Introduction
Invasive plant (IP) species can affect the structure and function of plant communities, particularly leading to a decrease in biodiversity (McGrath & Binkley Reference McGrath and Binkley2009, Keet et al. Reference Keet, Ellis, Hui, Novoa and Le Roux2021, Ahmad Dar et al. Reference Ahmad Dar, Ahmad, Singh, Kumar Kohli, Singh and Batish2023). However, the mechanisms that facilitate their establishment are poorly understood. A significant factor contributing to the success of IPs is their capacity to interact with soil, particularly through litter decomposition. This interaction can influence soil physicochemical properties, enzyme activities and the structure of soil microbial communities, thereby facilitating the invasion process (Dekanova et al. Reference Dekanova, Svitkova, Novikmec and Svitok2021, Firmino et al. Reference Firmino, Brasil, Martins, Ligeiro, Tonin, Goncalves Junior and Juen2021, Maan et al. Reference Maan, Kaur, Sharma, Singh, Batish, Kohli and Arora2022).
The degree of IP invasion exhibits variation in invaded environments, accompanied by a gradient of succession after colonization in new habitats and the gradual formation of large mono-dominant communities (Fenouillas et al. Reference Fenouillas, Ah-Peng, Amy, Bracco, Dafreville and Gosset2021). This phenomenon is primarily attributed to the stronger growth performance, reproductive capacity, phenotypic plasticity and stress tolerance of IPs in comparison to native plants (Davidson et al. Reference Davidson, Jennions and Nicotra2011). Consequently, leaves of IPs and natives may decompose together at different mixing ratios under a gradient of invasion. The decomposition rate of IPs is typically greater than that of natives, providing more nutrients for the metabolic activity and diversity of soil microorganisms (particularly decomposers), which in turn facilitates the successful colonization of IPs (Dekanova et al. Reference Dekanova, Svitkova, Novikmec and Svitok2021, Firmino et al. Reference Firmino, Brasil, Martins, Ligeiro, Tonin, Goncalves Junior and Juen2021, Maan et al. Reference Maan, Kaur, Sharma, Singh, Batish, Kohli and Arora2022, Vujanović et al. Reference Vujanović, Losapio, Milić and Milić2022). The invasion degree of IPs may affect soil physicochemical properties, soil enzyme activities and the metabolic activity and diversity of soil microorganisms via decomposition processes. Several IPs, particularly those belonging to the Asteraceae family, can occur in the same area (Wang et al. Reference Wang, Li, Li, Zhong, Xu, Yu and Du2023). Thus, there is a need for studies that examine the association between the invasion degree and decomposition processes of multiple Asteraceae IPs. However, current progress in this field is relatively limited.
This study aimed to elucidate the effects of the co-decomposition of four Asteraceae IPs, namely Conyza canadensis (L.) Cronq., Conyza sumatrensis (Retz.) Walker, Erigeron annuus (L.) Pers. and Solidago canadensis L., along a gradient of invasion, and the native Asteraceae plant Pterocypsela laciniata (Houtt.) Shih on the decomposition rate, soil physicochemical properties, soil enzyme activities and diversity of soil bacterial communities (SBCs). The four IPs are capable of establishing expansive, monodominant communities with minimal latency following the successful invasion of habitats in China. Consequently, the four IPs have been considered as malignant invasive species in China. The four IPs and P. laciniata show similar growing-season characteristics: their maximum growth naturally occurs between April and August in China. The four IPs and P. laciniata are found in similar habitats, including agro-ecosystems, wastelands and near main roads in China, and they reach similar heights of up to c. 2–3 m. Pterocypsela laciniata can coexist with one or more of the four IPs in the same ecosystem in China.
The following questions were investigated: (1) Is there a greater decomposition rate of the four IPs in comparison to P. laciniata? (2) Does decomposition of the four IPs increase soil enzyme activities and SBC alpha-diversity? (3) Do the decomposition rate of the four IPs, soil enzyme activities and SBC alpha-diversity increase as the invasion degree of the IPs increases?
Materials and methods
Study design
Leaves of the four IPs and P. laciniata were collected in Zhenjiang (32.1633–32.2092°N, 119.4565–119.5293°E), China, in May 2022.
