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Article

The Influence of Exogenous Nitrogen Input on the Characteristics of Phytolith-Occluded Carbon in the Kandelia obovata Soil System

by
Huiming You
1,2,3,
Lidi Zheng
1,2,3,
Weibin You
4,5,
Fanglin Tan
1,2,3,*,
Fangyi Wang
4,5,
Yan Cao
4,5,6,
Tongchao Le
1,2,3,
Jie Lin
1,2,3 and
Jiangrong Lv
4,5
1
Fujian Academy of Forestry, Fuzhou 350012, China
2
Wetland Ecosystem Research Station in Quanzhou Estuary, Quanzhou 362000, China
3
Fujian Provincial Key Lab of Forest Silviculture and Forest Product Processing Utilization, Fuzhou 350012, China
4
College of Forestry, Fujian Agriculture and Forestry University, Fuzhou 350002, China
5
Fujian Southern Forest Resources and Environmental Engineering Technology Research Center, Fuzhou 350002, China
6
College of Finance, Fujian Jiangxia University, Fuzhou 350108, China
*
Author to whom correspondence should be addressed.
Forests 2023, 14(11), 2202; https://doi.org/10.3390/f14112202
Submission received: 11 September 2023 / Revised: 2 November 2023 / Accepted: 3 November 2023 / Published: 6 November 2023
(This article belongs to the Special Issue Coastal Forested Wetland Conservation and Carbon Function)
Browse Figures
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Abstract

:
Phytolith-occluded Ccarbon (PhytOC) is an important carbon sink in wetland ecosystems and a mechanism for long-term carbon sequestration. In recent years, nitrogen pollution has become increasingly severe and poses a threat to the healthy development of coastal ecological environments and socio-economic development; therefore, studying the impact of nitrogen deposition on the sequestration potential of PhytOC in the soil of coastal wetlands is highly significant. In the present study, two indoor tidal simulation experiments were set up with and without the planting of vegetation. The sequestration capacity and factors that influence soil PhytOC in the Kandelia obovata soil system were compared and analyzed under five nitrogen concentrations. The analysis shows that with the introduction of Kandelia obovata, the occluded carbon content of the soil phytoliths was significantly increased by 31.45% compared with the non-plant group, and the PhytOC content of the soil increased by 7.94%. The exogenous nitrogen input reduced the PhytOC content of the soil, with a rate of decline exceeding 26%. The PhytOC of the soil phytoliths and the PhytOC content of the soil in the planting group increased with increasing nitrogen concentration, while that of the non-plant group decreased as the concentration of nitrogen increased. The non-plant group was more affected by the exogenous nitrogen concentration than the planting group, and the soil microbial biomass carbon and microbial biomass nitrogen were the main factors that influenced changes in the PhytOC. In conclusion, nitrogen input has a significant inhibitory effect on soil PhytOC sequestration potential in coastal wetlands. Planting Kandelia obovata helps to improve the stability of carbon in wetland soil.

