Interactions

Underground
Soil biodiversity,mutualism,and ecosystemprocesses

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Diana H. Wall and John C. Moore

biodiversity
Soilsiderable hasreceivedcon- late from knowledge of sister species
-

attention be-
recently living above ground to devise ways
cause of greater recognition that Whole assemblages of to sustainably manage soils. As is
soil species and their interactions
belowground species may generallythe case for organismsthat
can influence a number of ecosystem inhabitsubsurfaceenvironments,the
processes (e.g., decomposition, net be necessary for coupling diversity of soil organisms is poorly
primary production, and trace gas known relative to that of organisms
production; Setala and Huhta 1991, the aboveground- that live above the surface, in part
Freckman et al. 1997, Naeem and Li because of the difficulty in extract-
1997, Groffman and Bohlen 1999). belowground nutrient ing and identifying organisms from
Recent scientific research on soil soil, and in part because diversity
biodiversity is increasing our baseline cycle and abundancevarygreatlywith soil
knowledge of the species richness habitat (Blairet al. 1996, Brussaard
(Lawton et al. 1996) and global dis- nary studies are focused on the spe- et al. 1997). Soil habitats differ con-
tribution (Brussaard et al. 1997, Wall cies that are critical for the mainte- siderablyin size and type (e.g., sand,
and Virginia in press) of soil organ- nance of ecosystem processes. The silt, or clay) of the soil particles; in
isms and of their economic value to information from such studies will the amount and flow of water and
ecosystems (Pimentel et al. 1997, contribute to future management of gases in soils; in the amount and type
Vitousek et al. 1997). This research soils and ecosystems under scenarios of carbon (e.g., roots or dead or-
has also identified gaps in our knowl- of increasing human-derived physi- ganic matter), which is a base of the
edge, such as the nature and extent cal, chemical, and biotic disturbances soil food chain; and in chemical fac-
of the linkages among belowground (e.g., plowing, pollution, elevated tors (e.g., salinity and pH) that inter-
systems (i.e., soils, freshwater sedi- CO2, and invasive species; Vitousek act with the organisms.
ments, and marine sediments; Freck- et al. 1997, Jones et al. 1998). The The apparent distribution and
man et al. 1997, Wagener et al. 1998). elucidation of soil biotic interactions, abundance of soil organisms is also
These increasingly interdiscipli- in particular mutualistic interactions, influenced by the spatial scale of
which we highlight in this article, studies of soil biota. Many species
Diana H. Wall (e-mail: diana@nrel.
offers additional evidence for the occur only in microsites around soil
colostate.edu),formerlyFreckman,is the importance
of soil biodiversity at the particles, whereas others have a
directorof the NaturalResourceEcology species and functional levels in the broader habitat distribution, mov-
Laboratoryand a professorin the depart- maintenance of ecosystem processes. ing through meters of soil vertically
ment of RangelandEcosystemScienceat or horizontally (Elliott et al. 1980).
Colorado State University,Fort Collins, The diversity of Soil ecosystems vary considerablyin
CO 80523. Shestudiessoil nematodeecol- species richness (Brussaard et al.
ogy in managedand extremedesert eco- organisms
in soils
1997). For example, nematode di-
systems.JohnC. Moore(e-mail:jcmoore@ An estimated 170,000 species of soil versity ranges from at least 374 spe-
bentley.unco.edu)is a scientistat theNatu- have been identified (Wall cies in the soils of a Cameroontropi-
ral ResourceEcology Laboratory,and a organisms
professorin the departmentof Biological
and Virginia in press). Table 1 shows cal forest (Lawton et al. 1998) to
Sciences, University of Northern Colo- the percentage of the described spe- three species, all endemic,in the soils
rado, Greeley, CO 80639. His research cies globally that have representa- of the Antarctic Dry Valleys (Freck-
focuseson soil food webs and linkagesto tives in soils; for some groups, the man and Virginia 1991). Global
ecosystem processes. ? 1999 American only habitat is the soil environment. biogeographicaldistributionsof spe-
Instituteof BiologicalSciences. Thus, it is not possible to extrapo- cies are better known for the larger

February 1999 109

University of California Press

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Table 1. The number of species in soils, ordered according to body width (Swift et al. 1979).a