Decomposition of the four IPs and P. laciniata was replicated through a polyethylene litter-bag experiment conducted from 1 November 2022 to 3 May 2023 (c. 182 days) in a greenhouse in Zhenjiang (32.2061°N, 119.5128°E). Six grams of air-dried leaves of the four IPs and/or P. laciniata were placed in each polyethylene litter-bag (dimensions: 10 × 15 cm; mesh size: c. 0.425 mm) as follows: (1) 6 g of leaves of P. laciniata (imitating conditions without invasion; PL); (2) 6 g of mixed leaves with 2 g of C. canadensis and 4 g of P. laciniata (imitating C. canadensis with light invasion; CCL); (3) 6 g of mixed leaves with 3 g of C. canadensis and 3 g of P. laciniata (imitating C. canadensis with moderate invasion; CCM); (4) 6 g of mixed leaves with 4 g of C. canadensis and 2 g of P. laciniata (imitating C. canadensis with heavy invasion; CCH); (5) 6 g of leaves of C. canadensis (imitating C. canadensis with full invasion; CC); (6) 6 g of mixed leaves with 2 g of C. sumatrensis and 4 g of P. laciniata (imitating C. sumatrensis with light invasion; CSL); (7) 6 g of mixed leaves with 3 g of C. sumatrensis and 3 g of P. laciniata (imitating C. sumatrensis with moderate invasion; CSM); (8) 6 g of mixed leaves with 4 g of C. sumatrensis and 2 g of P. laciniata (imitating C. sumatrensis with heavy invasion; CSH); (9) 6 g of leaves of C. sumatrensis (imitating C. sumatrensis with full invasion; CS); (10) 6 g of mixed leaves with 2 g of E. annuus and 4 g of P. laciniata (imitating E. annuus with light invasion; EAL); (11) 6 g of mixed leaves with 3 g of E. annuus and 3 g of P. laciniata (imitating E. annuus with moderate invasion; EAM); (12) 6 g of mixed leaves with 4 g of E. annuus and 2 g of P. laciniata (imitating E. annuus with heavy invasion; EAH); (13) 6 g of leaves of E. annuus (imitating E. annuus with full invasion; EA); (14) 6 g of mixed leaves with 2 g of S. canadensis and 4 g of P. laciniata (imitating S. canadensis with light invasion; SCL); (15) 6 g of mixed leaves with 3 g of S. canadensis and 3 g of P. laciniata (imitating S. canadensis with moderate invasion; SCM); (16) 6 g of mixed leaves with 4 g of S. canadensis and 2 g of P. laciniata (imitating S. canadensis with heavy invasion; SCH); (17) 6 g of leaves of S. canadensis (imitating S. canadensis with full invasion; SC). Polyethylene litter-bags were buried in pastoral soil at a depth of c. 2 cm in planting pots (top diameter: 30 cm; height: 24 cm), with one polyethylene litter-bag per planting pot. The pastoral soil was not sterilized. Three replicates were performed per treatment (3 replicates × 17 treatments (i.e., P. laciniata + 4 species of IPs × 4 degrees of invasion) = 51 planting pots/polyethylene litter-bags).
Following experimental treatment, all polyethylene litter-bags were collected. Decomposed leaves were subjected to a moderate washing process and air-drying procedure to analyse the variables associated with decomposition. Soil samples were collected from a depth of c. 1 cm adjacent to polyethylene litter-bags and passed through a 2-mm sieve to measure soil variables and SBC structure.
Determination of decomposition variables, soil variables and SBC structure
The cumulative mass loss (CML), decomposition coefficient (k), expected k of mixed leaves and mixed-effect intensity of co-decomposition (MEIC) were analysed.
The pH, moisture, electrical conductivity, total organic carbon, soluble organic carbon and microbial carbon in soil were assayed. Activities of several soil enzymes involved in the soil carbon cycle were examined, including polyphenol oxidase, fluorescein diacetate (FDA) hydrolase, cellulase, β-glucosidase, β-xylosidase and sucrase.
