INFLUENCE OF POCKET GOPHERS ON MEADOW VOLES IN A TALLGRASS PRAIRIE
BENJAMIN
A. KLAAS,
BRENT
J. DANIELSON,
AND KIRKA. MOLONEY
Department of Animal Ecology, 124 Science II, Iowa State University, Ames, IA 50011 (BAK, BJD) Department of Botany, Iowa State University, Ames, L4 50011 (BAK, KAM) Present address of BAK: 11 17A East Cota, Santa Barbara, CA 931 03 Creation of mounds by plains pocket gophers (Geomys bursarius) may affect the distribution of meadow voles (Microtus pennsylvanicus) and subsequent patterns of herbivory.
An association between abundance of meadow voles and density of neighborhood mounds
might be expected if voles use mounds as feeding sites (positive association), or if vole
avoid mounds due to lack of cover (negative association). Mounds also may indirectly
affect vegetative patterns, if mounds affect the distribution of herbivores. During two consecutive summers, we livetrapped voles and mapped mounds on three 80 m X 80 m plots.
Regressions of vole captures at each trap station against the number of mounds within a
range of radii of each trap were consistently negative across most spatial scales, but strongest correlation was found to be at 10 m. In all cases, bivariate scattergrams revealed a
"factor-ceiling" distribution, with data points widely scattered below an upper limit. We
also conducted an experiment to determine if seedlings had a greater or lesser mortality
due to small-mammal herbivory when growing on mounds versus off mounds. A two-tailed
paired t-test on the proportion of seedlings eaten after 13 days failed to show differences
between on-mound and off-mound rates of herbivory (P = 0.066); however, prior analyses
showing voles avoiding areas with high rates of disturbance give weight to the hypothesis
that seedlings growing off mounds experience higher rates of herbivory. Thus, through a
second-order indirect effect, the presence of gopher mounds could lead to distinct changes
in the plant community.
Key words: Geomys bursarius, Microtus pennsylvanicus, disturbance, gopher mounds,
microtine, indirect effects, seedling survival, tallgrass prairie
construction and maintenance of burrow
systems is expelled periodically to the surface, creating a mound. These small patches
of bare soil create microhabitats that differ
from undisturbed soil in plant species composition and biomass (Hobbs and Mooney,
1985; Grant et al., 1980; Martinsen et al.,
1990; Moloney and Levin, 1996; cf. Williams and Cameron, 1986). They also differ
in soil chemistry (Grant and McBrayer,
1981; Reichrnan et al., 1993; Zinnel and
Tester, 1990), and mounds are even known
to be positively correlated with the presence
of some species of grasshoppers (Huntly
and Inouye, 1988).
Gophers are known to directly affect the
plant community in tallgrass prairies
Fossorial rodents occur on all continents
except Australia and Antarctica (Andersen,
1987) and have been shown to have dramatic impacts on plant communities (Andersen, 1987; Huntly and Inouye, 1988;
Reichman and Jarvis, 1989). In North
America, all below-ground herbivorous
mammals are from the family Geomyidae
(Nowak, 1991). They create extensive burrow systems that serve for both foraging
and all other day-to-day activities. They are
solitary and actively defend their burrows
from conspecifics (Hansen and Miller,
1959).
Pocket gophers have been recognized as
important agents of soil movement (Grinnell, 1923; Mielke, 1977), and soil from
Journal of Mammalogy, 79(3):942-952, 1998
942
August I998
KLAAS ET &.---GOPHERS
AND VOLES IN TALLGRASS PRAIRIE
(Brotherson, 1982; Gibson, 1989; Huntly
and Inouye, 1988; Huntly and Reichman,
1994; Reichman, 1988; Reichman et al.,
1993; Reichman and Smith, 1985; Tilrnan,
1983; Williams et al., 1986). In fact, Huntly
and Inouye (1988:792)state that the effects
of gopher mounds "cascade through the entire trophic web." This may be especially
true in tallgrass prairies where perennial
grasses may limit availability of sunlight.
Low-light levels at the soil surface may inhibit establishment of dicots (Hartnett and
Keeler, 1995; Martinsen et al., 1990).
