Directory UMM :Data Elmu:jurnal:A:Applied Soil Ecology:Vol13.Issue1.Sep1999:
Applied Soil Ecology 13 (1999) 45±55
Effects of altered soil-water availability on a
tallgrass prairie nematode community
T.C. Todd*, J.M. Blair, G.A. Milliken
Department of Plant Pathology, Division of Biology and Department of Statistics, Kansas State University, Manhattan, KS, USA
Received 28 September 1998; received in revised form 17 March 1999; accepted 17 March 1999
Abstract
Climate change predictions for the Great Plains region of North America include reduced growing season precipitation. The
consequence of this prediction for soil fauna and belowground processes was investigated at two spatial scales by integrating
experimental manipulation of soil moisture levels with natural variation in soil-water availability. Experiments consisted of (1)
reciprocal core transplants across a regional precipitation gradient and (2) supplemental irrigation applied across a local
topographic gradient. This report examines functional-level responses by the tallgrass prairie nematode community to
differences in soil moisture levels over a four-year period. Effects on nematode community structure were complex and
dependent upon nematode trophic habit and depth in the soil pro®le. The strongest and most consistent responses to changes in
soil-water availability were displayed by herbivorous taxa, with 71% higher densities observed under wetter soil conditions
across experiments and years. Responses of microbial-feeding nematodes were more variable, with lower densities observed,
in some cases, in the presence of experimentally-increased soil moisture levels. Effects of regional differences in soil-water
availability on the nematode community were uniformly restricted to depths >20 cm. Community responses to short-term
changes in soil moisture were not consistent with patterns in community structure developed under different natural moisture
regimes, suggesting divergent short-term and long-term responses of belowground biota and processes to changes in soil-water
availability. # 1999 Elsevier Science B.V. All rights reserved.
Keywords: Climate change; Community structure; Nematode; Soil moisture; Tallgrass prairie
1. Introduction
The Great Plains region of North America is dominated by grassland ecosystems whose distributions are
determined primarily by an east±west precipitation
gradient (Weaver, 1954; Risser et al., 1981). Grassland
*Corresponding author. Tel.: +785-532-1350; fax: +785-5325692; e-mail: nema@plantpath.ksu.edu
types range from the xeric shortgrass prairie at the
western edge of the region to the mesic tallgrass
prairie at the eastern edge. Primary productivity across
this gradient is also related strongly to precipitation
(Sala et al., 1988). Within grassland types and particularly for frequently-burned tallgrass prairie, often
soil moisture is the best predictor of aboveground net
primary productivity because it re¯ects longer-term
patterns of precipitation and water use (Knapp et al.,
1998).
0929-1393/99/$ ± see front matter # 1999 Elsevier Science B.V. All rights reserved.
PII: S 0 9 2 9 - 1 3 9 3 ( 9 9 ) 0 0 0 2 2 - 0
46
T.C. Todd et al. / Applied Soil Ecology 13 (1999) 45±55
Recent models of global climate change include
predictions of decreased growing season precipitation
for the Great Plains region (Karl et al., 1991). The
generic effects of reduced precipitation on aboveground productivity in North American grasslands
can be surmised based on spatial (east±west gradient)
and temporal (drought cycles) patterns in these two
variables but much less is known about the relationships between soil moisture and belowground processes for these same ecosystems. Pulses of root
growth, decomposition, and biotic activity have been
observed following precipitation events (Hayes and
Seastedt, 1987; Elliot et al., 1988) but long-term
belowground responses to altered precipitation patterns have not been investigated. Given that a large
proportion of primary production in temperate grasslands occurs belowground (Coleman et al., 1976;
Risser et al., 1981) and that processes such as nutrient
cycling are strongly regulated by soil fauna (Hunt et
al., 1987; Elliot et al., 1988; Seastedt et al., 1988), a
better understanding of the interaction of soil moisture
regimes, ecosystem processes, and belowground food
webs is essential to any evaluation of the long-term
consequences of climate change for Great Plains
grasslands.
Nematodes represent a major component of soil
food webs in grassland ecosystems, interacting with
other soil biota through multiple trophic pathways
(Elliot et al., 1988; Ransom et al., 1998). Their
in¯uence on ecosystem processes in grasslands has
been well documented and includes effects on primary
production through herbivory (Smolik, 1977; Stanton
et al., 1981; Ingham and Detling, 1990) and on
nutrient cycling through grazing of microbial decomposers (Ingham et al., 1985, 1986a, b; Hunt et al.,
1987). The trophic structure of the nematode community has been shown to be a reliable index of soil food
web structure, particularly in relation to decomposition pathways (Neher and Campbell, 1994; Todd,
1996). Based on these characteristics, an understanding of nematode community responses (as well as
those of other soil fauna) to altered precipitation
patterns appears to be a prerequisite for predicting
ecosystem-level responses to climate change.
The objective of the present study was to assess
nematode community responses, including changes in
trophic structure, temporal dynamics, and vertical
distribution, to experimentally-altered soil-water
availability at two spatial scales: (1) a regional scale,
using reciprocal core transplants across a naturallyoccurring precipitation gradient; and (2) a local scale,
using supplemental irrigation across a topographic
gradient encompassing natural differences in soilwater availability. Both experiments were designed
to assess the long-term effects of differences in soilwater availability on soil fauna (using existing natural
gradients), as well as determine the short-term
responses of the faunal community to experimental
manipulation of soil moisture. Responses of soil
microarthropods have been published separately
(O'Lear and Blair, 1999).
2. Materials and methods
2.1. Reciprocal core transplant experiment
The study was conducted at two sites across an
east±west precipitation gradient. The more mesic site
was located at the Konza Prairie Research Natural
Area (KPRNA), a 3487 ha tallgrass prairie located
12 km south of Manhattan, Kansas (398050 N, 968350
W). The more arid mixed-grass prairie site was located
at the Fort Hays Agricultural Experiment Station
(FHAES) located 240 km west of KPRNA (388750
N, 998200 W). Long-term mean annual precipitation is
835 mm at KPRNA and 580 mm at FHAES. Soils at
both sites were texturally-similar silt loams overlaying
silty clay loams, although the clay content below
30 cm was notably higher at the KPRNA site. The
KPRNA soil was a Reading silt loam (®ne, mixed,
mesic Typic Argiudoll) and the FHAES soil was a
Harney silt loam (®ne, montmorillonitic, mesic Typic
Argiustoll). The dominant vegetation at the KPRNA
site consisted of the warm-season grasses Andropogon
gerardii Vitman (big bluestem), Panicum virgatum L.
(switchgrass), and Sorghastrum nutans (L.) Nash
(indian grass). The dominant vegetation at the FHAES
site included the cool-season midgrass Pascopyrum
smithii (Rydb.) Love (western wheatgrass), the warmseason shortgrasses Bouteloua curtipendula (Michx.)
Torr. (side-oats grama), B. gracilis (H.B.K.) Lag. Ex
Grif®ths (blue grama), and Buchloe dactyloides
(Nutt.) Engelm. (buffalograss), and the tallgrass A.
gerardii. Both sites were burned in April of each year
of the study.
T.C. Todd et al. / Applied Soil Ecology 13 (1999) 45±55
Seventy intact soil cores (25 cm diameter 70 cm
deep) encased in open-ended PVC cylinders were
extracted from each site during the autumn of
1993 using a hydraulic soil coring machine (Swallow
et al., 1987). Cores were collected from areas
within each site that were dominated by A. gerardii.
Half of the cores were replaced in their original
holes and the remaining half were transplanted
into holes at the reciprocal site. The experimental
design at each location consisted of 35 sets of paired
cores (one from each site) arranged in a randomized
complete block design. Five pairs of cores were
collected from each site for destructive sampling
in May and October/November of each year (1994±
1996) and sectioned into 0±10, 10±20, 20±40, and
40±60 cm depth increments. The remaining ®ve pairs
of cores were reserved for future sampling to assess
longer-term trends.
