Experimental evidence for the effects of additional water, nutrients and physical disturbance on invasive plants in low fertility Hawkesbury Sandstone soils, Sydney, Australia

Authors


M. R. Leishman (tel. +61 29850 9180; fax +61 29850 8245; e-mail michelle.leishman@mq.edu.au).

Summary

  • 1The environmental conditions of a site are thought to influence its invasibility by exotic plants. We tested the effects of physical disturbance, water and nutrient addition on growth and survival of a total of 28 plant species from urban bushland remnants on low fertility Hawkesbury Sandstone soils in Sydney, Australia. Species were classified as native (to Australia, including the local community) or exotic (from outside Australia) and as non-invasive or invasive.
  • 2In a glasshouse experiment the treatments were control (natural soil), added water, added nutrients and added water and nutrients. We found significant differences in response of the plant types to additional nutrients but not to water. Under additional nutrients, exotic invasive species had better survival than all other plant types. There were strong biomass responses to added nutrients for all plant types except native non-invasives. In contrast, the survival and growth of all plant types were similar under control and additional water treatments.
  • 3In a field experiment the factors were site (high and low nutrient soils) and physical disturbance but survival differed between plant types only in relation to site. Exotic species had much better survival than native species at the high nutrient site only. Exotic invasive species had the strongest biomass responses to the high nutrient site while native and exotic non-invasive species showed relatively smaller growth responses.
  • 4Differences between invasive and non-invasive plants were not consistent between exotic and native species. Exotic invasives had greater survival than exotic non-invasives under high nutrient conditions in both experiments, and only exotic invasives showed consistently strong biomass responses to nutrient addition. For native species, there were no differences between invasives and non-invasives in survival in high nutrient conditions in the glasshouse or field; however, only invasive species showed a positive growth response to high nutrient conditions.
  • 5This study provides clear evidence that the success of exotic invasive species in this low fertility vegetation community is facilitated by the addition of nutrients. It would appear that on relatively infertile (particularly phosphorus-limited) sites, invasive species cannot take advantage of additional resources provided by physical disturbance or water addition due to overwhelming nutrient-limitation. We suggest that a combination of the environmental conditions (nutrient-enrichment) and invading species having traits that allow high survival and faster growth in response to nutrients, may allow successful invasion in Hawkesbury Sandstone communities.

Introduction

Understanding the mechanisms that determine successful invasion of a community by introduced plants is an important area of ecological research and is of both theoretical and applied interest. Successful invasion depends on a number of factors, including the attributes of the invaders, the characteristics of the community and propagule availability (Lonsdale 1999). In this paper we focus on the environmental conditions of the site as a determinant of success of exotic and invasive plant species in the low fertility Hawkesbury Sandstone vegetation communities of Sydney, Australia.

There are several environmental factors that are thought to contribute to community invasibility, including removal of biomass associated with physical disturbance, changes to natural disturbance regimes and resource enrichment (D’Antonio et al. 1999). There is substantial correlative evidence that invasion by exotic plants is associated with physical disturbance such as construction of tracks, roads and buildings (Knops et al. 1995; Kotanen et al. 1998; Fine 2002; Ross et al. 2002). Changes to flooding frequency (Hood & Naiman 2000; Brown & Peet 2003), and grazing and fire regimes (see D’Antonio et al. 1999 for a comprehensive review) may also facilitate invasion. High nutrient availability (either natural conditions or enriched by human activities) is also strongly correlated with invasion success in a wide variety of vegetation communities (Fogarty & Facelli 1999; Stohlgren et al. 1999; Kalkhan & Stohlgren 2000; Li & Norland 2001; King & Buckney 2002; Kolb et al. 2002; Ostertag & Verville 2002; Bashkin et al. 2003; Lake & Leishman 2004).

Experimental studies have manipulated a range of factors to assess their relative importance for invasion success. Burke & Grime (1996) manipulated fertilizer and soil disturbance along gradients in limestone grassland and showed that invasion was strongly related to availability of bare ground, but that invasion was most successful where both availability of bare ground and nutrients were high. Similar results were found by Hobbs & Atkins (1988) for exotic plants in woodland and shrubland remnants in western Australia. Other studies have shown that different combinations of factors such as physical disturbance and high water availability (White et al. 1997; Davis & Pelsor 2001), and physical disturbance, fire and nutrients (Gentle & Duggin 1997; Duggin & Gentle 1998), enhance success of invasive plants. Some studies have manipulated only single factors such as biomass removal (Rachich & Reader 1999) or soil nutrients (Huenneke et al. 1990) and found positive correlations with invasion success. However, the links between invasion success and environmental factors such as physical disturbance, enhanced water and nutrient availability are not yet adequately understood (D’Antonio et al. 1999), with relatively few studies examining several disturbance factors for large numbers of species within a community.

