Dynamics and characteristics of biogenic silica and macro- and microelements in decomposing litter in the Min River estuary, southeast China

Many studies regarding the decomposition dynamics of plant litter have been undertaken over previous decades (Prescott, 2005, 2010), with these found to be fundamental for nutrient cycling and play a significant role in ecosystem productivity and global climate change (Liski et al., 2003; Moretto and Distel, 2003; Tuomi et al., 2009; Schaller and Struyf, 2013; Ochoa-Hueso et al., 2019). Marsh ecosystems are characterized by fast plant growth and high biomass (Struyf and Conley, 2009), with a great majority (approximately 80%) of the annual plant production becoming litter (Bouchard and Lefeuvre, 2000; Struyf et al., 2007). The decomposition of plant litter in marshes, especially in tidal marshes, affects the accumulation of organic matter and the transfer of nutrients and chemical elements, as well as influences the potential export of materials toward ambient environments (White and Howes, 1994). Although both biotic and abiotic factors controlling litter decomposition rates have been widely researched, knowledge regarding the dynamics of elements during the process is limited to only a few nutrients: C, N, and P (Osono and Takeda, 2004; Gautam et al., 2016; Gautam et al., 2019). Compared with these macroelements, the dynamics of silicon (Si) and other microelements during litter decomposition have received limited attention (Berg and Laskowski, 2005).

Si is a “beneficial” element for plants, providing structural support (Epstein, 1994; Schoelynck et al., 2010) and alleviation against biotic and abiotic stressors (Ma, 2004; Massey et al., 2006; Pavlovic et al., 2013). Wetland plants take up dissolved Si (DSi) from the soil or water to increase their rigidity and survival chances, which accumulate as biogenic silica (BSi) in plant tissues (Schoelynck et al., 2010). After vegetation dieback and subsequent litter decay, BSi is gradually released back into the abiotic environment and is usually transferred to DSi in the water (Bartoli, 1983; Struyf et al., 2007; Struyf and Conley, 2009; Vandevenne et al., 2013). Tidal marshes have been shown to accelerate the cycling process at the land–sea interface (Struyf et al., 2006). For example, the decomposition of Phragmites australis (PA) in a small freshwater tidal marsh resulted in more than 40% of DSi export in Belgium (Struyf et al., 2007). To date, the few studies that have examined BSi content in plants being linked to litter decomposition remain controversial on decomposition rate, dynamics, and factors (Eleuterius and Lanning, 1987; Cornelissen and Thompson, 1997; Struyf et al., 2007; Schaller and Struyf, 2013; Alfredsson et al., 2016; Emsens et al., 2016). Inconclusive interactions between litter BSi and other litter quality parameters are reasons for such debate (Schoelynck et al., 2010; Cooke and Leishman, 2012; Schaller et al., 2012). Schaller and Struyf (2013) concluded that Si availability in marshes dominated by PA plays an important role in C sequestration, nutrient cycling, and remobilisation during aquatic litter decay. In estuarine wetlands, release by plants might affect the rate of nutrient export, especially for Si, toward the open water and eventually the oceans, thereby affecting the global nutrient cycle (Ehrenfeld et al., 2005; Borrelli et al., 2012; Struyf and Conley, 2012; Liu et al., 2019; Ochoa-Hueso et al., 2019; Xia et al., 2020).

Heavy metal pollution is common globally, especially in estuarine marshes, where large quantities of heavy metals are imported (Duarte et al., 2010), threatening food security and creating extreme risks to human health (Liu et al., 2019; Wang et al., 2020). Although it has been well-documented that accumulated metals can retard litter decomposition processes (Tyler, 1976; Laskowski et al., 1994; Johnson and Hale, 2004), it is unknown whether such metals influence BSi release by marsh litter. Additionally, knowledge regarding the coupling relationship of BSi and other macro- and microelements (such as C, N, and some heavy metals) in the decomposing litter is relatively scarce. The effect of these elements on litter decomposition is critical in estuarine marshes, which is the land–ocean transition zone, because elements released from litter fundamentally influence the coastal wetland ecosystem and oceanic red tides.