1. Introduction

In recent years, the issue of global change has become increasingly severe; consequently, researchers have increasingly focused on identifying a long-term, stable carbon sink mechanism. Soil is the largest carbon pool in terrestrial ecosystems, emitting approximately 11-fold more carbon dioxide into the atmosphere each year than fossil fuel carbon emissions. The accumulation and changes of carbon pools in soil can directly affect the global carbon balance; this represents the main factor underlying global climate change [1]. Improving the carbon sequestration capacity of soil ecosystems is therefore a vital measure if we are to mitigate global warming.
Mangrove wetlands are carbon sinks with a high carbon storage capacity on land and represent an important source of greenhouse gas emissions in the atmosphere [2,3]. For many years, mangrove wetlands have been considered an effective way to purify pollutants in coastal waters, and large amounts of sewage and wastewater can be discharged without restriction, making mangrove wetlands the main buffer zone for the coastal deposition of nitrogen [4]. When mangrove plants are in a “nitrogen-starved” state, the introduction of external nutrients promotes their growth, at least within a certain range [5]. The promotion of plant growth is mainly achieved through the acquisition of nutrients in the soil to increase its biomass, thereby reducing the soil organic carbon storage. According to a recent report, when plant biomass increases, there is a reduction in the amount of carbon that the soil can actually store. This mutually contradictory relationship can reduce the capacity of soil for carbon sequestration [6].
Mangrove forests are situated at the land–sea interface area and are subject not only to nitrogen deposition but also to input from land sources [7], meaning the input of exogenous nitrogen is bound to increase [8]. Against the backdrop of dual carbon targets aimed at combatting global warming and increasing the carbon sequestration capacity of ecosystems, Southeast Asia, East Asia, and South America are increasing their efforts to establish mangrove forests [9,10,11]. However, due to the unique growth characteristics of mangrove forests, it is unclear whether the large-scale construction of mangrove forests will enhance the organic carbon storage capacity of coastal ecosystems or potentially deteriorate the carbon sequestration capacity of soil. Previous studies by our research group showed that methane emissions increased after the introduction of mangrove plants in coastal bare tidal wetlands; in addition, methane emissions also increased as the nitrogen concentration increased [12], demonstrating that an increase in the exogenous nitrogen concentration will accelerate the decomposition of soil organic matter [13]. This practice could also reduce the extent of stable organic carbon in the soil, ultimately affecting the soil’s capacity for carbon sequestration. This is a pressing scientific issue that requires urgent attention globally.
Thus far, many studies have investigated the organic carbon stability of soil at both the domestic and international levels. In particular, stable-state soil carbon, such as phytolith-occluded carbon (PhytOC), has become a popular research topic over recent years [14,15,16]. PhytOC is a form of organic matter that is generated during the formation of phytoliths, an inert form of organic carbon that can be stored in soil for an extended period without participating in the atmospheric carbon cycle [17]. PhytOC represents a highly stable carbon sequestration mechanism and an essential component of the carbon pool in soil. Relatively little is known about the specific role of PhytOC in wetland ecosystems [18]; most of the existing studies have focused on high-silicon plants (Poaceae) and soil in estuaries and lakes. Moreover, many of these studies have focused on wetlands dominated by herbaceous plants; only a few studies have focused on mangrove wetlands [16,19,20]. Studies on carbon fixation related to phytoliths in wetland ecosystems have mainly focused on the carbon fixation of phytoliths in plants, with particular emphasis on utilizing the carbon content of leaves or litter to estimate the carbon fixation potential of the entire ecosystem [21,22]; however, this method of estimation may not be accurate, and it cannot accurately estimate the carbon sequestration potential of the entire coastal wetland ecosystem, especially in mangrove ecosystems where the soil represents a vital carbon sink.
Currently, research on phytoliths has primarily centered on their current state; there is a notable lack of research focused on the specific factors that influence the state of phytoliths with respect to carbon. Consequently, we know very little about how PhytOC is formed [23,24]. In light of increasing global nitrogen deposition and considering the essential role of mangrove wetland ecosystems in global carbon storage stability and the specific growth characteristics of mangrove plants, it is crucial that we develop an accurate understanding of the relationship between PhytOC and nitrogen factors and to analyze the mechanisms that influence changes in PhytOC [7]. By performing a series of simulation studies, we aimed to answer three key scientific questions. First, would the introduction of mangrove plants in coastal bare wetlands enhance the ability of these wetland systems to cope with the effect of increased external nitrogen concentrations on soil carbon stability? Second, what is the specific impact of the introduction of mangrove plants on stable organic carbon, such as PhytOC, in the soil of coastal bare wetlands? Finally, what are the specific factors in soil and plants that influence the formation of PhytOC? The main objective of this study is to identify the impact of external nitrogen input on the characteristics of PhytOC in mangrove ecosystems and provide a significant basis for enhancing the accuracy of carbon sink estimation in coastal waters and formulating restoration.

2. Materials and Methods

2.1. Tidal Simulation Experiments

This part of our research involved two groups: a planting group and a non-plant group. The former represented the carbon sequestration potential of the entire system, including phytoliths, while the latter represented the carbon sequestration potential of phytoliths in the absence of plants. The difference between these two systems reflected the carbon sequestration potential of phytoliths after the introduction of Kandelia obovata.
The experiment was conducted in the tidal simulation laboratory of the Fujian Academy of Forestry Sciences. The tidal simulation system was composed of an automatic tidal simulation trough device and control system. The automatic tidal simulation trough device is divided into an upper trough and a lower trough: the upper trough is simulated grass (length × width × height = 1.0 m × 1.0 m × 1.0 m) and the lower trough is a storage tank. The soil medium in the simulation tank was taken from the estuary wetland of Quanzhou Bay, with a salinity of 12 ppt. The system was set to semi-diurnal, thus reflecting the tidal form of the Kandelia obovata forest in the estuary wetland. The system featured one semi-diurnal cycle every 12 h, with two semi-diurnal floods per day. The flooding method was submergence, with a 4 h flooding time. During flooding, the water surface reached 70 cm above the surface of the culture soil.

2.2. Culture Medium, Kandelia Obovata Seedling Cultivation, and Nitrogen Fertilizer Treatment

The experimental culture medium was taken from the wetland of the estuary of Quanzhou Bay, and a 0–30 cm soil layer was used. Before the cultivation experiment began, the system was operated for one month. The properties of the simulated soil are shown in Table 1.
Kandelia obovata seedlings were grown in sandy soil in April 2019 and were transplanted into the simulation tank after the growth of two new leaves. There were 48 seedlings in each simulation tank, and the sediment in each tank was 20 cm high. The formal simulation experiment began after pre-cultivation for approximately seven days to allow the plants to adapt to the environment.
Two groups and five nitrogen input levels were set up for this experiment, with three replicates for each treatment. Nitrogen was added at 2.5-fold, 5-fold, 10-fold, and 15-fold higher than the mean total nitrogen deposition of almost 2 gN·m−2·a−1 in Xiamen, a location that is close to the study area [25]. Five nitrogen concentrations were used for each experiment (N0 = 0, N1 = 5, N2 = 10, N3 = 20, and N4 = 30 gN·m−2·a−1) and a NH4NO3 solution was used as the nitrogen source [26]. During the cultivation period, nitrogen was applied once a month for a total of 6 times, which was input in the form of a NH4NO3 aqueous solution. Each treatment level had 3 replicates, and one simulation tank was one replicate. A sketch of the experimental setup is shown in Figure 1.