In this study, we report on the effect of physical disturbance, water and nutrient addition on growth and survival of 28 exotic and native plant species that are typical of urban bushland remnants on Hawkesbury Sandstone-derived soils in Sydney, Australia. Australia is a particularly good place to study invasions due to its isolation as an island continent and consequent unique and largely endemic biota. In the Sydney region, there are substantial areas of natural bushland remaining. Many of these bushland reserves are on soils derived from Hawkesbury Sandstone, where the soil infertility and steep topography have precluded development (Benson & Howell 1990). Hawkesbury Sandstone soils are shallow, with low water-retaining capacity and are noted for their low nutrient concentrations, in particular of phosphorus (typically 30–80 mg kg−1, Beadle 1962). These soils support a variety of vegetation communities, including heathland, shrubland and woodland, and are species-rich, with over 1500 native plant species recorded (Benson & Howell 1990). Early work by Beadle (1962) showed that soil phosphate was the major factor delimiting these plant communities. The vegetation is subject to relatively frequent fire and consequently native species have a range of mechanisms to survive regular biomass removal from fire.

The bushland reserves of Sydney's urban areas are subject to a variety of changed environmental conditions due to their proximity to development, including physical disturbance at the edges and along tracks, and water and nutrient addition from urban stormwater runoff. Earlier observational studies in these vegetation communities have shown that reserves subject to nutrient enrichment are highly invaded by exotic species (Clements 1983; Riley & Banks 1996; King & Buckney 2002; Lake & Leishman 2004), while areas of physical disturbance only generally do not support exotic plants (Lake & Leishman 2004).

Here we present results from complementary manipulative glasshouse and field experiments to test hypotheses that invasive plants have stronger survival and growth responses than non-invasives when subjected to disturbance factors that are thought to be associated with invasion in this community: (i) when grown with additional water; (ii) when grown with additional nutrients; and (iii) in physically disturbed conditions. Species were classified as: (i) native to the community and non-invasive; (ii) native to Australia (the Sydney region or elsewhere) and invasive; (iii) exotic (i.e. introduced from outside Australia) and non-invasive; and (iv) exotic and invasive. Few previous studies have separated native and exotic species into invasive and non-invasive (but see Smith & Knapp 2001; Lake & Leishman 2004).

Methods

glasshouse experiment. the effect of additional water and nutrients on invasive and non-invasive native and exotic plants

Study species

Seventeen plant species were selected a priori from four categories (Table 1): plant species native to Hawkesbury Sandstone vegetation and non-invasive (native non-invasive); species native to Australia (including the Sydney region) but considered to be invasive in Sydney (native invasive); species exotic to Australia that are common invaders in Hawkesbury Sandstone vegetation (exotic invasive); and species exotic to Australia that are naturalized in Sydney, but are not currently considered invasive (exotic non-invasive). We included the category native invasive as many plants that have been introduced to the Sydney region from other parts of Australia for horticultural reasons have become invasive. The climate and soil conditions of the natural ranges of such species are very similar to the conditions experienced in the Sydney region and most of the species are from families, and even genera, represented in the native Hawkesbury Sandstone flora. Consequently, we believe that these should be considered separately from invasive species from outside Australia.

Table 1.  Species used in both the glasshouse and field experiments. Each species was classified as either native non-invasive (native NI), native invasive (native I), exotic non-invasive (exotic NI) or exotic invasive (exotic I)
SpeciesFamilyGrowth formPlant typeSeed reserve mass (mg)Experiment
Acetosa sagittata (Thunb.) L.A.S. Johnson & B.G. BriggsPolygonaceaeClimberExotic I  1.601
Asparagus aethiopicus L.AsparagaceaeHerbExotic I 38.871
Bidens pilosa L.AsteraceaeHerbExotic I  0.501, 2
Cortaderia selloana (Schult. & Schult.f) Asch. & Graebn.PoaceaeGrassExotic I  0.111
Cotoneaster glycophyllus Franch.MalaceaeShrub/small treeExotic I  0.532
Foeniculum vulgare Mill.ApiaceaeHerbExotic I  2.511, 2
Ligustrum sinense Lour.OleaceaeShrubExotic I 11.511, 2
Senna pendula (Willd.) H.S. Irwin & BarnebyFabaceae – CaesalpinioideaeShrubExotic I 18.502
var. glabrata (Vogel) H.S. Irwin & Barneby     
Sida rhombifolia L.MalvaceaeHerbExotic I  1.612
Sonchus oleraceus L.AsteraceaeHerbExotic I  0.162
Verbena bonariensis L. var. bonariensisVerbenaceaeHerbExotic I  0.072
Agapanthus praecox Willd. ssp. orientalis (F.M. Leight.) F.M. Leight.AlliaceaeHerbExotic NI  6.501
Canna indica L.CanaceaeHerbExotic NI 72.21, 2
Dietes bicolor Sweet ex G. DonIridaceaeHerbExotic NI 15.531, 2
Erythrina crista-galli L.Fabaceae – FaboideaeTreeExotic NI187.341, 2
Acacia baileyana F. Muell.Fabaceae – MimosoideaeTreeNative I 19.302
Acacia saligna (Labill.) H.L. Wendll.Fabaceae – MimosoideaeShrubNative I 11.901, 2
Grevillea robusta A. Cunn. ex R. Br.ProteaceaeTreeNative I 10.112
Paraserianthes lophantha (Willd.) I.C. Nielsen ssp. lophanthaFabaceae – FaboideaeShrub/small treeNative I 32.382
Pittosporum undulatum Vent.PittosporaceaeTreeNative I  4.911, 2
Acacia linifolia (Vent.) Willd.Fabaceae – MimosoideaeShrubNative NI  8.302
Allocasuarina distyla (Vent.) L.A.S. JohnsonCasuarinaceaeShrubNative NI  0.972
Banksia ericifolia L.f. ssp. ericifoliaProteaceaeShrubNative NI 15.601, 2
Bossiaea heterophylla (Vent.)Fabaceae – FaboideaeHerbNative NI  8.301
Casuarina glauca Sieber ex Spreng.CasuarinaceaeTreeNative NI  0.261
Eucalyptus sclerophylla (Blakely) L.A.S. Johnson & BlaxellMyrtaceaeTreeNative NI  0.351
Hakea dactyloides (Gaertn.) Cav.ProteaceaeShrubNative NI 15.272
Hardenbergia violacea (Schneeve.) SternFabaceae – FaboideaeClimberNative NI 30.671, 2