Nematodes were extracted from 100 cm3 subsamples of mixed soil from each depth section following
uniform mixing using a modi®ed Christie±Perry technique (Christie and Perry, 1951). Counts were adjusted
based on an average extraction ef®ciency of 30% for
the dominant taxa present (Seastedt et al., 1987).
Nematodes were identi®ed to family or genus level
and assigned to the following trophic groups based on
Yeates et al. (1993) and Todd (1996): (1) herbivore
(root-feeding; Helicotylenchus and Paratylenchinae
comprised 68% of this group across dates and locations); (2) fungivore (hyphal-feeding; 67% Tylenchidae); (3) microbivore (bacterial- and unicellular
eucaryote-feeding; 52% Cephalobidae); (4) omnivore/predator (primarily invertebrate feeding; 89%
of this group consisted of large species in the Dorylaimida). A complete list of the dominant nematode
taxa of the KPRNA tallgrass prairie site and their
trophic groupings can be found in Ransom et al.
(1998).
The data were analyzed as a strip±strip plot design
with core origin, depth, and sampling date as strip
factors nested within location. The analysis used a
strip-plot model (Milliken and Johnson, 1992) and the
GLM and Mixed procedures in SAS (Statistical Analysis Systems Institute Inc., 1989; Littell et al., 1996).
Nematode densities were log10-transformed to reduce
heterogeneity of variances for analysis of variance and
mean comparisons. Untransformed means are presented in tables and ®gures.
47
2.2. Irrigation transect experiment
The study was conducted on an annually burned
KPRNA site with the same general characteristics as
described for the reciprocal core transplant study. The
experiment utilized two existing replicate irrigation
pipelines (140 m in length), which traversed a topographic gradient of soil-water availability ranging
from drier uplands to wetter lowlands (Knapp et al.,
1994). The upland soil in this gradient was a Clime±
Sogn complex (®ne, mixed mesic Udic Haplustoll)
and the lowland soil was an Irwin silty clay loam (®ne
mixed mesic Pachic Argiustoll). Both soils were
texturally similar (21±22% sand, 41±44% silt, 34±
38% clay) and both sites contained vegetation characteristic of the tallgrass prairie, as described above.
Supplemental irrigation was applied during May
through September of each year to offset growing
season moisture de®cits. Timing and amounts of
irrigation supplements were based on measured rainfall amounts and estimated evapotransporation
(Knapp et al., 1994). Growing season precipitation
and supplemental irrigation amounts, respectively,
were 735 and 357 mm for 1995, 561 and 234 mm
for 1996, and 400 and 313 mm for 1997.
Sixteen 3 m diameter plots were established for
sampling, with two replicate irrigated and two replicate nonirrigated control plots located on each of two
topographic sites (upland and lowland) per pipeline.
This resulted in four plots for each site-treatment
combination. Irrigated plots within a topographic site
were located on opposite sides of each of the two
irrigation pipelines (2±3 m from the pipeline); control
plots were similarly located along each of two parallel,
non-irrigated control transects (O'Lear and Blair,
1999).
Composite samples consisting of two 5 cm diameter 20 cm deep soil cores were collected from each
plot on two (1995) or three (1996±1997) dates during
the growing season. Gravimetric soil water content
was determined by oven-drying (608C) 50 cm3 subsamples of soil. Nematodes were extracted from
100 cm3 subsamples of soil and enumerated as
described for the previous study. The data were
log10-transformed and analyzed as a strip±strip plot
design, with irrigation treatment, site (topographic
position), and sampling date as strip factors, using
the SAS procedures described above.
48
T.C. Todd et al. / Applied Soil Ecology 13 (1999) 45±55
3. Results
3.1. Reciprocal core transplant experiment
Mean annual precipitation at FHAES was 42% less
than that at KPRNA (616 vs. 1053 mm) during the
present study. For all years of the study, differences in
annual precipitation between locations (32±56%)
were consistently larger than the long-term average
difference of 30%. Seasonal patterns of precipitation
for both locations have been reported in O'Lear and
Blair (1999).
Table 1 summarizes the variation in nematode densities associated with location (site where the cores
Table 1
Analyses of variance and main effect means for nematode trophic group densities from the reciprocal core transplant experiment, 1994±1996
Source of variation
Year
Month
Month year
Error (month year)
Location
Error (loc)
Origin
Origin loc
Error (origin loc)
Depth
Depth loc
Error (depth loc)
Depth origin
Depth origin loc
Error (depth origin loc)
df
2
1
2
40
1
8
1
1
8
3
3
24
3
3
24
Mean squares
herbivores
fungivores
5.14
1.08
3.70
1.82
12.19*
1.78
145.38**
0.15
2.39
130.98**
1.49
1.21
139.38**
5.34**
0.99
3.73
0.77
5.60*
1.47
3.60
1.70
13.48*
8.07*
1.54
16.53**
0.49
1.07
7.61**
4.80**
1.24
microbivores
0.12
35.04**
21.78**
1.98
0.82
3.12
71.50**
53.71**
2.51
223.60**
3.29
5.30
33.25**
9.47
3.43
omnivore/predators
7.80
73.61**
16.34*
4.90
0.12
3.43
4.73
17.70
13.90
171.01**
13.65*
3.52
5.56
6.54
5.19
Main effect means (thousands per square meter)
Year (n 160)
1994
1995
1996
670
786
766
596
748
629
287
277
301
89
104
70
Month (n 240)
May
October
602
879
470
845
260
316
80
96
Location (n 240)
FHAES
KPRNA
589
893
611
705
296
280
81
95
Origin (n 240)
FHAES
KPRNA
953
529
662
654
325
251
82
94
Depth (n 120)
0±10 cm
10±20 cm
20±40 cm
40±60 cm
558
723
1041
641
943
536
703
450
604
228
214
106
138
75
77
61
*
p 0.05.
p 0.01.
**
T.C. Todd et al. / Applied Soil Ecology 13 (1999) 45±55
49
Fig. 1. Densities of herbivorous nematodes in cores originating
from (a) FHAES and (b) KPRNA at four depths and two locations
averaged across month and year. An asterisk indicates a significant
difference between locations within depth according to leastsquares means of log10-transformed data (p 0.05). Data are
means of 30 observations.
Fig. 2. Densities of microbivorous nematodes in cores originating
from (a) FHAES and (b) KPRNA at four depths and two locations
averaged across month and year. An asterisk indicates a significant
difference between locations within depth according to leastsquares means of log10-transformed data (p 0.05). Data are
means of 30 observations.
resided during the experiment) and origin (site where
the cores originated), as well as sampling date and
depth. Although core origin consistently accounted for
a larger portion of the variation in nematode densities
than did location, the implied importance of historic
soil moisture conditions is misleading. Major differences due to core origin were restricted exclusively to
the lowest soil depth (see Fig. 1), resulting in large
depth origin interaction terms (Table 1). This effect
appeared to be adequately explained by textural differences between the two soils at that depth (see
Section 2). Abrupt decreases in nematode densities
in KPRNA cores below the 40 cm depth (Figs. 1 and
2), were coincident with a notable increase in clay
content. No such delineation in both soil texture and
nematode densities was observed for FHAES cores.
This pattern was present at initiation of the experiment
and remained constant throughout the sampling period. When the 40±60 cm depth was excluded from the
analyses of variance, no effects due to core origin were
observed. Thus, no long-term effects of soil moisture
differences were discernable in the nematode data.
