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Diminishing effects of ant mounds on soil heterogeneity across a chronosequence of prairie restoration sites
ARTICLE IN PRESS Pedobiologia 49 (2005) 359—366
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Diminishing effects of ant mounds on soil heterogeneity across a chronosequence of prairie restoration sites Diana R. Lane, Hormoz BassiriRad Department of Biological Sciences, University of Illinois at Chicago, Chicago, IL 60607-7060, USA Received 15 March 2005; accepted 2 April 2005
KEYWORDS Ant mounds; Nitrogen cycling; Grassland; Restoration; Soil heterogeneity
Summary It is well recognized that mound-building ants affect soil and vegetation heterogeneity, yet little is known about the extent to which such changes are propagated through time. We compared soil properties from ant mounds (built by Formica montana and Acanthamyops claviger) and from adjacent prairie soils at three tallgrass prairie restoration sites in the Midwestern United States, ranging in age from 8 to 26 years post-restoration of native species on former row-crop agriculture plots. We were particularly interested in N-dynamics on and off the mounds. All of the soil variables measured showed the greatest difference between mound and prairie soils at the 8year old site. At that site, we found that ant mounds had significantly higher concentrations of total N, dissolved organic N, and NH+4 compared to prairie soil. Differences in concentrations of these nitrogen pools between mound and prairie soils were, however, lost with increasing time since restoration. The lack of N-enrichment at the older sites suggests that nutrient enrichment of ant mounds may be a transient phenomenon in certain ecosystems. To our knowledge, this is the first report that illustrates a critical, but a temporally dynamic role of ant mounds in creating resource heterogeneity in a restoration project. & 2005 Elsevier GmbH. All rights reserved.
Introduction Mound-building ants play a significant role in creating and maintaining soil heterogeneity in North American grassland ecosystems (Culver and
Beattie, 1983; Gibson, 1989; Carlson and Whitford, 1991; Wagner et al., 2004). Physical soil properties, including soil texture, bulk density, soil temperature, and soil moisture, are often different within ant mounds compared to surrounding soil (Rogers
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E-mail addresses: [email protected] (D.R. Lane), [email protected] (H. BassiriRad). 0031-4056/$ - see front matter & 2005 Elsevier GmbH. All rights reserved. doi:10.1016/j.pedobi.2005.04.003
ARTICLE IN PRESS 360 and Lavigne, 1974; Laundre´, 1990; Carlson and Whitford, 1991; Wagner, 1997; Wagner et al., 2004). Mound soils can also be enriched in macroand micro-nutrients and have higher nitrogen mineralization rates compared to surrounding soils (Baxter and Hole, 1967; Petal et al., 1977; Culver and Beattie, 1983; Kelly et al., 1996; Wagner, 1997; MacMahon et al., 2000). Ants in tallgrass prairie have indirect effects on vegetation and soils through excavation of mounds and incorporation of organic material into their nests, in contrast to the seed-harvesting ants in arid- and semi-arid habitats (e.g., Pogonomyrmex spp.), which consume seeds and clear large ‘‘disks’’ of vegetation around the mound (MacMahon et al., 2000). The documented importance of ants in ecosystem functioning suggests that ants could play a significant role in creating and maintaining heterogeneity in soil fertility during the process of habitat restoration. In the Midwest region of the United States, where less than 1% of tallgrass prairie remains intact, restoration of tallgrass prairie grasslands has been undertaken on former rowcrop agricultural sites where soils have been homogenized through decades of cultivation. The need to increase soil heterogeneity at these sites has been recognized, but many suggested techniques for soil modification are not appropriate for use in large areas (Collins et al., 1998). Although the presence of native prairie ants at tallgrass prairie restoration sites has been noted (Trager, 1990; Petersen et al., 1998), there have been no attempts to evaluate successional changes in the spatial extent and functional consequences of ant activity at restoration sites or in unmanaged native plant communities. We tested the hypothesis that mound-building ants at restoration sites increase soil heterogeneity through the creation of ant mounds with distinct physical and/or chemical properties compared to surrounding soils. We used a 26-year chronosequence of tallgrass prairie restoration sites at Fermi National Accelerator Laboratory (FermiLab) outside of Chicago, IL, USA to test this hypothesis.
Materials and methods Study site This study took place at a chronosequence of tallgrass prairie restoration sites at Fermi National Accelerator Laboratory (FermiLab), approximately 48 km west of Chicago, IL, USA (Jastrow, 1987, 1996). Restoration of tallgrass prairie began in 1975
D.R. Lane, H. BassiriRad using sites which had been converted from native prairie to row-crop agriculture in the mid-1800s (R. Lootens, 2001, personal communication). The first restoration site was planted in 1975 with over 70 plant species collected from nearby prairie remnants (Betz, 1986). In subsequent years, sites were planted with seeds harvested from this and later sites. Seeding rates were similar in all sites, but exact records of the seed mixes were not kept (Sluis, 2002). This study was part of a larger evaluation of changes in soils and vegetation properties across the FermiLab chronosequence (Lane, 2002). Seven sites were included in the study: five restoration sites planted in 1975, 1985, 1993, 1997, and 2000; an old-field that was taken out of cultivation in 1994; and a prairie remnant located 6 km north of FermiLab (West Chicago Prairie). These sites are referred to by their age in 2001 when sampling took place (i.e., the site planted in 1975 is the 26-year old site). The 8-, 16-, and 26-year old sites were selected for more intensive sampling of ant-mound characteristics to determine if the degree of alteration of soil properties for ant mounds varied with time since restoration. Vegetation studies at FermiLab have demonstrated that succession proceeds rapidly, resulting in climax C4 prairie grasses dominating net primary productivity after approximately eight growing seasons (Jastrow, 1987; Lane, 2002. To the greatest extent possible, study sites were selected that had similar soils and similar fire histories. Because we were sampling sites that had already been created, exact matches of conditions were not possible. All seven study sites were located on silt loam soils, although the official soil classifications differed slightly. The four youngest restoration sites and the old-field were located on Barrington silt loam, while the oldest restoration site was mostly on Wauconda silt loam with some small areas of Drummer silty clay loam. The prairie remnant was located on Mundelein silt loam (Goddard, 1979; Mapes, 1979). The restored sites had been burned on a 2-year rotation since 1992, with the most recent burn before sampling being April 2000. West Chicago also is burned on a 2-year rotation, with the most recent burn before sampling being November 1999. The old-field and 1year old site have never been burned. Because the design of the study compares ant mound soil to bulk soil within a site, any differences in soil type or fire history across sites are unlikely to affect the within-site comparisons. Two mound-building ant species were found at the sites in this study. Formica montana Emery is a predatory ant and has its greatest abundance in
ARTICLE IN PRESS Effects of ant mounds on soil heterogeneity tallgrass prairies. Acanthomyops claviger Roger harvests ‘‘honeydew’’ from root-feeding aphids which are tended in their nests (Trager, 1998).