Species were classified as invasive or non-invasive using the criteria developed by Lake & Leishman (2004). Invasive species were those listed as problem weeds (e.g. Buchanan 1981; Robinson 1991), occurring widely and locally dominant. Exotic non-invasives were those species that are found in isolated populations in low abundance only. These classifications were verified by bushland field officers from local councils. We tried to ensure when selecting species that each plant category contained a range of growth forms, although inevitably the native categories were dominated by woody perennial species while the exotic categories were dominated by climbers and herbs. This simply reflects the nature of the common native and exotic species of this community. We attempted to account for this by including the term species within each plant type for the statistical analyses.

In order to avoid concerns that our results were dependent on the definition of exotic used, we also analysed the data using only three categories: native, exotic non-invasive and exotic invasive. For this classification, exotic was defined as any species introduced from outside the Sydney region. The results from these analyses were not substantially different from those using the original four categories (see Results). However, as this analysis does not allow us to assess consistent differences between invasive and non-invasive species or differences between exotic invasive and native invasive species, only results from analyses based on four plant types are discussed.

Experimental design

Seeds were collected from a variety of individuals at different locations throughout Sydney bushland or were from commercial seed suppliers who collect from the Sydney region. Seeds of all species were set to germinate in moist Petri dishes at varying times to ensure that all germinated seeds were at the same stage of development at the time of planting. Heat treatments or scarification to promote germination were used as required. Germinated seeds (radicle just emerged) were planted into pots (one per pot) in a temperature-controlled glasshouse at Macquarie University during one week in October 2001. Pots measured 10 cm in diameter by 13 cm depth and contained an equal mix of river sand and Hawkesbury Sandstone soil collected from Lane Cove National Park. The Hawkesbury Sandstone soil was mixed with river sand as the amount of soil available was limited. However, analyses of the Hawkesbury Sandstone soil compared with the soil/river sand mix showed no difference in total P content. Seedlings were allocated to one of four treatments, with 15 replicates of each species in each treatment. The treatments were control (C), added water (W), added nutrients (N) and both added water and nutrients (WN). The C treatment was simply natural Hawkesbury Sandstone soil with minimal water provided for plant growth in the glasshouse. The W, N and WN treatments were designed to increase water and nutrient availability to levels consistent with soils receiving nutrient-rich stormwater runoff (e.g. adjacent to urban creeks or below stormwater outlets at the residential/bushland interface). Treatments were as follows: C, watered with 125 mL water per pot twice weekly; W, watered with 125 mL water per pot four times weekly; N, as for C plus approximately 0.5 g of complete fertiliser (N : P : K ratio – 23 : 4 : 18; Aquasol™; Hortico, Arthur Yates & Company, Homebush, NSW, Australia) once per week; WN, as for W plus approximately 0.5 g complete fertiliser (Aquasol™) once per week. The treatments were continued for 7 weeks before harvesting, by which time mortality had stabilized. The maximum and minimum temperatures in the glasshouse during this time were 27.4 °C and 16.2 °C, respectively.

