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. 2017 Dec 22;121(3):561–569. doi: 10.1093/aob/mcx172

A greater foraging scale, not a higher foraging precision, may facilitate invasion by exotic plants in nutrient-heterogeneous conditions

Bao-Ming Chen 1,2,3,✉, Jin-Quan Su 1,2,3, Hui-Xuan Liao 1,2,3, Shao-Lin Peng 1,2,3,✉
PMCID: PMC5838839  PMID: 29309538

Abstract

Background and Aims

Soil nutrient heterogeneity has been proposed to influence competitive outcomes among different plant species. Thus, it is crucial to understand the effects of environmental heterogeneity on competition between exotic invasive and native species. However, the effects of soil nutrient heterogeneity on the competition between invasive and native plants have rarely been linked to root foraging behaviour.

Methods

In this study, a competition experiment was performed with two invasive–native species pairs (BP–VC, Bidens pilosa vs. Vernonia cinerea; MM–PS, Mikania micrantha vs. Paederia scandens) grown under homogeneous and heterogeneous conditions in a common greenhouse environment. Root activity was assessed by determining the amount of strontium (Sr) taken up by the shoot of each species.

Key Results

The invasive species exhibited a greater foraging scale, whereas the native species exhibited a higher foraging precision. A trade-off between foraging scale and precision was observed within each pair of invasive–native species. Compared with soil homogeneity, soil heterogeneity significantly increased the biomass of the two invasive species, B. pilosa and M. micrantha, under competitive conditions. Within each pair, the invasive species exhibited greater relative competitive ability with respect to shoot mass, and considerably more Sr taken up by the invasive species compared with the native species. The Sr acquisition results indicate that nutrient-poor conditions may facilitate the competitive ability of the native species V. cinerea, whereas M. micrantha may possess a stronger competitive ability regardless of soil nutrient conditions.

Conclusion

Soil nutrient heterogeneity has the potential to promote the invasion of these two exotic species due to their larger foraging scale, stronger competitive ability and greater root activity relative to their counterpart native species. The present work highlights the importance of soil heterogeneity in plant invasion, particularly with regards to root foraging traits and competition between invasive and native plants.

Keywords: Bidens pilosa, competition, foraging, Mikania micrantha, nutrient heterogeneity, Paederia scandens, plant invasion, Vernonia cinerea

INTRODUCTION

Disturbances are often claimed to facilitate plant invasions (Lozon and MacIsaac, 1997). The overall results of meta-analyses indicate that disturbance has a positive impact, particularly on exotic plant species (Jauni et al., 2015), and increased resource availability and altered disturbance regimes often differentially increase the performance of invaders relative to native species (Daehler, 2003). The ‘fluctuating resource theory’ indicates that disturbance negatively impacts resident species and their resource uptake, which increases the amount of resources available and creates opportunities for invasion by new species (Davis et al., 2000). Such increases in resources benefit exotic plants because of their high resource use efficiency (Funk and Vitousek, 2007). At the establishment stage, exotic invasive plants are exposed to root competition with native plant species (Theoharides and Dukes, 2007) and are subjected to soil nutrient heterogeneity.

Environmental heterogeneity can promote species coexistence by allowing species to take advantage of conditions that are unfavourable for their competitors (Chesson, 2000). Thus, plant invasions may be promoted when environmental heterogeneity provides opportunities for invader establishment (Davis and Pelsor, 2001; Melbourne et al., 2007; Brandt and Seabloom, 2011). Traits related to nutrient acquisition and use contribute greatly to the competitive ability and invasion success of exotic plant species (Pyšek and Richardson, 2007; Van Kleunen et al., 2010). In general, exotic invasive plants exhibit a higher resource capture ability and higher utilization capacity compared with native plants. These differences have been clearly demonstrated in leaf traits (above-ground traits), with exotic invaders often presenting a higher photosynthetic rate, specific leaf area, photosynthetic nitrogen use efficiency, as well as photosynthetic energy use efficiency and lower leaf construction costs relative to native plants (Baruch and Goldstein, 1999; Funk and Vitousek, 2007; Feng et al., 2008; Van Kleunen et al., 2010; Kaur et al., 2012). However, above- and below-ground traits function differently and might not be related to resource uptake in a similar manner (Weemstra et al., 2016). Additionally, the processes that determine the distribution of plant root growth in the soil are poorly understood in comparison with analogous above-ground processes (Cahill and McNickle, 2011). Examination of traits related to below-ground resource uptake can provide further insight into invasive plant responses to soil environments. At the root level, plants have developed foraging mechanisms that allow them to alter their root architecture, allocation, morphology and physiology in response to variable resource supplies (Drew and Saker, 1975; Hodge, 2004, 2006; Cahill and McNickle, 2011). Root foraging traits include the development of extensive root systems (foraging scale) and the ability to concentrate roots in high-resource patches (foraging precision) (Campbell et al., 1991; de Kroon and Mommer, 2006).