Breaks in the prairie canopy caused by gopher mounds may counteract this effect and
provide recruitment sites for seedlings.
This, in turn, may result in a greater diversity of plants (Martinsen et al., 1990; Williams and Cameron, 1986; Williams et d.,
1986). However, if mounds act as recruitment sites for seedlings, it follows that herbivores, which favor seedlings as forage,
could be found in higher abundance in areas
of high disturbance. Conversely, breaks in
the prairie canopy might be avoided if they
expose herbivores to predators (Batzli and
Lesieutre, 1995; Getz et al., 1987; Jekanoski and Kaufman, 1995; Kotler et al., 1988).
Only one previous study has examined
the influence of gophers on distribution of
another mammalian herbivore common to
tallgrass prairies. Whittaker et al. (1991)reported that adult male meadow voles (Microtus pennsylvanicus) showed a positive
relationship with mounds and that voles, in
general, crossed gopher mounds more than
would be expected if they moved at random. However, reasons for such a relationship are unknown.
We tested two hypotheses. First, we hypothesized that distributions of mounds and
the most abundant mammalian herbivore in
our area, the meadow vole, would be
strongly correlated. Second, we hypothesized that gopher activity would indirectly
affect rates of herbivory on seedlings.
METHODS
Study site and field methods.-The study was
conducted at Anderson Prairie, an 81-ha pre-
943
serve in Emrnet Co., NW Iowa, 3.5 k m NW of
the town of Estherville. The study area had a
moderately diverse (ca. 160 plant species) blacksoil tallgrass prairie with native (e.g., Andropogon gerardii, Sorghastrum nutans) and exotic
(e.g., Bromus inermis, Poa pratensis) grass species in abundance. In May 1994, we staked out
three 80-m by 80-m study plots, separated by
2100 m each. We put permanent stakes at 10 m
intervals throughout plots, creating three plots of
64 10-m by 10-m cells. These three plots (hereafter referred to as the N, SE, and SW plots)
comprised a long-term study of spatial relationships of gopher mounds, small mammals, and
vegetation patterns.
Surveys of gopher mounds.-On
23 May
1994, we counted all extant gopher mounds in
each 10- by 10-m cell of the three plots. At ca.
1-week intervals thereafter, we located all new
gopher mounds within the three plots and
marked them with small plastic garden stakes.
We recorded number of fresh mounds in each
cell of the plots during each survey. Thus, for
any cell within a plot during any given time period, the number of newly created gopher
mounds was determined. On the N plot, we used
a surveying transit to map locations of all gopher mounds and trap locations. With a relatively high degree of accuracy, we were able to obtain the location and timing (within ca. 1 week)
of all gopher mounds created between 23 May
1994 and 3 August 1995 on the N plot. On the
SE and SW plots, only weekly counts of mounds
for each cell were recorded.
Censuses of small mammals.-From the initial counts of mounds on 23 May 1994, we categorized each 10- by 10-m cell in each study
plot by its level of disturbance. Cells were assigned to categories of zero, low (1-2 mounds),
medium (5-7 mounds), or high ( > l o mounds)
disturbance (gaps between categories ensured a
wide range of distinctly different levels of disturbance; some cells fell in between categories,
but 87.5% were contained in the four categories). In each plot, five cells from each category
were chosen randomly as trapping cells. Within
a trapping cell, five Sherman live traps were
placed in fixed locations for the duration of the
study (Fig. 1).
We livetrapped rodents for 3 consecutive days
each week from 31 May to 11 August 1994 and
from 9 May to 3 August 1995. The 100 Sherman
live traps on each plot were opened on Monday,
JOURNAL OF MAMMALOGY
Vol. 79.No. 3
FIG.1.-Live-trapping design for meadow voles for the N (North) plot on Anderson Prairie. Each
shaded 10- by 10-m cell had five Sherman live traps equally spaced in the arrangement shown above.
