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535
Ecological Monographs,
69(4), 1999, pp. 535–568
q
1999 by the Ecological Society of America
PLANT REMOVALS IN PERENNIAL GRASSLAND:
VEGETATION DYNAMICS, DECOMPOSERS, SOIL BIODIVERSITY, AND
ECOSYSTEM PROPERTIES
D
AVID
A. W
ARDLE
,
1,4
K
AREN
I. B
ONNER
,
1,4
G
ARY
M. B
ARKER
,
1,5
G
REGOR
W. Y
EATES
,
2
K
ATHRYN
S. N
ICHOLSON
,
1
R
ICHARD
D. B
ARDGETT
,
3,6
R
ICHARD
N. W
ATSON
,
1
AND
A
NWAR
G
HANI
1
1
AgResearch, Ruakura Agricultural Research Centre, Private Bag 3123, Hamilton, New Zealand
2
Landcare Research, Private Bag 11052, Palmerston North, New Zealand
3
School of Biological Sciences, University of Manchester, Oxford Road, Manchester, M13 9PT, UK
Abstract.
The consequences of permanent loss of species or species groups from plant communities are
poorly understood, although there is increasing evidence that individual species effects are important in modifying
ecosystem properties. We conducted a field experiment in a New Zealand perennial grassland ecosystem, creating
artificial vegetation gaps and imposing manipulation treatments on the reestablishing vegetation. Treatments
consisted of continual removal of different subsets or ‘‘functional groups’’ of the flora. Wemonitored vegetation
and soil biotic and chemical properties over a 3-yr period.
Plant competitive effects were clear: removal of the C
3
grass
Lolium perenne
L. enhanced vegetative cover,
biomass, and species richness of both the C
4
grass and dicotyledonous weed functional groups and had either
positive or negative effects on the legume
Trifolium repens
L., depending on season. Treatments significantly
affected total plant cover and biomass; in particular, C
4
grass removal reduced total plant biomass in summer,
because no other species had appropriate phenology. Removal of C
3
grasses reduced total root biomass and
drastically enhanced overall shoot-to-root biomass ratios. Aboveground net primary productivity (NPP) was not
strongly affected by any treatment, indicating strong compensatory effects between different functional com-
ponents of the flora.
Removing all plants often negatively affected three further trophic levels of the decomposer functional food
web: microflora, microbe-feeding nematodes, and predaceous nematodes. However, as long as plants were present,
we did not find strong effects of removal treatments, NPP, or plant biomass on these trophic groupings, which
instead were most closely related to spatial variation in soil chemical properties across all trophic levels, soil
N in particular. Larger decomposer organisms, i.e., Collembola and earthworms, were unresponsiveto any factor
other than removal of all plants, which reduced their populations. We also consideredfive functional components
of the soil biota at finer taxonomic levels: three decomposer components (microflora, microbe-feeding nematodes,
predaceous nematodes) and two herbivore groups (nematodes and arthropods). Taxa within these five groups
responded to removal treatments, indicating that plant community composition has multitrophic effects at higher
levels of taxonomic resolution. The principal ordination axes summarizing community-level data for different
trophic groups in the soil food web were related to each other in several instances, but the plant ordination axes
were only significantly related to those of the soil microfloral community. There were time lag effects, with
ordination axes of soil-associated herbivorous arthropods and microbial-feeding nematodes being related to
ordination axes representing plant community structure at earlier measurement dates. Taxonomic diversity of
some soil organism groups was linked to plant removals or to plant diversity. For herbivorous arthropods,
removal of C
4
grasses enhanced diversity; there were negative correlations between plant and arthropod diversity,
presumably because of negative influences of C
4
species in the most diverse treatments. There was evidence of
lag relationships between diversity of plants and that of the three decomposer groups, indicating multitrophic
effects of altering plant diversity.
Relatively small effects of plant removal on the decomposer food web were also apparent in soil processes
regulated by this food web. Decomposition rates of substrates added to soils showed no relationship with
treatment, and rates of CO
2
evolution from the soil were only adversely affected when all plants were removed.
Few plant functional-group effects on soil nutrient dynamics were identified. Although some treatments affected
temporal variability (and thus stability) of soil biotic properties (particularly CO
2
release) throughout the ex-
periment, there was no evidence of destabilizing effects of plant removals.
Our data provide evidence that permanent exclusion of plant species from the species pool can have important
consequences for overall vegetation composition in addition to the direct effects of vegetation removal, and
various potential effects on both the above- and belowground subsystems. The nature of many of these effects
is driven by which plant species are lost from the system, which depends on the various attributes or traits of
these species.
Key words: biodiversity; community structure; competition; decomposition; ecosystem properties; functionalgroups;plant
traits; removal experiments; soil food web; stability.
Manuscript received 10 October 1997; revised 1 October 1998; accepted 15 October 1998.
4
Present address: Landcare Research, P.O. Box 69, Lincoln 8152, New Zealand. E-mail: wardled@landcare.cri.nz
5
Present address: Landcare Research, Private Bag 3127, Hamilton, New Zealand.
6
Present address: Department of Biological Science, Institute of Natural and Environmental Sciences, University of Lan-
caster, Lancaster LA1 4YQ, UK.
536
DAVID A. WARDLE ET AL.
Ecological Monographs
Vol. 69, No. 4
I
NTRODUCTION
A major issue in ecological research involves the
effects of individual species and groups of species on
community-level and ecosystem-level attributes (Hob-
bie 1992, Lawton 1994). It is becoming increasingly
appreciated that invasions of ecosystems by new spe-
cies have profound effects on ecosystem function (Vi-
tousek and Walker 1989, Vitousek et al. 1997). In ad-
dition, anthropogenic activity is causing rapid loss of
species from many of Earth’s ecosystems (Ehrlich and
Ehrlich 1981, E. O. Wilson 1988), raising the issue of
how loss of species alters community- and ecosystem-
level properties and processes (Schulze and Mooney
1993). From an applied perspective, managed, produc-
tion-oriented systems have frequently (although not al-
ways) involved maintenance of biological communities
with an artificially low plant and herbivore species di-
versity, and recent focus has been on the ecological
consequences of deliberate addition of more species
(with corresponding shifts in species composition) in
both agricultural (Vandermeer 1988, Giller et al. 1997)
and forested (Wormald 1992) landscapes.
When a plant species is lost from a given community,
often there are important consequences for the re-
maining floristic components of that community, es-
pecially if that species is potentially dominant (Gross
1980, Fowler 1981, Hils and Vanket 1982, Aarsson and
Epp 1990). The positive effects of the loss of one plant
species on the other plant species often stem from the
competitive effects of that species (J. B. Wilson 1988),
although, in some instances, loss of a species can also
have negative consequences for the remaining flora
(Calloway 1995). Studies of the loss of a dominant
species from an ecosystem (e.g., Abdul-Fatih and Baz-
zaz 1979, Armesto and Pickett 1985, Gurevitch and
Unnasch 1989, Wardle and Barker 1997) provide in-
direct evidence that dominant species may suppress
overall diversity by preventing establishment of other
species. Removal of selected species can have negative
effects on total plant biomass and productivity, es-
pecially if species have separate niches and demon-
strate complementary resource use. When niche over-
lap is high and competition for resources is intense,
loss of a given species can be largely compensated for
by the other species, resulting in overall biomass and
productivity being less sensitive to species removal
(Lawton and Brown 1993, Hooper and Vitousek 1997,
Hooper 1998).
Although most studies involving manipulations of
plant communities have focused on floristic changes
following removal of a subset of the flora, a more com-
plete picture of the effects of losses of plant species in
an ecosystem can be gained by simultaneously consid-
ering the response of other trophic levels, e.g., by uti-
lizing a food web-based approach (Wiegert and Owen
1971, Schoener 1989, Pastor et al. 1993, Wardle 1995,
Wootton et al. 1996). In particular, the decomposer food
web is a critical component of most ecosystems be-
cause it is directly responsible for regulating key eco-
system processes such as decomposition and nutrient
mineralization. Formal trophic dynamic models using
prey-dependent predator–prey interactions (e.g., Ro-
senzweig 1971, Oksanen et al. 1981) and studies pre-
senting evidence for the existence of trophic cascades
(Carpenter and Kitchell 1988) indicate that biomasses
of some trophic levels are likely to respond to alteration
of basal resources (e.g., through changes in net primary
production due to removal of a plant species) whereas
others are not because their biomasses are regulated by
higher trophic levels. There is recent evidence from
soil food webs that the biomass of different trophic
levels responds rather uniformly to the amounts of ba-
sal resources added (Mikola and Seta¨la¨ 1998
b
), al-
though little is known about how changes in the com-
position of basal resources (e.g., due to changes in plant
community structure) affect higher trophic levels in soil
food webs. Further, at finer levels of taxonomic reso-
lution, shifts in species composition and diversity at
the basal (plant) trophic level have the potential to
induce corresponding changes in higher trophic levels
of soil food webs (Griffiths et al. 1992, J. Zak et al.
1994), although this issue remains largely unexplored.
Understanding soil food web structure at the level
of functional groups provides clues to a better under-
standing of ecosystem function (Wardle et al. 1998
b
)
because of the role of the structure and dynamics of
soil food webs in influencing decomposition and min-
eralization processes (Bengtsson et al. 1996, Mikola
and Seta¨la¨ 1998
a
), and, ultimately, ecosystem produc-
tivity (Ingham et al. 1985, Seta¨la¨ 1995). However, at
finer levels of taxonomic resolution, little is known
about whether changes in taxonomic composition of
organisms within trophic levels are important at the
ecosystem level, and the available evidence is ambig-
uous (Andre´n et al. 1995, Mikola and Seta¨la¨ 1998
c
).
Further, there is indirect evidence of important feed-
backs existing between the structure of plant and soil
communities (e.g., Bever 1994, Bever et al. 1997). Ef-
fects of removal of plant species on decomposer food
webs therefore have the potential to influence ecosys-
tem properties by altering those processes that soil food
webs regulate.
In the present investigation, we sought to determine
the effects of plant composition on community- and
ecosystem-level attributes in a perennial grassland in
New Zealand, both aboveground and belowground. We
achieved this by performing experimental removals of
different plant functional groups in small field plots
over a 3-yr period. Specifically, our intention was to
test each of the following four hypotheses: (1) removal
of subsets of the existing flora results in increased di-
versity, biomass, and productivity of the remaining flo-
ra, but the total (overall) biomass and productivity is
November 1999 537
PLANT COMPOSITION AND ECOSYSTEM PROPERTIES
reduced because of partially compensatory interactions
between floristic components; (2) modification of the
producer trophic level has important effects on some
trophic levels, but not others, because of the interplay
of top-down and bottom-up forces in regulating soil
food webs; (3) shifts in plant community-level attri-
butes such as composition and diversity are important
determinants of composition and diversity at higher
trophic levels in soil food webs; and (4) removal of
plant functional groups, representing permanent exclu-
sion of plant species from the species pool, has im-
portant consequences for ecosystem-level processes
and properties such as primary production, biomass,
decomposer activity, nutrient levels, and ecosystem
stability. The ultimate goal of our study was to deter-
mine the general consequences of removal of floristic
components, and the resultant shifts in composition, in
order to understand how species losses are manifested
at both the community and ecosystem levels.
M
ETHODS
System and approach
Over the past few centuries,
;
75% of New Zealand’s
forest vegetation cover has been cleared, and much of
this land is currently under perennial grassland, which
is primarily managed for livestock production. In the
Waikato district of New Zealand’s North Island, the
majority of grazed land is utilized for managing dairy
cattle. Here, the grasslands are dominated by intro-
duced perennial herbaceous species, mainly the C
3
grass
Lolium perenne
L. and the legume
Trifolium re-
pens
L., with significant levels of winter-annual C
3
grasses (principally
Poa annua
L.), summer-annual C
4
grasses, and several short-lived, dicotyledonous weed
species.
In grazed perennial grasslands in New Zealand, plant
regeneration is mainly concentrated in disturbed or de-
nuded patches or gaps resulting from disturbance such
as cattle feeding and treading, summer droughting, and
invertebrate infestations; these gaps can be up to 20
cm in diameter (Panetta and Wardle 1992). Establish-
ment of plant seedlings usually occurs in these gaps,
and it is the processes and biotic interactions occurring
in these gaps that ultimately contribute to the species
composition of the pasture (Panetta and Wardle 1992).
This mechanism is widespread throughout temperate
perennial grasslands, including both Europe (Bullock
et al. 1994, 1995) and North America (Platt and Weiss
1977, Goldberg and Werner 1983, Kotanen 1997). The
net result is a mosaic of patches of different ages and
varying species composition.
