Correspondence: Laura G. Perry, 420 North Sherwood Street, Fort Collins, CO 80521, USA (e-mail email@example.com).
1Invasive plants pose a major threat to native plant communities around the globe. Current methods of controlling invasive vegetation focus on eradication of existing populations, and are often effective only in the short term. Manipulating resource availability to give native species a competitive advantage over invasive species could reduce ecosystem vulnerability to invasion and might more effectively control invasive vegetation. We evaluated this approach for controlling invasions of sedge meadow communities by Phalaris arundinacea, a widespread invasive grass in North American wetlands.
2To test whether lowering nitrogen (N) availability would allow a wetland sedge, Carex hystericina, to suppress Phalaris competitively, we examined Carex and Phalaris competition under a range of inorganic N concentrations (25–400 mg kg−1) in a glasshouse. We lowered N availability in wetland soil using carbon enrichment and repeated harvests of a cover crop, and then created a N gradient by applying NH4-N to the N-depleted soil.
3In soil without carbon added, competition with Phalaris reduced Carex biomass by 91%, while competition with Carex did not influence Phalaris, as is commonly observed in sedge meadows. Phalaris biomass was five times Carex biomass in mixed stands. Conversely, in soil depleted of available N via carbon enrichment, competition with Carex reduced Phalaris biomass by 82%, while competition with Phalaris reduced Carex biomass by only 32%, indicating that Carex is the superior competitor for N. Carex biomass was six times Phalaris biomass in mixed stands in the carbon-enriched soil.
4Carbon enrichment lowered soil inorganic N by 10–30 mg kg−1. NH4-N addition mitigated the negative effects of carbon on Phalaris growth and competitive ability, indicating that carbon enrichment altered competitive outcomes by lowering N availability. Greater Carex N uptake efficiency under N-poor conditions appeared to account for the Carex competitive ability for N.
5Synthesis and applications. Carex dominance in carbon-enriched soil strongly suggests that lowering soil inorganic N to < 30 mg kg−1 in restored wetlands would allow establishing sedge meadow communities to suppress Phalaris invasions. Low-N soils might be achieved via carbon enrichment, vegetation harvests and reduced N inputs. Reducing community vulnerability to invasion by manipulating resource availability appears to be a promising approach to invasive species management.
Invasive species present a major challenge to ecological conservation (Mooney & Drake 1986; Di Castri, Hansen & Debussche 1990; Williamson 1996). Most current methods for suppressing invasions are focused on the removal of established populations and are often inadequate to prevent invasions over the long term. Managing ecosystems to reduce their vulnerability to invasion may be a more effective strategy for invasive species control (Hobbs & Humphries 1995). One such approach would be to manipulate resource availability in ecosystems vulnerable to invasion so that native plant species could competitively suppress invasive species. We explored the potential effectiveness of such an approach for suppressing Phalaris arundinacea L. (reed canarygrass), an invasive perennial grass, in restored prairie pothole wetlands.
Current methods to control Phalaris invasions are aimed at eradication of extant populations and are effective only in the short term. Phalaris stands can be removed using herbicide applications in combination with burning or disking over several years (Preuninger & Umbanhowar 1994; Solecki 1997), but following these treatments Phalaris populations quickly re-establish from seed bank reserves (Preuninger & Umbanhowar 1994). Because Phalaris is prevalent in the landscape, propagules for future invasions are readily available. Repeating control measures indefinitely to address recurring Phalaris invasions is not only expensive but also interferes with native plant community establishment.
If N enrichment is responsible for Phalaris invasions in sedge meadow communities, then Phalaris invasions might be competitively suppressed if N availability in prairie potholes is reduced. Of the few attempts that have been made to control invasive species by lowering N availability in N-enriched ecosystems, many have been at least partly successful (Wheeler & Shaw 1991; Koerselman & Verhoeven 1995; Zinc & Allen 1998; Morghan & Seastedt 1999; Pashke, McLendon & Redente 2000; Maron & Jeffries 2001). However, to our knowledge no studies have examined explicitly the role of competitive suppression as a mechanism of invasive species control under N-poor conditions.