In the Min River estuarine marsh, the native species include PA and Cyperus malaccensis (CM), with Spartina alterniflora (SA) starting to invade this marsh in 2002 and gradually becoming the dominant species. Originally, different plant communities were distributed zonally from the land to the sea (Tong et al., 2010). In recent years, there has been a high load of total pollutants (8.6–12.9 × 10⁵ tonnes) from industrial and urban sewage and mining enterprises entering the Min River basin (Li et al., 2020). This marsh is now contaminated with multiple heavy metals, mainly caused by human interferences (Hou et al., 2009). Levels of Cu, Pb, Zn, and Cd in this marsh soil are higher than those in most estuarine wetlands in China (Cai, 2011).

The objective of the present study was to explore the dynamics of BSi, C, N, and heavy metals (Cu, Cr, Zn, Cd, Pb, Al, Mn, and Fe) in three litter types of CM, PA, and SA using the litterbag approach during in situ experiments. Additionally, the litter BSi amount was linked to C, N, and heavy metal amount to compare their release rates and explore their mutual correlation. Several key abiotic factors and the accompanying changes in BSi and other elements were addressed to determine the effects of litter decomposition on the Min River estuary wetland ecosystem.

The sites chosen for the present study are located in an intertidal zone of the Shanyutan marsh (119°34′12“–119°40′40” E, 26°00′36“–26°03′42” N), the largest tidal marsh (approximately 893 hm²) in the Min River estuary, southeast China (Figure 1; Liu et al., 2006). The mean annual temperature is 19.6 °C and the average annual precipitation is 1,350 mm (Zheng et al., 2006). The marsh sediment in this area is dominated by saline soil, and the main vegetation species include PA, CM, and SA from the seawall to the sea. More detailed descriptions of the sites are provided by Tong et al. (2011) and Gao et al. (2019).

The litterbag technique was used to study the litter decomposition in the experimental plots (black symbols in Figure 1), which were placed at the center of each plant community, from October 2014 to March 2016. In September 2014, the standing withered aboveground litter was collected from three single communities, which were PA-, CM- and SA-dominated. The litter was washed with tap water and then deionized water, chopped into 10-cm pieces, and oven-dried at 80 °C until it reached a constant weight. Oven-dried litter (25 g) was placed in 20 × 30 cm nylon litterbags with a mesh size of 0.2 × 0.2 mm for in situ decomposition. The 0.2 × 0.2-mm mesh size allowed free entry of soil microorganisms that might fragment the litter and prevented any significant loss of fragmented litter by macroinvertebrates. Thus, the decomposition process was mainly mediated by microflora.

On October 18, 2014, three bamboo stakes of distances between 20 and 30 m were positioned in the experimental plots of the three plant communities. Litterbags were randomly tiled at the sediment surface in the different plant communities, with only one side of the litterbag contacting the ground. The litterbags were fixed to the bamboo stakes with approximately 3 m of ropes to prevent the litterbags from being carried away by the tide. Three replicate bags were removed from each stake on the 7th, 15th, 28th, 56th, 91st, 148th, 190th, 224th, 285th, 343rd, 400th, 460th, and 520th day and immediately brought back to the laboratory. Thus, we had 3 species × 3 replicates × 13-time samplings = 117 samples in total. These collected litterbags were immediately transferred to the laboratory and cleaned with slow-running tap water to remove the adhering sediments and macroinvertebrates. The litter remains in the bags were carefully removed and cleaned by hand using deionized water and oven-dried at 80 °C until a constant weight. The oven-dried samples were successively weighed and finely ground for subsequent chemistry analysis.

To extract BSi, 30 mg of litter powder was digested for 5 h with Na₂CO₃ (0.1 mol/L) at 85 °C (DeMaster, 1981; Struyf et al., 2005). Dissolved BSi in the extractions was measured by the Molybdate blue spectrophotometric method (Saccone et al., 2006).

Total organic C and N content in the litter was measured with a Vario EL III Element Analyser (Elemental Scientific Instruments, Langenselbold, Germany).