We used vegetation gaps as our experimental unit to
investigate how removals of plant functional groups
affect the ecological properties of grasslands at the spa-
tial scale of pasture gaps. We created artificial, deve-
getated gaps and allowed the vegetation to recolonize
over time, with the imposition of treatments consisting
of continual removal of different plant functional
groups. This approach is conceptually based on the
‘‘removal experiment’’ approach that is often used to
study plant competition (Harper 1977, Aarssen and Epp
1990, Herben et al. 1997).
Site and experimental setup
The experimental site was a perennial grassland,
dominated by herbaceous plant species of mainly Eu-
ropean origin, and grazed by dairy cattle, near Ham-
ilton in the Waikato district (37
8
45
9
S, 175
8
15
9
E). It
was grazed over an approximately monthly rotation to
a height of 4–6 cm, typical of many grazing systems
in New Zealand. Consequently, competitive interac-
tions above ground are probably much less important
than those below ground (see J. B. Wilson 1988). The
climate is warm temperate, and the site has a long-term
mean annual rainfall of 1204 mm/yr (Fig. 1). The soil
present is a Horotiu silt loam (Vitric Hapludand) and
at the start of the experiment had 13.0% C, 0.06% N,
and a pH of 5.1 at 0–7.5 cm depth.
The experimental site occupied an area of 0.5 ha,
which was subdivided into 10 blocks of 0.05 ha each
that served as the units of replication. Within each
block, six 0.8
3
1.2 m ‘‘plots’’ were set up. Within
each plot, six subplots (hereafter referred to as ‘‘gaps’’)
were set up; these gaps were circular, 20 cm in diameter,
and arranged in a 3
3
2 grid in the plot so that all gaps
were
$
20 cm apart. The size of gap that we selected
has been previously shown to be appropriate for in-
vestigating biotic interactions in model plant commu-
nities with similar species compositions and soils (War-
dle and Barker 1997). Permanent wooden pegs were
placed in the corners of each plot; a portable steel frame
was constructed that fitted over the entire plot (and
around the pegs) and contained six 20 cm diameter
circles matching exactly the location of the six gaps in
the plot. This frame enabled relocation of each gap with
considerable accuracy. In addition to these gaps, one
further gap was established in each replicate block for
destructive harvesting to provide baseline (
t
5
0) data.
The gaps were created by killing all of the vegetation
within them. This was achieved by spraying each gap
separately with two nonresidual herbicides, glyphosate
(formulated as Round-up) at 2 kg ai/ha, and tribenuron
(formulated as Granstar) at 30 g ai/ha, on 27 January
1994. To prevent the herbicide from affecting vege-
tation outside each gap, a large plastic funnel with a
bottom inside diameter of 20 cm was pressed to the
ground when the herbicide was applied to that gap. All
dead vegetation and emerging seedlings were removed
regularly from each gap until the start of the experiment
at 1 March 1994.
The six gaps within each plot were randomly as-
signed to six different treatments. These treatments in-
volved removal of different plant functional groups,
and were maintained by regular (2–4 weekly) manual
hand-weeding of unwanted seedlings as they emerged
538
DAVID A. WARDLE ET AL.
Ecological Monographs
Vol. 69, No. 4
F
IG
. 1. Total monthly rainfall and mean
monthly air temperature over the study period,
measured at the Ruakura Agricultural Centre
(Hamilton),
;
2 km from the study site.
during the entire course of the experiment. The treat-
ments were:
1) Removal of all plants. This was intended to serve
as a baseline treatment for assessing soil biological and
chemical properties.
2) Removal of all C
4
grasses (occupying 0–57% of
total plant biomass, depending on season and year).
Over 96% of the C
4
grass biomass consisted of summer-
annual species, namely
Panicum dichotomiflorum
Michx. and
Digitaria sanguinalis
(L.) Scop.
3) Removal of all C
3
annual grasses (occupying
0–49% of total biomass). Practically all of the biomass
consisted of the winter-annual
P. annua.
4) Removal of all C
3
grasses (occupying 22–53% of
total biomass). Over 98% of the biomass consists of
P. annua
and
L. perenne.
This treatment was intended
to correspond to treatment (2) by enabling comparison
of C
3
and C
4
grass removal effects (cf. Wedin and Til-
man 1993, Campbell et al. 1996).
5) Removal of dicotyledonous weeds (occupying
5–25% of total biomass). These are essentially short-
lived, rapidly growing ruderal species, and represent
the majority of plant species in these grasslands. The
split between monocotyledonous and dicotyledonous
plant species is recognized as a fundamental functional
split because of the clear separation of niches and strat-
egies of the two sets of species (Wilson and Roxburgh
1994, Wardle and Barker 1997).
6) Removal of no plants.
All plant species in the study site and encountered
during the investigation are listed in Table 1. It is as-
sumed for the purposes of this study that most of the
effects observed in each gap (both aboveground and
belowground) can be attributed to the plant species
occupying these gaps. In this context, edge effects of
the surrounding vegetation are assumed to be of minor
importance because the plants are usually maintained
at a height of
,
6 cm, and because root biomass in the
plant-free gaps was very low compared to that in the
others (see
Results
). Effectively, the plant-free gaps
operated as ‘‘blanks’’ against which other treatment
effects could be assessed.
Over the course of the experiment, the study area
was subjected to periodic light grazing (with a mean
stocking rate of 2.2 cows/ha) and a grazing rotation
length of 1 mo.
Vegetation assessment and harvest
In addition to the
t
5
0 harvest on 1 March 1994,
destructive harvesting took place on six separate oc-
casions (14 September 1994, 7 March 1995, 19 Sep-
tember 1995, 5 March 1996, 17 September 1996, and
5 March 1997); these dates were selected because sum-
mer-annual plant biomass at the study area is maximal
in early March and winter-annual biomass is maximal
in mid-September. For each destructive harvest, all of
the gaps from one randomly selected plot in each block
were selected and processed. For each of those gaps
harvested at the end of the experiment (on 5 March
1997), the vegetation composition was nondestructive-
ly assessed monthly during the entire course of the
experiment. Cattle were excluded from the entire ex-
periment for
$
1 wk prior to each assessment date. Mea-
surements on each gap were performed by using point
quadrat analysis (Goodall, 1952, Jonasson 1983, as de-
scribed by Wardle et al. 1995
a
) to determine the total
ground cover of each component plant species present.
We used a pointing frame with points 2 cm apart, and
took measurements in a grid pattern so that 50 points
were measured for each gap at each sampling; we re-
corded the total number of intercepts for each species.
For each gap subjected to the all-removal treatment
November 1999 539
PLANT COMPOSITION AND ECOSYSTEM PROPERTIES
T
ABLE
1. List of plant species encountered during theexperimental period, their functional groupings, and families towhich
they belong (in parentheses). Bold type denotes the dominant species in functional groups.
Functional group Species
C
4
grasses
Digitaria sanguinalis
(L.) Scop.,
Panicum dichotomiflorum
Michx.,
Paspalum dilatatum
Poir.,
P. distichum
L. (all Gramineae)
C
3
annual grasses
Poa trivialis
L.,
Poa annua
L. (all Gramineae)
C
3
perennial grasses
Bromus wildenowii
Kunth,
Dactylis glomerata
L.,
Lolium perenne
L. (all Gramineae)
Clovers
Trifolium repens
L. (Leguminosae)
Dicotyledonous weeds
Achillea millefolium
L. (Asteraceae),
Amaranthus hybridus
L. (Amarantheraceae),
Anagallis ar-
vensis
L. (Primulaceae),
Aphanes
sp. (Rosaceae),
Bellis perennis
L. (Asteraceae),
Capsella
bursa-pastoris
(L.). Med. (Brassicaceae),
Cerastium glomeratum
Thiull. (Caryophyllaceae),
Chenopodium album
agg. (Chenopodiaceae),
Conyza canadensis
(L.) Cronq. (Asteraceae),
Coronopus didymus
(L.) Sm. (Brassicaceae),
Crepis capillaris
(L.) Wallr. (Asteraceae),
Dau-
cus carota
L. (Umbelliferae),
Geranium molle
L. (Geraniaceae),
Gnaphalium spicatum
Lam.
(Asteraceae),
Hypochaeris radicata
L. (Asteraceae),
Leontodon taraxacoides
(Vill.) Merat
(Asteraceae),
Modiola caroliniana
(L.) G. Don (Malvaceae),
Montia
sp. (Portulacaceae),
Ox-
alis
sp. (Oxalidaceae),
Plantago lanceolata
L. (Plantaginaceae),
P. major
L. (Plantagina-
ceae),
Polygonum aviculare
agg. (Polygonaceae),
Portulaca oleracea
L. (Portulacaceae),
Prunella vulgaris
L. (Labiatae),
Ranunculus repens
L. (Ranunculaceae),
Rumex obtusifolius
L. (Polygonaceae),
R. pulcher
L. (Polygonaceae),
Sagina procumbens
L. (Caryophyllaceae),
Sonchus asper
(L.) Hill (Asteraceae),
Spergula arvensis
L. (Caryophyllaceae),
Stellaria me-
dia
(L.) Vill. (Caryophyllaceae),
Taraxacum officinale
Weber (Asteraceae),
Veronica arvensis
L. (Scrophulariaceae)
and harvested on 5 March 1997, all emerging seedlings
weeded from the gap during the entire experiment were
identified to species level and counted.
Exactly 2 wk prior to each destructive harvest, the
vegetation present in each gap was trimmed to 1 cm
height, and cattle were then excluded until harvest. On
the harvest date (by which time the vegetation had
grown to a height of 4–6 cm), the vegetation was again
trimmed to 1 cm height and the clipped material was
collected to enable determination of net aboveground
production over the 2-wk period (Wardle et al. 1994).
The remaining vegetation was then trimmed at ground
level; the sum of this material and that clipped for
productivity assessment for each gap represented the
total standing aboveground plant biomass at harvest
(i.e., following two weeks’ growth since trimming). All
clipped material (i.e., both 0–1 cm and
.
1 cm height)
was hand-sorted in the laboratory into the component
species, and was oven-dried (80
8
C, 24 h) for produc-
tivity and biomass determinations of each species.
After vegetation removal, two intact soil cores (each
2.5 cm diameter
3
7.5 cm depth) were collected from
each gap for soil microarthropod determinations. Then
the soil in the entire gap was sampled to 7.5 cm depth
using a 20 cm diameter corer; this soil was immediately
taken to the laboratory and processed.
Belowground assessments
The intact cores sampled for microarthropod mea-
surements were placed into a Tullgren invertebrateex-
tractor (Merchant and Crossley 1970, as described by
Wardle et al. 1995
b
), and were left for
;
4 d, after which
the arthropods in the collection fluid were counted and
classified into feeding groups. The total soil sample
from each gap (i.e., that making up the 20 cm diameter
core) was carefully hand-sorted within 24 h of collec-
tion, and all larger invertebrates (mainly insects and
earthworms) present were enumerated and identified to
species level. All live roots were then removed from
the sample and hand-sorted into three root diameter
classes, i.e.,
,
1 mm, 1–3 mm, and
.
3 mm, and oven-
dried for mass determination.
The soil was then subsampled and 250 mL of soil
was used for nematode determination by using a tray
variant of the Baermann method (Southey 1986, Yeates
et al. 1993
b
). Total nematodes were counted under a
stereomicroscope at 40
3
and then were killed and fixed
with double-strength FA 4:1 (100 mL 40% formalde-
hyde:10 mL glacial acetic acid : 390 mL distilled wa-
ter). Subsequently, an average of 126 specimens from
each sample was identified to nominal genus or family
level and placed into six functional groupings occu-
pying three trophic levels, following Yeates et al.
(1993
a
,
b
). These trophic levels (with component func-
tional groups in brackets) are: microbefeeders (bacte-
rial feeders and fungal feeders); predators (top preda-
tors and ‘‘omnivores,’’ i.e., predators that feed at more
than one trophic level), and herbivores (plant parasites
and plant associates).
The remaining soil was sieved (mesh size 4 mm) for
soil microbial and chemical measurements. Microbial
basal respiration was determined as described by War-
dle et al. (1993). This involved adjusting 15 g (dry
mass) soil to 55% moisture content (on a dry mass
basis) by either gradual air-drying or rewetting with a
fine mist, placing it in 169-mL airtight incubation ves-
sels, and incubating at 22
8
C. CO
2
-C evolution between
1hand4hofincubation was then determined by
injecting 1-mL subsamples of headspace gas into an
infrared gas analyzer. Substrate-induced respiration
(SIR; a relative measure of active microbial biomass)
was determined using the approach of Anderson and
Domsch (1978), as modified by West and Sparling
(1986) and Wardle et al. (1993). This was performed
540
DAVID A. WARDLE ET AL.