In contrast to the absence of an identi®able effect of
historic soil moisture, differences in soil moisture
conditions between locations during the present study
did in¯uence nematode densities. Herbivorous nematode densities were 52% higher (p 0.03) at KPRNA
than at FHAES across cores, depths, and years. Herbivore, fungivore, and microbivore densities all exhibited three-way interactions (p 0.06) among origin,
location, and depth of soil cores, with differences
between locations consistently restricted to the lower
50
T.C. Todd et al. / Applied Soil Ecology 13 (1999) 45±55
soil pro®les (Figs. 1 and 2). Herbivorous nematode
densities at the lower soil depths tended to be higher in
cores residing at KPRNA compared to those at
FHAES, regardless of core origin (Fig. 1). In contrast,
the effect of location on microbivorous nematodes,
while still restricted to the lower soil depths, depended
upon core origin. Microbivore densities in FHAES
cores were lower (p 0.05) when residing at KPRNA
vs. FHAES, while those in KPRNA cores were higher
(p 0.05) at KPRNA vs. FHAES (Fig. 2). Fungivore
densities displayed patterns similar to those observed
for microbivores (data not shown). Location year
interactions (p 0.05; not included in Table 1) also
occurred for several trophic groups. Fungivore and
omnivore/predator densities were higher at KPRNA in
1995, the year with the greatest difference in precipitation between locations (O'Lear and Blair, 1999),
but tended to be lower in other years. Lower microbivore densities were observed at KPRNA compared
to FHAES in 1996.
As detailed above, a high clay content in the 40±
60 cm depth of the KPRNA cores restricted densities
of all trophic groups, resulting in large origin depth
interaction effects (Table 1). Above this depth, nematode densities were generally distributed similarly in
the two soil pro®les, although vertical distribution of
individual trophic groups varied considerably. Microbivores were the most strati®ed group, with >50% of
the total population occurring at the 0±10 cm depth
(Table 1, Fig. 2). Fungivore and omnivore/predator
groups were also concentrated in the upper 10 cm
of the soil pro®le but to a lesser extent than microbivores (Table 1). Herbivores were more evenly distributed in the soil pro®le (above 40 cm) in cores
originating from KPRNA, or tended to be concentrated at lower soil depths in cores originating from
FHAES (Table 1, Fig. 1).
Variability in the depth distribution of nematodes
occurred across sampling dates, as indicated by large
depth month and depth year interactions
(p < 0.01; not included in Table 1) for several groups.
This variability did not, however, encompass large
changes in the general patterns of vertical distribution
already described. For example, microbivore densities
were more strongly strati®ed on autumn than on spring
sampling dates but densities remained highest at the
0±10 cm depth and lowest at the 40±60 cm depth in
both cases.
Fig. 3. Gravimetric soil moisture content of cores collected for
nematode extraction from control and irrigated plots averaged
across upland and lowland sites. An asterisk indicates a significant
difference between irrigation treatment within date according to
least-squares means of log10-transformed data (p 0.05). Data are
means of eight observations.
3.2. Irrigation transect experiment
The moisture content of soil cores collected for
nematode assay was 19% higher, on average, in
irrigated plots across sampling dates but moisture
differences varied with month and year (p < 0.001).
Soil moisture was signi®cantly higher (p 0.05) in
irrigated vs. control plots on ®ve of eight dates
(Fig. 3). Moisture content did not vary between sites
(upland vs. lowland). Volumetric soil water content,
determined by a time domain re¯ectometry (TDR) soil
moisture monitoring system (Campbell Scienti®c),
and daily precipitation amounts for these plots have
been reported by O'Lear and Blair (1999) for 1995,
the year with the greatest observed differences in soil
moisture between irrigation treatments.
Herbivores were the only trophic group to display a
moderately consistent response to irrigation across
sampling dates, with a 90% increase (p 0.07) in
average densities in irrigated vs. control plots. Irrigation date interactions (p 0.08) were observed for
herbivore, fungivore, and microbivore densities
(Table 2). Herbivore densities were higher
(p 0.05) in irrigated plots on four of eight dates,
with signi®cant responses observed in every year of
the study (Fig. 4(a)). Microbivorous nematodes, in
contrast, exhibited higher (p 0.05) densities with
irrigation only on the July 1995 sampling date when
soil moisture differences between treatments were
greatest (Fig. 4(b)). Densities of this trophic group
51
T.C. Todd et al. / Applied Soil Ecology 13 (1999) 45±55
Table 2
Analyses of variance and main effect means for nematode trophic group densities from the irrigation transect experiment, 1995±1997
Source of variation
df
Mean squares
herbivores
Year
Month (year)
Error (month year)
Site
Error (Site)
Irrigation
Error (irr)
Irr site
Error (irr site)
Site year
Site month (year)
Error (site month year)
Irr year
Irr month (year)
Error (irr month year)
Irr site year
Irr site month (year)
Residual error
2
5
7
1
1
1
1
1
1
2
5
7
2
5
7
2
5
7
**
0.797
0.831**
0.058
0.004
0.025
4.849
0.067
0.106
0.014
0.156
0.073
0.218
0.586**
0.344*
0.052
0.008
0.023
0.082
fungivores
*
0.276
1.288**
0.059
0.055
0.056
0.270
0.018
0.139
0.002
0.154*
0.112*
0.023
0.104
0.230*
0.032
0.037
0.018
0.055
microbivores
**
0.721
0.921**
0.057
0.105
0.020
0.111
0.004
0.017
0.012
0.072
0.104
0.085
0.228
0.258
0.078
0.057
0.242
0.118
omnivore/predators
1.667**
0.258
0.087
0.085
0.147
0.034
0.463
0.299*
0.001
0.036
0.150
0.087
0.130
0.068
0.115
0.044
0.068
0.045
Main effect means (thousands per square meter)
Year (n 48)
1995
1996
1997
1541
1420
2214
2151
1888
2737
830
822
1231
240
207
438
Month (year) (n 16)
July 95
October 95
June 96
August 96
October 96
June 97
August 97
October 97
1341
1740
876
1087
2297
1435
2585
2622
1987
2315
959
1287
3417
1271
2427
4513
621
1040
496
665
1304
717
1142
1832
216
264
188
121
313
408
444
463
Site (n 64)
Upland
Lowland
1843
1653
2257
2287
903
1051
291
313
Irrigation (n 64)
Control
Irrigated
1206
2290
2256
2289
961
993
309
295
*
p 0.05.
p 0.01.
**
tended to be comparable or lower in irrigated vs.
control plots on most of the other sampling dates.
Similarly, fungivore densities were higher (p 0.05)
in irrigated plots on the July, 1995 and June, 1996
sampling dates but no consistent responses were
observed across the remaining dates (data not shown).
Irrigation resulted in 15% higher omnivore/predator
densities in upland soils but 14% lower densities in
52
T.C. Todd et al. / Applied Soil Ecology 13 (1999) 45±55
Fig. 4. Densities of (a) herbivores and (b) microbivores in control
and irrigated plots averaged across upland and lowland sites. An
asterisk indicates a significant difference between irrigation
treatment within date according to least-squares means of log10transformed data (p 0.05). Data are means of eight observations.
lowland soils (signi®cant irrigation site interaction,
p 0.04) across dates.
Topographic effects were rare and, when observed,
varied across sampling dates. Fungivorous nematodes
were the only trophic group displaying dissimilar
population densities between upland and lowland
sites, with differences dependent on both month and
year (Table 2). This group tended to be more abundant
in upland soils early in the growing season and more
abundant in lowland soils late in the growing season
(data not shown).
4. Discussion
The responses of individual nematode trophic
groups to experimentally-altered soil moisture levels
were surprisingly consistent across experiments, seasons, and years. The largest responses were observed
with herbivorous taxa, where increased soil moisture
due to core transplantation or irrigation resulted in
increases of 52% and 90%, respectively, in nematodes
densities across years. The magnitude of the response
in the mesic tallgrass prairie irrigation experiment was
unexpected given that growing-season precipitation
across years was within 10% of the long-term average.
