Resource utilization conditions as biochar of an invasive plant Spartina alterniflora in coastal wetlands of China

Converting feedstocks of invasive plants into biochar is a new and cost‐effective measure for their control, and benefits for the sustainable development of native ecosystems. Spartina alterniflora, an invasive plant widely distributed in coastal wetlands of China, was used to produce biochar. We aimed to analyze how S. alterniflora biochar properties changed with desalination of feedstocks, pyrolysis temperature, and residence time. Results showed that desalting feedstocks increased biochar pH, stability, porosity, and surface area, but diminished biochar yield and polarity. Pyrolysis temperature positively affected biochar pH, surface area, and pore volume, while it had negative effects on biochar yield, oxygen and hydrogen contents, hydrogen/carbon and oxygen/carbon ratios, pore size, and function groups. However, residence time of pyrolysis had slight effects on biochar properties. The results are valuable for optimizing pyrolysis temperature and pretreatment measure of feedstocks, to tune S. alterniflora biochar properties for specific environmental usage.


| INTRODUCTION
Invasive plants have caused serious damages to native biodiversity, local habitats, and even public health and economy by outcompeting with native plants and rapidly expanding (Liao, Gao, & Fang, 2013;Pimentel, 2002). Various clearing measures, such as clipping, pulling, digging, and applying herbicides, are widely used to control invasive plants (Shimeta, Saint, Verspaandonk, Nugegoda, & Howe, 2016;Tang et al., 2009;Waryszak, Lenz, Leishman, & Downey, 2018). Although some successes have been achieved, these measures always bring high cost, and chemical measures may impose damages to native species (Liao et al., 2013;Simmons et al., 2007). Furthermore, physical clearing measures leave amounts of plant wastes, and lead to serious environmental pollution (de Lange, Stafford, Forsyth, & le Maitre, 2012). Utilizing these wastes as a kind of resource presents a promising and sustainable strategy for management of invasive plants (Liao et al., 2013).
As an environmentally benign material, biochar attracts increasing attentions for the resource utilization of invasive plant wastes by transforming them into valued materials (Liao et al., 2013). Biochar is produced by pyrolyzing organic matters at high temperature with limited or no oxygen supply (Ahmad et al., 2014;Moore et al., 2018), and has promising use in carbon storage, environmental remediation, soil amelioration, and agricultural productivity improvement Xu et al., 2017;Zhang et al., 2017). These environmental applications of biochar | 637 XIA et Al. are attributed to its high organic C contents, large specific surface area and porosity, and diverse functional groups .
S. alterniflora, a rhizomatous plant native to Northern American coast, was introduced to China in 1979 for protecting beach and promoting siltation (Lu & Zhang, 2013;Zheng et al., 2016). It distributes widely in Chinese coastal wetlands nowadays, and difficult to clear because of its strong adaptation and propagation ability Wang et al., 2008). The annual biomass of S. alterniflora in China is estimated to be higher than 2 × 10 6 t (Lu & Zhang, 2013), presenting a promising and sustainable feedstock for biochar. However, S. alterniflora is a salt marsh plant with high salt contents (Qin et al., 2016). The produced biochar may present risks during its utilization in environmental remediation, thus desalination treatment for diminishing salt contents in feedstocks is needed to reduce potential environmental risks. Although biochar properties vary with feedstock types (Ahmad et al., 2014;Li, Harris, Anandhi, & Chen, 2019;Ronsse, van Hecke, Dickinson, & Prins, 2013), whether desalination treatment of the same feedstock affects biochar properties is not well known.
Biochar properties are affected not only by feedstock types but also by pyrolysis conditions such as pyrolysis temperature and residence time (Zhao, Ta, & Wang, 2017;Zhou et al., 2018). Characterizing S. alterniflora biochar that pyrolyzed under different conditions is critical to produce biochar with specific properties for environmental usage. Efforts have been taken to produce S. alterniflora biochar at 700°C and 400°C for 2 hr, and the biochar was used to remove heavy metal (e.g., copper and lead) from water Li et al., 2013). However, less data can be acquired from previous studies to fully understand S. alterniflora biochar properties.
In the study, untreated and desalted S. alterniflora feedstocks were pyrolyzed under different temperature and residence time to produce biochar. Biochar physical (e.g., yield), chemical (e.g., pH and elemental composition), and surface properties (e.g., surface morphology, surface area, porosity, and functional groups) were examined. We aimed to (a) reveal whether and how desalination treatment of feedstocks affected biochar properties, (b) analyze how S. alterniflora biochar properties changed with pyrolysis temperature and residence time. These results help identify the optimal pyrolysis conditions to get specific biochar during resource utilization of S. alterniflora, and provide data for environmental application of biochar.

