Abstract
Biochar made from seaweed biomass of marine farms established for water pollutant remediation may be a promising amendment for soil remediation in the same coastal territory. The study aimed to assess the soil Cu-immobilizing, pH neutralizing, and nutrient improvement capabilities of a seaweed biochar when incorporated into degraded soil of the same coastal territory (Puchuncaví District, central Chile). Experimental design considered five treatments; degraded soil of Puchuncaví valley (C-), C- amended with either local seaweed biochar (B), vermicompost (V), or its mixture (BV), and a background soil (C+). Experimental soils were placed in pots and kept in a greenhouse (4 weeks). Lolium perenne was then sown and cultivated until week 11. Treatments amended with biochar (B and BV) significantly increased soil pH, available nitrogen and decreased Cu2+ ions. These treatments reached very high EC values but had no negative effect on plant yield. Regarding plant growth, V and BV significantly increased biomass, but V resulted in higher yield because of its higher nutritional status. It was concluded that seaweed biochar, made from local seaweed biomass of a coastal marine water pollutant remediation farm, may be an effective soil amendment for degraded soils of the same coastal territory, although its combination with an organic amendment should be considered.
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Seaweed Biochar (Sourced from Marine Water Remediation Farms) for Soil Remediation: Towards an Integrated Approach of Terrestrial-Coastal Marine Water Remediation
Rosanna Ginocchio,a,b,* Matías Araya,b,c,d,e Jéssica Machado,a,b Luz María de la Fuente,a,b Fabiola Orrego,b Eduardo C. Arellano,a,b and Loretto Contreras-Porcia b,c,d,e
Biochar made from seaweed biomass of marine farms established for water pollutant remediation may be a promising amendment for soil remediation in the same coastal territory. The study aimed to assess the soil Cu-immobilizing, pH neutralizing, and nutrient improvement capabilities of a seaweed biochar when incorporated into degraded soil of the same coastal territory (Puchuncaví District, central Chile). Experimental design considered five treatments; degraded soil of Puchuncaví valley (C-), C- amended with either local seaweed biochar (B), vermicompost (V), or its mixture (BV), and a background soil (C+). Experimental soils were placed in pots and kept in a greenhouse (4 weeks). Lolium perenne was then sown and cultivated until week 11. Treatments amended with biochar (B and BV) significantly increased soil pH, available nitrogen and decreased Cu2+ ions. These treatments reached very high EC values but had no negative effect on plant yield. Regarding plant growth, V and BV significantly increased biomass, but V resulted in higher yield because of its higher nutritional status. It was concluded that seaweed biochar, made from local seaweed biomass of a coastal marine water pollutant remediation farm, may be an effective soil amendment for degraded soils of the same coastal territory, although its combination with an organic amendment should be considered.
DOI: 10.15376/biores.18.3.4637-4656
Keywords: Soil metal pollution; Aided phytostabilization; Soil remediation; Macroalgal biochar; Residue valorization; Integrated territorial remediation
Contact information: a: Agronomy and Forestry Faculty, Pontificia Universidad Católica de Chile, Av. Vicuña Mackenna 4860, Santiago, Chile; b: Center of Applied Ecology and Sustainability, Pontificia Universidad Católica de Chile, Av. Libertador Bernardo O Higgins 340, Santiago, Chile; c: Departamento de Ecología y Biodiversidad, Facultad de Ciencias de la Vida, Universidad Andres Bello, Santiago, Chile; d: Centro de Investigación Marina Quintay (CIMARQ), Facultad de Ciencias de la Vida, Universidad Andres Bello, Quintay, Chile; e: Instituto Milenio en Socio-Ecología Costera (SECOS), Santiago, Chile;
* Corresponding author: rosanna.ginocchio@uc.cl
INTRODUCTION
Globally, coastal zones have long become active for urbanization and industrialization (Halpern et al. 2015; Ausili et al. 2020). As a result of historical and/or current industrial pollution, both terrestrial and marine ecosystems of many coastal territories have been significantly affected (He et al. 2014; Yanes et al. 2018; Zhai et al. 2020). Generally, remediation actions to reduce environmental risks in these territories are performed independently. For polluted coastal marine waters, passive processes for in situ pollutant uptake through biosorption methods have been implemented (de Freitas et al. 2019) and offer many advantages (e.g., simple implementation, low operating cost, high efficiency, no additional nutrient requirements, and relatively low energy input) (Michalak et al. 2013; Bordoloi et al. 2017; Liu et al. 2019). In contrast, in situ remediation techniques for physicochemically degraded soils, based on the application of soil amendments, are widely implemented because of their fast, low-cost, and easy application (Palansooriya et al. 2020). Among other factors, the election of soil amendments depends on the type of pollutants present (i.e., organic and/or inorganic), their bioavailable fraction, and the degree of other physical (i.e., compaction or reduction of organic matter) and/or chemical (i.e., acidification, salinization, nutrient loss) soil alterations (Palansooriya et al. 2020). Through delivering cost-effective remediation techniques and fulfilling green and sustainable remediation principles (because of their low life cycle environmental footprints), the use of proper bioadsorbents and soil amendments has been widely used for environmental remediation (Hou and Al-Tabbaa 2014).
Yet, the opportunity remains for an integrated approach of coastal marine water and terrestrial remediation in coastal territories. Specifically, some bioadsorbents generated from coastal marine water remediation could potentially be processed for pollutant removal and thus reused as amendments for soil remediation in the same territory. This approach may not only reduce waste disposal and secondary pollution (normally associated with the reuse of residues) (Shi et al. 2018) but may also reduce remediation costs and support socioeconomical development of local communities in the territory. Indeed, emerging post-sorption technologies now enable the manufacturing of value-added key adsorption products that can subsequently be used for/in (i) fertilizers, (ii) catalysis, (iii) carbonaceous metal nanoparticle synthesis, (iv) feed additives, and (v) biologically active compounds (Kumar Reddy et al. 2017). These new strategies ensure the sustainable valorization of post-sorption materials (with their ecological affability, biocompatibility, and widespread accessibility) as an economically viable alternative to the engineering of other green chemicals (Kumar Reddy et al. 2017; Tawfik et al. 2022).