This contrasts with observations from the more xeric
shortgrass prairie, where plant-feeding nematode
responses to supplemental irrigation and nitrogen
were highly variable and often neutral (Smolik and
Dodd, 1983). A positive relationship between soil
moisture and herbivorous nematode densities has been
observed on wheatgrasses in the Utah desert (Grif®n et
al., 1996). Of course, individual nematode species will
exhibit preferences for speci®c soil moisture conditions (Schmitt and Norton, 1972) and functional group
responses to changes in water availability are likely to
vary both within and among ecosystems, depending
on the dominant taxa present. Nevertheless, the shortterm responses of total herbivore densities to increased
(or decreased) soil moisture levels were consistent
across a range of environments in the present study.
The remaining trophic groups displayed few signi®cant responses to changes in soil moisture. Fungivore and microbivore densities were higher in the
presence of supplemental irrigation on the date with
the lowest soil moisture content (and the greatest
difference in soil moisture between treatments) but
other responses to increased soil moisture were as
likely to be negative as positive, particularly for the
microbivores. In this case, the response is consistent
with the inverse relationship between the C : N ratio of
microbial biomass and water availability in tallgrass
prairie, re¯ecting an increase in the activity of bacteria
relative to fungi under drier conditions (Rice et al.,
1998). Microbivore densities have been observed to
increase concomitantly with increases in microbial N
and bacterial biomass in tallgrass prairie soils (Todd,
1996). Reduced microbivore densities under wetter
soil moisture regimes would, therefore, be consistent
with expected changes in microbial communities.
In the present study, microbivore populations which
developed under different soil moisture conditions
displayed differential responses to altered soil-water
availability, re¯ecting the importance of historic soil
moisture conditions. Whether this results from siterelated differences in nematode species composition
or from belowground food webs or processes that have
diverged under long-term differences in soil-water
availability remains to be determined. Regardless of
the mechanism, trends in nematode responses to soilwater availability do appear to differ among ecosystems. Our observations contrast with those from the
T.C. Todd et al. / Applied Soil Ecology 13 (1999) 45±55
shortgrass prairie, for example, where fungivorous
(Tylenchidae), microbivorous, and predaceous nematodes were all more responsive to supplemental water
and N than herbivorous nematodes (Smolik and Dodd,
1983). In a recent study of a perennial agricultural
system, only omnivorous genera of the Dorylaimida
responded (positively) to irrigation intensity (Porazinska et al., 1998). Such con¯icting results emphasize
that nematode responses to changes in climatic variables, such as water availability, should not be generalized across ecosystem types. Functional group
responses to changes in soil-water availability will
re¯ect the preferences of the major constituent taxa
present, as previously noted, but will also be determined by resultant changes in belowground processes
as mediated by historic conditions.
Seasonal patterns of herbivorous nematode densities in tallgrass prairie are typically related to root
phenology and biomass, especially during periods of
drought (Rice et al., 1998). Large decreases in root
production have been documented during drought
years at KPRNA (Hayes and Seastedt, 1987) but, in
the present study, root responses to altered soil moisture levels did not follow this simple trend. While cores
originating from FHAES had lower belowground
plant biomass than those originating from KPRNA
as expected, there was a trend for reduced belowground biomass at the more mesic KPRNA site compared to the more xeric FHAES site following core
transplantation (Blair et al., in preparation). Additionally, estimates of root biomass were not signi®cantly
affected by irrigation at KPRNA, although root biomass was greater in lowland vs. upland plots (Todd,
unpublished data). Together, these observations suggest that herbivorous nematode responses to changes
in soil moisture result from abiotic effects and are
independent of root responses. This hypothesis is
improbable, however, based on the comparative lack
of, or inverse, responses of the remaining trophic
groups to increased soil moisture levels and given
compelling arguments to the contrary (Grif®n, 1984;
Todd, 1996; Rice et al., 1998). It is more likely that the
dynamic nature of root production and the rapid turnover of roots in prairie soil confounded the relationship between precipitation patterns and root dynamics
in the present study. Pulses in new root production, as
measured by root windows, are ephemeral, with much
higher rates of turnover than can be measured for root
53
biomass (Hayes and Seastedt, 1987). Alternatively, the
herbivore response may re¯ect the increased N availability that accompanied wetter conditions in the
reciprocal core experiment (Blair et al., in preparation). The tallgrass prairie is characterized by N
limitation and herbivorous nematode densities in this
ecosystem respond positively to the increased nutrient
status of roots following N fertilization (Todd, 1996).
The experiments in the present study were designed
to encompass both short- and long-term effects of soilwater availability. Transplanted cores in the reciprocal
core transplant experiment permitted investigation of
the relationship between changes in soil-water availability and short-term responses by the nematode
community, while comparison of soil cores from their
respective sites of origin provided insights about
nematode communities derived under different annual
precipitation regimes. Similarly for the irrigation
transect experiment, short- and long-term nematode
responses to changes in soil-water availability could
be deduced, respectively, through comparison of irrigation treatments and topographical sites (soil moisture and net primary production are typically greater in
lowlands than in uplands; Knapp et al., 1993; O'Lear
and Blair, 1999). In both instances, short-term
responses were inconsistent with long-term differences. For example, short-term increases in herbivorous nematode densities in response to increased soil
moisture levels were documented in both experiments
but herbivore densities did not differ between soil
cores at their site of origin (with the exception of
the 40±60 cm depth, where differences were related to
soil texture, not location), nor did they differ between
upland and lowland sites, despite greater root biomass
for the lowlands (Todd, unpublished data). Thus, it
appears that the observed nematode responses may not
be indicative of more complex long-term responses to
changes in water availability. Resolution of this issue
awaits the longer-term measurements planned for the
present study.
Patterns of vertical distribution for nematodes in
KPRNA and FHAES soils were generally similar to
those reported for tallgrass and mixed-grass prairies,
with all trophic groups concentrated in the upper
20 cm of soil depth (Risser et al., 1981; Smolik and
Lewis, 1982). A notable exception was observed with
herbivore densities in FHAES-originated cores, where
nearly 70% of the population occurred below 20 cm. It
54
T.C. Todd et al. / Applied Soil Ecology 13 (1999) 45±55
is important to further note that all of the signi®cant
differences in nematode densities between locations
occurred at depths below 20 cm, regardless of soil
origin. These observations emphasize that grassland
nematode communities and their responses to climate
change may not always be accurately represented with
the standard 20 cm sampling depth.
5. Conclusions
Our data indicate that altered soil-water availability
related to potential changes in climate in the Great
Plains region will result in complex changes in the
structure of soil food webs in the grasslands of the
region. Tallgrass prairie nematode community
responses to experimentally-altered soil moisture
were dependent upon trophic habit, with plant-feeding
taxa responding rapidly and favorably to increased
moisture levels, while microbial-feeding taxa were as
likely to be negatively as positively impacted. These
variable responses appear to be the opposite of
expected responses from nematode communities in
the more xeric grasslands of the region (Smolik and
Dodd, 1983). Further complicating any predictions of
grassland ecosystem responses to climate change,
O'Lear and Blair (1999) reported that soil microarthropod communities in tallgrass prairie were negatively impacted by increased soil water content,
suggesting that responses among soil invertebrate
groups in this ecosystem are likely to be highly
variable. Finally, the data imply that short-term
responses by soil biotic communities may not suf®ciently predict the long-term consequences of climate
change, emphasizing the necessity of assessing such
responses over relatively long time scales.
Acknowledgements
The authors thank T. Oakley and the staff at Konza
Prairie Research Natural Area and the KSU Agricultural Research Center at Hays for ®eld and laboratory
assistance and plot maintenance. Research was funded
by the US Department of Energy's National Institute
for Global Environmental Change (DOE/NIGEC)
through the NIGEC Great Plains Regional Center at
the University of Nebraska, Lincoln. Financial support
does not constitute DOE endorsement of the views
expressed in this article. Contribution no. 99-119-J
from the Kansas Agricultural Experiment Station,
Manhattan.
