Estuaries and Coasts

, Volume 33, Issue 5, pp 1225–1236

Can Plant Competition and Diversity Reduce the Growth and Survival of Exotic Phragmites australis Invading a Tidal Marsh?

Authors

    • University of New Hampshire, Jackson Estuarine Laboratory
  • David M. Burdick
    • Department of Natural Resources and the EnvironmentUniversity of New Hampshire, Jackson Estuarine Laboratory
Article

DOI: 10.1007/s12237-010-9328-8

Cite this article as:
Peter, C.R. & Burdick, D.M. Estuaries and Coasts (2010) 33: 1225. doi:10.1007/s12237-010-9328-8

Abstract

The rapid proliferation of Phragmites australis in North America has challenged resource managers to curb its expansion and reduce the loss of functional tidal marsh. We investigated whether native plant competition could reduce the ability of Phragmites to invade a tidal marsh, and if plant diversity (species richness, evenness, and composition) altered the competitive outcome. Immature Phragmites shoots and four native halophytes were transplanted to small but dense field plots (~1,200 shoots m−2) comprising three community structure types (Phragmites alone, Phragmites + 1 native species, and Phragmites + 4 native species). Interspecific competition significantly reduced Phragmites aboveground biomass, shoot length production, density, and survival by approximately 60%. Additionally, plots planted with greater native diversity contained Phragmites with the lowest growth and survival, potentially indicating diversity-enhanced resource competition. Competition consistently reduced the growth of Phragmites even under favorable conditions: lack of strong tidal flooding stresses as well as elevated nutrient pools.

Keywords

BiodiversityRichnessCommon reedInvasive species managementHalophyteSalt marsh

Introduction

Phragmites australis (Cav.) Trin ex Steud. (commonly referred to as “common reed”) is a rhizomatous perennial grass inhabiting every continent except Antarctica (Haslam 1972). In North America, P. australis was historically described as a minor component of coastal marshes (Orson et al. 1987; Chambers et al. 1999), but over the last century, it has dramatically expanded its geographic distribution along the Atlantic seaboard and invaded many tidal marshes (Chambers et al. 1999; Meyerson et al. 2000; Saltonstall 2003). Currently, P. australis is considered a nuisance species (i.e., a species that causes ecological or economic harm) because it has adversely affected the structure and functions of coastal marshes, which provide many services beneficial to human and wildlife populations. Acres of salt marsh, once dominated by short native grasses, rushes, and sedges, have given way to stands of common reed that can extend over 3 m tall (Haslam 1972; Chambers et al. 1999; Meyerson et al. 2000). Although a handful of studies (summarized by Hershner and Havens 2008) note some benefits of P. australis invasion (e.g., enhanced nutrient retention and comparable avifauna habitat based on densities), the majority of studies link natural community invasion by this species to functional degradation. Colonization of heterogeneous coastal marshes by P. australis often results in homogenous stands (Keller 2000; Meyerson et al. 2000), which the majority of studies suggest exhibits substantially less ecosystem services compared with the mosaic pattern of native marsh vegetation (Zedler et al. 2001; Burdick and Konisky 2003; Lathrop et al. 2003). Besides floral diversity, other salt marsh services negatively impacted by the invasion of P. australis include alterations to nutrient cycling (Findlay et al. 2003; Windham and Meyerson 2003), carbon storage (Windham and Lathrop 1999), and wildlife use. Experimental studies have identified declines in bird abundance (Benoit and Askins 1999), nekton abundance and diversity (Warren et al. 2001; Able et al. 2003; Raichel et al. 2003), and benthic invertebrate abundance (Raichel et al. 2003) after P. australis expands into a salt marsh.

The recent invasion of P. australis into coastal marshes and its ability to out compete native marsh plants is unlikely to be attributed to one factor, but rather an array of factors (Burdick and Konisky 2003). There is evidence linking nuisance populations of P. australis to an exotic variety (Saltonstall 2002) introduced to North America during the nineteenth century (Lindroth 1957). The exotic strain of P. australis (hereinafter referred to as Phragmites), which now appears to be the dominant variety along the eastern coast of North America, exhibits a strong competitive ability coupled with wide physiological tolerances and mechanisms to avoid abiotic stresses. The most obvious competitive advantage for Phragmites arises from its tall shoots (3 m), which shade the much shorter native salt marsh plants (0.2–0.8 m). Phragmites also possesses a tolerance to physical and chemical stresses associated with tidal flooding, demonstrated by its ability to flourish in soil with pore water salinities up to 15–20 ppt (Lissner and Schierup 1997; Konisky and Burdick 2004; Vasquez et al. 2005) and soil pore water hydrogen sulfide up to 0.3–0.4 mM (Chambers et al. 1999; Seliskar et al. 2004). Further enhancing the success of Phragmites is its ability to avoid the stresses of waterlogging and toxic hydrogen sulfides by oxygenating its rhizosphere (Haslam 1972) and reducing tidal flooding by increasing marsh surface elevation (Windham and Lathrop 1999; Warren et al. 2001).