To determine whether sedge meadow species can competitively suppress Phalaris when N availability is low, we examined competition between Phalaris and a common sedge meadow species, Carex hystericina Muhl. (porcupine sedge), in a glasshouse under a range of inorganic N concentrations, including low N availability (25 mg kg−1 inorganic N). Our specific objectives were to (i) examine the effects of N availability on the outcome of competition between Carex and Phalaris, and (ii) evaluate whether lowering N availability in restored sedge meadow wetlands might be an effective strategy for suppressing Phalaris invasion.
Competition between Carex and Phalaris was evaluated in a glasshouse under an array of soil N conditions. Wetland soil was depleted of available N by repeated harvests of a forage grass followed by carbon enrichment. Carbon amendments to carbon-limited soils stimulate microbial immobilization of available N (Tisdale, Nelson & Beaton 1985). N-depleted wetland soil without carbon added was used as a control to assess the effects of carbon addition. A range of N addition rates were applied to both the carbon-amended soil and the non-amended soil to create gradients in available N.
A Glencoe clay loam (Cumulic Endoaquoll) soil was collected in November 1998 from a drained wetland in Chanhassen, Minnesota, USA. The soil was homogenized in a soil mixer, steam-sterilized, placed in 132, 13-cm deep, basins in a naturally lit, variable temperature glasshouse, and sown with Lolium perenne var. aristatum Wlld. (annual ryegrass) at a rate of 6 g seed m−2. In five harvests conducted over 1 year, 16 kg (dry weight) of L. perenne above-ground biomass were removed from the basins. Bowman & Paul (1992) reported L. perenne foliar N concentrations of 2·2–4·2%, which suggests that roughly 515 g N were removed in biomass.
In February 2000, the depleted soil was removed from the basins and, to increase the volume of soil, mixed with fresh soil, collected from the same source in November 1999, at a depleted to fresh soil ratio of 4 : 1 by volume. The mixed soil was steam-sterilized, and a portion of it used to fill 44, 47·5 × 35·5 × 13-cm, basins. The remainder was amended with pine sawdust (i.e. carbon, C), at a soil to sawdust ratio of 2 : 1 by volume (9 : 1 by weight) and used to fill another 88 basins. The sawdust was 39·2% C and 0·21% N (University of Minnesota Research Analytical Laboratory, St Paul, MN).
The soil amended with carbon was 6·1% C and 0·31% N, had a pH of 7·7, and contained 13 mg kg−1 P, 107 mg kg−1 SO4-S, 83 mg kg−1 K, 4318 mg kg−1 Ca, 326 mg kg−1 Mg, 37 mg kg−1 Mn, 3·4 mg kg−1 Zn, 1·0 mg kg−1 Cu and 60 mg kg−1 Fe. The non-amended soil was 4·5% C and 0·32% N, had a pH of 7·6, and contained 8 mg kg−1 P, 99 mg kg−1 SO4-S, 90 mg kg−1 K, 4582 mg kg−1 Ca, 363 mg kg−1 Mg, 14 mg kg−1 Mn, 3·2 mg kg−1 Zn, 1·2 mg kg−1 Cu and 70 mg kg−1 Fe (University of Minnesota Research Analytical Laboratory; Dahnke 1988).
The two carbon addition treatments (carbon, no carbon) were combined with four NH4-N addition rates in an incomplete factorial design to yield six soil N treatments. Basins with carbon added were subjected to four NH4-N addition rates: 0·00, 0·025, 0·25 and 1·25 g N week−1 basin−1. Basins without carbon added were subjected to two NH4-N addition rates: 0·00 and 0·25 g N week−1 basin−1. Throughout the text and figures, basins with carbon added are referred to as C-0·00, C-0·025, C-0·25 and C-1·25. Basins without carbon added are referred to as NC-0·00 and NC-0·25.
The six soil N treatments were combined with five competition treatments in a complete factorial design. Carex and Phalaris were each sown in monoculture at densities of 500 and 1000 viable seeds m−2, and in mixture at a density of 500 viable seeds m−2 of each species. Sowing densities were chosen to mimic viable seed densities in natural sedge meadow seed banks (Galatowitsch & Biederman 1998). Seed viability was estimated from tetrazolium analyses of 200 seeds of each species (Grabe 1970). Carex and Phalaris seed were obtained from Prairie Moon Nursery (Winona, MN) and Premium Seed Company Inc. (Shakopee, MN), respectively. Carex seed was surface sterilized for 10 min in 50% bleach, rinsed, and cold-stratified at 4 °C in deionized water for 12 weeks prior to sowing. Phalaris seed was stored dry at 20 °C. To synchronize Carex and Phalaris germination, Carex and Phalaris seed were stored wet on a 14-h 30 °C day, 10-h 20 °C night schedule for 7 days and 2 days prior to sowing, respectively. In response to low germination rates (approximately 50% of the desired densities), both species were resown in all basins in week 4.
