Perspective Chapter: Plant Invasion and Ecosystem Litter Decomposition

Abstract

Litter decomposition plays an important role in the biogeochemical cycling of elements in ecosystems. Plant trait differences especially between invasive and native species lead to changes in litter decomposition rates. The litter decomposition rate is influenced by climatic factors such as seasonal variations, humidity, temperature, and rainfall, where species litter may have different responses. This review aims to better understand how litter decomposes in ecosystems associated with plant invasion and global changes. It also reviews the effects of various factors on litter degradation as well as how quickly invasive litter decomposes and contributes to greenhouse gases (GHGs) emissions. Single species litter or only aboveground litter studies may not sufficiently represent ecosystem dynamics; therefore, the co-determination of above- and belowground litter in a mixture of species diversity is required in different biomes interaction with global change factors. As a result, comprehensive litter degradation studies must be conducted in order to understand the turnover rate of nutrients and other elements in these sensitive ecosystems.

1. Introduction

Litter decomposition is an important process of nutrient cycling in ecosystems. It releases various elements into the soil back to support the plant. The root system absorbs nutrients and provides a source, realizing the exchange of chemical elements within the ecosystem. It is estimated that more than 90% of the nutrients absorbed by plants of nitrogen and phosphorus and more than 60% of mineral elements are returned to the soil through litter degradation hence biogeochemical cycling [1]. Moreover, many studies focused on aboveground litter and few studies found on belowground litter decomposition; however, the combination of both and their environmental condition may well define the ecosystem litter decomposition dynamics.

Invasive species-associated traits have impacts on litter input and litter quality, which possibly alter soil chemistry and change in microbial biomass and activities influences by climatic changes, monitoring the litter decomposition rate dynamics [2, 3, 4, 5]. Litter traits of invasive species are leading factor determining the influences of decomposition rate [2, 6]. Invasive species may get advantage over native species due to higher-quality litter from invasive species. In addition, invasive species have fast growth, higher leaf traits, leaf toughness, and high-nutrient content governing decomposition rate. However, decomposition litter’s non-additive effects may differ from single species decomposition.

Plant invasion and their associated traits-enhanced decomposition rate are also predicted to alter GHGs emission to the atmosphere [7, 8]. Plant invasion alter GHGs emission through its litter input, quality, and changes in soil microbes [9, 10]. However, global change factors through interaction WITH plant invasions indirectly or directly affect litter decomposition. Elevated carbon dioxide (CO₂), nitrogen (N) deposition, and ultraviolet B (VU-B) radiation have been reported to alter decomposition rate of invasive plants [7, 11]. The data presented in this chapter were obtained from professional websites and diverse databases. We conducted a survey in the Web of Science, Google Scholar, PubMed, Science Direct, Springer, CAB abstracts, Taylor, and Francis using different keywords including plant invasion, litter decomposition, GHGs, decomposer, etc., to obtain relevant information regarding litter decomposition in the context of plant invasion and global climate change.

2. Litter decomposition in natural ecosystems

Ecologically, litter refers to dead plant materials or detached from a living plant [9]. Aboveground plant organs (i.e., stem, leaves, and reproductive organs) and belowground plant organs (i.e., roots) form plant litters. These litters decompose through biological (soil microorganism such as bacteria and fungi), physical (abiotic forces such as wind, temperature, moisture, light), and chemical processes, converting organic matter into nutrients and CO₂ [12], hence, maintaining soil nutrients and soil fertility, by vigorously giving support to plant diversity [13]. In turn, microorganism heterotrophic respiration returns CO₂ to the atmosphere [14]. Flora is significantly influenced by litter decomposition, where litter adds nutrients to the ecosystem as recycling of nutrients. Litter decomposition rates are dynamics affected by microbes and soil fauna influences by climatic conditions, rainfall, temperature, and seasonal fluctuations. Litter chemistry is also involved, which influences the decomposition process and soil microbial activities [15]. Slow decomposition adds nutrients stocks and organic matter to the soil; however, fast decomposition rates offer more nutrients to meet plant intake requirements [16]. Additionally, litter chemistry (i.e., organic compounds, N content, C/N ratio), which varies to plant organs (leaves, stem, root, etc.) and plant species (i.e. native vs. invasive), influences the litter quality and decomposition rate [9, 17]. Litter decomposition varies at species level (i.e., native vs. invasive), predicting that species with high N and ash content as well as low C/N and lignin content resulted in high litter decomposition rate [18]. Above- and belowground litters have different environmental conditions where the temperature and precipitation play a key role in difference between leaf and root litter decomposition. Decomposer organisms are another factor, and their biomass decreases in shift community with increase in soil depth. The coordination between leaf and fine root litter decomposition may weaken by divergent decomposition position, yet their mechanism and differences in regulating factors are still unexplored.