Ecological Monographs
Vol. 69, No. 4
as for basal respiration, but with an amendment of 6000
m
g glucose/g soil at the beginning of the incubation.
The ratio of basal respiration to SIR was used as a
relative measure of the microbial metabolic quotient,
inversely related to microbial efficiency (Anderson and
Domsch 1985). This quotient is based upon Odum’s
theory of ecosystem succession (Odum 1969), and is
elevated in relatively disturbed or stressed situations
in which the microbial biomass allocates most of the
available C resources to respiration (C loss) rather than
to biomass growth and maintenance. For obtaining rel-
ative measures of active bacterial and fungal biomass,
the selective inhibition technique of Anderson and
Domsch (1975), as modified by West (1986) and War-
dle et al. (1993), was used. This was performed as for
the SIR measurements, except that when the glucose
was added, 10 000
m
g/g of the bacterial inhibitor strep-
tomycin sulphate was also added for bacterial assess-
ment, and 15000
m
g/g of the fungal inhibitor cyclo-
heximide was added for fungal assessment.
Relative total microbial biomass was determined by
the fumigation–incubation method of Jenkinson and
Powlson (1976), as described by Wardle et al. (1993).
Briefly, this involved fumigating (with chloroform) one
15 g (dry mass) subsample amended to 55% moisture
content, and leaving another subsample (16.67 g dry
mass, 55% moisture) unfumigated, reinoculating the
fumigated sample with 1.67 g dry mass soil, and in-
cubating both subsamples for 10 d at 22
8
C in 500-mL
airtight containers, each with a vial of 20 mL 1.0 mol/L
NaOH. Total CO
2
-C released in each container was
assessed by titrating this NaOH against 0.5 mol/L HCl.
The difference in CO
2
-C release between the fumigated
and nonfumigated soil is assumed to be proportionally
related to the total (chloroform-susceptible) microbial
biomass (Jenkinson and Powlson 1976).
For each sample collected on the final sampling date
(5 March 1997), the microbial community structure
was characterized by determining the phospholipid fat-
ty acid (PLFA) composition. Lipids were extracted
from soil using the method of Bligh and Dyer (1959),
as modified by White et al. (1979) and described by
Bardgett et al. (1996). Briefly, 1.5 g (fresh mass) sub-
samples were repeatedly extracted in a one-phase mix-
ture of chloroform, methanol, and citrate buffer (1:2:
0.8 by volume). Extracts were split into two phases by
adding chloroform and buffer; the lower lipid-contain-
ing phase was transferred to a test tube, dried under a
stream of nitrogen, and stored at
2
20
8
C. Lipids were
dissolved in chloroform and fractionated on glass col-
umns containing activated silicic acid. The neutral lip-
ids and glycolipids were eluted with chloroform and
acetone, respectively, and the phospholipids were elut-
ed with methanol. The phospholipid fraction was dried
under a stream of nitrogen and stored at
2
20
8
C until
preparation of fatty acid methyl esters. Samples were
then dissolved in a methanol–toluene mixture and sub-
jected to a mild alkaline methanolysis (Dowling et al.
1986). Resulting fatty acid methyl esters were analyzed
and quantified using a Hewlett Packard 5890 II gas
chromatograph (GC) equipped with a 5972A mass-se-
lective detector (MDSII; Hewlett Packard, San Diego,
California, USA), together with appropriate standards.
Fatty acid nomenclature used was as described by Fros-
tega˚rd et al. (1993
a
,
b
). The abundance of the fatty acid
18:2
v
6 was used as a measure of the phospholipids
derived from fungi, because it is found only in eu-
karyotes and is abundant in a range of fungal species
(Federle 1986). The other main microbial lipids iden-
tified are generally specific to subsets of the bacterial
component of the soil microflora. The ratio of phos-
pholipid 18:2
v
6 to the sum of bacterial phospholipids
was used as a relative measure of fungal to bacterial
biomass (Bardgett et al. 1996).
For each of the soil samples collected on 5 March
1997, decomposition potential was also measured, es-
sentially as described by Wardle et al. (1998
a
). A sub-
sample of soil was amended to 55% moisture content
(dry mass basis) and was used to fill a 9 cm diameter
petri dish, which was then sealed and left to equilibrate
at 22
8
C for 3 d. After this time, a pre-weighed strip of
cellulose filter paper (
;
0.2 g) was inserted into the soil
in each dish; the dish was again resealed and incubated
at 22
8
C for 4 wk. After this time, the filter paper was
removed and cleaned, and the oven-dry dry mass
(80
8
C, 2 h) remaining was determined.
For each soil sample collected at each date, the fol-
lowing chemical analyses were determined: soil pH;
total C concentration through loss on ignition; total N
through Kjeldahl analysis; total P as described by Jack-
son (1958); bicarbonate-extractable P by the Olsen P
method; and ammonium and nitrate contents through
Technicon auto-analysis following extraction with 2
mol/L KCl. In addition, water-soluble C concentrations
were determined as described by Wardle and Ghani
(1995); this involved extracting 10 g (dry mass) soil
in 20 mL water and centrifuging this for 20 min, fol-
lowed by filtration, dichromate oxidation, and titration
with Fe
2
1
.
Data analysis
Responses of plant and soil variables to the plant
removal treatments were analysed by using ANOVA,
following appropriate transformations; least significant
difference (LSD) and standard error of the mean (
SEM
)
values were derived from these for expressing data
variability and comparisons of treatments. Temporal
variability of selected vegetation and soil properties
across the six harvest dates (incorporating variation due
to both inter-year climate differences and season) was
determined by calculating coefficient of variation (
CV
)
values across times (cf. Tilman 1996) for each treat-
ment
3
block combination, with the 10 blocks serving
as the units of replication. Spatial variability was cal-
culated as the
CV
across replicate blocks for each treat-
ment
3
sampling time combination, with sampling
November 1999 541
PLANT COMPOSITION AND ECOSYSTEM PROPERTIES
time as the unit of replication; this was permissible
because different, randomly selected plots were har-
vested at different dates. Correlation analyses were
used to test for relationships between soil organism
variables and plant and soil variables (usually within
sampling times), and, in most cases, the plant-free gaps
(all-plant removal treatment) were excluded because
inclusion of zero values for plant-associated variables
for these gaps would have violated assumptions about
normality of data. Community-level data (i.e., matrices
of taxa
3
gaps) for each of six groups (plants, microbes
[PLFA data], microbe-feeding nematodes, predaceous
nematodes, herbivorous nematodes, and herbivorous
arthropods) were summarized by the use of the ordi-
nation technique detrended correspondence analysis
(Hill and Gauch 1980), but by using detrending by
polynomials, rather than by segments, to enhance ro-
bustness (Ter Braak 1987).Ordinations were performed
by the CANOCO package, version 3.15 (Ter Braak
1987, 1988), and the principal ordination axes were
related to treatments by ANOVA and to the ordination
axes of the other trophic levels through correlation
analysis.
R
ESULTS
Vegetation dynamics
In the devegetated gaps, seedlings emerged contin-
uously over the 3-yr period (Fig. 2). Seedlings of four
C
4
grass species appeared during the experiment, with
most of those in the 1994–1995 summer consisting of
Panicum dichotomiflorum
and, in the subsequent sum-
mers, of
Digitaria sanguinalis.
Large numbers of pe-
rennial C
3
grass seedlings (mostly
Lolium perenne
with
traces of
Bromus wildenowii
Kunth and
Dactylis glom-
erata
L.) emerged in the first few months, with very
few appearing thereafter. Appreciable numbers of an-
nual C
3
grass seedlings (
Poa annua
with traces of
Poa
trivialis
L.) emerged each winter.Dicotyledonous weed
seedlings emerged in most months, with maximal val-
ues during the winter; 33 species were identified, with
no clearly dominant species and with the four most
abundant species (Fig. 2) collectively accounting for
less than half of the seedlings present. Low levels of
Trifolium repens
emerged throughout the experiment.
It is assumed that these seedling measurements rep-
resent an approximate measure of the potentially avail-
able pool of seedlings available for recruitment into
gaps during the course of the experiment.
The C
4
grasses responded strongly to the various
plant removal treatments, especially in the first and
third years (Fig. 3, Table 2). The strongest effects re-
sulted from removal of the C
3
grasses (
L. perenne
and
P. annua
in combination) on
P. dichotomiflorum
cover,
total C
4
grass cover, and C
4
grass species richness dur-
ing the 1994–1995 and 1996–1997 summers. These
effects appear to be caused by
L. perenne,
because
removal of C
3
annual grasses generally did not have
much effect. There were no consistent treatment effects
on
D. sanguinalis.
None of the plant removal treatments had significant
effects on
L. perenne
cover when data were analyzed
on an annual basis (Table 2), but there were ephemeral
significant effects for some sampling dates over the
first 12 mo (Fig. 4), with the highest
L. perenne
cover
sometimes resulting from removal of dicotyledonous
weeds and the lowest cover usually occurring in the
plots from which C
4
grasses had been removed. There
were no detectable treatment responses for
P. annua
(Table 2, Fig. 4), but there were important inter-year
differences, with a much greater cover by
P. annua
in
the first year than in the other two.
None of the dicotyledonous weed species present in
our study showed a statistically significant response to
the treatments that we imposed (
P
.
0.20 for each
species when data were pooled for each year). When
total dicotyledonous plant biomass was considered,
however, there were important treatment effects (Table
2, Fig. 5), which were due to the very strong positive
response to the C
3
grass removal treatment, and were
presumably caused by the removal of competition from
L. perenne.
These effects of
L. perenne
reduced not
only the total cover of dicotyledonous weeds, but also
their species richness, particularly during the cooler
months.
When the cover of
T. repens
was analyzed on an
annual basis, there were significant treatment effects
only in the first year (Table 2), with greatest cover in
the plots in which all C
3
grasses had been removed
(Fig. 6). However, in the subsequent two years, there
were also shorter term significant effects of the C
3
grass
removal treatments, with both enhancement of
T. re-
pens
by
L. perenne
removal in the cooler months, and
reduction of
T. repens
by
L. perenne
removal in the
warmer months (particularly during the summer of
1995–1996). Dynamics of
T. repens
cover in the C
3
grass removal treatment were clearly out of synchrony
with those in the other four treatments, which generally
did not differ much from each other.
The removal treatments had statistically significant
effects on total plant cover (Table 2), but these effects
were typically small (Fig. 7); the greatest negative ef-
fects were caused by the removal of all C
3
grasses
(occupying 22–53% of the total cover in the control
treatment). Total cover in the treatment with all of the
plant functional groups present generally did not differ
much from the C
3
annual grass removal, C
4
grass re-
moval, and dicotyledonous weed removal treatments.
However, in the late summer (February–March) of each
of the three years (i.e., when C
4
grass biomass is nor-
mally maximal), there was a brief period in which plant
cover was least for the C
4
grass removal treatments.
There were large increases in total plant cover, reflect-
ing high productivity, in the first three months of the
study. Total species richness differed significantly be-
tween treatments (Fig. 7), with the lowest richness oc-
542
DAVID A. WARDLE ET AL.
Ecological Monographs
Vol. 69, No. 4
F
IG
. 2. Total numbers of seedlings emerging (and removed) per gap (all plant-removal treatment;
n
5
10) each month
over the entire study period. Length of vertical bars shows magnitude of
6
1
SD
(same scale as vertical axes).
November 1999 543
PLANT COMPOSITION AND ECOSYSTEM PROPERTIES
Fig. 3. Total cover (determined by total number of intercepts by 50 points) of C
4
grass species and total C
4
grass species
richness, in relation to plant removal treatments. Symbols:
m
, all C
3
annual grasses removed;
n
, all C
3
grasses removed;
m
,
all dicotyledonous weeds removed;
V
, no plants removed. Vertical bars depict the magnitude of the standard error of the
mean (
SEM
) (same scale as vertical axes).
544
DAVID A. WARDLE ET AL.
Ecological Monographs
Vol. 69, No. 4
T
ABLE
2. Results of ANOVA testing for significance of treatment (species removal) effects on various ground cover and
species richness parameters, corresponding to the data depicted in Figs. 3–7.
