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Keywords:

  • colonization;
  • invasive species;
  • pre-emption;
  • priority effect;
  • submersed macrophyte;
  • Vallisneria americana

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  • 1
    With biological invasions causing widespread problems in ecosystems, methods to curb the colonization success of invasive species are needed. The effective management of invasive species will require an integrated approach that restores community structure and ecosystem processes while controlling propagule pressure of non-native species.
  • 2
    We tested the hypotheses that restoring native vegetation and minimizing propagule pressure of invasive species slows the establishment of an invader. In field and greenhouse experiments, we evaluated (i) the effects of a native submersed aquatic plant species, Vallisneria americana, on the colonization success of a non-native species, Hydrilla verticillata; and (ii) the effects of H. verticillata propagule density on its colonization success.
  • 3
    Results from the greenhouse experiment showed that V. americana decreased H. verticillata colonization through nutrient draw-down in the water column of closed mesocosms, although data from the field experiment, located in a tidal freshwater region of Chesapeake Bay that is open to nutrient fluxes, suggested that V. americana did not negatively impact H. verticillata colonization. However, H. verticillata colonization was greater in a treatment of plastic V. americana look-alikes, suggesting that the canopy of V. americana can physically capture H. verticillata fragments. Thus pre-emption effects may be less clear in the field experiment because of complex interactions between competitive and facilitative effects in combination with continuous nutrient inputs from tides and rivers that do not allow nutrient draw-down to levels experienced in the greenhouse.
  • 4
    Greenhouse and field tests differed in the timing, duration and density of propagule inputs. However, irrespective of these differences, propagule pressure of the invader affected colonization success except in situations when the native species could draw-down nutrients in closed greenhouse mesocosms. In that case, no propagules were able to colonize.
  • 5
    Synthesis and applications. We have shown that reducing propagule pressure through targeted management should be considered to slow the spread of invasive species. This, in combination with restoration of native species, may be the best defence against non-native species invasion. Thus a combined strategy of targeted control and promotion of native plant growth is likely to be the most sustainable and cost-effective form of invasive species management.

Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The world's ecosystems are experiencing an increasing number of invasions of non-indigenous species (Vitousek et al. 1997). Most species fail to colonize successfully but some flourish in new environments, often with negative consequences on local community composition, ecosystem functioning and services to human society (Chapin et al. 2000). Such changes in the environment brought about by invasive species highlight the importance of understanding effective methods that limit a system's invasibility. One such method may be the restoration of native plant species that can decrease the colonization success of an invader (Bakker & Wilson 2004).

The colonization success of a potential invader is, in part, influenced by its traits. While many traits can be associated with establishment success, high output of plant propagules or animal offspring is often cited as an important species trait of an invader (Kolar & Lodge 2001). This makes intuitive sense because the chances increase that a species establishes successfully when more individuals are introduced to a site in time and/or in space. Thus, from a management perspective, reducing the number of individuals released and the number of release events, often referred to as propagule pressure (Allendorf & Lundquist 2003), could curb the success of a potential invader (Kolar & Lodge 2001).

Colonization success of a potential invader can also be influenced by the environmental characteristics of a site. A system saturated with competitors and therefore with a low level of niche opportunity (Shea & Chesson 2002) is less likely to be successfully invaded by non-native species. However, even when communities appear to be saturated, existing species may facilitate the establishment of other species (Levine 1999). Here, facilitation can modify environmental conditions, such as pH, nutrients or oxidation of water or sediments, and render the habitat more hospitable to other species. While species traits and environmental characteristics may separately affect invasion success, the interaction of the two factors may be equally important (Shea & Chesson 2002). For example, a species with a high propagule output has a greater chance of invading a habitat with a low density of competitors than a habitat saturated with competitors.

We report here the results of studies that explored the colonization success of a highly invasive submersed aquatic macrophyte, Hydrilla verticillata (L.F.) Royle, that can occur as monoecious and dioecious strains that differ in distribution, growth form and competitive interactions (M. D. Netherland, personal communication). The monoecious strain is dominant in Chesapeake Bay, Maryland, USA, where our study was located; this strain was therefore used in our experiments. Hydrilla verticillata is native to tropical Asia and was first discovered in the USA in 1960 in two locations in Florida. By the early 1970s it was found in all major drainage areas in the state. It is currently reported in 21 states in the USA. Hydrilla verticillata has many of the traits that are commonly attributed to invasive species. It has specialized growth, physiological and reproductive characteristics that have permitted it to become a dominant species in a broad range of freshwater ecosystems (Langeland 1996). It also has a history of invasion and covers an extensive geographical range in its region of origin. Hydrilla verticillata produces large quantities of vegetative propagules in the form of fragments and turions. The fragments are capable of floating in the water column from days to weeks before settling and rooting. Finally, because this macrophyte disperses primarily through fragments, it has an ‘always-ready’ strategy associated with successful colonization of new areas (Barrat-Segretain & Bornette 2000).