A ground sample of 0.04 g was digested with 2 mL of HNO₃ (70%) and 2 mL of H₂O₂ (30%) at 180 °C for 10 h in closed 60-mL Teflon bottles (Savillex, Minnetonka, MN, USA). Digested samples were diluted with 1% HNO₃, and the concentration of heavy metals (Cr, Cu, Cd, Zn, Pb, Al, Mn, and Fe) in all samples was determined with inductively coupled plasma mass spectrometry (XSeriesII; Thermo Company, Waltham, MA, USA) analysis. Quality assurance and control were assessed with duplicates (three replications), method blanks, and certified reference material (GBW10020) from the National Research Center for Standards in China for each batch of samples (two blanks and one standard for every 30 samples). The temperature and conductivity of the topsoil (0–10 cm in depth) were measured with a portable instrument (Spectrum Technologies, Inc.; Chicago, IL, USA), whereas the pH of the topsoil was determined with a portable pH meter (HACH-sensION3; Loveland, CO, USA).

To correlate litter decomposition rates with measures of litter quality, litter decomposition rate (k, d^–1), litter release rate (P, %), and the accumulation index (AI, %) were calculated for each litter replicate using the following equations, respectively (Olson, 1963; Swift et al., 1979; Harmon et al., 1999):

where X_t is the mass at time t, X₀ is the initial mass, and t is time (days).

where C_t is the content or concentration of BSi or macro- or microelements in the litter at time t and C₀ is the initial content or concentration at the beginning of the experiment. P can reflect the loss rate of nutrients or heavy metals from the litter at the end of decomposition. AI can represent the accumulation or release status of elements in the litter. An AI value greater than 100% indicates net accumulation of BSi or macro- or microelements in the litter. A value less than 100% means net release. “j” stands for BSi, C, N, or heavy metals.

A one-way analysis of variance was performed on the original data to analyze the significant differences in decomposition rates and the amounts and AIs of BSi, C, N, and heavy metals among the three litter species. Regression analyses were used to determine the exponential relationships between the natural logarithm of the mass remains and the decomposition days. Pearson’s correlation analysis was used to correlate the BSi content in the litter with the chemical parameters (C, N, C/N ratios, and heavy metals) of the litter and the environmental indices.

The mass loss rate of the three litter species increased during the early decomposition stage and was stable during the later stage, indicating that litter decomposition had almost stopped (Figure 2). After 520 days of in situ decomposition, only 14.71% PA, 13.63% SA, and 7.93% CM of the initial litter mass was left in the litterbags. Comparison of the decomposition process for each species revealed that CM exhibited the highest decomposition rate (0.005 d^–1), followed by SA (0.004 d^–1) and PA (0.003 d^–1) with no significant differences (P > 0.05; Table 1). Significantly higher t_0.95 (time needed for 95% of the litter dry mass to decompose) was observed for PA (442 days) than for SA (438 days) and CM (281 days).

The initial BSi content and mean C/N ratio are shown in Table 1. As the decomposition process proceeded, BSi, C, and N amounts in the litter decreased for all species with a rapid decline during the initial period and a slow release during the later period. The release dynamics of BSi and C were relatively steady, whereas the release dynamics of N were irregular, with a fluctuating variation during the middle period (Figure 3). The release dynamics significantly differed among the species for N amount (P < 0.05) but not for BSi and C. BSi amount in PA was significantly different to those of CM and SA (P < 0.05); however, no statistical differences were observed between CM and SA (P > 0.05). After 520 days of decomposition in the three species, the BSi release rate was the highest, followed by that of C and N. The BSi release rates in PA, SA, and CM were 97.23%, 96.75%, and 98.64%, respectively, whereas those for C were 85.05%, 87.68% and 92.85%, and those for N were 85.45%, 81.45%, and 78.71%, respectively.

The AIs of the three litter species for BSi, C, and N were all less than 100%, indicating net release throughout the 520 days of decomposition. The trend for AI_BSi resembled that of AI_C, with little variation during most of the experiment for the three litter species. In contrast, the trend for AI_N differed among the three litter species, with higher CM AIs showing that the N release rate for CM was lower than those of PA and SA. For C and N, toward the end of the experiment (after 400 days), AI had slightly increased except for N of SA, indicating that the three litter species completely released C and N during the decomposition process, but after a certain period, they began to accumulate C and N from the ambient environment. However, there was a net release of BSi from the decomposing litter in the Min River estuary marsh. For BSi and C, no significant correlations were found among the AIs of the three species (P > 0.05). For N, the AI of CM was significantly different from those of PA and SA (P < 0.05); however, no statistical differences were observed between PA and SA (P > 0.05).