| Feedstock preparation
S. alterniflora was collected from the Yellow River estuary in Dongying city, China. The collected S. alterniflora feedstocks were washed using deionized water to remove surface contaminations. Half of feedstock materials were soaked in deionized water to get the desalted feedstocks. Multiple experiments determined that desalting feedstocks for 3 hr in deionized water with the feedstock-water ratio of 1 g:25 ml can reduce salt contents in feedstocks to a normal level below 1.84% ( Figure S1). The desalted and untreated feedstocks were chopped into short segments (<5 mm) and air-dried for 7 days. The feedstock segments were dried in an oven for 24 hr under 105°C, and sealed in plastic bags.

| Pyrolysis method for biochar
To avoid air flowing into ceramic crucibles and create an oxygen-limited atmosphere, the oven-dried feedstocks were tightly packed into ceramic crucibles, which were then covered by two layers of aluminum foil. The crucibles filled with feedstocks were pyrolyzed under high temperature in muffle furnace (SX-G16103) with limited oxygen supply. After the temperature in muffle furnace decreased to 25°C, the crucibles were taken out. The produced biochar was sealed in plastic bags and marked feedstock type (desalted or untreated), pyrolysis temperature, and residence time.
Our previous thermogravimetric analysis showed that S. alterniflora feedstocks were not thermally stable due to the sharp mass loss as increasing temperature up to 350°C ( Figure S2). While the feedstocks presented stable mass loss at temperature above 350°C, and followed by slight mass loss above 650°C. Thus, to reveal the dynamics of biochar properties with pyrolysis temperature, feedstocks were pyrolyzed at temperature of 350°C-650°C in 50°C intervals for 2 hr, which is a widely used residence time. Biochar produced from S. alterniflora at 450°C had higher adsorption capacity (Qiu, Zhou, Han, & Zhang, 2018). Feedstocks were pyrolyzed at 450°C for 0.5, 1, 2, and 3 hr based on previous studies to reveal the dynamics of biochar properties with residence time (Chandra & Bhattacharya, 2019;Kong, Gao, Zhou, Zhao, & Sun, 2018;Shaaban et al., 2014). The temperature in muffle furnace was raised at a rate of 5°C/min.

| Analysis of biochar properties
The yield, pH, elemental composition, surface morphology, surface area, porosity, and functional group of S. alterniflora biochar were measured.
The weight ratio of biochar to feedstock was used to represent biochar yield (Chandra & Bhattacharya, 2019). The pH was measured using pH probe (SL1000, Hach) at the biochar-deionized water ratio of 1 g:20 ml after shaking for 1 hr and standing for 5 min (Ahmad et al., 2018). Elemental composition (C, H, O, and N) was measured with elemental analyzer (Vario EL cube, Elementar). Surface morphology was obtained using scanning electron microscopy (SEM, JSM-6480LV, Hitachi). The nitrogen gas adsorption/desorption isotherms were analyzed at −196°C with automatic instruments (ASAP 2460, Micromeritics). The pore size and volume were calculated using Barrett-Joyner-Halenda equation, and the surface area was calculated using Brunauer-Emmet-Teller equation . Functional groups were identified using Fourier transformed infrared spectroscopy (FTIR; Zhao et al., 2018). FTIR spectra were obtained from 400 to 4,000 cm −1 in 4 cm −1 intervals with an FTIR spectrometer (Nicolet 6700, Thermo Fisher).

| Statistical analysis
SPSS Statistics software version 17.0 (SPSS Inc.) was used to perform the statistical analysis of the data. Basic analysis of mean, minimum, and maximum was conducted for biochar properties. The correlations between biochar properties (yield and pH) and pyrolysis (temperature and residence time) were fitted using the Curve Estimation procedure.