We tested two alternative hypotheses, that pre-existing native vegetation would (i) reduce the colonization success of invasive species (the pre-emption hypothesis); and (ii) facilitate the colonization of H. verticillata (the facilitation hypothesis). Complementary to the first two hypotheses, we tested the hypothesis (iii) that increasing propagule availability would increase the invasion success of H. verticillata into pre-existing native vegetation (the propagule pressure hypothesis). The hypotheses were tested in 2003 using replicated field and greenhouse experiments, where the field experiment provided the necessary realism to understand an invaded system open to influxes of nutrients and propagules. The greenhouse experiment, on the other hand, provided a best case for invasion resistance by controlling propagule influx and allowing the native plant to draw-down nutrients. To test the former set of alternative hypotheses, we compared colonization of H. verticillata into experimental patches of live Vallisneria americana Michaux and plastic V. americana to an unplanted treatment, to separate the physical effects of pre-existing live or plastic plants from the effects of live plants on nutrient concentrations. To test the latter propagule pressure hypothesis, we compared H. verticillata colonization success into the three planted and unplanted treatments subjected to a H. verticillata biomass gradient in the field and controlled H. verticillata fragment introductions in the greenhouse.

Materials and methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

study site

We conducted the field research in summer 2003 at the Otter Point Creek National Estuarine Research Reserve, Abingdon, Maryland, USA (39°27′N, 76°16′W). This water body in the upper Chesapeake Bay contains 106 ha of tidal freshwater habitat. The maximum depth is 1·5 m, with a mean tidal range of 0·3 m. The Otter Point Creek Reserve is of particular interest because the presence of the monoecious strain of H. verticillata was first documented here in the summer of 2002 (J. Bortz, unpublished data). Besides H. verticillata, the submersed aquatic plant community at the study site supported Ceratophyllum demersum L., Elodea canadensis Michx., Heteranthera dubia (Jacq.) MacM., Myriophyllum spicatum L., Najas sp., Potamogeton crispus L., P. perfoliatus L., P. pusillus L., Stuckenia pectinata (L.) Böerner, Vallisneria americana and Zannichellia palustris L. Myriophyllum spicatum was the dominant species at the site in 2002, and H. verticillata has been the dominant species since 2002.

treatments

Vallisneria americana is used frequently in Chesapeake Bay to restore submersed aquatic plant beds because it was a dominant species in freshwater portions of the Bay before European settlement of the region (Brush & Hilgartner 2000) and can be propagated easily. For these reasons and because V. americana is a native macrophyte that poses little conflict with recreational interests, we decided that V. americana would represent the native freshwater submersed macrophyte community of the region.

In both field and greenhouse experiments, we created an unplanted control treatment (Bare), a treatment planted with V. americana (Vallisneria) and a treatment planted with plastic plants resembling V. americana (Plastic), to distinguish between potential mechanisms of competition and facilitation. Specifically, we predicted that if species are interacting through nutrient exploitation, H. verticillata colonization would be lower in the Vallisneria treatment than the other two treatments, effectively lending support for the pre-emption hypothesis. If so, we expected nutrient levels to be lower in the Vallisneria treatment than the Bare and Plastic treatments. Furthermore, we predicted that, if V. americana either physically inhibits or facilitates H. verticillata colonization, H. verticillata colonization would be lower (lending support for the pre-emption hypothesis) or higher (lending support for the facilitation hypothesis), respectively, in the Plastic treatment compared with the Bare treatment. Logically, the null hypothesis of no effect would be supported if no inhibitory or facilitative effects were detected. Finally, we predicted that colonization of H. verticillata into existing patches of V. americana would be greater in areas of higher H. verticillata biomass in the field or in greenhouse mesocosms with higher fragment introduction (lending support for the propagule pressure hypothesis).

field experiment

We used polypropylene strapping (1·3 cm wide × 0·04 cm thick) to create artificial plants that mimicked the morphology of V. americana such that the ability to trap propagules and to affect the light environment would be equal. To test for equal effects on light, we measured light levels under the canopies of live and plastic plants (see the greenhouse methods). We did not test for equal propagule trapping ability because the test would have required detailed flume studies. Each individual plastic plant was 45 cm tall and had eight leaves. We then fastened 17 of these plants into each of 30 plastic trays measuring 34 × 24 × 9 cm. Sixty empty trays and 30 trays with the plastic plants were filled to within 1 cm of the top of the tray with substrate that was an equal mix of commercially available topsoil and sand. The final 1 cm was then filled with sand to reduce the loss of substrate to the water column. On 14 April 2003, 30 of the bare trays were seeded with V. americana. All trays were then placed in the greenhouse and submersed in 20 cm dechlorinated domestic water. Because of poor germination, we planted 17 live V. americana plants in the previously seeded trays on 23 May 2003. Resulting V. americana densities were 209 plants m−2, which was similar to reported natural densities of this species (Korschgen & Green 1988). All trays (30 with live V. americana, 30 with plastic plants and 30 unplanted) were then maintained in the greenhouse at the University of Maryland Center for Environmental Science's Appalachian Laboratory for 35 days, to permit the V. americana to root sufficiently before placement in the field.