Measurements

The survival of seedlings was recorded weekly. After 7 weeks, remaining plants were harvested and the roots and shoots washed free of soil. Maximum root and shoot lengths were measured to the nearest 0.5 cm, then roots and shoots were separated and oven-dried at 60 °C for 48 hours before weighing. Leaf samples were then ground finely, and analysed for total percentage of nitrogen by the dry combustion method using a Leco CHN-900 Analyser (Leco Corporation, St Joseph, USA). One mature leaf was randomly selected and removed from each plant before drying and its area (measured with a flat-bed scanner and image analysis software, DELTA-T, Cambridge, UK) and dry weight were determined separately in order to calculate specific leaf area. Due to mortality, this resulted in 2–15 replicates per species per treatment. Soil was taken from five pots in each treatment of 10 different species (Banksia, Casuarina, Hardenbergia, Acacia, Pittosporum, Acetosa, Bidens, Ligustrum, Canna and Erythrina) in order to determine the soil phosphorus concentrations of each treatment. Soil samples were bulked for treatment and analysed for total P using an acid digestion method (Murphy & Riley 1962). We chose to measure total P as it incorporates both organic and inorganic forms, providing a more stable and replicable measure of soil P than available P. Furthermore, total P provides a comparable measure with previous work on enhanced nutrients in urban bushland soils on Hawkesbury Sandstone (e.g. Clements 1983; Leishman 1990; King & Buckney 2002; Leishman et al. 2004).

Statistical analysis

Percentage survival was analysed using repeated measures analysis of variance, with week of measurement as the repeated factor. All other variables were analysed using mixed model anova. The fixed factors for all analyses were nutrient treatment (additional nutrients or not), water treatment (additional water or not) and plant type (native non-invasive, native invasive, exotic non-invasive and exotic invasive), while species (nested within plant type) was included as a random factor. All interactions between these factors were included in the analyses. However, possible effects of growth form were not tested directly. When we found a significant interaction (at P < 0.05) between species (within plant type) and nutrient treatment, each plant type was analysed in a separate anova with species and nutrient treatment as factors. No significant interactions between species (within plant type) and water treatment were found. All variables were examined for normality and heterogeneity of variance and log transformed when necessary. Analyses were performed using SPSS Version 11.0 (SPSS, November 2001).

field experiment. the effect of physical disturbance and elevated soil nutrients on invasive and non-invasive native and exotic plants

Experimental design

We conducted a factorial experiment at two sites in the Ecology Reserve at Macquarie University. The natural vegetation is low woodland, dominated by species of Eucalyptus, Banksia, Grevillea and Hakea and the soil is derived from Hawkesbury Sandstone and is shallow and infertile, with low water-retaining capacity. However, within a section of the Reserve there is an area of introduced soil fill, associated with the construction of a road decades previously, that is relatively fertile and supports largely exotic vegetation, such as Solanum mauritianum, S. nigrum, Ligustrum sinense, Verbena bonariensis and Sida rhombifolia. The soil in this area has a greater silt and organic matter content than the surrounding sandstone soil, with greater water-retaining capacity. The site is located adjacent to a drainage line that contains stormwater runoff after significant rain from the sports fields upslope. We describe the two sites as low and high nutrient; however, it is likely that the high nutrient site also had higher soil moisture due to its topographic location and texture. In order to minimize any moisture differences between the two sites, we watered all plots regularly throughout the experiment.

We grew 21 plant species (Table 1) selected a priori from four categories (native non-invasive, native invasive, exotic non-invasive and exotic invasive) under all combinations of site (nutrient level) and physical disturbance (disturbed or not). As for the glasshouse experiment, we attempted to ensure that all growth form types were represented within each plant type.

The experiment was a random block design within site where the sites were low and high nutrient soils. Within each site, 10 plots were marked out with five plots randomly allocated to the physical disturbance treatment and five plots left undisturbed. Within each plot there were three replicates of each of the 21 species. Each plot measured 1 × 1 m and was surrounded with wire netting to exclude large herbivores such as rabbits and possums. For disturbed plots we removed all above-ground biomass and dug the soil to a depth of 5 cm using a small trowel and hoe a few days before planting. Disturbed plots were kept clear of other biomass throughout the experiment. This disturbance was intended to simulate the physical disturbance associated with construction of tracks and power-line easements. Soil samples to a depth of 10 cm were taken adjacent to each plot and bulked within treatments. Soil was air-dried, sieved at 2 mm and analysed for total P using an acid digestion method (Murphy & Riley 1962).

Seeds of all species were set to germinate in moist Petri dishes to ensure that all germinated seeds were at the same stage of development at time of planting, as for the glasshouse experiment. Seeds were planted into plots over 7 days from 9 August 2002. Germinated seeds were planted 10 cm apart along rows at a depth of 5–10 mm, with each row separated by 10 cm. Planting positions for all seeds within plots were randomly allocated. We watered each plot with 10 L of water twice a day for the first week and then 10 L of water three times per week for the remainder of the experiment.

