Opposing effects of soil biota on a native plant shoot and root growth in the presence of a invasive competitor

doi:10.21203/rs.3.rs-3211845/v1

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Opposing effects of soil biota on a native plant shoot and root growth in the presence of a invasive competitor

https://doi.org/10.21203/rs.3.rs-3211845/v1

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Aims: Soil biota can affect native and alien species differently, and consequentially promote or suppress alien species invasion. However, how soil biota influence the competition between native and alien species has rarely been explored. Methods: Here, our study tested how the rhizosphere biota of the invasive plant Alternanthera philoxeroides and its native congener A. sessile in China affected their competition with a greenhouse experiment.

Results: We found that soil biota, regardless from the rhizosphere of the native or the invasive plant, increased native plant total and shoot mass in the presence of the invasive plant but not in the presence of conspecific individual. Furthermore, soil biota from its own rhizosphere soils decreased native plant root mass in the presence of the invasive plant. Therefore, the native plant accumulated more shoot and total mass, but less root mass than the invasive plant only in the presence of soil biota.

Conclusions: Overall, our results highlight the importance of exploring the roles of soil biota in plant competition within a whole plant framework.

Alien plant invasions

plant competition

plant-soil interactions

soil biota

species co-existence

Alien invasive plants pose a major threat to native plant diversity (Powell et al. 2013), and elucidating the mechanisms of their invasions is a central goal of invasion biology (van Kleunen et al. 2018). Amounting evidences have demonstrated that soil biota can promote or hinder plant invasions (Callaway et al. 2004; Dawson and Schrama 2016). Plants are known to condition soil biotic communities that in turn positively, neutrally or negatively influence subsequent conspecific and heterospecific individuals grown in the same soils (termed as plant-soil feedbacks) (Bever et al. 1997; van der Putten et al. 2013). For instance, some invasive plants may establish and maintain dominances in a novel environment due to the release of their co-evolved specialist soil pathogens or the recruitment of generalist pathogens that asymmetrically suppress native plants (Suding et al. 2013). In contrast, invasive plants also suffer stronger negative effects from soil biota conditioned by other native plants, thereby becoming less competitive in communities containing native plants (Callaway et al. 2013). To date, however, the majority of existing studies testing how soil biota affect plant invasion only compared plant-soil interactions between native vs. alien species in the absence of competition, and thus whether soil biota confer competitive advantages to alien species rather than native species remains unclear (but see Larios and Suding 2015; Crawford and Knight 2017; Koorem et al. 2020).

When two plants compete, the performances of both individuals may be affected through the changes in soil biotic communities and other important abiotic factors (e.g. water, light and nutrient availability). Thus, plant competition has the potential to alter the magnitudes and directions of plant-soil interactions mediated by soil biota (Casper and Castelli 2007; Jing et al. 2015; Bezemer et al. 2018; Xi et al. 2020; Huangfu et al. 2022). Compared to the presence of conspecific individual (intraspecific competition), the presence of heterospecific individual (interspecific competition) may intensify the negative effects of soil biota on the focal plant via the proliferations of soil pathogens (spillover effects), and this result was only found in weaker competitor Anthoxanthum odoratum (Xue et al. 2018). However, presence of interspecific competition may also relieve the focal plant from the negative plant-soil interactions by suppressing its host-specific soil pathogens (dilution effects) (Shannon et al. 2012). Although these studies have indicated that the effects of soil biota depended on competitive environment and species identity, whether the presences of intra- vs. interspecific competition influence plant-soil interactions between native and invasive plants differently is unclear. Given the importance of the relative strength of intra- vs. interspecific competition in species co-existence (Aschehoug et al. 2016; Adler et al. 2018), such information will shield new insights into the role of soil biota in plant invasions and co-existence.