Experimental sites at the Otter Point Creek field location were chosen based on the H. verticillata cover estimates of the previous year (2002). We selected two separate areas at Otter Point Creek that supported high (> 40% cover) to low (< 40% cover) densities of H. verticillata. In each of the two areas, we placed one experimental site in high cover, one in low cover and one midway between the high- and low-density sites, to create a biomass gradient associated with differences in propagule flux across the gradient. Measurement of propagule flux at the different sites was attempted with little success using methods described in Rybicki et al. (2001); thus existing site H. verticillata biomass, which readily produces propagules through fragmentation, was used as a surrogate for propagule pressure. All of the trays were transported to the field location on 28 June 2003 and immediately placed in the experiment sites. Five replicates of each Bare, Plastic and Vallisneria treatment were randomly placed in each site. Sediments at the site were soft enough to allow the trays to be pushed down until the top of the tray was flush with the natural sediment. Trays were placed approximately 2 m from one another and anchored in place with PVC pipe run through the centre of each tray.

To evaluate whether experimental units were indeed placed in high, medium and low densities of existing H. verticillata, we collected all above-ground biomass of each submersed aquatic macrophytes species in four randomly placed 1-m2 quadrats at each of the six experimental sites on 17 September 2003. The biomass was not rinsed because we perceived the biomass of attached detritus and epiphytic growth to be negligible. We later dried all biomass at 60 °C for 24 h and weighed the material.

We used a portable water current meter (Model 201D; Marsh-McBirney, Frederick, MD) to measure current velocity at each of the six experimental sites over a 24-h period between 25 and 26 July 2003, to test for equal current velocities between sites at different times during the tidal cycle. Velocities were measured at 10 cm above the sediment surface and just below the water surface. We also recorded depths with a PVC depth rod at each of the sites on the hour during this period.

To identify any nutrient-related mechanisms affecting the colonization success of H. verticillata, we analysed soil pore water for total nitrogen and total phosphorus in 10 randomly selected trays per treatment. We permanently installed mini-tension lysimeters (Daiki Corp., Tokyo, Japan), placed horizontally in the soil approximately 5 cm beneath the soil surface, and collected approximately 15 mL water for analysis during two sampling periods. The first soil pore water was collected on 11 July 2003. Because of time constraints imposed by Hurricane Isabel, the final soil pore water collection did not occur in the field. Instead, on 17 September 2003, all trays were collected, sealed in plastic bags and transported intact to the laboratory. Soil pore water was collected the next day from the same trays as before using the previously installed lysimeters. We stored all water samples frozen at –19 °C for 4 months until analysis. Each water sample was digested, autoclaved and analysed for total nitrogen (TN) and total phosphorous (TP) on a Lachat QuikChem Automated Flow Injection Analysis System (APHA 1998). TN and TP were analysed to account for potential shifts in inorganic and organic nutrient pools during storage.

The content of each tray was sifted to separate the substrate from the plant material. Biomass was separated into tubers, turions and above-ground biomass for H. verticillata and total biomass for V. americana. All vegetative material was dried for 24 h at 60 °C and then weighed.

We observed in the field that pumpkinseed sunfish Lepomis gibbosus L. were nesting in several of the trays and consequently removing some amount of substrate in these trays. When the trays were collected, marks had been left on the sides of the trays from algal growth, indicating how much substrate had been removed. Based on these marks, we quantified the disturbance in each tray as a percentage of the substrate that had been removed.

greenhouse experiment

To control environmental conditions and regulate propagule input, we replicated the field experiment in greenhouse mesocosms (26 cm diameter × 36 cm height) using 16 unplanted mesocosms as controls (Bare), 16 mesocosms planted with V. americana (Vallisneria) and 16 mesocosms planted with the plastic plants (Plastic). Substrate was added to a depth of 9 cm. Thirteen plastic plants (36 cm tall) were added to the Plastic treatment and 13 live V. americana plants to the Vallisneria treatment such that the density of plastic and live plants was identical in the greenhouse and field experiments.