Plant group Dependent variable df
Year 1
FP
Year 2
FP
Year 3
FP
C
4
grasses
P. dichotomiflorum
cover 3, 27 4.31 0.013 1.13 0.353 3.06 0.045
D. sanguinalis
cover 3, 27 1.14 0.352 1.78 0.178 0.98 0.418
Total cover 3, 27 4.73 0.008 1.73 0.183 5.43 0.005
Total species richness 3, 27 6.05 0.003 0.97 0.420 5.41 0.005
C
3
grasses
L. perenne
cover 3, 27 1.49 0.239 0.08 0.969 0.84 0.482
P. annua
cover 2, 18 0.47 0.636 0.56 0.582 1.15 0.339
Dicotyledonous weeds Total cover 3, 27 5.18 0.006 8.18 0.001 2.95 0.051
Total species richness 3, 27 3.20 0.039 4.72 0.009 5.79 0.003
Clovers
T. repens
cover 4, 36 6.93
,
0.001 0.53 0.717 0.49 0.741
All plants Total cover 4, 36 7.26
,
0.001 2.83 0.039 6.21 0.001
Total species richness 4, 36 16.68
,
0.001 6.89
,
0.001 20.70
,
0.001
Notes:
Analyses are performed separately for each of the three years, with each data value consisting of cover or species
richness values for each gap, averaged over all of the measurement events for that year, and with the 10 replicate blocks
serving as the units of replication.
F
IG
. 4. Total cover of the two main C
3
grass species,
Lolium perenne
and
Poa annua,
in response to removal treatments.
Symbols:
m
, all C
3
annual grasses removed;
n
all C
3
grasses removed;
m
, all dicotyledonous weeds removed;
M
, all C
4
grasses removed;
V
, no plants removed. Vertical bars depict the magnitude of the standard error of the mean (
SEM
) (same
scale as vertical axes).
November 1999 545
PLANT COMPOSITION AND ECOSYSTEM PROPERTIES
F
IG
. 5. (A) Total cover of the five most abundant dicotyledonous weedspecies in response to removal treatments,averaged
across all the gaps in which plants of this functional group were permitted (
n
5
40). Symbols:
v
,
Plantago lanceolata
;
M
,
Ranunculus repens
;
m
,
Stellaria media
;
n
,
Cerastium glomeratum
;
m
,
Taraxacum officinale.
(B) Total cover of dicotyledonous
weed species, and (C) their species richness. Vertical bars depict the magnitude of the standard error of the mean (
SEM
)
(same scale as vertical axes).
546
DAVID A. WARDLE ET AL.
Ecological Monographs
Vol. 69, No. 4
F
IG
. 6. Total cover of
Trifolium repens
in response to plant removal treatment. Symbols:
m
, all C
3
annual grasses removed;
n
all C
3
grasses removed;
m
, all dicotyledonous weeds removed;
M
, all C
4
grasses removed;
V
, no plants removed. Vertical
bars depict the magnitude of the standard error of the mean (
SEM
) (same scale as vertical axes).
curring in the gaps in which the dicotyledonous weeds
(i.e., by far the most species-rich functional group) had
been removed.
The plant aboveground biomass and productivity
data showed strong seasonality (Fig. 8). For the C
4
grasses, both variables were generally greatest for the
C
3
grass removal treatments each summer, whereas the
C
3
grasses did not show consistent responses to any
treatments. For the majority of sample dates, dicoty-
ledonous weed biomass and productivity were greatest
when C
3
grasses had been removed. For
T. repens,
biomass and productivity were usually greatest in the
C
3
removal treatment each September, but
T. repens
biomass was generally less in this treatment than in the
other treatments each March. There were no consistent
effects of removal treatments on total aboveground bio-
mass or net primary productivity, but there were some
important inter-year differences. Production of C
3
pe-
rennial and annual grasses and biomass of annual C
3
grasses were highest in the first year, with declining
amounts in the second and third years.
Total root biomass was consistently less in the C
3
removal treatments than in the other treatments (Fig.
9) and, consequently, the shoot-to-root mass ratio was
greater in this treatment than in the others. The shoot-
to-root ratio was often less in the C
4
grass removal
treatments than in the other treatments, particularly for
the March samplings. Root biomass in the gaps with
all plants removed was usually
,
10% of that in the
other treatments.
The species removal treatments resulted in a corre-
sponding reduction in various measures of species rich-
ness calculated for the biomass data, but only for some
sampling occasions (Fig. 10). Removal of dicotyle-
donous weeds resulted in reduced species richness rel-
ative to the other treatments throughout the experiment;
during the March samplings, the same was also true of
the C
4
grass removal treatment. When diversity was
assessed on a ‘‘functional group’’ basis (Fig. 10), the
C
3
grass removal treatment resulted in the lowest di-
versity, but the other removal treatments induced only
relatively small reductions in diversity.
Removal of plant functional groups did not consis-
tently alter temporal and spatial variability of either
plant biomass or productivity measures (Table 3). In
relation to temporal variability (encompassing both in-
ter-year and inter-seasonal variability across all six
sampling occasions for each replicate block), total plant
biomass varied least in the C
3
annual grass removal
treatment, indicating that removal of the C
3
winter-
annual
P. annua
from the species pool had stabilizing
effects. Spatial variability of both aboveground bio-
mass and primary productivity over the 10 replicate
blocks was significantly greater in the C
3
grass removal
treatment than in at least some of the other treatments.
Soil abiotic properties
Although the soil chemical characteristics that we
measured generally showed both significant temporal
and spatial variability, there was little evidence of any
soil chemical response, even when all of the vegetation
was removed (Table 4). The only treatment response
that was significant at
P
5
0.05 was for total soil P,
which over the course of the study was less in the C
3
grass removal treatment (mean P content over exper-
iment
5
0.182%) and the all-plant removal treatment
(mean P content
5
0.183%) than in the other treatments
(range
5
0.190–0.193%). In addition, treatment effects
on both water-soluble C and total N concentrations
were marginally nonsignificant at
P
5
0.05, with the
C
3
grass removal and all-plant removal treatments
yielding lower values than the other treatments. For
most of the soil chemical properties, there were im-
portant differences between the 10 replicate blocks (Ta-
November 1999 547
PLANT COMPOSITION AND ECOSYSTEM PROPERTIES
F
IG
. 7. Total plant cover and species richness in response to plant removal treatments. Symbols:
m
, all C
3
annual grasses
removed;
n
all C
3
grasses removed;
m
, all dicotyledonous weeds removed;
M
, all C
4
grasses removed;
V
, no plants removed.
Vertical bars depict the magnitude of the standard error of the mean (
SEM
) (same scale as vertical axes).
ble 4), as reflected by the relatively high values of the
spatial
CV
(mean/
SD
) across blocks for some of the
variables at the start of the experiment, i.e., soil C
(6.7%), soluble C (23.5%), soil N (17.7%), mineral N
(63.8%), soil P (19.2%), bicarbonate-extractable P
(38.1%), and pH (30.1%). Soil moisture content dif-
fered significantly between treatments (
F
2, 314
5
7.24,
P
,
0.001), because the plant-free treatment had a
greater moisture content (mean across all dates
5
42.9%, dry mass basis) than did the other treatments,
which did not differ significantly from each other
(mean for remaining treatments
5
40.4% moisture).
Soil microbial biomass and activity
Those variables based on soil microbial biomass and
activity showed statistically significant treatment re-
sponses during most of the experimental period, par-
ticularly from the second year onward (Fig. 11). This
was mostly due to the effects of the all-vegetation re-
moval treatment, which caused detectable and consis-
tent reductions in SIR (active biomass), flush of CO
2
after fumigation (total biomass), the SIR to organic C
ratio, and basal respiration. The microbial metabolic
quotient, inversely related to microbial efficiency, was
weakly, although significantly, enhanced by the all-
vegetation removal treatment. Both the bacterial and
fungal components of the active biomass (i.e., those
measured by selective inhibition) followed the same
pattern as SIR (data not presented), although removal
of all plants caused a slight (but significant) shift from
bacteria toward fungi over the final two years of the
experiment (Fig. 11). The other treatments did not dif-
fer much, although many of the biomass-related prop-
erties were slightly enhanced in the nonremoval treat-
ment relative to the others at the end of the experiment
(Fig. 11). There were some important overall temporal
trends, with the bacterial to fungal ratio generally in-
creasing in all treatments throughout the study. De-
composition of added cellulose in the soils collected
on 5 March 1997 did not show a significant response
to the removal treatments (
F
5,41
5
1.96,
P
5
0.105;
data not presented).
Our results show that there was no apparent rela-
tionship between microbial biomass (or related vari-
548
DAVID A. WARDLE ET AL.
Ecological Monographs
Vol. 69, No. 4
F
IG
. 8. Aboveground standing plant biomass and net primary productivity of various plant functional groups in response
to plant removal treatments. Symbols:
m
, all C
3
annual grasses removed;
n
all C
3
grasses removed;
m
, all dicotyledonous
weeds removed;
M
, all C
4
grasses removed;
V
, no plants removed. Vertical bars depict the magnitude of the standard error
of the mean (
SEM
) (same scale as vertical axes). Position of error bars with respect to
y
-axis is arbitrary.
November 1999 549
PLANT COMPOSITION AND ECOSYSTEM PROPERTIES
F
IG
. 9. Total plant root biomass, and ratio of net shoot
mass to root mass, in response to plant removal treatments.
Symbols:
m
, all C
3
annual grasses removed;
n
all C
3
grasses
removed;
m
, all dicotyledonous weeds removed;
M
, all C
4
grasses removed;
V
, no plants removed. Vertical bars depict
the magnitude of the standard error of the mean (SEM) (same
scale as vertical axes).
F
IG
. 10. Total species richness per gap, and Shannon-
Weiner diversity indices using plant biomass data at both the
species level and the functional group level. Functional
groups used are C
4
grasses (nearly all annuals), C
3
annual
grasses, C
3
perennial grasses, dicotyledonous short-lived
weeds, and perennial clovers. Symbols are as for Fig. 9.
T
ABLE
3. Temporal and spatial variability for plant biomass and production variables.
Measurement Response variable
Treatment by removal of:
C
4
grasses
C
3
perennial
grasses
C
3
annual
grasses
Dicoty-
ledonous
weeds Nothing LSD
0.05
\
Temporal variability† Total aboveground biomass 0.402 0.282 0.393 0.370 0.359 0.094
NPP§ 0.598 0.450 0.524 0.536 0.493 0.159
Total root biomass 0.432 0.524 0.522 0.465 0.419 0.166
Spatial variability‡ Total aboveground biomass 0.322 0.318 0.467 0.354 0.386 0.115
NPP§ 0.427 0.418 0.553 0.361 0.414 0.153
Total root biomass 0.390 0.465 0.484 0.459 0.380 0.162
† Expressed as the coefficient of variation (
CV
5
mean/
SD
) across sampling dates for each treatment for each replicate
block.
‡ Expressed as the
CV
across blocks for each treatment for each sampling time.
§ Aboveground net primary productivity.
\
The least significant difference at
P
5
0.05 after ANOVA.
ables), and plant biomass or NPP (Table 5), meaning
that altering these plant variables did not lead to a
corresponding alteration of biomass in the next highest
trophic level (primary saprophytes) or the processes it
regulates (soil CO
2
evolution, decomposition) over the
course of the experiment. Instead the strongest corre-
lates were soil chemical properties such as soil mois-
ture, C, N, and pH.
The vegetation removal treatments did not affect the
temporal variability of either SIR or the fumigation CO
2
flush (Table 6). However, there were important treat-
ment effects on the temporal variability of basal res-
piration, with the
CV
values for the C
3
annual grass
removal treatment being lower than for some of the
other treatments. Temporal variability of SIR, fumi-
gation CO
2
flush, and basal respiration did not show
detectable relationships with either plant biomass or
diversity variables, other than a positive relationship
550
DAVID A. WARDLE ET AL.
Ecological Monographs
Vol. 69, No. 4
T
ABLE
4. Summary of ANOVAs for soil chemical properties over the entire experimental period, testing for plant removal
treatment, and sampling time and blocking effects.
Soil property
Plant removal
effect (PL)
F
5, 314
P
Time effect (T)
F
5, 314
P
PL
3
T interaction
F
25, 314
P
Blocking effect
F
9, 314
P
Total soil C 1.17 0.323 57.37
,
0.001 0.42 0.994 27.05
,
0.001
Water-soluble C 1.88 0.096 145.67
,
0.001 0.69 0.871 1.79 0.070
Total N 1.87 0.098 28.06
,
0.001 0.54 0.966 29.60
,
0.001
Mineral N 0.62 0.684 17.10
,
0.001 1.33 0.139 1.67 0.094
Total P 2.36 0.040 36.54
,
0.001 0.53 0.971 40.62
,
0.001
Bicarbonate-extractable P 1.48 0.196 14.79
,
0.001 0.57 0.976 15.31
,
0.001
Soil pH 1.30 0.262 13.69
,
0.001 1.05 0.399 4.34
,
0.001
Notes:
Time effects could be tested in these analyses without risk of problems associated with pseudoreplication (cf.