Each of the 30 treatments was replicated four times. The experiment was arranged in an incomplete randomized block design on five benches, with benches as blocks. Four of the five competition treatments were included in each of the five blocks, with the excluded treatment for each block chosen at random. This design reduced statistical power to discern effects of competition, but did not reduce power to discern effects of other factors or treatment interactions (Cochran & Cox 1950). Basins were placed in separate bench sections, which were lined with rubber pond-liner and filled with water to a depth of 11 cm, which was level with the soil in the basins. Water flowed into the basins through slits in the basin walls, saturating but not flooding the basin soils. An additional two replicates of each of the six soil N treatments, in which seeds were not sown (hereafter ‘unsown basins’), were included for measurements of soil inorganic N in the absence of plant N uptake.
The experiment began in March 2000 and was maintained for 25 weeks on a 14-h 30 °C day, 10-h 20 °C night schedule. The benches were illuminated to approximately 600 µmol m−2 s−1 by 10 400 Watt high-pressure sodium lamps. Water levels were maintained daily. NH4-N was added weekly in the appropriate amounts to each basin as ammonium sulphate ([NH4]2SO4) in 2·5-l water poured over the soil surface. Initial soil sulphur concentrations were sufficiently high (> 100 mg kg−1) to preclude effects of SO4-S addition. To ensure that N was the limiting nutrient, 17·4 mg kg−1 P was added during soil mixing as superphosphate (8·7% P) to raise potentially available P in soils with and without carbon added above the level (15–20 mg kg−1) at which P affects Phalaris growth (Mallarino et al. 1983). Also, 1·04 g SO4-S, 0·98 g K, 0·40 g Ca, 0·24 g Mg, 2·5 mg Mn, 2·5 mg B, 0·3 mg Zn and 0·1 mg Cu (Hoagland & Arnon 1938) were added to the water around each basin in week 1.
measurements and analysis
Soil inorganic N concentrations in the unsown basins were determined biweekly and in the sown basins were determined in weeks 6, 10, 17 and 24. Four 1·5 × 10-cm cores were collected from each basin and homogenized. Thirty grams of each sample were dried for 120 h in a 65 °C forced-air drying oven and weighed to determine soil moisture. Eight grams of wet soil were shaken in 25 ml of 2 N KCl with a reciprocal shaker for 30 min, after which the KCl extracts were filtered with Sarstedt seraphas® plasma filters (Sarstedt Inc., Newton, NC) and stored at 4 °C (Mulvaney 1996). NH4-N and NO3-N concentrations, corrected for soil moisture, were determined using a two-channel Wescan N Analyser (Wescan Instruments, Inc., Deerfield, IL) (Carlson 1986). Two unsown basins, a C-0·25 and a C-1·25 basin, developed cyanobacteria infestations early in the experiment and exhibited high inorganic N concentrations relative to expected concentrations and to replicate basins. Inorganic N concentrations in these basins were excluded from the means after week 1.
Population densities were determined in week 8 by counting individuals in the centre 0·04 m2 (15 × 25 cm, inside a 10-cm border) of each basin. Carex and Phalaris above-ground and below-ground biomasses were harvested in week 25 from the centre 0·04 m2 of each basin. Biomass samples were separated by species, dried for 48 h in a 65 °C forced-air drying oven and weighed. Root fragments in Carex/Phalaris mixtures that were not identifiable to species were weighed separately and assigned to the two species in proportion to the species’ identified below-ground biomass in each basin.
Above-ground tissue N concentrations were determined from 0·15-g biomass subsamples, finely ground and digested for 1 h at 370 °C in 3·5 ml sulphuric acid with one ST-Auto Kjeldahl Fishertab™ (Fisher Scientific Co., Pittsburgh, PA) (Bremner 1996). N concentrations in digested subsamples were determined using a Wescan N Analyser (Carlson 1978). N content in above-ground biomass (g m−2) was determined by multiplying tissue N concentrations by above-ground biomass.