We began the experiment on 23 May 2003. On 19 August 2003, 10-cm long H. verticillata fragments with 10–20 nodes fragment−1, collected from Little Seneca Lake, Burdette, Maryland, were added to each of the treatments at densities of 0, 1, 5 or 10 fragments mesocosm−1. The dry mass of each fragment, measured on additional fragments of the same length, was 9·8 ± 0·1 mg (mean ± SE), which equated to 0, 0·2, 0·9 and 1·8 g m−2 introduced to 0, 1, 5 and 10 fragment treatments, respectively. We collected soil pore water from five randomly selected containers per treatment on 26 August 2003, using the same methodology as the field experiment. Water column nutrients from the same containers were sampled on 10 November 2003, rather than soil pore water, because H. verticillata was interacting more with the environment in the water column as a result of poor rooting in the substrate in Vallisneria treatments. We measured light availability under the canopies of plastic and live V. americana using a Model LI-1400 light meter (Li-Cor, Lincoln, NE), to test for similarity in effects on light availability. Biomass was sifted and separated into tubers, turions and above-ground biomass for H. verticillata and total biomass for V. americana. All samples were dried for 24 h at 60 °C and then weighed.

statistical analysis

One-way anova or a non-parametric equivalent was used to test for differences among treatments in the field and greenhouse experiments. Because data often could not be transformed to meet the assumptions of normality, we used Spearman correlation analysis to test for correlations among sunfish disturbance, H. verticillata tuber biomass and total V. americana biomass in field trays. Spearman correlations also tested for a relationship between rooted H. verticillata biomass and overall biomass production. We used an ancova to assess the effects of site–treatment interactions on the dependent variable H. verticillata tuber biomass based on the categorical variable treatment and the continuous covariate pre-existing H. verticillata biomass or disturbance by sunfish.

All biomass measurements were recorded as 100% dry matter. We used SAS software (SAS Institute 2001) for all statistical tests. Unless noted otherwise, we evaluated statistical significance at P < 0·05 and we report values as means ± SE.

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

field experiment

Mean above-ground H. verticillata biomass at each of the six sites ranged from 20·4 to 71·5 g m−2. Cover ranged from 14·5% to 100%. Sites 5 and 6 supported more H. verticillata biomass than sites 1 and 2, while sites 3 and 4 supported an intermediate amount of H. verticillata biomass (Fig. 1). Sunfish disturbance in the trays at sites 3, 4 and 6 was about three times that of the trays at the other sites (Fig. 1). The tidal range from 25 July to 26 July 2003 at the six sites averaged 58 cm. The mean depth at the sites was 45 cm at low tide and 103 cm at high tide. Average depth differed by 13 cm between the shallowest site (site 4) and the deepest site (site 1). Water current velocities measured throughout a 24-h period at the six sites never exceeded 0·02 m s−1.

image

Figure 1. Pre-existing Hydrilla verticillata biomass (a) and sunfish disturbance (b) at each of six sites in Otter Point Creek (n = 5 site−1; mean + 1 SE). Bars sharing a lowercase letter are not significantly different (Tukey-Kramer HSD multiple pairwise comparisons, α= 0·05).

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Pre-emption and facilitation hypotheses

All planted and unplanted treatments accumulated the same amount of total H. verticillata biomass (anova, F2,86 = 0·82, P= 0·44; Fig. 2a) and above-ground H. verticillata biomass (anova, F2,86 = 0·62, P= 0·54). Vallisneria americana biomass and H. verticillata tuber biomass in the Vallisneria treatment were negatively correlated (Spearman correlation, rs = −0·58, n= 30, P < 0·001). The Plastic treatment accumulated more H. verticillata tuber biomass than the Bare or Vallisneria treatments (Kruskal–Wallis test statistic = 17·66, d.f. = 2, P < 0·001; Fig. 2b).

image

Figure 2. Total Hydrilla verticillata biomass (a) and H. verticillata tuber biomass (b) in field mesocosms planted with an unplanted control (Bare), plastic Vallisneria look-alikes (Plastic), and Vallisneria americana (Vallisneria). Error bars are means + 1 SE. Different lowercase letters denote significant differences (Tukey-Kramer HSD multiple pairwise comparisons, α= 0·05).

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Soil pore water nutrients in the experimental trays declined between July and September (Fig. 3). Total phosphorous was higher in the Bare treatment than in the other two treatments in September (anova, F2,27 = 6·41, P= 0·005) but not in July (F2,22 = 1·53, P= 0·24). Total nitrogen did not differ between the Vallisneria and Bare treatments on either sampling date (anova, F2,22 = 0·78, P= 0·47 and F2,27 = 1·58, P= 0·22).

image

Figure 3. Soil pore water nutrient concentrations in samples extracted from field mesocosms planted with an unplanted control (Bare), plastic Vallisneria look-alikes (Plastic), and Vallisneria americana (Vallisneria). Error bars are means + 1 SE. Total phosphorus (P) and nitrogen (N) declined from July to September 2003. Only September phosphorus concentrations differed significantly among treatments, as shown by using different lowercase letters to denote significant differences (Tukey-Kramer HSD multiple pairwise comparisons, α= 0·05).