Interestingly, several studies have found the differential responses between plant above- and belowground parts (e.g. shoot and root) to soil biota (Hendriks et al. 2015; Wang et al. 2021). For example, the negative effects of soil biota on root growth could be stronger than the ones on shoot growth because plant roots established associations with soil biota earlier than shoots (van der Putten and Peters 1997). Alternatively, this pattern may come the opposite (i.e. shoots suffer weaker negative effects of soil biota) due to relatively larger size/biomass of shoots rather than roots (Mommer et al. 2010). Plant shoots and roots have also been proved to respond differently to the interactive impacts of soil biota and plant competition (Koorem et al. 2020; Huangfu et al. 2022). Hence, such spatial variations may contribute to the different competitive dominances between native and invasive plants. However, no study has tested the role of soil biota in both above- and belowground competition between phylogenetically related native and alien invasive species.

Thus, we studied how soil biota influence the inter- vs. intraspecific competition for the invasive plant Alternanthera philoxeroides and its native congener A. sessilis in China. This system is well suitable for our study. A. philoxeroides co-occurs with A. sessilis along its latitudinal range and their competitive abilities differ in both above- and belowground parts (Lu et al. 2015a, b, 2016). Moreover, the invasive plant suffer a greater negative effect of soil biota on shoot growth than the native plant only when grown in its ‘foreign soil’ rather than ‘home soil’ (Wang et al. 2021), suggesting that soil biota may promote A. philoxeroides invasions. However, this pattern is absent for the effects of soil biota on root growth (Wang et al. 2021), so the observed differences in above- and belowground plant-soil interactions may result from the interactions of soil biota origin and plant part. Besides, our findings may be inaccurate in the field as we did not include competition as an experimental factor. Furthermore, other factors (e.g. the latitudinal variations in plant population and soil biota) were also neglected, leaving their potential impacts on plant growth and invasions unexplored.

To assess whether soil biota confer competitive advantages for the invasive plant and facilitate its invasion, we grew native and invasive plants of the same population under intra- or interspecific competition in the absence of soil biota or in the presence of soil biota from rhizosphere of conspecific and heterospecific individuals that were originated from five latitudinal sites in a greenhouse experiment. Based on plant total, shoot and root mass, we quantified the effects of soil biota as their ln response ratios between inoculated vs. non-inoculated soils respectively (Brinkman et al. 2010). Then, we explored the interactive impacts of soil origin (conspecific vs. heterospecific soils), competition treatment (intra- vs. interspecific competition) and plant species (alien vs. native species) on these soil biota effects on total, shoot and root mass separately, with soil sample site (five sites) and plant population (two populations) as random factors. We also tested the differences between total, shoot and root mass of these two species under either intra- or interspecific competition in the absence or presence of soil biota. Specifically, we predicted that (1) the negative effects of soil biota on the native plant (total and shoot mass) would be weaker when intraspecific competition was altered to interspecific competition, regardless of soil origin; (2) interspecific competition might intensify the negative effects of soil biota on root mass only for the native plant, while this pattern might be absent for the invasive plant potentially due to its greater defence to root infection (Lu et al. 2015b); and (3) if so, soil biota would increase the above-ground competitive ability of the native plant in the presence of the invasive plant, but would decrease its below-ground competitive ability.

Study species

Alternanthera philoxeroides (Amaranthaceae), native to South America, has invaded an area up to 36.8 °N in China (Lu et al. 2013). Alternanthera sessilis, native to China, frequently co-occurs with A. philoxeroides across its whole latitudinal ranges (Lu et al. 2015a). In China, the invasive plant propagates only via clonal stems and buds which make it difficult to manage (Lu and Ding 2010). In comparison to its native congener, the invasive plant mainly has coarse roots with thick cuticles and higher root-to-shoot mass ratio, therefore being highly resistant to root infection (Lu et al. 2015b).