Illumina PE250 was employed to analyse the SBC structure. The primers 341F and 806R were employed to perform amplification of the V3–V4 region of the 16S rRNA genes of the SBC (Wear et al. Reference Wear, Wilbanks, Nelson and Carlson2018). Further analysis was conducted using previously described methods (Liu et al. Reference Liu, Du, Li, Li, Zhong and Xu2024).
The determination methods for decomposition variables, soil variables and SBC structure are described in Appendix S1, Table S1.
Statistical analysis
Multiple comparison with Tukey’s test was employed to statistically analyse the differences in the studied variables between the various treatments. Correlation patterns between CML and k, soil variables and SBC alpha-diversity were estimated via the application of principal component analysis (PCA) with a permutational multivariate analysis of variance (PERMANOVA) test. Two-way analysis of variance (ANOVA) was used to estimate the effects of invasion degree and plant species on CML and k, soil variables and SBC alpha-diversity; P ≤ 0.05 was considered statistically significant. Statistical analyses were conducted using IBM SPSS Statistics (26.0).
Results
The CML and k of C. canadensis with heavy invasion and S. canadensis with light and heavy invasion were less than those of P. laciniata (P < 0.05; Figs 1a,g,h & 2a,b,e,f), whereas those of C. canadensis with full invasion were larger than in P. laciniata (P < 0.05; Figs 1a,b & 2g,h). There were no significant differences in the CML and k between P. laciniata, C. sumatrensis and E. annuus regardless of invasion degree (Figs 1 & 2). The CML and k of S. canadensis were less than those of the other three IPs, especially with light and heavy invasion (P < 0.05; Fig. 2a,b,e,f).
(a–h) Differences in the cumulative mass loss and decomposition coefficient between the native plant Pterocypsela laciniata (Houtt.) Shih and the same species invasive plant with a gradient of invasion. Data (means ± standard errors; n = 3) with different letters indicate statistically significant differences. PL = P. laciniata; CCL = Conyza canadensis (L.) Cronq. with light invasion; CCM = C. canadensis with moderate invasion; CCH = C. canadensis with heavy invasion; CC = C. canadensis with full invasion; CSL = Conyza sumatrensis (Retz.) Walker with light invasion; CSM = C. sumatrensis with moderate invasion; CSH = C. sumatrensis with heavy invasion; CS = C. sumatrensis with full invasion; EAL = Erigeron annuus (L.) Pers. with light invasion; EAM = E. annuus with moderate invasion; EAH = E. annuus with heavy invasion; EA = E. annuus with full invasion; SCL = Solidago canadensis L. with light invasion; SCM = S. canadensis with moderate invasion; SCH = S. canadensis with heavy invasion; SC = S. canadensis with full invasion.
(a–h) Differences in the cumulative mass loss and decomposition coefficient between the native plant Pterocypsela laciniata (Houtt.) Shih and different invasive plants with the same invasion degree. Data (means ± standard errors; n = 3) with different letters indicate statistically significant differences. Abbreviations are the same as in Fig. 1.
The MEIC of P. laciniata and C. sumatrensis was positive; the MEIC of P. laciniata and S. canadensis was negative (P < 0.05; Appendix S1, Fig. S1f,l). The MEIC of P. laciniata and C. canadensis was positive with light and moderate invasion but was negative with heavy invasion (P < 0.05; Appendix S1, Fig. S1c). The MEIC of P. laciniata and E. annuus was positive with moderate invasion but was negative with light and heavy invasion (P < 0.05; Appendix S1, Fig. S1i).
Decomposition of C. canadensis and S. canadensis increased soil pH (P < 0.05; Appendix S1, Figs S2a & S3a). Decomposition of the four IPs irrespective of invasion degree generally increased soil microbial carbon content above that of P. laciniata, and the maximum content of soil microbial carbon was observed under decomposition of S. canadensis (P < 0.05; Appendix S1, Figs S2f, S3f, S4f & S5f). Decomposition of C. sumatrensis and E. annuus irrespective of invasion degree (except for E. annuus with moderate invasion) reduced soil FDA hydrolase activity more than that of P. laciniata (P < 0.05; Appendix S1, Figs S4j & S5j).