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Effects of altered soil-water availability on a
tallgrass prairie nematode community
T.C. Todd*, J.M. Blair, G.A. Milliken
Department of Plant Pathology, Division of Biology and Department of Statistics, Kansas State University, Manhattan, KS, USA
Received 28 September 1998; received in revised form 17 March 1999; accepted 17 March 1999
Abstract
Climate change predictions for the Great Plains region of North America include reduced growing season precipitation. The
consequence of this prediction for soil fauna and belowground processes was investigated at two spatial scales by integrating
experimental manipulation of soil moisture levels with natural variation in soil-water availability. Experiments consisted of (1)
reciprocal core transplants across a regional precipitation gradient and (2) supplemental irrigation applied across a local
topographic gradient. This report examines functional-level responses by the tallgrass prairie nematode community to
differences in soil moisture levels over a four-year period. Effects on nematode community structure were complex and
dependent upon nematode trophic habit and depth in the soil pro®le. The strongest and most consistent responses to changes in
soil-water availability were displayed by herbivorous taxa, with 71% higher densities observed under wetter soil conditions
across experiments and years. Responses of microbial-feeding nematodes were more variable, with lower densities observed,
in some cases, in the presence of experimentally-increased soil moisture levels. Effects of regional differences in soil-water
availability on the nematode community were uniformly restricted to depths >20 cm. Community responses to short-term
changes in soil moisture were not consistent with patterns in community structure developed under different natural moisture
regimes, suggesting divergent short-term and long-term responses of belowground biota and processes to changes in soil-water
availability. # 1999 Elsevier Science B.V. All rights reserved.
Keywords: Climate change; Community structure; Nematode; Soil moisture; Tallgrass prairie
1. Introduction
The Great Plains region of North America is dominated by grassland ecosystems whose distributions are
determined primarily by an east±west precipitation
gradient (Weaver, 1954; Risser et al., 1981). Grassland
*Corresponding author. Tel.: +785-532-1350; fax: +785-5325692; e-mail: nema@plantpath.ksu.edu
types range from the xeric shortgrass prairie at the
western edge of the region to the mesic tallgrass
prairie at the eastern edge. Primary productivity across
this gradient is also related strongly to precipitation
(Sala et al., 1988). Within grassland types and particularly for frequently-burned tallgrass prairie, often
soil moisture is the best predictor of aboveground net
primary productivity because it re¯ects longer-term
patterns of precipitation and water use (Knapp et al.,
1998).
0929-1393/99/$ ± see front matter # 1999 Elsevier Science B.V. All rights reserved.
PII: S 0 9 2 9 - 1 3 9 3 ( 9 9 ) 0 0 0 2 2 - 0
46
T.C. Todd et al. / Applied Soil Ecology 13 (1999) 45±55
Recent models of global climate change include
predictions of decreased growing season precipitation
for the Great Plains region (Karl et al., 1991). The
generic effects of reduced precipitation on aboveground productivity in North American grasslands
can be surmised based on spatial (east±west gradient)
and temporal (drought cycles) patterns in these two
variables but much less is known about the relationships between soil moisture and belowground processes for these same ecosystems. Pulses of root
growth, decomposition, and biotic activity have been
observed following precipitation events (Hayes and
Seastedt, 1987; Elliot et al., 1988) but long-term
belowground responses to altered precipitation patterns have not been investigated. Given that a large
proportion of primary production in temperate grasslands occurs belowground (Coleman et al., 1976;
Risser et al., 1981) and that processes such as nutrient
cycling are strongly regulated by soil fauna (Hunt et
al., 1987; Elliot et al., 1988; Seastedt et al., 1988), a
better understanding of the interaction of soil moisture
regimes, ecosystem processes, and belowground food
webs is essential to any evaluation of the long-term
consequences of climate change for Great Plains
grasslands.
Nematodes represent a major component of soil
food webs in grassland ecosystems, interacting with
other soil biota through multiple trophic pathways
(Elliot et al., 1988; Ransom et al., 1998). Their
in¯uence on ecosystem processes in grasslands has
been well documented and includes effects on primary
production through herbivory (Smolik, 1977; Stanton
et al., 1981; Ingham and Detling, 1990) and on
nutrient cycling through grazing of microbial decomposers (Ingham et al., 1985, 1986a, b; Hunt et al.,
1987). The trophic structure of the nematode community has been shown to be a reliable index of soil food
web structure, particularly in relation to decomposition pathways (Neher and Campbell, 1994; Todd,
1996). Based on these characteristics, an understanding of nematode community responses (as well as
those of other soil fauna) to altered precipitation
patterns appears to be a prerequisite for predicting
ecosystem-level responses to climate change.
The objective of the present study was to assess
nematode community responses, including changes in
trophic structure, temporal dynamics, and vertical
distribution, to experimentally-altered soil-water
availability at two spatial scales: (1) a regional scale,
using reciprocal core transplants across a naturallyoccurring precipitation gradient; and (2) a local scale,
using supplemental irrigation across a topographic
gradient encompassing natural differences in soilwater availability. Both experiments were designed
to assess the long-term effects of differences in soilwater availability on soil fauna (using existing natural
gradients), as well as determine the short-term
responses of the faunal community to experimental
manipulation of soil moisture. Responses of soil
microarthropods have been published separately
(O'Lear and Blair, 1999).
2. Materials and methods
2.1. Reciprocal core transplant experiment
The study was conducted at two sites across an
east±west precipitation gradient. The more mesic site
was located at the Konza Prairie Research Natural
Area (KPRNA), a 3487 ha tallgrass prairie located
12 km south of Manhattan, Kansas (398050 N, 968350
W). The more arid mixed-grass prairie site was located
at the Fort Hays Agricultural Experiment Station
(FHAES) located 240 km west of KPRNA (388750
N, 998200 W). Long-term mean annual precipitation is
835 mm at KPRNA and 580 mm at FHAES. Soils at
both sites were texturally-similar silt loams overlaying
silty clay loams, although the clay content below
30 cm was notably higher at the KPRNA site. The
KPRNA soil was a Reading silt loam (®ne, mixed,
mesic Typic Argiudoll) and the FHAES soil was a
Harney silt loam (®ne, montmorillonitic, mesic Typic
Argiustoll). The dominant vegetation at the KPRNA
site consisted of the warm-season grasses Andropogon
gerardii Vitman (big bluestem), Panicum virgatum L.
(switchgrass), and Sorghastrum nutans (L.) Nash
(indian grass). The dominant vegetation at the FHAES
site included the cool-season midgrass Pascopyrum
smithii (Rydb.) Love (western wheatgrass), the warmseason shortgrasses Bouteloua curtipendula (Michx.)
Torr. (side-oats grama), B. gracilis (H.B.K.) Lag. Ex
Grif®ths (blue grama), and Buchloe dactyloides
(Nutt.) Engelm. (buffalograss), and the tallgrass A.
gerardii. Both sites were burned in April of each year
of the study.
T.C. Todd et al. / Applied Soil Ecology 13 (1999) 45±55
Seventy intact soil cores (25 cm diameter 70 cm
deep) encased in open-ended PVC cylinders were
extracted from each site during the autumn of
1993 using a hydraulic soil coring machine (Swallow
et al., 1987). Cores were collected from areas
within each site that were dominated by A. gerardii.
Half of the cores were replaced in their original
holes and the remaining half were transplanted
into holes at the reciprocal site. The experimental
design at each location consisted of 35 sets of paired
cores (one from each site) arranged in a randomized
complete block design. Five pairs of cores were
collected from each site for destructive sampling
in May and October/November of each year (1994±
1996) and sectioned into 0±10, 10±20, 20±40, and
40±60 cm depth increments. The remaining ®ve pairs
of cores were reserved for future sampling to assess
longer-term trends.
