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Research Article
Uprooting is a promising tool to control invasive giant ragweed and recover native diversity
expand article infoChaeho Byun, Kripal Singh, Sun Hee Hong§, Jangho Lee, Tae Kyung Yoon|, Hojeong Kang
‡ Andong National University, Andong, Republic of Korea
§ Hankyong National University, Anseong-si, Republic of Korea
| Sangji University, Wonju, Republic of Korea
¶ Yonsei University, Seoul, Republic of Korea
Open Access

Abstract

Ambrosia trifida (giant ragweed) is an invasive species that causes habitat destruction and competitively excludes native plants in many parts of Europe and Asia. In this study, we evaluated the effects of selective cutting and uprooting on A. trifida and native plant diversity, as well as the effects of sowing the seeds of native annual, perennial and woody species after eradication. We hypothesised that: (i) selective uprooting will be more effective than cutting in controlling invasion by A. trifida because fewer propagules would be left behind, with no increase in the number of existing invasive propagules and (ii) sowing native seeds will increase invasion resistance and accelerate the recovery of native plant diversity. The eradication methods were applied in July 2022, seeds were sown in March 2023 and the response variables (i.e. importance values (%) of A. trifida and diversity index (H') of native species) were measured in September 2023. The importance values of A. trifida were lowest and diversity index of native species was highest in the uprooting treatment, supporting the first hypothesis. Sowing native seeds following invasion removal did not exert significant additional suppressive effects on invasion or increase native species diversity. These results reveal that selective uprooting is a promising tool to control A. trifida and to support the recovery of native diversity, while sowing native seeds does not improve the quality of restoration.

Key words

Ambrosia trifida, ecological restoration, eradication methods, diversity index, hand-pulling, native diversity, invasive plant management, selective cutting, selective uprooting

Introduction

Biological invasion is a major factor contributing to global ecological and socioeconomic instability (Simberloff et al. 2013; Roy et al. 2023). Invasive alien plants cause biodiversity loss through the competitive exclusion of native species, ultimately leading to the loss of valuable endemic species (Vilà et al. 2011; Jaureguiberry et al. 2022; Adhikari et al. 2023). Invasive plants often disrupt ecosystem processes (Pearson et al. 2018), such as nutrient and water cycling (Vilà et al. 2011) and alter the soil composition (Castro‐Díez et al. 2019). Several plant species in introduced areas produce allergens (Shackleton et al. 2016) and cause severe health issues. Shifts in biological integrity and natural ecosystem processes due to invasive plants affect the supply of ecosystem services, livelihoods and human well-being (Shackleton et al. 2018). Therefore, managing plant invasion is crucial for conserving biodiversity and sustaining natural ecosystems and human health. The management of invasive species includes the early identification of new invasive species, prevention of spread, eradication of existing invasive species and subsequent restoration initiatives (Pyšek and Richardson 2010).

Ambrosia trifida L., or giant ragweed, is an annual herb native to North America (Laforest et al. 2024). It is adapted to a wide range of habitats, including agricultural fields, roadsides and disturbed areas, contributing to its invasive success in Europe and East Asia (Abul‐Fatih and Bazzaz 1979; Soltani et al. 2011; Chauvel et al. 2021). Its rapid growth, high seed production and tolerance to a variety of ecosystem disturbances and environmental conditions allow it to outcompete native plants and associated fauna (Regnier et al. 2016; Dong et al. 2020a; Chauvel et al. 2021; Wang et al. 2022; Xian et al. 2023; Chen et al. 2024). The plant was unintentionally introduced into the Republic of Korea in 1970, probably as a contaminant of agricultural equipment and/or crop seed. It has been considered an invasive species since 1999 (Park et al. 2012); initially, it was discovered near the demilitarised zone, in the central region of Korea (Lee et al. 2010). After it spread throughout the country, it was registered as an ecosystem-disturbing species (Lee et al. 2010; Yin et al. 2010; Kim 2017; Montagnani et al. 2017; Li et al. 2022). Ambrosia trifida has high reproductive ability and is difficult to remove once established. It grows quickly, attains heights of up to 5 m and forms high densities, greatly reducing the growth of native species and economic crops in cultivated areas. Pollen from flowers of A. trifida can also cause allergies (Ling et al. 2022). Therefore, the eradication of A. trifida and restoration of native diversity is of paramount socioeconomic and ecological importance.