N use efficiency (Vitousek 1982; Shaver & Melillo 1984; Bridgham et al. 1995) was determined for each species in each basin by dividing above-ground biomass by the N content in above-ground biomass. N uptake efficiency (Bridgham et al. 1995; Shaver & Melillo 1984) was calculated for each species in each basin as the difference between the N content in above-ground biomass in N-fertilized basins and the N content in above-ground biomass in unfertilized basins, divided by the total N added to the basin, following Bock (1984). Subtracting the N content in unfertilized basins corrected for differences in background N availability between basins with and without carbon added. Low N use efficiency indicates either inefficient biomass production per unit N or luxury N consumption (Chapin 1980). Low N uptake efficiency indicates low ability to acquire available N (Bridgham et al. 1995).
Carex and Phalaris mean population densities, total biomass, root : shoot ratios, N use efficiency and N uptake efficiency were compared among blocks, competition treatments, carbon addition treatments and NH4-N addition rates with four-way manovas using SAS statistical software (Anonymous 1990). Soil NH4-N and NO3-N concentrations in sown basins were compared among blocks, species (Carex, Phalaris, Carex/Phalaris), total sowing densities, carbon addition treatments and NH4-N addition rates with five-way anovas, with week of measurement as a repeated-measures factor. Within-subject comparisons (i.e. species comparisons in the manovas and week of measurement comparisons) were performed using the Wilks’ Lambda statistic (Morrison 1976). F statistics for between-subject comparisons were computed using type III sums of squares. When interactions were significant, post-hoc anovas using Bonferroni adjusted α-values were used to identify significant effects within groups. To remove significant heteroscedasticity, total biomass, root : shoot ratios and soil N concentrations were log-transformed, and population densities, N use efficiency and N uptake efficiency were square root-transformed for analysis.
soil inorganic n: unsown basins
Soil inorganic N was almost entirely NH4-N rather than NO3-N in unsown basins (Fig. 1). Carbon addition reduced mean initial (week 1) NH4-N concentrations in unsown basins from 28·05 ± 1·7 to 13·6 ± 2·2 mg kg−1 (anova, F1,5 = 51·96, P < 0·001). NH4-N concentrations remained 10–30 mg kg−1 lower in basins with carbon added than in basins without carbon added (in soils with the same NH4-N addition rate) in nearly every week of the experiment (Fig. 1). NH4-N addition increased NH4-N concentrations in unsown basins over time (Fig. 1). There were no discernible trends in NO3-N concentrations with regard to time, NH4-N addition rate or carbon addition.
soil inorganic n: sown basins
As in unsown basins, soil inorganic N in sown basins was almost entirely NH4-N (Table 1) rather than NO3-N, which rarely exceeded 3·0 mg kg−1 (data not shown). Mean soil NH4-N concentrations in Phalaris monocultures and Carex/Phalaris mixtures were 51% lower in basins without carbon added than in those with carbon added for basins with the same NH4-N addition rate (species × carbon, F2,86 = 5·74, P= 0·005); NH4-N concentrations in Phalaris monocultures and Carex/Phalaris mixtures were particularly low in basins without carbon added in weeks 6 and 10 and particularly high in basins with carbon added in weeks 10, 17 and 24 (Table 1). In basins without carbon added, mean NH4-N concentrations were 65% lower in Pjalaris monocultures and Carex/Phalaris mixtures than in Carex monocultures in week 6 (F2,26 = 28·57, P < 0·001) and 28% lower in week 10 (F2,26 = 18·49, P < 0·001) (species × carbon, F2,86 = 5·74, P = 0·005). Mean NH4-N concentrations were higher in NC-0·25 basins than in NC-0·00 basins in all weeks but week 6 (time × carbon × N, F3,84 = 2·84, P = 0·043). Among basins with carbon added, mean NH4-N concentrations were higher in C-1·25 basins than in basins with lower NH4-N addition rates (F3,86 = 90·11, P < 0·001), particularly in weeks 10, 17 and 24 in Carex monocultures, which appeared to reach a limit to N uptake (time × species × N, F18,238 = 3·11, P < 0·001). NH4-N concentrations did not differ significantly among sown basins with carbon added with lower N addition rates (Tukey HSD, P > 0·05).