Collection of soils and plants

Since the composition of soil biota communities can change greatly across the latitude, such latitudinal variations in soil biota might contribute to the differential outcomes of plant-soil interactions between co-occurring native and invasive plants (Lu et al. 2018; Wilschut et al. 2019). Hence, we collected the rhizosphere soils of both A. sessilis and A. philoxeroides monocultures at five sites in China in October 2018 (Guangdong/GD: 23.3 °N; Guangxi/GX: 25.2 °N; Hubei/HU: 28 °N; Henan/HE: 34.8 °N; Shandong/SD: 36.1 °N), which have been investigated in our previous study (Lu et al. 2018). Briefly, soil cores (2.5 cm in diameter, 10 cm in depth) of each species were collected at five locations (at least 10 km apart) for each soil sample site in order to account for spatial heterogeneity. All soils were immediately stored in plastic bags and were kept at 4°C. Moreover, varying populations/genotypes of a specific native or alien species can also interact differently with the same soil biota mainly due to the intraspecific variation in plant population (Allen et al. 2018; Huang et al. 2021), so we collected stems for each species at GD and SD sites respectively (hereafter southern and northern populations). The collection of soils and plants was finished within two weeks

In our lab, all soil samples of each site and rhizosphere species combination were mixed and passed through a 2.5-mm sieve to homogenize soil and remove plant tissue. For each sample, the mixed soil was used to prepare soil inoculum (Wang et al. 2019). Specifically, we added 900 g pure water to 100 g fresh soil (9: 1, w/w) in a 2-L beaker, stirred completely for 30 s and sieved through a 212-µm sieve to produce the final soil inoculum. Moreover, enough top soils (0–10 cm) from a local field were collected and sterilized with γ-radiation (dose > 25 Gy). To exclude the impact of any abiotic factor and only focus on soil biota, we added 100 ml pre-prepared watery inoculum to 1.5-L pots filled with 1200 ml sterile soils (1: 12, v/v) as inoculated soil treatment, and also added 100 ml pure water to such pots as non-inoculated soil treatment. Field-collected stems of each species from two populations were cultivated by putting their cut stems into sterile soils until greenhouse experiment. All tools used in these procedures were sterilized by bleach immersion (24 hrs).

Greenhouse experiment

From May to September 2019, we conducted our experiment in a same greenhouse in Wuhan, China (Wang et al. 2021). To clarify the interactive impacts of soil biota from varying latitudinal sites and plant hosts, as well as plant competition on performances of A. sessilis and A. philoxeroides and the outcomes of their plant-soil interactions, we transplanted similar-size stems of each species from the same population into the pots under intra- and interspecific competition (Fig. 1). For pots added with soil inoculum, we assigned each pot to one of six planting treatments (each replicated six times): (1) southern, A. sessilis + A. sessilis; (2) southern, A. philoxeroides + A. philoxeroides; (3) northern, A. sessilis + A. sessilis; (4) northern, A. philoxeroides + A. philoxeroides; (5) southern, A. sessilis + A. philoxeroides; and (6) northern A. sessilis + A. philoxeroides. For pots added with pure water, we assigned each pot to one of six planting treatments (each replicated five times). Totally, our experiment had 390 pots (5 soil sample sites × 2 soil origins × 6 planting treatments × 6 replicates, as well as 6 planting treatments × 5 replicates in sterile soils). During the experiment, we placed these pots randomly and readjusted their positions weekly. We watered plants with pure water if necessary. Three months later, we harvested plant shoots and rinsed roots to remove the adhering soils. We dried shoots and roots at 80°C (48 hrs), and then weighed them respectively. Plant total mass was calculated as the sum of shoot and root mass.