A number of mechanical (physical), chemical and biological eradication methods for invasive plant species have been developed (Kettenring and Adams 2011; Weidlich et al. 2020), with variable outcomes in terms of invasion control (Pearson et al. 2016; Chenot et al. 2018; Courkamp et al. 2022) and recovery of native plant communities (Boxriker et al. 2022; Farmilo and Moxham 2023). The mechanical approach involves the physical removal of invasive species through cutting, mowing, uprooting, burning, mechanical harvest and other similar approaches. Except in cases where uprooting is applied, re-sprouting and habitat disturbance facilitate re-invasion and hinder the recovery of native communities (Schooler et al. 2010; Byun et al. 2020a; Nagy et al. 2022). Chemical application is the most frequently used method (Kettenring and Adams 2011) to eradicate specific plant species before and/or after germination. However, the application of herbicides, such as glyphosate, indaziflam, 2,4-2,4-dichlorophenoxyacetic acid and picloram, deters native vegetation and fauna (Carlson and Gorchov 2004; Robichaud and Rooney 2021; Donaldson and Germino 2022) and many nations banned their use to control weeds and invasive species (Peng et al. 2020; Pergl et al. 2020). Although the introduction of natural enemies, such as insects and pathogens (bacteria, fungi, viruses etc.), can hinder the germination, growth and spread of invasive plants (Clewley et al. 2012), this approach is logistically complex and not well investigated (David and Lake 2023; Shen et al. 2023). The mechanical method in which invasive species are uprooted is considered a new tool to control invasion (Kollmann et al. 2011) and to have multiple advantages compared with conventional methods, such as cutting because it does not leave any reproductive or regenerative parts of plants behind. This is important because this species can regrow from its roots or stem fragments after cutting or disturbance, which contributes to its resilience and ability to spread rapidly, making it a challenging invasive species to manage. However, selective uprooting can be labour-intensive and time-consuming and its efficiency is unclear, in part owing to the small number of relevant studies (Pickart et al. 1998a; Pickart et al. 1998b; Ussery and Krannitz 1998). Recent empirical studies, systematic reviews and meta-analyses clearly indicate that the use of control methods alone does not facilitate the recovery of native communities, suggesting that it is imperative to consider active restoration initiatives (Kettenring and Adams 2011; Adams et al. 2020; Singh and Byun 2023). For example, sowing native seeds can contribute to the recovery of native communities (Kettenring and Adams 2011).

Extensive research suggests that sowing native seeds after the removal of invasive species can establish native vegetation cover and reduce the probability that invasive species regrow and establish as a result of niche pre-emption and resource utilisation (Levine et al. 2004; Enloe et al. 2005; Sheley et al. 2006). Therefore, native seed addition following invasion control is essential for restoring native diversity (O’Donnell et al. 2016; Johnson et al. 2018). The presence of functionally similar and dissimilar species can provide clues about the potential of various native species to protect against invasion (Sheley and James 2010; Byun et al. 2013). However, Yannelli and colleagues reported that seed density (propagule pressure in ecological terms) is more effective than trait similarity with respect to invasion suppression (Yannelli et al. 2020). Therefore, it is critical to determine if sowing native seeds suppresses invasion and facilitates the recovery of native diversity, as well as the effects of species of different functional groups.

Ambrosia trifida is a noxious weed and its control has been a challenging task at introduced sites and in its native range. The suppression of A. trifida in agricultural fields by the application of various herbicides, growing cover crops and diversifying cropping systems is rarely successful (Kouame et al. 2023; Silva et al. 2023; Werle et al. 2023). Similarly, in natural ecosystems, such as grasslands, the impact of mechanical eradication methods on the spread of A. trifida varies and the approach is generally either ineffective or only slightly effective (Byun and Lee 2018; Park et al. 2020; Byun et al. 2020b; Byun 2023). Intense mowing management of A. trifida followed by sowing native seed suppressed invasion up to 77%; however, seeding did not amplify suppression or facilitate native recovery (Byun et al. 2020b). The competitive ability of A. trifida was not suppressed, even when grown with eight native species from three functional groups (Byun and Lee 2018). However, the effectiveness of selectively targeting only invasive species (A. trifida in this study) by cutting (removing aboveground plant parts) or uprooting (pulling out whole plant) has not been tested. In addition, the impact of sowing native seeds following the selective eradication of A. trifida on native diversity is not known.

This study, therefore, aimed to investigate the effectiveness of mechanical control, including selective uprooting and selective cutting, on the dominance of A. trifida. Although the eradication of invasive species can suppress their dominance to some extent, the recovery of native diversity requires additional assistance (e.g. through sowing seeds following invasive plant removal) (Enloe et al. 2005; Sheley et al. 2006; Kettenring and Adams 2011; Adams et al. 2020; Singh and Byun 2023). Sowing seeds of various functional groups can further protect against invasion through trait similarity (annuals), structural asymmetry (perennials) and diversity (three species). Therefore, we sowed seeds of nine native species from three functional groups (i.e. annual, perennial and woody species) after invasion removal to evaluate whether there are additional benefits in the suppression of A. trifida invasion. We hypothesised that selective uprooting will be more effective than cutting in controlling invasion by A. trifida, because uprooting leaves fewer propagules behind and does not add to the number of existing propagules. We also hypothesised that sowing native seeds will protect against invasion and suppress A. trifida through limiting similarity with annuals and increasing diversity and will accelerate the recovery of native diversity.