Table 1. Mean NH4-N concentrations (mg kg−1) in sown basins in weeks 6, 10, 17 and 24. NH4-N concentrations were log-transformed for analysis. The means and standard errors presented are back-transformed statistics from transformed data. n= 8 for Carex monocultures and Phalaris monocultures; n= 4 for Carex/Phalaris mixtures
Soil N treatment
As expected, population densities in the high-density monocultures (2544 ± 145 m−2) were nearly twice population densities in the low-density monocultures (1327 ± 88 m−2) (F2,50 = 75·44, P < 0·001). Phalaris densities (2028 ± 97 m−2) were also higher than Carex densities (1206 ± 117 m−2) (F1,50 = 90·76, P < 0·001) and mean densities of both species were higher in basins with carbon added (1717 ± 107 m−2) than without carbon added (1417 ± 124 m−2) (F1,50 = 5·81, P= 0·020). Because individual growth rates and rhizomatous reproduction were higher in low-density treatments, however, differences in sowing density appeared to be of limited importance to biomass production. For example, mean total biomass did not differ between high- and low-density monocultures (F1,68 = 0·69, P= 0·410), despite a twofold difference in density. For simplicity, we grouped biomass data for the two monoculture sowing densities in the figures and text.
We examined interspecific competition between Carex and Phalaris by comparing total biomass in Carex/Phalaris mixtures to total biomass in monocultures (Fig. 2). Because the outcomes of competition were different in basins with and without carbon added (species × competition × carbon, F2,50 = 4·40, P= 0·001), we present the biomass results from the two carbon addition treatments separately.
Competition in soil without carbon addition
In basins without carbon addition (Fig. 2), mean Carex biomass was reduced by an order of magnitude, from 2338·6 ± 280·7 to 221·8 ± 56·4 g m−2, by interspecific competition (F2,14 = 58·84, P < 0·001). In contrast with Carex (species × competition, F2,14 = 36·74, P < 0·001), mean Phalaris biomass was not significantly affected by interspecific competition. Mean Phalaris biomass was five times mean Carex biomass in Carex/Phalaris mixtures. NH4-N addition increased mean biomass of both species in basins without carbon added (F1,14 = 125·10, P < 0·001), but resulted in a greater increase in mean Phalaris biomass (419%) than in mean Carex biomass (228%) (species × N, F1,14 = 10·86, P = 0·005).
Competition in soil with carbon addition
In basins with carbon added, interspecific competition reduced both mean Phalaris biomass and mean Carex biomass (F2,32 = 39·26, P < 0·001; Fig. 2). Mean Phalaris biomass was reduced more by interspecific competition when NH4-N addition rates were low (C-0·00 and C-0·025) than when NH4-N addition rates were higher (by 82% compared with 42%) (species × competition × N, F6,32 = 3·47, P = 0·009; competition × N, F6,32 = 3·92, P = 0·005), while NH4-N addition did not significantly alter the influence of interspecific competition on mean Carex biomass (competition × N, F6,32 = 0·81, P = 0·566). Consequently, in C-0·00 and C-0·025 basins, mean Phalaris biomass was reduced significantly more by interspecific competition than was mean Carex biomass (species × competition, F2,14 = 10·74, P = 0·002). In C-0·00 and C-0·025 basins, averaged across competition treatments, mean Phalaris biomass (170·0 ± 24·6 g m−2) was less than one-third mean Carex biomass (617·7 ± 60·6 g m−2) (F1,14 = 131·46, P < 0·001), whereas in C-1·25 basins (species × N, F3,32 = 50·66, P < 0·001) mean Phalaris biomass (5645·6 ± 622·7 g m−2) was three times mean Carex biomass (1882·3 ± 399·7 g m−2) (F1,5 = 29·64, P = 0·003). Carex made up 92% of the biomass in Carex/Phalaris mixtures in C-0·00 and C-0·025 basins, but only 17% of the biomass in Carex/Phalaris mixtures in C-1·25 basins.
