Does soil biodiversity depend upon metabiotic activity and in¯uences?
John Saville Waid
1,*School of Microbiology, La Trobe University, Bundoora, Victoria 3083, Australia
Received 1 May 1998; received in revised form 1 October 1998; accepted 25 February 1999
Abstract
A central tenet of biological science is that living organisms modify their environments. Metabiosis is a form of ecological dependence in which one organism or a functional group of organisms must modify the environment before another organism or functional group of organisms can live or thrive in it. Soil ecosystems are modi®ed by metabionts to create habitats or supply resources for which dependent organisms may adapt, evolve and hence diversify. Thus, the diversity of the soil biota and its functional capabilities may to a large extent be the result of and dependent upon metabiotic activity and in¯uences. Examples of metabiotic activity in soil ecosystems are: plants are the main source of O2 for the soil biota; decomposers
deplete soil O2 thus enabling the growth of microaerophiles or anaerobes; ammonium released by bacterial deamination
supports the growth of autotrophic ammonium-oxidisers; burrowing earthworms improve soil drainage and create aeration channels for aerobic biota; detoxi®cation of plant residues by biodegraders permits proliferation of toxin-sensitive organisms; wood decay by microbes creates habitats for arthropods associated with rotting wood; arthropod comminution of litter liberates nutrients that facilitate microbial activity. Some metabionts, the panmetabionts, had a global in¯uence by modifying the biosphere, its evolving biota and by maintaining its biogeochemistry. For example, during the development of the biosphere the cyanobacteria began the transformation of the atmosphere through the production of O2. The accumulation of
atmospheric O2had an overwhelming in¯uence on the formation of soils, their physico-chemistry and biology, in particular
the evolution of diverse major groups of aerobic terrestrial organisms (plants, fungi and animals). Many practices to improve soil fertility, e.g. agro-forestry, mulching, legume inoculation, minimum tillage are applications of metabiotic techniques, which maintain or improve soil biodiversity and its functional potentiality. Conversely, where ecosystems are degraded through human activity, e.g. forest destruction, irrigation with saline water, strip-mining, deep tillage, there is an inevitable reduction of species of animals and plants. It can also result in the loss of some components of the soil community, e.g. mycorrhizal fungi, macrobiota such as invertebrates, with a consequent reduction in or a loss of the metabiotic activities of functional groups of the soil biota. Types of metabiotic action include facilitation, ecological engineering, commensalism and keystone predation. Metabiosis must rank with biotic interrelationships and interactions, such as competition, predation or mutualism, in its effects upon soil communities and ecosystems.#1999 Elsevier Science B.V. All rights reserved.
Keywords:Metabiosis; Panmetabiosis; Biotic interactions; Biodiversity; Soil ecosystems; Ecological engineers
1. Introduction
Soil is an outstanding example of a natural system where living organisms have and still play a major role in the development of its physico-chemical features. 1Present address: PO Box 760, Buderim, Queensland 4556,
Australia.
*Corresponding author. Tel.: 458-896; fax: +61-754-769-183
E-mail address:jswsbbbud@peg.apc.org (J.S. Waid)
Soils contain a motley medley of habitats occupied by a great diversity of organisms performing an over-whelming variety of functions. Our knowledge of the abundance and functioning of the various components of the soil community and of the range of mechanisms whereby the different soil inhabitants interact with one another is far from complete. Those interrelationships where the effects are direct, such as the trophic mutualistic, parasitic, predatory types of interactions and competition for resources, have been reasonably well investigated (Jones et al., 1994). However, there are a number ofindirecttypes of interrelationships and interactions that have mechanisms and ecosystem functions which also need to be fully elucidated. We need to answer the following questions: Do indirect types of interactions affect biological and functional diversity? If so how? Can the effects of indirect interactions upon biological and functional diversity be measured? Do indirect interactions confer resilience on ecosystem functioning by maintaining the survival of biological diversity and the sustain-ability of an ecosystem when the environment changes?