Methods

Study site

Experimental plots were installed in July 2022 at two sites in Busan, Republic of Korea separated by 18 km. Site #1 was located at 1200-5 Daejeo 2-dong, Gangseo-gu (35°11'46"N, 128°58'02"E) and site #2 was located at 1211 Hadan-dong (35°05'29"N, 128°56'40"E) (Fig. 1). The sites represent a typical riparian habitat that was originally dominated by A. trifida (> 90% cover).

Figure 1.

Map of the study sites and aerial view of blocks. Blocks A, B are located at site 1 and blocks C–F are located at site 2 in Busan, Republic of Korea.

Removal of invasive A. trifida and sowing native seeds

We applied a split-plot design with main plots consisting of different eradication methods and subplots consisting of different seed mixtures for sowing. Based on the cover and distribution of A. trifida, two blocks at site 1 and four blocks at site 2 were established. Thus, a total of six blocks were prepared. Each block was 10 m × 10 m. Within each block at each site, three main plots measuring 2 m × 2 m were randomly developed and equidistant. All plots were placed 2 m inside the block and plots were situated with distance of 2 m from each other. Three plots represented three treatments (i.e. control (no action), selective cutting and selective uprooting). The layout of the main plots at the six blocks in two sites is shown in Suppl. material 1: fig. S2). Selective cutting and uprooting involved the removal of individuals of A. trifida only, with minimal disturbance to other vegetation. In the case of cutting, all A. trifida individuals were removed by manual cutting using secateurs (pruning shears) and all other plant individuals were left intact. Individuals of A. trifida were cut from the lowest part of the plant stem (right above the ground). For the uprooting treatment, the entire plant, including roots, was uprooted or pulled out from the plots. As A. trifida has a fibrous root system, manual uprooting was easy. Any disturbance to original native plant communities, such as touching them, was minimised. All removal treatments were applied on 20 July 2022 (i.e. shortly before blooming). Within each main plot of 2 m × 2 m, four subplots measuring 1 m × 1 m were prepared for four sub-treatments. Three subplots were sown with three different seed mixtures and the remaining unsown subplot was used as the control. In seed mixture 1 (SM1), the seeds of three annual species (Lactuca indica, Elsholtzia splendens and Portulaca oleracea) were sown at 200 viable seeds of each species per subplot (i.e. 600 seeds m-2 per subplot). A similar method was followed for sowing seed mixture 2 (SM2) including three non-woody perennials (Phragmites australis, Pennisetum alopecuroides and Plantago asiatica) and seed mixture 3 (SM3) with three woody perennials (Lespedeza bicolor, L. juncea and Sorbaria sorbifolia). Seeds in each mixture were broadcast very close to the ground. Each seeded subplot was watered with a 15 L plastic watering pot. Manual watering of each subplot was done only at this stage. The application of seed mixtures was completed between 3 and 4 March 2023.

Species selection and functional classification

Nine native species from three functional groups, annual (Lactuca indica, Elsholtzia splendens and Portulaca oleracea), non-woody perennials (Phragmites australis, Pennisetum alopecuroides and Plantago asiatica) and woody perennials (Lespedeza bicolor, Lespedeza juncea and Sorbaria sorbifolia) were identified for the current experiment. These native species were selected, based on their ability to suppress invasive plants in previous pot and field scale studies (Byun and Lee 2018; Byun et al. 2020b; Byun 2023), availability of their seeds in the market, their high germination rates, their distribution (native to S. Korea) and their ability to maximise functional diversity. The plant nomenclature used in this paper is the same as that used in the PLANT List (http://www.theplantlist.org), which lists accepted names and Flora of Korea Editorial Committee (2007).

Seed preparation

Seeds of native plants were purchased from authorised seed suppliers (in winter 2022). Seeds were obtained from multiple suppliers, because they could not be obtained from a single supplier. Seed suppliers included Aram Seeds (Seoul, Republic of Korea), Xplant (Seoul, Republic of Korea) and New Korea Farm (Seongnam, Republic of Korea) and others. Seed viability was standardised by applying the same number of viable seeds per species (600 seeds m-2) to experimental units. To determine the percentage of viable seeds, a germination test was conducted in the laboratory. All seeds were cold-stratified (6 months) at 3 °C before the germination test, following standard methods (Lindig-Cisneros and Zedler 2001). Then, 100 seeds per species were placed on three Petri dishes with Whatman® No. 1 filter paper moistened with 6 ml of distilled water under fluorescent light. Only species with high germination rates (above 5%) were used for the field experiment.