Mound characteristics For all seven study sites, the density of mounds in July 2001 was determined by counting mounds and dividing by the area of the sampling plot (9 m 13.5 m). The basal area of each ant mound was determined using the following formula for an ellipse (Baxter and Hole, 1967): Basal area ¼ pR1 R2 where R1 and R2 were the short and long perpendicular radii measured on the mound. Total ant mound area was divided by plot area (121.5 m2) to obtain the relative basal area of ant mounds at each site. Soil was sampled from three active ant mounds at each of the 8-, 16-, and 26-year old sites on November 16, 2001. Mounds were chosen randomly from among all the active mounds mapped in the 9 m 13.5 m sampling plot in July 2001. Active mounds had ants present or clear evidence of recent ant activity. Within a site, mounds sampled were separated by an average of 6.5 m, with a range of 3–8.7 m. The mound sample (5 cm diameter 15 cm deep) was collected 20 cm from the mound edge following the short radius of the mound (R1); the prairie, or ‘‘off-mound,’’ sample was collected on the short radius and in the opposite direction 20 cm away from the mound edge. Soil samples were transported to the laboratory on ice and weighed to determine bulk density. Cores were collected with a fixed-sleeve-type corer (AMS core sampler, American Falls, ID, USA). Soil cores were sieved through a 4 mm sieve and root fragments larger than 2 mm were picked out by hand. A 20 g sub-sample was dried at 105 1C and used for moisture determination. A 10 g soil subsample was extracted with 100 mL of 1 M KCl (Robertson et al., 1999) and a sub-sample analyzed for NO 3 and NH4 þ; a second aliquot was digested with a perchlorate digestion and analyzed for total dissolved N (both analyses: AlpKem autoanalyzer, Model 300, Clackamas, OR; Kansas State University Soil Testing Laboratory, Manhattan, KS, USA). Dissolved organic N (DON) was calculated as total dissolved N minus inorganic N. Soil texture (percent sand, silt, clay) was determined using the hydrometer method on a 50 g sub-sample of air-dried soil at the Kansas State University Soil Testing Laboratory. Total N and C were measured using flash combustion followed by gas chromatography (Fisons NA 2500, Carlo-Erba
361 Instruments Inc., Milan, Italy). As no carbonates were present in the sample, total C is equivalent to organic C. Linear regression analysis was used to determine whether there was a significant change in antmound area or density with increasing restoration age. The old field and native prairie sites were excluded from regressions because no restoration age can be assigned to these plots. Enrichment of mound soils was calculated as the difference between mound and prairie soil properties for each set of paired samples (N ¼ 3 pairs per site). A one-way analysis of variance was used to determine if there were significant differences across sites in the enrichment of mound soil for a set of soil properties. For variables with a significant F-test (Po0:05), Tukey’s honest significant different (HSD) test was used for post-hoc comparisons of site means. In addition to evaluating significant differences in mound enrichment across sites, we also analyzed the data for significant differences between mound versus prairie samples within each site. Means and standard errors for soil properties were calculated for the three mound and prairie replicate samples at the 8-, 16- and 26-year old sites. Within each site, a paired t-test was used to determine significant differences between mound versus prairie samples. Because three t-tests were conducted for each variable, a Bonferroni correction was applied so that differences were considered to be significant at the Po0:017 level (a ¼ 0:05=3). This correction minimizes the risk of a Type I error, but increases the risk of a Type II error. To address this issue, differences that were significant at a level of 0:017oPo0:05 were regarded as marginally significant. All analyses were conducted using S-plus 4.5 (MathSoft, 1997).
Results Total basal area of ant mounds increased significantly (from 0.25% to 1% of ground area) with increasing time since restoration (Fig. 1). At the native prairie, however, ant mounds covered only 0.02% of ground area. During the first 16 years following restoration, there was an increase in the area per mound with increasing time since restoration, but no significant increase in the density of ant mounds (r 2 ¼ 0:06, F 1;2 ¼ 0:14, P ¼ 0:75) (Fig. 1, Table 1). Between 16 and 26 years of restoration, however, the density of mounds increased sharply from 165 to 905 ha1 while the average size of mounds declined from 0.42 to 0.12 m2 (Table 1).
ARTICLE IN PRESS 362
D.R. Lane, H. BassiriRad
Old field 1.0
Chronosequence
% Total area with ant mounds
Native prairie 0.8
0.6 2 r = 0.97, p = 0.002
0.4
0.2
0.0
0
10
20
30
Site age (years)
Figure 1. Increase in relative basal area of ant mounds with increasing restoration age across a chronosequence of tallgrass prairie restoration sites at FermiLab outside of Chicago, IL, USA. An old field and native prairie are shown for comparison but not included in the regression because no restoration age is associated with these sites. Linear regression is as follows: Area (%) ¼ 0.035*Age+0.13, F 1;3 ¼ 91:1, r 2 ¼ 0:97, P ¼ 0:002.
Table 1. Ant mound density and mean area of mounds for a prairie restoration chronosequence, an old field, and a remnant prairie site Site
Mound density (No. ha1)
Area per mound (m2)
Old field 1-year 4-year 8-year 16-year 26-year Remnant prairiea
412 247 165 329 165 905 82
0.07 0.10 0.13 0.10 0.42 0.12 0.02
a
(0.03) (0.03) (0.12) (0.07) (0.29) (0.04)
Only one ant mound was found at the remnant prairie.