Effects of carbon addition
For Phalaris and Carex in monoculture, and for Phalaris in Carex/Phalaris mixtures, mean biomass was greater in basins without carbon added than in basins with carbon added (species × competition × carbon, F2,50 = 4·40, P = 0·001), for basins with the same NH4-N addition rate. For Carex in Carex/Phalaris mixtures, in contrast, mean biomass was 74% lower in basins without carbon added than in basins with carbon added (F1,14 = 8·53, P = 0·017). Carbon addition reduced mean Phalaris biomass more than it reduced mean Carex biomass (species × carbon, F1,50 = 64·81, P < 0·001), even when Carex/Phalaris mixtures were excluded from the analysis (species × carbon, F1,68 = 11·98, P < 0·001). NH4-N addition tempered the negative effect of carbon addition on mean biomass of both species (carbon × N, F1,50 = 46·69, P < 0·001). In the absence of NH4-N addition, mean biomass averaged across species was 73% lower in basins with carbon added than in basins without carbon added; with NH4-N addition (0·25 g week−1 NH4-N), mean biomass was only 36% lower in basins with carbon added than in basins without carbon added.
root : shoot ratio
Mean root : shoot ratios did not differ significantly between species or among competition regimes (Fig. 3). NH4-N addition reduced mean root : shoot ratios, averaged across species, from 1·58 ± 0·11 with no NH4-N addition to 0·21 ± 0·02 with the highest NH4-N addition rate (F3,50 = 154·49, P < 0·001). Both Carex and Phalaris tended to allocate a greater proportion of their biomass to roots in basins with lower NH4-N addition rates (C-0·00, C-0·025 and NC-0·00), and to shoots in basins with higher NH4-N addition rates (C-0·25, C-1·25 and NC-0·25). Carbon addition increased mean root : shoot ratios (F1,50 = 15·72, P < 0·001) for basins with the same NH4-N addition rate. In basins without NH4-N added, carbon addition increased mean root : shoot ratios more for Carex in Carex/Phalaris mixtures than for Carex in monoculture or for Phalaris (species × competition × carbon × N, F2,50 = 5·26, P = 0·009).
n use efficiency
Mean Phalaris N use efficiency (Fig. 4) was higher than mean Carex N use efficiency in most soil N treatments (149·7 ± 6·4 compared with 131·5 ± 5·4 g biomass g N−1) (F1,49 = 44·04, P < 0·001), particularly in basins without carbon added (species × carbon, F1,49 = 23·08, P < 0·001). However, mean Carex N use efficiency was higher than mean Phalaris N use efficiency in C-0·00 basins (155·7 ± 4·6 compared with 134·4 ± 8·1 g biomass g N−1) (species × N, F3,49 = 7·54, P < 0·001) and in C-1·25 Carex/P. arundinacea mixtures (species × competition × N, F6,49 = 4·76, P = 0·001). Mean Carex and Phalaris N use efficiencies were similar in C-0·25 monocultures. For both species, mean N use efficiency was similar among most NH4-N addition rates in basins with carbon added, but decreased by 63% in C-1·25 basins (F3,31 = 68·70, P < 0·001). NH4-N addition also reduced mean N use efficiency in basins without carbon added (F1,14 = 64·92, P < 0·001). Mean N use efficiency was lower in basins without carbon added than in basins with carbon added at the same NH4-N addition rate (F1,49 = 45·29, P < 0·001), particularly for Phalaris (species × carbon, F1,49 = 23·08, P < 0·001) and particularly in basins with no NH4-N addition (carbon × N, F1,49 = 7·94, P = 0·007).
n uptake efficiency
Mean Carex N uptake efficiency (Fig. 5) declined from 91·8 ± 18·9 g g−1 to 36·1 ± 7·3 g g−1 with increasing NH4-N addition rates among basins with carbon added (F2,22 = 7·17, P = 0·004). In contrast (species × N, F2,31 = 44·95, P < 0·001), mean Phalaris N uptake efficiency increased from 4·8 ± 3·0 to 91·4 ± 11·9 g g−1 with increasing NH4-N addition rates among basins with carbon added (F2,23 = 40·82, P < 0·001). Mean Carex N uptake efficiency was greater than mean Phalaris N uptake efficiency in C-0·025 basins (F1,4 = 115·06, P < 0·001), whereas mean Phalaris N uptake efficiency was greater than mean Carex N uptake efficiency in C-1·25 basins (F1,5 = 9·85, P = 0·026). Mean Phalaris N uptake efficiency was also greater than mean Carex N uptake efficiency in basins without carbon added (NC-0·25) (F1,5 = 17·52, P = 0·009). Mean N uptake efficiency of both species was lower in Carex/Phalaris mixtures than in monoculture (F2,31 = 13·11, P < 0·001), but mean Carex N uptake efficiency was reduced more than mean Phalaris N uptake efficiency by competition (species × competition, F2,31 = 6·77, P = 0·004).