Percentageof global
Described species described species that
Body width Taxonomic group in soilb (x 1000) Reference are found in soilc
1-2 am Bacteriad 1.7 Akimovand Hattori 1996, 49-66
Brussaardet al. 1997
3-100 gm Fungi 18-35 Brussaardet al. 1997 48
5-120 gm Nematoda (roundworms) 5 Brussaardet al. 1997 20
15-100 gm Protozoa 1.5 Brussaardet al. 1997 3.8
80 gm-2 mm Acari (mites) 20 David Walter,personal 66
communication
30 Brussaardet al. 1997
150 gm-2 mm Collembola(springtails) 6.5 Brussaardet al. 1997 ?
300 gm-1 mm Diplura 0.659 Ravlin 1996 100
0.8e Maddison1997

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500 gm-4 mm Symphyla 0.16f Scheller1982b 100
500 jm-1 mm Enchytraeidae(pot worms) 0.6 Brussaardet al. 1997 100
500 gm-4 mm Isoptera(termites) 1.6 Bignelland Eggleton1998, 61
David Bignell,personal
communication
Formicoidea(ants) 8.8 Brussaardet al. 1997 63
2-20 mm Isopoda (sowbugs, 5 Brusca1997 50
pillbugs)
1-50 mm Chilopoda(centipedes) 2.5g Hoffman 1982 100
Pauropoda 0.5h Scheller1982a 100
Diplopoda (millipedes) 10i Hoffman 1990 100
Oligochaete(earthworms) 3.627 Brussaardet al. 1997 82
Dipteralarvae(flies, 60i McAlpine1990 50
blackflies)

aModified from Wall and Virginia (in press).
bSpecies in litter and decaying logs are included in the estimate of soil-
dwelling species.
cBased on highest estimates in Wall and Virginia (in press).
dBacteria estimates do not include estimates of genetic diversity using
molecular techniques.
eThe majority of Dipluran species are found in soil (Maddison 1997);
thus, the number of described soil-dwelling Diplura is assumed to be
equal to the total number described.
fSymphyla live in soil and litter (Scheller 1982b); thus, the number of
described soil-dwelling species is assumed to be equal to the total
number described.
gChilopoda live in soil, leaf litter, rotting woods, and caves (Maddison
1997); thus, the number of described soil- and litter-dwelling species is
assumed to equal the total number of described species.
hPauropoda live preferably in soils and woodland litter (Scheller 1982a);
thus, the number of described soil and litter species is assumed to be
equal to the total number of described species.
iDiplopoda are characteristic of the upper soil and litter horizons
(Hoffman 1990); thus, the number of described soil- and litter-dwelling
species is assumed to be equal to the total number described.
jWe calculated the number of described species in soils based on
McAlpine's estimate that, for the United States, 50% of Dipteran species
are encountered in studies of soil biota (McAlpine 1990).

soil species (e.g., vertebrates, earth-
worms, and ants), for species that
occur in regions that are delineated
according to geopolitical rather than
ecological concepts, and for species
important to agriculture. The latter
include both plant pests (e.g., plant
parasitic nematodes and fungal
pathogens, such as Phytophthora
parasitica and Phytophthora citroph-
thora, both of which cause disease in
citrus trees) as well as beneficial sym-
bionts (e.g., mycorrhizae and nitro-
gen-fixing bacteria; Silver et al. 1996,
Brussaard et al. 1997). Estimates of
species richness and distribution of
soil microbes and invertebrates should
increase rapidly as molecular tech-
niques are used more frequently for
analyses.
Identifying, enumerating, and de-
termining life histories of soil organ-
isms is further confounded by the
temporal scale at which species oc-
cur in soils, that is, whether they are
temporary or permanent inhabitants
of soil during their life cycle. Because
of variation in temporal scale, com-
parisons of species across landscapes
may require multiple sampling loca-
tions, techniques, and times, and such
comparisons can be fraught with er-
ror (Blair et al. 1996, Freckman and
Reichman in press, Wall and Vir-
ginia in press).
Ecosystem scientists have histori-
cally grouped species of similar mor-
phologies and have used knowledge
of a few species in a group to classify
that group's role in ecosystems. For
example, all bacteria that produce
methane, and all nematodes whose
mouthparts are morphologically
similar, have been grouped into
"functional groups" (Root 1967,
Moore et al. 1988a, Hawkins and
MacMahon 1989, Yeates et al.
1993). Measurements of the changes
in biomass, abundance, and fre-
quency of these functional groups
were then compared to the rate of
change in an ecosystem process (such
as the loss of a known amount of
organic matter during decomposition)
to deduce the role of the group in the
ecosystem.
These kinds of experiments, to-
gether with direct observation, field
manipulation, microcosm, stable iso-
tope, and molecular techniques, have
shown that the functional groups of
organisms in soils-from microbes,
tardigrades, and rotifers to the larger
macroinvertebrates and vertebrates-
contribute substantially to essential
ecosystem services, such as soil fer-
tility, prevention of erosion, decay
and cycling of organic matter, break-
down of hazardous wastes, biologi-
cal control of agricultural and hu-
man pathogens, cleansing of water,
and composition of the atmosphere
(Daily 1997). However, a major chal-
lenge to identifying the importance
of individual species for ecosystem