Emergence and survival of each seedling was monitored weekly for 14 weeks. At 13 weeks post-planting, all seedling heights (to apical meristem for dicots and to tip of longest leaf for monocots and Foeniculum) were recorded to the nearest 5 mm. At the end of 14 weeks all surviving seedlings were harvested, separated into roots and shoots, then oven-dried at 60 °C for 48 hours and weighed.

Statistical analysis

All variables were analysed using mixed model anova. The fixed factors were site (low nutrient or high nutrient), physical disturbance (physically disturbed or not) and plant type (native non-invasive, native invasive, exotic non-invasive and exotic invasive). Species (nested within plant type) was included as a random factor. All interactions between these factors were included in the analyses. Plant types were not analysed separately as no significant interactions between species (within plant type) and site or physical disturbance were found. All variables were examined for normality and heterogeneity of variance and log transformed when necessary. Analyses were performed using SPSS Version 11.0 (SPSS, November 2001).

Results

glasshouse experiment. the effect of additional water and nutrients on invasive and non-invasive native and exotic plants

Soil total P concentrations for each of the treatments were: C, 84 ± 2 mg kg−1; W, 86 ± 2 mg kg−1; N, 152 ± 6 mg kg−1; and WN, 153 ± 8 mg kg−1.

Survival

In order to test the hypotheses that there are differences in responses to added nutrients and water among plant types, we looked for significant interactions between plant types and treatment. We found a significant interaction between nutrient treatment, plant type and week (F15,260 = 1.85, P = 0.028) for plant survival. Under both the C and W treatments, survival of all plant types was high and did not change with time, although exotic non-invasive species generally had lower survival than the other plant types (Fig. 1). Under both treatments with additional nutrients (N and WN), survival of all plant types declined with time, suggesting that the high nutrient availability or some other factor was causing mortality. In the N treatment, the plant type with the highest survival was exotic invasives, followed by exotic non-invasives, then native invasives, with native non-invasive species having the lowest survival with additional nutrients. However in the WN treatment, survival of exotic non-invasives, native invasives and native non-invasives was similar, while survival of exotic invasives was much higher.

Figure 1.

Proportion of seedling survival (mean ± SE) over time for each of the four treatments (control, added water, added nutrients, added water and nutrients) for the glasshouse experiment. The scales of x- and y-axes are the same for all panels. Lines represent different plant types (native non-invasive = solid line, open triangle; native invasive = solid line, closed triangle; exotic non-invasive = dashed line, open circle; exotic invasive = dashed line, closed circle).

Growth

There was a weak but non-significant interaction between plant type and nutrient treatment (nutrient × plant type F3,13 = 3.20, P = 0.058) for total biomass. Figure 2 illustrates differences in response to added nutrients among the four plant types, with native non-invasive species showing negligible biomass increases compared with the other plant types, particularly the exotic invasives. Overall there were significant differences in total biomass between the treatments, with plants grown with both additional water and nutrients showing the strongest response (nutrient × water F1,12 = 21.38, P = 0.0006). The results for total biomass largely reflected the results for shoot biomass. There was a significant interaction between nutrient and plant type (F3,13 = 4.29, P = 0.025), with native non-invasive species showing much smaller increases in shoot biomass with additional nutrients or additional water and nutrients compared with the other plant types (Fig. 2). Similarly, the greatest shoot growth response was due to the combination of additional water and nutrients (nutrient × water F1,12 = 14.78, P = 0.002). There was also a significant nutrient × species (plant type) interaction (P = 0.015) for shoot biomass, with significant variation in species responses to additional nutrients within each of the plant types where analysis was possible: exotic invasive (F5,299 = 45.45, P < 0.0001), exotic non-invasive (F3,139 = 26.16, P < 0.0001), and native non-invasive (F4,177 = 21.93, P < 0.0001). Only two native invasive species were studied and Acacia showed a large increase in shoot biomass in response to nutrients, whereas Pittosporum had a much smaller increase, similar to that of the native non-invasive species. For the other three plant types we could not detect any pattern in response in relation to growth form; however, low numbers within each plant type make this problematic. There were no significant interactions between plant type and treatment for shoot length. Shoot length responded positively overall to the WN treatment only (nutrient × water F1,9 = 10.82, P = 0.009).

Figure 2.

Seedling biomass after 7 weeks for each plant type in each treatment in the glasshouse experiment. Shaded portion of bar represents the mean root biomass; unshaded portion of bar represents the mean shoot biomass. Error bars represent one standard error of mean total biomass.

For root biomass there was a weak but non-significant interaction between plant type and nutrient treatment (nutrient × plant type F3,14 = 3.19, P = 0.057) and root biomass responded overall to nutrient addition only (F1,14 = 12.29, P = 0.003). Interestingly, exotic invasive species had generally higher root : shoot ratios than other plant types (F3,14 = 6.22, P = 0.007, Fig. 3), although there were no significant plant type × W (F3,108 = 0.34, P = 0.79) or plant type × N (F3,13 = 0.81, P = 0.51) interactions.