Statistical analysis

All statistic analyses were conducted in R 4.1.2 (R core team 2021). We calculated the individual total, shoot and root mass for both native and invasive plants under intra- or inter-specific competition respectively. We quantified the effects of soil biota based on total, shoot and root mass between inoculated (live) and non-inoculated (sterile) soils, which were calculated as ln(biomass_live/biomass_sterile) (Brinkman et al. 2010). We used linear mixed models to assess the impacts of soil origin (conspecific vs. heterospecific individual’s rhizosphere, fixed factor), competition treatment (intra- vs. interspecific competition, fixed factor), plant species (A. sessilis vs. A. philoxeroides, fixed factor), their interactions (fixed factor), plant population (two populations, random factor) and soil sample site (five sites, random factor) on soil effects on total, shoot and root mass separately using the lme4 package (Bates et al. 2015). For those significant interactive impacts (e.g. the interaction of soil origin, competition treatment and plant species and the interaction of competition treatment and plant species), we tested the differences among treatment combinations by the adjusted means partial difference tests using the agricolae package (Mendiburu 2021). Two-sample student’s t-tests were then utilized to test the differences between soil effects under intra- vs. interspecific competition if there was no above-mentioned significant interactive impact. We utilized one-sample student’s t-tests to determine whether soil effects differed from zero (P ≤ 0.05), where values higher or lower than zero note positive or negative effects of soil biota.

For plants that grown in inoculated soils, we used similar linear mixed models to test the impacts of soil origin (fixed factor), competition treatment (fixed factor), plant species (fixed factor), their interactions (fixed factor), plant population (random factor) and soil sample site (random factor) on their total, shoot and root mass separately. For plants that grown in non-inoculated soils, linear mixed models were also performed to assess the impacts of competition treatment (fixed factor), plant species (fixed factor), their interaction (fixed factor) and plant population (random factor) on total, shoot and root mass separately. For those significant interactive effects, we tested the differences among treatment combinations as described before. Also, two-sample student’s t-tests were utilized to test the differences between total, shoot and root mass of the native vs. invasive plants if there was no significant interactive effect.

The effects of soil biota on both total and shoot mass were affected by the interaction of competition treatment and plant species (Table S1). Under intraspecific competition, soil biota generally decreased the total and shoot mass for the native or invasive plant (Fig. 2). Only for the native plant, the negative soil effect on either total or shoot mass became weaker as intraspecific competition was switched to interspecific competition (Fig. 2), and these differences were also found for the native plant in the presence of conspecific and heterospecific soil biota (Fig. S1). In contrast, we found no significant difference between soil effect on total or shoot mass for the invasive plant between the two competition treatments, regardless of soil origin (Figs. 2 and S1).

The effect of soil biota on root mass was affected by the interaction of soil origin, competition treatment and plant species (Table S1). Soil biota decreased root mass for the native plant that grown in heterospecific soils under intraspecific competition, but did not decrease root mass for the invasive plant that grown in each soil origin (Fig. 3). Soil biota from its own rhizosphere soils also decreased root mass for the native plant under interspecific competition, but the negative effect on root mass was stronger than that under intraspecific competition (Fig. 3). But for the invasive plant, soil effect on root mass did not significantly vary between two competition treatments, regardless of soil origin (Fig. 3).

When grown in non-inoculated soils, the native plant produced more shoot mass and less root mass than the invasive plant under intraspecific competition though their total mass did not significantly vary (Table S2, Fig. 4A, C, E). Similarly, when grown in inoculated soils, the native plant also performed better in shoot growth and worse in root growth than the invasive plant under intraspecific competition (Table S3, Fig. 4D, F), and such differences were found in the presence of conspecific and heterospecific soil biota (Fig. S2B-C). Interestingly, the native plant outperformed the invasive plant in total and shoot growth under interspecific competition in the presence of soil biota rather than in the absence of soil biota, regardless of soil origin (Figs. 4A-D and S2A-B). On contrary, the native plant produced less root mass than the invasive plant under interspecific competition in the presence of conspecific soil biota (Fig. S2C), thereby leading to its worse root growth in the presence of soil biota but not in the absence of soil biota (Figs. 4E-F).

In this study, we found that soil biota, regardless from the rhizosphere of the native or invasive plant, benefited the native plant under interspecific competition primarily due to the response of shoot mass. But from the aspect of root growth, soil biota benefited the invasive plant in the presence of its native congener when grown in its home soils. Consequently, the native plant produced more shoot and total mass, but less root mass than the invasive plant in the presence of soil biota but not in the absence of soil biota. Together, these results may suggest that the net effects of soil biota on the competition between these two plants will depend on both the responses and relative contributions of above- vs. belowground tissues to their competition.

