Invasive plant indirectly regulates native plant decomposition by affecting invertebrate communities
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].
References (60)
- et al.
Seasonal features of zooplankton assemblages in the nearshore area of southeastern Lake Michigan
J. Great Lakes Res.
(1980) - et al.
Community respiration of decomposing plants in Oregon estuarine marshes
Estuar Coast Shelf S
(1984) - et al.
Priming effects in different soil types induced by fructose, alanine, oxalic acid and catechol additions
Soil Biol. Biochem.
(2005) - et al.
A colorimetric method for ammonia in natural waters
Water Res.
(1970) - et al.
Exotic plant invasions and the enemy release hypothesis
Trends Ecol. Evol. (Amst.)
(2002) - et al.
Rapid response to shoot removal by the invasive wetland plant, alligator weed (Alternanthera philoxeroides)
Environ. Exp. Bot.
(2007) - et al.
Effects of water quality characteristics on the algicidal property ofAlternanthera philoxeroides (Mart.) Griseb. in an aquatic ecosystem
Biochem. Syst. Ecol.
(2012) The impact of the invasive shrub Lonicera maackii on the decomposition dynamics of a native plant community
Ecol. Appl.
(2012)- et al.
Functional diversity of crustacean zooplankton communities: towards a trait-based classification
Freshw. Rev.
(2007) - et al.
Freshwater Algae: Identification and Use as Bioindicators
(2010)
No evidence of aquatic priming effects in hyporheic zone microcosms
Sci Rep-UK
Positive priming of terrestrially derived dissolved organic matter in a freshwater microcosm system
Geophys. Res. Lett.
Soil carbon stocks in experimental mesocosms are dependent on the rate of labile carbon, nitrogen and phosphorus inputs to soils
Funct. Ecol.
Invasive plants versus their new and old neighbors: a mechanism for exotic invasion
Science
Bacteria and algae in stream periphyton along a nutrient gradient
Freshw. Rev.
Two microinvertebrate affect microbial and macroinvertebrate-driven litter breakdown
Freshw. Rev.
Uptake and decomposition of the herbicide propanil in the plant Bidens pilosa L. Dominating in the Yangtze Three Gorges Reservoir (TGR), China
Environ Sci Pollut R
Impacts of invasive riparian knotweed on litter decomposition, aquatic fungi, and macroinvertebrates
Biol. Invasions
Feeding ecology of stream invertebrates
Annu Rev Ecol Evol S
The use of invertebrate functional groups to characterize ecosystem attributes in selected streams and rivers in south Brazil
Stud Neotrop Fauna E
Effects of burial on leaf litter quality, microbial conditioning and palatability to three shredder taxa
Freshw. Rev.
Benthic algae stimulate leaf litter decomposition in detritus-based headwater streams: a case of aquatic priming effect?
Ecology
Experimental assessment of a possible microbial priming effect in a humic boreal lake
Aquat. Sci.
Predation of cyanobacteria by protozoa
Can. J. Microbiol.
Effects of exotic plant invasions on soil nutrient cycling processes
Ecosystems
A user-friendly guide to the ciliates (Protozoa, Ciliophora) commonly used by hydrobiologists as bioindicators in rivers, lakes, and waste waters, with notes on their ecology
Freshw. Rev.
Soil respiration in a mixed oak forest
Oikos
Negative priming effect on organic matter mineralisation in NE Atlantic slope sediments
PLoS One
Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness
Ecol. Lett.
The role of invertebrates on leaf litter decomposition in streams – a review
Int. Rev. Hydrobiol.
Cited by (3)
Response of aquatic plant decomposition to invasive algal organic matter mediated by the co-metabolism effect in eutrophic lakes
2023, Journal of Environmental ManagementCitation Excerpt :It has been reported that the decomposition rate of microorganisms is highly sensitive to the response of plant characteristics, and the decomposition process is staged (Song et al., 2010; Creamer et al., 2015; Zhan et al., 2021). However, current studies mainly focus on the effect of different plant species on microbial decomposition rate, and few reports have further explored the insight plant components (Zhao et al., 2021; Chen et al., 2022). To analyze the changes in the components of aquatic plants is therefore crucial to understand the differences in microbial decomposition processes.