Our results demonstrate that in carbon-enriched soil with low N availability (< 30 mg kg−1 inorganic N), C. hystericina, a native sedge, competitively suppresses P. arundinacea establishment (Fig. 2). Conversely, in soil without carbon added, P. arundinacea competitively suppresses C. hystericina establishment (Fig. 2), as has often been observed in restored prairie pothole wetlands (Budelsky & Galatowitsch 2000; Green & Galatowitsch 2002). NH4-N addition reversed the outcome of competition in carbon-enriched soil, and substantially reduced the negative effects of carbon addition on Phalaris and Carex biomass in monoculture (Fig. 2), strongly suggesting that N was limiting in carbon-enriched soil and that lowered soil inorganic N (by 10–30 mg kg−1; Fig. 1) accounted for the effects of carbon enrichment on competition. To our knowledge, this study is the first to identify environmental conditions under which native sedge meadow vegetation can achieve dominance over Phalaris.
Carex dominance over Phalaris in carbon-enriched soil suggests that Carex is the superior competitor for N (sensuTilman 1982), contradicting the assertion that Phalaris is an inherently superior competitor to sedge meadow species under all environmental conditions (Wetzel & van der Valk 1998). Other studies have suggested that Phalaris is a superior competitor to sedge meadow species under both N-rich and N-poor conditions (Wetzel & van der Valk 1998; Green & Galatowitsch 2001, 2002), as one might conclude from the NC-0·00 and NC-0·25 Carex/Phalaris mixtures in the present study (Fig. 2). At inorganic N concentrations higher than 30 mg kg−1, competition between Carex and Phalaris may often be for some resource other than N. Both Carex and Phalaris allocated substantially more biomass to shoot material in response to higher NH4-N addition rates (Fig. 3), suggesting that at higher inorganic N concentrations competition may have been for light.
mechanisms ofcarexsuperior competitive ability for n
Greater Carex N uptake under N-poor conditions appears to best explain Carex dominance under N-poor conditions. Mean Carex N uptake efficiency was nearly 20 times greater than mean Phalaris N uptake efficiency in C-0·025 basins (Fig. 5). Greater N use efficiency may account in part for the greater Carex biomass in C-0·00 basins, but cannot account for Carex dominance in C-0·025 basins because mean Phalaris N use efficiency was greater than mean Carex N use efficiency in C-0·025 basins (Fig. 4). Greater allocation to root material is probably not the mechanism of greater Carex N uptake efficiency under N-poor conditions because Carex and Phalaris root : shoot ratios were similar under almost all experimental conditions (Fig. 3). Instead, greater N absorption capacity (Chapin 1980) of Carex roots probably accounts for the greater Carex N uptake efficiency.
explanation forcarexrelative success in high-n, carbon-enriched soil
The relatively small effect of Phalaris on Carex biomass in C-0·25 and C-1·25 basins, compared with that in basins without carbon added (Fig. 2), suggests that the low initial N availability (Fig. 1) in carbon-enriched basins may have had a lasting effect on Carex and Phalaris competitive ability. Slow initial Phalaris growth in carbon-enriched basins allowed Carex to establish concurrently with Phalaris rather than beneath an established Phalaris canopy (L. Perry, personal observation), which may have prevented Phalaris from completely suppressing Carex establishment once N availability increased in C-0·25 and C-1·25 basins (Fig. 1). It is possible that Carex establishment in C-0·25 and C-1·25 basins reflects some effect of carbon enrichment, other than lowered N availability, that reduced Phalaris competitive ability. However, the fact that NH4-N addition removed the negative effects of carbon addition on Phalaris biomass (Fig. 2) strongly suggests that the effects of carbon enrichment were mediated by lowered N availability.