Plant root growth is plastic, resulting in non-uniform root distributions in soil. Compared with native plants, invasive plants show greater root proliferation and increased root N uptake rates in nutrient-rich patches (Drenovsky et al., 2008; James et al., 2009), indicating that invasive plants can exhibit both a greater foraging scale and higher foraging precision (Rajaniemi and Reynolds, 2004). However, trade-offs between the foraging scale and precision are considered to contribute to the coexistence of competitors (Campbell et al., 1991; Grime, 2007). Therefore, we predicted that in conditions where native and invasive species appear to coexist, there may be a trade-off between foraging scale and precision.

Plant root growth plasticity is influenced by soil resource distribution and the presence of neighbours (Hutchings and de Kroon, 1994; Hodge, 2004). Plants can integrate information about nutrients and neighbouring plants, and can adjust their foraging behaviour accordingly (Cahill et al., 2010). Drenovsky et al. (2008) suggested that under competitive conditions, four invasive species would be able to pre-empt resources in nutrient patches because of faster interception (i.e. high relative growth rates and greater root foraging precision), and recent studies have shown that exotic invasive plants exhibit a greater root foraging ability than non-invasive species (Keser et al., 2014, 2015). However, the competition between invasive and native species under heterogeneous and homogenous conditions was not investigated in these studies. The ability of exotic invasive species to become established and spread is related to their ability to suppress resident species competitively (Levine et al., 2003). Different species display different strategies for dealing with both nutrients and neighbours, and nutrient foraging behaviour alone does not necessarily predict behaviour in relation to neighbours (McNickle et al., 2016). The underlying mechanisms of plant invasion can be better understood by examining root foraging traits under competition and heterogeneous nutrient conditions. In general, exotic invasive plants exhibit a higher growth rate than native plants (Pyšek and Richardson, 2007; Van Kleunen et al., 2010; Reichmann et al., 2016). Faster growing species will be more effective foragers because their higher growth rates enable them to ‘discover’ and exploit nutrient patches faster (Fransen et al., 1999). Therefore, we predicted that the competitive ability of invasive species relative to co-occurring native species will increase in heterogeneous compared with homogeneous environments.

Herein, we present the results of a pot experiment designed to explore root foraging traits and the effects of nutrient heterogeneity on the competition between invasive and native species. We selected two invasive–native species pairs (Bidens pilosa var. radiata and Vernonia cinerea; and Mikania micrantha and Paederia scandens) in southern China. The following three questions were addressed. (1) Do root foraging traits differ between the invasive and native species? (2) Is there an invasive–native pair trade-off between foraging scale and foraging precision? (3) Does soil nutrient heterogeneity influence competitive interactions between the invasive and native species? To address these questions, each species was grown alone or was subjected to competition under homogeneous and heterogeneous nutrient conditions in a greenhouse, and the nutrient foraging responses and performance of each species were compared. In addition, strontium (Sr) was applied to both the homogenous and heterogeneous soils to determine root activity.

