Elsevier

Limnologica

Volume 92, January 2022, 125939
Limnologica

Invasive plant indirectly regulates native plant decomposition by affecting invertebrate communities

https://doi.org/10.1016/j.limno.2021.125939Get rights and content

Abstract

Invasive plants may have variable effects depending on their interactions with native species, yet few studies have examined the phenomenon of the invasive plant-mediated priming effect. To investigate the priming of invasive species on native leaf litter decomposition, we allocated two native leaf species of contrasting recalcitrance (Neosinocalamus affinis and Ficus virens) in single and double species mixtures with and without invasive Alternanthera philoxeroides, and then incubated them for 65 days in a eutrophic shallow lake. Invasive plant addition promoted decomposition of F. virens and a mixture of two native plants, with positive priming effects of 25.47 % for F. virens and 30.49 % for the mixture based on mass loss, respectively. However, the decomposition of N. affinis was inhibited, with a negative priming of −16.55 %. In total, the associated faunal communities comprised 15 microinvertebrate taxa, 10 meioinvertebrate taxa, and 11 macroinvertebrate taxa. Among these, sarcodina (omnivores) were shared components colonizing all plant materials, while ciliates (filter-collectors) and cladocerans (filter-collectors) mostly colonized the mixture of native species and mixture × A. philoxeroides materials. The abundances of rotifers (filter-collectors) and chironomids (gather-collectors) were the highest in F. virens × A. philoxeroides materials. Compared to the faunal assemblage without A. philoxeroides treatments, the invertebrate richness and abundance, microalgae abundance and microbial respiration were more than one times higher with A. philoxeroides treatments. Our findings indicate that the priming effect can be induced by invasive A. philoxeroides, invertebrate community played an important role in this process.

Introduction

With the rapid rate of ecosystem degradation worldwide, it has become increasingly important to understand how invasive plants alter ecosystem function and species diversity (Claeson et al., 2013; McCary et al., 2016; Zenni et al., 2020). Invasive plants have successfully invaded numerous ecosystems and have been shown to greatly alter ecosystem processes such as nutrient cycling and decomposition (Hattenschwiler et al., 2005; Zenni et al., 2020). Furthermore, the litters produced by most invasive plants have high contents of nutrients and low contents of lignin and polyphenolics, and therefore tends to decompose faster and release nutrients more rapidly (Callaway and Aschehoug, 2000; Weidenhamer and Callaway, 2010). Although the impacts of invasive plant species on native plant communities have been well demonstrated (Keane and Crawley, 2002; Levine et al., 2003; Watts et al., 2010), very little is known regarding the phenomenon of invasive plant-mediated priming on the decomposition of native plant detritus.

Allelochemicals produced by invasive plants mainly consisted of alcohols, ketones, and terpenoids (Kato-Noguchi, 2020), which can be prone to biochemical reactions and oxidative decomposition after dilution (Scavo et al., 2019; Zhu et al., 2020). Concurrently, the invasive plants may release exudates such as polysaccharides, monosaccharides and amino acids (Zuo et al., 2012). These labile organic matters (LOM) presumably may stimulate the decomposition of more recalcitrant organic matter (ROM) by providing high-quality resource subsidies to heterotrophic invertebrates and microbial populations (Halvorson et al., 2019). This phenomenon is known as the priming effect (PE). Being critical primary producers, Alternanthera philoxeroides is one of the most widely distributed invasive plants in the littoral areas of eutrophic lakes (Wilson et al., 2007; Henriksen et al., 2018), which have high contents of nutrients and low contents of lignin and polyphenolics (Zuo et al., 2012), and may produce large amounts of labile carbon exudates during their growth and decomposition phases. Therefore, it is expected that the addition of A. philoxeroides could prime the decomposition of native plant detritus.

In freshwater environments, some studies have reported no or negative priming (i.e., decreased decomposition rates) with addition of LOM (Gontikaki et al., 2013; Bengtsson et al., 2014), indicating that the input of LOM may stimulate heterotrophic decomposer activity, yet this stimulation is not coupled to increased ROM turnover because microbial heterotrophs likely allocate LOM to growth, respiration, or reproduction instead of Carbon (C) removal (Halvorson et al., 2019). Others have reported positive priming (i.e., increased decomposition rate) with the additions of LOM (e.g., labile microalgal exudates) on the decomposition of ROM (Danger et al., 2013; Bianchi et al., 2015), which revealed that the input of LOM could stimulate heterotrophic decomposition of recalcitrant C (Dorado-García et al., 2016). However, the ecology of invertebrates involved in the ROM decomposition in the field situation remains less studied.