Nematodes were extracted from 100 cm3 subsamples of mixed soil from each depth section following
uniform mixing using a modi®ed Christie±Perry technique (Christie and Perry, 1951). Counts were adjusted
based on an average extraction ef®ciency of 30% for
the dominant taxa present (Seastedt et al., 1987).
Nematodes were identi®ed to family or genus level
and assigned to the following trophic groups based on
Yeates et al. (1993) and Todd (1996): (1) herbivore
(root-feeding; Helicotylenchus and Paratylenchinae
comprised 68% of this group across dates and locations); (2) fungivore (hyphal-feeding; 67% Tylenchidae); (3) microbivore (bacterial- and unicellular
eucaryote-feeding; 52% Cephalobidae); (4) omnivore/predator (primarily invertebrate feeding; 89%
of this group consisted of large species in the Dorylaimida). A complete list of the dominant nematode
taxa of the KPRNA tallgrass prairie site and their
trophic groupings can be found in Ransom et al.
(1998).
The data were analyzed as a strip±strip plot design
with core origin, depth, and sampling date as strip
factors nested within location. The analysis used a
strip-plot model (Milliken and Johnson, 1992) and the
GLM and Mixed procedures in SAS (Statistical Analysis Systems Institute Inc., 1989; Littell et al., 1996).
Nematode densities were log10-transformed to reduce
heterogeneity of variances for analysis of variance and
mean comparisons. Untransformed means are presented in tables and ®gures.
47
2.2. Irrigation transect experiment
The study was conducted on an annually burned
KPRNA site with the same general characteristics as
described for the reciprocal core transplant study. The
experiment utilized two existing replicate irrigation
pipelines (140 m in length), which traversed a topographic gradient of soil-water availability ranging
from drier uplands to wetter lowlands (Knapp et al.,
1994). The upland soil in this gradient was a Clime±
Sogn complex (®ne, mixed mesic Udic Haplustoll)
and the lowland soil was an Irwin silty clay loam (®ne
mixed mesic Pachic Argiustoll). Both soils were
texturally similar (21±22% sand, 41±44% silt, 34±
38% clay) and both sites contained vegetation characteristic of the tallgrass prairie, as described above.
Supplemental irrigation was applied during May
through September of each year to offset growing
season moisture de®cits. Timing and amounts of
irrigation supplements were based on measured rainfall amounts and estimated evapotransporation
(Knapp et al., 1994). Growing season precipitation
and supplemental irrigation amounts, respectively,
were 735 and 357 mm for 1995, 561 and 234 mm
for 1996, and 400 and 313 mm for 1997.
Sixteen 3 m diameter plots were established for
sampling, with two replicate irrigated and two replicate nonirrigated control plots located on each of two
topographic sites (upland and lowland) per pipeline.
This resulted in four plots for each site-treatment
combination. Irrigated plots within a topographic site
were located on opposite sides of each of the two
irrigation pipelines (2±3 m from the pipeline); control
plots were similarly located along each of two parallel,
non-irrigated control transects (O'Lear and Blair,
1999).
Composite samples consisting of two 5 cm diameter 20 cm deep soil cores were collected from each
plot on two (1995) or three (1996±1997) dates during
the growing season. Gravimetric soil water content
was determined by oven-drying (608C) 50 cm3 subsamples of soil. Nematodes were extracted from
100 cm3 subsamples of soil and enumerated as
described for the previous study. The data were
log10-transformed and analyzed as a strip±strip plot
design, with irrigation treatment, site (topographic
position), and sampling date as strip factors, using
the SAS procedures described above.
48
T.C. Todd et al. / Applied Soil Ecology 13 (1999) 45±55
3. Results
3.1. Reciprocal core transplant experiment
Mean annual precipitation at FHAES was 42% less
than that at KPRNA (616 vs. 1053 mm) during the
present study. For all years of the study, differences in
annual precipitation between locations (32±56%)
were consistently larger than the long-term average
difference of 30%. Seasonal patterns of precipitation
for both locations have been reported in O'Lear and
Blair (1999).
Table 1 summarizes the variation in nematode densities associated with location (site where the cores
Table 1
Analyses of variance and main effect means for nematode trophic group densities from the reciprocal core transplant experiment, 1994±1996
Source of variation
Year
Month
Month year
Error (month year)
Location
Error (loc)
Origin
Origin loc
Error (origin loc)
Depth
Depth loc
Error (depth loc)
Depth origin
Depth origin loc
Error (depth origin loc)
df
2
1
2
40
1
8
1
1
8
3
3
24
3
3
24
Mean squares
herbivores
fungivores
5.14
1.08
3.70
1.82
12.19*
1.78
145.38**
0.15
2.39
130.98**
1.49
1.21
139.38**
5.34**
0.99
3.73
0.77
5.60*
1.47
3.60
1.70
13.48*
8.07*
1.54
16.53**
0.49
1.07
7.61**
4.80**
1.24
microbivores
0.12
35.04**
21.78**
1.98
0.82
3.12
71.50**
53.71**
2.51
223.60**
3.29
5.30
33.25**
9.47
3.43
omnivore/predators
7.80
73.61**
16.34*
4.90
0.12
3.43
4.73
17.70
13.90
171.01**
13.65*
3.52
5.56
6.54
5.19
Main effect means (thousands per square meter)
Year (n 160)
1994
1995
1996
670
786
766
596
748
629
287
277
301
89
104
70
Month (n 240)
May
October
602
879
470
845
260
316
80
96
Location (n 240)
FHAES
KPRNA
589
893
611
705
296
280
81
95
Origin (n 240)
FHAES
KPRNA
953
529
662
654
325
251
82
94
Depth (n 120)
0±10 cm
10±20 cm
20±40 cm
40±60 cm
558
723
1041
641
943
536
703
450
604
228
214
106
138
75
77
61
*
p 0.05.
p 0.01.
**
T.C. Todd et al. / Applied Soil Ecology 13 (1999) 45±55
49
Fig. 1. Densities of herbivorous nematodes in cores originating
from (a) FHAES and (b) KPRNA at four depths and two locations
averaged across month and year. An asterisk indicates a significant
difference between locations within depth according to leastsquares means of log10-transformed data (p 0.05). Data are
means of 30 observations.
Fig. 2. Densities of microbivorous nematodes in cores originating
from (a) FHAES and (b) KPRNA at four depths and two locations
averaged across month and year. An asterisk indicates a significant
difference between locations within depth according to leastsquares means of log10-transformed data (p 0.05). Data are
means of 30 observations.
resided during the experiment) and origin (site where
the cores originated), as well as sampling date and
depth. Although core origin consistently accounted for
a larger portion of the variation in nematode densities
than did location, the implied importance of historic
soil moisture conditions is misleading. Major differences due to core origin were restricted exclusively to
the lowest soil depth (see Fig. 1), resulting in large
depth origin interaction terms (Table 1). This effect
appeared to be adequately explained by textural differences between the two soils at that depth (see
Section 2). Abrupt decreases in nematode densities
in KPRNA cores below the 40 cm depth (Figs. 1 and
2), were coincident with a notable increase in clay
content. No such delineation in both soil texture and
nematode densities was observed for FHAES cores.
This pattern was present at initiation of the experiment
and remained constant throughout the sampling period. When the 40±60 cm depth was excluded from the
analyses of variance, no effects due to core origin were
observed. Thus, no long-term effects of soil moisture
differences were discernable in the nematode data.