Human activities in coastal regions, which have also steadily increased over the past century, may contribute to Phragmites expansion (Chambers et al. 1999; Rice et al. 2000; Bertness et al. 2002). Examples of anthropogenic disturbances to coastal marshes include direct effects of development and coastal marsh management (e.g., filling, dredging, and ditching), indirect effects of residential development and urbanization (e.g., tidal restrictions, increased runoff, and eutrophication), and global impacts such as climate change (summarized in Bart et al. 2006). These activities appear to facilitate invasion by increasing Phragmites’ propagule distribution, engineering a more benign habitat, or disturbing native competitors.

Native competitors provide an important ecological barrier to invading plants by competing for essential resources. Competition, defined as a negative effect one species has upon another by limiting access to or by consuming a particular resource thereby limiting its availability (Keddy 1989), can influence the composition of salt marsh plant communities (Barbour 1978; Bertness and Ellison 1987; Pennings and Callaway 1992; Emery et al. 2001; La Peyre et al. 2001). Field studies indicate competition with native species reduces the success of Phragmites. For instance, Konisky and Burdick (2004) found evidence that Phragmites was a superior competitor to most native species, but was still slightly inhibited by interspecific competition. Other studies have found more pronounced effects of native competitors on Phragmites leading to slower expansion (Amsberry et al. 2000; Minchinton 2002; Minchinton and Bertness 2003) and reduced colonizing success (Wang et al. 2006).

The diversity of native competitors plays a critical role in the success of invading species. Theory predicts that greater biodiversity, defined as the variety of life at all levels from genetic to landscape differences, can reduce the success of invaders (Elton 1958) through greater productivity (Hutchinson 1959; Tilman et al. 1997) and strong interspecific interactions (Case 1990). Hutchinson (1959) attributed greater resource efficiency of diverse ecosystems to the process of community-wide character displacement, which occurs when similar species overlap in range, and as a result of competition, one or more characters are altered (Brown and Wilson 1956), thereby limiting genotypic or phenotypic similarities relating to resource use (Abrams 1983). Over time, species continue to diverge (character displacement) at every level of the community until all habitats or niches in an ecosystem are each occupied by the most competitive species. Because the occupant of each niche is largely determined by resource competition (Van Valen 1965), less resource efficient species will likely be replaced by more efficient ones (Tilman 1982), leading to a competitively superior species within each niche. In an ecosystem where physical and chemical gradients arise in time and space, several specialist species should be more efficient at resource utilization than a single generalist species (Elton 1958; Hutchinson 1959; Tilman 1982). In order for a species to successfully invade a community near saturation (i.e., the number of species present in a community that allow their niches to be as close together as possible without competitive exclusion), it must displace one or more species currently occupying its preferred niche dimensions, unlike an ecosystem with low diversity, which likely has niche dimensions not yet inhabited (Elton 1958; Tilman 1982). In addition, an enhanced competitive environment created by larger communities also leaves invaders more susceptible to stochastic mortality (Tilman 2004). Evidence for depressed invasion rates with enhanced plant diversity has not been tested in coastal marshes, but has been documented in grassland field plots (Naeem et al. 2000; Kennedy et al. 2002).

We investigated whether native plant competition could reduce the ability of Phragmites to invade a tidal marsh, and if plant diversity altered this relationship. We analyzed morphological features of single Phragmites shoots over one growing season planted in field plots with differences in community structure. The community structure of our field plots was manipulated by transplanting native marsh species, exposing Phragmites to differences in plant competition, composition, richness, and evenness. Our hypotheses are that (1) native competitors planted with Phragmites in field plots will reduce the growth and survival of Phragmites relative to plots without competitors and (2) diversity of native plants will further reduce the growth and survival of Phragmites relative to those planted with only one competitor, due to greater resource competition.