The Puchuncaví District in central Chile serves as an example of a coastal territory where both land (Puchuncaví Valley) and marine (Quintero Bay) ecosystems have been heavily polluted and degraded because of historical and current industrial operations. In fact, this territory is considered an environmental sacrifice zone because of the broad range of industrial activities along its shoreline since the 1960s, which includes the settlement of a copper smelter and a thermoelectric plant (Hormazabal et al. 2019). A recent study reported high concentrations of heavy metals in the water column near Quintero bay (Cu: 28 to 741 µg L−1, As: 9 to 348 µg L−1, Cd: 0.091 to 0.243 µg L−1, and Pb: 0.093 to 3.425 µg L−1) with similar concentrations being reported for two sites 5 km (Caleta Horcón) and 19 km (Cachagua) north of the industrial park (Oyarzo-Miranda et al. 2020). Furthermore, soils of the Puchuncaví valley have been strongly degraded (both physically and chemically) and characterized as acidic, depleted in organic matter and nitrogen, and as being enriched with metals (e.g., Cu, Zn, Pb, and Cd) and metalloids (e.g., As) (Ginocchio 2000; Ginocchio et al. 2004; Neaman et al. 2009). As such, several research studies and local government efforts have been directed at coping with the environmental risks of pollutants and soil degradation. Remediation actions for land (Muena et al. 2010; Córdova et al. 2011; Neaman et al. 2012; Ulriksen et al. 2012; Pardo et al. 2018) as well as coastal marine waters and sediments (Parra et al. 2015; Oyarzo-Miranda et al. 2020; Latorre-Padilla et al. 2021a, 2021b) have been suggested as cost-effective alternatives.
In the last decade, an experimental brown algae (Macrocystis pyrifera) seaweed farm had been established at Quintero Bay to encourage in situ pollutant (organic and inorganic) remediation of its coastal marine waters. The project was funded by a regional Chilean grant (Fondo de Innovación para la Competitividad [Innovation Fund for Competitiveness], FIC Algas 2017, n° 30397482-0). The species of M. pyrifera was selected based on its ability to grow to considerable sizes in a wide range of environmental conditions, representing a great advantage in terms of biomass productivity (Schiel and Foster 2015). Moreover, compared to other brown seaweeds, M. pyrifera has a higher capacity to accumulate metals (Davis et al. 2003; Latorre-Padilla et al. 2021b), which renders its biomass a potentially effective bioadsorbent for in situ clean-up of coastal marine waters. Whilst seaweed biomass can normally be used as a raw product for the food, animal feed, cosmetics, and nutraceuticals industries (Rotter et al. 2020), pollutant-rich seaweed biomass must be discarded.
Several studies have demonstrated that seaweed biomass may be a promising raw material for the production of biochar (a carbon-rich product produced via thermal decomposition under oxygen-limited conditions and at relatively low temperatures) (Chen et al. 2015; Roberts et al. 2015a; 2015b; 2015c; Cha et al. 2016; Contreras-Porcia et al. 2018). In recent years, because of its potential use as a soil amendment, biochar has become a subject of important scientific and commercial interest (Guo et al. 2020). Several studies have shown that biochar can remediate the physical and chemical properties of degraded soils (Curaqueo et al. 2014; Obia et al. 2016; Amin et al. 2017), which in turn promotes plant development (Al-Wabel et al. 2013; Amin et al. 2017; Godlewska et al. 2017; De Sousa Lima et al. 2018). Biochar made from macroalgae biomass has low carbon content and relatively low cation exchange capacity, but high pH (8.0 to 10.1), nitrogen, and extractable phosphate contents (Bird et al. 2011). Macroalgal biochars present more similarities to those produced from poultry litter relative to those derived from ligno-cellulosic feedstocks (Bird et al. 2011). Due to these positive characteristics, macroalgal biochar has properties that may provide direct nutrient benefits to soils and may be particularly useful for application on acidic soils (Bird et al. 2011; Yu et al. 2017). However, electrical conductivity (15.3 to 61.2 mS cm-1) and extractable Na (range 141 to 812 cmol(+) kg-1) in biochars from saline macroalgal species is high, unlike freshwater species that have lower values (2.8 mS cm-1 and 24 cmol(+) kg-1, respectively) (Bird et al. 2011), which may restrict their use as soil amendment. Few studies have assessed the pros and cons of the use of seaweed-derived biochar as a soil amendment for in situ soil remediation (Bird et al. 2011). Biochar produced from pollutant-rich seaweed biomass (obtained from the Quintero Bay seaweed farms) represents a promising opportunity to implement a low-cost local amendment for degraded soil remediation in the Puchuncaví valley using an integrated bioremediation approach for this coastal territory, as long as its salinity is not a restriction to plant growth.
The primary aim of the present study was to assess the Cu-immobilizing and neutralizing capabilities of seaweed-derived biochar when incorporated into the acidic and metal(loid)-enriched soils of the Puchuncaví valley, to assess improvement of the soil’s nutritional content for plants and to assess any impact in soil salinity (based on the results from small-scale and short-term laboratory experiments). Because the organic matter content and nutritional status of the chemically degraded Los Maitenes soil had been very low, the secondary aim of the study was to assess another organic amendment (vermicompost) for soil remediation. The present study represents the first research step towards field site evaluations.
EXPERIMENTAL
Study Area and Soil Sample Collection
Soil samples were collected from the Puchuncaví valley, Valparaíso Region, a semiarid Mediterranean climate-type ecosystem located in the coastal area of central Chile (Fig. 1), with an historical average annual precipitation of 351 mm, mainly collected in winter (May and August) and an average annual temperature of 14.4 °C. Since 1964, soil in this area has been heavily degraded via the emission of sulfur dioxide (SO2) and metal(loid)-rich particulate matter (such as copper, zinc, cadmium, and arsenic) from the Ventanas industrial complex. Whilst environmental regulations (established in the 1990s) achieved a considerable reduction in pollutant emissions, the cumulative effect of more than 35 years of industrial activity in this area resulted in heavily polluted and eroded soils (Ginocchio 2000; Ginocchio et al. 2004; Neaman et. al. 2009) as well as polluted coastal marine waters (Oyarzo-Miranda 2020).