2.3. Extraction and Calculation of Phytoliths

After six months of cultivation, we carefully collected leaves from the Kandelia obovata; these were washed thoroughly and then dried. Soil samples were collected according to the three-point method. The roots were removed, dried in a ventilated place, and then ground through a 100-mesh sieve for subsequent analysis.
The extraction of phytoliths was carried out using a microwave digestion method but with some modifications to improve the extraction efficiency [27,28]. The effective silicon was extracted from the soil samples using a citric acid buffer solution, and specific concentrations were determined by the molybdenum blue colorimetry method [29]. The content of the PhytOC was determined using an alkali-soluble spectrophotometric method [30]. The total carbon and total nitrogen contents of the soil and plants were determined by an elemental analyzer. The soil microbial biomass C was measured by a total organic carbon analyzer after chloroform fumigation–K2SO4 solution extraction, and the microbial biomass N was measured by an automatic intermittent analyzer after chloroform fumigation–K2SO4 solution extraction. The urease was determined by indophenol colorimetry, and the sucrase was determined by colorimetry [31]; the acid phosphatase was determined by kit method, the soil phosphorus content was determined by a sodium hydroxide melting–molybdenum antimony sulfate anti-colorimetric method, the sulfate content was determined by barium sulfate turbidimetry, and the pH was determined by the potentiometric method [32].
The basic indicators of the phytoliths were calculated using the following equations, in accordance with previous literature [30,33,34]. The following equations were used for both the leaf and soil samples.
Phytoliths content (g·kg−1) = phytolith weight (g)/dry biomass of leaf (soil) (kg)
Occluded carbon content of phytoliths (g·kg−1) = Organic carbon content in phytolith (g)/phytolith weight (kg)
PhytOC content of leaf (soil) (g·kg−1) = Organic carbon content in phytolith (g)/dry biomass of leaf (soil) (kg)
The occluded carbon content of the phytoliths is the organic carbon content in one kilogram of phytoliths, and the PhytOC content in the leaf and soil is the organic carbon content in one kilogram of leaf or soil.
The occluded carbon content of the phytoliths indicates the carbon sequestration potential of the phytoliths themselves. The PhytOC content in the leaf and soil indicates the long-term carbon sequestration capacity of the Kandelia obovata and soil and characterizes the carbon sequestration efficiency of the phytoliths [35].

2.4. Statistical Analysis

The Kolmogorov–Smirnov test was used for testing the normality of the data. p > 0.05 indicated that the variable follows a normal distribution. The statistical analysis involved analysis of variance (ANOVA) and Duncan’s method. A correlation analysis between the key variables was performed using Pearson’s method. p < 0.05 signified statistical significance. The statistical analysis and its charts were performed using origin2018 software. The correlation coefficient diagram was made by R3.5.2.

3. Results

3.1. Effect of Nitrogen Input on PhytOC Characteristics in Kandelia Obovata

Without nitrogen fertilization, the phytolith content in Kandelia obovata was 3.57 g·kg−1, the occluded carbon content of the phytoliths was 408.82 g·kg−1, and the PhytOC content in Kandelia obovata was 1.46 g·kg−1. With nitrogen fertilization, there was a significant change in the phytolith content of Kandelia obovata. As shown in Figure 1, nitrogen fertilization significantly changed the phytolith content of Kandelia obovata, ranging from 3.05 to 5.10 g·kg−1. The content increased significantly under the N1 treatment, remained largely unchanged under the N2 and N3 treatments, and was significantly higher under the N4 treatment when compared to other treatments (p < 0.05).
There was no significant change in the occluded carbon content of the phytoliths in Kandelia obovata with nitrogen fertilization, and there were no significant differences between the different nitrogen treatment levels. As shown in Figure 2, the occluded carbon content of the phytoliths in the Kandelia obovata leaves generally decreased as the nitrogen concentration increased. In addition, the occluded carbon content of the phytoliths under the N1 concentration was higher than that of other treatments.
With nitrogen fertilization, there was a significant change in the PhytOC content of the leaf (p < 0.05). As shown in Figure 2, the PhytOC content of leaf initially increased, then decreased, and then increased again as the nitrogen concentration increased. The carbon content was highest under the N1 treatment and was significantly higher than all the other treatments (p < 0.05). The carbon content also increased with the increasing nitrogen concentration in the N2 to N4 treatment groups.

3.2. Effects of Mangroves and Exogenous Nitrogen Input on the Characteristics of PhytOC in Coastal Wetland Soil

3.2.1. Effects of Mangroves and Exogenous Nitrogen Input on Phytoliths Content in Coastal Wetland Soil

Figure 3A demonstrates that the introduction of Kandelia obovata and exogenous nitrogen input exerted significant influence on the content of phytoliths in coastal wetland soil (p < 0.05); however, their interaction was not significant (p > 0.05). The phytolith content in the Kandelia obovata group was lower (p > 0.05) than that in the no-plant group under various concentration treatments. Overall, the soil phytolith content in the planting group decreased by 18.96% when compared to the no-plant group. Following the nitrogen input, the phytolith content in the Kandelia obovata group decreased by 5.69% but increased by 2.66% in the no-plant group. The phytolith content in the Kandelia obovata planting group increased as the nitrogen concentration increased.