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Bare and Vallisneria treatments experienced 50% higher sunfish disturbance than trays with plastic plants (F2,86 = 3·65, P= 0·03). While sunfish disturbance could have been a potentially confounding factor in the experiment, an ancova with disturbance as the continuous variable and treatment (Bare, Vallisneria, Plastic) as the categorical variable showed no significant effects of disturbance on the accumulation of H. verticillata tuber biomass in trays, while treatment effects across the three treatments remained significant (ancova, F32,56 = 0·79, P= 0·76 for overall model, d.f. = 30, P= 1·0 for disturbance and d.f. = 2, P= 0·01 for treatment).

Vallisneria americana grew vigorously in the field experiment, topping out at the water surface and expanding vegetatively beyond the trays. The biomass of V. americana in trays at the end of the growing season ranged between 40 g m−2 and 330 g m−2 and differed among the six sites (anova, F5,24 = 14·42, P < 0·001). Differences in V. americana biomass in trays were negatively correlated with field H. verticillata cover (Spearman rank correlation, rs = –0·83, n = 30, P < 0·001) and biomass (rs = −0·55, n= 30, P= 0·002) at the six sites but not with sunfish disturbance (rs = −0·06, n= 30, P= 0·8).

Propagule pressure hypothesis

The six sites differed in how much H. verticillata tuber biomass was accumulated in trays (anova, F5,83 = 5·74, P < 0·001). Hydrilla verticillata tuber biomass accumulation in trays was positively correlated with existing above-ground H. verticillata biomass at the six sites (Spearman correlation, rs = 0·376, n= 89, P < 0·001). Trays in site 5, one of the high-density sites (Fig. 1), accumulated significantly more H. verticillata tuber biomass than all other sites except for site 4, an intermediate density site (Tukey-Kramer HSD multiple pairwise comparisons, α= 0·05). Thus an ancova found a significant interaction between existing H. verticillata above-ground biomass and treatment at the six sites (F5,83 = 13·59, P < 0·001; Fig. 4).

image

Figure 4. Hydrilla verticillata tuber biomass production (means ± 1 SE) in field mesocosms planted with Vallisneria americana (Vallisneria), plastic Vallisneria look-alikes (Plastic), and an unplanted control (Bare). Treatment responses are reported here as a function of H. verticillata biomass at the six experimental sites. Two sites supported the same biomass (20 g m−2) and data are therefore superimposed.

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greenhouse experiment

Pre-emption and facilitation hypotheses

Vallisneria americana biomass at the end of the experiment ranged between 210 g m−2 and 310 g m−2 among experimental units and did not differ among fragment introduction treatments (anova, F3,12 = 1·13, P= 0·37). The total biomass of H. verticillata increased during the study period in all experimental units that had H. verticillata fragments introduced to them. Analyses on the length and biomass of individual H. verticillata fragments could not be performed because plants unavoidably fragmented during the experiment and at harvesting. Fragments trapped at the surface of containers were able to send roots more than 20 cm through the water column before penetrating the substrate. Based on total accumulated H. verticillata biomass, H. verticillata colonization success was poorest in the Vallisneria treatment (anova, F2,33 = 6·27, P= 0·005). Only one H. verticillata fragment successfully rooted in any of the V. americana planted experimental units, and H. verticillata fragments appeared very chlorotic in these units. In contrast, plastic plants did not decrease H. verticillata colonization success. Across all treatments, H. verticillata fragments that were able to take root were observed to grow more vigorously than non-rooted fragments. Spearman correlations revealed positive correlations between rooted H. verticillata biomass and total H. verticillata biomass (r = 0·83, n= 36, P < 0·001) as well as between rooted H. verticillata biomass and H. verticillata tuber biomass (r = 0·86, n= 36, P < 0·001).

Total nitrogen (anova, F2,12 = 0·48, P = 0·63) and total phosphorous (anova, F2,12 = 2·34, P= 0·14) in the soil pore water did not differ among treatments 12 weeks after planting V. americana in the experimental units. Because few H. verticillata fragments were observed rooting in the Vallisneria treatment, water column nutrients were analysed instead of soil pore water at the end of the experiment to reflect more appropriately the nutrient environment that H. verticillata fragments were encountering. Water column nutrient analyses showed more total nitrogen in the Bare treatment than in the Vallisneria treatment but not the Plastic treatment (anova, F2,12 = 6·89, P= 0·01; Fig. 5). No differences in total phosphorous concentration in the water column were observed among treatments (anova, F2,12 = 0·86, P= 0·45; Fig. 5). Total nitrogen concentrations in the water column were comparable to nutrient concentrations in the field (National Estuarine Research Reserve System, unpublished data; Fig. 5). Total phosphorus concentrations in the field were approximately four times that of the greenhouse experiment. Light was twice as high at the sediment surface in Bare trays and did not differ between the Plastic and Vallisneria treatments (anova, F2,45 = 42·55, P < 0·001).