Using a shovel, two composite topsoil batches (0 to 20 cm depth; n = 10 (totaling 60 kg)) were sampled for use in this study. The first batch (C-) represented chemically and physically degraded soils collected from Los Maitenes, an area located 2 km southeast of the Ventanas industrial complex, known for its soil acidification and high concentrations of Cu, Zn, As, and Cd (Neaman et al. 2009; Cárcamo et al. 2012; Rueda-Holgado et al. 2016). The second batch (C+) represented background soils collected from Maitencillo, a coastal area located 11 km north of Los Maitenes, where the soil has not been affected by atmospheric pollutants derived from the Ventanas industrial complex (Neaman et al. 2009; Muena et al. 2010). Composite soil samples from both areas were stored in closed polyethylene containers before being transferred to the laboratory where respective samples were sieved to < 2 mm with a nylon mesh and oven-dried at 60 °C for 24 h. Thereafter, samples were manually homogenized, and a batch of each soil type was sent to the Soil Analysis Laboratory of the Pontificia Universidad Católica de Valparaíso, Quillota, Chile for physicochemical determinations. The obtained results are summarized in Table 1.
Table 1. Physicochemical Characteristics of Chemically Degraded Topsoil from Los Maitenes (C-) and Background Topsoil from Maitencillo (C+)
EC, electric conductivity; CEC, cation exchange capacity; OM, organic matter
Fig. 1. Satellite image (Google Earth) and Chilean map showing the Puchuncaví District in central Chile that includes Quintero Bay and the Puchuncaví valley (dotted circle). Seaweed biomass for biochar production was obtained from coastal marine cultivation areas located along Quintero Bay (experimental remediation farm, FIC Algas project). Soil collection areas in the valley included Los Maitenes (degraded soil) and Maitencillo (background soil) sites. The Ventanas industrial complex, established in the 1960s, is indicated by a red box.
Characteristics of Study Soil Amendments: Seaweed Biochar and Vermicompost
The seaweed biochar used in the present study was produced from air-dry M. pyrifera biomass. The latter was harvested from individuals that had been cultivated for 120 days in coastal waters of the experimental remediation farm in Quintero Bay (FIC Algas 2017, project n° 30397482-0) and which had been exposed to pollutant (organic and inorganic) emissions from the Ventanas industrial complex (Parra et al. 2015). Dried Macrocystis biomass was transferred to the Waste and Bioenergy Management Center of Universidad de la Frontera and subjected to a slow pyrolysis process in a specialized furnace with a stainless-steel reactor and two thermocouples. A constant N2 flow (0.5 L min-1) was used for air displacement. Starting at room temperature, constant biomass heating at a rate of 20 to 50 °C h-1 was implemented until a final temperature of 450 °C was reached (Araya et al. 2021). A biochar yield of 53.3% was obtained, with an ash content of 69.9%. General characteristics of produced biochar can be found in Araya et al. (2021).
Due to the absence of an intensive washing pretreatment of the seaweed biomass or deashing post-treatment, given the prioritization of productivity for commercial purposes (Araya et al. 2021), the elevated ash and EC values of biochar obtained in this study had been considerably higher than that of other types of biochar (Tag et al. 2016). This is to be expected, since the algae came from a saline environment (Bird et al. 2011), finding concentrations of sodium in seaweed biomass between 27 and 55 g kg-1 (Neveux et al. 2014). However, washing of seaweed biomass results in a reduction of the sodium concentration by approximately 95% (Neveux et al. 2014).
Metal(loid) contents of seaweed biochar and other characteristics are shown in Table 2. Noteworthy was the observation that even though seaweed biomass used for biochar production in the present study came from a highly contaminated environmental matrix (Oyarzo-Miranda et al. 2020), metals adsorbed in the seaweed biomass subsequently remained in the tars of the pyrolysis process (Araya et al. 2021).
In the present study, to better cope with low levels of OM and nutrient soil deficiency of degraded Los Maitenes soil (C-), commercial vermicompost (ANASAC) was used as a secondary soil amendment. The selected vermicompost had a pH of 7.7, EC of 6.53 dS m-1, OM content of 14%, and an N-nitrate content of 118 mg kg-1 as stated in the label.
Table 2. Chemical Characteristics of Seaweed Biochar
EC, electric conductivity; CEC, cation exchange capacity; OM, organic matter
Experimental Design
A total of five soil treatments were assessed in the present study, the background soil of Maitencillo (C+), the physicochemical degraded soil of Los Maitenes (C-), and three experimentally amended conditions for the C- soil (Table 3). The latter was designated as B (seaweed biochar), V (vermicompost), and BV (seaweed biochar and vermicompost). The treatments consisted of six replications each and thus totaled 30 experimental units. To assess the effect of biochar and/or vermicompost in the physico-chemical properties of C- soil, experimental soil mixtures using single and combined amendments were prepared (as shown in Table 3). Batches of C- soil were mixed with 1% seaweed biochar and/or 3% vermicompost (dry weight basis, dw), which had been equivalent to doses of 22.3 ton ha-1 and 67.05 ton ha-1, respectively. The biochar dosage was determined via laboratory assays, aimed at neutralizing the C- soil (up to pH 6.5), while the vermicompost dosage was defined based on previous area-related studies (Goecke et al. 2011; Cárcamo et al. 2012; Neaman et al. 2012). A fifth treatment, combining both amendments at their respective doses, was also incorporated (Table 3).
Table 3. Soil Treatments Used to Assess the Effects of Seaweed Biochar and Vermicompost on the Remediation of Chemically Degraded Los Maitenes Soil (C-)
Single and combined treatments of B and V were based on dry weight percentages and background soil from Maitencillo (C+) was included for comparison
Batches (6 kg, dry weight) of each experimental soil were prepared by adding the substrates in 10-L polyethylene bottles and mixing the components in an automatic roller (Tecco YGR) at 11 rpm for 20 min. The gravimetric water content at 100% field capacity of all experimental soils (amended and not amended) was estimated according to the method by Klute (1986) to define irrigation regimes for weight loss. Thereafter, the soil from each experimental soil was poured into six 1-L plastic pots (800 g of soil per pot) with holes for drainage. Pots with experimental soils (total of 30 experimental units) were randomly placed on benches in a greenhouse under a controlled temperature (26 ± 2 °C) and natural light and photoperiod (spring period). Positioning of pots was randomized once a week to avoid edge effects, and they were watered at 70% of field capacity every other day over 11 weeks. As suggested in the literature, soil chemical equilibration was supported during an initial 4-week period (España et al. 2019). Then, at the beginning of the fifth week, 0.6 g of Lolium perenne var. Belinda seeds (a species commonly used for assessing soil acidity and metal toxicity) were sown in every pot (Arienzo et al. 2004).