Decomposition of the four IPs resulted in changes in SBC beta-diversity (Appendix S1, Figure S6) and in the presence of numerous dominant biomarkers of SBCs (Appendix S1, Fig. S7).
The CML and k of P. laciniata and the four IPs were closely correlated with electrical conductivity, moisture, total organic carbon and soluble organic carbon contents and polyphenol oxidase activity in soil (Appendix S1, Fig. S8).
Decomposition of the four IPs did not significantly affect SBC alpha-diversity (P > 0.05; Appendix S2, Figs S9–S16 & Table S2).
Discussion
We show that invasion degree and species identity of IP appear to be the most significant factors influencing decomposition rate of C. canadensis and S. canadensis. This may be attributed to variance in soil physicochemical properties, especially electrical conductivity, moisture and total organic carbon and soluble organic carbon contents, under conditions of decomposition of the two IPs. This phenomenon may also be attributed to changes in SBC beta-diversity and the emergence of distinct dominant biomarkers of SBCs resulting from the decomposition of the two IPs. Nevertheless, the decomposition rates of C. sumatrensis and E. annuus were comparable to those of P. laciniata regardless of invasion degree, possibly because the percentages of soluble and recalcitrant substances in the leaves of the three plant species are similar. Thus, invasion degree and species identity of IP are not the most significant factors influencing the decomposition rate of C. sumatrensis and E. annuus. The nutrient cycling facilitated by litter decomposition may be of greater importance to the successful invasion of C. canadensis, particularly in the context of full invasion, than that of the other three IPs.
Leaves of S. canadensis decomposed more slowly than those of the other three IPs, particularly with light and heavy invasion; this could be related to alterations in SBC metabolic activity and SBC beta-diversity and the emergence of numerous dominant biomarkers of SBCs associated with the decomposition of S. canadensis. Thus, the role of nutrient cycling mediated by litter decomposition may be less prominent in the successful invasion of S. canadensis, especially with light and heavy invasion, than in the cases of the other three IPs. Therefore, species identity of IP emerges as a pivotal factor influencing the decomposition rate of the different IPs.
The MEICs of IPs and natives may be altered as a consequence of the litter of IPs and natives being mixed along an invasion gradient. Co-decomposition of P. laciniata and C. sumatrensis could be synergistic, whereby the two species decompose more rapidly when present together, regardless of invasion degree. Conversely, co-decomposition of P. laciniata and S. canadensis could be antagonistic, with the two species decomposing more slowly together regardless of invasion degree. This phenomenon is largely attributable to the interspecific facilitation or interference of chemical substances contained in mixed litter, respectively (Barbe et al. Reference Barbe, Mony, Jung, Santonja, Bartish and Prinzing2018, Kouadio et al. Reference Kouadio, Koné, Touré, Konan, Yapo and Abobi2023). Thus, P. laciniata can facilitate the invasion of C. sumatrensis via accelerated nutrient cycling, which is mediated by a synergistic effect of co-decomposition irrespective of invasion degree. This may result in P. laciniata actively cooperating with or even creating favourable conditions to facilitate C. sumatrensis invasion. Conversely, P. laciniata can impede the invasion of S. canadensis by slowing nutrient cycling, which is mediated by antagonistic co-decomposition irrespective of invasion degree.
The exudation of secondary metabolites by IPs can alter soil physicochemical properties during decomposition (Ahmad Dar et al. Reference Ahmad Dar, Ahmad, Singh, Kumar Kohli, Singh and Batish2023). Decomposition of C. canadensis and S. canadensis resulted in a higher soil pH than that of P. laciniata, possibly through the release of alkaline or other substances into the soil conducive to alkalization (e.g., anions) during decomposition (McGrath & Binkley Reference McGrath and Binkley2009). Alternatively, this outcome could be ascribed to a diminution in the generation of H+ via a reduction in the secretion of acidic substances present in the leaves of C. canadensis and S. canadensis (Zhong et al. Reference Zhong, Xu, Yu, Cheng, Wang and Wei2022).
