Brussaard 1997
Brussaard 1997
Brussaard 1997
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564 ? Royal Swedish Academy of Sciences 1997 Ambio Vol. 26 No. 8, Dec. 1997
http://www.ambio.kva.se
subseun
X.:
- X
X h (:-'METAYGAIG
ICROFAUNA)
todesb and
proo to zoans.::'::::':::IROAN
r... ..........
n RDTO
COMLEIONOFby :::.:
.::::::::HUMIICATON .:.::::::::::::..........succlitertIrYandfo
ssios..:k....1 gazer
Phytophagous Collembolans
Nematodes
FOLIAR Pdcous
HERBIVORES Cryptostigmatic Miles
Roots Mites\ .
Earthwoseceous
DECOMPOSERS Detritus e toe
BIOTURBATORS Bcteophagous
Nematodes -
_
Figure2. Conceptualdiagramof an interactionweb,
showing the mainspheres of influenceof the biota in soil,
interactingwith plants directly(continuousarrows)or CFlagebllaes Amba |
indirectly(hatchedarrows)(60). B ^acMohgus__
Ambio Vol. 26 No. 8, Dec. 1997 ? Royal Swedish Academy of Sciences 1997 565
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Group Functions
Free-living bacteria Elemental immobilization; elemental mineralization; mutualistic intestinal associations; resource for grazing animals;
genesis of biofilms; plant growth promoters; helpers in mycorrhizal associations; pathogens of plants; parasites and
Rhizobial bof soil animals; synthesis of humic materials; soil aggregation; decomposers of agrochemicals and xenobiotics
Rhizobial bacteria N2-fixing plants given competitive advantage; resource for root-feeding nematodes and other animals
Non-mycorrhizal fungi Elemental immobilization; elemental mineralization; mutualistic and commensal associations;
resource for arthropods and protozoan and nematode grazers, and for some other fungi; redistribution of
nutrients; conditioning of detritus; parasites of arthropods and nematodes; synthesis of humic materials;
soil aggregation; decomposers of agrochemicals and xenobiotics
Mycorrhizalfungi Mycorrhizal plants given competitive advantage by the following mechanisms: mediation of transport of
essential elements and water from soil to plant roots; mediation of plant-to-plant movement of essential elements and
carbohydrates; sequestration of essential elements present in forms not available to plant; regulation of water and ion
movements through plants; regulation of photosynthetic rate of plants;
regulation of C allocation below ground; decreased seedling mortality;protection from root diseases and root herbivores.
Genesis of root mycosphere for bacteria; high-quality resource for mesofaunal and microfaunal grazers
Protozoa Grazers of bacteria and fungi; enhance microbial growth; enhance C and N availability to higher trophic levels; key
components of microbial-loop systems; prey for nematodes and mesofauna; host of bacterial pathogens; parasites of
higher-level organisms
Nematodes Grazers of bacteria and fungi; enhance C and N availability to higher trophic levels; disperse
bacteria and fungi; root herbivores / plant parasites; parasites / predators of microfauna, mesofauna
and insects; prey for meso- and macrofauna
Mites Grazers of bacteria and fungi; consumption of plant litter and animal carcasses; predators on nematodes and insects;
root herbivores; dispersal of microorganisms; dispersal and vectoring of helminth parasites; host for protozoan parasites;
parasites and parasitoids of insects and other arthropods; prey for macrofauna; micro-ecosystem engineers
Insects-General Grazing of rhizosphere microorganisms; dispersal of microorganisms; predators of other soil organisms; decomposers of
plant and animal matter;
Insects-Root herbivores Modification of plant performance below ground by root herbivory (modification of plant performance above
ground by root herbivory and modification of herbivore populations above ground through changes in plant physiology
resulting from herbivory below ground)
Insects-Collembola Grazing of microflora and microfauna especially in rhizosphere; consumption of plant litter and
animal carcasses; micropredators of nematodes, tardigrades, rotifers; dispersal of microorganisms; dispersal of helminths
and cestode parasites; host for parasites; prey for macrofauna ; microecosystem engineers
Insects-Ants Bioturbators; enhancement of microbial growth; keystone species for inquilinous fauna and plants associated with anthills
Insects-Termites Bioturbators; enhancement of microbial growth; keystone species for inquilinous microorganisms and fauna and plants
associated with mounds
Enchytraeids Fragmentation of plant litter;enhancement of microbial growth; bioturbators; dispersal of microorganisms
Earthworms Bioturbators; enhancement of microbial growth; dispersal of microorganisms and algae; host of protozoan and other
parasites
grams. Based on estimates of reannealingof soil DNA, Torsvik It is estimatedthatonly 5% of living fungi have been described
et al. (9) suggested 4000 independentbacterialgenomes in 1 g (11). The wide rangeof estimates(18 000-35 000 species of soil
of forest soil. Accounting common genes, the bacterialspecies fungi) is caused by the fact that it is unknownhow many of the
definition, and extrapolationto rarespecies, this would amount approximately72 000 described fungi are restrictedto above-
to perhaps20 000-40 000 bacterialspecies in 1 g of soil (10). ground plant parts. Fungi forming macroscopicalfruiting bod-
The gap in knowledge is very apparentif this number is com- ies can often be identified in the field in temperateand boreal
paredto describedbacterialspecies; 4100, most of which are not forestsand many partialinventoriesexist. The mycorrhizalfungi,
soil inhabitants.The situation is even more primitive for soil i.e. fungi forming mutualistic associations with plant roots,
archaeain which only a few methanogensand methylotrophsare presentuniqueproblems.The arbuscularmycorrhizal(AM) fungi
known,but DNA analysis suggests many more types are present. are probablyamongstthe commonestfungi on earth.Many spe-
Certainfunctional groups of bacteriaare importantin cycles cies seem to have a very wide distribution,but species concepts
of specific elements. Althoughthereis considerableredundancy need to be reassessed by modem methods and adequateknowl-
among bacteria for these processes, e.g., N2 fixation, there is edge is available only for agriculturaland similar soils and eco-
growing recognition that there is considerable diversity at the systems. The ectomycorrhizalfungi show a much higher degree
kinetic, physiological, or niche level that is of importanceto the of specificity comparedto the AM fungi (12). Many of them can
process. It is this diversity that may be very importantto eco- be classified as macrofungi,and will thus be included in the in-
system functioning.The main functional groups, listed accord- ventoriesmade by classical fungal taxonomists,but are difficult
ing to the pertinentelement, are: to identify in the soil when not forming aerialfruit bodies.
