Effects of arbuscular mycorrhizal fungi on root foraging and competitive ability between native and invasive plants

doi:10.21203/rs.3.rs-3412944/v1

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Effects of arbuscular mycorrhizal fungi on root foraging and competitive ability between native and invasive plants

https://doi.org/10.21203/rs.3.rs-3412944/v1

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Background and Aims

Besides the direct uptake of nutrients by roots, plants can acquire nutrients through the aid of arbuscular mycorrhizal fungi (AMF). AMF play a crucial role in plant growth and competitive abilities. However, few studies have investigated the effects of AMF on root-foraging, and their interactive effects on competition between native and invasive species in response to heterogeneous nutrients.

Methods

Two invasive plants and their two co-existing native plants of the Asteraceae family were selected to create a common garden experiment involving three factors (heterogeneous vs. homogeneous phosphorus, with vs. without AMF inoculation, and monoculture vs. mixture).

Results

AMF significantly reduced the foraging scale of the invasive species, Bidens pilosa, and decreased the precision of the invasive species, Praxelis clematidea, and the native species, Emilia sonchifolia. There were significant interactive effects of AMF and phosphorus heterogeneity on plant biomass and nutrient uptake. Heterogeneity significantly decreased the tolerance ability of B. pilosa but increased that of P. clematidea. In the homogeneous treatment, AMF significantly decreased the suppression ability of B. pilosa, while in the heterogeneous treatment, AMF decreased that of P. clematidea. Heterogeneous phosphorus with AMF increased the suppression relative interaction intensity of B. pilosa but decreased that of P. clematidea.

Conclusion

The interactive effects of AMF and phosphorus heterogeneity on root foraging and competitive abilities differ between invasive and native plants and show invasive-native pair differences. These findings provide valuable insights into the interactive effects of AMF and roots on nutrient uptake and competition in different nutrient distributions.

Alien

AMF

exotic

plant invasion

root foraging precision

root foraging scale

Soil nutrients are often spatially heterogeneous (Jackson and Caldwell 1993; Gross et al. 1995; Farley and Fitter 1999). This is particularly true for phosphate because of its low solubility and diffusivity (Hinsinger, 2001; Felderer et al., 2013). Plants can selectively place their roots in nutrient-rich patches, which can lead to a higher acquisition of nutrients and better performance in heterogeneous environments (Hodge, 2004; Cahill and McNickle, 2011; Zhang et al., 2019). Plants respond to variations in nutrient distribution by adjusting their root investment, morphology, and physiology to improve their root foraging abilities (Jackson et al., 1990; Hodge, 2004; Kembel and Cahill, 2005; Wang et al., 2022). Morphological plasticity enables plants to enhance their acquisition of essential resources by generating different resource-acquiring structures in response to different environmental conditions, which is referred to as root foraging ability (De Kroon and Hutchings, 1995; Fransen, 1999; Fransen et al., 1999a, 1999b). The root foraging scale (development of the root system) and precision (ability to proliferate more roots within nutrient-rich patches) are often used to reflect root foraging behaviour (Campbell et al., 1991; Kembel and Cahill, 2005). It has been suggested that there is a trade-off between root foraging scale and precision (Campbell et al., 1991); however, some studies offer different results (Einsmann et al., 1999; Rajaniemi and Reynolds, 2004).

Besides the direct uptake of nutrients by roots, plants can acquire nutrients through the aid of arbuscular mycorrhizal fungi (AMF), and host plants and fungal symbionts benefit from the reciprocal exchange of mineral and organic resources (Smith et al., 2011; Bennett and Groten, 2022). Owing to the smaller diameter of hyphae and lower metabolic cost of hyphal growth, AMF may be more flexible in response to nutrient patches than roots (Hodge, 2006). Mycorrhizal fungi have been reported to have a strong influence on root proliferation (Cui and Caldwell, 1996; Cheng et al., 2016), and therefore, change root foraging and plant nutrient uptake strategies (Tibbett, 2000; Felderer et al., 2013; Chen et al., 2016; Chippano et al., 2021). However, AMF colonization is not always beneficial for plants, as mycorrhizal associations vary from mutualism to parasitism, depending on the host species, soil fertility, and other environmental conditions (Klironomos, 2003; Shah et al., 2009; Facelli et al., 2010). Therefore, it is essential to consider root foraging and AMF to better understand nutrient uptake under heterogeneous conditions.