Five cells were chosen randomly for trapping from each of four classes of initial densities of gopher
mounds. Blank cells were surveyed for mound building but not for vole activity. The distribution of
blank cells does not imply anything about the distribution of mounds. The SE (Southeast) and SW
(Southwest) plots were trapped in a similar manner. Traps were run for 3 consecutive days each week
for 11 weeks in 1994 and 14 weeks in 1995.
Tuesday, and Wednesday evenings at ca. 1700
h. Traps were baited with a small handful of dry
oats. We checked traps the next mornings beginning at ca. 0700 h. Captured animals were identified, weighed, sexed, ear-tagged, and released.
Thus, for any given trap during any given time
period, counts of numbers of individuals and
captures were obtained.
Seedling herbivory experiment.-We assessed
the impact that germination site (on- versus offmound) had on herbivory rates of seedlings using garden peas transplanted to the N plot in
1995. On 4 July 1995, we planted and germinated in a greenhouse 450 Wando variety garden
pea seeds in #9 Jiffy peat pellets. Seeds were
watered every day until germination, and then
every other day for 14 days. After 14 days when
the seedlings had reached an average height of
ca. 50 mm, they were transplanted to the N plot.
The experiment was conducted on this plot because it was the most mesic of the three plots,
thereby maximizing transplanting success. This
plot also had the highest amount of gopher activity.
For this experiment 37 mounds were selected
randomly from a pool of gopher mounds created
during the previous 3 weeks. We planted a clus-
ter of nine pea seedlings (3 by 3 arrangement)
in a square array ca. 10 cm on a side. We replaced the soil, leaving the mound appearing as
before except for the nine seedlings growing in
its center. On 12 mounds, we placed small (250
mm diameter, 250 mm tall) cylindrical exclosures of 6.4-mm mesh hardware cloth over seedlings, pushing exclosures 30-50 mm into the
soil to secure them. Those exclosures prevented
voles from eating seedlings. Over another 12
mounds, we placed exclosures similar to the first
set but with three 100- by 100-mm openings
("doors") at equal intervals along the base.
Those exclosures allowed voles access to seedlings but controlled for other unknown effects
that exclosures may have on seedling survival.
The remaining 13 mounds were used for
paired on-mound versus off-mound treatments.
Each off-mound treatment was located 1 m west
of the on-mound treatment. After parting the litter layer away from the area desired for planting,
nine seedlings were placed in a 3 by 3 arrangement identical to other treatments. After planting, we repositioned litter and surrounding vegetation to mimic an undisturbed gennination.
Seedlings in all treatments were watered after
August 1998
KLAAS ET =.-GOPHERS
AND VOLES IN TALLGRASS PRAIRIE
planting. Sufficient rains during the following 2
weeks made further watering unnecessary.
All treatments were checked for evidence of
small mammal herbivory at 5 and 13 days after
planting. We noted seedlings for their status
(alive or dead), herbivory by insects (holes
chewed in leaves), small mammals (stems
clipped off at an angle), or none. After day 13,
we removed all of the seedlings and exclosures
from the study plot.
Data analysis.-To determine how local disturbances such as gopher mounds affect vole activity, it was necessary to define the term "local" explicitly. Arbitrarily imposing a single
scale of observation may miss significant interactions at other scales of space or time (Levin,
1992). Therefore, we explicitly looked across a
range of spatial and temporal scales and objectively determined the most appropriate spatial
scale. That scale is referred to as the "neighborhood" when describing the relationship between voles and mounds. After proper spatial
and temporal scales were identified, we examined data to identify consistent trends in relationships between densities of voles and
mounds. That information was then coupled
with the experiment on the herbivory of seedlings.
We used the high-resolution mound data taken
with surveying equipment from the N plot to
determine spatial and temporal scales at which
gopher mounds most strongly influenced abundance of voles. We counted the number of
mounds produced in a specified time (e.g.,
mounds created in 1994) and within given distances of each trap station. Those distances comprised a range of radii, r, from each trap location.
Occasionally, those circles did not fall totally
within the plot. In those cases, the following
edge correction was used to adjust for low
counts from missing data:
where C,, was the edge-corrected count, b was
the proportion of the circle contained within the
study plot, and C is the uncorrected count from
the mound data.