The changes in the amounts and AIs of heavy metals during decomposition for the three litter species showed that their dynamics were specific for each litter type (Figures 4 and 5). The amount of most of the heavy metals first increased and then decreased, except for Mn and Cr that showed the opposite trend. After 520 days of decomposition, PA, SA, and CM litter had released 87.50%, 72.82%, and 76.48% of their initial Cr amount and 67.01%, 85.14%, and 84.20% of their initial Mn amount, respectively (Table 2). There were also some decreases in Cu (22.91%), Zn (76.44%), and Cd (87.91%) in CM litter and Zn (34.29%) in PA litter. Nevertheless, other metals in other species were characterized by an increase in metal amounts during the decomposition process (Table 2). For different species, PA litter had higher Cu, Cd, Pb, Al, and Fe amount. SA litter was enriched in most metals except for Mn, whereas CM litter released most metals except for Pb, Al, and Fe.

The AIs of Cd were all lower than 100%, showing net release in the three litter species. The AIs of Mn were mostly lower than 100%; therefore, Mn was predominantly released by the three litter species during decomposition with some exceptions for PA. Higher content and AI of Cr and Zn during most early stages characterized their enriching, whereas both content and AI of Cr and Zn decreased from approximately the 250th day, indicating their releasing pattern during the later stages. Mn, Cr, and Zn were predominantly released during the decomposition of the three litter species, whereas there was net release of Cd. Thus, the AIs of the other heavy metals, including Cu, Pb, Al, and Fe, were higher than 100%, and their amounts increased, with the highest value found during the middle stage of decomposition, showing their enriching process.

Litter decomposition is an important pathway controlling nutrient cycling in wetlands (Jordan et al., 1989). Litter quality affects litter decomposition rates, and the C/N ratio is often used as a predictor of decomposition rates because it reflects the ratio of carbohydrate and lignin to protein in the litter, that is, a high ratio usually results in a low decomposition rate (Moretto and Distel, 2003). In the present decomposition experiment, the decomposition rates significantly differed among the species in the order of CM > SA > PA, which is consistent with Tong et al. (2011). CM showed the highest decomposition rate (0.005 d^–1) and required the shortest time (281 days) for 95% decomposition of 25 g of dry litter (Figure 2 and Table 1). There were few differences between PA and SA for the decomposition rate and t_0.95. The mean C/N ratio of CM during decomposition was lower than that of SA (Table 1), which could account for the higher average decomposition rate of CM. Nevertheless, the relationship between the C/N ratio and decomposition rate is not absolute. SA, which had the highest C/N ratio, showed a lower decomposition rate than that of CM and a higher decomposition rate than that of PA. Inhibited decomposition is attributed to a high C/N ratio because decomposition is alleviated when N is added to the solution (Rosemond et al., 2010). High C/N ratios (greater than 30) could hamper plant decomposition because of microbes (Atkinson and Cairns, 2001). Hence, high C/N ratios (42.91 ± 1.77) and the 0.2-mm mesh size, which only allowed the entry of microorganisms, led to lower decomposition for SA in the present study.

PA, a herb with high lignin and cellulose content (Gessner, 2000), had the lowest decomposition rate (0.003 d^–1) and required the longest time (442 days) for the decomposition of 25 g dry litter in the present study (Figure 2 and Table 1). Schaller and Struyf (2013) showed that reed leaf litter decay by heterotrophic microbes (as the central part of litter decay) was strongly influenced by Si availability during plant growth, with higher decay rates for the litter with higher Si content. However, this is inconsistent with the results of the present study, where plant litter with higher BSi content had lower decay rates for PA, SA, and CM in the Min River estuary. This can be explained by the discrepancy between the leaves and the entire plant. Additionally, litter decomposition rates among the three species had nonsignificant correlations with soil pH, conductivity, and temperature (P > 0.05), implying that these abiotic factors might have a negligible influence on litter decomposition rates for a long-term study in the Min River estuary.