The role of invertebrates in plant decomposition has been well studied (Risse-Buhl et al., 2015). Based on their morphological characteristics (e.g., mouth part specialization) and behavioral mechanisms (e.g., mode of feeding), invertebrates can be classified into five categories: shredders, gathering-collectors, filtering-collectors, scrapers and predators (Cummins and Klug, 1979). Of these, shredders can transform coarse particulate organic matter (size 1 mm) into fine particulate organic matter (FPOM) (size 50 mm – 1 mm). Collectors further decompose FPOM to ultra-fine particulate organic matter (UFPOM; size 0.5–50 mm) by collecting organic matter incorporated into the sediment from the water column (Vannote et al., 1980). Scrapers feed on UFPOM and attached algal communities (periphyton). Predators derive their metabolic energy from living animal tissue (Graça, 2001). Some previous studies have reported that invasive plants significantly affected the composition and distribution of invertebrates (Toft et al., 2003; Little et al., 2020; Mutshekwa et al., 2020).

Many freshwater ecosystems receive large inputs of plant leaves from the riparian zone, and this leaf quality is always a predominant driver of litter decomposition. The magnitude and direction of PE on litter decomposition may not only depend on decomposer activities (Halvorson et al., 2019), but also the initial quality of leaf litter (Tian et al., 2019). Generally, leaf litter with a lower C:N ratio and lignin content would be expected to yield a more significant PE (Wang et al., 2015). The quality of ROM may alter the colonization of decomposers because of their substrate preference. For example, ROM with a lower C:N ratio and lignin content tended to increase the relative abundance of invertebrates (Danger et al., 2012). Therefore, the magnitude and direction of PE may be altered by changing the quality of ROM due to decomposer colonization (Wang et al., 2015). However, our understanding is still limited by the scarce information on decomposing responses to diff ;erent ROM decomposition.

To address the priming of invasive plants for native leaf litter decomposition, we assembled bags with dry leaves of the native plants Neosinocalamus affinis and Ficus virens in single and double species mixtures with and without invasive A. philoxeroides. We incubated them at the sediment-water interface of an urban lake, Jianhu Lake, China, for 65 days. We hypothesized that: (1) Addition of an invasive plant would alter the decomposition of native species via positive or negative priming; (2) the litter-associated invertebrate communities may also play an essential role in plant priming.

Section snippets

Study area

The study was conducted in a eutrophic lake, Jianhu Lake (107.15 E, 29.45 N; 285 m above sea level), situated in the Three Gorges Reservoir area in Chongqing city, China. The water column has a mean depth of 2.6 m, with an area of 1.5 km2. The experimental site was in the southern branch of Jianhu Lake. The community of plants involved comprised several species: invasive Alternanthera philoxeroides, native Neosinocalamus affinis, Ficus virens, Cyperus alternifolius, and Canna indica. N. affinis

Initial quality of the three studied plants and their decomposition

The initial qualities of A. philoxeroides, N. affinis, and F. virens differed significantly (Table S1). Specifically, A. philoxeroides has the highest initial quality. For two native plants, N. affinis exhibited a higher content for C, cellulose and hemicellulose, as well as C: N and C: P ratio. In contrast, F. virens was higher in N and P content, total phenol as well as N:P ratio. Generally, the initial qualities of the three species increased in the order N. affinis < F. virens < A.

The priming effect of invasive plant addition

After the first witness of the PE in terrestrial soil (Löhnis, 1926), many studies in terrestrial ecosystems have shown that inputs of LOM frequently tend to accelerate the decomposition of more ROM (Bradford et al., 2008). However, this phenomenon has not been tested in aquatic ecosystems (Halvorson et al., 2019). Until recently, knowledge regarding the phenomenon of algae-mediated priming on decomposition in aquatic environments, mainly on allochthonous plant input, has developed (Danger et

Conclusion

Our study indicates that the addition of invasive plant A. philoxeroides can alter the decomposition of different native plants. The subsequent effect can be mediated by the change in taxonomic and functional diversity of associated invertebrates and microalgae, which was induced by using specific species. We further emphasized the potential importance of aquatic invertebrates and the initial quality of native plants in PE-related decomposing processes in aquatic ecosystems. Given the ubiquity

Statement of human and animal right

All applicable international and/or national guidelines for the care and use of animals were followed.

Compliance with ethical standards

Statement of human and animal rights: All applicable international and/or national guidelines for the care and use of animals were followed.

Declaration of Competing Interest

The authors declare that they have no conflict of interests.

Acknowledgments

We sincerely thank the anonymous reviewers for their helpful comments on the manuscript. The authors also thank all the students in their research group for their help in the field.

This study was supported by grants from the Research Project of Yangtze Normal University [010730103]; National Natural Science Foundation of China [51709007].

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