Materials and Methods

Study Site

The experiment was conducted at the northern section of Meadow Pond Marsh (42.936°N, 70.801°W) in Hampton, Rockingham County, NH, USA. The study site is a back barrier marsh growing on coarse over-wash deposits, which borders a relatively small tidally influenced water body (~23.6 ha). Meadow Pond Marsh, part of the largest marsh complex in New Hampshire, has historically been impacted by human activities, particularly tidal restrictions, marsh fill, and adjacent upland development (Fig. 1). Residential and road development altered the natural inlet to the site, and as a result, tidal exchange had been designated as severely restricted by the NRCS (USDA 1994). Additionally, residential developments and roads border the west, north, and east areas of the marsh. Phragmites, Typha angustifolia (narrowleaf cattail), Spartina patens (salt marsh hay), and Spartina alterniflora (smooth cordgrass) form a mosaic of communities with other saline and brackish species composing the marsh vegetation (Burdick et al. 2009).
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Fig. 1

Aerial image of Meadow Pond Marsh in Hampton, NH, USA (42.936°N, 70.801°W) outlining the location of the vegetation plots

In 1996, tidal exchange was increased in Meadow Pond after a larger culvert was installed at the southern inlet, but the northern section of the marsh is flooded irregularly and dominated by invasive Phragmites. In the winter of 2004, Phragmites along with the upper 10 to 40 cm of sediment were removed as a part of a larger restoration effort that was aimed at enhancing tidal flooding of the marsh surface. Both restoration measures appear to have slightly increased tides in the study area, but tides still do not exhibit a regular semi-diurnal pattern. For several days each month, spring tides would completely and continuously inundate the high marsh due to the accumulation of tidal waters upstream of the new culvert. In contrast, neap tides only occasionally flooded the low marsh. The average tidal range was 0.24 ± 0.01 m for spring tides and 0.09 ± 0.01 m for neap tides. Edaphic conditions indicated a brackish marsh with oxidized soils (Peter 2007; Table 1).
Table 1

Plot elevations and pore water chemistry across marsh planting zones

 

High marsh

Low marsh

 

Elevation (m)

1.01 ± 0.01

0.85 ± 0.01

*

Salinity (ppt)

23 ± 1

25 ± 1

ns

Redox (mV)

−24 ± 69

−7 ± 36

ns

Sulfides (μM)

92 ± 44

6 ± 1

ns

Means of elevation, salinity, redox Eh, and sulfide concentration are reported ±SE. Pore water was obtained using a stainless steel “sipper.” Salinity and redox potential were determined in the field using a hand-held refractometer and a Thermo-Orion combination redox/pH meter with a platinum redox electrode, respectively. At the laboratory, pore water sulfide was determined with colorimetric analysis using Cline’s reagent (Cline 1969). Plot elevations are connected to NAVD 1988 through a nearby benchmark

ns non-significant

*p < 0.05

Experimental Design

The effects of plant competition on Phragmites were examined in a one-factor randomized complete block design. Densely vegetated plots 30 by 30 cm in size were planted across three distinct community structure types, which included Phragmites planted alone (PA), Phragmites planted with one native species (P + 1), and Phragmites planted with four native species (P + 4). The community structure treatments were designed to measure the effects of interspecific competition (PA vs. Phragmites planted with native competitors), species richness (one vs. four native species), evenness (J of 0.99 vs. zero), and composition (high marsh vs. low marsh species) on Phragmites. Each treatment level was randomly placed within the high or low marsh and replicated 12 times, yielding 36 plots (Fig. 2). Plots were evenly assigned to two marsh zones to examine the physical and chemical stresses on Phragmites, but because soil flooding and pore water chemistry were similar in the high and low marsh due to irregular flooding patterns (Table 1), marsh zone was only treated as a blocking factor.
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Fig. 2

a Design of vegetation plot placements for testing the effects of community structure on the growth and survival of Phragmites. Community structure treatment levels were randomly assigned within two blocking factors (elevation and replicate). PA Phragmites planted alone, P + 1 Phragmites planted with one native species, P + 4 Phragmites planted with four native species. b An example of each treatment level is shown with cells filled in black, Phragmites; vertical lines, S. alterniflora; horizontal lines, S. patens; cross-hatch, J. gerardii; and gray, D. spicata. Boxes represent a 30 × 30 cm planting plot