Measurements and statistical analyses

In August 2023, the number of shoots, plant height and plant cover of all species (including A. trifida) in each treatment and control plot were measured. For the number of shoots, we counted all shoots of each species in each plot manually. To determine plant cover, the percentage of each species was estimated using reference frames representing 50% and 25% of the total plot area. The main response variable was the importance value index, calculated based on the abundance of A. trifida. The importance value index (IVI) is a crucial metric in ecological studies, particularly when assessing the performance and impact of an invasive species (Byun et al. 2020b). IVI integrates multiple factors to provide a comprehensive picture of a species’ dominance and ecological role within a community. IVI values were calculated by summing the relative plant cover (%) and the relative shoot density (%). This holistic approach is essential for understanding how invasive species perform relative to native species. High IVI values for an invasive species indicate that it is not only widespread, but also occupies a significant portion of the community’s resources. This can highlight an invasive species’ potential to outcompete and displace native species, altering community structure and ecosystem functions (Kohli et al. 2004). Additional main variables were the Shannon–Wiener diversity index (H') of all species (Keylock 2005) in each quadrat and invasive seed yield. The raw diversity index datasheets are included in Suppl. materail 2. To test the re-invasion potential of A. trifida, seeds were harvested on 9 November 2023 (all individuals were fully mature) in each subplot (Ferreras and Galetto 2010; Leskovsek et al. 2012; Goplen et al. 2016). All seeds of only A. trifida within each quadrat were manually detached by hands. The seed yield was measured as an indicator of the potential for invasion in the future. Seeds were oven-dried for 48 hours at 80 °C before measuring their yields in each treatment. Given that invasive seed yield in subplots did not show any specific pattern, data are not presented here.

ANOVA was used to evaluate the effects of various treatments on response variables. A generalised linear mixed model (REML; F-test) was used to account for the random block design (Bolker et al. 2009). In the ANOVA analysis model, main factors of treatments (different eradication methods for Fig. 2. and different seed mixtures within each eradication method for Fig. 3) and the site factors were included along with the random block effect. The three main response variables were: (1) the importance of the value index, calculated, based on the abundance of A. trifida, (2) the Shannon–Wiener diversity index (H') of all species in each quadrat and (3) invasive seed yield (g, log-transformed).

Figure 2.

Effects of various eradication methods on Ambrosia trifida performance (importance values (a) and seed yield (b)) and plant community diversity (c). Error bars indicate standard errors. Bars with the same letters were not significantly different at P < 0.05.

Figure 3.

Effects of sub-treatments (sowing native seeds) within main treatments (eradication methods) on the importance values of Ambrosia trifida (a) and diversity of native plant communities (b). Error bars represent standard errors. Bars with the same letters were not significantly different. SM1 stands for seed mixture 1 (annuals), SM2 for non-woody perennials, SM3 for woody perennials.

The normality of residuals and homoscedasticity were evaluated, and the response variables were transformed when necessary. Amongst the main response variables, only invasive seed yield (g) was log-transformed during analysis. When significant (P < 0.05) treatment effects were detected, t-tests were used to compare means of treatments. ANOVA and correlation analyses were conducted using JMP (SAS Institute Inc., Cary, NC, USA). Pearson correlation coefficients were calculated for A. trifida importance values and the diversity index (H’) using data for 2023 in JMP.

Results

Response of invasive species A. trifida and native diversity to control measures

The effects of different control measures on the performance of A. trifida (Fig. 2a, b) and diversity of native plant communities (Fig. 2c), as well as the effects of sowing native seeds on invasion (Fig. 3a) and native diversity (Fig. 3b) were determined. The main eradication method had significant effects on abundance of A. trifida (F2,50 = 9.5624; P = 0.0003) and the effect of the site factor was also significant (F1,3 = 21.8288; P = 0.0167). The importance values for A. trifida were significantly lower in uprooting treatments than in control and cutting treatments (Fig. 2a). In addition, site 2 had much more abundant A. trifida populations than site 1 (as site factor). The seed yield of A. trifida was marginally affected by the control method (F2,31 = 3.2787; P = 0.0511) (Fig. 2b). Similarly, the main eradication method had significant effects on native diversity (F2,53 = 8.9271; P = 0.0005), but the effect of the site factor was not significant (F1,3 = 7.2109; P = 0.0747). Uprooting significantly increased native diversity; however, cutting did not improve diversity over that in the control (Fig. 2c).