Weakened negative plant-soil interactions via the release of soil-borne pathogens are considered as an important mechanism promoting plant invasions (Inderjit and van der Putten 2010; Suding et al. 2013). Results of our greenhouse experiment found that both total and shoot growth of the native or invasive plant were negatively influenced by soil biota originated from each species’ rhizosphere under intraspecific competition, showing a stronger role of soil-borne enemies than mutualists (Kulmatiski et al. 2008). However, soil effect on total or shoot mass did not significantly vary between the two species that grown in conspecific and heterospecific soils, contrary to a previous study (Wang et al. 2021). The reason may be that southern and northern populations of each species responded differently to our experimental treatments (the impact of population as a random factor was significant), which is consistent with other studies (Allen et al. 2018; Huang et al. 2021). Moreover, soil effect on root mass was negative and neutral for the native and invasive plants that grown in heterospecific soils under intraspecific competition respectively, but their difference was insignificant (Fig. 3). Overall, these findings suggest that soil biota may not benefit this invasive plant via asymmetrically suppressing total, above- and belowground performances of its native congener.

Interestingly, the native plant suffered a weaker negative soil effect on its total or shoot mass under interspecific competition than under intraspecific competition (Fig. 2), in line with existing studies (Casper and Castelli 2007; Shannon et al. 2012). Also, such differences were found for the native plant in conspecific and heterospecific soils, while did not occur for the invasive plant when cultivated in each soil origin (Fig. S1). One possible explanation is that this invasive plant suppressed some host-specific soil pathogens for its native congener when they were grown together, as A. philoxeroides at low densities could also rapidly develop taxonomically distinct communities of soil pathogens (Wang et al. 2021). Our findings in combination with other studies (Casper and Castelli 2007; Shannon et al. 2012) show that the negative plant-soil interactions on plant total and shoot growth may be more apparent under interspecific competition than under interspecific competition, as predicted by the first hypothesis. On contrary, only soil biota from its own rhizosphere soils decreased root mass for the native plant in the presence of the invasive plant, and the negative effect on root mass was greater than that under intraspecific competition (Fig. 3). Furthermore, this pattern was absent for the invasive plant potentially due to its higher resistance to root infection (e.g. soil pathogens) (Lu et al. 2015b). This agrees with our second prediction and suggests that the presence of interspecific competition can amplify the negative effects of soil biota on weak rather than strong plant competitors (e.g. A. sessilis vs. A. philoxeroides), in line with other studies (Xue et al. 2018; Xi et al. 2020). Thus, the differences between the impacts of competition on above- and belowground plant-soil interactions suggest that plant shoots and roots can also respond differently to their interaction impacts via biomass allocation or niche differentiation (Hendriks et al. 2015; Koorem et al. 2020), which has great implications in plant invasions and co-existence (Lekberg et al. 2018; Ke and Wan 2020).

Moreover, the native plant produced more shoot mass and less root mass than the invasive plant in the absence or presence of soil biota under intraspecific competition. In contrast, there was no difference between their total mass, that is, soil biota did not benefit the invasive plant from the aspect of total growth when compared to its native congener. Surprisingly, the native plant outperformed the invasive plant in its total and shoot growth under interspecific competition, regardless of soil origin (Figs. 4 and S2). This may be the result of the weaker negative effects of conspecific and heterospecific soil biota on the native plant when competing with the invasive plant, as we discussed before. But from the aspect of belowground competition, the native plant accumulated less root mass than the invasive plant in the presence of soil biota from its rhizosphere but not the other’s rhizosphere, which also corresponds to the differential outcomes of their plant-soil interactions (Figs. 3 and S2). Overall, soil biota may benefit the native plant in the presence of its invasive competitor primarily due to the response of shoots, while in contrast, soil biota promoted root mass for the invasive plant, as predicted by our third hypothesis. Given that the higher root mass allocation (i.e. root-to-shoot ratio) may enable A. philoxeroides to tolerate aboveground herbivory (Lu et al. 2015b), soil biota are expected to promote its performances and invasions when competing with its native congener in the presence of aboveground herbivores.