Figure 3.

Ratio of root biomass : shoot biomass (mean + 1 SE) after 7 weeks growth for each plant type in each treatment in the glasshouse experiment.

Leaf traits

Specific leaf area did not differ significantly among plant groups (plant type F3,9 = 2.8, P = 0.09); however, there was an apparent trend of lower specific leaf area for the native species. Specific leaf area did not vary significantly among treatments (nutrient F1,9 = 0.28, P = 0.59; water F1,9 = 0.03, P = 0.87). Not surprisingly, leaf nitrogen was greatest with additional nutrients (F1,9 = 40.52, P = 0.0001), but there were no differences overall in leaf nitrogen between plant types (F3,9 = 0.41, P = 0.76), nor did leaf nitrogen vary among plant types (nutrient × plant type F3,9 = 0.61, P = 0.62).

field experiment. the effect of physical disturbance and elevated soil nutrients on invasive and non-invasive native and exotic plants

Soil total P concentrations measured 32–37 mg kg−1 for the low nutrient site and 200–210 mg kg−1 for the high nutrient site

Survival

There were significant differences in survival of the plant types in relation to soil fertility (site × plant type F3,22 = 8.75, P = 0.0005) but not physical disturbance (physical disturbance × plant type F3,22 = 0.07, P = 0.98). Native non-invasive and native invasive species showed no difference in survival among the treatments, or possibly a slight decline with high soil nutrients (Fig. 4). In contrast, exotic non-invasive and exotic invasive species had much higher survival on the high nutrient site, irrespective of physical disturbance.

Figure 4.

Percentage seedling survival (mean + 1 SE) after 14 weeks for each plant type in each treatment (low nutrient/not physically disturbed, low nutrient/physically disturbed, high nutrient/not physically disturbed, high nutrient/physically disturbed) in the field experiment.

Growth

There were significant differences in total biomass among plant types grown on the different sites (site × plant type F3,13 = 4.59, P = 0.02), with exotic invasive species showing the strongest biomass responses to high nutrient soil. Native invasive species had a relatively small increase in biomass in the high nutrient soil while the other two plant types showed little biomass response to differences in soil fertility (Fig. 5). The results were similar for shoot biomass (site × plant type F3,13 = 4.34, P = 0.03) and shoot height (site × plant type F3,15 = 13.60, P = 0.0002) but not for root biomass (site × plant type F3,13 = 1.14, P = 0.34). Exotic non-invasives generally had the largest biomass of the four plant types under all treatments but not greater shoot length. Root and stem biomass were greatest across plant types grown in high nutrient and physically disturbed conditions (root biomass, disturbance × site F1,17 = 5.27, P = 0.03; shoot biomass, disturbance × site F1,11 = 57.89, P = 0.02).

Figure 5.

Seedling biomass after 14 weeks growth for each plant type in each treatment in the field experiment. Shaded portion of bar represents the mean root biomass; unshaded portion of bar represents the mean shoot biomass. Error bars represent one standard error of mean total biomass.

comparison with analyses of three plant types

The pattern of results was very similar when three rather than four plant types were used. However, some marginally non-significant results became significant (e.g. glasshouse biomass for nutrient × plant type, glasshouse specific leaf area for plant type), while the significance of other results was considerably reduced (glasshouse root : shoot ratio). Importantly, significant interactions for plant type were again found only with nutrient level (glasshouse experiment) or site type (field experiment), thus confirming that there were differences in the response of the plant types to nutrient levels but not water addition or physical disturbance.

Discussion

differences among plant types in their response to physical disturbance, additional water and nutrients

In this study we tested a number of hypotheses on the success of invasive and non-invasive plants subject to physical disturbance, water and nutrient addition. We found no evidence from the glasshouse experiment for our first hypothesis, that invasive plants have stronger survival and growth responses than non-invasives when grown with additional water. There were no differences in survival or biomass of any of the plant types (native non-invasive, native invasive, exotic non-invasive and exotic invasive) when grown with additional water compared with control conditions. It is possible that the soil moisture availability of the control treatment in the glasshouse was greater than normal field conditions, resulting in no clear difference between control and additional water treatments. However, given the low water retention capacity of the soil used in the experiment and the low frequency of watering of the control, we do not believe this to be the case. Furthermore, pots with the additional water treatment were constantly damp, which we believe is similar to the conditions in the field for soils receiving stormwater runoff. This suggests that in relatively infertile communities, such as the Sydney sandstone vegetation, invasive species are unable to take advantage of additional water due to the overwhelming nutrient limitation of the system.