| Biochar yield and pH
S. alterniflora biomass experienced a weight loss near 60% at 350°C, and biochar yield ranged from 23.82% in 650°C to 42.39% in 350°C (Figure 1a). S. alterniflora biochar yield showed a steady decreasing trend as increasing temperature from 350°C to 650°C. The yield of biochar produced from untreated and desalted feedstocks decreased 30% and 40% as increasing temperature up to 650°C, respectively ( Figure 1a). The yield of biochar produced from untreated and desalted feedstocks decreased only 3.64% and 3.45% with residence time increased from 0.5 to 3 hr, respectively ( Figure 1b). The yield of biochar produced from untreated S. alterniflora was higher than that produced from desalted feedstocks (Figure 1).
S. alterniflora biochar was strongly alkaline with pH ranging from 10.04 to 11.46 (Figure 2a). The pH showed a sharp increase as increasing temperature from 350°C to 500°C, and became steady above 500°C with slight decline from 600°C to 650°C (Figure 2a). The maximum pH of S. alterniflora biochar occurred at 500°C, 11.46, and 11.04 for biochar produced from desalted and untreated feedstocks, respectively. As residence time of pyrolysis increased from 0.5 to 3 hr, the pH only increased 0.21 and 0.24 units for biochar produced from desalted and untreated feedstocks, respectively (Figure 2b).

| Elemental composition
Pyrolysis of raw feedstocks decreased O and H contents, and increased C and N contents (Figure 3a,b).
Carbonization during pyrolysis induced the increase of C contents in S. alterniflora biochar, although the increasing trend was observed with slight fluctuation. The O and H contents declined as increasing pyrolysis temperature, and N contents in S. alterniflora biochar showed F I G U R E 2 Changes in biochar pH with pyrolysis temperature (a) and residence time (b) F I G U R E 3 Changes in biochar elemental contents (a, b), H/C ratio (c), and O/C ratio (d) with pyrolysis temperature. C, carbon; H, hydrogen; O, oxygen no significant changing trend with pyrolysis temperature (Figure 3a,b).
The H/C and O/C ratios in S. alterniflora biochar decreased as increasing temperature (Figure 3c,d). However, the O/C ratio in biochar produced from desalted feedstocks increased as increasing temperature from 600°C to 650°C, and that of biochar produced from untreated feedstocks increased as increasing temperature from 550°C to 650°C.
Although O/C ratio increased at high temperature, they were still lower at high temperature of 500°C-650°C than that at low temperature of 350°C-450°C (Figure 3d).
The C, H, O, and N contents in biochar showed no significant changes with different residence time (Figure 4a,b). The H/C and O/C ratios showed slight decreasing trends as residence time increased from 0.5 to 3 hr (Figure 4c,d).
The C, H, O, and N contents in biochar produced from untreated S. alterniflora were lower than that produced from desalted feedstocks (Figures 3 and 4). The O/C ratio of biochar produced from desalted S. alterniflora generally was lower than that produced from untreated feedstocks (Figures 3 and 4).
The H/C ratios showed no significant difference between biochar produced from desalted and untreated feedstocks (Figures 3 and 4).

| Surface morphology
Raw feedstocks had little pore, and pores appeared in biochar as increasing pyrolysis temperature ( Figure 5). S. alterniflora biochar pyrolyzed at 350°C showed visible tube-like pore structures, and the pore wall of tube-like structures became thinner and even collapsed as increasing temperature. Micropores occurred on the pore wall and micropores quantity increased as increasing temperature ( Figure 5). Contrasting with pyrolysis temperature, residence time had no significant effects on biochar surface morphology ( Figure 6).
The pore shape of biochar produced from desalted S. alterniflora was more irregular than that produced from untreated feedstocks, and the quantity of meso-and micropores in desalted biochar was higher than untreated biochar F I G U R E 4 Changes in biochar elemental contents (a, b), H/C ratio (c), and O/C ratio (d) with residence time. C, carbon; H, hydrogen; O, oxygen F I G U R E 5 SEM images of raw feedstocks and biochar produced at different temperatures (only images at 350°C and 650°C were shown). SEM, scanning electron microscopy F I G U R E 6 SEM images of Spartina alterniflora biochar produced at residence time of 0.5, 1, and 3 hr. SEM, scanning electron microscopy ( Figures 5 and 6). The difference of SEM images was consistent with results of biochar surface area and porosity (Figure 7).

| Surface area and porosity
Biochar surface area and porosity significantly varied with pyrolysis temperature in the study, but showed no apparent changing trends with residence time (Figure 7). Surface area and pore volume of S. alterniflora biochar were relatively low, and showed no significant changing trends with temperature increased from 350°C to 500°C (Figure 7). Significant increases of surface area, mesopore volume, and total pore volume were found as increasing temperature from 550°C to 650°C (Figure 7).
Average pore diameter of biochar produced from untreated feedstocks decreased as increasing temperature, and presented a sharp decrease from 450°C to 500°C (Figure 7). Average pore diameter of biochar produced from desalted feedstocks showed a changing trend of single peak curve as increasing temperature, and the peak occurred at 450°C (Figure 7). The surface area and porosity of biochar produced from desalted S. alterniflora were higher than that produced from untreated feedstocks (Figure 7).