Characteristically organisms bring about physical and chemical changes to their habitats. These mod-i®cations, whether ephemeral of enduring, alter the environment so that some species are enabled to live and ¯ourish, and others may adapt and evolve to occupy the novel habitats, while others are decimated or fail to grow. Metabiosis is a type of biological action whereby single species or functional groups of organisms create, maintain or modify environments and habitats enabling other species to grow, survive and perhaps evolve. My purpose is to speculate on the possible involvement of metabiosis by modifying or creating habitats in maintaining the biological diver-sity and consequently the functional diverdiver-sity of soil systems.
2. Metabiosis defined
GarreÁ (1887) coined the termmetabiosis, which in The New Shorter Oxford English Dictionary (Brown, 1993) is de®ned as `a form of ecological dependence in which one organism must modify the environment before the second is able to live in it'. This term is used by some microbiologists but rarely by other
biologists. A broader de®nition, more appropriate to ecological situations, is: `a form of ecological dependence in which one organism or a functional group of organisms must modify the environment before the second organism or a functional group of
organisms is able to live or thrive in it' (Waid, 1997).
The organisms responsible for metabiotic changes to the environment are called metabionts. The changes caused by metabionts include physical and chemical modi®cations to habitats on a micro- or a macro-scale. Some changes are momentary, at the other extreme they endure for 109years or more, for example the presence of photosynthetically-derived O2 in the
atmosphere for 2109years or more.
Metabiosis has potential as a useful generic term (analogous to terms such as parasitism, antagonism, mutualism, competition, predation) to describe all non-associative interrelationships between species or groups of organisms where one dependent species or group bene®ts as a result of modi®cations to the environment by the metabiont.
The characteristic features of metabiosis described by Waid (1997) are summarised in Table 1.
Table 1
Characteristics of metabiosis (modified from Waid, 1997)
1.Significance of relationship to the metabiont
*A metabiont can be unaffected, positively affected or negatively affected by its interrelationships with dependent organisms
*The interrelationship may maintain and prolong the existence of the microhabitat, ecosystem or environment in which the metabiont lives
2.Positive and negative effects of metabiosis
*An environment modified by a metabiont may favour some of the organisms or functional groups originally present but the remainder may be disadvantaged
*Some environments modified by metabionts may enable new genotypes to develop, hence promoting diversification
3.Specificity of metabiotic relationships
*Metabiotic interrelationships may be non-specific or specific 4.Spatial relationships of metabionts to dependent organisms
*Varies from close contact to remoteness
5.Timing, duration and scale of influence of metabiotic effects
*Dependent organisms can coexist with, survive or even develop after the death of the metabiont
*The duration of a metabiotic effect can range from a momentary influence to one of 109years or more
3. Origins of metabiosis
The biota of the primitive biosphere would have diversi®ed as the earliest known forms of life, the Archaebacteria and Eubacteria, emerged and evolved. There is no certainty about which organisms colonised the exposed regolith to form the terrestrial biosphere or when these events took place. All possible habitats would have remained anaerobic until the atmosphere had become enriched with O2derived from oxygenic
photosynthesis. The anaerobic biota occupying primi-tive ecosystems probably consisted of distinct groups, such as anaerobic chemolithotrophs deriving energy from hydrogen oxidation, sulphate reduction, aceto-genesis or methanoaceto-genesis; anaerobic phototrophic bacteria and; anaerobic chemorganotrophs consuming organic compounds formed abiotically or by the biosynthetic activities of the chemolithotrophs and phototrophs.
One can only speculate about the possible types of interrelationships that developed among the earliest biochemical groups of bacteria that evolved. No doubt competition for organic nutrients would have been intense. Yet, the emergence of predatory, parasitic or mutualistic organisms might have taken considerable time. But the organic and inorganic chemistry of the primitive biosphere would have been undergoing con-stant change because of the emergence of an ever broadening range of new strains of bacteria with novel biochemical capabilities. It is conceivable that the bacterial communities would have been challenged by the accumulation of new organic substrates to exploit, toxic metabolites to detoxify or acquire resis-tance to and new electron acceptors and donors to utilise. Also new potential habitats and niches would have been created as a result of bacterial action, e.g. pH and redox changes, detoxi®cation of inorganic substances. Thus, changes to the environment brought about by pioneer strains of anaerobic bacteria might have enabled new strains to evolve to exploit the newly-formed habitats. In other words, metabiosis may have been a very potent type of interrelationship even among the earliest forms of bacteria.