3.2.2. Effects of Mangroves and Exogenous Nitrogen Input on Occluded Carbon Content of Phytoliths in Coastal Wetland Soil

Figure 3B shows that the introduction of Kandelia obovata and an exogenous nitrogen input significantly influenced the occluded carbon content of phytoliths in coastal wetland soil (p < 0.05), although the interaction between these factors was not significant (p > 0.05). Except for the N1 treatment group, the occluded carbon content of the phytoliths of the Kandelia obovata planting group was higher than that in the no-plant group under other concentration treatments (p < 0.05). Overall, the occluded carbon content in the phytoliths of the planting group increased by 31.45% when compared to the no-plant group. The application of nitrogen increased the occluded carbon content of the phytoliths in the Kandelia obovata group, although there was a slight reduction in this trend for the N4 concentration. In contrast, the no-plant group showed a decreasing trend in the occluded carbon content with the increasing nitrogen concentration. Following the nitrogen input, the occluded carbon content in the soil phytoliths decreased by more than 26%, with the Kandelia obovata group exhibiting a lower rate of reduction than the no-plant group (Table 2). The rate of change for occluded carbon content in the soil phytoliths of the Kandelia obovata increased with the increasing nitrogen concentration when compared to that of the no-plant group (Table 3). In the N1 treatment group, the occluded carbon content of the phytoliths in the planting group was lower than that in the no-plant group; this trend was reversed in the other concentration treatments.

3.2.3. Effects of Mangroves and Exogenous Nitrogen Input on PhytOC Content of Soil in Coastal Wetland Soil

Figure 3C shows that the introduction of Kandelia obovata had no significant effect on the PhytOC content of soil in coastal wetland soil (p > 0.05), whereas an exogenous nitrogen input did have a significant impact (p < 0.05). In addition, there was a significant interaction between these two factors (p < 0.05). With the exception of the N1 and N2 treatment groups, the PhytOC content of the soil in the planting group was significantly higher than that in the non-plant group under other N concentrations (p < 0.05), with an average increase of 7.94% in PhytOC content of the soil when compared to the non-plant group. The application of nitrogen increased the PhytOC content of the soil in the planting group with increasing nitrogen concentrations, although a slight reduction was observed in response to the N4 concentration. In contrast, the no-plant group exhibited a decreasing trend in the PhytOC content of the soil with increasing nitrogen concentration. Following the application of nitrogen, the PhytOC content of the soil decreased by more than 28%, with the planting group showing a rate of reduction that was similar to that of the non-plant group (Table 2). The rate of change rate in the PhytOC content of the soil in the planting group increased with the increasing nitrogen concentration when compared to that of the non-plant group (Table 3). In the N1 treatment group, the PhytOC content of the soil in the planting group decreased by 33.63% when compared to the non-plant group, showing a slight reduction in the N2 treatment group and a significant increase with the other concentrations.

3.3. Correlation Analysis between Soil PhytOC and Other Factors

3.3.1. Correlation Analysis between Mangrove Plants, Nitrogen Concentration, and Soil PhytOC in Coastal Wetlands

We observed a significant correlation between the occluded carbon content of soil phytoliths with mangrove plants and the nitrogen concentration (p < 0.01; Table 4), and the correlation coefficient is greater than 0.5. The PhytOC content of the soil was significantly correlated with the nitrogen concentration (p < 0.01) and the phytolith content was significantly correlated with the mangrove plants (p < 0.01). Moreover, the effect of the nitrogen concentration on the occluded carbon content of the phytoliths and PhytOC content of the soil in coastal wetlands soil was greater than the effect of the mangrove plants (0.642 > 0.533, 0.578 > 0.162; respectively).

3.3.2. Correlation Analysis between Soil PhytOC, the Soil Environment, and Plant Factors in the Planting Group

In a previous study, we analyzed carbon–nitrogen stoichiometric characteristics of the plants–soil–microbial biomass system in response to nitrogen addition [13]. In the present study, we included a range of other indicators to analyze the correlation characteristics between soil PhytOC, the soil environment, and plant factors in the planting group. Figure 4 shows that the nitrogen concentration and microbial biomass carbon were significantly correlated with the occluded carbon in the phytoliths (p < 0.05) with the highest correlation coefficient (0.602 and 0.573). The second most significant factor was the microbial biomass of nitrogen. The PhytOC content of the soil was significantly correlated with the microbial biomass of carbon (p < 0.01), with a maximum correlation coefficient of 0.724. The soil SiO2 content was the next most significant factor and showed a significant correlation with the PhytOC content (p < 0.05). The correlation coefficient of the total carbon content in the soil was 0.512; this was comparable to that of the soil SiO2 content. Compared to the occluded carbon content in the phytoliths, the soil carbon environment had a greater impact on the PhytOC content of the soil than nitrogen; however, the opposite was true for occluded carbon in the phytoliths, where the impact of the soil nitrogen environment was greater. The microbial biomass of carbon in the soil was significantly correlated with the PhytOC content of the soil (−0.573; p < 0.05) and occluded carbon content of the phytoliths (−0.724; p < 0.01); these correlations were greater than other factors, making microbial biomass of carbon the main influencing factor.