Vegetation plots, regardless of community structure treatment, were planted with four Phragmites shoots, which were individually cut from clonal stands on site, removed, grown in a greenhouse, and returned as healthy plants to the site in 4 weeks to reduce mortality caused by transplantation. Shoots were selected if they were 10–25 cm in height and contained at least two nodes on their rhizomes. PA plots contained four Phragmites shoots. P + 1 plots also contained four Phragmites shoots, but were planted with 21 plugs of one of two native species (Fig. 2). High marsh P + 1 plots were planted with S. patens, while low marsh P + 1 plots were planted with S. alterniflora to identify the effects of species composition. Both Spartina grasses were chosen because of their natural dominance in New England marshes in their respective marsh zone. P + 4 plots contained four Phragmites shoots planted alongside four common New England salt marsh perennials: Distichlis spicata (spike grass), Juncus gerardii (black grass), S. alterniflora, and S. patens. The placement of each species within each plot was randomly selected. Three species were planted with five plugs and one randomly selected species with six plugs to standardize species evenness (Fig. 2). Species evenness of native plants approached unity, Pielou’s J = 0.998,
$$ J = \frac{\text{Hi}}{{{\hbox{Ln}}(S)}} $$
where Hi is the Shannon Wiener diversity index and S is the species richness.

All planting units were separated by 7.5 cm to optimize and standardize shoot resource competition within and between species (Huddleston and Young 2004). Native plants were purchased and shipped from nurseries as 5-cm-diameter plugs with multiple shoots per plug. Native plants had little variability in shoot height (15–25 cm) and experienced a low mortality (<5%). All plants were acclimated to 15–20 ppt before transplanting to Meadow Pond Marsh.

Planting Procedure

Vegetation plots were prepared by digging 10 cm deep to loosen the sediment and remove the remaining rhizome fragments of Phragmites. Native grasses and Phragmites shoots, totaling over 700 planting units, were planted in late May 2005. Shoot densities in P + 1 and P + 4 plots were relatively high (~1,200 shoots m−2) and comparable with high marsh shoot densities of undisturbed salt marshes (Bertness and Ellison 1987).

During the first 2 weeks, dead plants were replaced weekly with excess plants kept on site in garden flats dug 5 cm into the sediment to offset mortalities caused by transplantation alone. Eleven (8%) of the planted Phragmites bare-root culms died and were replaced. After the first 2 weeks, any shoot or plug that died was not replaced, but instead recorded. To maintain plot treatment levels, invading plants from outside of the plots were cut to 1 cm of the soil surface every week. Since invading plants were not allowed to emerge and were minimal across treatments, their effect was considered negligible for all plots.

Response Variables

The initial aboveground biomass of Phragmites was estimated by drying and weighing similarly sized shoots to those planted also in late May 2005. A total of 31 Phragmites shoots were chosen based on heights varying from 5 to 80 cm. Shoot heights, shoot diameters, and live dry weight aboveground biomass were measured. A log–log relationship of aboveground biomass to shoot height and diameter (Ln Biomass (g) = 0.787 × Ln Culm Diameter (mm) + 0.982 × Ln Culm Height (cm) −5.08; adjusted R2, 0.927; F = 191; p < 0.0001) was established to obtain an initial aboveground biomass estimate for each planted shoot. Final aboveground biomass was obtained by weighing dried Phragmites shoots at the close of the growing season in late September 2005.

Aggregate shoot length production, shoot density, and shoot survival of Phragmites were assessed every 3 weeks. Aggregate shoot length production was calculated by subtracting the initial shoot height from the maximum shoot height(s) for each individual plant. In the instances when multiple shoots emerged from a single Phragmites plant, the sum of all live shoot heights was used as the maximum shoot height. Shoots greater than 6 cm in height were counted and measured to the tip of the tallest green leaf. Shoot densities were measured as the greatest number of live shoots that developed at any one time from the initial planted bare-root culms. Lastly, shoot survival was calculated by dividing the total number of live shoots at the end of the experiment by the total number of shoots.

Phragmites shoots experienced high aphid density. Aphids can impair the health of a plant by draining plant sap from phloem vessels and potentially transferring disease (Summers and Newton 1989; Dilwith et al. 1991). To include possible effects of aphid attachment on Phragmites, aphid infestation was estimated by determining what percentage of the initial four planted Phragmites shoots experienced aphid grazing at any time during the growing season.

Statistical Analysis

Statistical analyses were performed using JMP (SAS Institute Inc. 2006, 6.0.2), and figures were created in Microsoft PowerPoint (Microsoft Office 2000) or SigmaPlot (SigmaPlot 2000, 6.10). Phragmites response variables were averaged for each plot before least squares analysis. An analysis of variance (ANOVA, α < 0.05) was used to examine the effects of community structure, and a t test (α < 0.05) was used to examine the effects of species composition, which were considered fixed factors. Residuals were examined, and data were transformed using log (y + 1) when appropriate (aboveground biomass, shoot density, and occurrence of aphids) to produce homogenous, normally distributed error. Means are reported with the standard error (SE).