image

Figure 5. Water column nutrient concentrations in samples extracted from greenhouse mesocosms planted with an unplanted control (Bare), plastic Vallisneria look-alikes (Plastic), and Vallisneria americana (Vallisneria). Total nitrogen (N) was higher in the Bare treatment than in the other two treatments, as shown by using different lowercase letters to denote significant differences (Tukey-Kramer HSD multiple pairwise comparisons, α = 0·05). Total phosphorus (P) did not differ among treatments. For comparison, we show nitrogen and phosphorus concentrations of two water quality monitoring stations at the study site (National Estuarine Research Reserve System, unpublished data). Data shown were collected in 2003 during the study period. One of the stations was unvegetated and one was vegetated. Error bars are means + 1 SE.

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Propagule pressure hypothesis

Increasing propagule numbers enhanced the success of H. verticillata colonization measured as tuber biomass accumulation (anova, F2,41 = 4·32, P= 0·02; Fig. 6) in the Plastic and Bare treatments. No tubers were produced in the Vallisneria treatment irrespective of how many fragments were introduced. Mean tuber biomass across all treatments for one-fragment introductions was 0·34 ± 0·19 g m−2, for 5-fragment introductions 0·68 ± 0·35 g m−2 and for 10-fragment introductions 2·33 ± 0·94 g m−2. The number of H. verticillata fragments added to the experimental units did not affect total nitrogen (anova, F3,11 = 1·86, P= 0·19) or phosphorus (F3,11 = 0·51, P= 0·68) concentrations in the water column.

image

Figure 6. Effects of Hydrilla verticillata propagule load (Fragment number) on the production of H. verticillata tuber biomass (means + 1 SE) in the substrate of greenhouse mesocosms planted with an unplanted control (Bare), plastic Vallisneria look-alikes (Plastic), and Vallisneria americana (Vallisneria). No tubers were produced in the Vallisneria treatment.

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Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The goals of our complementary field and greenhouse experiments were to test whether H. verticillata colonization success is inhibited (pre-emption hypothesis) or facilitated (facilitation hypothesis) by pre-existing vegetation. In a separate experiment, we tested whether H. verticillata colonization is associated with propagule pressure of the invading species (propagule pressure hypothesis). These hypotheses are discussed below to elucidate patterns of H. verticillata invasion, to identify processes explaining the patterns, and to identify an effective management strategy to guard against invasion and invasive species spread.

pre-emption hypothesis

For the pre-emption hypothesis to be supported, we expected the Vallisneria and/or Plastic treatments in the field and greenhouse to decrease H. verticillata colonization compared with the Bare treatment. However, pre-existing live and plastic plants in the field did not decrease H. verticillata colonization, defined as the establishment of standing biomass of the invading species (Fig. 2a). Even when considering H. verticillata tuber biomass production, a more robust measure of colonization success, the Vallisneria and Plastic treatments did not lower H. verticillata colonization in the field (Fig. 2b). However, V. americana biomass and H. verticillata tuber production were negatively correlated in field trays, and tuber production was greater in the Bare treatment than in the Vallisneria treatment in five out of the six experimental sites (Fig. 4), which lends some credence to the pre-emption hypothesis. In contrast, H. verticillata colonization by fragments was virtually prohibited by pre-existing populations of V. americana but was not significantly decreased by plastic plants in the greenhouse experiment (Fig. 6), supporting the pre-emption hypothesis for live plants but not for plastic plants. These results from the greenhouse experiment suggest the hypothesis that pre-emption is driven by nutrient draw-down of live plants (Fig. 5) rather than by plants decreasing light availability under their canopies or imposing a physical barrier that decreases the chances of propagules reaching the sediment surface. Results from the field experiments are less conclusive in supporting the pre-emption hypothesis because continuous nutrient replenishment from tides and river inputs may not allow live plants to draw down nutrients to concentrations that would have an effect on the outcome of competition. Indeed, even though total nitrogen concentrations were comparable, total phosphorus concentrations in the water column were four times higher at vegetated and unvegetated sites in the field than in planted and unplanted greenhouse mesocosms (Fig. 5).