We obtained mound counts at 10 different radii (2.5 to 25.0 m in 2.5-m increments around
each trap location) for four sets of temporally
categorized mound data: all mounds, mounds
from June 1994, mounds from June-September
945
1994, and mounds from March-June 1995. We
calculated a series of 40 nonpararnetric rank regressions (Conover, 1980) with number of vole
captures at each trap location as the dependent
variable and number of mounds within the given
radius of the trap as the independent variable.
Data containing all mounds, "all mounds," were
used as an estimate of the general-spatial-disturbance rate (i.e., local probability of disturbance),
and compared to 1994 and 1995 tallies of vole
captures. The three remaining sets of mound
counts were compared with tallies of vole captures only when the mound data preceded vole
data. Thus, vole captures from 1994 were not
compared with 1995 mounds, because voles
from 1994 could not be dependent on mounds
that had yet to be created. We plotted correlations of those regressions across the range of
radii to determine the search radius with the
highest descriptive power. This radius was called
the "neighborhood" and was used for all subsequent comparisons of mound disturbance and
vole abundance.
In exploring the temporal-scale issue, we divided mounds from 1994 and 1995 into two
groups each: mounds from June 1994, mounds
from July-August 1994, mounds from MarchMay 1995, and mounds from June 1995. Four
nonparametric rank regressions (Conover, 1980)
were compared using numbers of vole captures
at each trap in 1995 as the dependent variable
and number of mounds within the radius of the
neighborhood (10-m radius) of each trap as the
independent variable. From those comparisons,
we determined the most descriptive temporal
scale, and it was used in all further analyses.
On the SE and SW plots, we only had counts
of the number of mounds within the 10-m by
10-m cells (not precise locations within each
cell). Thus, we used the neighborhood radius (10
m) from the previous analyses of the N-plot with
a technique for estimating counts of gopher
mounds within the neighborhood of the trap (a
circle of radius, r, from each trap location).
Count estimates, C, were determined by the
equation:
where n was the number of cells contained within the circular neighborhood of the trap, p, was
the proportion of the area of the circle contained
in cell i, and c, was the number of mounds in
946
JOURNAL OF MAMMALOGY
cell i. When a circle was not wholly contained
within a study plot, an edge correction was
needed:
where C, was the edge-corrected mound count
and b was the proportion of the circle contained
within the study plot.
Using mound counts from this procedure, we
ran nonparametric rank regressions (Conover,
1980) for vole captures in 1994 and 1995 at the
temporal scale determined from the analyses of
the N plot. To establish that the weighted-average technique was an adequate estimate of
neighborhood disturbance rates, we applied the
technique to the N-plot data and compared count
estimates to those generated from the moundsearch program. We then compared rank regressions from all three plots to look for a consistent
relationship of voles to gopher mounds.
Density of local mounds, by itself, may not
dictate mean activity of meadow voles at a given
location. However, mound density may influence
one or more extremes in vole activity. This type
of relationship is common in ecological field
data (Blackbum et al., 1992; Kaiser et al., 1994;
Thomsen et al., 1996). For example, Thomsen
et al. (1996) found that gopher activity affects
the maximum number of flowers at a given location. At high levels of gopher activity, density
of flowers can range only from none to very
low. At locations with lower gopher activity, the
maximum number of flowers that is observed at
a given location increases, although the minimum number is still zero. Thomsen et al. (1996)
referred to those types of patterns as "factor
ceiling" distributions, with the independent variable placing a cap on values of the dependent
variable. We have adapted a method from Blackburn et al. (1992) to evaluate our data with those
ideas in mind. In this approach, regressions were
performed on only the upper percentiles of the
data (vole captures per trap) in discrete intervals
of the independent variable (mound density),
thereby fitting a least-squares line to the upper
bound of the data distribution. For a given comparison of voles versus mounds, we divided the
independent variable (mound density) into k
equal intervals according to the equation:
Vol. 79, No. 3
where n was the sample size and p was the desired percentile to examine. In this case, we
wanted to look at upper limits of vole activity,
so we used the 95% level; therefore, k = 10
intervals in these regressions. For each interval,
we plotted maximum number of vole captures,
and we performed a simple linear regression.