Response of A. trifida and native diversity to sowing native seeds following invasion control

Sowing native seeds did not have significant effects on the A. trifida importance value (F9,41 = 0.7458; P = 0.6653), while the main eradication treatments had significant effects (F2,41 = 9.2215; P = 0.0005) and the effect of the site factor was also significant (F1,3 = 21.5360; P = 0.0168) in a nested experimental design. The importance values of A. trifida were much lower in the subplots with uprooting than in the control (no seed added) (Fig. 3a). Sowing native seeds did not influence the diversity index (F9,44 = 0.7998; P = 0.6184), despite significant effects of eradication (F2,44 = 8.6236; P = 0.0007) and the effect of the site factor was not significant (F1,3 = 7.2109; P = 0.0747) in a nested experimental design. The diversity index was much higher in the subplots with uprooting than in the control (Fig. 3b).

Variations in plant cover of native species after eradication, but before sowing native species and after sowing seeds, were also observed (Table 1). Only four (one of each woody and annual and two of perennials) out of nine sown species were established. One of the most abundant native species was a woody species (L. bicolor Turcz.) (Table 1). However, this species was already observed in the community before sowing native seeds. The annual herb L. indica L. amongst the sown species was absent in the existing native vegetation and showed a many-fold increase in its cover (Table 1). There was little success in the establishment of the perennial grass P. australis. Three native annual herbs, Acalypha australis, Commelina communis and Persicaria lapathifolia, one annual legume, Glycine soja and one perennial herb, Stellaria aquatica, had appeared after eradiation of A. trifida and sowing native species. The establishment of these species after restoration initiatives, regardless of whether or not seeds of these plants were included in the seed mixture, is likely due to a decrease in competition for resources in the absence of A. trifida, a strong competitor, facilitative effects of companion native species and differences in the growth season of these species. Humulus japonicus, a perennial invasive climber, appeared immediately after the eradication of A. trifida, but its abundance decreased slightly after sowing native seeds. Another invasive annual herb, Lactuca scariola, was present before restoration initiatives began, but disappeared afterwards. One non-native annual herb, Bidens pilosa, a non-target species, also disappeared after eradication of A. trifida and sowing native species (Table 1). A significant negative correlation was observed between importance values of A. trifida and diversity index (Fig. 4).

Table 1.

Plant species and their cover before sowing native seeds (August 2022) and after sowing native seeds (September 2023). Species names in bold font were the sown species. PC, plant cover (%).

Species names Growth habit Native or not Invasiveness Sown species PC 2022 (%) PC 2023 (%)
Lespedeza bicolor Turcz.# Perennial legume Native Sown 23.00 37.25
Humulus japonicus Siebold & Zucc. Perennial climber Native Invasive 46.12 36.80
Pueraria lobata Maesen S. M. Almeida ex Sanjappa & Predeep Perennial vines Native 28.37 34.00
Melothria japonica L. Annual climber Native 10.67 33.22
Lactuca indica L. # Annual herb Native Sown 0 21.83
Rubus parvifolius L. Perennial shrub Native 20.00 15.63
Acalypha australis L. Annual herb Native 0 14.50
Achyranthes bidentata var. japonica (Miq.) Nakai Annual herb Native 16.70 14.18
Pennisetum alopecuroides (L.) Spreng.# Perennial grass Native Sown 17.00 13.33
Commelina communis L. Annual herb Native 0 11.49
Artemisia indica Willd. Annual herb Native 2.50 10.75
Persicaria perfoliate (L.) H.Gross Annual climbing Native 7.00 7.57
Paederia foetida L. Perennial herb Native 18.5 7.20
Setaria viridis (L.) P. Beauv. Perennial grass Native 7.00 6.04
Cocculus trilobus (Thunb.) DC. Climbing shrub Native 8.25 5.50
Equisetum arvense L. Perennial herb Native 3.00 5.50
Stachys japonica L. Perennial herb Native 7.00 5.17
Phragmites australis (Cav.) Trin. ex Steud.# Perennial grass Native Sown 0 4.75
Glycine soja Siebold & Zucc. Annual legume Native 0 4.14
Artemisia lancea Van. Perennial Native 8.75 3.73
Digitaria ciliaris (Retz.) Koeler Annual grass Native 0.67 3.65
Persicaria lapathifolia (L.) Delarbre Annual herb Native 0 3
Stellaria aquatica (L.) Scop Perennial herb Native 0 1.25
Lactuca scariola L. Annual herb Non-native Invasive 21.00 0
Fallopia dumetorum (L.) Holub Annual climber Native 1.00 0
Amphicarpaea bracteata edgeworthii Benth. Annual climber Native 6.67 0
Bidens pilosa L. Annual herb Non-native 20.00 0
Figure 4.

Relationship between the importance values of Ambrosia trifida and diversity index (H') of plant communities.