Inorganic N in these soils was largely present as NH+4; on average, inorganic N was 87% NH+4 and 13% + NO 3 for bulk soil and 75% NH4 and 25% NO3 for antmound soil. DON was a substantial portion of the extractable N at these sites; on average, total dissolved N was 59% inorganic N and 41% DON for bulk soil and 61% inorganic N and 39% DON for antmound soil. For six of seven measured soil properties (only excluding DON), the percentage difference between mound and prairie soil was highest at the 8-year-old site compared to the 16- or 26-year old
site (Figs. 2 and 3). Enrichment of ant mounds was significantly greater at the 8-year old site compared to the 16-year old site for soil moisture, inorganic N, total dissolved N, and total C (Tukey’s HSD test, Po0:05; results not shown). Enrichment of ant mounds was significantly greater at the 8year old site compared to the 26-year old site only for soil moisture, because of greater variability at the 26-year-old site. Within the 8-year-old site, there were significant differences between mound and prairie soil samples for total C (P ¼ 0:009), NH+4 (P ¼ 0:016), and DON (P ¼ 0:009). In addition, there were marginally significant differences between mound and prairie soil samples for bulk density (P ¼ 0:02), soil moisture (P ¼ 0:04), and total N (P ¼ 0:019). These differences were noted as marginally significant because the p-value fell between the Bonferroni corrected significance level (Po0:017) and a standard 95% confidence level (Po0:05). In contrast, within the 16-year old site, there was a significant difference between mound and prairie soil samples only for bulk density (P ¼ 0:0003), and a marginally significant difference only for DON (P ¼ 0:048). Within the 26-year old site, there were no significant differences between mound and prairie soil samples (P40:05 for all variables). There were no significant effects of ant mounds on percent sand, silt, or clay at any of the three sites (results not shown).
ARTICLE IN PRESS Effects of ant mounds on soil heterogeneity 8 yr. old
363 16 yr. old
26 yr. old
Bulk density (g cm-3)
1.0
p < 0.05
**
*
** p < 0.001
0.5 -46% -62%
-44%
On-mound Off-mound
0.0 30 31% -0.8%
20
2.1%
10
Total C (%)
Soil moisture (%)
p < 0.017
4
80%
9.4%
* 2
-7.9%
0
Figure 2. Soil physical properties at tallgrass prairie restoration sites of three different ages. Bars represents means71 std. err, n ¼ 3 samples per site. Percentage values within bars indicate the average difference between the paired mound and prairie samples. 8 yr. old
On-mound Off-mound
26 yr. old p < 0.05 * p < 0.017
3
+
NH4 (µg g-1)
-
NO3 (µg g-1)
6
16 yr. old
800%
170%
0 10 5 250%
*
Total N(%)
0
Diss. Org. N (µg g-1)
160%
29%
28%
-4. 2%
-9.5%
323%
104%
0.4 0.2 0.0
22%
8 * 4 213% 0
Figure 3. Soil nitrogen status at tallgrass prairie restoration sites of three different ages. See Fig. 2 for details.
Discussion Measurements of ant-mound basal area and antmound soil quality presented opposing trends over time: while the surface area covered with ant
mounds increased with increasing restoration age, the relative enrichment of ant mounds decreased. Several different lines of evidence all supported two central conclusions, (1) ant mounds were highly distinct from prairie soils at the 8-year old site, (2) these differences were transient and did not persist at the 16- and 26-year old sites. First, six of seven soil variables measured showed the greatest percentage difference between mound and prairie soils at the 8-year-old site (Figs. 2 and 3). Second, results from an ANOVA demonstrated that the relative enrichment of ant mounds at the 8-year old site for soil moisture, inorganic N, total dissolved N, and total C was significantly greater than at the 16-year old site. Third, paired t-tests demonstrated that total N, DON, NHþ 4 , and total C were significantly higher for mound versus prairie soil at the 8-year old site, but none of the soil measures were significantly different for mound versus prairie soil at the 26-year old site. These effects in tallgrass prairie are distinct from the pattern seen with harvester ants (Pogonomyrmex barbatus) in desert environments, where nutrient concentrations increase with colony age compared to surrounding soils (Wagner et al., 2004). Our results suggest that nutrient enrichment can be a transitory property of ant mounds in tallgrass prairie. Carlson and Whitford (1991) had noted that ‘‘nutrient enrichment of mounds y appears ubiquitous among mound-building ants’’; but these results suggest that ant mounds in restored tallgrass prairie do not fit into their paradigm.
ARTICLE IN PRESS 364 Comparisons of the 8- and 26-year old sites suggest that the lack of differentiation between mound and prairie soils at the 26-year-old site is likely a function of changing conditions in the prairie soil. For example, the total N content of ant mounds was identical at the 8- and 26-year-old sites (0.28%), but the prairie soil had a higher N content at the 26-year old site compared to the 8year old site (0.31% versus 0.23%). Thus, the enrichment of ant mounds over time did not keep pace with the increase in total N of the prairie soil following 26 years of restoration. Because the surface of an active ant mound lacks plant cover, the ant mound loses the continual input of root and leaf litter that occurs on vegetated soil. If the active incorporation of organic matter by ants into the ant nest is equal to or less than the organic input that would occur in the absence of ants, then we would expect that there would be no relative enrichment of soil on ant mounds. This hypothesis is consistent with other reports (Carlson and Whitford, 1991; Whitford and DiMarco, 1995) that have compared several sites and concluded that the degree of enrichment of ant mounds is negatively correlated with the productivity of the surrounding area. Another possibility is that the boundaries of an ant-mound might become more diffuse over time, so that a sample taken 20 cm away from a mound edge at the 26-year old site includes a diffuse antmound signal, while an off-mound sample at the 8-year-old site does not include an ant-mound signal. We took our ‘‘off-mound’’ sample relatively close to the edge of the mound (20 cm), because we were interested in examining whether ant mounds represented significantly enriched discrete microsites. Our observation of a lack of differentiation at the 26-year old site between the discrete antmound area (the visible boundaries of the ant mound) and the nearby off-mound area still holds true, whether or not the mechanism results either from a relatively lower enrichment of ant-mound soil or from increasing enrichment of surrounding areas. Changes in bulk density over time paralleled the changes in total N content. In particular, data from intermediate age plots indicated that most of the observed age-dependent convergence between ant mounds and the surrounding soil had already occurred within the first 16 years of restoration. Ant mounds at the 16-year old site had significantly lower bulk density than prairie soil, but the relative difference between mound and prairie soil at the 16-year old site was smaller than at the 8-year old site because bulk density in prairie soil had decreased with increasing restoration age.