During the 1st, 4th, and 11th weeks of the assay, following the methodology described by Vulkan et al. (2000), 5 to 7 mL aliquots of soil pore water had been collected from all pots using Rhizon® pore water samplers (Rhizosphere Research Products, Wageningen, Netherlands). These samples were stored in acid-washed polyethylene vials and were analyzed for pH (combined pH electrode, Sensorex 120C), electrical conductivity (EC) (conductivity-meter, Schott Gerate CG858), and ionic copper (Cu2+) (selective Cu ion electrode, Orion, model 9629 BN; calibrated using a diamino acetic acid solution) (Rachou et al. 2007). pCu2+ (Cu activity) was calculated from the obtained Cu2+ values (according to Eq. 1):
pCu2+ = –log [Cu2+] (1)
By week 11, the root and shoot biomass of L. perenne in each pot had been harvested. Aerial biomass was washed with deionized water and blotted dry with absorbent paper prior to fresh biomass determination. Roots were separated from soils by spraying tap water (at a low pressure) onto the roots over a fine-mesh sieve (allowing for the removal of soil while retaining thin roots). Root and aerial biomass were oven-dried to a constant weight (dried at 45 °C in an air-forced cabinet for 72 h) before determining dry weight biomass.
Statistical Analysis
A two-way analysis of variance (ANOVA) was performed (with a Tukey HSD posteriori test) to compare differences in chemical properties of pore water among treatments and time. A one-way ANOVA was used to contrast the root and shoot biomass of L. perenne among treatments. When data did not meet conditions to perform parametric tests, logarithmic transformations, as described in Zar (1984), were performed. All data processing was performed using the SPSS 23 (IBM, Armonk, NY, USA) and Infostat (UNC, 2020p, Córdoba, Argentina) statistical programs.
RESULTS AND DISCUSSION
Experimental Soils: Physicochemical Characteristics
As expected, the most successful neutralization of C- soil was obtained after biochar incorporation (with or without vermicompost) (Table 4). At the tested doses of the present study (Table 3), incorporation of vermicompost also reduced soil acidity, although less efficiently than seaweed biochar. Indeed, incorporation of biochar increased the pH of C- soil by 2.4 units (up to pH 6.6) followed by incorporation of vermicompost by 2.0 units (up to pH 6.1) (Table 4). This was unsurprising because biochar is known for its neutralization effects that may be attributed to its alkalinity (Ding et al. 2017; Yu et al. 2017; Moore et al. 2018). Soil neutralization via these soil amendments could furthermore be associated with the presence of phenolic, carboxyl, and hydroxyl functional groups in both vermicompost and biochar (which react with soil H+ and thereby reduce H+ concentrations and increase the pH level) (Ding et al. 2017; Oliveira et al. 2017; Yu et al. 2017; Araya et al. 2021).
Due to the high salinity of the seaweed biochar (27.4 dS m-1; Table 2) of the present study, it was not surprising that biochar amended C- soils showed high EC soil values (with or without vermicompost) (Table 4), even at the low (1%) dose applied to C- soil. Incorporation of vermicompost did not affect EC values (Table 4). The CEC of amended soils (B, V, and BV) was lower than that of C- soil (with values ranging from 3.22 to 4.11 cmol kg-1). Due to the dilution effect of adding amendments (particularly in the case of vermicompost), the total metal(loid) concentrations of amended soils were slightly reduced (Table 4).
Table 4. Initial Physicochemical Parameters of Experimental Soils
* Codes explained in Table 3
EC, electric conductivity; CEC, cation exchange capacity; OM, organic matter
Lastly, incorporation of biochar or vermicompost improved nutritional content of C- soil, but only vermicompost improved OM content (1.7-fold) of C- soil (to even higher values than that of the C+ soil) (Table 4). Specifically, available N, P, and K levels in C- soil increased 1.7-, 1.9-, and 11.1-fold after incorporation of biochar and 2.2-, 1.5-, and 3.1-fold after incorporation of vermicompost (Table 4). Therefore, available N increased much more (2.2-fold) after vermicompost incorporation than with biochar incorporation alone (1.7-fold). Findings from the present study agreed with previously described results regarding selected soil amendments (Amoah-Antwi et al. 2020; Kheir et al. 2021).
Experimental Soils: Pore Water Chemistry
Soil neutralization was rapidly achieved after the application of both amendments and significantly increased with the progression of time as shown by soil pore water values (Table 5). Specifically, B and BV treatments reached the highest pH values, with only slight variation detected throughout the 11 weeks. The pH value in vermicompost treatments (V and BV) also increased (up to pH 6.51 by week 11), although it should be noted that the initial pH of 5.7 had been nearly one unit higher than that of C- soil (Table 5). Whilst a gradual pH increase over time was observed in the pore water for all treatments, the magnitude of this increase varied among the treatments and the different sampling dates (Table 5). The C- soil showed the lowest pH values throughout the experiment and little variation was found throughout subsequent weeks. It is known that several factors may influence long-term soil pH changes (e.g., the microbial decomposition of OM and the nitrification process) (Cárcamo et al. 2012), as observed in soil pore waters of the present study.
Table 5. Variation of pH, EC, and pCu2+ in Experimental Soils over Time (during weeks 1, 4, and 11)
Data are presented as means with standard deviation. Electrical conductivity (EC) that exceeded the measurement capacity of the conductivimeter is expressed as > 20. F and P values of two-way ANOVA for pH and pCu2+ levels are provided.
Biochar amended C- soil (B and BV) reached very high EC values (> 20 mS cm-1), resulting in saline pore water values (particularly at the onset of the assay) (Table 5). While these EC values tended to decrease with time (in all treatments), EC values of the B and BV treatments were still higher than 14 mS cm-1 by week 11 (indicating high salt concentrations) (Table 5). Generally, the high EC values of biochar can be explained by its high ash content, high surface-area-to-volume ratio (Ullah et al. 2020), and a particularly high Na concentration when of marine origin (Bird et al. 2012). All three characteristics were true for the seaweed biochar used in the present study. Therefore, the increase of EC in biochar-amended soils could be explained by either the high contribution of ionic nutrients (that can promote plant growth) or the presence of cationic and anionic salts (that can cause toxicity symptoms in plants), which suggests that the present´s study increase in pore water EC rather reflects the increase in nutrient ions (such as K, Mg, or Ca). However, to test this hypothesis, analyses to quantify seaweed biochar salt concentrations and to assess its potential toxicity to plants are needed.