Discussion

When invasive plants are partially removed, the effects on re-invasion can vary depending on the mode of reproduction of the invasive species, such as sexually (through seeds) and asexually (through rhizomes), as well as the persistence of the seed bank. For instance, re-sprouting from roots, rhizomes and plant stubs occurs in various invasive species (e.g. Cyperus rotundus, Lantana camara, Phragmites australis and Rosa rugosa), facilitating re-invasion after cutting or mowing aboveground plant parts. However, as observed in the current study on A. trifida (Fig. 2a), selective uprooting can significantly reduce the dominance of such invasive species. Similar results were found in a study of the sand dune invasive species Rosa rugosa (an invasive shrub in north-western Europe with negative effects on coastal biodiversity) (Kollmann et al. 2011), in which no re-sprouting was detected 2 months after uprooting. However, in the current study, uprooting reduced the abundance of A. trifida after 1 year. Mechanical control, including uprooting, cutting and ploughing, is an effective measure to eradicate Ambrosia species (Gerber et al. 2011). Generally, habitat disturbance caused by the mechanical removal of invasive plants facilitates re-invasion and hinders the recovery of native diversity. For instance, ploughing can significantly disrupt the soil environment, while mowing down all species can eliminate valuable native plants that resist A. trifida invasion. Selective uprooting, on the other hand, minimally impacts the habitat, preserving native vegetation and facilitating the eradication of invasive species A. trifida, ultimately benefitting native diversity. This expectation is supported by our results (Fig. 2c) demonstrating a significantly higher diversity of plant communities in uprooting plots than in control or cutting plots. The insignificant suppressive effect of selective cutting in the current study is contrary to results of an earlier study in which a 77% reduction in A. trifida importance values was reported after cutting all plant species (Byun et al. 2020b). The lack of a significant reduction in A. trifida abundance in the current study might be explained by a difference in the extent of the disturbance (Fox 1979; Byun et al. 2020b). Although the selective nature of cutting in this study was not destructive to the habitat and other vegetation, re-sprouting from A. trifida plant stubs and belowground plant parts did not support an increase in native plant diversity in this treatment (Fig. 2c). This indicates that A. trifida has strong potential to regrow and flower from remaining plant parts at the removal site. In a previous study, after clipping aboveground stems of A. artemisiifolia four times in a growing season, > 67% of individuals survived and, amongst these, > 97% flowered (Patracchini et al. 2011). Our findings on the seed yield of A. trifida in cutting and uprooting treatments (Fig. 2b) were consistent with these earlier results.

The addition of native seeds following invasion control is an effective strategy for controlling re-invasion and increasing biodiversity (Bucharova and Krahulec 2020); however, this approach has not been investigated extensively (Kettenring and Adams 2011; Singh and Byun 2023) and the results of various studies have been contradictory (Patracchini et al. 2011; Byun and Lee 2018; Byun et al. 2020b; Dong et al. 2020a; Wang et al. 2022). The responses of invasive species and native diversity to sowing native seeds following invasion control can be neutral, positive (facilitation) or negative (suppression) depending on various factors, including the identity of invasive species, removal strategy (Flory and Clay 2009; Kollmann et al. 2011; Cutting and Hough‐Goldstein 2013), diversity, density and features of seeds (Falk et al. 2013) and ecological conditions (Reinhardt Adams and Galatowitsch 2008). The responses of A. trifida invasive species to annual seed mix (SM1) were insignificant, but negative in control plots and significant, but positive in the cutting plots (Fig. 3). The suppressive effect of annuals on A. trifida abundance might be explained by the concept of limiting trait similarity (Yannelli et al. 2017), suggesting that interspecific similarity (annuals in this case) leads to the competitive exclusion of invasive species (Macarthur and Levins 1967). Given that cutting did not reduce the abundance of A. trifida (Fig. 2) or increase diversity index (Fig. 3a), annuals might have facilitated further invasion in the cutting plots. A consistent increase in invasive seeds and decrease in native seeds at invaded sites can also contribute to A. trifida invasion and inhibit diversity recovery. A decrease of up to 83% in native seeds was reported within 8 years of A. trifida invasion (Wang et al. 2022). We detected the suppression of A. trifida invasive species in response to sowing native seeds in selective uprooting plots; however, the magnitude of the effect was similar for seed mixtures including annual and woody species (Fig. 3a). The perennial seed mix following uprooting had a greater suppressive effect on A. trifida invasion than those of both annual and woody seed mixes. Thus, the eradication of A. trifida by uprooting and follow-up restoration by sowing native seeds can be an effective strategy to protect against its invasion. The lower seed yield of A. trifida in uprooting plots supports this assumption.