Many studies have shown that AMF significantly influence plant competition (West 1996; Zobel et al., 1997; Stanescu and Maherali, 2017; Sun et al., 2022). AMF can interconnect plant root systems through common mycorrhizal networks (CMNs) of hyphae, which can influence mineral nutrient uptake by roots between interconnected individuals and, accordingly, affect competition (Weremijewicz and Janos, 2013; Lin et al., 2015). In nature, plants are exposed to heterogeneity of nutrients and neighbouring plants. When competing for underground resources with neighbours, plants alter the spatial distribution of their roots and foraging abilities (Cahill et al., 2010; Mommer et al., 2012; Colom and Baucom, 2020; Garlick et al., 2021). At the same time, root foraging ability can influence the competitive ability of plants (Rajaniemi, 2007), and more effective root-foraging behaviour confers higher competitive ability in heterogeneous environments (Fransen et al., 2001). Resource competition has long been considered a major mechanism determining the success of invasive species (Levine et al., 2003). Studies have shown that exotic invasive plants exhibit greater root-foraging capacities than non-invasive species (Keser et al., 2014, 2015). Furthermore, AMF can form novel symbioses with exotic invasive plants and play a crucial role in their growth and competitive abilities (Callaway et al., 2001; Pringle et al., 2009; Menzel et al., 2017; Aslani et al., 2019; Chen et al., 2020; Sun et al., 2022). However, few studies have investigated the effects of AMF on root-foraging, and their interactive effects on competition between native and invasive species in response to heterogeneous nutrients.

The specific questions evaluated were as follows: (i) What are the effects of AMF on the scale and precision of root foraging? and (ii) How do AMF influence competition between invasive and native plants in both homogeneous and heterogeneous nutrient conditions? In this study, two invasive and two coexisting native species were selected, and they live symbiotically with AMF. The two invasive species were Bidens pilosa var. radiata (also called Bidens alba or Bidens pilosa L.) and Praxelis clematidea, widely distributed in South China, and the two native species were Emilia sonchifolia and Eupatorium chinense. As our previous study has shown that the two exotic invasive plants had a larger foraging scale, and the two native plants had higher precision (Chen et al., 2018), we predicted that AMF could reduce the root foraging scale of the invasive species and reduce the root foraging precision of the native species. In general, exotic invasive plants exhibit a higher growth rate than native plants, and their higher growth rates allow them to 'discover' and exploit nutrient patches faster, leading to a stronger competitive ability of invasive plants (Van Kleunen et al., 2010; Gioria and Osborne, 2014). By preferentially allocating mineral nutrients to faster-growth or larger host plants, AMF in CMNs can increase competition (Weremijewicz et al., 2016). Therefore, we hypothesised that heterogeneity and AMF could improve the growth and competitive ability of invasive species.

Study site and seed collection

The experiment was conducted in the glasshouse of the Ecological Research Station in Haizhu Wetland National Park, Guangzhou (23°04'38"N, 113°18'9"E), where the climate is subtropical monsoon.

Seeds were collected from 3–5 wild populations on Xiaoguwei Island, Guangzhou, Guangdong Province, South China. Each species' seeds were thoroughly mixed for later use.

Soil collection and preparation

The soil was collected from the Zengcheng district of Guangzhou (23°05'–23°37'N, 113°32'–114°00'E). Vermiculite and soil were air-dried, sieved through a 2 mm sieve, and sterilised using ⁶⁰Co gamma-irradiation at 10kGy (Wang et al., 2020). After sterilisation, the soil, sand, and vermiculite were mixed at a volume ratio of 4:1:5 and the pots were filled. The nutrient concentration of the soil mixture was quite low, with a total C of 1.69 ± 0.03 g kg^− 1, total N of 0.74 ± 0.02 g kg^− 1, and total P of 0.58 ± 0.02 g kg^− 1 dry soil.

Experimental design

We employed a completely randomised three-factor design with 24 treatments of soil P spatial distribution (homogeneous and heterogeneous), AMF (G. mosseae inoculation, without G. mosseae inoculation), and six planting treatments (four species monocultures, two mixed cultures of invasive and native species B. pilosa and E. sonchifolia, P. clematidea and E. chinense) (Fig. 1). Each treatment was repeated five times.