Litter decomposition is one of the most important ecosystem processes that can modulate elemental biogeochemistry (Berg and Laskowski, 2005; Prescott, 2005). The release and retention of nutrients in the litter directly determine the nutritional status of the marsh ecosystem and ultimately affect the ecosystem productivity (Tong et al., 2011; Zhang et al., 2014). After vegetation dieback and subsequent litter decay, Si, C, and N are gradually released back into the ambient environment (Struyf and Conley, 2009; Vandevenne et al., 2013). However, the amount and AI of N in PA, SA, and CM showed an increasing trend during the early stages of in situ decomposition. N is a limiting factor for the growth of decomposer populations (Blair, 1988). Hence, many studies have stated that N dynamics in the decomposing litter are generally characterized by an initial immobilization phase followed by a release, indicating that insufficient N might limit decomposer activity during the early stages (Blair, 1988; Parton et al., 2007; Manzoni et al., 2010; Van Nevel et al., 2014).

We observed that the BSi/C and BSi/N patterns steadily decreased during decomposition, except for a few time points (Figure 6). Therefore, BSi was removed from the decomposing litter much faster than C and N, which supports the findings of Struyf et al. (2007). During the first 50 days, the dramatic dynamics of BSi/(C, N) might be due to interactions with abiotic and biotic factors. Thus, it is important to study plant decomposition during the initial stage, in which large soluble nutrients are rapidly released. Schaller and Struyf (2013) found that the aquatic litter decomposition process is controlled in the tropics mainly by microbes. Microorganisms in litter can absorb nutrients from the surrounding environment to maintain their activity, which increases the decomposition of nutrients in the litter (Liao et al., 2008). In nutrient-rich environments, soil bacteria thrive and accelerate decomposition (Fierer et al., 2012). Between the 200th and 350th day, BSi/C values increased, which was attributed to more C released than BSi. For CM, BSi/(C, N) values were lower than those of PA and SA, thus implying CM released less BSi than those of the other two species.

To date, the effects of BSi content in litter on decomposition rates have remained unclear. Several researchers have suggested that high litter BSi content hampers decomposition (Cornelissen and Thompson, 1997); however, the opposite patterns have also been reported (Schaller and Struyf, 2013). In the present study, the BSi release rate and the initial BSi content were 97.23% and 85.46 mg/g in PA, 96.75% and 50.67 mg/g in SA, and 98.64% and 45.91 mg/g in CM, respectively (Table 1). Therefore, there was no relationship between the BSi decomposition rate and the initial content. Moreover, for the three species, the average release rates of C and N were 88.52% and 81.87%, respectively. BSi in PA, SA, and CM was released thoroughly into the Min River estuary; however, it was not the same for C and N. AIs of C, N, and BSi in the three litter species were lower than 100%; therefore, there were net releases of these three elements by PA, SA, and CM during the 520 days of decomposition. Litter decomposition is an important resource of BSi in wetland ecosystems, and it exports rich BSi to the estuary or sea, affecting the wetland and global nutrient cycling.

Previous studies have indicated that the release or accumulation of metals during litter decomposition involves the following two major processes: the release of metals from the litter as they oxidize and the retention of metals on organic films of the litter (Pellenbarg, 1984; Du Laing et al., 2006). For the different heavy metals in the three marsh plants in the present study, Al and Fe were present at high levels, but other heavy metals (especially Pb and Cd) were present in minute quantities. The change in the content of heavy metals during decomposition showed that their dynamics were distinct for each litter type (Figures 4 and 5). The amounts of heavy metals increased in the beginning and decreased afterward, except for Mn that showed the opposite trend. An increase in the metal amount is attributed to different factors such as contamination by sediment particles, passive sorption onto recalcitrant organic fractions, and active accumulation by microbial colonizers (Breteler et al., 1981; Gadd, 1993; Zawislanski et al., 2001; Kovacova and Sturdik, 2002). As litter decomposition proceeds, organic acids forming during the humification could create stable complexes with metals and, therefore, affect the metal solubility and speciation (Fox and Comerford, 1990). Subsequently, litter rich in humic substances might have oxygen-containing functional groups to bind heavy metals and form stable complexes (Laskowski et al., 1995). Thus, as the amount of humic substances increases during decay, presumably more metal ions can be bound to the decomposing litter (Gautam et al., 2019). In the present study, analogous results were found, in which most heavy metals began to enrich the litter during the later decomposition period, which was attributed to heavy pollution from multiple heavy metals due to gradually enhanced human interferences in the Min River estuary (Hou et al., 2009; Cai, 2011). The AIs of Al, Fe, Pb, and Cu were mostly greater than 100%; therefore, there was net accumulation of these metals during the 520 days of in situ decomposition. Cd, Mn, Cr, and Zn showed net release during the majority of the decomposition period. Therefore, as the plant litters decomposed, they acted differently to enrich or release heavy metals. Simultaneously, the heavy metal amount in the wetland soil or ambient surroundings affects the enrichment or release of these metals by the litters (Weis and Weis, 2004; Du Laing et al., 2006; Keuskamp et al., 2015; Li et al., 2020). Fungi can accumulate and transfer significant amounts of elements from organic and mineral soil to decomposing litters (Tyler, 2005; Van Nevel et al., 2014).