Factor-ceiling regressions were done for the
three plots at the spatio-temporal scales identified by analyses of the N plot described above.
We examined factor-ceiling regressions for consistent trends.
In analyzing the experiment on the herbivory
of seedlings, data were tallied as the proportion
of each replicate eaten by small mammals. Because of small samples, zeroes in the data were
given the value of 1/4n, and ones (100% mammal herbivory) were given the value of (n 114)ln (where n = 9, the number of seedlings
within each replicate) following the suggestion
of Snedecor and Cochran (1980). Values were
arcsin square-root transformed to normalize data
(Snedecor and Cochran, 1980). Transformed
values for exclosures with doors were tested
with a one-tailed t-test to see if they differed
significantly from zero. We performed a twotailed paired t-test on the rates of mean herbivory for the transformed on-mound and offmound data.
Effects of gopher mounds on voles.-In
1994, 260 voles (1,043 captures) were captured, and in 1995, 161 voles (739 captures)
were captured. The N plot had the highest
number of individuals and captures in 1994
and the most individuals in 1995 (Table 1).
Seven-hundred-eighty mounds were counted in 1994 and 1,261 in 1995. The N plot
had the highest numbers of mounds in both
years, followed by the SE plot and the SW
plot (Table 1). There was a great deal of
variation within plots; the number of
mounds within a 10-m by 10-m cell ranged
from 0 to 32 in 1994 and zero to 44 in
1995. The number of vole captures at a trap
location varied from zero to 26 in 1994 and
zero to 12 in 1995.
One cell in the N plot contained a disproportionately high number of vole captures (92 captures in 1994 and 25 captures
August 1998
KLAAS ET AL.-GOPHERS
AND VOLES IN TALLGRASS PRAIFUE
947
TABLE1.-Summary statistics of meadow vole capture and individual live-trapping data and gopher mound surveys from 1994 and 1995. Individual totals were estimatedfrom tallying unique eartag numbers in the data set. Retagged individuals were not counted in this total.
Plot
1994 vole
captures
1994
individual
voles
1995 vole
captures
1995
individual
voles
1994
mounds
1995
mounds
N
SE
SW
Total
490
324
229
1,043
119
67
74
260
301
324
114
739
68
61
32
161
432
182
166
780
650
392
219
1,261
in 1995 versus an average number of captures in other N-plot cells of 20.95 and
14.53, respectively). That cell was distinctly different in vegetation and soil moisture
and lower in relative elevation than and other cells. Because of extremes in vole abundance and environmental factors, capture
data of voles from that cell were omitted in
all analyses.
All slope estimates were negative for
nonparametric rank regressions of vole captures on the numbers of gopher mounds
across the 10 neighborhood radii on the N
plot. Squared correlation values ranged
from 0.001 (voles in 1995 versus mounds
in 1995 at 25 m) to 0.261 (voles in 1995
versus mounds in 1994 at 10 m). In the four
sets of regressions, a 10-m radius was con-
It 1995 v o l s versus 19!+tmounds ]
I
2.5
5
+- 1995v01~versusaum0unds
1
-A-
1994 v o l s versus 19!+tmounds
+
1995vol~versuslw5mounds
7.5 10 12.5 15 17.5 20 22.5 25
Radius (m)
FIG. 2.---Comparison of correlation values for
each of 10 neighborhood radii in four sets of
nonparametric rank regressions of voles versus
mounds, on the N plot (capture data for voles
from one cell were identified as an outliner and
left out of all analyses).
sistently the most descriptive, with the exception of voles in July-August 1994 versus mounds in June 1994 (Fig. 2), where 15
m had a slightly higher correlation. Thus, a
neighborhood radius of 10 m was used in
all subsequent analyses.
In using the weighted-average technique
(equation 3) for estimating mound densities
in the 10-m neighborhoods around each
trap station, the N-plot regressions produced correlations that were very similar to
regressions that used data obtained by precisely surveying locations of individual
mounds (Table 2). Thus, that technique was
used to analyze data from the SE and SW
plots. Like the N plot, all regressions for
the SE plot were negative (Table 2). However, regressions with the highest correlations were voles in 1995 versus mounds in
1995 and voles in 1995 versus all mounds
(both r., = 0.232).