2.1 Aboveground litter

Aboveground litter is an organic horizon originated by the plant materials on soil surface [19]. This aboveground organic horizon formation depends on the litterfall rate and decomposition rate of plant materials [20]. Leaves are the main component of forest litter, accounting for about 70%, contributing to more than any aboveground plant organs. In addition, leaves contributed more to nutrient budget in short term, and its decomposition is faster than any other plant organ in grassland and forest [21]. The functional trait syndromes of coarse stem components may not be coordinated with those of other organs [22]; as a result, their afterlife effects on decomposability are poorly coordinated [23]. However, its decomposition rate and turnover may be slow, which is less important in short-term nutrient cycling. Nevertheless, forests have a lot of coarse woody debris (such as branches, stumps, and coarse roots), and leaf decomposition rates alone are not enough to forecast organic matter dynamics [24, 25]. The aboveground litterfall may be influenced by seasonal behavior, characteristics of plantation/species such as aboveground biomass, volume, canopy closure [26], and the environmental condition of the region [27]. On the other hand, litter chemistry and climatic condition play a key role in decomposition rate [28]. Such regulating factors define the differences in aboveground versus belowground litter decomposition, being a gap in the development of ecological research.

2.2 Belowground litter

Most studies have shown that the decomposition rate of root litter is significantly lower than that of leaf litter [21, 29, 30]. The decomposition environment of root litter is very different from that of aboveground litter, and the regulating factors are different [31, 32, 33]. Therefore, the decomposition rate of leaves and its controlling factors cannot be used to infer root decomposition. Sun et al. [34] 6-year findings on 35 species show that based on the rate of decomposition, leaves litter (77%) was higher than root litter (35%), with different regulating factors where leaves decomposition is controlled mainly by lignin:nitrogen ratio; however, non-lignin carbon compounds (phenols and tannins) played a dominant role in root decomposition. In addition, there is no correlation between fine root and leaf litter decomposition rates among different tree species. Moreover, the root size in diameter that may also play an important role in decomposition rate is still controversial [35]. For a long time, due to the limitations of technology and methods, the research of underground ecosystem has become a bottle that restricts the development of ecology [36]. The decay and decomposition of the root system are of great significance to the carbon cycle and the availability of nutrients in the soil. Therefore, in the future, research on the decomposition of underground root litter (such as aboveground and underground whole, roots of different diameters) should be strengthened, especially influencing control mechanism under the background of global change (Figure 1).

Figure 1.

Litter inputs (above- and belowground) co-determine the quality, quantity of litter, and decomposability; and therefore, the dynamics of biogeochemical cycle. A resource acquisitive plant community (a, b) produces litter of consistently higher decomposability than a resource conservative plant community (c, d) (modified from Freschet et al. [21]). In addition, the majority of invasive species in position of higher resource acquisition than native species (see collection of studies [37, 38]), but this may vary or not be the same in regions. Therefore, invasive species may fit to the resource acquisitive plant model to determine their composability but regional differences and environmental factors may influence litter decomposition rate.