D.R. Lane, H. BassiriRad We realize that small sample sizes in this study (three mounds per age) require a cautious approach to generalizing our results. Because of this small sample size, our mean values may not reflect true within-site means. Sampling mounds at additional sites and increasing the number of mounds sampled would help to confirm the trends noted here. The use of multiple lines of evidence and the fact that we found significant differences between mound and prairie soils at the 8-year old site at the P ¼ 0:017 level suggests that these results are quite robust despite limited statistical power. Furthermore, the trend of increasing similarity between mound and prairie soils with increasing time since restoration was consistent across almost all of the physical and chemical properties measured. This study is the first report of ant colonization increasing dramatically in response to tallgrass prairie restoration. There was a significant increase in ant-mound area across the chronosequence, but no consistent change in ant-mound size or density. The estimate of relative basal area for ant mounds at the 26-year old restoration site (1.0%) was lower than the relative area for Formica cinerea mounds at a Wisconsin prairie (1.7%) (Baxter and Hole, 1967) but much higher than the relative area of ant mounds at the remnant prairie site in this study (0.02%). There are few other published estimates of the relative area of ant mounds in tallgrass prairie, so it is difficult to determine whether ant mound colonization at the restored sites has recovered to values appropriate for similar prairie types and soils. Low ant mound area at the remnant prairie site in this study (which is poorly drained) is likely to be an underestimate for a welldrained prairie (Blom et al., 1991). The increase in ant mound area with increasing restoration age found in this study contrasts with the results of Foster and Kettle (1999) who found that the mound-building ant Formica subsericea was common on unplowed prairie in Kansas but almost absent in nearby restored prairies. They found 113–122 mounds per hectare in the remnant prairie, and fewer than 4 mounds per hectare in restored prairie. Further study is needed to determine if different patterns of ant colonization in restored prairies are a function of soil characteristics or of the particular species of ant that is present.
Implications for Soil and Vegetation Heterogeneity The physical presence of ant mounds as areas free from vegetation creates significant spatial heterogeneity within the restoration sites. Because the turn-over rate of ant mounds is high e.g., the
ARTICLE IN PRESS Effects of ant mounds on soil heterogeneity half-life of large Formica obscuripes mounds can be 10 years or less (King and Sallee, 1956), the process of ant-mound construction and abandonment results in the creation of open establishment sites within the generally closed canopy of tallgrass prairie. Smallscale disturbances, such as ant mounds and badger mounds, can play a significant role in maintaining species richness and spatial heterogeneity in prairie (Platt, 1975; Gibson, 1989) and may contribute to species diversity in prairie restorations that lack the diversity characteristic of native prairies. Additional research on the pattern of vegetation on- and around active and abandoned mounds is needed to determine the specific effects of ant mounds on vegetation patterns at restoration sites. Ant mounds created the most heterogeneity in soil chemical and physical properties at the 8-year old restoration site. At this site, ant mounds represent significantly enriched nutrient microsites. Such patches of high fertility could have marked effects on plant growth or reproduction (Whitford, 1988; Wagner, 1997) and on the activity and density of soil biota (MacMahon et al., 2000). This enrichment, however, appears to be a transient phenomenon at the restoration sites. At young sites, there are few ant mounds, but they have disproportionately large effects on soil heterogeneity because of significant nutrient enrichment. As the sites become more productive, the relative enrichment of mounds decreases even as the antmound area increases. Thus, ants appear to play a dynamic role at tallgrass prairie restoration sites: creating soil heterogeneity at younger sites and opening up space for plant establishment at older sites. This phenomenon clearly warrants further study because of the importance of creating and maintaining soil and vegetation heterogeneity at restoration sites and in native communities.
Acknowledgements We thank J. Trager for identification of ants. We thank J. Jastrow, C. Whelan, J. Lussenhop, and H. Howe for comments on an earlier version of the manuscript. We thank Fermi National Accelerator Laboratory and the DuPage County Forest Preserve District for access to research sites. This research was supported by an EPA ‘‘STAR’’ fellowship to D. Lane and an NSF Dissertation Improvement Grant to D. Lane and H. BassiriRad.
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365 Betz, R., 1986. One decade of research in prairie restoration at the Fermi National Accelerator Laboratory (FermiLab) Batavia Illinois. In: Clamby, G.K., Pemble, R.H., editors. The Prairie—Past, Present, and Future. Proceedings of the Ninth North American Prairie Conference, Fargo, North Dakota, 29 July–1 August 1984. Tri-College University Center for Environmental Sciences, North Dakota State University, Fargo, pp. 179–185. Blom, P.E., Clark, W.H., Johnson, J.B., 1991. Colony densities of the seed harvesting ant Pogonomyrmex salinus (Hymenoptera: formicidae) in seven plant communities on the Idaho National Engineering Laboratory. J. Idaho Acad. Sci. 27, 28–36. Carlson, S.R., Whitford, W.G., 1991. Ant mound influences on vegetation and soils in a semiarid mountain ecosystem. Am. Midland Nat. 126, 125–139. Collins, S.L., Knapp, A.K., Hartnett, D.C., Briggs, J.M., 1998. The dynamic tallgrass prairie: synthesis and research opportunities. In: Knapp, A.K., Briggs, J.M., Hartnett, D.C., Collins, S.L. (Eds.), Grassland Dynamics: Long-Term Ecological Research in Tallgrass Prairie. Oxford University Press, New York, pp. 193–221. Culver, D.C., Beattie, A.J., 1983. Effects of ant mounds on soil chemistry and vegetation patterns in a Colorado montane meadow. Ecology 64, 485–492. Foster, J., Kettle, W.D., 1999. Distribution of a moundbuilding ant on native and restored prairies in northeastern Kansas. Prairie Nat. 31, 21–31. Gibson, D.J., 1989. Effects of animal disturbance on tallgrass prairie vegetation. Am. Midland Nat. 121, 144–154. Goddard, T.M., 1979. Soil Survey of Kane County. Illinois. United States Department of Agriculture Soil Conservation Service, Washington, DC. Jastrow, J.D., 1987. Changes in soil aggregation associated with tallgrass prairie restoration. Am. J. Bot. 74, 1656–1664. Jastrow, J.D., 1996. Soil aggregate formation and the accrual of particulate and mineral-associated organic matter. Soil Biol. Biochem. 28, 665–676. Kelly, R.H., Burke, I.C., Lauenroth, W.K., 1996. Soil organic matter and nutrient availability responses to reduced plant inputs in shortgrass steppe. Ecol. 77, 2516–2527. King, R.L., Sallee, R.M., 1956. On the half-life of nests of Formica obscuripes Forel. Proc. Iowa Acad. Sci. 63, 721–723. Lane, D. R., 2002. Changes in carbon and nitrogen cycling across a twenty six-year chronosequence of prairie restoration. Ph.D., University of Illinois at Chicago, Chicago. Laundre´, J., 1990. Soil moisture patterns below mounds of harvester ants. J. Range Manag. 43, 10–12. MacMahon, J.A., Mull, J.F., Crist, T.O., 2000. Harvester ants (Pogonomyrmex spp. ): their community and ecosystem influences. Ann. Rev. Ecol. Syst. 31, 265–291. Mapes, D.R., 1979. Soil survey of Du Page and part of Cook Counties, Illinois. United States Department
ARTICLE IN PRESS 366 of Agriculture Soil Conservation Service, Washington, DC. MathSoft, 1997. S-PLUS 4 Guide to Statistics. Data Analysis Products Division, MathSoft, Seattle. Petal, J., Nowak, E., Jakubezyk, H., Czerwinski, Z., 1977. Effect of ants and earthworms on soil habitat modification. Ecol. Bull. 25, 501–503. Petersen, C.E., Zwolfer, K., Frandkin, J., 1998. Ant fauna of reconstructed tallgrass prairie in northeastern Illinois. Trans. Illinois State Acad. Sci. 91, 85–90. Platt, W.J., 1975. The colonization and formation of equilibrium plant species associations on badger disturbances in a tallgrass prairie. Ecol. Monogr. 45, 285–305. Robertson, G.P., Sollins, P., Ellis, B.G., Lajtha, K., 1999. Exchangeable ions, pH, and cation exchange capacity. In: Robertson, G.P., Coleman, D.C., Bledsoe, C.S., Sollins, P. (Eds.), Standard Soil Methods for Long-Term Ecological Research. Oxford University Press, New York, pp. 106–114. Rogers, L.E., Lavigne, R.J., 1974. Environmental effects of western harvester ants on the shortgrass plains ecosystem. Environ. Entomol. 3, 994–997.