Copper activity (pCu2+) values significantly increased after the incorporation of amendments (B, V, and BV), which suggests an important decrease in soluble Cu concentrations in C- soil (Table 5). As expected, the incorporation of biochar had been more effective in decreasing soluble Cu levels (3.8-fold) than that of vermicompost alone (1.4-fold). However, pCu2+ values also significantly decreased for all treatments over time, indicating an overall increase in Cu solubility over time irrespective of treatment (Table 5). Yet, the biggest changes were detected for B and BV treatments, where pCu2+ decreased from 20.24 to 13.95 and from 17.41 to 11.73, respectively (Table 5). The magnitude of this decrease was 3 to 5 times higher than that of the C- soil (which only decreased from 5.71 (week 1) to 2.64 (week 11), suggesting that the incorporation of biochar significantly decreased Cu solubility in the chemically degraded soil, at least for the duration of this assay. The effect of biochar on metal availability depends on its original feedstock and its processing temperature (Wu et al. 2017; Araya et al. 2021). As such and because of contrasting results, the potential of biochar to modify soil metal availability has been widely discussed. Some authors have found that biochar reduces the mobility and bioavailability of metals (mainly ascribed to its liming effect) (Jones et al. 2016; Wu et al. 2017; O’Connor et al. 2018), whereas others have found that metal(loid) concentrations in pore water of biochar amended soils may increase. For example, Beesley et al. (2010) found that Cu and As concentrations in pore water of biochar amended soils increased more than 30-fold, which could be explained by a significant increase of Dissolved Organic Carbon (DOC). In general, biochar produced at < 500 °C has a high DOC content that could, in turn, promote the solubilization and mobilization of Cu into soil pore water, due to the formation of Cu-DOC complexes (Ahmad et al. 2014; Hameed et al. 2019). Yet, in the present study, Cu activity significantly decreased in soil pore water after incorporation of seaweed biochar with C- soil (the biochar having been produced at < 500 °C). Moreover, this effect lasted 11 weeks after biochar application.
Plant Growth Parameters
Shoot biomass (dry weight basis, dw) of ryegrass plants that had been cultivated in experimental soils varied significantly among the treatments (P < 0.001) (with the lowest value recorded for C- soil (0.75 g) and the highest value recorded for V treatment (2.52 g) (Fig. 2a). All amended C- soils (B, V, and BV) showed significantly higher shoot biomass than that of C- soil, although, unexpectedly, B and BV treatments were not statistically different to the C+ soil (as was seen for V treatment) (Fig. 2a). Similar to shoot biomass, all amendments significantly increased root biomass (dw) compared to that of the C- soil (P < 0.001) (Fig. 2b), although none were statistically different from C+ soil (Fig. 2b). Pearson single correlations among plant biomass and soil pore water parameters (pH, EC, and pCu) showed positive and statistically significant correlations among root biomass and pH (r = 0.53) as well as shoot biomass and EC (r = 0.43). No single correlation of significance had been detected among pCu and L. perenne shoot or root biomass.
Fig. 2. Variation of shoot (a) and root (b) dry biomass of Lolium perenne plants grown in C- and C+ soils and amended C- soils (B, V, and BV) (n = 6). Letters indicate significant differences among treatments according to a Tukey HSD test (P < 0.05).
Seaweed biochar and/or vermicompost incorporation to C- soil resulted in a positive and significant response for dry biomass of L. perenne, with similar (B and BV) or even higher (V) yields than the C+ (background) soil. These results suggest that, at the experimental dosage tested, the use of both soil amendments had been effective to restore the soil chemistry of C- soils (discussed above) and to sustain normal growth of the indicator plant. For vermicompost (V) incorporation, shoot yield was even higher than that of the background soil. These results agreed with previous findings that biochar (Abd El-Azeem et al. 2013; Roberts et al. 2015b, 2015c; Godlewska et al. 2017) and vermicompost (Kheir et al. 2021) may be used as soil amendments for the remediation of chemically degraded soils. Changes in metal and nutrient availability are mainly governed by changes in soil pH (González et al. 2015). Because biochar tends to alkalize soils, it can reduce metal availability. In addition, nutrient availability could be reduced if the amendment changed the soil pH beyond its optimal range (5.5 to 6.8) (Lehmann et al. 2015). For example, N, K, Ca, and Mg deficiencies can occur when the pH goes below the optimal range, whereas the solubility of Fe, P, Mn, Zn, and Cu can decrease when the pH goes above the optimal range (Cortés-D et al. 2013). In this study, soil pH in the optimum range was achieved by incorporating vermicompost with acidified soils. However, biochar application then increased soil pore water pH above 6.8, which might explain its lesser effect on plant dry biomass.
Some studies have suggested that, while biochar promotes metal immobilization, it may also decrease the availability of macro and micro-nutrients (resulting in nutrient deficiencies for the plant). For example, a study by Rees et al. (2015) on the cultivation of L. perenne and Noccaea caerulescens illustrated that biochar incorporation with acidic soils improved the nutritional condition of the soil and decreased metal solubility. Yet biochar incorporation with soils of a higher pH decreased nutrient availability (mainly due to soil alkalization and changes in negative exchange sites for metal cations and nutrients) (Rees et al. 2015). The relationship between pH and biochar exchange sites was also studied by Gang et al. (2019), who found that there are pH ranges in which the nutrients provided by the biochar may become more/less available. For example, when the pH of an acidified soil increases, the adsorption of NH4+ also increases (due to the increase of negative charges on the substrate). In contrast, when soil pH increases above 8, NO3– adsorption decreases (because the negative charge of OH– binds to the positive charges on the surface of the biochar) (Gang et al. 2019). As a result, the combined use of biochar with other amendments has been recommended to achieve the reduction of metal availability whilst contributing to soil fertility and favoring plant growth (Wu et al. 2017; Xu et al. 2017). For example, a study by Wang et al. (2016) found that the combination of compost and biochar resulted in significantly greater benefits than single biochar when it came to fresh root and shoot biomass of mung bean (Vigna radiata) plants. Yet, in the present work, the combined incorporation of seaweed biochar and vermicompost (BV) did not induce a better plant response (at least not with the tested doses).