MATERIALS AND METHODS

Study species

Two pairs of herbaceous species were selected; each pair consisted of an exotic invasive species and a co-occurring native competitor: B. pilosa var. radiata and V. cinerea (hereafter BP–VC pair) are annual forbs of the family Asteraceae, and M. micrantha and P. scandens (hereafter MM–PS pair) are perennial vines. Details pertaining to the species are provided in Table 1. Bidens pilosa (Asteraceae) was unintentionally introduced into Hong Kong in 1857 and is currently widespread across southern and western China, where it has formed extensive stands in old fields and along road margins (Xu et al., 2012). Mikania micrantha (Asteraceae) was first introduced into Hong Kong as early as 1919 and then spread to South China, where it has formed dense populations in forests, plantations and rural areas (Zhang et al., 2004; Xu et al., 2012). The two native species, V. cinerea (Asteraceae) and P. scandens (Rubiaceae), commonly co-occur with their counterpart invasive species B. pilosa and M. micrantha, respectively.

Table 1.

Information on the two invasive–native species pairs.

Pairs Species Family Origin Life form
BP–VC Bidens pilosa var. radiata Asteraceae Invasive Annual upright forb
Vernonia cinerea Asteraceae Native Annual upright forb
MM–PS Mikania micrantha Asteraceae Invasive Perennial vine
Paederia scandens Rubiaceae Native Perennial vine
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Seeds of each species were collected from 3–5 wild populations growing on Xiaoguwei Island, Guangzhou, South China (23.03–23.07°N, 113.35–113.41°E), where local communities were invaded by the two exotic species (we observed invader coverage >60 %).

Experimental design

In a greenhouse experiment, the invasive and native species were grown alone and in competition with their co-occurring counterparts. The planting treatment was crossed with two levels of a nutrient heterogeneity treatment (i.e. heterogeneous or homogenous) (Fig. 1), and these treatments were replicated five times. We employed a randomized block design, in which each of the five replicates was randomly assigned to one of the five blocks. In addition, to estimate the root activity of the plant species in the nutrient-poor and nutrient-rich patches, an extra heterogeneous treatment for each pair of species (six pots per block) involving Sr application was established in each block. In this treatment, SrCl2 was applied to both species pairs in each block and was used as a tracer to identify root activity, as described below.

Fig. 1.

Fig. 1.

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Schematic representation of the experimental design. Pots were divided into four quadrants (1, 2, 3 and 4). Each species within a species pair was grown alone and in competition with the other member of the pair under homogeneous and heterogeneous nutrient conditions. ‘I’ indicates the position of the invasive plant and ‘N’ indicates the position of the native plant. Under heterogeneous conditions, quadrant 2 was nutrient rich, and quadrant 3 (as well as quadrants 1 and 4) was nutrient poor. Grey represents homogeneous soil; dark shading represents nutrient-rich soil; and white represents nutrient-poor soil. The total nutrient availability was similar between the treatments. In addition, Sr (represented by stars) was applied to both quadrants 2 and 3 under the heterogeneous condition and only to quadrant 2 under the homogeneous condition (details in the Materials and Methods).

To test the effect of nutrient heterogeneity, we generated homogeneous and heterogeneous soil nutrient patches. The experimental growth pots (20 cm in diameter and 18 cm deep) were divided into four quadrants (Fig. 1). In the heterogeneous nutrient treatment, quadrant 2 of each pot was filled with rich soil (sand and potting soil in a 1:1 proportion by volume, total N = 105.0 mg L–1 and total P = 230.0 mg L–1), and the other three quadrants were filled with poor soil (sand and potting soil in a 17:1 proportion by volume, total N = 11.7 mg L–1 and total P = 25.6 mg L–1). The homogeneous nutrient treatment was composed of sand and potting soil in a 1:5 ratio by volume and involved the same total nutrient contents (total N = 35.0 mg L–1 total P = 76.7 mg L–1) as in the heterogeneous pots. Pot size was held constant across all treatments.

All seeds were germinated on double layers of wet filter paper in Petri dishes in a growth chamber (12 h light, 28 °C; 12 h dark, 23 °C), and the seedlings were transplanted after 7 d of culture in a seedling bed under common greenhouse conditions. To prevent damage to young roots, we retained the soil attached to the seedlings. One seedling of the invasive species was grown in the middle of quadrant 1, and one seedling of the native species was grown in quadrant 4. In monocultures, the same volume of attached soil was placed in quadrant 1 for the native species or quadrant 4 for the invasive species to maintain nutrient levels consistent with those of the plants in the mixtures. All pots containing each species pair were transplanted within a 24 h period to eliminate the effects of germination time of the different species (Manea and Leishman, 2011).