In contrast to the absence of an identi®able effect of
historic soil moisture, differences in soil moisture
conditions between locations during the present study
did in¯uence nematode densities. Herbivorous nematode densities were 52% higher (p 0.03) at KPRNA
than at FHAES across cores, depths, and years. Herbivore, fungivore, and microbivore densities all exhibited three-way interactions (p 0.06) among origin,
location, and depth of soil cores, with differences
between locations consistently restricted to the lower
50
T.C. Todd et al. / Applied Soil Ecology 13 (1999) 45±55
soil pro®les (Figs. 1 and 2). Herbivorous nematode
densities at the lower soil depths tended to be higher in
cores residing at KPRNA compared to those at
FHAES, regardless of core origin (Fig. 1). In contrast,
the effect of location on microbivorous nematodes,
while still restricted to the lower soil depths, depended
upon core origin. Microbivore densities in FHAES
cores were lower (p 0.05) when residing at KPRNA
vs. FHAES, while those in KPRNA cores were higher
(p 0.05) at KPRNA vs. FHAES (Fig. 2). Fungivore
densities displayed patterns similar to those observed
for microbivores (data not shown). Location year
interactions (p 0.05; not included in Table 1) also
occurred for several trophic groups. Fungivore and
omnivore/predator densities were higher at KPRNA in
1995, the year with the greatest difference in precipitation between locations (O'Lear and Blair, 1999),
but tended to be lower in other years. Lower microbivore densities were observed at KPRNA compared
to FHAES in 1996.
As detailed above, a high clay content in the 40±
60 cm depth of the KPRNA cores restricted densities
of all trophic groups, resulting in large origin depth
interaction effects (Table 1). Above this depth, nematode densities were generally distributed similarly in
the two soil pro®les, although vertical distribution of
individual trophic groups varied considerably. Microbivores were the most strati®ed group, with >50% of
the total population occurring at the 0±10 cm depth
(Table 1, Fig. 2). Fungivore and omnivore/predator
groups were also concentrated in the upper 10 cm
of the soil pro®le but to a lesser extent than microbivores (Table 1). Herbivores were more evenly distributed in the soil pro®le (above 40 cm) in cores
originating from KPRNA, or tended to be concentrated at lower soil depths in cores originating from
FHAES (Table 1, Fig. 1).
Variability in the depth distribution of nematodes
occurred across sampling dates, as indicated by large
depth month and depth year interactions
(p < 0.01; not included in Table 1) for several groups.
This variability did not, however, encompass large
changes in the general patterns of vertical distribution
already described. For example, microbivore densities
were more strongly strati®ed on autumn than on spring
sampling dates but densities remained highest at the
0±10 cm depth and lowest at the 40±60 cm depth in
both cases.
Fig. 3. Gravimetric soil moisture content of cores collected for
nematode extraction from control and irrigated plots averaged
across upland and lowland sites. An asterisk indicates a significant
difference between irrigation treatment within date according to
least-squares means of log10-transformed data (p 0.05). Data are
means of eight observations.
3.2. Irrigation transect experiment
The moisture content of soil cores collected for
nematode assay was 19% higher, on average, in
irrigated plots across sampling dates but moisture
differences varied with month and year (p < 0.001).
Soil moisture was signi®cantly higher (p 0.05) in
irrigated vs. control plots on ®ve of eight dates
(Fig. 3). Moisture content did not vary between sites
(upland vs. lowland). Volumetric soil water content,
determined by a time domain re¯ectometry (TDR) soil
moisture monitoring system (Campbell Scienti®c),
and daily precipitation amounts for these plots have
been reported by O'Lear and Blair (1999) for 1995,
the year with the greatest observed differences in soil
moisture between irrigation treatments.
Herbivores were the only trophic group to display a
moderately consistent response to irrigation across
sampling dates, with a 90% increase (p 0.07) in
average densities in irrigated vs. control plots. Irrigation date interactions (p 0.08) were observed for
herbivore, fungivore, and microbivore densities
(Table 2). Herbivore densities were higher
(p 0.05) in irrigated plots on four of eight dates,
with signi®cant responses observed in every year of
the study (Fig. 4(a)). Microbivorous nematodes, in
contrast, exhibited higher (p 0.05) densities with
irrigation only on the July 1995 sampling date when
soil moisture differences between treatments were
greatest (Fig. 4(b)). Densities of this trophic group
51
T.C. Todd et al. / Applied Soil Ecology 13 (1999) 45±55
Table 2
Analyses of variance and main effect means for nematode trophic group densities from the irrigation transect experiment, 1995±1997
Source of variation
df
Mean squares
herbivores
Year
Month (year)
Error (month year)
Site
Error (Site)
Irrigation
Error (irr)
Irr site
Error (irr site)
Site year
Site month (year)
Error (site month year)
Irr year
Irr month (year)
Error (irr month year)
Irr site year
Irr site month (year)
Residual error
2
5
7
1
1
1
1
1
1
2
5
7
2
5
7
2
5
7
**
0.797
0.831**
0.058
0.004
0.025
4.849
0.067
0.106
0.014
0.156
0.073
0.218
0.586**
0.344*
0.052
0.008
0.023
0.082
fungivores
*
0.276
1.288**
0.059
0.055
0.056
0.270
0.018
0.139
0.002
0.154*
0.112*
0.023
0.104
0.230*
0.032
0.037
0.018
0.055
microbivores
**
0.721
0.921**
0.057
0.105
0.020
0.111
0.004
0.017
0.012
0.072
0.104
0.085
0.228
0.258
0.078
0.057
0.242
0.118
omnivore/predators
1.667**
0.258
0.087
0.085
0.147
0.034
0.463
0.299*
0.001
0.036
0.150
0.087
0.130
0.068
0.115
0.044
0.068
0.045
Main effect means (thousands per square meter)
Year (n 48)
1995
1996
1997
1541
1420
2214
2151
1888
2737
830
822
1231
240
207
438
Month (year) (n 16)
July 95
October 95
June 96
August 96
October 96
June 97
August 97
October 97
1341
1740
876
1087
2297
1435
2585
2622
1987
2315
959
1287
3417
1271
2427
4513
621
1040
496
665
1304
717
1142
1832
216
264
188
121
313
408
444
463
Site (n 64)
Upland
Lowland
1843
1653
2257
2287
903
1051
291
313
Irrigation (n 64)
Control
Irrigated
1206
2290
2256
2289
961
993
309
295
*
p 0.05.
p 0.01.
**
tended to be comparable or lower in irrigated vs.
control plots on most of the other sampling dates.
Similarly, fungivore densities were higher (p 0.05)
in irrigated plots on the July, 1995 and June, 1996
sampling dates but no consistent responses were
observed across the remaining dates (data not shown).
Irrigation resulted in 15% higher omnivore/predator
densities in upland soils but 14% lower densities in
52
T.C. Todd et al. / Applied Soil Ecology 13 (1999) 45±55
Fig. 4. Densities of (a) herbivores and (b) microbivores in control
and irrigated plots averaged across upland and lowland sites. An
asterisk indicates a significant difference between irrigation
treatment within date according to least-squares means of log10transformed data (p 0.05). Data are means of eight observations.
lowland soils (signi®cant irrigation site interaction,
p 0.04) across dates.
Topographic effects were rare and, when observed,
varied across sampling dates. Fungivorous nematodes
were the only trophic group displaying dissimilar
population densities between upland and lowland
sites, with differences dependent on both month and
year (Table 2). This group tended to be more abundant
in upland soils early in the growing season and more
abundant in lowland soils late in the growing season
(data not shown).
4. Discussion
The responses of individual nematode trophic
groups to experimentally-altered soil moisture levels
were surprisingly consistent across experiments, seasons, and years. The largest responses were observed
with herbivorous taxa, where increased soil moisture
due to core transplantation or irrigation resulted in
increases of 52% and 90%, respectively, in nematodes
densities across years. The magnitude of the response
in the mesic tallgrass prairie irrigation experiment was
unexpected given that growing-season precipitation
across years was within 10% of the long-term average.