Lynn Margulis (1998) pointed out that the conven-tional notion that `soil biota began to diversify when plants began to accumulate perennial biomass' is ill-conceived. Her statement does not deny such plants have had a considerable in¯uence on the diversity of
the soil macrobiota and plant symbionts. However, the ®ndings of Torsvik et al. (1990), Tiedje and Zhou (1996) and Tiedje et al. (1999) have revealed that the diversity of soil bacteria is overwhelmingly high. This suggests that the diversity of the precursors of the bacterial component of the extant soil biota increased considerably in the ca. 3.1109 years from when bacteria ®rst emerged to the time when land-dwelling perennial plants appeared in the fossil record (ca. 0.6109years ago). Such diversity may have devel-oped from the successive effects of metabiotic inter-relationships among the inhabitants of primitive ecosystems and later on in soil ecosystems before perennial land plants had emerged. The extreme age of the Archaebacteria and the Eubacteria may account for the considerable resilience and adaptability of extant free-living bacteria in all soil ecosystems studied.
4. Panmetabiosis
Those metabionts having a global in¯uence, e.g. oxygenic photosynthesizers, chemolithotrophs, nitro-gen-®xers, denitri®ers and methanogens, through modifying the biogeochemistry of the biosphere are named panmetabionts (Waid, 1997). The oxygenic photosynthetic bacteria (cyanobacteria, `blue green algae') appeared ca. 3.7109 years ago. At ®rst the O2they evolved accumulated in geological
for-mations, then in the oceans and the atmosphere, where the ozone shield was formed. Schlesinger (1991) has described the release of O2to an anaerobic Earth as
`perhaps the strongest reminder we have for the in¯uence of the biota on the geochemistry of the Earth's surface'. It resulted in the oxidation and the detoxi®cation of hazardous reduced forms of many metallic elements, e.g. conversion of Fe2
to Fe3
, which became immobilised in geological formations. It permitted the development of organisms possessing biochemical pathways utilising O2, i.e. the aerobic
photosynthesi-zers, who appeared ca. 1.3 to 2.0109 years ago. Thus, the presence of O2has had an enduring in¯uence
on the formation of soils, their physico-chemistry, biology and pedology. Indeed, it is possible new forms of life evolved, and hence an increase in biochemical diversity, during a succession of panmetabiotic events, e.g. CH4production, SO42
ÿ
reduction, O2production
through oxygenic photosynthesis and culminating in the formation of the ozone shield, thus causing major changes to the biosphere and permitting evolving groups of organisms to colonise land.
5. Metabiotic interactions in soil ecosystems
Microbiologists culturing mixtures of microorgan-isms encounter metabiosis (sensuGarreÁ, 1887) when strains fail to grow unless the deliberate or accidental presence of other strains alters the culture vessel environment to favour the growth-retarded strains. Metabionts may enrich the culture medium with essential growth factors, alter the medium pH or, lower the O2tension, thereby creating environments
more favourable for dependant organisms. Examples of analogous metabiotic interactions are found within the ecological context of soils where, respectively, rhizosphere microorganisms depend upon growth fac-tors derived from roots; plants and microorganisms bene®t from reductions to soil pH caused by the acid-forming activities of autotrophic S-oxidising bacteria and; microaerophiles and anaerobes bene®t from reductions in soil O2concentrations caused by
respir-ing aerobic organisms.
The examples of metabiosis mentioned so far are indirect and non-speci®c interrelationships between the metabionts and the dependent organisms. How-ever, in soil ecosystems there are numerous examples of speci®c metabiotic dependency involving nutrient transformations, e.g. the nutritional-dependency of NH4
-oxidisers for CH4 formed by methanogens;
S-oxidising thiobacilli for reduced inorganic S com-pounds (e.g. H2S) formed by anaerobic
microorgan-isms and; Desulfovibrio and other SO4 2ÿ
-reducing microorganisms for SO42ÿformed by aerobic
micro-organisms (Waid, 1997). Interestingly, such metabio-tic activity, e.g. the formation of metallic sulphides, may precede the need of the dependent organisms for a prolonged period. Also, the interacting pairs of
organ-isms or functional groups do not necessarily occupy the same microhabitat or a similar ecological niche, e.g. methanogens and methanotrophs.