It is also important to note that elevated EC values of B and BV treatments had no relevant effects on plant yield. It is well known that potential plant toxicity, based on high EC soil values, depends on several factors related to salt concentration and composition (e.g., having high cation (K, Mg, Na), anion (NO3, SO4, Cl), or other ion (Mo, Al, and B) concentrations) (Wallender and Tanji 2011). In this study, the high macronutrient contribution of biochar suggests that its cationic component may be contributing to its high EC, which would thus not be toxic to the organisms growing in the soil. Generally, the high EC values of biochar can be explained by its high ash content, a high surface-area-to-volume ratio (Ullah et al. 2020), and a particularly high Na concentration when of marine origin (Bird et al. 2012). All three characteristics were true for the seaweed biochar used in the present study. Therefore, the increase of EC in biochar amended soils could be explained by either the high contribution of ionic nutrients (that can promote plant growth) or the presence of cationic and anionic salts (that can cause toxicity symptoms in plants), which suggests that the present study’s increase in pore water EC rather reflects the increase in nutrient ions (such as K, Mg, or Ca). However, to test this hypothesis, analyses to quantify seaweed biochar salt concentrations and to assess its potential toxicity to plants are needed.
Incorporation of selected seaweed biochar and/or vermicompost with degraded soil of Los Maitenes (C-) proved to be effective for the improvement of relevant physical (OM) and/or chemical soil parameters (pH, Cu availability, and macronutrient availability), and subsequently allowed for proper L. perenne growth (at least over the short term of 11 weeks). Findings from the present study thus agreed with previously described results regarding soil amendments (Amoah-Antwi et al. 2020; Kheir et al. 2021). The findings furthermore suggested that the use of seaweed biochar as a soil amendment might be more effective than vermicompost for potential in situ and large-scale soil remediation in the Puchuncaví valley (inducing chemical improvements at a third of the application dosage). Indeed, while incorporated at a lower dose than vermicompost, seaweed biochar resulted in significantly higher soil neutralization and reduced free Cu2+ ions in soil pore water (even 11 weeks after its application). Whilst the present study represents a promising step toward field site evaluations, lower doses of vermicompost or other locally available organic amendment candidates must first be considered in similar laboratory-scaled experiments.
CONCLUSIONS
- Seaweed biochar, produced at a slow pyrolysis temperature (450 °C) from M. pyrifera macroalgae biomass (grown at an experimental remediation farm in Quintero Bay), proved to be an effective amendment for remediation of degraded soils from the Puchuncaví valley under laboratory controlled conditions. At a low application dose (1%), it effectively increases pH, neutralizes the soil, and immobilizes its Cu ions, whilst improving macronutrient levels over the short-term period of 11 weeks. These achieved soil improvements were able to restore indicator plant (L. perenne) yield levels to that of the background soil (irrespective of the soil salinization detected after biochar incorporation).
- Although seaweed biochar was effective in increasing soil pH and, therefore, reducing both soil acidity and Cu solubility in degraded soil of Los Maitenes, the authors recommend the combined use with vermicompost, or another organic amended, to better contribute to restore the soil OM levels and soil fertility and thereby favor plant growth. This approach could be particularly useful if aided phytostabilization with native plants is the preferred technique to encourage in situ soil remediation.
- The positive experimental results obtained under laboratory-controlled conditions in the present study show the potential of an integrated terrestrial-coastal marine water remediation approach for the Puchuncaví District. However, further remediation studies under field conditions are needed as well as project evaluations and assessments of economic feasibility.
ACKNOWLEDGMENTS
This study was funded in Chile by ANID PIA/BASAL FB0002, by the FIC Algas 2017 project n° 30397482-0, and the ANID Millennium Science Initiative Program ICN 2019_015.
REFERENCES CITED
Abd El-Azeem, S. A. M., Ahmad, M., Usman, A. R. A., Kim, K.-R., Oh, S.-E., Lee, S. S., and Ok, Y. S. (2013). “Changes of biochemical properties and heavy metal bioavailability in soil treated with natural liming materials,” Environ. Earth Sci. 70, 3411-3420. DOI: 10.1007/s12665-013-2410-3
Ahmad, M., Rajapaksha, A. U., Lim, J. E., Zhang, M., Bolan, N., Mohan, D., Vithanage, M., Lee, S. S., and Ok, Y. S. (2014). “Biochar as a sorbent for contaminant management in soil and water: A review,” Chemosphere 99, 19-23. DOI: 10.1016/j.chemosphere.2013.10.071
Al-Wabel, M. I., Al-Omran, A., El-Naggar, A. H., Nadeem, M., and Usman, A. R. A. (2013). “Pyrolysis temperature induced changes in characteristics and chemical composition of biochar produced from conocarpus wastes,” Bioresource Technology 131, 374-379. DOI: 10.1016/j.biortech.2012.12.165
Amin, A. E.-E. A. Z., Eissa, M. A., El-Eyuoon Abu Zied Amin, A., and Eissa, M. A. (2017). “Biochar effects on nitrogen and phosphorus use efficiencies of zucchini plants grown in a calcareous sandy soil,” Journal of Soil Science and Plant Nutrition 17(4), 912-921. DOI: 10.4067/S0718-95162017000400006.
Amoah-Antwi, C., Kwiatkowska-Malina, J., Thornton, S. F., Fenton, O., Malina, G., and Szara, E. (2020). “Restoration of soil quality using biochar and Brown cial waste: A review,” Science of The Total Environment 722, article ID 137852. DOI: 10.1016/j.scitotenv.2020.137852
Araya, M., Rivas, J., Sepúlveda, G., Espinoza-González, C., Lira, S., Meynard, A., Blanco, E., Escalona, N., Ginocchio, R., Garrido-Ramírez, E., et al. (2021). “Effect of pyrolysis temperature on copper aqueous removal capability of biocar derived from the kelp Macrocystis pyrifera,” Applied Sciences 11(19), article 9223. DOI: 10.3390/app11199223.