3.3.3. Correlation Analysis between Soil PhytOC and Other Indicators in the Non-Plant Group

Our analysis shows that in the non-plant group, the nitrogen concentration was significantly correlated with both the occluded carbon content in the phytoliths and the phytolith content (p < 0.01; Figure 5). Moreover, the microbial biomass of nitrogen was significantly correlated with both the phytolith content (p < 0.01) and the occluded carbon content in the phytoliths (p < 0.01). Nitrogen was identified as the primary factor affecting the characteristics of PhytOC in the non-plant group; this was followed by acid phosphatase activity. Furthermore, the correlation coefficient between the exogenous nitrogen concentration and PhytOC in the non-plant group was >0.87, while the maximum correlation coefficient in the planting group was only 0.60. These data indicate that the mangrove ecosystem was less affected by exogenous nitrogen and that planting mangrove plants in coastal wetlands can enhance the ability of coastal ecosystems to cope with global changes.

4. Discussions

4.1. The PhytOC Sequestration Capability of Kandelia obovata and Soil Phytoliths

For the first time, the PhytOC content of soil was determined to be 1.46 g·kg−1; this indicates a significant ability to sequester PhytOC. These data suggest that the PhytOC sequestered by Kandelia obovata during its growth process could reduce global CO2 levels in a very effective manner. Previous studies have reported differences in the content of phytoliths, the occluded carbon content of phytoliths, and the PhytOC content of soil in various plants in a range of ecosystems, including wetlands, forests, and grasslands [19,20,23,33,36,37]. Previous research has reported that the wetland plants with the highest PhytOC content are Cynodon dactylon, Arthraxon hispidus, and Phragmites australis, with values of 64.2, 39.7, and 23.3 mg·g−1, respectively [38]. We demonstrated that the leaf phytolith content of Kandelia obovata is lower than that of Cunninghamia lanceolata and Cyclobalanopsis glauca. The mean PhytOC content of the Kandelia obovata soil sample was determined to be 2.16 g kg−1; this is significantly higher than that of woody plants reported in previous studies, and only lower than that of bamboo forest soil [39,40]. It might be because Kandelia obovata is a “nitrogen-hungry” plant, which will relatively promote the accumulation of steady-state carbon, resulting in a higher sample phytolith carbon content of the soil than other woody plants. These data confirm that mangroves have a high capability for high carbon sequestration. The soil PhytOC content of the planting group was significantly higher than that of the non-plant group, thus indicating that planting Kandelia obovata can effectively enhance the carbon stability and PhytOC sequestration potential of wetland soil.

4.2. Variation of Soil Plant PhytOC Sequestration Capability in Coastal Wetlands with Regards to Nitrogen Deposition

The introduction of mangroves did not have a significant impact on the soil PhytOC content; however, the interaction between the mangrove introduction and exogenous nitrogen input led to a significant change in the soil PhytOC content. This indicates that under the backdrop of increasing global change relating to exogenous nitrogen inputs, large-scale mangrove cultivation in coastal wetlands will have a notable impact on the carbon stability of the soil system; thus, the impact of the nitrogen input must not be ignored [41]. Following the application of nitrogen, the soil phytolith carbon content of both the planting group and the non-plant group decreased, possibly due to the decrease of C/N in the soil system after the exogenous nitrogen input, which aggravates the decomposition of organic carbon [13], thus inhibiting the phytolith carbon sequestration capability of wetland soil systems and reducing the carbon stability of the soil system. The rate of the soil PhytOC content reduction in the planting group was lower than that of the non-plant group. The soil PhytOC content in the planting group increased with increasing nitrogen concentration, while the non-plant group showed the opposite trend. This could be attributed to the robust adaptation of Kandelia obovata to external nitrogen. Plants preferentially absorb and utilize exogenous nitrogen for growth accumulation. Within a specific concentration range, the decrease in the organic carbon content of the soil is relatively lower in comparison to the non-plant planting group, which aids in the buildup of stable carbon in the soil. Conversely, in the non-plant group, an increase in the exogenous nitrogen application leads to a higher organic carbon decomposition requirement for the system. As a result, the opposite trend is observed. These data suggest that the introduction of mangrove plants can increase the ability of coastal wetland systems to cope with nitrogen deposition. However, at low concentrations, planting Kandelia obovata in bare wetlands may lead to a reduction in soil carbon stability and the PhytOC sequestration capability. As the nitrogen concentration increases, the introduction of Kandelia obovata could significantly improve the soil carbon stability of coastal wetlands. To a certain extent, this practice could effectively deal with the adverse effects of increasing nitrogen concentration on soil carbon stability; furthermore, this coping ability increases as the nitrogen concentration increases.
The effect of nitrogen application on the PhytOC sequestration ability observed in the present study differed from that reported in previous studies. In a previous study, researchers found that a certain level of nitrogen fertilization greatly enhanced the carbon sequestration of phytoliths on degraded grasslands in northern China, while an excess of nitrogen fertilizer inhibited PhytOC sequestration [35]. In another study, researchers found that nitrogen fertilization increased the PhytOC sink in the grasslands of northern China [42]; this may be related to differences in plant species, their nutritional requirements, nitrogen concentration, and the specific form of input [43,44]. If we consider mangrove plants under “nitrogen-starved” conditions, the application of an external nutrient source will promote growth, at least within a certain range.