110 BioScience Vol. 49 No. 2

processes has been to separate the
activities of the individual species
within a functional group and to de-
termine how species interact to per-
form the ecosystem function.
Nutrient cycling and
soil biodiversity
Nutrient cycling involves the trans-
formation of molecules from organic
to inorganic forms through processes
mediated by both organisms and the
nonliving portion of the soil envi-
ronment. The majority of terrestrial
primary production is not consumed
by herbivores; rather, it is decom-
posed into inorganic compounds by
microbes and their consumers (Swift
et al. 1979). The decomposition of
organic material into inorganic mol-
ecules is one of the more important
ecosystem services performed by soil
organisms, particularly microbes.
Decomposition involves comminu-
tion, chemical degradation, and
leaching of organic substrates. Com-
minution, or physical fragmentation
of detritus, occurs during feeding by
small invertebrates. Chemical deg-
radation is carried out by enzymes
produced by bacteria, fungi, proto-
zoa, and invertebrates. Leaching is
the removal of soluble organic com-
pounds, typically sugars and weak
acids, from dead organic matter and
detritus. These processes are highly
interactive. For example, comminu-
tion of detritus by small arthropods
and earthworms increases its surface
area, thereby facilitating further colo-
nization and invasion by microbes
and leaching of soluble substrates
(Swift et al. 1979).
The rate at which detritus decom-
poses depends on temperature and
moisture, on the type (quality) and
quantity of substrate, and on the
organisms that are present. Tempera-
ture and moisture affect decomposi-
tion rates through their influence on
soil organisms. Warmer and wetter
climates promote decomposition,
whereas colder and drier conditions
inhibit decomposition.
If key taxa are excluded from or
added to litter, the decomposition of
plant material may be altered (Butcher
et al. 1971, Seastedt 1984, Moore
1988). For example, as litter decom-
poses it undergoes a form of faculta-
tive succession (sensu Connell and
February 1999
Slatyer 1977, Wardle et al. 1995) by
microbes and invertebrates. Bacteria
and fungi colonize the litter and
modify it in ways that make it more
palatable to invertebrates such as
arthropods (Anderson 1973, Grant
1976, Ettema 1998, Covich et al.
1999). Once arthropods colonize the
litter, decomposition accelerates due
to a combination of comminution
and the enhancing effects of micro-
fauna (e.g., microarthropods, nema-
todes, and protozoa) on the growth
rates of the microbes.
An elegant illustration of these
processes and the importance of spe-
cies-specific life history traits and
behavior on community organiza-
tion and ecosystem processes comes
from Newell's (1984a, 1984b) studies
of the litter layer of Sitka spruce (Picea
sitchensis). The site in the United King-
dom that she investigated was domi-
nated by two litter-decomposing ba-
sidiomycetes-the slow-growing
Mycena galopus and the rapid-grow-
ing Marasmius androsaceus-and by
the fungal-feeding collembolan
Onychiurus latus, a microarthropod.
The collembolan preferentially
grazed the fast-growing M. andro-
saceus, thus shifting the balance from
M. androsaceus to M. galopus. At
the same time, the rate of decompo-
sition of spruce litter declined.
These kinds of successional pro-
cesses are not unique to the decom-
position of plant litter. For example,
the rate at which a vertebrate carcass
decomposes in a tropical forest can
be linked to the succession of the 118
insect taxa involved. This situation
provides a tool used in forensic medi-
cine (Richards and Goff 1997); that
is, the successional stage of insects
present enables the time from death
to be calculated.
There are strong parallels between
the decomposer communities of soils
and the microbial loop of marine
habitats and freshwater lakes (Cole-
man 1994). A key difference between
the terrestrial and aquatic systems is
the degree to which primary produc-
tion and decomposition interact. In
soils, spatial and temporal distances
between primary production (sub-
strate) and decomposition are much
less than in aquatic systems (Wagener
et al. 1998). As a result, in soils,
plant-produced substrates and de-
composers have coevolved specific
associations, and nutrient dynamics
are intimatelytied to the decomposi-
tion of plant litter and substrates
produced by plant roots. The asso-
ciations are best characterized as
mutualistic interactions and reveal
the importance of biodiversity for
ecosystem functioning in soil.