Hurlbert 1984) because different, randomly selected plots were harvested at different sampling times. All data analyses of
soil chemical components are calculated on a concentration per unit soil mass basis.
F
IG
. 11. Microbial biomass and activity variables in relation to plant removal treatments. Symbols:
v
, all plants removed;
M
,C
4
grasses removed;
m
,C
3
annual grasses removed;
n
, all C
3
grasses removed;
m
, dicotyledonous weeds removed;
V
,
no plants removed. Vertical bars depict the magnitude of
SEM
values (same scale as vertical axes).
between the
CV
of basal respiration and the
CV
of plant
biomass (Table 7). However, temporal variability of
basal respiration was negatively related to soil C and
N concentrations and positively related to temporal
variability of soil N. Spatial variability of soil microbial
properties showed detectable treatment responses (Ta-
ble 6), with removal of annual C
3
grasses enhancing
variability relative to most other treatments, and with
November 1999 551
PLANT COMPOSITION AND ECOSYSTEM PROPERTIES
the no-plant removal treatment showing less variability
than the other treatments for basal respiration.
Microbial community composition
When considered separately, the principal phospho-
lipid fatty acids (PLFAs) generally responded to treat-
ments in a similar manner to that found for the micro-
bial biomass data (Fig. 12), with the concentration of
each PLFA usually being significantly less in the all-
plant removal treatment than in some of the other treat-
ments. There were also important differences in PLFA
composition (and, hence, in microbial community
structure) between the five treatments with plants pres-
ent (Fig. 12). The treatments did not have a significant
effect on the total amounts of bacterial PLFAs (
F
5,42
5
1.36,
P
5
0.260) or the total microbial PLFAs (
F
5,42
5
1.42,
P
5
0.236), although the levels were least in the
all-plant removal treatment. The ratio of bacterial to
fungal PLFAs was also not significantly related totreat-
ment (
F
5,42
5
1.18,
P
5
0.545).
The Shannon-Weiner diversity index for the micro-
bial PLFAs ranged from 2.57 to 2.63 across the six
treatments, with treatment effects being nonsignificant
(
F
5,42
5
1.18,
P
5
0.336). Further, when all the treat-
ments except the all-plant removal treatments were
considered, PLFA diversity was not significantly cor-
related with plant species diversity (Shannon-Weiner
index), either at the same sampling date (Fig. 13) or
at earlier vegetation measurement dates (Fig. 14). How-
ever, PLFA diversity did show some relatively weak
negative associations with plant functional group di-
versity (Shannon-Weiner index) at earliermeasurement
dates (Fig. 14). With regard to the ordination analyses
of the PLFA data, the main axis was not significantly
related to treatment (
F
5,42
5
1.79,
P
5
0.136), but the
second axis showed a marginally significant treatment
response (
F
5,42
5
2.56,
P
5
0.041), with the all-plants-
removed or only C
4
-grasses-removed treatments being
separated from the other treatments (data not pre-
sented). Further, there were highly significant corre-
lations between the PLFA and plant community ordi-
nation results (Fig. 13), suggesting detectable effects
of plant community structure on microbial community
structure. There were no lag effects of plant community
structure on microbial community structure, with the
PLFA ordination data being most closely related tothat
of the plant community measured at the same time (Fig.
14).
Soil nematode functional and trophic groups
The treatments that we imposed had significant ef-
fects on various components of the nematode fauna,
but these were intermittent and only detectable for
some of the sampling dates (Fig. 15). Generally, the
all-plant removal treatment resulted in lower numbers
of bacterial-feeding nematodes than did the other treat-
ments; during the second half of the experiment, there
was also an apparent reduction of these nematodes in
the C
3
grass removal treatment. Toward the end of the
study, the nonremoval treatment also supported more
bacterial-feeding nematodes than did most of the other
treatments. Fungal-feeding nematodes were less re-
sponsive to treatments, although there were important
treatment effects for the 7 March 1995 sampling, with
the all-plant removal treatment and (to a lesser extent)
the C
4
grass removal treatment supporting fewer nem-
atodes than did the other treatments. For the final two
years, the numbers of top predatory nematodes were
consistently less in the all-plant removal treatment than
in most of the others; the C
3
grass removal treatments
often resulted in more nematodes than the C
3
annual
grass and C
4
grass removal treatment, indicative of ben-
eficial effects of removing
L. perenne.
Omnivorous
nematodes were less abundant in the all-plant removal
treatment than in most of the other treatments from 7
March 1995 onward, although there were also some
negative effects of removing all C
3
grasses. In sum-
mary, for those functional groups involved in the de-
composer food web, it is apparent that the strongest
decrease in biomass was obtained either by removing
all plants, or through removing all C
3
grasses. Plant
pathogens and plant associates showed less obvious
trends, and although differences between treatments
sometimes emerged, these were generally sporadic.
There were important temporal differences between
treatments, with top predatory nematodes showing
maximal population density later in the study and the
other functional groups generally showing maximal
densities at earlier samplings.
Microbe-feeding nematodes showed the strongest
correlations with plant properties early in the experi-
ment, and nematode–microbial correlations tended to
be stronger for the winter samplings (Table 8). Mi-
crobe-feeding nematodes were also consistently related
to soil chemical properties, particularly soil N. Top
predatory nematodes were negatively correlated with
microbe-feeding nematode numbers at the end of the
experiment, and also showed consistent negative re-
lationships with soil N (Table 8).
Temporal variability of nematode populations in
each of the nematode functional groups was not sig-
nificantly related to treatment (data not presented). Fur-
ther, temporal variability of these groups did not show
significant correlations with plant biomass or produc-
tivity, or their temporal variability (data not presented).
In addition, temporal variability of those functional
groups dependent on the microbial energy channels was
not correlated with any of the microbial variables or
their temporal variability. However, the
CV
of the pop-
ulations of top predatory nematodes was significantly
correlated with both soil N content (
r
5
0.474,
P
,
0.001) and the
CV
of soil N content (
r
52
0.389,
P
5
0.007). Similarly, there were few consistent treatment
effects on the spatial variability of soil nematodes, al-
though the spatial
CV
for the fungal-feeding and plant-
parasitic nematodes was significantly greater in the di-
552
DAVID A. WARDLE ET AL.
Ecological Monographs
Vol. 69, No. 4
T
ABLE
5. Pearson’s correlation coefficient values between selected soil microbial properties and plant mass, diversity, and
soil abiotic properties for the final winter (17 September 1996) and summer (5 March 1997) sampling dates.
Plant variables
Microbial variable Sampling
date NPP§
Above-
ground
biomass
MtoD
biomass
ratio
\
Root
biomass
Shannon-Weiner
diversity index
Species Functional
groups
SIR† 17 Sep 1996 0.111
2
0.136 0.066 0.039
2
0.015
2
0.083
5 Mar 1997 0.077 0.034 0.137 0.108
2
0.131
2
0.049
BR‡ 17 Sep 1996 0.067
2
0.025 0.233 0.190
2
0.166 0.053
5 Mar 1997 0.276 0.267 0.143 0.148 0.050
2
0.081
Bacteria: fungi 17 Sep 1996
2
0.063
2
0.110 0.260 0.109
2
0.113
2
0.131
5 Mar 1997
2
0.052
2
0.001
2
0.152 0.230 0.270 0.142
BR: SIR 17 Sep 1996
2
0.106 0.099 0.056 0.071
2
0.049 0.127
5 Mar 1997 0.179 0.180
2
0.056 0.017 0.185 0.023
Fumigation CO
2
flush 19 Sep 1996
2
0.285*
2
0.135
2
0.070 0.027 0.220
2
0.142
5 Mar 1997 0.181 0.283* 0.024 0.138 0.106 0.030
SIR: Total C 17 Sep 1996 0.159
2
0.175 0.091
2
0.021
2
0.047
2
0.076
5 Mar 1997 0.164
2
0.014 0.093 0.094 0.038 0.016
Decomposition rate of cellulose 5 Mar 1997
2
0.082
2
0.136 0.081
2
0.084
2
0.220
2
0.095
Notes:
The non-plant-removal gaps are not included in the analysis. Correlation coefficients that differ significantly from
zero (
n
5
50) are indicated by asterisks: *
P
,
0.05, **
P
,
0.01, ***
P
,
0.001.
† Substrate-induced respiration.
‡ Basal respiration.
§ Net aboveground primary productivity.
\
M, monocot; D, dicot.
cotyledonous weed removal treatment than in some of
the other treatments (data not presented).
Soil nematode community composition
At finer taxonomic levels of resolution, the effects
of plant functional group removal on nematodes were
much clearer (Fig. 16). Over the entire experimental
period, 15 taxa showed distinct responses to treatments,
and there were clear differences between the six treat-
ments with regard to the overall community compo-
sition of nematodes (Fig. 16). These community-level
effects were matched by a reduction in Shannon-Weiner
diversity indices calculated for the microbe-feeding
nematodes in the C
3
grass removal treatment, but this
was not the case for diversity indices for herbivorous
or predaceous nematodes or for nematode functional
groups (Table 9). Further, nematode diversity indices
were not related to those of plants or microbes (PLFA
data) at the end of the experiment (Fig. 13). However,
there were apparent lag effects, with taxonomic diver-
sity indices for microbe-feeding nematodes on 5 March
1997 being most closely related to plant functional
group diversity indices (point quadrat analysis data) of
the same gaps 3 mo earlier, and with predaceous nem-
atode diversity indices showing marginally significant
negative relationships with plant species diversity in-
dices at some earlier sampling dates (Fig. 14). No lag
effects were apparent with regard to herbivorous nem-
atode diversity indices. It is therefore apparent that
diversity indices calculated for nematodes are at best
only weakly related to those of lower trophic levels.
The taxon-specific responses of microbe-feeding
nematodes to treatments were also reflected in the or-
dination analyses; ordination scores differed signifi-
cantly between treatments for at least one of the two
main axes for all sampling dates except the first one
(Table 10). In particular, there were often large differ-
ences between the all-plant removal treatment, or the
C
3
-grass removal treatment, and most of the others. In
contrast, ordination analyses of the herbivorous nem-
atode trophic level showed no consistent treatment ef-
fects (data not presented). There was no close rela-
tionship between the ordination axes of any of the nem-
atode trophic levels and those of plants, but ordination
axes for predaceous nematodes were strongly signifi-
cantly correlated with those of the two next lowest
trophic levels (Fig. 13). Further, lag effects were ap-
parent, with the ordination axes of the microbe-feeding
and predaceous nematodes being most closely corre-
lated with those of the plant community (point quadrat
analysis data) 1 mo earlier and 2 mo earlier, respec-
tively (Fig. 14).
Soil-associated mesofauna and macrofauna
The mesofaunal components of the decomposer food
web were not strongly influenced by plant species re-
moval effects. Removal of all plants resulted in reduced
populations of Collembola relative to the other treat-
ments, but there were no clear or consistent differences
among the other five treatments (Fig. 17). Mite pop-
ulations were low and sporadic, and treatment effects
were nonsignificant over the experimental period for
November 1999 553
PLANT COMPOSITION AND ECOSYSTEM PROPERTIES
T
ABLE
5. Extended.
Soil chemical variables
Soil moisture Soil C Soil N Soil pH
0.532*** 0.172 0.409** 0.485***
0.409** 0.344* 0.249 0.647***
0.372** 0.279* 0.389** 0.354*
0.239 0.393** 0.259 0.393***
2
0.356*
2
0.058 0.061 0.026
2
0.143
2
0.140
2
0.144
2
0.043
2
0.205 0.022
2
0.095
2
0.217
2
0.233 0.135 0.028
2
0.368**
0.234 0.213 0.480*** 0.374**
0.372** 0.306* 0.240 0.671***
0.286*
2
0.335* 0.129 0.378**
0.108
2
0.511***
2
0.227 0.423**
2
0.074 0.126 0.244
2
0.143
T
ABLE
7. Pearson’s correlation coefficients between tem-
poral variability of microbial biomass or activity measure-
ments (determined as coefficients of variation across six
sampling dates) and various plant and soil properties,
across the 50 replicate block
3
treatment combinations
(plant-free treatment gaps are not included in analysis).