D.R. Lane, H. BassiriRad Sluis, W.J., 2002. Patterns of species richness and composition in recreated grassland. Restor. Ecol. 10, 677–684. Trager, J.A., 1990. Restored prairies colonized by native prairie ants (Missouri, Illinois). Restor. and Manage. Notes 8, 104–105. Trager, J. C., 1998. An introduction to ants (Formicidae) of the tallgrass prairie. In: Missouri Prairie J. Jamestown, ND, pp. 4–8. Northern Prairie Wildlife Research Center Home Page. http://www.npwrc.usgs.gov/resource/1999/ants/ants.htm. Wagner, D., 1997. The influence of ant nests on Acacia seed production, herbivory and soil nutrients. J. Ecol. 85, 83–93. Wagner, D., Jones, J., Gordon, D., 2004. Development of harvester ant colonies alters soil chemistry. Soil Biol. Biochem. 36, 797–804. Whitford, W.G., 1988. Effects of harvester ant (Pogonomyrmex rugosus) nests on soils and a spring annual, Erodium texanum. Southwest. Nat. 33, 482–485. Whitford, W.G., DiMarco, R., 1995. Variability in soils and vegetation associated with harvester ant (Pogonomyrmex rugosus) nests on a Chihuahuan Desert watershed. Biol. Fertil. Soils 20, 169–173.
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Diminishing effects of ant mounds on soil heterogeneity across a chronosequence of prairie restoration sites Diana R. Lane, Hormoz BassiriRad Department of Biological Sciences, University of Illinois at Chicago, Chicago, IL 60607-7060, USA Received 15 March 2005; accepted 2 April 2005
KEYWORDS Ant mounds; Nitrogen cycling; Grassland; Restoration; Soil heterogeneity
Summary It is well recognized that mound-building ants affect soil and vegetation heterogeneity, yet little is known about the extent to which such changes are propagated through time. We compared soil properties from ant mounds (built by Formica montana and Acanthamyops claviger) and from adjacent prairie soils at three tallgrass prairie restoration sites in the Midwestern United States, ranging in age from 8 to 26 years post-restoration of native species on former row-crop agriculture plots. We were particularly interested in N-dynamics on and off the mounds. All of the soil variables measured showed the greatest difference between mound and prairie soils at the 8year old site. At that site, we found that ant mounds had significantly higher concentrations of total N, dissolved organic N, and NH+4 compared to prairie soil. Differences in concentrations of these nitrogen pools between mound and prairie soils were, however, lost with increasing time since restoration. The lack of N-enrichment at the older sites suggests that nutrient enrichment of ant mounds may be a transient phenomenon in certain ecosystems. To our knowledge, this is the first report that illustrates a critical, but a temporally dynamic role of ant mounds in creating resource heterogeneity in a restoration project. & 2005 Elsevier GmbH. All rights reserved.
Introduction Mound-building ants play a significant role in creating and maintaining soil heterogeneity in North American grassland ecosystems (Culver and
Beattie, 1983; Gibson, 1989; Carlson and Whitford, 1991; Wagner et al., 2004). Physical soil properties, including soil texture, bulk density, soil temperature, and soil moisture, are often different within ant mounds compared to surrounding soil (Rogers
Corresponding author. Stratus Consulting, P.O. Box 4059, Boulder, CO. 80306-4059, USA. Tel.: 01 303 381 8000; fax: 01 303 381 8200.
E-mail addresses: [email protected] (D.R. Lane), [email protected] (H. BassiriRad). 0031-4056/$ - see front matter & 2005 Elsevier GmbH. All rights reserved. doi:10.1016/j.pedobi.2005.04.003
ARTICLE IN PRESS 360 and Lavigne, 1974; Laundre´, 1990; Carlson and Whitford, 1991; Wagner, 1997; Wagner et al., 2004). Mound soils can also be enriched in macroand micro-nutrients and have higher nitrogen mineralization rates compared to surrounding soils (Baxter and Hole, 1967; Petal et al., 1977; Culver and Beattie, 1983; Kelly et al., 1996; Wagner, 1997; MacMahon et al., 2000). Ants in tallgrass prairie have indirect effects on vegetation and soils through excavation of mounds and incorporation of organic material into their nests, in contrast to the seed-harvesting ants in arid- and semi-arid habitats (e.g., Pogonomyrmex spp.), which consume seeds and clear large ‘‘disks’’ of vegetation around the mound (MacMahon et al., 2000). The documented importance of ants in ecosystem functioning suggests that ants could play a significant role in creating and maintaining heterogeneity in soil fertility during the process of habitat restoration. In the Midwest region of the United States, where less than 1% of tallgrass prairie remains intact, restoration of tallgrass prairie grasslands has been undertaken on former rowcrop agricultural sites where soils have been homogenized through decades of cultivation. The need to increase soil heterogeneity at these sites has been recognized, but many suggested techniques for soil modification are not appropriate for use in large areas (Collins et al., 1998). Although the presence of native prairie ants at tallgrass prairie restoration sites has been noted (Trager, 1990; Petersen et al., 1998), there have been no attempts to evaluate successional changes in the spatial extent and functional consequences of ant activity at restoration sites or in unmanaged native plant communities. We tested the hypothesis that mound-building ants at restoration sites increase soil heterogeneity through the creation of ant mounds with distinct physical and/or chemical properties compared to surrounding soils. We used a 26-year chronosequence of tallgrass prairie restoration sites at Fermi National Accelerator Laboratory (FermiLab) outside of Chicago, IL, USA to test this hypothesis.