Mutualisms
In contrast to soil ecology, tradi-
tional plant ecology focuses on the
competitiveabilitiesof differentplant
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species. Communities are seen as
being shaped by the adaptation of
the plants to the region and by their
abilities to securelimiting resources.
Marine ecology has also focused on
adaptation, competition, and preda-
tion. For example, the classic studies
of Connell (1961a, 1961b) andPaine
(1966) illustrated how competition
and predation interact to shape the
diversity and distribution of marine
algae and invertebrates. Likewise,
much of the freshwater aquatic lit-
erature on the dual roles of the rate
of primary production (bottom-up
forces) and regulation by predators
(top-down forces) has focused on
predation and competition. Elegant
experiments and models showing
how these factors govern trophic
structures within lakes and streams
aretriumphsof modernecology (Car-
penter et al. 1985, Power 1990,
Wooton and Power 1993).
Studies of soil organisms do not
dispute the roles of competition and
predation in shaping soil communi-
ties, but they highlight the impor-
tance of mutualisms (i.e., interac-
tionsbetweenspeciesthathavepositive
effects on each of theirgrowth rates).
Two classes of mutualismshave been
identified:symbioticandnonsymbiotic
(Boucher et al. 1982, Moore 1988,
Price 1988). Symbiotic mutualisms
involvean intimatephysiologicallink
between the species. Nonsymbiotic
mutualisms arise through interac-
tions that may or may not involve
physical contact. Simplemathemati-
cal models of symbiotic mutualisms
indicate that the interactions are in-
herently unstable and should not
persist (Pimm 1982). Yet symbiotic
mutualisms are an integral part of
terrestrialecosystems.The dominant
plant species of every mature or cli-
max terrestrial ecosystem are en-
I11
gaged in some form of symbiotic
mutualism with soil microbes.
A formal theoretical treatment of
nonsymbiotic mutualism has yet to
emerge. However, the outcomes of
nonsymbiotic mutualisms frequently
resemble what some ecologists call
indirect effects. For example, a
predator's suppression of an herbi-
vore and the subsequent decrease in
herbivory experienced by plants
could be construed as both an indi-
rect effect and a form of nonsymbiotic
mutualism.
Mutualisms within
the rhizosphere
Much like the soil litter layer, the
plant root is an important region of
nutrient dynamics. The rhizosphere
includes the soil that surrounds and
is influenced by plant roots. Much of
the photosynthate that plants pro-
duce is diverted to roots for root
growth and exudates and thereby
provides a carbon source for soil
species. The amount of carbon allo-
cated to root growth varies with the
type of plant. In grassland plants,
the ratio of shoot to root production
is roughly 1:1 (50% above ground,
50% below ground), whereas the
shoot:root ratio of forest plants is
much higher (Jackson et al. 1996).
The belowground allocation of pho-
tosynthate represents a dynamic
source of organic inputs to soil for
many terrestrial ecosystems that is
important for structuring soil bio-
diversity. Therefore, estimates of net
primary production require more
than just crude estimates of above-
ground production and belowground
production at 0-10 cm, as has tradi-
tionally occurred. Such estimates are
starting to include estimates of below-
ground carbon sequestration and
root growth to considerable depths
(Jackson et al. 1996).
Plant roots are a tangled mess of
cells and organic secretions. Roots
can be divided into a continuum of
overlapping regions of activity start-
ing at the tip of a growing root and
working back to the crown of the
plant, just at the soil surface (Trofy-
mow and Coleman 1982). The root
tip is the site of growth. A growing
root produces numerous cells and
secretions as it penetrates soils, pro-
viding many substrates as a source of
112
food for soil microflora and inverte-
brates. One type of secretion is
mucigels, slimy carbon substrates
made up largely of sugar that serve
as lubricants. Despite the presence
of mucigels, many new and old root
cells are sloughed off from the shear-
ing forces that accompany the root's
movement through the soil.
Beyond the root tip is a zone of
intense nutrient exchange. Water and
soluble forms of nitrogen are taken
up by the root, and the root leaks
low molecular weight carbon com-
pounds, or exudates, into the soil. In
grasses, for example, 17% of the
fixed carbon is lost via exudation
(Milchunas and Lauenroth 1992).
Root hairs are numerous in this re-
