicates that more than 10,000 infective units per ml are present in some soils. This is approximately 10,000 times the quantity needed to initiate AM that will sustain a host plant. In other words, the reproductive effort of these AM fungi is directed towards formation of huge numbers of reproductive units, some of which will survive the various disturbances of the habitat.
The survival of these units is unclear. The fungi are present as blastopsores and hyphal fragments, and both can function as propagules. Molecular measures indicate that a few propagules of species adapted to cropping will survive in soil for up to 7 years in the absence of an appropriate host plant, though most propagules apparently die within 6 months. Moisture causes some propagules to germinate, return to quiescence has been observed in some taxa such as the fine endophyte. Without a living root, the germinated propagules usually die. Some spores of species in the genera Acaulospora and Glomus have a period of dormancy or maturation, prior to attaining the potential to germinate. The length of dormancy is highly variable even within one species in one location. The variation in dormancy may provide species adapted to cultivation the capacity to survive many of the exingencies of cropping.
Interestingly, isolates of one species have been found around the world. Glomus mosseae is cosmopolitan, common in disturbed soil, and genetically similar around the world. The species is easy to isolate from dried root fragments and dried soil. The fungus is readily identified because of the funnel-shaped hyphal attachment. The widespread and apparently recent distribution of this species with cropping indicates that it may be possible to unwittingly reduce diversity of native species and replace them with unselected weedy AM fungi. The consequences of replacement are unclear.
Finally, cropping is extremely unstable and unpredictable. Crops may be sown annually, but the crop species may change according to the rotation. In many parts of Australia, sowing is delayed if insufficient rain has fallen, leading to a longer period of fallow where a host is absent. Further, the soils are commonly cultivated prior to sowing, to remove weeds and prepare a seed bed to maximise seedling emergence. Cultivation shatters the mycelium in the soil, reducing the fungal population measurably. Finally, even once the crop is established, irrigation, fertiliser and pesticides are applied and these may reduce or halt fungal activity temporarily.
The AM fungi in cultivated soils are ruderal or weedy species. We have not compared the functional attributes of “K” and “r” selected AM fungi. Indeed, most laboratory studies of the function of AM fungi have used weedy species. One consequence of this approach is that we have a very sound understanding of the function of AM fungi as weeds, but a poor appreciation of the attributes of fungi which require long periods of establishment and interaction.
One might predict that characteristics that increase over time, such as the rate of development of the hyphal network in soil, will be greater in “K” selected fungi. Thus studies of the aggregation of soil by AM fungi will underestimate the contribution of the fungi because the weedy species that have been used in experiments will direct more energy to reproduction as spores than establishment and maintenance of a mycelium.
This essay has explored one small aspect of the effect of disturbance on arbuscular mycorrhizal fungi. Disturbance is a major contributor to determining fungal diversity and biomass at any one location. The consequences of disturbance on fungi is, in many ways, analogous to disturbance on other organisms. Though only limited measures have been used to consider the issue, the theory surrounding effects of disturbance on plants and animals seems to apply to these fungi.
Falk D.A., Palmer M.A. and Zedler J.B.Eds. (2006) Foundations of Restoration Ecology, SERI,
Zak J.C. Response of soil fungal communities to disturbance. In: The Fungal Community eds GC Carroll and DT Wicklow.