Linear contrasts were used to examine differences in means among the treatment levels of community structure (α = 0.05). To test the effect of native plant competition on Phragmites, the mean of PA plots was compared with the pooled means of P + 4 and P + 1 plots. To test the effect of plant composition and diversity on Phragmites, P + 4 plots were compared with P + 1 plots. A Bonferroni correction was applied to the alpha (α) to control the family-wise error rate (0.05/5 = 0.01). In addition, a multivariate analysis of variance (MANOVA, sum response, α < 0.05) was used to examine the effects of species composition and diversity.

Results

Different community structures (PA, P + 1, and P + 4) resulted in significant differences in Phragmites aboveground biomass, aggregate shoot length production, shoot density, shoot survival, and likelihood to host aphids (Fig. 3). More specifically, the aboveground biomass of Phragmites declined sharply with greater complexities in community structure. Aggregate shoot length production, shoot density, shoot survival, and the occurrence of aphids experienced significant but more gradual declines with greater complexities in community structure, with P + 4 always resulting in the most dramatic effect.
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Fig. 3

The effects of community structure on Phragmitesa aboveground biomass, b aggregate shoot length production, c shoot density, d shoot survival, and e the occurrence of aphid attachment were analyzed in a one factor ANOVA with F ratios and p values reported in the upper right corner of each panel. Bars represent means ± SE (n = 12). p values above solid lines connecting PA to P + 1 and P + 4 are the results of linear contrasts testing the effect of interspecific competition on Phragmites. p values above solid lines connecting P + 1 to P + 4 are the results of linear contrasts testing the effect of species richness and evenness on Phragmites

The growth and survival of Phragmites was significantly reduced if planted with neighboring species when the effect of competition was tested by a linear contrast comparing P + 1 and P + 4 plots to PA plots (Fig. 3). The presence of native competitors severely reduced the aboveground biomass of Phragmites by 83.7%. Additionally, competition reduced aggregate shoot length production by 60.0%, density by 48.3%, and survival by 58.8%. Native competitors also reduced the likelihood of Phragmites to host aphids by 74.2%, potentially indicating a less healthy plant.

The reduction of Phragmites growth and survival by the presence of native competitors was enhanced by greater competitor diversity (indicated by species richness, one versus four competitors; and species evenness, J = 0.998 in P + 4 plots and J = 0.000 in P + 1 plots). Greater species richness and evenness, as tested by a linear contrast comparing the means of plots planted with four native species to plots planted with one native species, significantly reduced the shoot length production of Phragmites over one growing season (\( {\hbox{P}} + {1} = {44}.{5} \pm {8}.{1} {\hbox{cm and P}} + {4} = {23}.{1} \pm {3}.{9} {\hbox{cm}} \); Fig. 3). Furthermore, Phragmites shoot density was 31.5% less in the higher diversity plots. Although not significant, plant diversity appeared to depress Phragmites shoot survival, aboveground biomass, and the likelihood to host aphids (e.g., reductions of 34.2%, 62.5%, and 69.4% respectively). Using a Bonferroni correction (α/n) to adjust for the family-wise error rate for five variable comparisons (α = 0.01) within the same experiment, greater species richness and evenness did not significantly depress any one Phragmites variable. To account for non-independent variables without using an α correction, the data were combined and ran in a multivariate model (MANOVA), which showed a significant difference due to the combined effects of diversity (p = 0.016).

The composition of native competitors affected the performance of Phragmites. Phragmites in P + 1 plots planted with S. patens had significantly greater aggregate shoot length production, shoot density, and a greater likelihood to host aphids than P + 1 plots planted with S. alterniflora (Fig. 4). Although not significant, Phragmites shoots in S. patens plots tended to show greater aboveground biomass (2.30 ± 0.70 g) and shoot survival (36.4 ± 9.2%) than those in S. alterniflora plots (0.92 ± 0.51 g and 27.7 ± 11.8%, respectively). A Bonferroni correction was also applied to species composition, adjusting for the family-wise error rate (α = 0.01) and reversing any prior significance. The results of a MANOVA, however, found a significant difference (p = 0.030) with regards to species composition. Even though S. patens appeared to have been a weaker competitor in this experiment, Phragmites planted alone always outperformed Phragmites planted in P + 1 plots regardless of the species composition (Fig. 4).
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Fig. 4