The variations in plant cover of native vegetation between 2022 and 2023 can be attributed to the combined effects of invasive species removal, sowing of native species, differences in growth habits, improved environmental conditions and interspecific interactions. The eradication of A. trifida may have reduced competition for resources, such as light, water and nutrients and, thereby, allowed other species to flourish. The sowing mixtures of native species would be expected to directly increase the presence and cover of these species. This is evident from the appearance of species that were absent in 2022, such as L. indica and P. australis in 2023. Annual species such as L. indica and A. australis can quickly colonise and cover ground within a single growing season. Perennials, on the other hand, might show more substantial growth over several years. This explains why some annual species were completely absent in 2022 and appeared in 2023 after sowing, while some perennials maintained or slightly increased their cover. For example, M. japonica increased its cover from 10.67% to 33.22%, indicating a competitive advantage or favourable conditions for this species post-eradication. Likewise, the increase in cover of L. bicolor from 23.00% to 37.25%, might be due to reduced competition and to its being a sown species.

While native seed sowing suppressed A. trifida invasion to different extents in each treatment, it did not impact the recovery of native diversity significantly. Sowing native seeds following invasion removal has been reported not to be a promising strategy for increasing native plant biodiversity, as reported in recent studies of A. trifida (Bucharova and Krahulec 2020; Byun et al. 2020b; Nagy et al. 2022) and other invasive plant species (Dickson and Busby 2009; Cutting and Hough‐Goldstein 2013; Tarsa et al. 2022). In addition, there were no differences amongst seeds of different functional groups with respect to native diversity recovery, regardless of the method employed for A. trifida invasion eradication (Fig. 3c). A recent greenhouse study also reported that the diverse native species of different functional groups does not suppress A. trifida (Byun and Lee 2018). However, the early arrival of native species strongly contained A. trifida invasion. There are multiple explanations for the lack of recovery of native diversity after seed addition: (1) Field conditions may not be favourable for seed germination; (2) An important factor in restoring native diversity using native seeds is appropriate seed density. Considering the harsh conditions and low germination rate, 600 seeds m-2 may not be a sufficient density (Burton et al. 2006; Reinhardt Adams and Galatowitsch 2008; Byun and Lee 2018; Shaw et al. 2020; Byun et al. 2020b; Tarsa et al. 2022); however, insignificant recovery with a high seed density has also been reported (Dickson and Busby 2009); (3) A narrow niche range of some of the native species did not support their dominance in current distinct habitat conditions (Pulliam 2000); (4) Seeds of perennials, such as P. australis and P. alopecuroides, were hairy (Suppl. material 1: fig. S1) and hardly encountered the ground or soil directly during sowing; it is, therefore, possible that these species could not grow and contribute to native diversity; (5) Commercial sources of seeds, generally agronomically propagated (Höfner et al. 2022), may contribute to low adaptability to targeted local conditions (Bucharova et al. 2019); (6) Sowing seeds of one functional group in each plot might not exert strong effects on diversity. More diversified functional groups or types of native seeds in seed mixtures are needed to better assess whether seeding native species counteracts invasive plants and restores native biodiversity; (7) A. trifida may be too difficult to control via native species (Byun and Lee 2018). Given that uprooting reduced invasion substantially, consistently uprooting A. trifida for a longer period, at least 3 years (soil seed-bank densities decreased by > 99% in 2 years (Dong et al. 2020b)), in a larger area to limit the arrival of invasive seeds and adding native seeds can facilitate the recovery of native diversity. We did not test the role of functional diversity; therefore, further studies should evaluate whether sowing seeds of all functional groups in combination restores native diversity.

Limitations of study

A major limitation of this study was relatively short monitoring time (1 year or less) after restoration. We think that longer monitoring would have yielded better results. The short monitoring time may explain, at least partly, why sowing native seeds did not bring any additional benefit to the control of, or resistance to, A. trifida invasion. The seed mixtures of three functional groups of native plant species were employed: annuals, non-woody perennials and woody perennials, because we wanted to determine which functional group was most effective in providing biotic resistance to invasion in the year following eradication of A. trifida. Annuals were expected to perform better as they are usually fast-growing and become established in the first year after eradication. This is also expected, based on the limiting similarity hypothesis (A. trifida is also an annual plant species). However, we did not find any difference in biotic resistance to invasion between the functional groups of seeds; in fact, there was no difference between sowing and not sowing seeds. We only monitored plots soon after eradication because we considered one year as the critical window for invasive species re-invasion. If invasive species are not controlled within this short time frame, then it will be difficult to stop re-establishment of the invasive species afterwards. As we were acutely aware of the limited timeframe of this study, we ended up measuring the invasive seed yield as an indicator for potential future re-invasion after one year of monitoring.