gion and are continually dying and
being replaced, as well as being at-
tacked by soil pathogens such as
nematodes and insects.
Farther up from the root tip, a
third zone is characterized by symbi-
otic mutualistic relationships be-
tween plants and microbes. Mycor-
rhizal fungi, actinomycetes (e.g.,
Frankia), and many Proteobacteria
(e.g., Bradyrhizobium and Rhizo-
bium) infect roots within this region.
Each of these mutualists has a unique
means of infecting and interacting
with the host plant. In all cases,
however, the plant provides shelter
and carbon, while the symbiont pro-
vides better access to a limiting nu-
trient (nitrogen or phosphorus). The
complexity of these mutualistic in-
teractions makes elucidation of their
contribution to ecosystem function-
ing challenging (Baumann 1998). For
example, because different strains of
Rhizobia infect different plant spe-
cies, the selection of a strain of Rhizo-
bia that will provide greater nitro-
gen fixation in legumes has been a
major area of agricultural research.
Adding to the complexity, the bacte-
rial-feeding nematode Acrobeloides
buetschlii feeds on nitrogen-fixing
bacteria in the rhizobial nodules,
decreasing nitrogen fixation by 80-
90% while at the same time carrying
the bacteria to other sites of the root
(Chantanao and Jensen 1969).
Beyond these regions, the root ages
and takes on a more structural role.
The cells that are sloughed off pos-
sess complex organic compounds and
decompose more slowly. The decom-
position process becomes more simi-
lar to that within the litter layer and
soil surface.
Mycorrhizae and secondary succes-
sion. The species-specific nature of
mutualistic interactions illustrate
that both functional groups and spe-
cies within a functional group influ-
ence community succession. For ex-
ample, the Piceance Basin of Western
Colorado is a series of eroded hills at
the base of the Rocky Mountains.
The lowlands and slopes are domi-
nated by sagebrush (Artemesia tri-
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dentata) and other species. Histori-
cally, the economy of the region was
driven by tourism, cattle ranching,
and hay production. In the mid-1970s
to early 1980s, the area was trans-
formed by the prospect of mining of
oil shale deposits. The plan was for
the shale to be mined, superheated to
extract the oil, and spread over the
landscape or in large human-made
mountains. Usually, restoration of
such damaged landscapes is focused
on re-creating the vegetative diver-
sity, but in several studies that have
mimicked the effects of mine tailings
and studied restoration (Reeves et al.
1978, Biondini et al. 1985a, 1985b,
Metzger et al. 1986) the focus was on
re-creating the functioning of and
the linkages between soil biodiversity
and the plant communities.
In one study, the experimental area
(the Piceance Basin in Colorado) was
denuded of vegetation and topsoil in
an effort to simulate the aftermath of
mining (Moore et al. 1988a). The
soils in half of the plots were further
treated with a soil fumigant, methyl
bromide, to kill off the soil biota.
One-third of each of the fumigated
and nonfumigated plots were seeded
with native vegetation at rates com-
parable to the seed production of
undisturbed sites, one-third were
seeded and planted with sagebrush
seedlings, and one-third were left
denuded. The number and biomass
of plant species and the densities and
activity of soil bacteria and fungi
were monitored.
Within 4 years, three patterns
emerged (Figure 1). First, after 1
year, the fungal densities remained
severely depressed in the fumigated
and denuded plots and, to a lesser
extent, in the nonfumigated and de-
nuded plots, as compared to undis-
turbed native plots. This pattern was
BioScience Vol. 49 No. 2
even more pronounced for the my- Figure 1. Mycorrhizae
c0)
corrhizal fungi. Unlike the fungi, the and secondary succes-
sion at the Piceance 0) a Ao A
bacterial biomass recovered within
Basin (Moore et al. 10' 3
the first year. Second, the sagebrush
in the fumigated plots experienced 1988b). (a) The influ- AA AOO
ence of mycorrhizalin-
the least growth. By contrast, the fection on the above- A 00
productivity of many of the shrubs ground production of
-a
C A
A
in the nonfumigated plots was com- individualplantedsage- '0 10'2
parable to that in the undisturbed brush (Artemisia tri- 0._ A
native communities. Third, the rela- dentata)in methylbro-
tive proportions of plant species (i.e., mide-fumigated (solid o
the structure of the plant commu- triangles)andnonfumi-
nity) in the seeded plots were a func- gated (open circles) -