, rather than voles in 1995
versus mounds in 1994 as in the N plot.
Of the four rank-regression slopes calculated for the SW plot, two were not significantly different from zero, one was positive, and one was negative (Table 2). We
examined scatter plots of the raw (unranked) data from all three plots of voles in
1995 versus mounds in 1995 (Fig. 3) to determine the cause. From visual inspection,
the SW plot, which produced a positive regression slope, looked similar to other
plots. Upon closer inspection, however, we
found that l5
loo points in Fig. were
null values for vole captures and mound
counts. Those 15 points pulled the left end
of the regression line down and created a
,
Vol. 79. No. 3
JOURNAL OF MAMMALOGY
948
TABLE2.-Correlation values for nonparametric rank regressions on four sets of comparisons of
voles versus mounds. Direction of the slope for each regression is given if the slope is difSerentfrom
zero ( P < 0.05). One cell from the N plot (5 of 100 points) was left out of the analyses as an outlier.
For the Nplot, the first column shows results of regressing ranks of vole captures against the number
of mounds in a 10-m search radius using mapped mound locations. The second column used the
weighted-average technique, which was also used for the SE and SW plots.
Regression
(voles versus
mounds)
1995 versus
1995 versus
1995 versus
1994 versus
1994
1994
1995
all
June
N plot
(surveyed data)
Sign of
slope
-
-
1.2
N plot
(weighted-average)
SE plot
(weighted-average)
SW plot
(weighted-average)
Sign of
slope
Sign of
slope
i-2
Sign of
slope
0.044
0.232
+
0.261
0.124
0.208
-
0.128
-
-
spurious positive bias in the relationship.
After eliminating those null values, the regression resulted in a negative slope that
did not differ from zero (P = 0.43). Thus,
significantly negative slopes were observed
for comparisons in the N and SE plots, but
only one of the four slopes on the SW plot
was significantly negative, although scatter
plots of data appeared very similar.
Further visual inspection of scatterplots
1.2
0.232
0.11
0.168
-
0.238
0
0.092
-
0.062
-
-
i-2
0
0.055
0.13
of mound densities and vole activity (Fig.
3) suggested that gopher activity may set
maximal levels to vole activity but not minimal levels. In such cases, factor-ceiling regressions may be more appropriate than
more conventional regression methods
(Thomson et al., 1996). Such regressions
were performed for all three plots comparing voles in 1995 to mounds in 1995,
mounds in 1994, and all mounds and com-
4
sw
-
.
...
. . ... .
.
.
I
)
I..
0..
a.
a.
.m
...
-
FIG. 3.-Scatter plots of vole capture at each trap station during July-August 1995 versus the
numbers of mounds created within 10 m of each trap station during March-May 1995. Rank regressions of these data show a significant negative slope for the N and SE plots, but a significant positive
slope for the SW plot. Note the different scale for mound densities on the N plot due to higher
mound-building activity.
August I998
KLAAS ET AL.-GOPHERS
AND VOLES IN TALLGRASS PRAIRIE
TABLE3.-Correlation values for 12 factorceiling regressions of voles versus mounds. One
cell from the N plot was left out as an outlier
(see text for explanation for factor-ceiling regressions). Slopes for all regressions were negative.
Comparison
Plot
Voles
Mounds
r2
P (slope
= 0)
e
."0
L
2
.i
L
0.2 -
4
w
0 .*5
0.1 -
U
N
SE
SW
1994
1995
1995
1995
1994
1995
1995
1995
1994
1995
1995
1995
June 1994
1994
1995
All years
June1994
1994
1995
All years
June 1994
1994
1995
All years
0.603
0.475
0.235
0.403
0.290
0.395
0.483
0.393
0.588
0.534
0.508
0.531
0.01
0.03
0.16
0.05
0.11
0.05
0.03
0.05
0.01
0.02
0.02
0.02
paring voles in July-August 1994 to
mounds in June 1994. Of the 12 factor-ceiling regressions, all had negative slopes, and
10 were significantly different from zero.