The experiment was conducted in a greenhouse on the east campus of Sun Yat-Sen University, Guangzhou, China. All plants were placed randomly within blocks and were watered once a week. The blocks were switched every 2 weeks, and the pots within each block were re-randomized every week.

Harvest W measurements

All plants were harvested 10 weeks after transplantation. First, we harvested the entire above-ground portion of each plant. In the monocultures, the root biomass was harvested from the four quadrants of each pot (Fig. 1). In the mixtures, we measured the intact root biomass of each species, not the roots of each species within each quadrant since it was impossible to separate the vertically cut roots by species. Root length was analysed using the LA-S root analysis system (Wseen Inc., Hangzhou, China). All plant tissues were dried at 60 °C for at least 72 h and then weighed.

Strontium injection and analysis

Strontium is used as a tracer to identify root activity in overlapping zones among coexisting plants (Veresoglou and Fitter, 1984; Mamolos et al., 1995; Fransen et al., 2001). In the present study, because we could not separate the roots by species within each quadrant in the mixtures, SrCl2 was injected into the nutrient-rich and nutrient-poor patches, as well as into equivalent locations in the homogeneous treatments. Sr uptake was measured and used to estimate the root activity of each species. Sr was applied to the plants twice, i.e. 3 weeks and 1 week before harvest. In the heterogeneous treatment, 15 mL of a 0.2 m SrCl2 solution was injected into quadrant 2 and quadrant 3 separately at a depth ranging from 2 to 6 cm (see Fig. 1). In the homogeneous treatment, an equivalent dose of the SrCl2 solution was applied to quadrant 2 at a similar depth. Then, the root activity of each species was assessed by determining the amount of Sr (mg per shoot) taken up by the shoots at the end of the experiment.

The dried shoots (0.2–0.4 g) were ground and subjected to organic matter digestion using nitric acid. The Sr concentration in the solution was measured using an atomic emission spectrometer (iCAP 6500 Duo, Thermo Fisher Inc., Waltham, MA, USA).

Calculations

To assess the root distribution, we analysed the foraging scale and precision of the plants. The foraging scale was represented by the root biomass and root length density (RLD) in the nutrient-rich patches, and the foraging precision with respect to both the root biomass and RLD was calculated according to Mou et al. (1997), as follows:

Precision = (Qrich–Qpoor)/Qtotal

where Qrich and Qpoor represent the root biomass or RLD in the nutrient-rich (quadrant 2) and nutrient-poor (quadrant 3) patches, respectively, and Qtotal represents the mean RLD in the four quadrants or the total root biomass of an individual plant.

The influence of competition on the target plant was determined using the relative interaction intensity (RII) (Armas et al., 2004), which was calculated as follows:

RII = (Fw–Fo)/(Fw+Fo)

where Fw is the performance of the target plant grown under competition, and Fo is the performance of the target plant grown alone. RII values range from –1 to 1. Negative values indicate a suppressive effect by neighbours, and less negative values indicate weaker competitive inhibition, while positive values indicate facilitation, and less positive values indicate weaker facilitation.

Statistical analysis

Within each pair of invasive–native species, we tested for significant species differences in foraging scale and precision using independent t-tests. We used two-way analysis of variance (ANOVA) to test for significant differences in total biomass and RII between invasive and native species within each pair, in the two levels of competition (monoculture vs. mixture) and in the species origin (invasive vs. native). We used three-way ANOVA to test for significant differences in Sr acquisition between invasive and native species within each pair, in the three soil heterogeneity treatments (homogeneous, nutrient-rich and nutrient-poor patches), and in the two levels of competition (monoculture vs. mixture). To illustrate further the interactions among these three factors, we conducted post-hoc tests to determine significant interactions between soil heterogeneity, competition and species origin. Within each species, we tested whether the effects of soil heterogeneity on Sr acquisition differed significantly between the homogeneous, nutrient-rich and nutrient-poor conditions using one-way ANOVA, and we tested whether the effects of soil heterogeneity on total biomass and RII differed significantly using independent t-tests. All analyses were performed using SPSS 20.0 for Windows (SPSS, Chicago, IL, USA).