Homogeneous and heterogeneous P were created by adding an aqueous solution of Ca(H₂PO₄)₂·H₂O with equal total P added to all treatments. Rectangular pots (26, 15, and 12 cm in length, width, and height, respectively) were used, and half of them were divided into three sections (7 + 12 + 7 cm = 26 cm) to maintain the same P content as in the homogeneous treatments. In the homogeneous treatment, the P concentration was 20 mg kg^− 1 soil throughout the pot. For the heterogeneous treatment, the pots were divided into three sections using thin plastic plates. Plants were planted in the middle of all the pots, where the P concentration was maintained at 20 mg kg^− 1 soil. The left and right sides of the heterogeneous pots were supplied with P-poor and P-rich patches, respectively, as shown in Fig. 1. The P concentration was maintained at 10 mg kg^− 1 P in the P-poor section and 100 mg kg^− 1 P in the P-rich section. The homogeneous and heterogeneous treatments had the same total P content. Simultaneously, 50 mL of Hoagland nutrient solution without P was added to each pot to reduce the limitations of other nutrients.

Before P treatment, the pots were inoculated with AMF. Glomus mosseae, which is symbiotic with most plants, was used for AMF inoculation. It was propagated symbiotically with white clover for two months in a greenhouse. The spore density of the inoculum was 100 spores g^− 1. Each pot contained 76 g of the inoculum at a depth of 3 cm in the soil.

After soil P and AMF treatments, the seedlings were transplanted into pots. Seeds were sterilised with 0.5% potassium permanganate, and rinsed with pure water for 10 min. They were then placed in Petri plates with double layers of wet filter paper for germination in a growth chamber at 22 ± 1°C and under 12 h of light and 12 h of darkness and then planted on a sterilised nursey tray after the emergence of the cotyledons. Seedlings of uniform size were chosen for transplantation into the centre of the pots. For the monoculture, one individual of each species was planted in each pot, while for the mixed culture, one individual each of native and invasive plants were planted in each pot. After two weeks, we created the P treatment again as the first time and then removed the inserted plastic plates between the sections of the heterogeneous pots after the locations of the plastic plates were marked (to separate them for collecting roots in each section).

The pots were rotated weekly to eliminate any potential effects of spatial heterogeneity in light and temperature in the glasshouse. All pots were watered every 2–3 days or as needed. Additionally, 50 mL of Hoagland nutrient solution without P was supplied to each pot every two weeks to provide other nutrients to the plants.

Harvest and measurements

Plants were harvested 80 days after transplantation. The shoot biomass was cut and dried at 60°C for 72 h. For homogeneous treatments, roots were gently washed free of soil under running water through a sieve. For the heterogeneous treatments, soil samples and roots were collected from the three sections separately (according to the marked locations of the sections), and the roots were gently washed free of soil under running water through a sieve. The roots were dried at 60°C for 72 h and weighed.

Shoots were ground and digested with H₂O₂/H₂SO₄ (conc.) to measure the concentrations of N and P using the Kjeldahl and vanadate-molybdate-yellow colorimetry methods. Shoot N and P uptake were calculated as N and P concentration multiplied by shoot biomass of each species.

The root length of each plant was analysed using the LA-S root analysis system (Wseen Inc., Hangzhou, China) after soaking in water to calculate the root length density.

Foraging scale and precision were analysed to assess the root distribution of the four species in the monoculture. The foraging scale was presented as the total root biomass of the plants (Bliss et al., 2002), and foraging precision was measured in terms of root biomass according to Campbell et al. (1991), as follows:

Precision = (Root-S_rich – Root-S_poor) / Root-S_total

where S_rich and S_poor indicate P-rich and P-poor sections, respectively. S_total indicates total biomass of root in each pot.

The total biomass of the four species was used to calculate the tolerance and suppression capacity of the invasive species B. pilosa and P. clematidea under heterogeneous and AMF treatments using the relative interaction intensity (RII) index of tolerance and suppression. The tolerance and suppression RII represent the ability of invasive plants to tolerate competition with native plants and suppress native plants, respectively (Fletcher et al., 2016). In this study, we calculated the tolerance and suppression RII of each invasive plant competing with its native neighbour as follows (Chen et al., 2020):

Tolerance RII = (Biomass _{Invasive-mix -} Biomass _{Invasive-mono)} / (Biomass _Invasive-mix + Biomass _{Invasive-mono)}

Suppression RII = – (Biomass _Native-mix -Biomass _Native-mono) / (Biomass _{Native -mix} + Biomass _Native-mono)

Higher tolerance RII and suppression RII reflect a stronger competitive ability of invasive plants.