Carbon: autotrophs;heterotrophs;methanotrophs,methylo- DNA techniques for identification of fungi, including my-
trophs;methanogens. corrhizalfungi that do not form fruitingstructuresare currently
Hydrogen:H2oxidizers;H2producers;butyrateoxidizers;pro- being developed, but with so many species involved this will
pionate oxidizers. take some time. Direct studies on DNA extractedfrom soil are
Nitrogen: N2fixers; denitrifiers;nitrifiers;DNRA (dissimila- not yet applicable.
tory nitrateto ammoniareducers);mineralizers;immobilizers.
Sulfur:sulfuroxidizers; S02- reducers. Protozoa
Iron: Fe2+oxidizers; Fe3"reducers. Protozoa are microscopically small,
unicellular organisms. It is assumed
Fungi that only 10% of soil protozoansare
Fungi are involved in a large known (13). Vickerman (14) sug-
number of mutualistic and other gested that the total number of spe-
organismalinteractionsin soil. The cies is close to 40 000. Protozoa are,
division between mutualistic and with nematodes,the principalmicro-
otherfungi is not clear, since fungi bial grazersin terrestrialsystems (15).
are part of many complex ammensal,commensal and competi- By classifying protozoabased on feeding preferences(bacterial
tive relationshipswith other soil organisms. Saprotrophicfood or fungal), habitat preferences (acidophilic or neutrophilic)or
chains involving fungi and other organisms may be also ecological weightings, it may be possible to relate changes in
mutualistic,but these relationshipsare poorly understood. diversity and/orbiomass to ecosystem functioning(16).
566 ? Royal Swedish Academy of Sciences 1997 Ambio Vol. 26 No. 8, Dec. 1997
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Ambio Vol. 26 No. 8, Dec. 1997 ? Royal Swedish Academy of Sciences 1997 567
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CONCLUDINGREMARKS
Except for a few studies, most researchrelated to the diversity
and functionalrole of differentgroupsof soil organismshas been
done for small assemblagesof species. More comprehensivedata
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Corresponding author: LijbertBrussaard is professor of soil VadakattuV.S.R. Gupta is a research fellow at the
biology at Wageningen AgriculturalUniversity. His research Cooperative Research Centre for Soil and Land
interests include rhizosphere ecology; the role of soil fauna Management in Adelaide, Australia. His research interests
in decomposition processes and nutrient cycling; and the include microbial interactions and their impact on the
relationships between belowground/ aboveground turnover of carbon and nutrients, and the survival of
biodiversity, and ecosystem functioning in naturaland agro- introduced bacteria, special emphasis on protozoan-
ecosystems. His address: Wageningen Agricultural microfloralinteractions. His address: CRCfor Soil and Land
University Dept. of EnvironmentalSciences, Soil Biology Management, PMBNo. 2, Glen Osmond, South Australia,SA
Group, Bornsesteeg 69, 6708 PD Wageningen, The 5064. Australia.
Netherlands. Tsutomu Hattori'smain research interests include the
Val M. Behan-Pelletier is a scientist with the Research phylogenetics and morphology of soil oligotrophic bacteria,
Branch of Agricultureand Agri-Food Canada in Ottawa. Her the diversity of protozoa in soil microaggregates and the
research interest is the systematics, biogeography and stochastic aspects of bacterial proliferationand protozoan
ecology of oribatid mites (Acari).Her address: Biological excystment in soil. His address: Attic Lab, Komegafukuro
Resources Program, ECORC,Agricultureand Agri-Food 1-6-2-401, Aoba-Ku,Sendai 980, Japan.