6. Metabiotic interactions resulting in increased biodiversity
Usually there is no apparent direct or immediate effect of metabiotic activity upon the metabiont; only the dependent organisms bene®t. Metabiotic activity triggers changes to the biodiversity of discrete soil microhabitats. For example, organic compounds are released during wood decomposition by lignocellu-lose-degrading white- and brown-rot fungi. These carbon sources support the development of a commu-nity of non-lignin or non-cellulose degrading fungi and bacteria. Such a community in time becomes associated with a diversity of consumers and preda-tors, e.g. myxomycetes, protozoa, nematodes, mites, collembola, nematode-trapping fungi etc. The initial metabiont (a wood-rot fungus) creates new but ephem-eral habitats for a diverse range of organisms, e.g. wood decay creates habitats and refuges for pods. Some of the dependent organisms, e.g. arthro-pods, nematodes and protozoa, function as metabionts. Arthropod comminution of the wood residues and the grazing of bacteria by protozoa and nematodes liberates facilitating microbial activity. The arthropods grazing mycelium often disperse fun-gal propagules or hyphae to new resources. This complexity of events is an example of facilitation, an ecological process, where one species in a succes-sional pathway improves conditions for the survival and growth of other species. The conceptual similarity of facilitation to metabiosis suggests it is a type of metabiosis.
Various strains of soil microorganisms, particularly bacteria, are involved in the detoxi®cation of natu-rally-formed toxic inorganics (S2ÿ
, NO2
ÿ
, NH4
) or the decomposition of organic compounds (hydrocar-bons, phenolics, terpenes, antibiotics) and some strains can adapt to degrade xenobiotics. Such meta-biotic activities permit toxin-susceptible plants and soil biota to survive or grow in the affected soils.
E.P. Odum (1969) stated that `ecological succession
com-munity-controlled even though the physical environ-ment determines the pattern, the rates of change, and often sets limits as to how far development can go'. Young and Ritz (1998) have developed an argument to show that in soil systems structural heterogeneity becomes as important as biological heterogeneity, i.e. biodiversity. However, current methods to quantify biological diversity and to identify the nature of inter-speci®c interactions in niche habitats in soil do not place the biological community in the spatial context of heterogeneous soil. As a result the link between the quanti®cation of organisms, their interactions with one another and the functioning of biodiversity in soil remains weak.
Many macroorganisms function as metabionts by altering the physical state of biotic or abiotic materials of soil habitats to favour the growth of other organ-isms. The processes and the organisms responsible for the physical modi®cation, maintenance and creation of habitats were called ecosystem engineering and ecosystem engineers, respectively, by Jones et al. (1994). Lawton (1994) de®ned ecosystem engineers `as organisms that directly or indirectly modulate the availability of resources (other than themselves) to other species, by causing physical state changes in biotic or abiotic materials. In doing so they modify, maintain and/or create habitats'. The conceptual simi-larity to metabiosis suggests that ecosystem engineer-ing is a type of metabiosis. Channels formed by decayed roots, earthworms burrows, voids formed by termites and the burrows of mammals provide ventilated and well-drained habitats and migratory channels for the soil microfauna and aerobic micro-¯ora. The burrowing, mixing and casting by earth-worms have considerable in¯uence upon the mineral and organic composition of soils, nutrient cycling, soil hydrology and drainage. Many termite species relo-cate detritus in the litter-soil pro®le and some of these transfer organic debris to habitats or nests creating environments favouring the growth of lignocellulose-degrading microorganisms. The elimination of such non-microbial metabionts (plants, macroarthropods, earthworms etc.) by soil management practices diminishes the diversity of the macrobiota but prob-ably impinges less severely upon the diversity and functional potential and activity of the microbiota (protozoa, bacteria, fungi etc.) surviving in microha-bitats or refuges, or persisting in a dormant state.