tion of mycorrhizal fungal densities. plots. (b) The relation- 101 I I I I

I

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Not all plant species form mycor- shipbetweenthe myco- 0.1 0.5 1 5 10 50
rrhizalinoculumpoten-
rhizal associations, however. Those tial (MIP) of the soil % root colonized
that do not-including invasive and (after Moorman and
weedy species, such as Russian thistle Reeves 1979) and the
(Salsola iberica = Salsola kali)- evenness of plant pro-
thrived in and ultimately overran the duction (HGrime) based Q)

disturbed plots. on Grime'scategoriza- i=. b U

It appears that the mycorrhizal tion of plants (Grime
1977) in methyl bro-
-1
fungi conferred a competitive ad-
vantage to their host through greater mide-fumigated (solid
nutrient acquisition. However, a sub- triangles), nonfumi- c
gated(opencircles),and
sequent study at a different site sug- undisturbed native
0)
gested that additional mechanisms plots (solid squares).
allow mycorrhizae to promote C)
growth of certain plants. The mycor- c0
rhizal fungi were pathogenic to the with ample light and C
seedlings of the nonmycorrhizal plant low levels of avail- c)
S. kali (Allen et al. 1989). In essence, Ahlh -li..-iLi
av?\^ n itroarpnn
LVc- . V.
one plant's benefactor was another Once established,
one's pathogen. The mycorrhizal M. faya and its soil
fungi were operating as both symbi- symbiont Frankia
otic and nonsymbiotic mutualists to alter the nitrogen
their host plants. status of the soil. For example, soil
nitrogen inputs within open cano-
Biological invasions of a symbiotic pies of M. faya were four times that
mutualism. The plant species Myrica of similar sites without the exotic
faya (fayatree) was introduced to plant (23.5 kg-ha-1-yr-1 versus 5.5
Hawaii from the Canary Islands by kg-ha-1.yr-1; Vitousek and Walker
Portuguese immigrants at the end of 1989). This added soil nitrogen be-
the nineteenth century. By the mid- comes available to other plant spe-
1980s, it had colonized more than cies, with long-term consequences.
34,365 hectares in the Hawaiian is- For example, an increase in nitrogen
lands. Based on the natural history may facilitate invasions by other ex-
of this plant, Vitousek et al. (1987) otic species (e.g., strawberry guava,
and Vitousek and Walker (1989) Psidium catleianum), to the detri-
argued that its attributes are impor- ment of native plant species.
tant at the level of the whole ecosys-
tem. M. faya forms a symbiotic asso- Nonsymbiotic mutualisms affect ni-
ciation with the nitrogen-fixing soil trogen availability and plant growth.
actinomycete Frankia. Unlike native Nonsymbiotic mutualisms are nu-
Hawaiian plant nitrogen fixers (Aca- merous in soil but less obvious than
cia koa and Sophora chrysophylla), symbiotic mutualisms. Within the
M. faya has an edible fleshy fruit with rhizosphere, sloughed cells, mucigels,
small seeds that pass intact through and exudates are rich carbon sources
the digestive systems of birds. These for bacteria and fungi. In the process
factors interact to make M. faya well of using these carbon sources, the
adapted to colonize recent lava flows, microbes also use nitrogen in the soil
pastures, and open, canopied forest that would be otherwise used by the
0.5 A AA
A A
A
1I A....
0.1 1.0 10 100
MIP
plants. However, as the microbial
populations increase, their consum-
ers (i.e., protozoa, nematodes, and
microarthropods) also increase. Be-
cause the microbes contain more ni-
trogen than these faunal consumers
can use, the animals release the inor-
ganic nitrogen back into the soil,
where it can be taken up by the
plants. Both laboratory and field
studies have demonstrated that ni-
trogen availability and plant growth
are higher in the presence of con-
sumers of microbes than in their ab-
sence (Clarholm 1985, Ingham et al.
1985, Setala and Huhta 1991).
The bacteria and fungi in the rhizo-
sphere form distinct assemblages of
species that operate as pathways to
cycle nutrients, but at different rates.
Bacteria and their consumers repro-
duce and turn over nutrients at faster
rates than fungi and their consumers
(Coleman et al. 1983, Moore and de
Ruiter 1997). The reproduction and
nutrient turnover rates translate into

February 1999 113

Figure 2. Decomposi- How intertwined are the decompos-
tion of reciprocally ers of an ecosystem with the plant
transplantedgrass and 100 a community? Several studies of de-
pine litter between a | - a a
composition in adjacent and geo-
lodgepole pine forest a graphically disparate ecosystems
and sagebrush-grass , b
meadownearFoxPark,c demonstrate how species, climate,
a and litter quality interact (Hunt et
Wyoming(Boyer1997,
Huntetal. 1988).Litter 90- b al. 1988, Ingham et al. 1989, Cole-
was placed in the field man et al. 1990, Boyer 1997, Lipari
in Octoberof the previ- 2 h
b 1997). For example, pine needles
ous year. Pine litter and grasses from adjacent lodgepole
placed in the meadow 0 I pine forests and sagebrush-grass
(open squares) showed meadows in the Medicine Bow
little decomposition 80 Mountains of Wyoming share soils