The effects of species composition on Phragmitesa aboveground biomass, b aggregate shoot length production, c shoot density, d shoot survival, and e the occurrence of aphids were analyzed in t tests with t and p values reported in the upper right corner of each panel. Bars represent means ± SE (n = 6). The horizontal lines represent the mean ± SE of PA plots (n = 12)

Discussion

The growth and survival of Phragmites was reduced by the presence of native species, presumably from resource competition. Phragmites shoots planted without native competitors present (PA) were clearly healthier and more productive than Phragmites shoots planted with native competitors (P + 1 and P + 4). The results we present on competition by native species are analogous to other Phragmites competition studies. Amsberry et al. (2000) were among the first to recognize the negative impacts neighboring plants had on the performance of Phragmites. Clusters of Phragmites (two to five shoots) transplanted into different marsh zones had a lower survival rate with neighboring plants present compared with without. In a Massachusetts salt marsh, Minchinton (2002) found that Phragmites expansion was significantly greater in areas with dead native plants previously killed off by wrack than areas with live native plants. And, Minchinton and Bertness (2003) found decreased growth and survival rates of Phragmites shoots when growing with native perennials in the high marsh. Unlike our experiment, previous field experiments utilized naturally growing established stands of native plants instead of manipulating native plant diversity by transplantation. More recently, Wang et al. (2006) examined the ability of Phragmites to re-colonize a marsh after it was removed by burning and herbicide application. Similar to our results, they found that Phragmites was less successful at colonizing a marsh if native grasses or shrubs were planted immediately after restoration.

In eastern tidal marshes, native plants largely compete with invasive Phragmites for three limiting resources: (1) space, (2) nutrients, and (3) light. First, native plants growing adjacent to Phragmites provide a physical barrier deterring the expansion of tillers, adventitious roots, and rhizomes. In a Mississippi salt marsh, Brewer (2003) concluded that the belowground morphology (i.e., dense mats of rhizomes and roots) of high marsh perennials was the main deterrent preventing low intertidal species from invading, and not belowground competition for nutrients. Disturbance to existing native vegetation, whether by natural wrack accumulation and die off or anthropogenic activities such as burial with fill material or yard waste, eliminates physical barriers and allows for more successful expansion of Phragmites (Minchinton 2002; Burdick and Konisky 2003). Secondly, competition for nutrients in the soil column, particularly nitrogen, can inhibit or potentially restrict Phragmites invasion. In a Rhode Island salt marsh, Minchinton and Bertness (2003) found reductions in Phragmites growth when growing within a matrix of native vegetation, but these effects were not as obvious in plots receiving regular nitrogen fertilization, suggesting belowground competition for nutrients was minimized in fertilized plots. And lastly, competition for light plays an important role in determining marsh communities (Levine et al. 1998; Emery et al. 2001). Phragmites appears to have the competitive advantage in obtaining light by allocating a larger fraction of its resources to aboveground production (Haslam 1971; Windham and Meyerson 2003), leading to tall, dense canopies averaging over five times the height of native marsh plants (Konisky and Burdick 2004). Although light was not measured, our results suggest that native competitors may be able to slow stand expansion of culms developing from rhizomes and tillers or prevent establishment (e.g., seed germination and rhizome fragment emergence) of this invasive grass by reducing light levels.

The majority of field studies along with the results presented here found decreased growth and survival of young Phragmites shoots when adjacent native plant canopies were present. Very little light penetrates through to the soil surface when native species are present, especially in the high marsh zone where dense turf species exist. In contrast, increased light levels at the surface of bare soils can induce Phragmites seeds to germinate or rhizome buds to emerge (Haslam 1972; Wijte and Gallagher 1996). At Meadow Pond, developing young Phragmites shoots appeared to be limited by light rather than nutrients. In a complementary experiment, regular fertilization did not alleviate the significant reductions in Phragmites growth and survival when planted with native competitors, suggesting that light and/or space and not nutrients was the limiting resources (Peter 2007). The effectiveness of native competitors on reducing Phragmites success, however, has mainly been demonstrated on seeds, transplants of young shoots, and buried rhizomes, which have been the main pathways for establishment into new sites. Once established, Phragmites becomes more resilient to mortality (Haslam 1971; Rice et al. 2000; Bart et al. 2006) and expands through vegetative reproduction. Native plants appear less effective at limiting well-established Phragmites stands through light competition because of the disparity in canopy heights, and the clonal nature of Phragmites shoots within stands, which appear to integrate resources through connected rhizomes (Amsberry et al. 2000).