There have been surprisingly few experimental studies that have shown that invasion success of exotic species is positively related to soil moisture, independent of other factors. Davis & Pelsor (2001) manipulated water and physical disturbance in old fields at Cedar Creek and found that one species of the three studied had increased invasion success with water addition independent of physical disturbance. Many sites within conservation reserves receive additional water through runoff generated by impervious surfaces such as roads and paved areas. Such sites are often subject to invasion by exotic plants (Knops et al. 1995; Kotanen et al. 1998; Gelbard & Belnap 2003). However, our results suggest that additional soil moisture is unlikely to be sufficient to facilitate success of exotic species in nutrient-limited vegetation types.

The second hypothesis tested was that invasive plants have stronger survival and growth responses than non-invasives when grown with additional nutrients. Both the glasshouse and field experiment provided strong evidence that exotic invasives had the highest survival rates compared with other plant types when grown in nutrient-enriched conditions, but native invasives did not differ from native non-invasives. Exotic species generally had higher survival rates than natives in nutrient-enriched conditions. The glasshouse experiment showed that all plant types except native non-invasive species had strong growth responses to added nutrients, while in the field only exotic invasives showed dramatic growth responses to additional nutrients. Exotic plants, whether invasive or non-invasive, had larger biomass and greater shoot length than native non-invasives in both the glasshouse and field experiments. In summary, not all invasive plants reacted strongly to nutrient addition, with only exotic invaders showing consistently strong responses. Thus it would appear that on the relatively infertile Hawkesbury Sandstone soils of the Sydney region, nutrient addition facilitates the success of exotic invaders. Further, exotic species that are naturalized but not currently invasive, may not become problem invaders in the future without changes in environmental conditions or phenotypes.

Thomson & Leishman (2004) showed that nutrient additions of 0.27 g P week−1 in a complete soluble fertilizer for 6 weeks (resulting in total P concentration of 260 mg kg−1) resulted in 100% mortality of native species grown in Hawkesbury Sandstone soils. Leishman et al. (2004) have shown that sites in Hawkesbury Sandstone vegetation with soil total P concentrations greater than 350 mg kg−1 have exotic plant cover of more than 80%. The decline in survival of all plant types grown in the additional nutrient treatment in the glasshouse therefore suggests that nutrient levels were higher than indicated by the results for soil total phosphorus. However, total P of stormwater-affected Hawkesbury Sandstone soils has been recorded at concentrations of up to 900 mg kg−1 (Leishman et al. 2004), suggesting that although soil P availability was higher in the glasshouse than the total P measurements indicated, the nutrient additions were not unrealistic compared with field conditions.

Within each of the four plant types in both experiments we used a range of growth forms. However, the nature of the common species for each plant type in the Hawkesbury Sandstone community resulted in some biases, for example exotics were dominated by herbs while natives were dominated by shrubs. On only two occasions did we find significant interactions between a factor and species within plant type and in neither of these cases could we discern a pattern of response in relation to growth form. Thus we do not believe that our results in relation to plant type were determined by their growth form mix, although we could not test this directly.

Our results are consistent with a number of published studies showing that exotic plant invasions are more common on naturally high-nutrient or nutrient-enriched soils (see Introduction) or that invasion by exotics is more successful where nutrients have been added experimentally (Hobbs & Atkins 1988; Huenneke et al. 1990; Burke & Grime 1996). Previous studies describing experiments where exotic and native species have been grown at varying nutrient levels have also shown that exotic species such as Tamarix ramosissima in riparian systems (Marler et al. 2001), Vulpia bromoides and Echium plantagineum in Eucalypt woodlands (Allcock 2002) and exotic composites in western Australia (Milberg et al. 1999) show greater positive growth responses to high nutrient concentrations than do native species (but see Lowe et al. 2002).

Physical disturbance (hypothesis 3) was found not to provide a relative advantage in survival or growth for invasive compared with non-invasive species. We have treated each of the factors physical disturbance, additional water and nutrients as being independent of each other in these experiments. However, this may not be the case, for example physical disturbance results in increased light on the soil surface and the removal of the boundary layer effect of the vegetation, which may result in reduced topsoil moisture. We attempted to mitigate this in the field experiment by regularly applying water to all plots. Similarly, in some systems additional water or physical disturbance may affect nutrient availability by allowing microbially mediated soil processes to take place. However, in this low fertility sandy soil, phosphorus is the limiting nutrient (Beadle 1962) and is supplied through inorganic forms, and thus is unlikely to be affected by water addition or physical disturbance. Finally, biomass removal associated with physical disturbance may increase nutrient availability by reducing demand. However, the very low concentrations of phosphorus available for plant growth in this system suggests that the additional phosphorus made available would be minimal. This suggests that vegetation communities on phosphorus-limited soils should be resilient to invasion generally, by either exotic or native species. In fact, Lake & Leishman (2004) found in a widespread survey of Hawkesbury Sandstone communities in the Sydney region that sites with only physical disturbance (i.e. adjacent to tracks) did not support exotic or native invasive plants, with the exception of one exotic species, Andropogon virginicus. Furthermore, these vegetation communities have well-developed mechanisms to survive regular fire and consequent biomass removal. Previous work has shown that fire in these communities does not facilitate invasion by exotic species (Thomson & Leishman, in press). Previous experimental studies that have manipulated physical disturbance have found that invasion is most successful where physical disturbance is combined with another factor, such as nutrient addition (Burke & Grime 1996) or high water availability (White et al. 1997), or in areas that are naturally high in nutrients such as wetlands (Rachich & Reader 1999). Thus it would appear that physical disturbance alone in communities limited by other resources such as low soil phosphorus does not facilitate invasion by exotic plants.