3. Factors impacting litter decomposition

Litter decomposition occurs by three major process: fragmentation, leaching, and catabolism [39, 40, 41]. Leaching is the process of removing soluble materials from degrading organic matter. Fragmentation occurs by soil fauna or abiotic agent produces substrate that benefits soil microbes. The catabolic activity of bacteria and fungi is mostly responsible for the chemical change of dead organic matter. Hence, the litter decomposition is regulated by three main factors: litter quality (litter physiochemical characteristics), physicochemical environment (abiotic), and decomposer organism (biotic) [42]. These factors are described in Figure 2.

Figure 2.

Various factors affecting litter degradation (modified from Krishna and Mohan [9]).

3.1 Litter quality

Litter quality can be explained by litter chemistry, which determines litter decomposition [43], and altering soil biota facilitates the decomposition of litter materials [44]. Hence, litter quality such as chemical properties, N concentration, as well C/N ratio controlled the release of nutrients and litter decay [45, 46, 47]. Studies investigating litter quality impacting decomposition are common [48], where C:N ratio and N content play a leading role followed by lignin:N ratio [48, 49, 50, 51]. Nevertheless, the existence of other regulating factors (soil biota, environment) interacting with litter quality makes complexity and is poorly understood. These variables and their impact on litter decomposition depend on plant species and soil characteristics. The quantity and quality of litter constituents, the chemical and physical environment, and decay entities are the key factors that influence organic matter conversion. Moreover, decomposer arrangement in the soil influences litter decomposition rate and nutrient dynamics [42].

3.2 Decomposer

The rate of litter decomposition is known to be affected by the abundance and arrangement of soil fauna and microbial communities at distinct stages of decomposition [52]. Organic material decomposition has significant role in nutrient cycling and energy flow in the ecosystem. Earlier research has identified the importance of a variety of bacteria and fungi in litter decomposition [9], which demonstrated that forest soil and related microbial communities play an important role in the decomposition of litter, under laboratory conditions. Fungi are the top decomposers in the soil microfauna, with a 75% better ability to decompose organic materials than other microbes [53]. Besides, bacteria that involved in litter decomposition mineralization process account for 25–30% of the total microbial biomass in the soil [54]. Generally, decomposers usually grow once the litter reaches the ground; however, the growth of microbes on the litter, particularly fungi, may start decomposition before the litter falls. The composition of microbial community that lives in the litter is determined by the litter qualities, soil characteristics, and changes in these characteristics through time [55]. The quantity and quality of litter input dependent on plant species also affects litter decomposition [4].

Beside bacteria and fungi, soil fauna (micro- and macro-invertebrates) because of their important involvement in mineralization processes, organic matter decomposition and nutrient cycling, as well as pedogenesis, which persist in the litter strata and on the soil upper layer, they are an important aspect of ecosystems [56]. Soil faunal activities primarily aid in the acclimatization of litter and the stimulation of microbial activity.

3.3 Soil and climate factors

Litter decomposition is influenced by the physical and chemical features of the soil. Texture is the most important of them all because it affects water and nutrient dynamics, porosity, permeability, and surface area [9]. Organic matter content, pH, nutrients, and cation exchange capacity are some of the most important chemical features. Among them, organic matter influences the major soil properties, such as soil physio-chemistry (pH, bulk density) affecting litter decomposition, also increasing microbial density [57]. Soil N is considered the primary regulating factor and had received worldwide attention, while phosphorus act as limiting nutrients because of poor availability and circulation in major forests. Furthermore, the rate of litter decomposition is influenced by soil temperature and N concentration. Although magnesium and potassium are important minerals for higher plants, they have little effect on microbial activity and are quickly eliminated from decomposing litter.