Materials and methods Study site This study took place at a chronosequence of tallgrass prairie restoration sites at Fermi National Accelerator Laboratory (FermiLab), approximately 48 km west of Chicago, IL, USA (Jastrow, 1987, 1996). Restoration of tallgrass prairie began in 1975
D.R. Lane, H. BassiriRad using sites which had been converted from native prairie to row-crop agriculture in the mid-1800s (R. Lootens, 2001, personal communication). The first restoration site was planted in 1975 with over 70 plant species collected from nearby prairie remnants (Betz, 1986). In subsequent years, sites were planted with seeds harvested from this and later sites. Seeding rates were similar in all sites, but exact records of the seed mixes were not kept (Sluis, 2002). This study was part of a larger evaluation of changes in soils and vegetation properties across the FermiLab chronosequence (Lane, 2002). Seven sites were included in the study: five restoration sites planted in 1975, 1985, 1993, 1997, and 2000; an old-field that was taken out of cultivation in 1994; and a prairie remnant located 6 km north of FermiLab (West Chicago Prairie). These sites are referred to by their age in 2001 when sampling took place (i.e., the site planted in 1975 is the 26-year old site). The 8-, 16-, and 26-year old sites were selected for more intensive sampling of ant-mound characteristics to determine if the degree of alteration of soil properties for ant mounds varied with time since restoration. Vegetation studies at FermiLab have demonstrated that succession proceeds rapidly, resulting in climax C4 prairie grasses dominating net primary productivity after approximately eight growing seasons (Jastrow, 1987; Lane, 2002. To the greatest extent possible, study sites were selected that had similar soils and similar fire histories. Because we were sampling sites that had already been created, exact matches of conditions were not possible. All seven study sites were located on silt loam soils, although the official soil classifications differed slightly. The four youngest restoration sites and the old-field were located on Barrington silt loam, while the oldest restoration site was mostly on Wauconda silt loam with some small areas of Drummer silty clay loam. The prairie remnant was located on Mundelein silt loam (Goddard, 1979; Mapes, 1979). The restored sites had been burned on a 2-year rotation since 1992, with the most recent burn before sampling being April 2000. West Chicago also is burned on a 2-year rotation, with the most recent burn before sampling being November 1999. The old-field and 1year old site have never been burned. Because the design of the study compares ant mound soil to bulk soil within a site, any differences in soil type or fire history across sites are unlikely to affect the within-site comparisons. Two mound-building ant species were found at the sites in this study. Formica montana Emery is a predatory ant and has its greatest abundance in
ARTICLE IN PRESS Effects of ant mounds on soil heterogeneity tallgrass prairies. Acanthomyops claviger Roger harvests ‘‘honeydew’’ from root-feeding aphids which are tended in their nests (Trager, 1998).
Mound characteristics For all seven study sites, the density of mounds in July 2001 was determined by counting mounds and dividing by the area of the sampling plot (9 m 13.5 m). The basal area of each ant mound was determined using the following formula for an ellipse (Baxter and Hole, 1967): Basal area ¼ pR1 R2 where R1 and R2 were the short and long perpendicular radii measured on the mound. Total ant mound area was divided by plot area (121.5 m2) to obtain the relative basal area of ant mounds at each site. Soil was sampled from three active ant mounds at each of the 8-, 16-, and 26-year old sites on November 16, 2001. Mounds were chosen randomly from among all the active mounds mapped in the 9 m 13.5 m sampling plot in July 2001. Active mounds had ants present or clear evidence of recent ant activity. Within a site, mounds sampled were separated by an average of 6.5 m, with a range of 3–8.7 m. The mound sample (5 cm diameter 15 cm deep) was collected 20 cm from the mound edge following the short radius of the mound (R1); the prairie, or ‘‘off-mound,’’ sample was collected on the short radius and in the opposite direction 20 cm away from the mound edge. Soil samples were transported to the laboratory on ice and weighed to determine bulk density. Cores were collected with a fixed-sleeve-type corer (AMS core sampler, American Falls, ID, USA). Soil cores were sieved through a 4 mm sieve and root fragments larger than 2 mm were picked out by hand. A 20 g sub-sample was dried at 105 1C and used for moisture determination. A 10 g soil subsample was extracted with 100 mL of 1 M KCl (Robertson et al., 1999) and a sub-sample analyzed for NO 3 and NH4 þ; a second aliquot was digested with a perchlorate digestion and analyzed for total dissolved N (both analyses: AlpKem autoanalyzer, Model 300, Clackamas, OR; Kansas State University Soil Testing Laboratory, Manhattan, KS, USA). Dissolved organic N (DON) was calculated as total dissolved N minus inorganic N. Soil texture (percent sand, silt, clay) was determined using the hydrometer method on a 50 g sub-sample of air-dried soil at the Kansas State University Soil Testing Laboratory. Total N and C were measured using flash combustion followed by gas chromatography (Fisons NA 2500, Carlo-Erba
361 Instruments Inc., Milan, Italy). As no carbonates were present in the sample, total C is equivalent to organic C. Linear regression analysis was used to determine whether there was a significant change in antmound area or density with increasing restoration age. The old field and native prairie sites were excluded from regressions because no restoration age can be assigned to these plots. Enrichment of mound soils was calculated as the difference between mound and prairie soil properties for each set of paired samples (N ¼ 3 pairs per site). A one-way analysis of variance was used to determine if there were significant differences across sites in the enrichment of mound soil for a set of soil properties. For variables with a significant F-test (Po0:05), Tukey’s honest significant different (HSD) test was used for post-hoc comparisons of site means. In addition to evaluating significant differences in mound enrichment across sites, we also analyzed the data for significant differences between mound versus prairie samples within each site. Means and standard errors for soil properties were calculated for the three mound and prairie replicate samples at the 8-, 16- and 26-year old sites. Within each site, a paired t-test was used to determine significant differences between mound versus prairie samples. Because three t-tests were conducted for each variable, a Bonferroni correction was applied so that differences were considered to be significant at the Po0:017 level (a ¼ 0:05=3). This correction minimizes the risk of a Type I error, but increases the risk of a Type II error. To address this issue, differences that were significant at a level of 0:017oPo0:05 were regarded as marginally significant. All analyses were conducted using S-plus 4.5 (MathSoft, 1997).