Statistical Analyses

All data were analysed using R v4.1.3 (R Core Team, 2022). A three-way analysis of variance (ANOVA) was used to analyse the effects of heterogeneity treatment, AMF inoculation, and competition on the total biomass and shoot N and P uptake of each species. A two-way ANOVA was used to analyse the effects of AMF and species on the scale of root foraging and the precision of monocultured plants. It was also used to test the effects of heterogeneity and AMF inoculation on the competitive ability (tolerance and suppression of RII) of the two invasive species, B. Pilosa and P. clematidea. Post-hoc multiple comparisons were performed to determine the differences for each species using the least significant difference method, in which the p values were adjusted using the Bonferroni method. In addition, an independent t-test was used to test whether the effects of AMF inoculation differed with respect to total biomass, shoot N and P uptake, root foraging scale, and precision of each species. Before performing ANOVA, the normality of distributions and homogeneity of variance were tested, and some data were logarithmically transformed to satisfy these assumptions.

Root foraging scale and precision

The scale and precision of root foraging were significantly affected by AMF, and there were significant differences in the scale and precision of foraging among the four species (Table 1). Without AMF inoculation, the invasive species B. pilosa and P. clematidea had the highest foraging scale and precision, respectively, whereas AMF inoculation eliminated their higher foraging scale and precision relative to the other species (Fig. 2a, 2b, 2c). The root-foraging scale of B. pilosa and the root-foraging precision of E. sonchifolia and P. clematidea (Fig. 2) were significantly reduced by AMF, resulting in a significant AMF × species interaction on foraging scale and precision (Table 1).

Table 1

Two-way ANOVA for the effects of AMF inoculation and species on root foraging scale and precision of monoculture plants. Species refers to the identity of the species being planted. Statistically significant values are in bold (p < 0.05). RLD indicates root length density.
		Foraging scale (mass)		Foraging Scale (RLD)			Foraging precision (mass)		Foraging precision (RLD)
Treatments	df	F	p	F	p	df	F	p	F	p
AMF	1	10.404	0.003	10.159	0.004	1	13.003	0.001	3.361	0.080
Species	3	38.766	< 0.001	23.333	< 0.001	2 ^#	17.37	< 0.001	15.102	< 0.001
AMF × S	1	7.507	< 0.001	2.664	0.067	1	6.962	0.004	0.778	0.471
^# The foraging precision of E. chinense cannot be determined since its roots do not spread in P-rich soil. Therefore, we measured the root foraging precision of three species, but without E. chinense.

Plant biomass

Heterogeneity had significant effects on the total biomass of the four species, while AMF and competition had significant effects on the total biomass of B. pilosa and E. sonchifolia (Table 2). The interactive effects of heterogeneity, AMF, and competition on the total biomass of the plants differed between species (Table 2). Without competition, heterogeneity increased the total biomass of B. pilosa and E. sonchifolia but had no significant effects on the total biomass of E. chinense regardless of AMF inoculation, whereas AMF decreased the total biomass of all species except E. chinense in the heterogeneous treatment (Fig. 3). With competition, heterogeneity increased the total biomass of all species, except E. chinense without AMF inoculation, whereas AMF significantly increased the total biomass of E. chinense in the heterogeneous treatment (Fig. 3).

Table 2

Three-way ANOVA analysis for the effects of heterogeneity, AMF inoculation, and competition on total biomass of plants. Statistically significant values are in bold (P < 0.05).
Species		B. pilosa		E. sonchifolia		P. clematidea		E. chinense
Treatments	df	F	p	F	p	F	p	F	p
Heterogeneity	1	129.118	< 0.001	93.705	< 0.001	152.123	< 0.001	13.113	0.002
AMF	1	11.919	0.002	20.994	< 0.001	0.640	0.430	2.291	0.145
Competition	1	73.783	< 0.001	106.487	< 0.001	0.039	0.845	2.379	0.138
H × AMF	1	22.836	< 0.001	0.000	0.989	9.377	0.005	11.170	0.003
H × C	1	33.261	< 0.001	5.003	0.032	29.302	< 0.001	7.380	0.013
AMF × C	1	12.721	0.001	12.482	0.001	0.013	0.909	2.920	0.102
H × AMF × C	1	7.604	0.010	5.430	0.026	0.108	0.745	2.439	0.133