| Functional groups
The FTIR spectra showed changes in functional groups with various pyrolysis temperature and residence time (Figure 8). In the given spectra, the peak at 3,400 cm −1 was linked with -OH group. The peaks at 2,923 and 1,435 cm −1 were linked with aliphatic -CH x stretching. The peak at 1,574 cm −1 corresponded to the presence of C=C stretching. The peak at band range of 1,110-1,114 cm −1 was linked with ether C-O-C group. The peak at 875 cm −1 was linked with the C-H group.
The intensity and diversity of functional groups on S. alterniflora biochar surface decreased as increasing pyrolysis temperature. At 650°C, there were almost no functional groups on biochar surface. The intensity of the -OH group was weak, and became negligible at temperature above 500°C. The -CH x group at 2,923 cm −1 only observed F I G U R E 7 Changes in biochar surface area (a), average pore diameter (b), total pore volume (c), and mesopore volume (d) with pyrolysis temperature at temperature of 350°C and 400°C. The intensity of the C=C group was higher at temperature below 450°C, and declined at temperature above 450°C. Maximum intensity of the C-O-C group for biochar produced from untreated feedstocks was observed at 500°C. However, the C-O-C group for biochar produced from desalted feedstocks only observed at 350°C. The intensity of the C-H group became negligible at 650°C (Figure 8a,b).
Residence time showed no influence on the intensities of C=C, -CH x , and C-H groups. The intensity of the -OH group was weak, and decreased as residence time increased from 0.5 to 3 hr. While the intensity of the C-O-C group decreased as residence time increased from 0.5 to 2 hr, and increased at a residence time of 3 hr (Figure 8c,d).
Except the C-O-C group, the intensity and diversity of the other functional groups had no significant difference between biochar produced from desalted and untreated S. alterniflora. The intensity of the C-O-C group in biochar produced from untreated S. alterniflora was higher than that produced from desalted feedstocks (Figure 8).

| Effects of pyrolysis conditions and desalination on biochar yield and pH
Biochar yield rapidly declined as increasing temperature at initial pyrolysis stage, and followed by steady decline (Keiluweit, Nico, Johnson, & Kleber, 2010;Zhao et al., 2018). The rapid decline of S. alterniflora biochar yield as increasing temperature was attributed to the removal of water and labile volatile matters from feedstocks . The steady decreasing trend of S. alterniflora biochar yield as increasing temperature was linked with the dehydration and thermal decomposition of cellulose and lignin (Chandra & Bhattacharya, 2019). Biochar yield slightly decreased as increasing residence time, which indicated the carbonization of S. alterniflora was almost completed in a short residence time. Mineral matters played catalytic roles in biochar formation (Raveendran, Ganesh, & Khilar, 1995). Desalination of F I G U R E 8 Changes in biochar functional groups with pyrolysis temperature (a, b) and residence time (c, d) feedstocks reduced S. alterniflora biochar yield due to the reduction of alkali metals.
The pH is one crucial factor determining the interactions between biochar and polar pollutants . High pH provided more negative surface charge and increased the electrostatic interactions with pollutants, while low pH increased the π-electron donoracceptor interactions and improved H-bonding for pollutants . Changes in biochar pH were attributed to the decomposition of organic and inorganic components and the formation of alkaline ash (Shinogi & Kanri, 2003). Similar to the changing trends of biochar alkalinity produced from canola, soybean, and peanut straws (Yuan, Xu, & Zhang, 2011), S. alterniflora biochar pH showed a sharp increase as increasing temperature from 350°C to 500°C. Biochar pH remained almost constant at high temperature due to the constant contents of ash (Shinogi & Kanri, 2003).
Four categories of biochar alkalinity have been proposed, that is, surface functional group, soluble organic compound, carbonate, and inorganic alkali salt (Fidel, Laird, Thompson, & Lawrinenko, 2017;Shi, Li, Ni, & Xu, 2019). The inorganic alkali salt was separated from feedstocks at pyrolysis temperature over 300°C, and thus increased biochar pH (Cao & Harris, 2010). Although alkali metals (e.g., Na + , Mg 2+ , and K + ) were leached from feedstocks by desalination, the pH of biochar derived from desalted S. alterniflora was higher than that of untreated feedstocks. In addition, the diversity and intensity functional groups had no significant difference between the two types of biochar. Therefore, the concentrations of soluble organic compound and carbonate in biochar were probably the main causes of S. alterniflora biochar alkalinity.