7. Human influences on soil biodiversity
Perhaps the major driving force for biodiversity in soil is the type, amount and chemical composition of the vegetation it supports because plants are the major source of the energy and organic nutrients on which the soil biota depends. Living vegetation also exerts spatially-remote effects on the physical environment in which soil organisms dwell. Examples of such effects given by Holling (1992) included vegetation in¯uencing litter layer types and depths, plant cover dampening temperature ¯uctuations in the surface soil and also reducing moisture loss rates from the soil surface. The presence of dead vegetation prolongs such metabiotic effects of the vegetation on soil communities but these cease once the land had been cleared of live plants or their residues.
Plants undoubtedly have a marked in¯uence on the structural and functional diversity of the soil macro-biota (earthworms, termites, other arthropods, etc.) and the replacement of natural vegetation by crops, especially continuous monocropping, may alter the composition and reduce the biomass of the microbiota. It is not clear if either the species diversity or func-tional diversity of the microbiota is reduced following the conversion of long-standing vegetation to a crop-ping regime other than for the possible loss of micro-organisms forming associations with plants or animals, e.g. symbionts and other associates.
Humans improve soil fertility by modifying the soil, e.g. sowing inoculated nitrogen-®xing legumes, plant-ing mycorrhiza-inoculated trees, addplant-ing fertilisers or nutrient-rich plant or animal residues, improving soil drainage, altering soil pH. These management prac-tices are the application of metabiotic techniques to the soil whereby it is modi®ed so that its functional diversity is altered by promoting certain biological activities (organic residue decomposition, nutrient assimilation or mineralisation, N2-®xation,
nitri®ca-tion, soil aggregation) or to check `negative' activities (denitri®cation, NH3 loss, build-up of plant
to diversify by adapting to degrade the xenobiotics, e.g. 2,4-D decomposing bacteria, or to tolerate them, e.g. DDT-tolerant invertebrates.
Kundu and Ladha (1995) showed how soil manage-ment affected soil functioning, and seemingly affected soil biodiversity, in intensely-cultivated wetland-rice soils where crop productivity and non-symbiotic bio-logical N2-®xation (BNF) have declined and fertiliser
N is required to maintain productivity. In continu-ously-wet soils shallow tillage (ca. 15±20 cm) can result in the formation of hard pans, which rice roots cannot penetrate to use sub-soil N. The concentration of O2 in the sub-soil declines because there is less
percolation of water to transport dissolved O2and also
no O2 input from living rice roots. The amount of
mineral N in the anoxic sub-soil decreases as there is no O2to support BNF by microaerophilic N2-®xation.
Rice plant residues accumulate in the ¯ooded plough layer and decompose under reducing conditions so that phytotoxic substances are formed. These include numerous organic substances as well as Fe2
, NO2
ÿ
and S2ÿ
, each of which adversely affect BNF organ-isms. This is a situation where the metabiotic in¯u-ences of the oxidising rhizosphere region of the rice and the input of rice root litter to the sub-soil micro-¯ora of N2-®xers and litter decomposers have been cut
off. In turn, the metabiotic in¯uences of microorgan-isms mineralising organic-N and the N2-®xers on the
rice plants have been suppressed or diminished in the sub-soil and the ¯ooded plough-layer, respectively. The volume (depth) of soil exploited by rice roots decreases as the hard pan forms. In the non-tilled soil beneath the pan the diversity of the active aerobic microorganisms would presumably decrease as it becomes anoxic. Microorganisms residing in an inac-tive state in the anoxic layers might survive and become reactivated once the soil conditions return to an aerobic state, e.g. following deep ploughing, or the soil below 20 cm might be recolonised by aerobic organisms through migration from the more aerobic surface soil resulting in a recovery of the overall functional and biological diversity of the microbial community.