Shoot N and P uptake

Overall, heterogeneity and competition increased the shoot N and P uptake of B. pilosa and P. clematidea, while heterogeneity increased but competition decreased the shoot N and P uptake of E. sonchifolia (Table 3, Fig. 4). However, AMF exhibited different effects on shoot N and P uptake from different species, and generally AMF had interactive effects with heterogeneity and competition on shoot N uptake (Table 3, Fig. 4).

Table 3

Two-way ANOVA for the effects of soil phosphorus heterogeneity, AMF inoculation on tolerance and suppression competitive ability of *B. Pilosa* and *P. clematidea*. Statistically significant values are in bold (p < 0.05).
		B. pilosa				P. clematidea
Treatments		Tolerance RII		Suppression RII		Tolerance RII		Suppression RII
	df	F	p	F	p	F	p	F	p
Heterogeneity	1	149.788	< 0.001	0.062	0.807	59.008	< 0.001	21.198	0.001
AMF	1	8.874	0.009	5.527	0.032	0.054	0.819	11.153	0.009
H × AMF	1	11.869	0.003	6.319	0.023	0.202	0.659	6.190	0.035

Competitive ability of the invasive species B. pilosa and P. clematidea

The competitive abilities of the two invasive species exhibited different responses to heterogeneity and AMF (Table 4 and Fig. 5). Heterogeneity significantly decreased the tolerance RII of B. pilosa but increased that of P. clematidea (Fig. 5A, 5C). In the heterogeneous treatment, AMF significantly promoted the tolerance RII of B. pilosa but had no significant effects in the homogeneous treatment, resulting in a significant heterogeneity × AMF interaction on tolerance RII (Table 4, Fig. 5A). Regarding suppressive competition, AMF significantly decreased the suppression RII of B. pilosa in the homogeneous treatment but decreased that of P. clematidea in the heterogeneous treatment, whereas heterogeneous phosphorus with AMF inoculation increased the suppression RII of B. pilosa but decreased that of P. clematidea (Table 4, Fig. 5B, 5D).

Table 4

Two-way ANOVA for the effects of heterogeneity and competition on mycorrhizal growth responsiveness (MGR) of plants. Statistically significant values are in bold (p < 0.05).
Treatments	df	B. pilosa		E. sonchifolia		P. clematidea		E. chinense
Treatments	df	F	p	F	P	F	p	F	p
Heterogeneity	1	2.571	0.128	3.655	0.074	5.977	0.026	33.099	< 0.001
Competition	1	17.831	0.001	0.696	0.416	1.060	0.319	31.071	< 0.001
H × C	1	5.557	0.031	5.929	0.027	0.460	0.507	23.162	< 0.001

In general, soil nutrients were distributed in a heterogeneous or patchy manner. Plants respond to soil nutrient heterogeneity by adjusting root morphology and physiological plasticity to improve their foraging ability (Jackson et al., 1990; Hodge, 2004; Kembel and Cahill, 2005), and soil nutrient heterogeneity often promotes the growth of invasive plants because they take advantage of the heterogeneous nutrients (James et al., 2009; Zhou et al., 2011; Wang et al., 2017; Shen et al., 2019; Liang et al., 2020; Wang et al., 2021). The results of the pair of invasive–native species (B. pilosa vs. E. sonchifolia) support our prediction that AMF significantly reduced the root-foraging scale of the invasive species and reduced the foraging precision of native species. In addition, AMF inoculation eliminated the foraging advantage of the two invasive species B. pilosa (advantage of scale) and P. clematidea (advantage of precision) over the native species (Fig. 2). Heterogeneity and AMF exerted different effects on the competitive ability of the two invasive species compared to their native counterparts (Fig. 5). On the other hand, competition altered the effects of AMF on plant growth, and these effects were dependent on P distribution (Fig. 5).