In general, IPs can increase soil carbon content by increasing inputs of carbon-containing substances to the soil (Vujanović et al. Reference Vujanović, Losapio, Milić and Milić2022). Decomposition of the four IPs irrespective of invasion degree generally increased soil microbial carbon content more than did decomposition of P. laciniata. The maximum content of soil microbial carbon was observed under decomposition of S. canadensis, especially with light, heavy and full invasion. Soil microbial carbon content may be enhanced under decomposition of the four IPs, with no discernible impact of invasion degree, and this is especially the case for S. canadensis under light, heavy and full invasion. A potential for greater microbial carbon sequestration in the soil is evident, particularly through the utilization of carbon by soil microorganisms during the decomposition of the four IPs, particularly S. canadensis.
IPs can also affect soil enzyme activities and SBC structure (Keet et al. Reference Keet, Ellis, Hui, Novoa and Le Roux2021, Woods et al. Reference Woods, Attea and McEwan2021). The release of carbon- and nitrogen-containing substances throughout decomposition facilitates this process, providing the vital nutrients required for the metabolism of soil microorganisms. Soil FDA hydrolytic capability was reduced under conditions of the decomposition of C. sumatrensis and E. annuus. This decline can be attributed to a decrease in nutrient availability and/or an increase in the rate of microbial metabolism in the soil under conditions of the decomposition of the two IPs. Furthermore, decomposition of the four IPs resulting in changes in SBC beta-diversity was demonstrated through the presence of numerous dominant biomarkers of the SBCs compared to with decomposition of P. laciniata. Differences in leaf quality of the four IPs and P. laciniata may lead to some species differentiation of the SBCs (Santonja et al. Reference Santonja, Rancon, Fromin, Baldy, Hättenschwiler and Fernandez2017, Keet et al. Reference Keet, Ellis, Hui, Novoa and Le Roux2021). Selective inhibition or facilitation caused by altered amounts, types and complexities of nutrients (e.g., carbon/nitrogen-containing and other recalcitrant substances) in the soil throughout the decomposition of the four IPs could also be responsible for this observation (Dekanova et al. Reference Dekanova, Svitkova, Novikmec and Svitok2021). Thus, some SBC taxa may persist while others may die over time due to decomposition of the four IPs. Decomposition of the four IPs mainly affected SBC structure rather than alpha-diversity.
Decomposition of plants can affect soil physicochemical properties, enzyme activities and SBC structure (Firmino et al. Reference Firmino, Brasil, Martins, Ligeiro, Tonin, Goncalves Junior and Juen2021, Ahmad Dar et al. Reference Ahmad Dar, Ahmad, Singh, Kumar Kohli, Singh and Batish2023). The decomposition rate of P. laciniata and the four IPs evidently affects electrical conductivity, moisture, total organic carbon and soluble organic carbon contents and polyphenol oxidase activity in the soil. The soil physicochemical properties and enzyme activities probably affect the release of substances, especially carbon-containing substances, from leaves during decomposition, and this in turn affects resource use and access to nutrients metabolized by the SBCs (Keet et al. Reference Keet, Ellis, Hui, Novoa and Le Roux2021).
Conclusions
Decomposition of the four IPs, irrespective of invasion degree, generally increased soil microbial carbon content compared to decomposition of P. laciniata, especially under conditions of decomposition of S. canadensis. Consequently, decomposition of the four IPs irrespective of invasion degree, and especially that of S. canadensis, may contribute to microbial carbon sequestration. Our findings showed that although IPs can have negative ecological impacts, their role in microbial carbon sequestration should be considered in management strategies, especially in wastelands and wilderness areas.
Supplementary material
To view supplementary material for this article, please visit https://doi.org/10.1017/S0376892925100131.
Acknowledgements
We are very grateful to the anonymous reviewers for their insightful and constructive comments that greatly improved this manuscript.
Financial support
The study was funded by Open Science Research Fund of Key Laboratory of Ocean Space Resource Management Technology (KF-2024-112), Carbon Peak and Carbon Neutrality Technology Innovation Foundation of Jiangsu Province (BK20220030) and Jiangsu Collaborative Innovation Center of Technology and Material of Water Treatment.
Competing interests
The authors declare none.
Ethical standards
Not applicable.