Soil or plant variable
CV
for microbial variable
SIR‡ Fumigation
CO
2
flush BR§
Mean NPP† 0.032 0.247
2
0.090
CV
of NPP 0.202
2
0.128 0.000
Mean plant biomass
2
0.024 0.138 0.043
CV
of mean plant bio-
mass 0.166 0.226 0.378**
Plant species richness
2
0.021 0.034
2
0.018
Shannon-Weiner di-
versity index (plant
species) 0.160 0.141 0.096
Shannon-Weiner di-
versity index (plant
functional groups) 0.078
2
0.009 0.127
Mean soil C 0.048 0.108
2
0.481***
CV
of mean soil C
2
0.245
2
0.148
2
0.031
Mean soil N
2
0.002 0.149
2
0.404**
CV
of mean soil N 0.138 0.012 0.536***
Note:
Correlation coefficients that differ significantly from
zero are indicated by asterisks: *
P
,
0.05, **
P
,
0.01,
***
P
,
0.001.
† Net primary productivity.
‡ Substrate-induced respiration.
§ Basal respiration.
T
ABLE
6. Temporal and spatial variability for microbial biomass and activity variables.
Measurement Response variable
Treatment by removal of:
All
plants C
4
grasses
C
3
annual
grasses All C
3
grasses
Dicoty-
ledonous
weeds No
plants LSD
0.05
\
Temporal variability† SIR§ 0.294 0.301 0.316 0.318 0.291 0.272 0.065
Fumigation CO
2
flush 0.153 0.196 0.210 0.219 0.199 0.181 0.047
Basal respiration 0.338 0.405 0.319 0.406 0.346 0.364 0.082
Spatial variability‡ SIR§ 0.193 0.212 0.272 0.239 0.218 0.233 0.047
Fumigation CO
2
flush 0.131 0.147 0.201 0.146 0.147 0.141 0.045
Basal respiration 0.217 0.198 0.202 0.190 0.209 0.159 0.045
† Expressed as the coefficient of variation (
CV
5
mean/
SD
) across sampling dates for each treatment for each replicate
block.
‡ Expressed as the
CV
across blocks for each treatment for each sampling time.
§ Substrate-induced respiration.
\
Least significant difference at
P
5
0.05 after ANOVA.
both saprophagous/fungivorous oribatid mites (
F
5, 314
5
1.25,
P
5
0.284) and predatory mites (
F
5, 314
5
0.38,
P
5
0.864). Further, none of these mesofaunal groups
showed statistically significant relationships with any
of the plant or soil variables when correlation analysis
was used (data not presented).
The earthworm (Lumbricidae) fauna consisted en-
tirely of two endogeic species, i.e.,
Aporrectodea cal-
iginosa
(Savigny) and
Lumbricus rubellus
Hoffmeister.
Although there were significant overall effects of treat-
ments on both species, the only treatment that had a
consistent influence was the all-plant removal treat-
ment, which generally reduced populations of both spe-
cies throughout most of the experimental period (Fig.
18). Correlation analysis revealed no detectable rela-
tionship between earthworm populations and plant bio-
mass or productivity (data not presented), and earth-
worms were not related to plant species composition
as long as plants were present.
A. caliginosa
sometimes
showed significant relationships with soil P, pH, and
N, but these relationships were not consistent over
time, and even when significant, correlation coeffi-
cients were usually below 0.40 (data not presented).
In contrast, the most abundant soil-associated her-
bivorous arthropod species present all showed clear
relationships with treatments (Fig. 19).
Floresianus
sordidus
Hustache (Curculionidae) only occurred in the
March samplings each year. Larval populations were
significantly reduced by all treatments except the C
3
annual grass, whereas adults were only significantly
reduced by the all-plant removal treatment.
Listroderis
difficilis
Germain (Curculionidae) was present only in
the 14 September 1994 sampling, where it appeared in
reasonable numbers; this species was significantly re-
554
DAVID A. WARDLE ET AL.
Ecological Monographs
Vol. 69, No. 4
F
IG
. 12. Concentrations of the principal microbial phospholipid fatty acids (PLFAs) in soil, in response to the plant
removal treatments, expressed as rank-transformed data. For each acid type, values expressed are mean rank (1
5
highest
concentration, 6
5
lowest concentration) for each treatment relative to the other treatments, averaged over all 10 replicate
blocks. All PLFAs are bacterial except for 18:2
v
6, which is fungal. Across treatments, bars for the same acid type that are
topped with the same letter are not significantly different (
P
.
0.05) according to the least significant difference (LSD) test
following ANOVA.
duced in the C
4
removal and all-plant removal treat-
ments.
Sitona lepidis
Gyllenhal (Curculionodae) oc-
curred only in the 17 September 1996 sampling, con-
sistent with its very recent accidental introduction to
New Zealand and subsequent rapid spread over the pre-
vious few months. Both adults and larvae were inhib-
ited in the all-plant removal treatment and (for adults)
in the C
3
and the C
4
grass removal treatments.
Nau-
pactus leucoloma
Boheman (Curculionidae) was abun-
dant at all sampling dates. Larval populations were
significantly elevated in the C
4
grass removal treatment
and suppressed in the all-plant removal treatment rel-
ative to the no-plant removal treatment; significant dif-
ferences were also apparent between the different re-
moval treatments.
Costelytra zealandica
(White) (Scar-
abaeidae), which was only present in the 7 March 1997
sampling, showed only relatively weak treatment re-
sponses. Populations of
Heteronychus arator
(F.) (Scar-
abaeidae), which were only present each March, were
enhanced in the C
4
grass and dicotyledonous weed re-
moval treatments relative to the nonremoval treatment.
Correlation analyses revealed few significant rela-
tionships between populations of herbivorous arthro-
pods and plant biomass or productivity. Further, or-
dination analyses of the herbivorous arthropod com-
munity structure at each sampling date revealed little
evidence of treatment effects (data not presented), and
there was no clear relationship with the ordination anal-
yses of the plant community structure of the same gaps
(Fig. 13). However, there was an important lag effect,
with the main arthropod ordination axis for the 5 March
1997 data being most strongly related to the ordination
axes of the plant community (point quadrat analysis
data) for the same gaps 2 mo earlier (Fig. 14).
Species richness of the herbivorous arthropod fauna
over the whole experiment was much less in the all-
November 1999 555
PLANT COMPOSITION AND ECOSYSTEM PROPERTIES
F
IG
. 13. Correlation coefficients between different trophic levels in decomposer and herbivore food chains, with regard
to community-level attributes (taxonomic diversity and ordination axis scores). Data used are from the 5 March 1997sampling
with data from the plant-free treatment excluded. Each of the correlation coefficients presented for the ordination data is a
multiple correlation coefficient between the main axis of the higher of the two trophic levels being considered and the two
main axes of the lower of the two trophic levels. Microflora data are from PLFA analysis. Percentages of total variation in
data set explained by ordination axes I and II respectively for each group are as follows: predaceous nematodes, 39.3, 22.6;
microbe-feeding nematodes, 15.8, 13.9; microflora, 44.9, 16.4; plants, 31.1, 9.7; herbivorous nematodes, 20.7, 14.4; herbiv-
orous arthropods, 25.7, 15.6. Asterisks indicate that the correlation coefficient is significantly different from 0: *
P
,
0.05;
**
P
,
0.01; ***
P
,
0.001.
plant removal treatment than in all of the other treat-
ments, which did not differ significantly from each oth-
er (Fig. 20). However, removal of C
4
grasses signifi-
cantly enhanced the Shannon-Weiner diversity index
relative to the nonremoval treatment. Further, there
were significant negative relationships between Shan-
non-Weiner diversity indices for plants and herbivorous
arthropods throughout the experiment (e.g., Fig. 13).
There was also a negative lag effect of plant functional
group diversity (point quadrat analysis data) and her-
bivorous arthropod data, with the strongest relation-
ships occurring between arthropod diversity at 5 March
1997 and plant functional diversity 3 mo earlier (Fig.
14).
D
ISCUSSION
Our study has shown that removal of plant functional
groups can have important effects on the composition
of the remainder of the flora, and that this can influence
vegetation dynamics, biomass, productivity, and di-
versity. These responses of the aboveground subsystem
have the potential to induce corresponding responses
in the belowground subsystem, influencing soil food
webs, community composition of soil organisms and
their diversity, and, ultimately, ecosystem properties
and processes. We now discuss each of these issues in
turn.
Vegetation responses
When a major component of the flora is removed
from the species pool, competition theory predicts that
other species should benefit and, therefore, at least par-
tially compensate for the lost production and biomass
of the removed species. The degree of compensatory
response detected should be related to the degree of
niche overlap between the removed and remaining spe-
cies, especially in relation to their utilization of limiting
resources (Hooper and Vitousek 1997). In our study,
such compensatory effects were often apparent, con-
sistent with the hypotheses that we proposed. The
strongest treatment responses by most components of
the flora were to the removal of all C
3
grasses (occu-
pying 22–53% of total biomass). Because removal of
C
3
annual grasses (occupying 0–49% of biomass) alone
did not exert much effect, we therefore conclude that
C
3
perennial grasses, consisting almost entirely of
Lol-
ium perenne,
were responsible for many of the treat-
ment effects that we observed, consistent with previous
investigations (Wardle et al. 1995
a
, Campbell et al.
1996). The data for the
L. perenne
3
Trifolium repens
interaction were, however, less consistent; there were
periods during the winter when
T. repens
growth was
strongly stimulated by
L. perenne
removal, and some
periods in the summer when it was strongly inhibited
by
L. perenne
removal (especially in early 1996). This
556
DAVID A. WARDLE ET AL.
Ecological Monographs
Vol. 69, No. 4
F
IG
. 14. Time lag correlation coefficients between community-level attributes of consumer organisms (assessed on 5
March 1997) and plants assessed on the same and earlier sampling dates for the same gaps. Analyses involve
n
5
50 gaps
(plant-free gaps not included); data points outside the dotted horizontal lines marked with
P
values are significantly different
from 0 at that level of probability. For the ordination subgraphs, each of the correlation coefficients presented is a multiple
correlation coefficient between the main axis of the consumer group and the two main axes of the plant community ordination.
SWI
5
Shannon-Weiner diversity index. Symbols for consumer organisms:
v
, herbivorous arthropods;
M
, herbivorous
nematodes;
V
, microflora (PLFA analysis);
m
, microbe-feeding nematodes;
n
, predaceous nematodes.
summer stimulation is inconsistent with studies indi-
cating generally suppressive effects of
Lolium
species
on
T. repens
(e.g., Mann and Barnes 1953, Harris
1987), whereas the suppressive effect of
L. perenne
removal in summer partially supports the observation
that this species is less suppressive of
T. repens
under
drier conditions (Thomas 1984).
Our data are consistent with the view that species
are not equal in terms of their ecosystem-level impli-
cations (Allen and Forman 1976, Goldberg 1987, Pow-
er et al. 1996).
L. perenne
clearly exerted a dispro-
portionate effect on the other components of the flora,
meaning that the ecophysiological traits of this species
presumably conferred some competitive advantage (see
Abdul-Fatih and Bazzaz 1979, Austin and Smith 1989,
Huston 1994, Wardle et al. 1998
a
). One such trait may
be the relative allocation of mass to aboveground and
belowground tissues;
L. perenne
clearly had a far lower
shoot to root ratio than did most of the other species;
removal of all C
3
grasses resulted in a highly significant
(and for the 7 March 1995 sampling, very large) en-
hancement of the total shoot mass to root mass ratio
November 1999 557
PLANT COMPOSITION AND ECOSYSTEM PROPERTIES
F
IG
. 15. Response of nematode functional groups to plant removal treatments. Symbols:
v
, all plants removed;
M
,C
4
grasses removed;
m
C
3
annual grasses removed;
n
, all C
3
grasses removed;
m
, dicotyledonous weeds removed;
V
,no
plants removed. Vertical bars depict the magnitude of the standard error of the mean (
SEM
) values (same scale as vertical
axes).
in the gaps. This means that
L. perenne
probably has
very different strategies for nutrient acquisition than
do plants of the other functional groups present in our
study (Chapin 1980, Ingestad and A
˚gren 1988).
The compensatory effects between different com-
ponents of the flora infer that removal of functional
groups does not generally cause large effects with re-
gard to total plant cover, biomass, or productivity.
However, intermittent effects are apparent. For exam-
ple, total aboveground plant biomass was much greater
on 7 March 1995, when C
3
grasses were removed, and
this is clearly due to the very high biomass of C
4
species
present in the C
3
grass removal gaps. This is because
removing
L. perenne
enables greater C
4
grass seedling
establishment, inducing greater C
4
grass growth during
periods in the summer when other species are sup-
pressed by moisture limitation. In contrast, removal of
C
4
grasses caused reduced total aboveground biomass
on 5 March 1996, and temporarily reduced total cover
in the late-summer period of each year. This is attrib-
utable to the inability of the other species present to
occupy part of the niche left vacant by removing C
4
grasses during the summer; the absence of C
4
species
simply results in a higher incidence of bare ground. In
a similar vein, removal of
L. perenne
results in reduced
total root biomass relative to the other treatments, sim-
ply because no other species is capable of occupying
as much of the soil volume as is
L. perenne.
558
DAVID A. WARDLE ET AL.