The effects of AMF on host plants range from mutualism to parasitism, with variations in soil nutrient availability (Johnson et al., 1997; van Der Heijden et al., 1998; Johnson et al., 2015; Jin et al., 2017; Brundrett and Tedersoo, 2018; Bennett and Groten, 2022). Our previous study showed that AMF facilitated the growth of B. pilosa under low P nutrient status, but inhibited its growth under high P nutrient status (Chen et al., 2020). Du et al. (2009) found that AMF can significantly modify the effects of clonal integration on the plasticity and performance of clonal plants in heterogeneous environments, and AMF may partly replace the benefits of clonal integration in low-nutrient habitats. Our monoculture results showed that AMF generally exhibited negative effects on plant growth, and these effects were species-specific and dependent on the soil P distribution (Fig. 2). The total biomass of the two invasive species, B. pilosa and P. clematidea, was significantly decreased by AMF under heterogeneous treatment rather than homogeneous treatment (Fig. 2), whereas heterogeneity decreased their mycorrhizal growth responsiveness (MGR) and shifted the positive effects of AMF to negative effects on the growth of B. pilosa (Table S1, Fig. S1). These results do not support our hypothesis that AMF facilitate the growth of invasive plants. Negative or parasitic effects of AMF on host plants often occur when the net cost of symbiosis exceeds the net benefits. The parasitic effects of AMF are known as 'cheating,' and are generally characterised by low nutrient delivery and/or high C demand by the fungus (Bennett and Groten, 2022). This was confirmed by our monoculture results, which showed that AMF significantly reduced the uptake of N and P from the shoots of E. sonchifolia under homogeneous treatment, and reduced the uptake of N and P from the shoots of B. pilosa and P. clematidea under heterogeneous treatment (Fig. 4). In general, plants can proliferate their roots or mycorrhizal hyphae to explore and acquire resources from nutrient-rich soil patches (Hodge, 2006), and invasive plants often differ in root-foraging traits (scale and precision) from those of native species (Rajaniemi and Reynolds, 2004; Drenovsky et al., 2008; Chen et al., 2018). Our previous study found that two exotic invasive plants (Bidens pilosa and Mikania micrantha) had a larger foraging scale, whereas two native plants (Vernonia cinerea and Paederia scandens) had higher precision (Chen et al., 2018). Given that the metabolic cost of hyphal growth is much lower owing to its smaller diameter, AMF may be more flexible in responding to soil nutrient patches than to roots (Hodge, 2006). Furthermore, when large numbers of roots and mycorrhizal fungal hyphae are close together, the mycorrhizal roots likely compete for limited soil nutrients (e.g., N and P), indicating a trade-off between root foraging and AMF (Felderer et al., 2013). However, little is known about the effects of AMF on root foraging in invasive and native species. Our results showed that AMF cheated the root-foraging scale and precision of the host plants. AMF cheated B. pilosa, and E. sonchifolia and P. clematidea by decreasing the root foraging scale and decreasing root foraging precision, respectively (Fig. 2). This indicates that there is a trade-off between root foraging traits and AMF inoculation (i.e., foraging scale versus AMF for B. pilosa and foraging precision versus AMF for E. sonchifolia and P. clematidea). The decrease in the precision of root foraging in E. sonchifolia and P. clematidea caused by AMF is supported by previous studies showing that inoculation with AMF inhibits the preferential allocation of roots in P-rich patches (Cui and Caldwell, 1996; Felderer et al., 2013).