Squared correlation values ranged from
0.235 to 0.603 (Table 3), thus providing
somewhat more consistent and stronger relationships between vole activity and density of local mounds than was found using
traditional techniques. All slopes were negative (P < 0.001), and 10 of 12 were significantly different from zero (P < 0.02). In
fact, highest correlations were seen in comparisons of the SW plot. Consistent correlations and negative slopes in all three plots
(Table 3) gave weight to the conclusion that
mound density set an upper limit on vole
activity.
Vole captures in 1995 were compared
across a range of temporal scales. Sets of
mound data at a temporal scale of 1-month
duration did not add more descriptive power than a temporal scale of 1 year. The combined mound data from 1994 and 1995 (all
mounds) showed an intermediate correlation
value as compared with separate regressions
of voles in 1995 versus mounds in 1994 and
voles in 1995 versus mounds in 1995 (Fig.
;i]
w
01
S
o
,
A11
,
'
,
.
,
,
,
'94 'June Jul- '95 ' ~ a r - ' J u n e '
'94 Aug
May '95
'94
'95
Mounds
FIG.4.--Comparisons of regressions of numbers of gopher mounds within 10 m of each trap
location and vole captures in 1995. Each bar
represents a different set of mound data. Analyses using temporal scales of < 1 year did not
explain patterns of variation in the vole-mound
relationship as well as scales of 2 1 year.
4). Thus, it appeared that the best predictor
of vole activity was number of mounds created during the previous summer.
EfSects of gopher mounds on herbivory.-No small-mammal herbivory was observed in the total-exclosure treatment. Of
remaining treatments, frequency of mammalian herbivory was lowest for exclosures
that had doors. That indicated that the hardware-cloth cages inhibited herbivory, although the average proportion of seedlings
that were consumed totally was significantly greater than zero in this treatment (P <
0.05).
Seedlings classified as having experienced herbivory by small mammals were
identical in appearance (leaves gone, stems
chewed off at an angle) to plants near hay
piles made by M. pennsylvanicus (B. A.
Klaas, in litt.). Thus, we conclude that total
exclosures were effective in excluding
small-mammal herbivores, and that we successfully identified herbivory by small
mammals.
Of the treatments without exclosures,
seedlings in the on-mound treatment expe-
950
JOURNAL OF MAMMALOGY
rienced less herbivory than seedlings in the
off-mound treatment, as measured by either
total number of seedlings eaten or average
proportion of seedlings eaten per array.
However, the observed difference in average proportion of seedlings eaten between
on-mound and off-mound treatments was
not significant (two-tailed paired t-test, P =
0.066).
Disturbance and herbivores.-If physical factors, such as gopher mounds, influence habitat selection by voles, each vole
must perceive its individual landscape at
some particular spatial scale when judging
local habitat quality. One reasonable estimate of such a scale might be the individual's home range. Home-range size can be
difficult to define (Burt, 1943; McNab,
1963), but the polygons describing daily activity patterns in M. pennsylvanicus given
by Madison (1985) show areas similar in
size to a circle with a 10-m radius. Bowers
et al. (1996) also estimated home-range
sizes for M. pennsylvanicus at different levels of habitat fragmentation. In contiguous
habitat, estimates of the radius of an average of home range were 9.5 m for adult
females and 10.5 m for adult males. It is,
perhaps, not coincidental that the radius of
a vole's home range and the radius producing the strongest vole-mound correlation at
a trap site (Fig. 2) are both ca. 10 m.
The factor-ceiling analysis is one of only
a few that have been decribed explicitly in
the ecological literature (Blackburn et al.,
1992; Kaiser et al., 1994; Maller et al.,
1983; Thomsen et al., 1996). Nonetheless,
this type of relationship may be quite common, and we believe that conclusions from
factor-ceiling regressions best describe of
the observed patterns from the field. Unfortunately, factor-ceiling regressions do
not provide much insight into factors that
might regulate the dependent variable (in
our case vole activity) below the ceiling.