Ecological Monographs
Vol. 69, No. 4
T
ABLE
8. Pearson’s correlation coefficients between nematode populations in the microbe-feeder and predator categories of
the decomposer food web, and the properties of lower trophic levels.
Net primary
productivity vs.
MFN‡ PN§
Total plant
biomass vs.
MFN PN
Soil N vs.
MFN PN
SIR vs.
MFN PN MFN vs. PN
Trophic levels
compared†
Sampling date 1 vs. 3 1 vs. 4 1 vs. 3 1 vs. 4 1 vs. 3 1 vs. 4 2 vs. 3 2 vs. 4 3 vs. 4
14 September
1994 0.140 0.184
2
0.067 0.246 0.306*
2
0.389** 0.426**
2
0.298* 0.025
7 March 1995 0.291*
2
0.090 0.292*
2
0.221 0.444**
2
0.330* 0.083
2
0.191
2
0.140
19 September
1995 0.362** 0.020 0.213 0.084 0.465***
2
0.413** 0.505***
2
0.175
2
0.305*
5 March 1996 0.109
2
0.175
2
0.152 0.021 0.361**
2
0.199 0.144
2
0.087
2
0.260
17 September
1996 0.086
2
0.065
2
0.071 0.030 0.330*
2
0.464***
2
0.014
2
0.155
2
0.477***
5 March 1997 0.016 0.109 0.147 0.005 0.016
2
0.070 0.072 0.128
2
0.481***
Note:
Correlation coefficients that differ significantly from 0 (at
N
5
50 gaps; plant-free gaps not included in the analysis)
are indicated by asterisks: *
P
,
0.05, **
P
,
0.01, ***
P
,
0.001.
† Numbering for trophic levels: 1, resource base (sensu Wardle 1995); 2, primary consumer; 3, secondary consumer; 4,
tertiary consumer. Relationships between trophic levels 1 and 2 are shown in Table 4.
‡ Microbe-feeding nematodes.
§ Predaceous nematodes (top predators and omnivores).
There were important patterns of temporal variation
throughout the study, with rapid initial increases in
cover, NPP, and biomass (reflecting colonization and
initial succession on the bare ground), followed by a
decline after a few months in most treatments, probably
due, in part, to unusually dry conditions during De-
cember 1994. Plant biomass and cover increased again
over the third year of the study as conditions became
more moist. It is unclear whether the system had
reached an asymptotic phase with regard to these plant
properties by the end of the study (or whether a longer
time period would be necessary for this to occur), al-
though there were no clear successional trends during
the final two years of the study. Exclusion of plant
functional groups from the species pool did not sig-
nificantly alter temporal variability of NPP or plant
biomass, and thus did not affect stability over the ex-
perimental period (with the exception of reduced vari-
ability in the C
3
annual grass removal treatment). Our
study was not of sufficient duration to separate the
effects of the two components of this temporal vari-
ability, i.e., inter-year and inter-seasonal (March vs.
September) variability, but despite this, our data still
provide little evidence that excluding components of
the total flora has destabilizing influences (cf. Tilman
1996). However, our study does provide clearevidence
that removal of
L. perenne
enhanced spatial variability
of both biomass and NPP across replicate blocks. There
were large differences between replicate blocks
throughout the study and it is apparent that the presence
of
L. perenne
was able to at least partially reduce this
variation and enhance uniformity across plots, at least
at the spatial scale that we considered.
Our results supported our hypotheses, in that re-
moval of
L. perenne
also enhanced the species richness
of the dicotyledonous weeds and, in the early summer
period, that of the C
4
grasses. This means that at the
within-gap scale, some plant species are simply ex-
cluded by competition from
L. perenne.
This is con-
sistent with earlier work pointing to the ability of some
plant species to reduce species richness of the remain-
der of the species pool (e.g., Gurevitch and Unnasch
1989, Ten Harkel and van der Muelen 1996, Collins et
al. 1998; but see Hils and Vankat 1982, Wardle and
Barker 1997). Our results suggest that compensatory
effects, such as we observed for plant cover, NPP, and
biomass, also occur with regard to plant species rich-
ness, in that removal of a subset of the flora can be
offset by a corresponding increase in the species rich-
ness of the remainder of the flora. This helps to explain
why removal of significant components of the flora
often did not result in a drop in overall species richness.
Decomposer food web responses
We found that removing all plants from gaps over a
3-yr period (i.e., resulting in zero NPP and plant bio-
mass) had adverse effects relative to the other treat-
ments for all three consumer trophic levels, indicative
of strong bottom-up control when extreme differences
in NPP and plant biomass occurred. This is consistent
with the study of Mikola and Seta¨la¨ (1998
b
), which
found that adding basal resources (which simulate in-
creased root NPP) can simultaneously increase biomass
in adjacent trophic levels, and is therefore partially
inconsistent with the predictions of both basic trophic-
dynamic models (e.g., Rosenzweig 1971, Oksanen et
al. 1981) and the hypotheses that we formulated. How-
ever, as long as plants were present, there were few
consistent relationships between these plant variables
and any of the decomposer food chain components.
Further, temporal patterns in NPP were not matched by
corresponding shifts in microbes or predatory nema-
November 1999 559
PLANT COMPOSITION AND ECOSYSTEM PROPERTIES
F
IG
. 16. Response of selected nematode taxa to plant removal treatments, averaged over the entire experimental period,
expressed as rank-transformed data. For each taxon, values are expressed are mean rank (1
5
highest concentration, 6
5
lowest concentration) for each treatment relative to the other treatments, averaged over all 60 replicate block
3
sampling
time combinations. Functional groupings: plant associates (
Cephalenchus
); plant parasites (
Heterodera, Helicotylenchus,
Pratylenchus
); bacterial feeders (Cephalobidae, Rhabditidae, Panagrolaimidae,
Plectus, Anaplectus
); fungal feeders (
Aphe-
lenchus, Aphelenchoides,
Leptonchidae); top predators (Mononchidae); omnivores (Dorylaimidae, Aporcelaimidae). For each
taxon, bars across treatments topped with the same letter are not significantly different (
P
.
0.05) according to the least
significant difference (LSD) test following ANOVA.
T
ABLE
9. Shannon-Weiner diversity index for taxa (mainly genera) in three nematode trophic groups, and for the nematode
functional group diversity (all nematodes were classified into the six functional groups shown in Fig. 15), in response to
vegetation removal treatments, averaged over the entire experimental period.
Nature of diversity Trophic grouping
Treatment by removal of:
All
plants C
4
grasses C
3
annual
grasses All C
3
grasses
Dicoty-
ledonous
weeds No
plants LSD
0.05
†
Diversity of taxa microbe feeders 1.66 1.61 1.69 1.46 1.62 1.72 0.16
herbivores 1.43 1.53 1.43 1.46 1.45 1.51 0.18
predators 0.65 0.83 0.67 0.73 0.73 0.77 0.20
Diversity of func-
tional groups all 1.70 1.70 1.66 1.71 1.71 1.69 0.10
† Least significant difference at
P
5
0.05, derived from ANOVA testing for treatment, time, treatment
3
time, and blocking
effects.
560
DAVID A. WARDLE ET AL.
Ecological Monographs
Vol. 69, No. 4
T
ABLE
10. Average detrended correspondence analysis (DCA) values (rank-transformed) for the two axes explaining the
greatest proportion of variation following ordination of the microbe-feeding nematode community data for each sampling
date.
Sampling date Ordination
axis
Total
variation
explained
(%)
Treatment by removal of:
All plants C
4
grasses C
3
annual
grasses All C
3
grasses
Dicoty-
ledonous
weeds No plants
14 Sep 1994 I 18.7 27.1
a
30.1
a
28.4
a
34.3
a
32.9
a
30.3
a
II 15.1 27.3
a
34.4
a
37.5
a
27.6
a
25.6
a
30.7
a
7 Mar 1995 I 19.3 22.8
bc
37.7
a
38.5
a
20.7
c
34.0
ab
29.5
abc
II 12.8 22.3
b
37.4
ab
29.2
ab
39.6
a
32.4
ab
22.3
b
19 Sep 1995 I 16.0 22.6
b
29.3
ab
29.3
ab
34.9
ab
37.3
a
29.8
ab
II 12.8 29.9
a
25.9
a
30.1
a
30.1
a
32.1
a
35.1
a
5 Mar 1996 I 18.2 35.5
a
31.1
a
27.3
a
30.2
a
32.3
a
26.5
a
II 12.7 28.8
ab
38.5
a
20.3
b
31.5
ab
34.5
a
29.7
ab
17 Mar 1996 I 19.1 24.5
b
32.9
ab
27.6
b
25.0
b
31.8
ab
41.4
a
II 11.9 30.4
ab
29.4
ab
29.4
ab
31.3
ab
42.2
a
20.4
b
5 Mar 1997 I 15.8 38.6
a
30.5
ab
28.5
ab
30.1
ab
26.2
ab
25.2
b
II 14.9 34.5
a
31.1
a
25.3
a
30.5
a
33.6
a
24.6
a
Note:
Numbers followed by the same superscript letter within each row are not significantly different at
P
,
0.05 (least
significant difference test following ANOVA on rank-transformed data).
F
IG
. 18. Population dynamics of the two most abundant
earthworm species in relation to plant removal treatments.
Symbols are as for Fig. 17.
F
IG
. 17. Collembola populations in relation to plant re-
moval treatments. Symbols:
v
, all plants removed;
M
,C
4
grasses removed;
m
C
3
annual grasses removed;
n
, all C
3
grasses removed;
m
, dicotyledonous weeds removed;
V
,no
plants removed. Vertical bars depict the magnitude of the
standard error of the mean (
SEM
) values (same scale as vertical
axes).
todes, although patterns of decline in NPP over much
of the study did correspond to a decline in microbe-
feeding nematodes. Generally, however, our results
suggest that as long as plants are present, the com-
ponents of the soil food chain that we considered are
not strongly driven by NPP in the manner hypothesized
(and sometimes shown) for aboveground food chains
(e.g., Oksanen et al. 1981, Power 1992, Vande Koppel
et al. 1996). Our failure to detect a consistent effect of
NPP on the measured soil food web components is
partially consistent with previous studies that have
found relationships between NPP and microbial bio-
mass to be either positive (D. Zak et al. 1994) or neg-
ative (Wardle et al. 1995
a
), and those that have shown
uncertain relationships between NPP and numbers of
microbe-feeding nematodes (Yeates and Coleman
1982, Yeates 1987).
We identify three possible reasons as to why our
hypotheses were not supported and why soil food web
properties may be only weakly related to plant variables
such as NPP and biomass. Firstly, soil food webs, un-
like aboveground food webs, are controlled by long-
term effects of litter input, so the effects of shifts in
these plant variables may be manifested over much
longer time scales than the 3-yr duration of our study.
In this context, it is apparent that relatively stable soil
November 1999 561
PLANT COMPOSITION AND ECOSYSTEM PROPERTIES
F
IG
. 19. Response of selected herbivorous arthropod taxa to plant removal treatments, averaged over the entire experi-
mental period, expressed as rank-transformed data. For each taxon, values expressed are mean rank (1
5
highestconcentration,
6
5
lowest concentration) for each treatment relative to the other treatments, averaged over all replicate block
3
sampling
time combinations. For each taxon, bars across treatments topped with the same letter are not significantly different (
P
.
0.05) according to the least significant difference (LSD) test following ANOVA. Data are only averaged over those sampling
dates for which the arthropod species was present, and ANOVA analyses only incorporate these dates.
chemical variables, especially soil C and N levels, were
much more strongly correlated with soil food web prop-
erties than were plant treatment effects, when all gaps
containing plants were considered. In particular, soil N
appeared to work as a bottom-up control, affecting all
components of the food chain, although these effects
were frequently negative for the predatory nematodes.
This latter effect is consistent with the negative asso-
ciation that sometimes occurs between predatory and
bacterial-feeding nematodes (Wardle etal. 1995
b
). Our
results suggest that effects of spatial variability on soil
properties, usually determined mainly by historical
vegetation properties over the past few centuries (Tate
1992), are more likely to determine soil food web com-
ponents than are contemporary patterns of plant bio-
mass or productivity. Secondly, with regard to the de-
composer organisms, the quality of organic matter en-
tering the soil may be more important than the amounts
of material added (Wardle and Lavelle 1997). In this
light, there were detectable effects of plant community
composition on components of the decomposer food
chain that we considered; in particular, both the C
3
and
C
4
grass removal treatments influenced the microbe-
feeding and top predatory nematode populations.