Competition has long been considered a major mechanism determining the success of some invasive species (Levine et al., 2003). Soil nutrient heterogeneity and AMF can influence the competitive ability and expansion of invasive plants (Gao et al., 2014; Zhang et al., 2017; Zhang et al., 2018; Gao et al., 2021; Luo et al., 2021). Gao et al. (2021) found that nutrient heterogeneity promoted the growth of invasive plants, but their relative abundance did not change when competing with the native community. Some studies have shown that AMF promote the competitive ability of invasive plants with native plants (Zhang et al., 2018; Dong et al., 2021), while others have found that AMF reduces the ability of invasive plants to compete with native plants (Luo et al., 2021). Additionally, other studies have suggested that AMF may contribute to the resistance to invasion of native plants and communities (Waller et al., 2016; Cheng et al., 2019). However, the interactive effects of nutrient heterogeneity and AMF on the competition between invasive and native plants remain unclear. Our results showed that heterogeneity and AMF had different effects on the competitive ability of the two invasive species compared to their native counterparts (Table 4, Fig. 5). Consistent with our prediction that heterogeneity can improve the competitive ability of invasive species, heterogeneity increased the competitive tolerance of the invasive species P. clematidea (Table 4; Fig. 5). However, inconsistent with our predictions, heterogeneity reduced the competitive tolerance of the invasive species B. pilosa (Table 4, Fig. 5). There was a significant heterogeneity × AMF interaction on tolerance and suppression RII of B. pilosa and suppression RII of P. clematidea (Table 4, Fig. 5). Under heterogeneous conditions, AMF increased the competitive tolerance of B. pilosa. This is supported by a meta-analysis showing that non-native plants outperform their native counterparts due to their high tolerance to competition rather than their strong suppressive ability (Golivets and Wallin, 2018). The results indicated that heterogeneity induced a stronger AMF effect on tolerance rather than on the suppression of B. pilosa (Fig. 5), which is consistent with the finding that strong competitors can select tolerance to competition more than the ability to suppress neighbours (Fletcher et al., 2016; Golivets and Wallin, 2018). However, this was not the case for another invasive species, P. clematidea. Heterogeneity induced a negative AMF effect on competitive suppression. Interestingly, similar to the competitive suppression of P. clematidea in the heterogeneous treatment, AMF decreased the suppression of B. pilosa in the homogeneous treatment group. This is consistent with results showing that the invasive species Centaurea solstitialis (yellow star thistle) was more strongly suppressed by the established native bunchgrass Stipa pulchra in the presence and absence of AMF (Waller et al., 2016).

It has been well documented that CMNs connect neighbours and exchange resources (e.g., C, N, and P) between plants (Barto et al., 2012; Wipf et al., 2019). We found that competition altered the effects of AMF on plant growth and nutrient uptake, and the effects were species-specific and dependent on the distribution of P. Competition significantly increased the MGR of B. pilosa under the heterogeneous treatment, and the MGR of E. sonchifolia under the homogeneous treatment (Table S1, Fig. S1). In general, competing with the invasive species B. pilosa significantly decreased shoot N and P uptake of the native species E. sonchifolia regardless of heterogeneity and AMF inoculation (Fig. 4). It seems that B. pilosa probably derived N and P via CMN to benefit from AMF, but its neighbour, E. sonchifolia contributed biomass for AMF to pay for the cost. However, this was not the case for another native–invasive pair (E. chinense and P. clematidea), where competition increased the positive effects of AMF on the uptake of N and P by E. chinense much more than that of its invasive counterpart P. clematidea (Fig. 4). These results imply that the effects of nutrient heterogeneity, AMF, and competition on plant growth and nutrient uptake show invasive-native pair differences.

Notably, different species of AMF have different functions (Reynolds et al., 2005; Wu et al., 2023), and the effects of AMF on invasive plants range from positive to negative depending on the host plant and fungal species (Aslani et al., 2019). Further studies are needed to explore the effects of different AMF species on the competition between native and invasive plants and to explain the role of AMF in the success of plant invasion in a heterogeneous environment.

Acknowledgments

We thank Carla M. D’Antonio and Hui-Xuan Liao for their valuable comments. We also thank the undergraduates Hui Xu and Ji-Kang Hu for their help harvesting plants and sampling soil.

Authors contribution

NNY, SLP, and BMC conceived and designed the experiment, NNY, XJW, SQF, and BMC carried out the experiment, NNY, HHD, HJZ and BMC analyzed the data, NNY and BMC drafted the manuscript, all authors contributed to its revision and approved the version to be submitted for publication.

Funding

This study was supported by the National Natural Science Foundation of China (31971556, 38100459), the Natural Science Foundation of Guangdong Province (2023A1515010669, 2020A1515011054), the Science and Technology Program of Guangzhou (202102020791), and the Hongda Zhang Science Research Fund of Sun Yat-sen University.

Data availability

Data are available on FigShare (https://figshare.com/s/1c3652bdf851e502f19c).

Competing interests The authors have no relevant financial or non-financial interests to disclose.

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Effects of arbuscular mycorrhizal fungi on root foraging and competitive ability between native and invasive plants

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Soil collection and preparation

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Root foraging scale and precision

Plant biomass

Shoot N and P uptake

Competitive ability of the invasive species B. pilosa and P. clematidea

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