Arienzo, M., Adamo, P., and Cozzolino, V. (2004). “The potential of Lolium perenne for revegetation of contaminated soil from a metallurgical site,” Science of The Total Environ. 319, 13-25. DOI : 10.1016/S0048-9697(03)00435-2
Ausili, A., Bergamin, L., and Romano, E. (2020). “Environmental status of Italian coastal marine areas affected by long history of contamination,” Frontiers in Environmental Science 8, article 34. DOI: 10.3389/fenvs.2020.00034
Beesley, L., Moreno-Jiménez, E., and Gomez-Eyles, J. L. (2010). “Effects of biochar and greenwaste compost amendments on mobility, bioavailability and toxicity of inorganic and organic contaminants in a multi-element polluted soil,” Environmental Pollution 158(6), article ID 2282e2287. DOI: 10.1016/j.envpol.2010.02.003
Bird, M. I., Wurster, C. M., de Paula, S. P. H., Bass, A. M., and de Nys, R. (2011). “Algal biochar production and properties,” Bioresource Technology 102, 1886-1891. DOI: 10.1016/j.biortech.2010.07.106
Bird, M. I., Wurster, C. M., de Paula Silva, P. H., Paul, N. A., and de Nys, R. (2012). “Algal biochar: Effects and applications,” GCB Bioenergy 4(1), 61-69. DOI: 10.1111/j.1757-1707.2011.01109.x
Bordoloi, N., Goswami, R., Kumar, M., and Kataki, R. (2017). “Biosorption of Co(II) from aqueous solution using algal biochar: Kinetics and isotherm studies,” Bioresource Technology 244, 1465-1469. DOI: 10.1016/j.biortech.2017.05.139
Cárcamo, V., Bustamante, E., Trangolao, E., de la Fuente, L. M., Mench, M., and Ginocchio, R. (2012). “Simultaneous immobilization of metals and arsenic in acidic polluted soils near a copper smelter in central Chile,” Environmental Science and Pollution Research 19(4), 1131-1143. DOI: 10.1007/s11356-011-0673-3
Cha, J. S., Park, S. H., Jung, S. C., Ryu, C., Jeon, J. K., Shin, M. C., and Park, Y. K. (2016). “Production and utilization of biochar: A review,” Journal of Industrial and Engineering Chemistry 40, 1-15. DOI: 10.1016/j.jiec.2016.06.002
Chen, H., Zhou, H., Luo, G., Zhang, S., and Chen, J. (2015). “Macroalgae for biofuels production: Progress and perspectives,” Renew. Sust. Energ. Rev. 47, 427-437. DOI: 10.1016/j.rser.2015.03.086
Contreras-Porcia, L, Araya, M., Garrido-Ramírez, E., Bulboa, C., Remonsellez, J. P., Zapata, J., Espinoza, C., and Rivas. J. (2018). “Biochar production from seaweeds,” in: Protocols for Macroalgae Research, B. Charrier, T. Wichard, and C. R. K. Reddy (Eds.), CRC Press, Boca Raton, FL, USA, pp. 175-185.
Córdova, S., Neaman, A, González, I., Ginocchio, R., and Fine, P. (2011). “The effect of lime and compost amendments on the potential for the revegetation of metal-polluted, acidic soils,” Geoderma 166, 135-144. DOI: 10.1016/j.geoderma.2011.07.022
Cortés, D. L., Pérez, J. H., and Camacho-Tamayo, J. H. (2013). “Relación espacial entre la conductividad eléctrica y algunas propiedades químicas del suelo [Spatial relation between electrical conductivity and some chemical soil properties],” Revista UDCA Actualidad & Divulgación Científica 16(2), 401-408.
Curaqueo, G., Meier, S., Khan, N., Cea, M., and Navia, R. (2014). “Use of biochar on two volcanic soils: Effects on soil properties and barley yield,” Journal of Soil Science and Plant Nutrition 14(4), 911-924. DOI: 10.4067/S0718-95162014005000072
Davis, T., Volesky, B., and Mucci, A. (2003). “A review of the biochemistry of heavy metal biosorption by Brown algae,” Water Research 37, 4311-4330. DOI: 10.1016/S0043-1354(03)00293-8
de Freitas, G. R., da Silva, M. G. C., and Vieira, M. G. A. (2019). “Biosorption technology for removal of toxic metals: A review of commercial biosorbents and patents,” Environmental Science and Pollution Research 26, 19097-19118. DOI: 10.1007/s11356-019-05330-8
De Sousa Lima, J. R., de Moraes Silva, W., Valente de Medeiros, E., Pereira Duda, G., Metri Corrêa, M., Pereira Martins Filho, A., Clermont-Dauphin, C., Celso Dantas Antonino, A., and Hammecker, C. (2018). “Effect of biochar on physicochemical properties of a sandy soil and maize growth in a greenhouse experiment,” Geoderma 319, 14-23. DOI: 10.1016/j.geoderma.2017.12.033
Ding, Y., Liu, Y., Liu, S., Huang, X., Li, Z., Tan, X., Zeng, G., and Zhou, L. (2017). “Potential benefits of biochar in agricultural soils: A review,” Pedosphere 27(4), 645-661. DOI: 10.1016/S1002-0160(17)60375-8
España, H., Bas, F., Zornoza, R., Masaguer, A., Gandarillas, M., Arellano, E., and Ginocchio, R. (2019). “Effectiveness of pig sludge as organic amendment of different textural class mine tailings with different periods of amendment-contact time,” Journal of Environmental Management 230, 311-318. DOI: 10.1016/j.jenvman.2018.09.022
Gang, H., Tan, Z., Zhang, L., and Huang, Q. (2019). “Preparation of biochar with high absorbability and its nutrient adsorption–desorption behavior,” Science of The Total Environment 694, article ID133728. DOI: 10.1016/j.scitotenv.2019.133728
Ginocchio, R. (2000). “Effects of a copper smelter on a grassland community in the Puchuncavi Valley, Chile,” Chemosphere 41(1–2), 15-23. DOI: 10.1016/S0045-6535(99)00385-9
Ginocchio, R., Carvallo, G., Toro, I., Bustamante, E., Silva, Y., and Sepúlveda, N. (2004). “Microspatial variation of soil metal pollution and plant recruitment near a copper smelter in central Chile,” Environmental Pollution 127, 343-352. DOI: 10.1016/j.envpol.2003.08.020
Godlewska, P., Schmidt, H. P., Ok, Y. S., and Oleszczuk, P. (2017). “Biochar for composting improvement and contaminants reduction. A review,” Bioresource Technology 246, 193-202. DOI: 10.1016/j.biortech.2017.07.095
Goecke, P., Ginocchio, R., Mench, M., and Neaman, A. (2011). “Amendments promote the development of Lolium perenne in soils affected by historical copper smelting operations,” International Journal of Phytoremediation 13(6), 552-566. DOI: 1080/15226514.2010.495150
González, M., Quiroz, I., Travieso, R., Chung, P., and García, E. (2015). “Determinación de medios de cultivo y pH para la masificación in vitro de cepas de Suillus luteus Aubl. asociadas a Pinus radiata D. Don y Scleroderma citrinum Pers. asociadas a Eucalyptus globulus Labill. de la región del Biobío, Chile [Determination of culture media and pH for the in vitro massification of Suillus luteus Aubl. strains associated with Pinus radiata D. Don and Scleroderma citrinum Pers. associated with Eucalyptus globulus Labill. from the Biobío region, Chile],” Revista Árvore 39(1), 105-113.