Sediment nutrients are key determinants of the outcome of competition between mature H. verticillata and V. americana plants (Smart, Barko & McFarland 1994; Van, Wheeler & Center 1999). For example, experiments by Van, Wheeler & Center (1999) showed that H. verticillata dominates the competition with V. americana under elevated nutrient conditions. These results are supported by observations within freshwater portions of Chesapeake Bay showing H. verticillata dominating in areas with high pore-water phosphorus concentrations and V. americana dominating in areas of low nutrient concentrations (Wigand, Stevenson & Cornwell 1997). Based on these studies, we predicted that substrate nutrients would be reduced in treatments with V. americana and that this nutrient reduction would decrease the success of H. verticillata colonizing areas dominated by V. americana. Indeed, soil pore water samples from the field collected 16 weeks after planting V. americana showed lower phosphorus concentrations in the Vallisneria treatment than the Bare treatment (Fig. 3) that can only be attributed to uptake of nutrients by V. americana. In contrast, nutrient reduction in the soil pore water of the Plastic treatment (Fig. 3) can only be attributed to uptake by H. verticillata that had colonized.

Nutrient assimilation by the shoots and leaves of submersed plants has been researched less thoroughly than uptake by roots. Madsen & Cedergreen (2002) concluded that submersed vegetation in Danish streams acquires adequate amounts of nitrogen and phosphorus from the water column. Our study shows that water column nitrogen levels were significantly lower in the greenhouse Vallisneria treatment than the Bare treatment (Fig. 5), suggesting nutrient uptake by V. americana. We observed that it took many weeks before H. verticillata fragments were able to root into the substrate, if they were able to at all, suggesting that mineral nutrients in the water column were the only nutrients available to the fragments during this period. Nutrient concentrations in the water column of the greenhouse Vallisneria treatment were lower than in the water column of the vegetated field site (Fig. 5), suggesting that critically low nutrient concentrations may have been reached in the greenhouse but not the field. If water column nutrient concentrations were indeed too low in the Vallisneria treatment to sustain the fragments while they produced roots, then V. americana inhibited colonization in the greenhouse by reducing nutrient concentrations in the water column to lower levels than H. verticillata could survive on. However, the exact nutrient concentrations at which H. verticillata fragments cannot survive for long periods floating in the water column will still need to be tested.

facilitation hypothesis

We expected the Vallisneria and Plastic treatments in the field and greenhouse to enhance H. verticillata colonization compared with the Bare treatment if propagules are physically trapped by plants as they are transported by water currents and waves. Because we introduced a set amount of propagules to greenhouse mesocosms, we expected facilitation to be manifested in the field only. Indeed, significantly more H. verticillata tuber biomass was produced in the Plastic treatment in the field than the other two treatments (Fig. 3b), supporting the facilitation hypothesis. This facilitative effect, in combination with the continuous replenishment of nutrients from tides and river inputs (Wigand et al. 2001), turbulence pushing particles into the canopy (Sand-Jensen & Pedersen 1999; Ghisalberti & Nepf 2002; Herb & Stefan 2005) and potentially high propagule inputs, appears to counteract the competitive effects of live plants observed in the greenhouse. Thus pre-emption effects are probably less clear in the field experiment because of complex interactions between competitive and facilitative effects and the physical estuarine environment.

propagule pressure and timing

We expected greater number of propagules to increase the chance of successful colonization by H. verticillata. Indeed, the propagule pressure hypothesis could not be falsified in either of the two experiments; in both cases higher propagule pressure increased chances of colonization across all treatments. Propagule fluxes were continuous and hence larger over time in the field than in the greenhouse. Thus H. verticillata was more successful in invading trays planted with V. americana in the field than the greenhouse mesocosms. In fact, the Vallisneria treatment in the greenhouse prohibited colonization irrespective of the number of fragments that were introduced; however, the number of propagules introduced may have been too few in the greenhouse to detect an effect of propagule pressure. Timing may have also influenced the results in the field and greenhouse experiments (Grace 1987), where colonization of field mesocosms by H. verticillata conceivably began as soon as mesocosms were placed in the field when V. americana was still immature. On the other hand, propagules were not introduced to greenhouse mesocosms until V. americana had matured in August. Thus V. americana in the greenhouse, in addition to its effects on nutrients in the water column, may have inhibited invasion more completely because of timing effects.

management implications

In his galvanizing book, Elton (1958) draws attention to the tremendous damage non-native species may inflict on ecosystems, human health and economic well-being if they are allowed to colonize new habitats and become dominant in a community. Aware of these threats, managers are faced with the challenge of preventing invasions, eradicating populations in early stages of invasion and controlling populations once they are established (Hulme 2006). The task is daunting and will require integrated management approaches that do not just spray chemicals to keep non-native populations in check but also restore native communities and alleviate extrinsic environmental stressors. Specifically, our study suggests that restoring native species and reducing propagule pressure of non-native species may be effective management objectives that, in combination, decrease the risk of invasion and the chances of spread of a highly invasive submersed aquatic macrophyte species.