One of the critical aspects of restoring native species using native seeds is the seed density. For instance, 600 pure live seeds (after considering germination rates per species) m-2 per subplot were sown. Originally, this density was considered sufficient in the initial experimental design, but under actual heterogeneous field conditions, many different factors can influence seeding efficiency. For example, the characteristics of experimental sites might not match the ecological niches of the restorative native species. In addition, it is also likely that seed density is reduced by their ingestion by some animals, such as birds, in the Spring. Considering these field limitations, we now consider that 10-fold higher seed density would have been required to obtain meaningful and significant results; in fact, this density was recommended by a seed-based restoration workshop at a conference of the Society of Ecological Restoration (SER).

Implications for practice

The findings of this study have strong implications for the management of invasive plants and recovery of native plant diversity: (1) Cutting to eradicate plant invasion can result in wasted effort and resources, particularly if the targeted species can regrow or re-sprout from remaining plant parts. In the current study, cutting was selective and resulted in minimal disturbances of native vegetation. However, invasion was suppressed to only a small extent with insignificant differences between cutting plots and the control plot. Complete and destructive cutting of the entire vegetation may further increase invasion by reducing native plant diversity; (2) Selective uprooting is a promising tool for invasive plant management. Complete removal of invasive species from invaded communities and ecosystems will reduce competition pressure on native species for space, light and nutrients and form invasive propagules (roots, rhizomes, seeds etc.) and increase the performance (germination, establishment and diversity) of native communities; (3) Sowing seeds of diverse species following removal of the invasive species is critical for the rapid recovery of native diversity; (4) Compared with selective uprooting, mowing of all species is not an effective strategy for the management of invasive plants because it does not leave any native species to resist re-invasion; (5) Although this study was conducted solely at two field sites within the Republic of Korea, our findings can readily be extrapolated to other countries. This generalisability stems from the underlying ecological principles uncovered, namely, the importance of leaving no propagule behind for achieving effective eradication outcomes. This fundamental principle is relevant, irrespective of geographic context, making it applicable across diverse regions; (6) Lastly, it is important to consider the potential environmental or ecological side effects of selective uprooting. For instance, hand-pulling to uproot all invasive plants can slightly disturb soil composition, potentially impacting soil microorganism communities and the legacy effects of soil on biogeochemical processes. Therefore, selective uprooting must be executed with meticulous care to minimise disturbances to the soil surface and other native species.

Conclusions

This study concludes that selective uprooting is a more effective tool than cutting for suppressing A. trifida invasion and increasing the diversity of native plant communities. The findings of this study support the expectation that uprooting of invasive species before flowering with minimum habitat disturbances can immediately reduce competition for remaining native species and concurrently can increase native diversity in the next growing season due to decreases in the number of seeds of A. trifida, the invasive species. Suppression of plant invasion further increased after sowing native seeds; however, this was only valid if the invasive plant was eradicated by uprooting. Therefore, sowing seeds to restore native diversity at sites where A. trifida invasion has been eradicated by cutting may result in the waste of native seeds, time and other resources. Sowing native seeds after removal of A. trifida by cutting and uprooting facilitated recovery of native diversity; however, uprooting followed by sowing native plants was more effective.

Acknowledgements

We thank Dr. Ho Choi and Dr. Norul Sobuj for their assistance with the fieldwork. We also thank Dr. Minwoo Oh for drawing the study site map in QGIS. We thank Eulsukdo Ecological Park Nakdonggang Estuary Eco Center for field cooperation.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (2022R1A2C1003504). This study was supported by a joint research project from the Ministry of Environment, Republic of Korea (Project number: 2021002270004).

Author contributions

CB conceptualised and designed the study; CB, KS and JL collected data, CB analysed and constructed graphs and tables; CB, KS and JL wrote the manuscript; SHH, TKY and HK reviewed and edited the manuscript; CB and SHH engaged in project collaboration.

Author ORCIDs

Chaeho Byun https://orcid.org/0000-0003-3209-3275

Kripal Singh https://orcid.org/0000-0003-2845-7160

Sun Hee Hong https://orcid.org/0000-0001-7581-0604

Jangho Lee https://orcid.org/0009-0006-3274-6378

Tae Kyung Yoon https://orcid.org/0000-0003-0627-0135

Hojeong Kang https://orcid.org/0000-0002-2088-6406

Data availability

Dataset was shared in the open access file directories of Figshare. https://doi.org/10.6084/m9.figshare.26425879.

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Supplementary materials

Supplementary material 1 

Supplementary information

Chaeho Byun

Data type: docx

Explanation note: fig. S1. Sown species: Photographs of native seeds used in this study. fig. S2. Experimental layout (blocks) in two sites.

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
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Supplementary material 2 

Diversity index raw datasheets

Chaeho Byun

Data type: xlsx

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
Download file (69.99 kb)
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