RESULTS

Root foraging scale and precision

Overall, the invasive species exhibited a greater scale of root foraging according to both root mass and RLD compared with the native species (Fig. 2A, B). Paederia scandens exhibited higher foraging precision than M. micrantha on the basis of root mass (Fig. 2C), and V. cinerea had higher foraging precision than B. pilosa on the basis of RLD (Fig. 2D).

Fig. 2.

Fig. 2.

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Foraging scale in terms of root mass (A) and RLD (B) and foraging precision in terms of root mass (C) and RLD (D) of each species in response to the heterogeneous nutrient treatment in their monocultures. RLD = root length density. The two invasive–native species pairs are B. pilosa (BP) vs. V. cinerea (VC) and M. micrantha (MM) vs. P. scandens (PS). Values are the means ± s.e., and different letters indicate statistically significant differences between species (Tukey’s HSD, P = 0.05).

Combining the foraging scale (Fig. 2A) and precision (Fig. 2C) in terms of root mass in the heterogeneous soil, the invasive species M. micrantha presented a greater foraging scale, while the native species P. scandens presented a higher foraging precision. However, for the foraging traits in terms of RLD, the invasive species B. pilosa presented a greater foraging scale, while the native species V. cinerea presented higher foraging precision (Fig. 2B, D). These findings suggest a trade-off between the foraging scale and precision (one pair in terms of root mass; the other pair in terms of RLD) within each pair of invasive–native species.

Effects of soil heterogeneity and competition on total plant biomass

The ANOVA results showed that heterogeneity, competition (monoculture vs. mixture) and species origin (invasive vs. native) had significant effects on the total plant biomass within each pair (Table 2). Overall, heterogeneity increased the biomass of each invasive–native species pair, but competition significantly reduced their biomass (Fig. 3). The total biomass of the invasive species was much higher than that of the native species within each invasive–native species pair (Fig. 3). The significant heterogeneity × species origin interaction within the MM–PS pair (Table 2) implied that growth of invasive and native species responded differently under the homogenous and heterogeneous soil conditions. Soil heterogeneity increased the biomass of M. micrantha in both the monoculture and mixture, but it only increased the biomass of P. scandens in the monoculture (Fig. 3). However, the absence of a significant heterogeneity × competition interaction within each species pair (Table 2) implied that competition between the invasive and native species did not differ between the homogenous and heterogeneous soil conditions.

Table 2.

Analysis of the effects of soil heterogeneity and competition on the total biomass of the two invasive–native species pairs BP–VC (B. pilosa vs. V. cinerea) and MM–PS (M. micrantha vs. P. scandens)

Species pair Variable Heterogeneity (H) Competition (C) Origin (O) H × C H × O C × O
d.f. 1 1 1 1 1 1
BP–VC F 4.262 15.532 170.254 0.281 3.239 1.491
P 0.047 <0.001 <0.001 0. 600 0.081 0.231
MM–PS F 71.542 17.991 855.058 2.287 43.622 0.400
P <0.001 <0.001 <0.001 0.140 <0.001 0.532
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Origin indicates invasive vs. native.

Fig. 3.

Fig. 3.

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Effect of nutrient heterogeneity (Homo, homogeneity; Hete, heterogeneity) and competition (Mono, monoculture; mixture) on total biomass. The two invasive–native species pairs are B. pilosa (BP) vs. V. cinerea (VC) and M. micrantha (MM) vs. P. scandens (PS). Values are the means ± s.e. Differences between the nutrient heterogeneity treatments are indicated by the corresponding levels of significance: n.s., P > 0.05; *P < 0.05, **P < 0.01, ***P < 0.001. Statistical analysis results are provided in Table 2.