Methanotrophs consume atmospheric CH4the
sec-ond most important greenhouse gas. Some ecosys-tems, e.g. undisturbed mature forests, wetlands, have the capacity because of the presence of methano-trophic communities to destroy CH4. For example,
Watson et al. (1997) have demonstrated a metabiotic role for plants growing on anaerobic peats by their ability to maintain an oxic rhizosphere by extruding O2from their root tips enabling active CH4oxidation
by methanotrophs inhabiting the peat. The extruded O2also diminished in situ CH4formation by
metha-nogens, which increased in rate following the removal of the plants from the peat. In cropped dryland soils, the CH4-oxidising activity of the methanotrophs is
susceptible to soil disturbance, e.g. clear-cutting, crop cultivation, drainage, N fertilisation, which can reduce, perhaps destroy, the methanotrophic activity of soil (HuÈtsch et al., 1994). The survival of metha-notrophic soil communities in undisturbed forest soils could depend on metabionts modifying or maintaining conditions in the soil environment to favour the growth and activity of methanotrophs, e.g. aerobic conditions, well-structured soil, continuous inputs of litter. An understanding of such metabiotic interactions might assist the quest to conserve or increase the CH4
-oxidising activity of soil.
8. Examples of metabiosis contributing to the biodiversity of ecosystems other than soils
Menge (1995) analysed experimentally-based stu-dies of direct and indirect effects in interaction webs in marine rocky habitats. Many of the interactions stu-died by Menge as direct or indirect effects can be considered to be metabiotic (Waid, 1997) and con-tribute to the biodiversity of the ecosystem studied,
e.g.direct effects: enhancement of recruitment,
provi-sion of habitat and shelter; indirect effects: keystone predation, trophic cascades, indirect mutualism, indir-ect commensalism and habitat facilitation. Indirindir-ect effects accounted for ca. 40% of the changes in community structure and of these keystone predation, where a predator indirectly increases the abundance of the competitors of its prey via consumption of the prey, was the most common (35%) of the indirect effects.
nutrient interactions involve transformations of N and S compounds by speci®c functional groups of micro-organisms, similar to those functional groups operat-ing in soil ecosystems. These interactions, many of which can be classed as metabiotic, continuously create new microbial niches that are quickly ®lled from the resident pool of rare and `cryptic' (and probably cosmopolitan species). Finlay et al. (1997) suggest that `microbial diversity has no discrete role to play with respect to ecosystem function. Reciprocal interactions between microbial activity and the phy-sical-chemical environment create a continuous turn-over of microbial niches that are always ®lled, so microbial diversity is a part of ecosystem function'.
9. Conclusions
The term metabiosis does not describe the numer-ous mechanisms whereby metabionts modify envir-onments for the bene®t of dependent organisms or for species to diversify. A plethora of possible mechan-isms of this type, which may be sub-categories of metabiosis, have been named and described but with some of these mechanisms there are varying de®ni-tions or interpretade®ni-tions of their meaning and how they operate under natural conditions (Callaway, 1998). The candidate list of these phenomena includes: commensalism (indirect, nutritional or physical); eco-logical engineeringphysical commensalism?; `indirect mutualism'; facilitation; priming of sub-strates; comminution; dissemination, e.g. dispersal of spores; `apparent predation'; keystone predation; `enemies' enemy'; facultative mutualism (protocoo-peration, synergism) and so on (Brock, 1966; Boucher et al., 1982; Atlas and Bartha, 1987; Moore, 1988). It would not be appropriate in the context of this paper to discuss this matter further but these terms do need to be standardised to avoid confusion.
Metabiosis is a term embracing a spectrum of commonly-observed types of biotic interactions in ecosystems, which involve modi®cations brought about by organisms to the physical, chemical or nutritional status of the environment. Research may establish that at sometime during their life cycles, or thereafter, a large proportion of soil organisms act as metabionts and modify soil habitats so other organ-isms are able to live, thrive or evolve in them and in
doing so conserve or increase the biological diversity of soil and its functional capabilities.
It would be useful and convenient for biologists to have a single ®ve-syllable single-word descriptor, i.e. metabiosis, to include all non-associative
interrela-tionshipswhereby organisms must modify the
envir-onment before the second organism or a functional group of organisms is able to live, thrive or evolve. As this ready-made term has been in existence for over a century (GarreÁ, 1887; Brown, 1993; Waid, 1997), apparently uncorrupted by over-use or misuse, there seems to be no obvious reason why it should not be considered for adoption as a standard and, thus avoid any confusion with less suitable terms.
Acknowledgements
I thank two anonymous referees for critical and constructive comment.
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