| Effects of pyrolysis conditions and desalination on elemental composition
The O and H contents declined due to deoxygenation and dehydration of feedstocks as increasing pyrolysis temperature (Li et al., 2015). The N contents in biochar were always affected by feedstock type instead of pyrolysis conditions ; thus, N contents in S. alterniflora biochar showed no significant changing trend with pyrolysis temperature.
The H/C and O/C ratios indicate biochar aromaticity and polarity, respectively (Cao et al., 2019;Tang et al., 2019). The lower H/C and O/C ratios indicated biochar pyrolyzed at higher temperature were more aromatic and less polar, which makes it more stable in environments (Leng & Huang, 2018;Wang, Li, Li, Yu, & Wang, 2019;Zhao et al., 2018). At lower temperature, high O/C ratio indicated more O-containing functional groups appeared in biochar surface, and high H/C ratio indicated more H-C bonds appeared in forms of biodegradable organic matters, which is available for plants and microorganisms (Chandra & Bhattacharya, 2019).
Most of metal salts were deposited in biochar during pyrolysis process, thus desalination reduced C, H, O, and N contents in S. alterniflora biochar. The low O/C ratio demonstrated low polarity and high stability of biochar produced from desalted S. alterniflora .

| Effects of pyrolysis conditions and
desalination on surface morphology, surface area, and porosity S. alterniflora biochar pyrolyzed at 350°C showed visible tube-like pore structures, which were attributed to the carbonaceous skeleton of feedstocks (Zhang, Liu, & Liu, 2015). As increasing temperature, the pore wall of tube-like structures became thinner and even collapsed due to the destruction of cell structures in feedstocks, which improved biochar porosity. The increase of biochar porosity as increasing temperature was conducive to the diffusion of substances into biochar inner, and provided more interfaces for pollutant adsorption and colonization of soil microorganisms (Chandra & Bhattacharya, 2019;Tan, Sun, Xu, Wang, & Xu, 2016).
The increase of surface area from 300°C to 500°C was attributed to the decomposition of cellulose, which induced the appearance of amorphous carbon structure and micropore as shown by SEM images . Significant increases of surface area, mesopore volume, and total pore volume from 550°C to 650°C were attributed to the degradation of lignin and release of hydrogen and methane (Taskin et al., 2019;Zhao et al., 2017). Low average pore diameter at high temperature (>500°C) was attributed to the formation of meso-and micropores .
The residence time and condensation of volatiles in biochar pores can be reduced by demineralization, which increase the amount and rate of volatiles release (Raveendran et al., 1995). Desalination treatment of feedstocks improved the surface area and porosity of S. alterniflora biochar. The higher surface area and porosity of biochar produced from desalted S. alterniflora indicated their higher adsorption capacity, because larger surface area and richer pore structures provide more opportunity for pollutants adsorption in biochar (Jiang, Lin, & Mbog, 2018).

| Effects of pyrolysis conditions and desalination on functional groups
The -OH group indicated the occurrence of H-bonding interactions in biochar (Li et al., 2013). The decrease of | 645 XIA et Al.
-OH group with increasing temperature was attributed to the dehydration of feedstocks (Chen, Yang, Wang, Zhang, & Chen, 2012;Zhao et al., 2017). The C = C group appeared in forms of aromatic hydrocarbons (Chandra & Bhattacharya, 2019). The C = C group intensity declined at temperature above 450°C due to the condensation of aromatic compounds (Li et al., 2017;Shen et al., 2019). The C-O-C group is one of the O-containing functional groups (Cui, Hao, Zhang, He, & Yang, 2016). The intensity of C-O-C group was changed by desalination, which was linked with the different forms of oxygen in desalted and untreated S. alterniflora that were converted to carbon chains containing C-O bonds during pyrolysis process (Wang et al., 2019). The C-H group appeared in form of aromatic ring and heteroaromatic compounds, and aromatic ring provides π-electrons to bond inorganic pollutants (Wang et al., 2019).

| CONCLUSIONS
S. alterniflora, an invasive plant in Chinese coastal wetlands, was pyrolyzed to produce biochar. Pyrolysis temperature and desalination treatment of feedstocks affected biochar properties. S. alterniflora biochar with high alkalinity, stability, surface area, and porosity can be achieved at pyrolysis temperature above 550°C. However, S. alterniflora biochar with diverse functional groups can be achieved at temperature below 500°C. Reducing metal salt contents in feedstocks improved the stability, surface area, and porosity of S. alterniflora biochar. The above pyrolysis parameters can be used by other researchers and managers to produce biochar with specific properties for environmental usage.