4.3. Correlations between a Range of Indices in Response to Nitrogen Deposition

Our study reveals that soil microbial biomass carbon and microbial biomass nitrogen are the primary factors that affect soil PhytOC content. Exogenous nitrogen had a greater impact on the non-plant group compared to the planting group. The microbial absorption and utilization of one portion of nitrogen requires the consumption of 25 portions of organic carbon. After the application of exogenous nitrogen, the impact on the soil and microorganisms is greater than that of the mangrove plants. It preferentially stimulates soil microbial activity, aggravates soil organic carbon decomposition [13], and inhibits the capability of phytolith carbon sequestration. Plants have a resource utilization strategy to adapt to their environment, which involves preferentially mitigating limiting conditions. In the case of nitrogen-deficient mangrove plants, the application of external nitrogen leads to its preferential utilization for plant growth. This results in less consumption of organic carbon by soil microorganisms for nitrogen absorption and utilization compared to the non-planted group. Consequently, it promotes the storage of phytolith carbon, enhances system stability, and effectively addresses increased nitrogen deposition.
In the present study, we identified a significant positive correlation between the soil PhytOC content and phytolith content, as well as the occluded carbon content of the phytoliths. These data suggest that management measures that increase the phytolith content and occluded carbon content in plants could effectively increase the retention capacity of PhytOC. However, in a previous study, Song et al. (2015) found no significant correlation between phytoliths and the occluded carbon content in Phragmites australis [45]. In another study, Sun et al. (2020) found no correlation between the phytolith content and the occluded carbon content in Triticum aestivum, Saccharum officinarum, and Setaria viridis, although a significant correlation was detected for the PhytOC content [46]. A previous study by Ying et al. (2015) involving seven species of subtropical trees showed that the occluded carbon content of the phytoliths was significantly correlated with both the phytolith content and the soil PhytOC content [47]. A previous study reported that phytolith content in soil and litter of different vegetation types was significantly correlated with the PhytOC content, and the soil phytolith content was significantly correlated with the soil SOC content [30]. The differences between our current findings and those of previous studies could be explained by differences in the plant species, phytoliths in different plant organs, and differences in the PhytOC content [48,49,50].
In the present study, we found no significant correlations between the soil PhytOC content, the phytolith content, and the occluded carbon content of the phytoliths. In a previous study, researchers found that there is a positive correlation between the soil PhytOC content and the occluded carbon content of soil phytoliths, as well as between the soil PhytOC content and organic carbon content [15,51]. The results of the present study are different from those reported by previous studies; this may be due to different ground vegetation coverage, the input of plant residues, the growth environment, and the stability of the phytoliths [19,52,53].
Under nitrogen treatment, the correlations between the various content indicators of phytoliths in Kandelia obovata changed notably and the correlations were weakened. We identified a significant positive correlation between the sequestration capacity of plant PhytOC and phytolith content, thus indicating that management measures to maximize the phytolith content could effectively deal with the adverse effects of nitrogen deposition and increase the retention of PhytOC in plants. We found that the correlations between different content indicators of soil phytoliths could show variation. The organic carbon content of soil phytoliths planted with Kandelia obovata was significantly positively correlated with the content of phytoliths. In addition, there was a significant positive correlation between the soil PhytOC content and the occluded carbon content of the phytoliths in the soil that was not planted with Kandelia obovata. In addition, the occluded carbon content of the phytoliths was significantly and positively correlated with the content of the phytoliths, thus indicating that management measures that maximize the content of soil phytoliths could effectively counteract the adverse effects of nitrogen deposition and increase the carbon storage capacity of phytoliths and the fixation of soil PhytOC. The observed changes in the correlations between the indicators of PhytOC under different nitrogen treatments may be due to a range of key factors, including plant species, growth location, spatial plant expansion, plant nutrient requirements, and human activities, all of which can significantly affect the accumulation of phytoliths. These changes could, in turn, influence the relationship between the PhytOC content and a range of content indicators [44,50,54].
Whether or not nitrogen deposition occurs, we found no evidence of a significant correlation between soil silicon, SiO2, and phytoliths. In a previous study, Sun et al. (2019) found that a silicon fertilizer application helped to improve the phytolith content of the rice plant [55]. Liu et al. (2020) supposed plant silicon storage and plant silicon content were positively correlated with bioavailable silicon in soils [17]. Chen et al. (2021) reported that the ability of plants to accumulate silicon significantly affects the content of phytoliths, which, in turn, affects the organic carbon content of the phytoliths [54]. The inconsistencies between previous studies may be due to differences in a range of factors, including the parent material, climate, plant species, and silicon demand in different ecosystems [55,56,57]. Previously, researchers estimated the content of phytoliths by considering the silicon content of both plants and soil [23,58]; however, our present study implies that such methodology may be associated with inherent limitations. Different types of soil and plant species can alter the relationships between effective soil silicon and phytoliths. Therefore, the accurate estimation of the content of phytoliths requires a comprehensive consideration of both the soil properties and plant species [52,56].
Currently, there is a need to strengthen research on the sequestration capacity of wetland PhytOC in several aspects. For example, the correlations between soil PhytOC and leaf PhytOC detected in the present study were small, possibly due to our focus on one-year-old seedlings, and therefore, a lower amount of litter in the simulated system. Future research should select natural and artificial mangroves of different ages and restoration years in the field to conduct soil PhytOC characterization research; this will help to clarify the main sources and influencing factors of PhytOC within a mangrove ecosystem.
The present study only focused on phytoliths in the leaves; however, plants have different numbers of phytoliths and PhytOC content in different organs [48]. Future research should investigate the specific characteristics of phytoliths in different organs and mangrove plants and plants of different ages to fully determine the distribution of phytoliths in different organs and improve our estimates of the PhytOC sink in wetland ecosystems. It is difficult to differentiate the impact of individual environmental factors on the formation of phytoliths due to the complexity and diversity of factors that can influence phytolith formation and the differences across plant species [25,28,40]. Therefore, studying the relationship between PhytOC formation rate, flux, and wetland environmental factors is necessary if we are to investigate effective management measures to increase the potential for PhytOC sequestration in wetlands [21,38].
By investigating the natural processes and maintenance mechanisms of carbon accumulation in wetland ecosystems, it will be possible to establish a model to evaluate and quantify the potential for PhytOC sequestration, along with the rate and stability of PhytOC sequestration. This will provide a theoretical basis for predicting carbon sinks in different ecosystems.