Our results raise the possibility that the promotive effects of soil biota on above- and belowground competitive abilities for the invasive plant may differ and depend on the origin of soil biota. However, it is unclear about whether and how the presence of interspecific competition changes the composition of soil biota, such as fungi, bacteria and nematode, because we did not sequence and characterize their composition. Thus, we provide no evidence of the linkages between those competitor-induced changes in soil biota and the outcomes of plant-soil interactions for both native and alien species as before (Lu et al. 2018; Wang et al. 2021). Moreover, all findings of our greenhouse experiment (e.g. plant growth and effects of soil biota) may occur when grown in soils from five sites as the impact of soil sample site as a random factor was not significant, which can explain the successful invasion and high-latitude expansions of the invader A. philoxeroides in China (Lu et al. 2018). Given that results of plant-soil interactions under controlled greenhouse may be inapplicable in natural systems (Kulmatiski et al. 2008; De Long et al. 2019), further field studies are required to verify our findings for multi-pair phylogenetically related native and alien species, and to test its potential in controlling alien species and protecting native species.

In summary, our study shows that the presence of the invasive species can relieve the native species from negative plant-soil interactions regardless of soil origin, which in turn promotes its total and shoot growth. However, soil biota promoted root growth for the invasive species in the presence of its native congener only when planted in its home soils. Hence, the native species accumulated more total and shoot mass, but less root mass than its invasive competitor only in the presence of soil biota. These results suggest that plant shoots and roots displayed asymmetrical responses to the interactive impacts of soil biota and interspecific competition, which emphasizes the necessity of exploring plant-soil interactions from a whole-plant perspective.

Acknowledgements

The authors would like to thank Bingbing Jia, Hao Xu, Shuai Jiang, and Xiaoqiu Sun for their assistance in the field and lab. This work was supported by NSF-China (31872034 and 31570540), Fundamental Research Funds for the Central Universities (2662020ZKPY007) and the start-up funding of Huazhong Agricultural University (101-110200201).

Author contributions

X.L. conceived this study and designed the experiments. X.T., C.W. and L.G. performed the experiments. H.Z. and X.L. analyzed data, interpreted the results and wrote the manuscript. All authors contributed to the final version of the article.

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SupportingInformation.docx
Supporting Information Table S1. The impacts of soil origin, competition treatment, plant species and their interactions on the effects of soil biota based on total, shoot and root mass. Significant results are shown in bold. Table S2. The impacts of competition treatment, plant species and their interaction on total, shoot and root mass of plants grown in non-inoculated soil. Significant results are shown in bold. Table S3. The impacts of soil origin, competition treatment, plant species and their interactions on total, shoot and root mass of plants grown in inoculated soil. Significant results are shown in bold. Figure S1. The effects of soil biota on (A) total and (B) shoot mass of the native (Alternanthera sessilis) and invasive (Alternanthera philoxeroides) plants under intra- or interspecific competition when plants were grown in soils collected from conspecific (home soil) and heterospecific (foreign soil) individuals. Error bars are 95% confidence intervals and asterisks show a significant difference from zero (P ≤ 0.05). P-values ≤ 0.05 shown above paired bars indicate a significant difference between these two competition treatments. Figure S2. (A) Total, (B) shoot and (C) root mass of the native (Alternanthera sessilis) and invasive (Alternanthera philoxeroides) plants under intra- or interspecific competition when plants were grown in soils collected from conspecific (home soil) and heterospecific (foreign soil) individuals. Mean + 1 SE. P-values ≤ 0.05 shown above paired bars indicate a significant difference between these two species.

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Opposing effects of soil biota on a native plant shoot and root growth in the presence of a invasive competitor

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Abstract

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Introduction

Methods

Study species

Collection of soils and plants

Greenhouse experiment

Statistical analysis

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Supplementary Files

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