Temperature, moisture, and other climatic conditions may influence the rate of litter decomposition. Several studies recorded slow and fast decomposition rate in winter and rainy season, respectively [58, 59, 60], and the higher decomposition in rainy season may be due to the higher micro-fungal population, which may increase with suitable moisture and sufficient rainfall. Zhang and Wang [28] examined 785 datasets demonstrated that mean annual temperature was important factor driving decomposition on global scale at different climatic zones. Kumar et al. [61] also found increase in litter decomposition rate and weight loss in rainy season with high microbial load and soil moisture. However, there is still controversy about which climate index best predicts decay rates. Although there is water in the soil, actual evapotranspiration is the most important factor in determining the litter decomposition rate [62]. In contrast, some studies disagreed with the concept of relation between litter decomposition and actual evapotranspiration as a reliable indicator of decay litters [63, 64, 65].

4. Plant invasion effects on litter input and decomposition rate

Increase in invasive species traits such as specific leaf area, leaf dry matter content, plant height and stem-specific density [66] accumulates high biomass, and nutrient contents, especially N, P, and K [67], produce high quantity, and quality litter further increases litter decomposition rate. Invasive plant litter input further increases microbial biomass [67], and soil enzymatic activities [67, 68] may be attributed to the fast decomposition rates.

Plant invasions in the invaded ecosystems can significantly change the ecosystem functioning. Invasive alien plants may have a significant impact on litter decomposition, which is one of these ecosystem services. According to reports, the C/N ratio can be used to calculate the decomposition of leaf litter, which varies at species level [69]. High-quality leaves (nutrient-rich leaves) decompose at a faster rate than low-quality leaves (nutrient-deficient leaves). Invasive species produce litter of higher chemical quality, which decompose rapidly and release high nutrients to the soil [70]. In general, species with high ash and nitrogen content, as well as low C/N ratios and lignin concentration, decompose quickly [71]. Patil et al. [70] found higher N and P concentration, and low lignin and C/N ratio in invasive species resulted in higher rate of litter decomposition when compared to native species. Several studies found that litter nitrogen concentration and the C/N ratio are closely linked to litter degradation rates [72]. Phosphorus concentrations and C/P ratio seemed to be strong indicators of degradation rate [73]. Plant litter lignin concentrations and lignin/N ratios are also good predictors of litter decomposition rate [69].

A meta-analysis of 94 studies across world by Liao et al. [74] demonstrated that invaded communities have a 117% rise in litter decomposition rates. In contrast, some findings revealed no change or even decrease in litter decomposition rate associated with invasive plants [3, 74, 75]. These effect differences of invasive species on litter decomposition rates may influence functional (litter) traits of invasive species and the communities [76]. Thus, functional traits can be a good and mechanistic approaches define variation in decomposition rates. Leaf traits have been found to affect litter quality and hence alter litter decomposition rates at species level [2, 77, 78]. Invasive species leaf traits are associated with fast growth, high specific leaf area, leaf thickness and toughness, low leaf dry matter content, and high leaf nutrient concentrations, and such traits are directly involved in high leaf decomposition rates [66, 79]. Study by Zhang et al. [80] found that litters of invasive Alternanthera philoxeroides decompose faster than annual native grass (Eragrostis pilosa), but in case of mixture, invasive litter decomposition rate was constant and caused increase in the native litter decomposition rate.

Single species do not sufficiently represent an ecosystem function and litter decomposition. Non-additive effects mainly depended on species composition and diversity may further strengthen by litter chemistry [81]. Mixed litter can change the chemical environment as well as the physical surface area of the litter where decomposition takes place. It can also have an impact on ecological processes including soil respiration [82], net N mineralization [83], and microbial activity in the soil. Invasive Solidago canadensis litter alone had higher N concentration, but in mixture with native Phragmites australis decreased the N concentration of Solidago canadensis litter but increased that of Phragmites australis litter [83]. Nutrient transfer across litters in mixture may have favorable non-additive effects [84]. The single species litter decomposition is possibly to shift by litter mixture, and that mixture litter effect has been observed as positive interaction in early stage and been shift to negative non-additive effect over certain time duration [83, 85]. Litter decomposition of invasive species is more depended on N and P than native species [6], and in a case of N transfer of invasive litter to native litter may slow down the decomposition rate, which may be influenced by secondary metabolites.