5. Conclusions

Kandelia obovata has a strong capacity to sequester carbon in its phytoliths; this ability can be further enhanced by increasing the amount of phytoliths and the organic carbon content. Planting Kandelia obovata can effectively improve the soil’s ability to sequester carbon in phytoliths. Nitrogen deposition at the N1 level enhanced the ability of Kandelia obovata to sequester carbon in phytoliths; however, above this level, there was an inhibition of phytolith carbon sequestration. Increasing the phytolith content could reduce the adverse effects of nitrogen deposition. Moreover, nitrogen deposition can inhibit the potential of PhytOC sequestration in soil, but planting Kandelia obovata, increasing the amount of phytoliths, and increasing the occluded carbon content in phytoliths could effectively counteract the negative effects of nitrogen deposition. We found that soil microbial biomass carbon and microbial biomass nitrogen are the main influencing factors of soil PhytOC, and the effect of exogenous nitrogen on the non-plant group was greater than that of planting group. These findings can serve as a reference for long-term research on stable PhytOC sinks and carbon cycling in wetland ecosystems. Moreover, our findings have important implications for evaluating long-term carbon sequestration in wetlands.

Author Contributions

Conceptualization, H.Y. and F.T.; Methodology, H.Y. and L.Z.; Software, W.Y. and Y.C.; Validation, F.T. and H.Y.; Formal analysis, F.W. and J.L. (Jiangrong Lv); Investigation, W.Y. and J.L. (Jie Lin); Resources, T.L. and F.T.; Data curation, H.Y. and L.Z.; Writing—original draft, H.Y.; Writing—review & editing, H.Y. and L.Z.; Visualization, H.Y. and Y.C.; Supervision, H.Y.; Project administration, F.T. and H.Y.; Funding acquisition, H.Y. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Forestry Science and Technology Project of Fujian Province (2022FKJ04) and Fujian Provincial Public Welfare Scientific Institutions Project (2019R1009-3).