soil n processes
As is probably often the case at the water's edge in natural prairie pothole wetlands (Neely & Baker 1989), daily soil surface saturation and dry-down cycles in the basins probably led to good conditions for nitrification and subsequent denitrification, leading to the near absence of NO3-N. The abundance of soil NH4-N, particularly in C-1·25 basins (Table 1 and Fig. 1), however, suggests that nitrification was limited, perhaps as in natural wetlands (Brinson, Bradshaw & Kane 1984; Neely & Baker 1989), by anaerobic conditions in the mainly saturated soils. Although carbon addition reduced soil NH4-N in the absence of plant growth (Fig. 1), this trend was not discernible in sown basins (Table 1). Instead, soil NH4-N in sown basins probably mainly reflects effects of N uptake, and may also reflect effects of root zone oxygen on nitrification. Specifically, the low initial NH4-N in no-carbon basins occupied by Phalaris (Table 1) was probably the result of rapid initial Phalaris growth in no-carbon basins (L. Perry, personal observation) leading to high N uptake and perhaps increased nitrification. Similarly, shallow Phalaris roots, and thus limited N uptake and root zone oxygen, under N-poor conditions probably accounted for the relatively high NH4-N in C-0·00 and C-0·025 Phalaris monocultures later in the experiment (Table 1).
Carex dominance over Phalaris under N-poor conditions (Fig. 2) indicates that maintaining low soil N availability (< 30 mg kg−1 inorganic N) in restored prairie potholes would allow sedge meadow species to slow or preclude Phalaris invasion. Further research is needed to examine interactions between more diverse sedge meadow communities and Phalaris under N-poor conditions. Creating N-poor conditions in restored prairie potholes is likely to require active reduction of soil N availability. While soil inorganic N concentrations in minerotrophic sedge meadows in northern Minnesota can be as low as 30 mg kg−1 (Bridgham, Updegraff & Pastor 1998), inorganic N concentrations in prairie potholes located in agricultural regions can exceed 700 mg kg−1 (Wetzel & van der Valk 1998). N availability in drained prairie potholes could be lowered prior to restoration with repeated harvests of cover crops or with carbon enrichment. Periodic vegetation harvests have been shown to be effective for creating and maintaining mesotrophic conditions in nutrient-enriched Dutch fens (Verhoeven & Schmitz 1991) and, to a limited extent, in North American grasslands (Maron & Jeffries 2001). Soil carbon amendments for lowering soil N availability have also received some recent attention in the literature (Wilson & Gerry 1995; Morghan & Seastedt 1999; Paschke, McLendon & Redente 2000). However, only two studies (Blumenthal, Jordan & Russelle 2003; Zinc & Allen 1998), in addition to the present study, describe methods and conditions under which carbon enrichment facilitates native species establishment. The large quantities of carbon that may be required to lower N availability sufficiently could make carbon enrichment difficult to apply over large spatial scales. In future research, it will be important to develop methods to reduce N availability in prairie potholes prior to carbon addition and to identify the minimum amount of carbon required to lower N availability sufficiently.
Although very low inorganic N concentrations may be attainable in restored prairie potholes, maintaining low N availability over time may be difficult. Inorganic N initially immobilized because of carbon enrichment becomes available again through mineralization after a significant portion of the added carbon is lost to the atmosphere via respiration (Tisdale, Nelson & Beaton 1985). Furthermore, any reductions in N availability may be offset over time by N inputs from the surrounding landscape (Neely & Baker 1989), particularly in agricultural landscapes where N inputs to wetlands can be high (Davis et al. 1981). To maintain inorganic N concentrations sufficiently low to prevent Phalaris invasions, it may be necessary to reduce N inputs to wetlands by controlling the movement of nutrients, for example with vegetation buffers (Dosskey 2001), and by minimizing sources of N pollution in the surrounding landscape.
When altered resource conditions such as N enrichment facilitate invasion, manipulating resource availability to confer a competitive advantage to native species over invasive species may often be an effective approach to invasive species control. Our results demonstrate that lowering N availability in wetland soil can be used to reverse outcomes of competition between a native and an invasive plant.
D. Blumenthal helped with the focus and design of the experiment. R. Becker, C. Kellogg, R. Shaw and an anonymous referee provided helpful comments on earlier versions of the manuscript. N. Genereux, M. McNearney, R. Meissner, S. Mosi, J. Mulhouse and A. Westhoff assisted with data collection. Funding was provided by a NSF Pre-doctoral Fellowship, a Louise Dosdall UM Endowed Fellowship, a Carolyn Crosby UM Endowed Fellowship, a UM Special Grant for Doctoral Dissertation, and a Sigma Xi Grant-in-Aid-of-Research. This is a publication of the University of Minnesota Agricultural Experiment Station.