5. Plant invasion effects on soil GHGs emissions via litter decomposition

The raising GHGs disrupt the natural ecosystems and challenge the management of natural habitats on a global scale. The anthropogenic activities are directly or indirectly involved in the production of these GHGs emissions. Plant invasion is one of the factors that alter GHGs emissions in many ways mainly by their litter quantity, quality, and soil microbe alteration involved in the production of GHGs emissions/process [9]. The numerous elements and chemicals that accumulate in plants are released into the environment via litter decomposition, leaching into the soil and diffusing into the atmosphere. As a result, these compounds are being reintroduced into the biogeochemical cycle. Soil chemical environment created by litters associated with invasion may shift biogeochemical processes through changes in litter decomposition rate. Grassland ecosystems invaded by Alternanthera philoxeroides or Solidago canadensis produced higher N₂O (60%) and CO₂ (30%) than that of non-invaded grassland ecosystems (dominated by Eragrostis pilosa or Sesbania cannabina) [86], where invaded ecosystem, produced more (155–361%) rapidly decomposing litter than that of non-invaded ecosystem [82], might be due the large litter input and higher C:N ratio associated with invasions. Another study by Zhang et al. [83] demonstrated that Solidago canadensis invasion loss (mass and N) was higher than native Phragmites australis, while native decreased and invasive increased N loss in a mixture litter (Figure 3).

Figure 3.

Litter decomposition and its role in biogeochemical cycle. The accumulated compounds and elements by plants returns to environment through litter degradation; conversion of these organic matter results in nutrients and GHGs into the atmosphere (modified from Krishna and Mohan [9], created with biorender, https://www.biorender.com/).

6. Interactive effects between plant invasions and other global change factors on litter decomposition

Biological invasions-associated traits alter soil chemistry [87], soil enzymatic activities [68], further impact on litter decomposition [7], which resulted in higher GHGs emission [88]. Nitrogen deposition and elevated CO₂ potentially affect litter decomposition through change in litter quality and quantity [7]. In contrast, elevated CO₂ decreased the invasive Triadica sebifera litter decomposition via change in litter quality [7]. Moso bamboo invasion decreased the sensitivity of decomposition rate in response to mean annual precipitation and mean annual temperature [89].

An increase in water level caused decrease in nutrient release and decomposition rate from invasive plant litter [90], which might be due to the decrease of anaerobic microbial activities in high water level [91]. Suitable moisture condition will offer more nutrients that increase microbial biomass and activities will further accelerate litter decomposition rate [92]; invasive species often associated with nutrient-rich litter will get an advantage in this case.

UV-B exposure during litter decomposition may have a direct effect on decomposition rates by changing photodegradation states or decomposer composition in the litter, whereas UV-B exposure during growth periods may alter plant chemistry and physical properties. Meta-analysis of six biomes by Song et al. [93] demonstrated that elevated VU-B directly (7%) and indirectly (12%) increased litter decomposition rate, while attenuated UV-B decreased the rate of litter decomposition. In addition, the interactive effect of UV-B and N deposition increased litter decomposition rate of moso bamboo [94], and coarse woody debris [11].

7. Conclusions

This review focuses on ecosystem litter decomposition in the context of plant invasion associated with global change factors. Litter quality and traits in association with soil microbes and environmental factors play a leading role in decomposition rate. Plant traits associated with plant invasion alter litter input, soil microbes, and soil enzymatic activity, and hence increase litter decomposition rates. Studies on single species, and/or only aboveground litter or belowground litter do not represent decomposition rate sufficiently in ecosystem. Therefore, there is required co-determination of species diversity in different biomes both above- and belowground litter with their associated environment, regulating factors, and global change factors.

Acknowledgments

The study was fanatically supported by Research Funding of Jiangxi Agricultural University (9232305172) and First-Class Discipline of Forestry of Jiangxi Province.

Conflict of interest

The authors declare no conflict of interest.