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. The sketch of experimental setup.
Figure 1. The sketch of experimental setup.
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Figure 2. Leaf phytolith content, occluded carbon content of leaf phytoliths, and PhytOC content in Kandelia obovata leaf under different nitrogen concentrations. Different letters indicate significant differences (p < 0.05).
Figure 2. Leaf phytolith content, occluded carbon content of leaf phytoliths, and PhytOC content in Kandelia obovata leaf under different nitrogen concentrations. Different letters indicate significant differences (p < 0.05).
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Figure 3. The characteristics of soil PhytOC in two simulated systems with different nitrogen inputs. Phytoliths content of soil (A), occluded carbon content of soil phytoliths (B), and PhytOC content of soil (C) in two simulated systems with different nitrogen concentrations. Different letters indicate significant differences (p < 0.05).
Figure 3. The characteristics of soil PhytOC in two simulated systems with different nitrogen inputs. Phytoliths content of soil (A), occluded carbon content of soil phytoliths (B), and PhytOC content of soil (C) in two simulated systems with different nitrogen concentrations. Different letters indicate significant differences (p < 0.05).
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Figure 4. Correlation coefficients of soil PhytOC with both soil and plant factors in the Kandelia obovata group. S-ACP: soil acid phosphatase activity; TP: total phosphorus content; SO4: sulfate content; TC: soil total carbon content; TN: soil total nitrogen content; C.N: soil carbon/nitrogen; MBN: microbial biomass nitrogen; MBC: microbial biomass carbon; UA: urease activity; SA: sucrase activity; LC: leaf carbon content; LN: leaf nitrogen content; NC: nitrogen concentration; FRW: fresh root weight; RC: root carbon content; RN: root nitrogen content; LPC: leaf phytolith content; LCCP: occluded carbon content of leaf phytoliths; LPCS: PhytOC content of leaf; SCCP: occluded carbon content of soil phytoliths; SPCS: PhytOC content of soil; SPC: soil phytolith content. * indicates a significant difference at the 0.05 level, ** indicates a significant difference at the 0.01 level.
Figure 4. Correlation coefficients of soil PhytOC with both soil and plant factors in the Kandelia obovata group. S-ACP: soil acid phosphatase activity; TP: total phosphorus content; SO4: sulfate content; TC: soil total carbon content; TN: soil total nitrogen content; C.N: soil carbon/nitrogen; MBN: microbial biomass nitrogen; MBC: microbial biomass carbon; UA: urease activity; SA: sucrase activity; LC: leaf carbon content; LN: leaf nitrogen content; NC: nitrogen concentration; FRW: fresh root weight; RC: root carbon content; RN: root nitrogen content; LPC: leaf phytolith content; LCCP: occluded carbon content of leaf phytoliths; LPCS: PhytOC content of leaf; SCCP: occluded carbon content of soil phytoliths; SPCS: PhytOC content of soil; SPC: soil phytolith content. * indicates a significant difference at the 0.05 level, ** indicates a significant difference at the 0.01 level.
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Figure 5. Correlation coefficients between soil PhytOC and other indices in the no-plant group. * indicates a significant difference at the 0.05 level, ** indicates a significant difference at the 0.01 level.
Figure 5. Correlation coefficients between soil PhytOC and other indices in the no-plant group. * indicates a significant difference at the 0.05 level, ** indicates a significant difference at the 0.01 level.
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Table 1. Physical and chemical properties of soil in the simulated test soil.
Table 1. Physical and chemical properties of soil in the simulated test soil.
Volumetric Weight (g·cm−3)TC Content (%)TN Content (%)NH4+–N (mg·kg−1)NO3–N (mg·kg−1)
0.63 ± 0.031.89 ± 0.130.13 ± 0.00253.24 ± 0.342.71 ± 0.12
Table 2. Changes of soil PhytOC characteristics following nitrogen input in different systems (%).
Table 2. Changes of soil PhytOC characteristics following nitrogen input in different systems (%).
IndexPlanting GroupNon-Plant Group
Phytolith content−5.692.66
Occluded carbon content of phytoliths−26.02−29.14
PhytOC content of soil−29.79−28.54
Table 3. The rate of change of soil PhytOC in the planting group under different nitrogen concentrations compared to the non-planting group (%).
Table 3. The rate of change of soil PhytOC in the planting group under different nitrogen concentrations compared to the non-planting group (%).
Nitrogen ConcentrationOccluded Carbon Content in PhytolithsPhytOC Content of Soil
N1−11.93−33.63
N244.08−0.67
N352.0038.40
N488.2656.78
Table 4. Correlation coefficients between mangrove plants, nitrogen concentration, and PhytOC in coastal wetland soil.
Table 4. Correlation coefficients between mangrove plants, nitrogen concentration, and PhytOC in coastal wetland soil.
IndexOccluded Carbon Content of PhytolithsPhytOC Content of SoilPhytoliths Content
Mangrove plant0.533 **0.162−0.718 **
Nitrogen concentration−0.642 **−0.578 **0.270
** indicates a significant difference at the 0.01 level.
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You, H.; Zheng, L.; You, W.; Tan, F.; Wang, F.; Cao, Y.; Le, T.; Lin, J.; Lv, J. The Influence of Exogenous Nitrogen Input on the Characteristics of Phytolith-Occluded Carbon in the Kandelia obovata Soil System. Forests 2023, 14, 2202. https://doi.org/10.3390/f14112202

AMA Style

You H, Zheng L, You W, Tan F, Wang F, Cao Y, Le T, Lin J, Lv J. The Influence of Exogenous Nitrogen Input on the Characteristics of Phytolith-Occluded Carbon in the Kandelia obovata Soil System. Forests. 2023; 14(11):2202. https://doi.org/10.3390/f14112202

Chicago/Turabian Style

You, Huiming, Lidi Zheng, Weibin You, Fanglin Tan, Fangyi Wang, Yan Cao, Tongchao Le, Jie Lin, and Jiangrong Lv. 2023. "The Influence of Exogenous Nitrogen Input on the Characteristics of Phytolith-Occluded Carbon in the Kandelia obovata Soil System" Forests 14, no. 11: 2202. https://doi.org/10.3390/f14112202

APA Style

You, H., Zheng, L., You, W., Tan, F., Wang, F., Cao, Y., Le, T., Lin, J., & Lv, J. (2023). The Influence of Exogenous Nitrogen Input on the Characteristics of Phytolith-Occluded Carbon in the Kandelia obovata Soil System. Forests, 14(11), 2202. https://doi.org/10.3390/f14112202

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