Whether the restoration of native communities enhances or decreases the chance of invasion by non-native species depends on whether native species facilitate or compete with non-native species. Thus the simple reintroduction of native species to a system may not always guard against the invasion by non-native species. In our case, however, we are encouraged by the results of our field experiment that suggest that beds of native V. americana are unlikely to have a net positive effect on colonization of H. verticillata because any facilitative effects of fragment trapping are counteracted by competitive effects. Thus restoring native plant beds of V. americana is unlikely to exacerbate problems of invasive species colonization. We are also encouraged by the results that showed that H. verticillata colonization was inhibited by reduced water column nutrients in closed greenhouse mesocosms, which suggests that the efficacy of planting native plants may be enhanced in systems that are relatively closed where internal cycling of nutrients limits nutrient availability. In our estuarine system, which is large and open to nutrient inputs from its watershed and tides, the efficacy of native plant restoration in curbing plant invasions is less certain and can only be useful in combination with a reduction of nitrogen and phosphorus inputs to waterways. While much progress has been made in decreasing nutrient loading in the Chesapeake Bay watershed (Kemp et al. 2005), external nutrient inputs are still too large for native plants to make an appreciable impact on nutrient availability and on curbing non-native plant colonization in our system. These challenges suggest that the mitigation of other environmental pressures (Hulme 2006) besides the biotic pressures imposed by the invading species is often paramount in curbing the success of an invasive species.

Species can dominate suboptimal habitats through high colonization rates maintained by high dispersal and/or high fecundity of a target species (Hastings 1980; Chesson & Warner 1981; Shmida & Ellner 1984). Thus chances of a non-native species establishing at a site that is dominated by native competitors increase when more propagules of the non-native species are introduced to the site. This suggests that propagule pressure needs to be minimized either by creating dispersal barriers or by controlling the source population. Indeed, H. verticillata tuber formation in trays dominated by V. americana was strongly influenced by H. verticillata density in the field, suggesting that reducing the number of H. verticillata fragments through reducing H. verticillata biomass could reduce its colonization success. Plant harvesters are commonly used to control submersed macrophyte biomass in areas where macrophyte biomass is a nuisance to humans or becomes an economic liability. However, the use of harvesters to control H. verticillata is frequently discouraged because the process creates large numbers of fragments that can re-colonize an area or spread the invasion (Owens et al. 2001). As H. verticillata colonization was inhibited in the greenhouse mesocosms through nutrient depletion, harvesters might be a potential control method only when and where water column nutrients are sufficiently low. Herbicides and biotic controls such as grass carp Ctenopharyngodon idella Valenciennes and released insects are alternative methods for controlling H. verticillata and other invasive macrophytes. Grass carp are indiscriminate (Bain 1993; Sutton 1996; Bonar, Bolding & Divens 2002) and illegal in many states, including Maryland. Control of H. verticillata by introduced insects has experienced only some success thus far (Langeland 1996; Allen & Center 1996; Van, Wheeler & Center 1998; Doyle et al. 2002) and is a contentious issue. Herbicides could be used to remove H. verticillata selectively from V. americana without creating fragments, and may be a superior and more cost-effective technology than repeated harvesting at the scale that the herbicides could be used. However, herbicides have limited efficacy in situations where the herbicide can easily be diluted by moving water (Netherland, Green & Getsinger 1991; Fox & Haller 1992; Netherland & Getsinger 1995), have been associated with plant resistance to herbicides over time (Michel et al. 2004; Arias et al. 2005) and are prohibited in many bodies of water such as Chesapeake Bay such that numerous permission requirements would need to be addressed. No approach to reducing propagule pressure is perfect; however, active and cost-effective management (e.g. harvesting and/or herbicides) should be considered to slow the spread of new infestations through decreasing propagule pressure.

In conclusion, the effective management of invasive species will in most cases require an integrated approach that (i) restores native communities to prevent non-native propagules from establishing; (ii) reduces propagule pressure of non-native species to decrease the chance of invasion; and (iii) reduces environmental stressors to enhance the competitive advantage of native species. Thus, just like switching a eutrophic system to a clear-water system dominated by macrophytes (Scheffer et al. 1993), switching a system from a non-native-dominated to a native-dominated state will require careful management of a combination of processes, including competitive dynamics, dispersal and external fluxes of nutrients.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Both authors contributed equally. This research was conducted under a graduate student fellowship awarded to T. B. Chadwell from the Estuarine Reserves Division, Office of Ocean and Coastal Resource Management, National Ocean Service, National Oceanic and Atmospheric Administration, and an award for graduate student support to K. A. M. Engelhardt from the Aquatic Ecosystem Restoration Foundation and the Aquatic Plant Management Society. We thank Julie Bortz, Jodi Brandt, Cindy Giffen, Clayton Kingdon and Madhura Kulkarni for their help in the field. Eva-Maria Koch, Phillip Townsend, Sherry Adams and four anonymous referees provided helpful comments on the manuscript.

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  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
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