Several previous studies have suggested that a combination of different factors (such as physical disturbance, water addition or nutrient addition) results in greater success of exotic invaders (Burke & Grime 1996; Gentle & Duggin 1997; White et al. 1997; Duggin & Gentle 1998). We found that the combination of additional water and nutrients resulted in largest total biomass, shoot biomass and shoot length across all plant types in the glasshouse experiment, while the combination of additional nutrients and physical disturbance resulted in the largest root and shoot biomass across all plant types in the field experiment. However, we only found significant interactions between plant type and nutrient condition in the two experiments, suggesting that it is not the combination of different factors (nutrient addition plus water addition or physical disturbance) that provides an advantage to exotics compared with natives, but simply nutrient addition alone.

Our results are largely consistent with the fluctuating resource hypothesis of invasibility proposed by Davis et al. (2000). Davis et al. (2000) suggest that a plant community is more susceptible to invasion when there is an increase in the amount of unused resources. Our results suggest that an increase in nutrient resources in the low fertility sandstone vegetation communities of Sydney does result in success of invasive exotic species, because these species have better growth and survival with additional nutrients compared with other plant types. However, the inherent nutrient limitation of these communities means that an increase in resources such as additional water or those associated with physical disturbance does not result in successful invasion, as even invasive species are unable to respond to the increased resources at such low rates of nutrient supply.

trait differences among plant types

Exotic species, particularly invasives, had significantly higher root : shoot ratios across all treatments, suggesting that they allocate relatively more to foraging for soil resources than other plant types. The trend, albeit non-significant, to greater specific leaf area in exotic species, is consistent with previous work on species of Hawkesbury Sandstone vegetation communities, which has found higher specific leaf area and foliar nitrogen and phosphorus in exotic species compared with natives (Haslehurst 2002; Lake & Leishman 2004). Large specific leaf area is among the suite of attributes (also including high photosynthetic capacity, high foliar nitrogen and short leaf lifespan, Reich et al. 1997) that is associated with fast growth. Such attributes of exotic plants have been found to differ consistently from co-occurring natives in a range of other habitats (Pattison et al. 1998; Baruch & Goldstein 1999; Durand & Goldstein 2001; Smith & Knapp 2001; Grotkopp et al. 2002), suggesting that fast growth under non-limiting conditions may contribute to the success of some exotic species.

Few previous studies have separated native and exotic species into invasive and non-invasive. Smith & Knapp (2001) examined 13 traits of two exotic invasive, five exotic non-invasive and six native species but did not find consistent differences between invasive and non-invasive exotic species, although this may have been due to the small numbers of species. Lake & Leishman (2004) studied nine traits of exotic invasive, exotic non-invasive and native species from Sydney Hawkesbury Sandstone communities and found that exotic invasives had consistently larger specific leaf area than exotic non-invasive species. Interestingly, the rather smaller difference found here did not translate to greater biomass under high nutrient conditions.

In summary, we found strong evidence that the success of invasive exotic species in these low fertility vegetation communities may be facilitated by the addition of nutrients. Other work in these communities has shown that exotic species are not limited by seed availability (King & Buckney 2001), that nutrient concentrations that are typical of such sites result in high mortality of native species (Thomson & Leishman 2004) and that exotic species are largely confined to areas of nutrient enrichment (Lake & Leishman 2004). Thus we suggest that a combination of the environmental conditions (nutrient-enrichment) and invading species having traits that allow high survival and, possibly, faster growth in response to nutrients, may allow successful invasion in this community.

Acknowledgements

We thank Lane Cove National Park for providing soil for the glasshouse experiment. We also thank the following people for assisting with glasshouse work or fieldwork: Megan Covey, Sarah Hill, Adele Norman, Bethany Puffett, Angela Sinclair and Zoe Summerville. Dave Warton provided helpful statistical advice and Angela Moles, Ian Wright and three anonymous referees provided constructive criticism of the manuscript. This research was funded by an Australian Research Council Queen Elizabeth II Fellowship and Large Grant to Leishman.

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