Our results showing the limited success of Phragmites (e.g., aggregate shoot length production and density) in the P + 4 plots may be partially due to plant diversity, which has been supported by theoretical and experimental evidence. In Minnesota grasslands, community invasibility was directly tested, resulting in a 90% reduction of non-native cover at the highest native species richness level compared with monocultures (Kennedy et al. 2002). Our results from a tidal marsh were similar, with a 91% reduction in Phragmites aboveground biomass when planted amongst four native species. Although the majority of studies have not been directly tested whether diversity increases community resistance to invasion, many have shown that diversity increases resource utilization and other ecosystem functions. For example, Tilman et al. (1997) manipulated plant diversities within savanna grasslands and found that species richness was positively related to plant productivity and total plant nitrogen, and negatively related to soil nitrogen and light penetration to the soil surface. Hence, field plots with greater diversity were more efficient at utilizing light and nitrogen resources. A similar study done in southern California found that net primary productivity, nitrogen cycling, and wildlife habitat (indicated by canopy complexes) were all enhanced after planting a number of different species as opposed to the traditional single species in a restoration site (Zedler et al. 2001).

Evidence supporting the relationship between plant diversity and an ecosystem’s ability to resist invasion can be applied over multiple scales. Two spatial scales germane to our research include the community and plot level. On a community scale, communities become more resource efficient and less susceptible to invasion when different specialist species occupy different niches derived from physical and chemical gradients (Hutchinson 1959; Tilman et al. 1997). On a plot scale, plant diversity can also impact ecosystem invasibility and other functions. Multiple species can provide differential root and canopy structures, allowing for further specialization of resource use. For example, J. gerardii creates a dense root matrix that competes for resources in the upper layer of the soil column, whereas S. alterniflora creates a sparser root structure that penetrates deeper into the soil. When both species grow adjacent to Phragmites, resource competition for nutrients may become enhanced through differential root structures competing for resources at different soil depths. Additionally, J. gerardii begins shoot emergence and peak productivity earlier in the growing season than most other halophytes (Bertness and Ellison 1987), providing greater resource efficiency across a temporal scale. Therefore, greater diversity results in differences in species morphology and phenology that may additionally enhance resource competition and reduce invasion.

Since biodiversity is currently regarded as an important issue both ecologically and politically, it is necessary to discuss all probable explanations of our results. Of the five variables characterizing the response of Phragmites to competition, all were depressed due to the P + 1 and P + 4 treatments, but only two showed significant declines from the P + 1 plots to the P + 4 plots. When a Bonferroni correction was applied to the tests, resulting in α = 0.01, no response variables were significantly depressed due to increased community structure. A MANOVA was used as an alternative statistical approach to quantify the potential effects of diversity, and the results of the sum response were significant (p = 0.016), suggesting that diversity appeared to have a significant negative effect on Phragmites success. However, the effects of diversity may be the result of a hidden treatment or a random effect. Of the list of potential hidden treatments discussed by Huston (1997), only one out of three has the potential to apply to our experiment: probability of experimental plots containing a species that has a dominant positive or negative effect on the function being measured. In our experiment, S. alterniflora appeared more effective at reducing Phragmites growth and density than S. patens (Fig. 4). When the original model was re-run excluding all P + 1 plots not containing S. alterniflora to test if the effects of diversity were a result of S. alterniflora being a dominant competitor, diversity became a non-significant effect for all of the Phragmites success variables. In other words, plots planted with four species including S. alterniflora were not significantly more competitive than plots planted with S. alterniflora alone. However, plots planted with four species (including S. alterniflora) did show more competitive impacts versus S. patens alone plots and versus the average of separately planted S. alterniflora only and S. patens only plots. The two major factors contributing to this difference include (1) S. alterniflora appeared more competitive than S. patens, and (2) the model “n” was halved, leading to overall higher variance. The use of S. alterniflora at the P + 1 level may have artificially created a significant diversity effect, but in order to fully understand the effects of composition on diversity, an examination of each native species used in this experiment would need to be conducted.