This contrasts with observations from the more xeric
shortgrass prairie, where plant-feeding nematode
responses to supplemental irrigation and nitrogen
were highly variable and often neutral (Smolik and
Dodd, 1983). A positive relationship between soil
moisture and herbivorous nematode densities has been
observed on wheatgrasses in the Utah desert (Grif®n et
al., 1996). Of course, individual nematode species will
exhibit preferences for speci®c soil moisture conditions (Schmitt and Norton, 1972) and functional group
responses to changes in water availability are likely to
vary both within and among ecosystems, depending
on the dominant taxa present. Nevertheless, the shortterm responses of total herbivore densities to increased
(or decreased) soil moisture levels were consistent
across a range of environments in the present study.
The remaining trophic groups displayed few signi®cant responses to changes in soil moisture. Fungivore and microbivore densities were higher in the
presence of supplemental irrigation on the date with
the lowest soil moisture content (and the greatest
difference in soil moisture between treatments) but
other responses to increased soil moisture were as
likely to be negative as positive, particularly for the
microbivores. In this case, the response is consistent
with the inverse relationship between the C : N ratio of
microbial biomass and water availability in tallgrass
prairie, re¯ecting an increase in the activity of bacteria
relative to fungi under drier conditions (Rice et al.,
1998). Microbivore densities have been observed to
increase concomitantly with increases in microbial N
and bacterial biomass in tallgrass prairie soils (Todd,
1996). Reduced microbivore densities under wetter
soil moisture regimes would, therefore, be consistent
with expected changes in microbial communities.
In the present study, microbivore populations which
developed under different soil moisture conditions
displayed differential responses to altered soil-water
availability, re¯ecting the importance of historic soil
moisture conditions. Whether this results from siterelated differences in nematode species composition
or from belowground food webs or processes that have
diverged under long-term differences in soil-water
availability remains to be determined. Regardless of
the mechanism, trends in nematode responses to soilwater availability do appear to differ among ecosystems. Our observations contrast with those from the
T.C. Todd et al. / Applied Soil Ecology 13 (1999) 45±55
shortgrass prairie, for example, where fungivorous
(Tylenchidae), microbivorous, and predaceous nematodes were all more responsive to supplemental water
and N than herbivorous nematodes (Smolik and Dodd,
1983). In a recent study of a perennial agricultural
system, only omnivorous genera of the Dorylaimida
responded (positively) to irrigation intensity (Porazinska et al., 1998). Such con¯icting results emphasize
that nematode responses to changes in climatic variables, such as water availability, should not be generalized across ecosystem types. Functional group
responses to changes in soil-water availability will
re¯ect the preferences of the major constituent taxa
present, as previously noted, but will also be determined by resultant changes in belowground processes
as mediated by historic conditions.
Seasonal patterns of herbivorous nematode densities in tallgrass prairie are typically related to root
phenology and biomass, especially during periods of
drought (Rice et al., 1998). Large decreases in root
production have been documented during drought
years at KPRNA (Hayes and Seastedt, 1987) but, in
the present study, root responses to altered soil moisture levels did not follow this simple trend. While cores
originating from FHAES had lower belowground
plant biomass than those originating from KPRNA
as expected, there was a trend for reduced belowground biomass at the more mesic KPRNA site compared to the more xeric FHAES site following core
transplantation (Blair et al., in preparation). Additionally, estimates of root biomass were not signi®cantly
affected by irrigation at KPRNA, although root biomass was greater in lowland vs. upland plots (Todd,
unpublished data). Together, these observations suggest that herbivorous nematode responses to changes
in soil moisture result from abiotic effects and are
independent of root responses. This hypothesis is
improbable, however, based on the comparative lack
of, or inverse, responses of the remaining trophic
groups to increased soil moisture levels and given
compelling arguments to the contrary (Grif®n, 1984;
Todd, 1996; Rice et al., 1998). It is more likely that the
dynamic nature of root production and the rapid turnover of roots in prairie soil confounded the relationship between precipitation patterns and root dynamics
in the present study. Pulses in new root production, as
measured by root windows, are ephemeral, with much
higher rates of turnover than can be measured for root
53
biomass (Hayes and Seastedt, 1987). Alternatively, the
herbivore response may re¯ect the increased N availability that accompanied wetter conditions in the
reciprocal core experiment (Blair et al., in preparation). The tallgrass prairie is characterized by N
limitation and herbivorous nematode densities in this
ecosystem respond positively to the increased nutrient
status of roots following N fertilization (Todd, 1996).
The experiments in the present study were designed
to encompass both short- and long-term effects of soilwater availability. Transplanted cores in the reciprocal
core transplant experiment permitted investigation of
the relationship between changes in soil-water availability and short-term responses by the nematode
community, while comparison of soil cores from their
respective sites of origin provided insights about
nematode communities derived under different annual
precipitation regimes. Similarly for the irrigation
transect experiment, short- and long-term nematode
responses to changes in soil-water availability could
be deduced, respectively, through comparison of irrigation treatments and topographical sites (soil moisture and net primary production are typically greater in
lowlands than in uplands; Knapp et al., 1993; O'Lear
and Blair, 1999). In both instances, short-term
responses were inconsistent with long-term differences. For example, short-term increases in herbivorous nematode densities in response to increased soil
moisture levels were documented in both experiments
but herbivore densities did not differ between soil
cores at their site of origin (with the exception of
the 40±60 cm depth, where differences were related to
soil texture, not location), nor did they differ between
upland and lowland sites, despite greater root biomass
for the lowlands (Todd, unpublished data). Thus, it
appears that the observed nematode responses may not
be indicative of more complex long-term responses to
changes in water availability. Resolution of this issue
awaits the longer-term measurements planned for the
present study.
Patterns of vertical distribution for nematodes in
KPRNA and FHAES soils were generally similar to
those reported for tallgrass and mixed-grass prairies,
with all trophic groups concentrated in the upper
20 cm of soil depth (Risser et al., 1981; Smolik and
Lewis, 1982). A notable exception was observed with
herbivore densities in FHAES-originated cores, where
nearly 70% of the population occurred below 20 cm. It
54
T.C. Todd et al. / Applied Soil Ecology 13 (1999) 45±55
is important to further note that all of the signi®cant
differences in nematode densities between locations
occurred at depths below 20 cm, regardless of soil
origin. These observations emphasize that grassland
nematode communities and their responses to climate
change may not always be accurately represented with
the standard 20 cm sampling depth.
5. Conclusions
Our data indicate that altered soil-water availability
related to potential changes in climate in the Great
Plains region will result in complex changes in the
structure of soil food webs in the grasslands of the
region. Tallgrass prairie nematode community
responses to experimentally-altered soil moisture
were dependent upon trophic habit, with plant-feeding
taxa responding rapidly and favorably to increased
moisture levels, while microbial-feeding taxa were as
likely to be negatively as positively impacted. These
variable responses appear to be the opposite of
expected responses from nematode communities in
the more xeric grasslands of the region (Smolik and
Dodd, 1983). Further complicating any predictions of
grassland ecosystem responses to climate change,
O'Lear and Blair (1999) reported that soil microarthropod communities in tallgrass prairie were negatively impacted by increased soil water content,
suggesting that responses among soil invertebrate
groups in this ecosystem are likely to be highly
variable. Finally, the data imply that short-term
responses by soil biotic communities may not suf®ciently predict the long-term consequences of climate
change, emphasizing the necessity of assessing such
responses over relatively long time scales.
Acknowledgements
The authors thank T. Oakley and the staff at Konza
Prairie Research Natural Area and the KSU Agricultural Research Center at Hays for ®eld and laboratory
assistance and plot maintenance. Research was funded
by the US Department of Energy's National Institute
for Global Environmental Change (DOE/NIGEC)
through the NIGEC Great Plains Regional Center at
the University of Nebraska, Lincoln. Financial support
does not constitute DOE endorsement of the views
expressed in this article. Contribution no. 99-119-J
from the Kansas Agricultural Experiment Station,
Manhattan.
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