Effects of soil heterogeneity on RII

The invasive species exhibited a greater relative competitive ability within each species pair with respect to the shoot (Fig. 4A). Only the invasive species M. micrantha had a higher root RII than the native species P. scandens (Fig. 4B), and soil heterogeneity had no significant effect on either the root or shoot RII (Table 3). The significant heterogeneity × species origin interaction within each pair (Table 3) implied that the shoot RII of the invasive and native species responded differently under homogenous and heterogeneous soil conditions. Soil heterogeneity significantly increased the shoot RII of the invasive species B. pilosa, but decreased that of the native species V. cinerea (Fig. 4A).

Fig. 4.

Fig. 4.

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Effect of nutrient heterogeneity on the shoot (A) and root (B) RII. The two invasive–native species pairs are B. pilosa (BP) vs. V. cinerea (VC) and M. micrantha (MM) vs. P. scandens (PS). Values are the means ± s.e. Statistical analysis results are provided in Table 3. For each species, differences between nutrient heterogeneities are shown by the corresponding level of significance (using independent t-tests) for each pair: n.s., P > 0.05; *P < 0.05.

Table 3.

ANOVA results for the shoot and root mass RII of the pairs of invasive and native species under homogeneous and heterogeneous conditions

Species pair Variable Shoot mass RII Root mass RII
Heterogeneity (H) Origin (O) H × O Heterogeneity (H) Origin (O) H × O
d.f. 1 1 1 1 1 1
BP–VC F 1.232 9.217 18.793 1.308 3.000 2.035
P 0.283 0.008 0.001 0.270 0.102 0.173
MM–PS F 0.787 195.726 3.419 0.388 34.598 0.015
P 0.388 <0.001 0.009 0.542 <0.001 0.904
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The two invasive–native species pairs are BP–VC (B. pilosa vs. V. cinerea) and MM–PS (M. micrantha vs. P. scandens).

Origin indicates invasive vs. native.

Root activity: Sr acquisition

Soil heterogeneity (nutrient-rich, nutrient-poor or homogeneous nutrient conditions) and competition (monoculture vs. mixture) significantly affected Sr acquisition, and the effects differed between the invasive and native species within each pair (Table 4). In general, Sr acquisition by all four species was reduced by competition, and it was higher in the nutrient-rich than in the nutrient-poor patches (Fig. 5; Table 4). Sr acquisition by the two invasive species was much higher than that of the two native species, and Sr acquisition by the invasive species B. pilosa was higher in the nutrient-rich than in the nutrient-poor patch under both monoculture and mixture conditions (Fig. 5). A significant interaction between soil heterogeneity, competition and species origin was observed for Sr acquisition within the BP–VC pair, while only a significant interaction between soil heterogeneity and species origin was observed within the MM–PS pair (Table 4).

Table 4.

ANOVA results for Sr acquisition by the pairs of invasive and native species grown alone and in competition with their counterparts under homogeneous and heterogeneous conditions (nutrient-rich and nutrient-poor quadrants)

Species pair Variable Heterogeneity (H) Competition (C) Origin (O) H × C H × O C × O
d.f. 2 1 1 2 2 1
BP–VC F 38.210 22.292 224.082 3.924 12.693 6.030
P <0.001 <0.001 <0.001 0.026 <0.001 0.018
MM–PS F 18.945 4.876 247.524 0.178 3.419 0.112
P <0.001 0.032 <0.001 0.837 0.041 0.739
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The two invasive–native species pairs are BP–VC (B. pilosa vs. V. cinerea) and MM–PS (M. micrantha vs. P. scandens).

Origin indicates invasive vs. native.

Fig. 5.

Fig. 5.

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Effect of nutrient heterogeneity (Homo, homogeneity; Hete, heterogeneity) and competition (Mono, monoculture; mixture) on Sr acquisition. The two invasive–native species pairs are B. pilosa (BP) vs. V. cinerea (VC) and M. micrantha (MM) vs. P. scandens (PS). Values are the means ± s.e. Different lower case letters for each species indicate statistically significant differences between the soil treatments. Statistical analysis results are provided in Table 4.