S. alterniflora appeared to be a more effective competitor than S. patens at inhibiting Phragmites establishment (Fig. 4; MANOVA, p = 0.030). Earlier experiments indicate otherwise, finding S. patens to be the better competitor with Phragmites when nutrients are limiting (Konisky and Burdick 2004), but competitive relationships within a tidal marsh can reverse with excessive nutrient loading (Levine et al. 1998; Emery et al. 2001). Enriched soils shift dominance in belowground competition for nitrogen to aboveground competition for light (Emery et al. 2001), perhaps allowing the taller S. alterniflora to be more competitive with Phragmites in our experiment. Other relatively poor belowground competitors in coastal marshes may also gain a competitive edge under nutrient enriched soils. Phragmites exhibits a high nutrient demand (Windham and Meyerson 2003), high allocation of resources towards aboveground biomass, and decreased vigor in nutrient-poor environments (Haslam 1972), all indicating its lack of competitive dominance for nutrients. When fertilized, Phragmites responds quickly by exhibiting greater survival, aboveground production, and stand expansion rates (Minchinton and Bertness 2003; Rickey and Anderson 2004; Saltonstall and Stevenson 2007), all of which increase its likelihood to outcompete native marsh grasses.

Soils at Meadow Pond appeared to have elevated nutrient availability as indicated by the lack of plant response to regular fertilization (Peter 2007), potentially due to site disturbances. Nutrient rich runoff may be entering the site as a result of the marsh’s highly developed watershed, including areas bordering the marsh. Moreover, plant removal prior to the study may have substantially increased nutrient pools through continued nutrient cycling of dead organic matter combined with the absence of live plants (Findlay et al. 2003). And, the site’s limited flooding by tidal waters may have led to greater nutrient availability for plant uptake due to the amelioration of physical and chemical stresses (e.g., salinity, sulfides, and anoxia; discussed in Morris 1980). At disturbed tidal marshes, we speculate that species with taller canopies that are normally poor competitors for nutrients (e.g., S. alterniflora) may be better competitors against invading Phragmites.

Aphid herbivory was initially recorded to determine the impacts on Phragmites health, but instead appears more useful as an indicator of plant health. Aphids were more likely to attach and feed on the largest and most successful Phragmites shoots, which were found in PA plots (Fig. 3). Others have observed aphids to selectively target healthier plants (Dilwith et al. 1991). Moreover, aphids may be attracted to plants growing in low diversity stands or monocultures, as herbivores are more likely to locate and remain on a host species when the host species is in dense monocultures (Root 1973). At Meadow Pond, the likelihood of Phragmites to host aphids may be due to the combined effects of Phragmites plant health and plot diversity.

Native plant competition consistently reduced the growth and survival of Phragmites despite conditions at Meadow Pond, which appeared to reduce competition for belowground resources (e.g., elevated nutrient pools and lack of tidal flooding stresses). While similar human disturbances tend to ameliorate stresses for both halophytic and brackish species, the benefit seems proportionally larger for brackish species such as Phragmites. Management of nuisance Phragmites populations may benefit from approaches that enhance ecological barriers to invasion by minimizing or eliminating anthropogenic impacts to tidal marshes. Until recently, management practices designed to control Phragmites populations have largely overlooked restoring environmental conditions and processes altered by human disturbance. Instead, previous practices employed species-specific approaches (e.g., burning, mowing, and spraying herbicides), which have not consistently produced long-term and self-sustaining results (Marks et al. 1994; Warren et al. 2001). Physical plant damage may only provide a temporary solution where environmental conditions and processes that facilitated invasion remain. Practices that address human disturbances include increasing tidal flooding, removing previous fill, reducing nutrient loads through reestablishing natural buffers surrounding the marsh, and limiting upland nutrient sources from contaminating surface runoff and groundwater. Our work indicates that maintaining dense native populations following Phragmites removal can impede reinvasion. Further, competition appeared to be enhanced from diverse plantings, whether from species richness or composition, and we recommend planting a diversity of native species to account for variable site conditions, stochastic events, and human disturbance. Limiting human disturbance coupled with species-specific practices to remove existing invaders and enhance interspecific competition will promote restoration success (Weisner and Graneli 1989; Asaeda et al. 2003).

Acknowledgments

We thank Garrett Crow, Aaren Freeman, Thomas Lee, and Barrett Rock for their comments on previous drafts on this manuscript. We are also grateful to Jessica Devoid, Alyson Eberhardt, Joanne Glode, Gregg Moore, and Robert Vincent for their assistance in the field, and again Alyson Eberhardt and Paul Sokoloff for assistance with analyses. The manuscript was improved by the insightful comments by two anonymous reviewers and the associate editor, Dr. Morten Pedersen. Primary funding for this research was provided by the New Hampshire Coastal Program, Department of Environmental Services under NOAA grant nos. NA17FZ2603 and NA170Z1529, and by NOAA’s Restoration Center, grant no. NA05OAR4171149. Additional funding was provided by the New England Chapter of the Society of Wetland Scientists. Jackson Estuarine Laboratory contribution no. 494.

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© Coastal and Estuarine Research Federation 2010