Thus, we can only speculate that it is probable that the lack of cover in areas of high
Vol. 79. No. 3
mound density may set the upper limit to
local vole activity, but other factors also
must regulate vole activity much of the
time.
Microtus pennsylvanicus has a host of
avian and terrestrial predators (Pearson,
1985) and is known to have an affinity for
habitat with a high percentage of cover
(Zirnmerman, 1965), presumably for protection. While voles consistently show negative relationships with gopher mounds at
the scale of ca. 300 m2, the plot with the
most vole captures and individuals in 1994
and most individuals in 1995 had the most
gopher mounds in both years, and the plot
with the least vole captures and individuals
in both years had the least mound activity
in both years (Table 1). This suggests that
at larger scales (ca. 6,400 mZ)environmental factors may affect abundances of voles
and gophers in the same manner, although
at smaller scales (ca. 300 m2)there is a negative relationship.
Temporally, a vole's perception of what
a gopher mound represents may change as
the mound ages and gradually becomes revegetated. The data suggest that voles are
affected most strongly by mounds of ca. 1
year of age (Fig. 4). However, finer temporal scales of resolution (i.e., intervals <
1 year) that produce weaker correlations
with vole activity may reflect social interactions between individuals that prohibit
immediate spatial reshuffling in response to
changes in habitat quality (e.g., mound density).
Significance of the negative correlation
between gopher activity and the upper limits on vole activity may be important in
structuring prairie plant communities if
mound density indirectly affects seedling
success, especially because all seedlings
that were attacked were killed. After 5 days
of our seedling experiment, only two seedlings had experienced herbivory by small
mammals. However, by day 13, 139 of 342
(41%) seedlings available to voles had been
attacked. Although we did not observe any
significant environmental changes that may
August 1998
KLAAS ET AL.-GOPHERS
AND VOLES IN TALLGRASS PRAIRIE
have caused the increase between days 613, 92% of the seedling arrays that experienced herbivory encountered it first in this
interval.
Survival of seedlings on mounds and off
mounds did not differ, although lower survival of seedlings on mounds was consistent with the negative relationship observed
between vole activity and gopher mounds.
We believe that the large variation in vole
activity in neighborhoods of low mound
density (i.e., regions of low mound density
do not necessarily have high vole activity)
may explain why this difference was not
more pronounced.
Because the majority of prairie plants are
perennials and many of them reproduce
clonally, recruitment from seed may not
play a major factor in structuring prairie
vegetation (Hartnett and Keeler, 1995).
However, a recent study of species richness
in tallgrass plant communities in Wisconsin
(Leach and Givnish, 1996) documented that
small fragments (0.24.6 ha) of native prairie have lost significant numbers of species
over the last 32-52 years. Leach and Givnish (1996) suggest that lack of natural
wildfires may be the cause of these extinctions, but if small fragments will not consistently support gopher activity, this also
may contribute to the slow decline. It also
is interesting that the plant species most
commonly lost in these prairie fragments
are legumes, which are highly desirable
items in the diet of M. pennsylvanicus (Lindroth and Batzli, 1984). In any event, if the
interaction between gophers and voles is
maintained for long periods of time, it has
the potential to affect vegetative patterns in
the form of species abundances and community heterogeneity and perhaps promote
high levels of plant species richness characteristic of tallgrass prairie ecosystems.
This research was made possible with the help
of grants to B. J. Danielson and K. A. Moloney
from the Iowa Department of Resources' Nongame Program and The State Preserves Board,
95 1
a grant to B. A. Klaas from The American Museum of Natural History Theodore Roosevelt
Fund for Mammalogy, and a scholarship to B.
A. Klass from The Friends of Iowa Lakeside
Laboratory. Field data were collected with the
help of J. Paulin, J. Verdon, and K. Wolfe-Bellin. Two anonymous reviewers provided many
helpful comments to an earlier draft of this
manuscript. Please send reprint requests to B. J.
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-
Submitted 8 Janualy 1997. Accepted 17 November
1997,
Associate Editor was Robert K. Rose.