Canada, K.W.Neatby Bldg., Ottawa, Ontario,Canada K1A David L. Hawksworthis the Directorof the CAB
0C6. InternationalMycological Institute in the UK.His address is:
David E. Bignell is associate professor in the Tropical InternationalMycological Institute, Bakeham Lane, Egham,
Biology and Conservation Unit, Universiti Malaysia Sabah. Surrey TW209TY, UK.
His interests span all aspects of termite biology, but Carole Klopatekis currentlyworking at the National
especially their nutritionalecology and role in soil Belowgraound Sustainability Program, USDAForest
ecosystem processes. His current address: Tropical Service, PO Box 96090, Washington DC 20090-6090. Her
Biology and Conservation Unit, Universiti Malaysia Sabah, address: Departmentof Microbiology, USDAForest Service,
Kampus Jalan Tuaran, Kilometer 19 Jalan Tuaran,88999 Arizona State University, Tempe, AZ 85287, USA.
Kota Kinabalu,Sabah, Malaysia. His permanent address:
School of Biological Sciences, Queen Mary&Westfield Patrick Lavelle is professor of ecology at Universite de
College, University of London, London El 4NS, UK. Paris VIand Directorof Laboratoired'Ecologie des Sols
Tropicaux at ORSTOM(Institut Francais de Recherche
Valerie K. Brown is Directorof the InternationalInstitute of
Scientifique pour le Developpement en Cooperation). His
Entomology. Her research interests are in experimental research interests include general soil ecology with a
community ecology, with particularinterests in the special emphasis set on earthwormecology and their
interactions between plants and soil-dwelling insects under management as part of sustainable practices in tropical
environmental change. Her address: InternationalInstitute
of Entomology, CAB International,56 Queen's Gate, London environments. His address: LEST/ORSTOM, 32 rue H.
Varagnat,93143 BONDYcedex, France.
SW7 5JR, UK.
David W. Malloch is in the Departmentof Botany at the
Wim Didden is assistant professor of soil biology at the
AgriculturalUniversity, Wageningen. His research interests University of Toronto. His research is centered on fungal
life histories, particularlythose intersecting life histories of
include carbon and nutrientflows in terrestrial ecosystems,
and the interactions of soil structure and soil biota, with other organisms. Other research includes taxonomy of
higher fungi and biology of Penicillium species occurring in
emphasis on the ecology of oligochaeta. His address: indoor environments. His address: Departmentof Botany,
AgriculturalUniversity, Dept. of EnvironmentalSciences,
Soil Biology Group, Bornsesteeg 69, 6708 PD Wageningen, University of Toronto, Toronto, Ontario,Canada, M5S3B2.
The Netherlands. Josef Rusek is Director of the Institute of Soil Biology,
Patricia Folgarait is a researcher from CONICET,Buenos Academy of Sciences of the Czech Republic at Ceske
Budejovice. His research interests include the ecology and
Aires, Argentina. Her research interests include ant
taxonomy of soil fauna, especially Collembola and Protura,
biodiversity and ecology in naturaland agro-forestry and its role in soil. His address: Institute of Soil Biology, Na
systems, biological control of ants, and soil biodiversity and sadkach 7, 370 05 Ceske Budejovice, Czech Republic.
functioning with special emphasis on mechanisms
maintaining soil fertility. Her address: IFEVA,Facultad de Bengt Soderstrom is in the Departmentof MicrobialEcology
Agronomia, Universidad de Buenos Aires, Avenida San at Lund University. His research interests include
Martin4453,1417 Buenos Aires, Argentina. mycorrhizalformation, plant-fungus interactions,
Carlos Fragoso is in the Institute of Ecology in Xalapa, environmental effects on mycorrhizalfunction and soil
Mexico. His research interests include the ecology of processes and structure/function relations in mycorrhizal
tropical earthworm communities, the taxonomy and systems. His address: Dept. of MicrobialEcology, Lund
University, Ecology Building, S-223 62 Lund, Sweden.
biogeography of eathworms and the influence of soil
macrofauna on soil fertility. His address: Laboratoriode James M.Tiedje is at the Centre for MicrobialEcology at
Suelos, Instituto de Ecologia, 2.5 km Antigua Carreteraa MichiganState University. His address: Centre for Microbial
Coatepec, AP 63, 91000 Xalapa, Ver, Mexico. Ecology, MichiganState University, 540 Plant and Soil
Diana Wall Freckman is director of the NaturalResource Science Building, East Lansing, Ml48824-1325, USA.
Ecology Laboratoryat Colorado State University. Her main Ross A. Virginiais Professor of EnvironmentalStudies at
research interests are the impact of environmental change DartmouthCollege. His research interests are focused on
on soil biodiversity and ecosystem processes, particularly understanding the impacts of humans on biogeochemical
the role of soil nematodes in biogeochemical processes. cycles, with an emphasis on soil biota and carbon and
Her address: NaturalResource Ecology Laboratory, nitrogen cycling in arid ecosystems of temperate and polar
Colorado State University, Fort Collins, CO 80523-1499, regions. His address: EnvironmentalStudies Program,
USA. DartmouthCollege, Hanover, NH03755, USA.
570 C Royal Swedish Academy of Sciences 1997 Ambio Vol. 26 No. 8, Dec. 1997
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