Results Total basal area of ant mounds increased significantly (from 0.25% to 1% of ground area) with increasing time since restoration (Fig. 1). At the native prairie, however, ant mounds covered only 0.02% of ground area. During the first 16 years following restoration, there was an increase in the area per mound with increasing time since restoration, but no significant increase in the density of ant mounds (r 2 ¼ 0:06, F 1;2 ¼ 0:14, P ¼ 0:75) (Fig. 1, Table 1). Between 16 and 26 years of restoration, however, the density of mounds increased sharply from 165 to 905 ha1 while the average size of mounds declined from 0.42 to 0.12 m2 (Table 1).
ARTICLE IN PRESS 362
D.R. Lane, H. BassiriRad
Old field 1.0
Chronosequence
% Total area with ant mounds
Native prairie 0.8
0.6 2 r = 0.97, p = 0.002
0.4
0.2
0.0
0
10
20
30
Site age (years)
Figure 1. Increase in relative basal area of ant mounds with increasing restoration age across a chronosequence of tallgrass prairie restoration sites at FermiLab outside of Chicago, IL, USA. An old field and native prairie are shown for comparison but not included in the regression because no restoration age is associated with these sites. Linear regression is as follows: Area (%) ¼ 0.035*Age+0.13, F 1;3 ¼ 91:1, r 2 ¼ 0:97, P ¼ 0:002.
Table 1. Ant mound density and mean area of mounds for a prairie restoration chronosequence, an old field, and a remnant prairie site Site
Mound density (No. ha1)
Area per mound (m2)
Old field 1-year 4-year 8-year 16-year 26-year Remnant prairiea
412 247 165 329 165 905 82
0.07 0.10 0.13 0.10 0.42 0.12 0.02
a
(0.03) (0.03) (0.12) (0.07) (0.29) (0.04)
Only one ant mound was found at the remnant prairie.
Inorganic N in these soils was largely present as NH+4; on average, inorganic N was 87% NH+4 and 13% + NO 3 for bulk soil and 75% NH4 and 25% NO3 for antmound soil. DON was a substantial portion of the extractable N at these sites; on average, total dissolved N was 59% inorganic N and 41% DON for bulk soil and 61% inorganic N and 39% DON for antmound soil. For six of seven measured soil properties (only excluding DON), the percentage difference between mound and prairie soil was highest at the 8-year-old site compared to the 16- or 26-year old
site (Figs. 2 and 3). Enrichment of ant mounds was significantly greater at the 8-year old site compared to the 16-year old site for soil moisture, inorganic N, total dissolved N, and total C (Tukey’s HSD test, Po0:05; results not shown). Enrichment of ant mounds was significantly greater at the 8year old site compared to the 26-year old site only for soil moisture, because of greater variability at the 26-year-old site. Within the 8-year-old site, there were significant differences between mound and prairie soil samples for total C (P ¼ 0:009), NH+4 (P ¼ 0:016), and DON (P ¼ 0:009). In addition, there were marginally significant differences between mound and prairie soil samples for bulk density (P ¼ 0:02), soil moisture (P ¼ 0:04), and total N (P ¼ 0:019). These differences were noted as marginally significant because the p-value fell between the Bonferroni corrected significance level (Po0:017) and a standard 95% confidence level (Po0:05). In contrast, within the 16-year old site, there was a significant difference between mound and prairie soil samples only for bulk density (P ¼ 0:0003), and a marginally significant difference only for DON (P ¼ 0:048). Within the 26-year old site, there were no significant differences between mound and prairie soil samples (P40:05 for all variables). There were no significant effects of ant mounds on percent sand, silt, or clay at any of the three sites (results not shown).
ARTICLE IN PRESS Effects of ant mounds on soil heterogeneity 8 yr. old
363 16 yr. old
26 yr. old
Bulk density (g cm-3)
1.0
p < 0.05
**
*
** p < 0.001
0.5 -46% -62%
-44%
On-mound Off-mound
0.0 30 31% -0.8%
20
2.1%
10
Total C (%)
Soil moisture (%)
p < 0.017
4
80%
9.4%
* 2
-7.9%
0
Figure 2. Soil physical properties at tallgrass prairie restoration sites of three different ages. Bars represents means71 std. err, n ¼ 3 samples per site. Percentage values within bars indicate the average difference between the paired mound and prairie samples. 8 yr. old
On-mound Off-mound
26 yr. old p < 0.05 * p < 0.017
3
+
NH4 (µg g-1)
-
NO3 (µg g-1)
6
16 yr. old
800%
170%
0 10 5 250%
*
Total N(%)
0
Diss. Org. N (µg g-1)
160%
29%
28%
-4. 2%
-9.5%
323%
104%
0.4 0.2 0.0
22%
8 * 4 213% 0
Figure 3. Soil nitrogen status at tallgrass prairie restoration sites of three different ages. See Fig. 2 for details.
Discussion Measurements of ant-mound basal area and antmound soil quality presented opposing trends over time: while the surface area covered with ant
mounds increased with increasing restoration age, the relative enrichment of ant mounds decreased. Several different lines of evidence all supported two central conclusions, (1) ant mounds were highly distinct from prairie soils at the 8-year old site, (2) these differences were transient and did not persist at the 16- and 26-year old sites. First, six of seven soil variables measured showed the greatest percentage difference between mound and prairie soils at the 8-year-old site (Figs. 2 and 3). Second, results from an ANOVA demonstrated that the relative enrichment of ant mounds at the 8-year old site for soil moisture, inorganic N, total dissolved N, and total C was significantly greater than at the 16-year old site. Third, paired t-tests demonstrated that total N, DON, NHþ 4 , and total C were significantly higher for mound versus prairie soil at the 8-year old site, but none of the soil measures were significantly different for mound versus prairie soil at the 26-year old site. These effects in tallgrass prairie are distinct from the pattern seen with harvester ants (Pogonomyrmex barbatus) in desert environments, where nutrient concentrations increase with colony age compared to surrounding soils (Wagner et al., 2004). Our results suggest that nutrient enrichment can be a transitory property of ant mounds in tallgrass prairie. Carlson and Whitford (1991) had noted that ‘‘nutrient enrichment of mounds y appears ubiquitous among mound-building ants’’; but these results suggest that ant mounds in restored tallgrass prairie do not fit into their paradigm.