Pearson’s correlation analysis results showed that the BSi amount was adversely correlated with N and some heavy metal amount in the three decomposing litter species, especially for Cu, Cd, Pb, Al, and Fe with significant correlation coefficients (Table 3), which persistently accumulated during the decay process except for Cd. Later in the decomposition process, the more the heavy metals such as Cu, Pb, Al, and Fe accumulated, the slower was the release of BSi that eventually stopped. Thus, we deduced that the N amount and these heavy metals in the litter restrained the BSi release. Such a finding requires further studies for confirmation. The BSi amount was also adversely correlated with the Zn and Mn amount with nonsignificant differences (P > 0.05). Significant negative correlation was found between the BSi and C amount for PA and CM but not for SA. Similarly, on comparing the start and end of experiments, it was found that a significantly lower C amount in the reed leaf litter correlated with a high BSi amount and significantly lower values for most other elements (such as N, Mn, Fe, and Cu; Schaller and Struyf, 2013). Further research is required to explore the positive correlation between the BSi and C amount for SA. A significant positive correlation between the BSi amount and C/N ratio for the three litter species was also observed; therefore, the high C/N ratio of the litter had a stimulative influence on BSi release by the litter.

In conclusion, the present study characterized the dynamics of BSi and other macro- and microelements, including C, N, and heavy metals, during 520 days of decomposition of PA, CM, and SA in the Min River estuary in southeast China. The decomposition rates significantly differed among the species in the order of CM (0.005 d^–1) > SA (0.004 d^–1) > PA (0.003 d^–1). The BSi amount generally decreased in the three litter species and significantly differed among the three species, and BSi was removed from the litter much faster than C and N. The present study clearly showed that there were net releases of BSi, C, and N by PA, SA, and CM, and Cd, Mn, Cr, and Zn were predominantly released, with a net accumulation of Cu, Pb, Al, and Fe during the decomposition period. Pearson’s correlation analysis results showed that the BSi amount was adversely correlated with the N, Cu, Cd, Pb, Al, and Fe amount with a significant correlation. The present study revealed that the decomposition of marsh litter is an important source of BSi and has far-reaching effects on ecosystem functioning in marshes of the Min River estuary.

The data generated for this study can be found at the following location: https://data.mendeley.com/datasets/h4v22c7ggv/1.

We thank the Natural Science Foundation of China for awarding funding to SJ Zhai to run the fund-Controlling factors of spatiotemporal distributing characteristics of Silicon in Min river estuary and its mechanism (Grant No. 41401114). SJ Zhai acknowledges the funding of “Study on the characteristics and influencing factors of silicon, carbon and nitrogen during litter decomposition in Min River Estuarine Wetland” from Science and Technology Department of Fujian Province under grant agreement 2016J01184.

The authors have no competing interests to declare.

Contributed to conception and design: SJZ

Contributed to acquisition of data: GYH, HG

Contributed to analysis and interpretation of data: SJZ, STQ

Drafted and/or revised the article: SJZ, STQ

Approved the submitted version for publication: SJZ

How to cite this article: Zhai, S, Qiu, S, Gao, H, Hou, G. 2020. Dynamics and characteristics of biogenic silica and macro- and microelements in decomposing litter in the Min River estuary, southeast China. Elementa Science of the Anthropocene 9(1). DOI: https://doi.org/10.1525/elementa.2021.00084

Domain Editor-in-Chief: Steven Allison, University of California, Irvine, CA, USA

Guest Editor: Juan Liu, Guangzhou University, Guangzhou, China

Knowledge Domain: Ecology and Earth Systems

Part of an Elementa Special Feature: Pan-Pacific Anthropocene