DISCUSSION

The present study investigated root foraging traits and plant competition mechanisms between invasive and native species under heterogeneous soil nutrient conditions. Significant differences in the foraging scale with respect to both the root mass and RLD were observed between the invasive and native species of each pair. There was a trade-off between the foraging scale and precision on the basis of root mass within the MM–PS pair, and a trade-off on the basis of RLD within the BP–VC pair (Fig. 2). Soil nutrient heterogeneity, competition (monoculture vs. mixture) and species origin (invasive vs. native) had significant effects on the plant growth and Sr acquisition within each pair; the invasive species performed better in terms of growth and Sr acquisition than the native species for both the monocultures and mixtures (Figs 3 and 5; Tables 2 and 4). These findings indicate that these invasive species have a more extensive foraging scale and exhibit greater root activity and stronger above-ground competitive ability (Fig. 4A) compared with their counterpart native species.

Effective foraging may be a trait that promotes the invasion of exotic plant species (Drenovsky et al., 2008; Keser et al., 2014). It has been reported that invasive plants have both a greater foraging scale and higher foraging precision than native plants (Rajaniemi and Reynolds, 2004; Drenovsky et al., 2008; James et al., 2009). Increasing root foraging scale and precision can substantially increase a plant’s metabolic costs, which may reduce any advantage invasive plants have over native species in terms of construction costs (Baruch and Goldstein, 1999; Osunkoya et al., 2010). Thus, it does not appear logical for successful exotic invasive plants consistently to exhibit both a greater foraging scale and higher foraging precision. In the present study, a trade-off between the foraging scale and precision was observed within the BP–VC pair based on RLD and within the MM–PS pair based on root mass, and the invasive species exhibited a greater foraging scale while the native species exhibited higher foraging precision (Fig. 2). Campbell et al. (1991) suggest that a trade-off should occur between the scale and precision of foraging, and dominant species may exhibit large-scale foraging, while subordinate species persist by foraging precisely in resource patches that are missed by dominant species. Hence, a greater foraging scale may facilitate rapid proliferation of the invasive species B. pilosa and M. micrantha roots in nutrient-rich patches, allowing these dominant species and coarse foragers to pre-empt the resources in these areas. Higher foraging precision may help V. cinerea and P. scandens (inferior species and fine foragers) to place their roots selectively in any area unexploited by the coarse foragers, allowing these species to take up the remaining resources.

Based on the monoculture results, Drenovsky et al. (2008) predicted that under competitive conditions, slow-growing species will probably be outcompeted due to resource pre-emption by fast-growing species. In nature, however, plants are simultaneously exposed to nutrient heterogeneity and to neighbours. Our results confirmed that under competitive conditions, the two invasive species (which grew faster than the native species, Fig. 3) exhibited higher shoot mass RII than the two native species (Table 3; Fig. 4A), and Sr acquisition by the invasive species was much greater than that of their counterpart native species (Table 4; Fig. 5). Effective root foraging behaviour confers a strong competitive ability in heterogeneous environments (Fransen et al., 2001), and competitive ability is more closely correlated with the foraging scale (which allows a plant rapidly to occupy a volume of soil with its roots) than with foraging precision (which allows a plant access to appropriate resources) (Rajaniemi, 2007; Mommer et al., 2011). This is supported by our observation that compared with soil homogeneity, soil heterogeneity significantly increased the biomass of the invasive species B. pilosa and M. micrantha (with a greater foraging scale) in the mixture (i.e. under competition), but not that of the native species V. cinerea and P. scandens (with a smaller foraging scale) (Figs 2A, B and 3). However, previous studies with mono-species culture (i.e. without competition) found that heterogeneous soil nutrient conditions significantly decreased the total biomass and the below-ground biomass of both invasive and non-invasive species compared with homogeneous conditions (Keser et al., 2015), and there was no significant main effect of soil heterogeneity on the above- or below-ground biomass of both the invasive and native forbs (Drenovsky et al., 2008). This indicates that previous studies under non-competitive conditions may misestimate the role of soil heterogeneity in plant growth and competitive ability, and consequently underestimate the facilitation of plant invasiveness under heterogeneous soil nutrient conditions. Furthermore, our shoot RII results for the BP–VC pair indicated that heterogeneity significantly increased the shoot RII of the invasive species B. pilosa but significantly decreased that of its counterpart native species (Fig. 4A), suggesting that this invasive species benefits more from heterogeneous soil conditions under competition compared with the other invasive species M. micrantha. Therefore, soil nutrient heterogeneity has the potential to promote the invasion of the two exotic species, and greater or more heterogeneous nutrient conditions may further contribute to the ability of these invasive species to invade and expand. Conclusions regarding the effects of soil heterogeneity on plant invasion should be made cautiously because of the different or even opposite effect of soil heterogeneity between competitive and non-competitive conditions. Species with different foraging traits may have different competitive advantages under different soil nutrient conditions (homogeneous, nutrient-rich and nutrient-poor). In competition below-ground, greater root activity (higher nutrient uptake) is likely to enhance subsequent growth (Berntson and Wayne, 2000). In the present study, Sr2+ was used as a tracer to assess the root activity of the species pairs under different nutrient conditions. Our results regarding Sr acquisition may explain the competitive ability of the invasive and native species under different soil nutrient conditions. Competition reduced Sr acquisition by the invasive species B. pilosa more than that by the native species V. cinerea under homogeneous conditions (–24.0 % vs. –44.4 %) and in nutrient-rich patches (–31.6 % vs. –60.4 %), while competition increased Sr acquisition by V. cinerea (+125.3 %) in nutrient-poor patches but decreased the Sr acquisition ability of B. pilosa by 40.4 % (Fig. 3). Thus, nutrient-poor conditions may increase the competitive ability of the native species V. cinerea relative to that of the invasive species B. pilosa, whereas M. micrantha may possess a stronger competitive ability than P. scandens regardless of soil nutrient conditions because competition reduced Sr acquisition by P. scandens to a much greater extent compared with M. micrantha under all three soil nutrient conditions (homogeneous, nutrient-rich and nutrient-poor conditions).