Thirdly, the complex interplay of top-down and bot-
tom-up forces that structure and stabilize decomposer
food webs (Wardle 1995, De Ruiter et al. 1995) is likely
to buffer food web components against shifts in NPP
and plant biomass and community structure. The soil
microbial biomass, which is the component that is most
likely to respond to shifts in NPP, has previously been
shown to be unresponsive to such changes, simply be-
562
DAVID A. WARDLE ET AL.
Ecological Monographs
Vol. 69, No. 4
F
IG
. 20. Response of herbivorous arthropod species rich-
ness and diversity (Shannon-Weiner index) to plant removal
treatments, averaged over the entire experimental period.
LSD is the least significant difference at
P
5
0.05, determined
following ANOVA testing for treatment, time, and blocking
effects.
cause it was grazed by microbe-feeding nematodes
(Yeates et al. 1997). Similarly, the complex nature of
predator–prey cycles that can occur between bacterial-
feeding and top predatory nematodes (Wardle et al.
1995
b
, Yeates and Wardle 1996) could reasonably be
expected to reduce the likelihood of detecting associ-
ations between these components at fixed sampling
times.
The larger soil decomposer animals, such as earth-
worms, Collembola, and mites, were highly unrespon-
sive to plant variables. Although populations of Col-
lembola and earthworms were often severely reduced
where plants were entirely excluded, as long as plants
were present, there was little evidence that NPP, plant
biomass, or plant species composition had important
effects on these organisms. Thus, even large differ-
ences in the quality and quantity of resource input, such
as that which occurred across treatments in our study,
do not emerge as significant population determinants
for the larger, generalist saprophagous organisms pres-
ent in our system.
Soil organisms: responses of community structure
and diversity patterns
Although whole-trophic-level responses to the ma-
nipulation of plant community structure were generally
weak, at finer levels of taxonomic resolution, there
were strong multitrophic responses to the manipulation
treatments, consistent with the hypotheses that we pro-
posed. With the PLFA data, most fatty acids of micro-
bial origin showed responses to treatments, although
the principal response was to the removal of all plants.
These results are generally consistent with earlier stud-
ies predicting that vegetation composition can operate
as a determinant of microbial community structure (J.
Zak et al. 1994), presumably because of the patterns
of specificity of different microbial species for re-
sources of different quality (Robinson et al. 1994).
These effects were also apparent at higher trophic lev-
els; for example, half of the microbe-feeding nematode
taxa depicted in Fig. 16 showed clear preferences for
treatments occupied by some plant species over those
occupied by others, indicating that plant community
structure affects microbe-feeding nematode commu-
nities by altering the types of microbes that are present.
There are few previous studies demonstrating such ef-
fects, although Freckman and Ettema (1993) and Was-
ilewska (1995) provide data suggesting that some bac-
terial-feeding nematode taxa are responsive to plant
species differences. Plant community effects may also
have the potential to affect taxonomic composition of
nematodes in the fourth trophic level; mononchid and
dorylaimid nematodes both showed clear treatment
preferences. The ordination data indicate that the struc-
ture of microbial, microbe-feeding nematode, and pre-
daceous nematode communities are linked to plant
community structure, although there are apparent time
lags for the latter two groups, reflective of the gener-
ation times of those nematodes. In this light, it is ap-
parent from Fig. 14 (top right subgraph) that the main
ordination axis summarizing the community structure
of the primary detrital consumers (microbes) was most
closely linked to that summarizing plant community
structure measured at the same date (i.e., 5 March
1997). The main axis for the secondary consumers (mi-
crobe-feeding nematodes) was most closely related to
that for the plant community measured 1 mo earlier;
and the main axis for the tertiary consumers (preda-
cious nematodes) was best related to that for the plant
community measured 2 mo earlier. Therefore, our data
show that removal of plants from an ecosystem can
have detectable effects on the community structure of
decomposer organisms, which may be manifested over
several trophic levels.
Curiously, herbivorous nematodes were less closely
linked to plant community structure than were those
nematodes involved in the decomposer food web, al-
though four taxa did show significant preferences for
some treatments over others. One particularly surpris-
ing result is that there were appreciable numbers of
herbivorous nematodes in the plant-free gaps, even af-
ter three years. The ability of plant-parasitic nematodes
to survive for lengthy periods in the absence of host
plants has been recorded previously (e.g., Harrison and
Hooper 1963, McKendry 1987), and may be due to
November 1999 563
PLANT COMPOSITION AND ECOSYSTEM PROPERTIES
survival strategies based on anhydrobiosis, at least in
dry conditions (Demeure and Freckman 1981), or be-
cause these nematodes could have survived on other
resources present in the soil, such as nonliving plant
material (see Eriksson 1974, Verdejo-Lucas and Pin-
ochet 1992) or soluble soil C (see Nicholas 1962).
Strong patterns of plant specificity were demonstrat-
ed by the main species of herbivorous arthropods pres-
ent. Populations of the commonest curculionid species
were generally smaller under the dicotyledonous weed
removal treatment than the nonremoval treatments,
consistent with literature suggesting that many of these
species prefer dicotyledonous rather than monocoty-
ledonous species (Parker and Berry 1950, May 1966,
1993, Lanterni and Marvaldi 1995). The beneficial ef-
fects of removal of C
4
grasses for
Naupactus leucoloma
are consistent with the inferior resource quality pro-
vided by C
4
species, such as low nitrogen levels and
high levels of recalcitrant structural carbohydrates
(Campbell et al. 1996, Wardle et al. 1998
b
). Further,
the higher levels of
Heteronychus arator
under some
of the treatments allowing dense grass cover is in agree-
ment with the known preferences of this species for
grass roots (Watson and Wrenn 1980, Watson andMars-
den 1981). The ordination results also demonstrate de-
tectable linkages between the community structures of
plants and herbivorous arthropods, although these are
complicated by a time lag due to the generation times
of the arthropod species present (Fig. 14).
A related issue is how plant diversity may affect the
diversity of other groups of organisms. We would ex-
pect that, with the enhanced habitat heterogeneity pres-
ent in a more diverse plant community, a wider range
of niches would be provided, facilitating a greater di-
versity of consumer organisms. This has often been
demonstrated for aboveground consumers (MacArthur
1965, Pimm 1991, Huston 1994), but only occasionally
for belowground herbivores (House 1989) and decom-
poser organisms (Anderson 1978, Barker and Mayhill
1999, Sulkava and Huhta 1998). Contrary to our hy-
potheses, we not only failed to find such a relationship,
but also actually detected a negative association be-
tween plant diversity (Shannon-Weiner index) and that
of some of the other groups that we considered. This
was especially apparent for the herbivorous arthropods,
probably because reducing plant diversity through re-
moving the C
4
grasses also improved the overall re-
source quality, enabling a greater frequency of some
of the arthropod fauna to occur. Inother words, a highly
diverse plant community consisting of a proportion of
species of low palatability may potentially support a
less diverse herbivorous arthropod fauna than would a
less diverse community consisting mainly of palatable
species. A similar (although weaker) pattern is apparent
with regard to the microflora (PLFA data) andthe pred-
atory nematodes (at least as revealed by the lag data
in Fig 14); the reasons are less clear, but this result
also appears to be reflective of the effects of resource
quality manifesting itself through several trophic lev-
els. The only negative treatment effect on the diversity
of any of the five consumer groups that we assessed
was the effect of C
3
grass exclusion on microbe-feeding
nematode diversity, but this appears to be a specific
response to
L. perenne
removal rather than to a reduc-
tion of grassland diversity. Therefore, there is little
evidence from our study to support the view that re-
ducing diversity in one trophic level is necessarily
matched by a corresponding loss of diversity in other
trophic levels. Rather, the response of consumer di-
versity to plant community attributes is more likely to
reflect the traits or characteristics of the plant species
present.
Ecosystem properties
Several recent experimental studies have attempted
to manipulate organism diversity and have interpreted
results in terms of the effects of loss of species from
ecosystems on ecosystem function (Naeem et al. 1994,
Tilman et al. 1996), ecosystem stability (Tilman 1996,
McGrady-Steed et al. 1997), and variability (Naeem
and Li 1997). Although these studies have concluded
that loss of species can have predictable adverse con-
sequences for ecosystem properties, the interpretations
of several of these findings remain controversial (see
Aarssen 1997, Garnier et al. 1997, Grime 1997, Huston
1997, Wardle 1998
a
). Although our study did not di-
rectly test for the effects of varying diversity, it does
directly address the issue of whether permanent exclu-
sion of species has important effects on ecosystem
properties and processes at the spatial scale that we are
considering. There is no evidence from our study to
support our hypothesis that permanent loss of subsets
of the flora has consistent unidirectional or negative
consequences for ecosystem properties, either above-
ground (e.g., NPP, standing biomass, plant cover) or
belowground (e.g., decomposition rates, soil CO
2
re-
lease, nutrient dynamics, biomasses of those organisms
that carry out decomposition-related processes). Fur-
ther, there are no clear, unidirectional effects of func-
tional group removal on either the stability (temporal
variability) or spatial heterogeneity (‘‘ecosystem reli-
ability’’; Naeem and Li 1997) of the properties that we
considered. Part of the reason we did not detect such
effects may be because our system seems to be largely
buffered against the effects of species removal; exclu-
sion of a subset of the flora may be compensated for
by increased production and biomass of other com-
ponents (see Hooper 1998).
It is also apparent that some ecosystem properties
responded more strongly to treatments than did others.
Aboveground responses were generally greater than
those below ground; exclusion of some components of
the flora often enhanced aboveground biomass and pro-
duction of the remaining components, especially when
treatments involved removal of
L. perenne.
Levels of
soil organisms were adversely affected by removal of
564
DAVID A. WARDLE ET AL.
Ecological Monographs
Vol. 69, No. 4
all plants, but as long as plants were present, vegetation
composition did not greatly alter components of the
decomposer subsystem, at least at the functional group
level of resolution. Because decomposer-related pro-
cesses are known to be regulated by the magnitude of
the active soil microbial biomass (Beare et al. 1991),
the biomass and populations of soil animals that cat-
alyze its turnover (Visser 1985), and the structure of
the decomposer food web (De Angelis 1992, Seta¨la¨
1995, Bengtsson et al. 1996), it is perhaps not sur-
prising that ecosystem properties determined by the soil
biota were less consistently correlated with treatments
than were many of the aboveground response variables.
Soil chemical properties such as C and N concentra-
tions were especially insensitive to treatment effects,
presumably because they reflect much longer term
changes than we could consider during the course of
this study (see Tate 1992), and possibly because of the
buffering effect of the relatively high soil organic mat-
ter levels characteristic of our study site (see De An-
gelis 1992, Wardle 1998
b
). Given that the microbial
biomass and the fauna that feed upon it are often closely
linked to soil C and N levels (Jenkinson and Ladd
1981), the soil biota also would have been buffered to
some extent against shifts in vegetation composition.
Our study demonstrates that the various responses
of ecosystem- and community-level properties to per-
manent exclusion of functional groups were ultimately
driven by traits of the component plant species. This
concurs with recent findings pointing to the role of
vegetation composition and the significance of domi-
nant plant species in driving how ecosystems function
(Hooper and Vitousek 1997, 1998, Tilman et al. 1997,
Wardle et al. 1997, Grime 1998). Ultimately, the ex-
clusion of a given plant species, or a group of plant
species, has the potential to affect a wide range of
community- and ecosystem-level attributes, both
above- and belowground. The nature of these effects
is likely to be governed mainly by the specific attributes
or traits of those species that are lost.
A
CKNOWLEDGMENTS
For technical support for the various components of this
study, we owe many thanks to N. Bell, M. Dexter, A. Firth,
J. Gow, T. James, F. Neville, B. Ryburn, and M. Vojvodic-
Vukovic. Many thanks also to B. Campbell and A. Rahman
for support and helpful discussions, and to P. Hunt and T.
Pearson for preparing the illustrations. P. Bellingham, D. Coo-
mes, J. Mikola, and H. Seta¨la¨ made numerous helpful com-
ments on an early draft, and M. Huston and two anonymous
referees provided very thorough reviews of the submitted
version that greatly enhanced the clarity and focus of the
manuscript. This work was supported by a Non-Specific Out-
put Funding vote from AgResearch, and by The N.Z. Foun-
dation for Science, Research and Technology.
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