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when comparedto place-
of similar origin and climate. Never-
ment in its own ecosys-
tem (solid squares). ...- . . theless, pine needles placed in the
Grasslitterdecomposed meadow decomposed at a slower rate
at similarratesin the 19-Jan 1-Apr 23-Jun 20-Sep than those in the forest, whereas
forest(opencircles)and grass shoots decomposed at similar
in the meadow (solid Retrievaldate rates, regardless of their location
circles).A surveyof the (Figure 2; Hunt et al. 1988, Boyer
fungiat the sitesfoundthat 24% of the fungalgenerain the meadowand 33% of those 1997).
inthe forestwereuniqueto thosesystems.Similarlettersindicateno significantdifference This result could be due to the
in mass remainingat that date. chemical composition of the litter,
which influences the growth of soil
a difference in the responses of the achieve these aims. One approach organisms. Pine needles have higher
pathways to disturbances and to the employs minimum tillage and low- concentrations of tannins and lignins-
availability (i.e., timing and quantity) input management practices to main- compounds that are difficult to de-
of nutrients that are limiting to plants. tain the soil profile in a more natural compose. At the community scale,
Agroecologists have worked to ex- state (Beare et al. 1992, Frey et al. in the soils in the meadows were domi-
ploit this interplay between plants press). The nutrient dynamics that nated by bacteria and their consum-
and soil biota to increase nitrogen ensue are more likely to mimic what ers (i.e., the bacterial pathway; sensu
uptake by plants and retention within is observed in native systems. How- Moore and Hunt 1988), whereas the
soil (Elliott and Coleman 1988). ever, this is a broad prescription that community in the forest was domi-
Comparisons of minimum tillage and must be used cautiously in light of nated by fungi and their consumers
conventional management practices site-specific concerns, such as soil (i.e., the fungal pathway), which are
in the United States, Canada, and pests and pathogens or soil drainage. better at decomposing the secondary
Europe have demonstrated that tim- The second approach attempts to compounds in pine needles (Ingham
ing is also critical to the relationship manipulate the nutrient pathways di- et al. 1989).
between soil biodiversity and plant rectly, through management of key A field study of hyphomycete fungi
productivity. For maximum benefit, species or processes (Venette and Ferris revealed that fewer than half of the
decomposition should be timed so 1997, Matson et al. 1998). For ex- genera were shared between the two
that maximum soil nitrogen is avail- ample, to increase their growth, crop sites. Isolates and combinations of
able during the period of plant plants can be inoculated with symbi- fungal species that were common
growth. However, historically, a otic rhizobia and mycorrhizae, as well and unique to each site were grown
common result of conventional agri- as with nonsymbiotic species, such as on media prepared from pine and
culture has been to disrupt this cycle nitrogen-fixing bacteria (Azospirillum grass extracts (Lipari 1997). The
by shifting nutrient dynamics from spp.; Okon and Labandera-Gonzalez growth and reproductive rates of the
the fungal pathway to the bacterial 1994) and phosphate-solubilizing fungi depended not only on the qual-
pathway, accelerating decomposition rhizobacteria (Toro et al. 1998). In ity of plant litter and on the presence
so that nitrogen mineralization occurs addition, soils have been inoculated of invertebrate grazers but also on
soon after the crop has been harvested with earthworms to enhance nutri- the presence of other fungi. In many
(Hendrix et al. 1986, Andren et al. ent dynamics and availability by instances, fungal isolates grown in
1990, Moore and de Ruiter 1991, means of the processes discussed tandem produced more hyphae and
Beare et al. 1992, Wardle 1995, Frey above (Edwards and Lofty 1980). spores than those grown in isolation
et al. in press). If conventional agricul- on similar media. In field experi-
ture were more finely tuned to the Mutualismswithin ments, Ettema and Bongers (1993)
natural cycles of soil biotic interac- the litter noted a similar "chain of connectiv-
tions, nitrogen retention would be
layer? ity," in this case between the bacte-
maximized, and more nitrogen would The litter layer is one of the more rial-feeding nematode species in-
be available to plants. prominent features of forests floors volved in decomposition. Thus, a
Two approaches have emerged to and, to a lesser extent, of grasslands. succession of species-dependent in-