It should be noted that root foraging traits may be associated with plant size. Larger plants may have a disproportionately large competitive effect (i.e. a greater per gram effect) if they can reach and exploit patches faster than smaller plants, obtaining the resources within those patches (Schwinning and Weiner, 1998). In the present study, the two invasive species exhibited a much higher biomass than their counterpart native species (Fig. 3); thus, size-asymmetric competition may occur between the invasive and native plants. Size asymmetry is expected to lead to competitive exclusion because larger plants can prevent smaller ones from meeting their minimum resource requirements through the appropriation of resources (Hutchings and de Kroon, 1994; Schwinning and Fox, 1995). This notion was confirmed by our results showing that on average, competition resulted in a more significant reduction in Sr acquisition by the two native species (smaller plants) compared with their counterpart invasive species (larger plants) relative to Sr acquisition by the species in the monocultures (Fig. 5; Table 4).

Most of the studies on competition between invasive and native plants are carried out under homogeneous conditions, or the studies regarding soil nutrient heterogeneity are conducted under monoculture conditions (without considering competition between invasive and native plants). Our findings indicate that soil nutrient heterogeneity has the potential to promote the invasion of these two exotic species due to their larger foraging scale, stronger competitive ability and greater root activity relative to their counterpart native species. Previous studies conducted under non-competitive conditions may underestimate the facilitation of plant invasiveness resulting from soil heterogeneity compared with the present study under competitive conditions. Additionally, nutrient-poor conditions may facilitate the competitive ability of the native species V. cinerea, while M. micrantha may possess a stronger competitive ability than P. scandens regardless of soil nutrient conditions. The present study suggests that the results of competition experiments must be interpreted with caution due to the different effects of soil nutrient heterogeneity and root foraging traits between invasive and native species. A future challenge is to investigate the underlying mechanisms of plant invasion from the perspective of foraging traits, considering not only a range of heterogeneous conditions but also the sizes of invasive and native species.

ACKNOWLEDGEMENTS

This study was supported by the Natural Science Foundation of Guangdong (2017A030313187), the National Natural Science Foundation of China (31670479), the Science and Technology Planning Project of Guangzhou (201607020027) and the Scientific Research Fund of Hongda Zhang, Sun Yat-Sen University.

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