ARTICLE IN PRESS 364 Comparisons of the 8- and 26-year old sites suggest that the lack of differentiation between mound and prairie soils at the 26-year-old site is likely a function of changing conditions in the prairie soil. For example, the total N content of ant mounds was identical at the 8- and 26-year-old sites (0.28%), but the prairie soil had a higher N content at the 26-year old site compared to the 8year old site (0.31% versus 0.23%). Thus, the enrichment of ant mounds over time did not keep pace with the increase in total N of the prairie soil following 26 years of restoration. Because the surface of an active ant mound lacks plant cover, the ant mound loses the continual input of root and leaf litter that occurs on vegetated soil. If the active incorporation of organic matter by ants into the ant nest is equal to or less than the organic input that would occur in the absence of ants, then we would expect that there would be no relative enrichment of soil on ant mounds. This hypothesis is consistent with other reports (Carlson and Whitford, 1991; Whitford and DiMarco, 1995) that have compared several sites and concluded that the degree of enrichment of ant mounds is negatively correlated with the productivity of the surrounding area. Another possibility is that the boundaries of an ant-mound might become more diffuse over time, so that a sample taken 20 cm away from a mound edge at the 26-year old site includes a diffuse antmound signal, while an off-mound sample at the 8-year-old site does not include an ant-mound signal. We took our ‘‘off-mound’’ sample relatively close to the edge of the mound (20 cm), because we were interested in examining whether ant mounds represented significantly enriched discrete microsites. Our observation of a lack of differentiation at the 26-year old site between the discrete antmound area (the visible boundaries of the ant mound) and the nearby off-mound area still holds true, whether or not the mechanism results either from a relatively lower enrichment of ant-mound soil or from increasing enrichment of surrounding areas. Changes in bulk density over time paralleled the changes in total N content. In particular, data from intermediate age plots indicated that most of the observed age-dependent convergence between ant mounds and the surrounding soil had already occurred within the first 16 years of restoration. Ant mounds at the 16-year old site had significantly lower bulk density than prairie soil, but the relative difference between mound and prairie soil at the 16-year old site was smaller than at the 8-year old site because bulk density in prairie soil had decreased with increasing restoration age.
D.R. Lane, H. BassiriRad We realize that small sample sizes in this study (three mounds per age) require a cautious approach to generalizing our results. Because of this small sample size, our mean values may not reflect true within-site means. Sampling mounds at additional sites and increasing the number of mounds sampled would help to confirm the trends noted here. The use of multiple lines of evidence and the fact that we found significant differences between mound and prairie soils at the 8-year old site at the P ¼ 0:017 level suggests that these results are quite robust despite limited statistical power. Furthermore, the trend of increasing similarity between mound and prairie soils with increasing time since restoration was consistent across almost all of the physical and chemical properties measured. This study is the first report of ant colonization increasing dramatically in response to tallgrass prairie restoration. There was a significant increase in ant-mound area across the chronosequence, but no consistent change in ant-mound size or density. The estimate of relative basal area for ant mounds at the 26-year old restoration site (1.0%) was lower than the relative area for Formica cinerea mounds at a Wisconsin prairie (1.7%) (Baxter and Hole, 1967) but much higher than the relative area of ant mounds at the remnant prairie site in this study (0.02%). There are few other published estimates of the relative area of ant mounds in tallgrass prairie, so it is difficult to determine whether ant mound colonization at the restored sites has recovered to values appropriate for similar prairie types and soils. Low ant mound area at the remnant prairie site in this study (which is poorly drained) is likely to be an underestimate for a welldrained prairie (Blom et al., 1991). The increase in ant mound area with increasing restoration age found in this study contrasts with the results of Foster and Kettle (1999) who found that the mound-building ant Formica subsericea was common on unplowed prairie in Kansas but almost absent in nearby restored prairies. They found 113–122 mounds per hectare in the remnant prairie, and fewer than 4 mounds per hectare in restored prairie. Further study is needed to determine if different patterns of ant colonization in restored prairies are a function of soil characteristics or of the particular species of ant that is present.
Implications for Soil and Vegetation Heterogeneity The physical presence of ant mounds as areas free from vegetation creates significant spatial heterogeneity within the restoration sites. Because the turn-over rate of ant mounds is high e.g., the
ARTICLE IN PRESS Effects of ant mounds on soil heterogeneity half-life of large Formica obscuripes mounds can be 10 years or less (King and Sallee, 1956), the process of ant-mound construction and abandonment results in the creation of open establishment sites within the generally closed canopy of tallgrass prairie. Smallscale disturbances, such as ant mounds and badger mounds, can play a significant role in maintaining species richness and spatial heterogeneity in prairie (Platt, 1975; Gibson, 1989) and may contribute to species diversity in prairie restorations that lack the diversity characteristic of native prairies. Additional research on the pattern of vegetation on- and around active and abandoned mounds is needed to determine the specific effects of ant mounds on vegetation patterns at restoration sites. Ant mounds created the most heterogeneity in soil chemical and physical properties at the 8-year old restoration site. At this site, ant mounds represent significantly enriched nutrient microsites. Such patches of high fertility could have marked effects on plant growth or reproduction (Whitford, 1988; Wagner, 1997) and on the activity and density of soil biota (MacMahon et al., 2000). This enrichment, however, appears to be a transient phenomenon at the restoration sites. At young sites, there are few ant mounds, but they have disproportionately large effects on soil heterogeneity because of significant nutrient enrichment. As the sites become more productive, the relative enrichment of mounds decreases even as the antmound area increases. Thus, ants appear to play a dynamic role at tallgrass prairie restoration sites: creating soil heterogeneity at younger sites and opening up space for plant establishment at older sites. This phenomenon clearly warrants further study because of the importance of creating and maintaining soil and vegetation heterogeneity at restoration sites and in native communities.
Acknowledgements We thank J. Trager for identification of ants. We thank J. Jastrow, C. Whelan, J. Lussenhop, and H. Howe for comments on an earlier version of the manuscript. We thank Fermi National Accelerator Laboratory and the DuPage County Forest Preserve District for access to research sites. This research was supported by an EPA ‘‘STAR’’ fellowship to D. Lane and an NSF Dissertation Improvement Grant to D. Lane and H. BassiriRad.
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