114 BioScience Vol 49 No. 2


teractions in soils appears to accom-
pany the stages of decomposition.
These findings provide an impor-
tant link between biodiversity and
ecosystem functioning across eco-
systems, but they reintroduce the
question of how interactions among
microbial and invertebrate species in
processes such as decomposition of
litter operate in structuring soil
communities. Microbial ecologists
have long suspected that bacteria
and fungi interact in tightly coupled
consortia to decompose complex
organic compounds. The species
within a consortia colonize a sub-
strate in sequence or in combination,
and each contributes enzymes that
degrade the substrates into simpler
organic and inorganic forms. Several
enzymes may be required to decom-
pose complex molecules, such as
lignins, and the absence of a key
enzyme may delay decomposition.
The fact that the meadow lacks the
diverse fungal community of the for-
est may explain why litter from the
forest was slow to decompose there:
Microbes unique to the forest were
absent in the meadow, no suitable
replacement was present, key en-
zymes were thus missing, and steps
in the decomposition sequence were
left undone.
The linkages between soil bio-
diversity, the plant, and nutrient cy-
cling are extremely complex. The
species compositions of plant com-
munities and microbial and inverte-
brate decomposer communities are
tightly coupled through plant litter
quality and quantity. Species within
the fungal and bacterial pathways
have also adapted to the chemical
composition of the substrates pro-
duced by the producer (plant root)
pathway. Changes in plant species
(and litter quality), such as occur
when new crop plant species are in-
troduced into agroecosystems or
when conventional agriculture is
changed to no-tillage agriculture,
therefore modify the bacterial and
fungal decomposer communities as
well as invertebrate diversity (Freck-
man and Ettema 1993, Swift and
Anderson 1994). Consequently,
changes in plant functional types and
litter through invasions of plant spe-
cies into soil systems undoubtedly
will have a major effect on bio-
diversityand nutrientcyclingin soils.
February 1999
CNP
a
Plants C,P - Litter
I\
Plants
N,PI \\ C,'I~
c| N,P
Mutualist
Downloaded from https://academic.oup.com/bioscience/article-abstract/49/2/109/239533 by guest on 12 March 2019
Grazers
Figure 3. Examples of symbiotic and nonsymbioticsoil mutualisms.(a) Symbiotic
mutualistsinclude mycorrhizalfungi, Frankia,and rhizobia. (b) Some nonsymbiotic
mutualistscontrolrhizospherenutrientavailability.(c) Othernonsymbioticmutualists
formconsortiathatcontroldecompositionandnutrientavailability.Ineachcase,plants
provide soil organisms with carbon, whereas soil organisms provide plants with
nitrogen,phosphorus,and other limitingnutrients.The plus and minus signs referto
positive and negativeinteractioneffects,respectively.The solid lines representtrophic
interactions,or directmass-nutrienttransfers,as in the case of plants and litter. The
dashedlinesrepresentnutrienttransfersthroughsoils, resemblingthe "indirecteffects"
cited in the literature.
Conclusions 1989), and agriculture (Moore and
de Ruiter 1991, Freckman and
Are the key taxa for ecosystem pro- Ettema 1993) are a only few ex-
cesses those involved in mutalistic amples of disturbances that affect not
interactions? The examples of sym- only species diversity (Lawton et al.
biotic and nonsymbiotic mutualistic 1996) and the composition of func-
interactions (Figure 3) that we have tional groups but also the rate of eco-
presented illustrate that in soils, these system processes. It is because plants
types of species-specific interactions and soil organisms have coevolved
between plants and soil organisms that the future management of global
have profound impacts on ecosys- soils must include knowledge of spe-
tem processes. Aboveground species cies and functional diversity.
may be functionally linked to entire
assemblages of belowground species, Acknowledgments
and whole assemblages of below-
ground species may be necessary for Research in the authors' laborato-
coupling the aboveground-below- ries was supported by grants from
ground nutrient cycle. The specific- the National Science Foundation
ity of many of these mutualistic in- (grant no. DEB 96-26813 and OPP
teractions indicates that even species 96-24743 to Diana H. Wall; grant
within a functional group may not no. DEB 92-57710 to John C. Moore)
be interchangeable with the same and is a contribution to the McMurdo
effect. Consequently, much of the Long Term Ecological Research pro-
vast belowground diversity may be gram (OPP 92-11773). The authors
necessary to maintain the ecosystem would like to thank Drs. Gina Adams,
structure and function we see today. Andy Parsons, Debra Coffin, and
Although the identities of the Don Strong, and Ms. Amy Treonis
majority of soil organisms are not and Mr. Dan Bumbarger, for their
known, disturbances to these spe- critical and helpful comments and
cies-specific mutalistic interactions discussions. This article is a project
alter species diversity, with effects at of the Committee on Soil and Sedi-
the ecosystem level. Pollution, in- ment Biodiversity and Ecosystem
cluding the mine shale example dis- Functioning, a component of
cussed earlier in the article, desertifi- DIVERSITAS, coordinated by
cation (Freckman and Virginia SCOPE.
115
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