Guo, M., Song, W., and Tian, J. (2020). “Biochar-facilitated soil remediation: Mechanisms and efficacy variations,” Frontiers in Environmental Science 8, article ID 521512. DOI: 10.3389/fenvs.2020.521512
Halpern, B. S., Frazier M., Potapenko, J., Casey, K. S., Koenig, K., Longo, C., Stewart Lowndes, J., Cotton Rockwood, R., Selig, E. R., Selkoe, K. A., and Walbridge, S. (2015). “Spatial and temporal changes in cumulative human impacts on the world’s ocean,” Nature Communications 6, article 7615. DOI: 10.1038/ncomms8615
Hameed, R., Cheng, L., Yang, K., Fang, J., and Lin, D. (2019). “Endogenous release of metals with dissolved organic carbon from biochar: Effects of pyrolysis temperature, particle size, and solution chemistry,” Environmental Pollution 255, article ID 113253. DOI: 10.1016/j.envpol.2019.113253
He, Q., Bertness, M. D., Bruno, J. F., Li, B., Chen, G., Coverdale, T. C, and Liu, J. (2014). “Economic development and coastal ecosystem change in China,” Science Reports 4, article 5995. DOI: 10.1038/srep05995
Hormazabal, N., Maino, S., Vergara, M., and Vergara, M. (2019). “Living in a sacrifice zone: A multi-scale analysis of Puchuncaví District, Chile,” Revista Hábitat Sustentable 9(2), 6-15. DOI: 10.22320/07190700.2019.09.02.01
Hou, D., and Al-Tabbaa, A. (2014). “Sustainability: A new imperative in contaminated land remediation,” Environmental Science and Policy 39, 25-34. DOI: 10.1016/j.envsci.2014.02.003
Jones, S., Bardos, R. P., Kidd, P. S., Mench, M., de Leij, F., Hutchings, T., Cundy, A., Joyce, C., Soja, G., Friesl-Hanl, W., et al. (2016). “Biochar and compost amendments enhance copper immobilisation and support plant growth in contaminated soils,” Journal of Environmental Management 171, 101-112. DOI: 10.1016/j.jenvman.2016.01.024
Kheir, A. M. S., Ali, E. F., Ahmed, M., Eissa, M. A., Majrashi, A., and Ali, O. A. M. (2021). “Biochar blended humate and vermicompost enhanced immobilization of heavy metals, improved wheat productivity, and minimized human health risks in different contaminated environments,” Journal of Environmental Chemical Engineering 9(4), article ID 105700. DOI: 10.1016/j.jece.2021.105700
Kumar Reddy, D. H., Vijayaraghavan, K., Kim, J. A., and Yun, Y. S. (2017). “Valorisation of post-sorption materials: Opportunities, strategies, and challenges,” Advances in Colloid and Interface Science 242, 35-58. DOI: 10.1016/j.cis.2016.12.002
Latorre-Padilla, N., Meynard, A., Oyarzún, F. X., and Contreras-Porcia, L. (2021a). “Ingestion of contaminated kelps by the herbivore Tetrapygus niger: Negative effects on food intake, growth, fertility, and early development,” Marine Pollution Bulletin 167, article ID 112365. DOI: 10.1016/j.marpolbul.2021.112365
Latorre-Padilla, N., Maynard, A., Rivas, J., and Loretto-Porcia, L. (2021b). “Transfer of pollutants from Macrocystis pyrifera to Tetrapygus niger in a highly impacted coastal zone of Chile,” Toxics 9(10), article 244. DOI: 10.3390/toxics9100244
Liu, C., Wang, Q., Jia, F., and Song, S. (2019). “Adsorption of heavy on molybdenum disulfide in water: A critical review,” Journal of Molecular Liquids 291, article 111390. DOI: 10.1016/j.molliq.2019.111390
Michalak, I., Chojnacka, K., and Witek-Krowiak, A. (2013). “State of the art for the biosorption process—a review,” Applied Biochemistry and Biotechnology 170, 1389-1416. DOI: 10.1007/s12010-013-0269-0
Moore, F., González, M. E., Khan, N., Curaqueo, G., Sanchez-Monedero, M., Rilling, J., Morales, E., Panichini, M., Mutis, A., Jorquera, M., et al. (2018). “Copper immobilization by biochar and microbial community abundance in metal-contaminated soils,” Science of The Total Environment 616–617, 960-969. DOI: 10.1016/j.scitotenv.2017.10.223
Muena, V., González, I., and Neaman, A. (2010). “Efectos del encalado y la fertilización nitrogenada sobre el desarrollo de Oenothera affinis en un suelo afectado por la minería del cobre [Effects of liming and nitrogen fertilization on the development of Oenothera affinis in a soil affected by copper mining],” Journal of Soil Science and Plant Nutrition 10(2), 102-114. DOI: 10.4067/S0718-27912010000200002
Neaman, A., Huerta, S., and Sauvé, S. (2012). “Effects of lime and compost on earthworm (Eisenia fetida) reproduction in copper and arsenic contaminated soils from the Puchuncaví Valley, Chile,” Ecotoxicology and Environmental Safety 80(1), 386-392. DOI: 10.1016/j.ecoenv.2012.04.013
Neaman, A., Reyes, L., Trolard, F., Bourrié, G., and Sauvé, S. (2009). “Copper mobility in contaminated soils of the Puchuncaví valley, central Chile,” Geoderma 150(3-4), 359-366. DOI: 10.1016/j.geoderma.2009.02.017
Neveux, N., Yuen, A. K. l., Jazrawi, C., He, Y., Magnusson, M., Haynes, B. S., Masters, A. F., Montoya, A., Paul, N. A., Maschmeyer, T., and de Nys, R. (2014). “Pre- and post-harvest treatment of macroalgae to improve the quality of feedstock for hydrothermal liquefaction,” Algal Research 6, 22-31. DOI: 10.1016/j.algal.2014.08.008
Obia, A., Mulder, J., Martinsen, V., Cornelissen, G., and Borresen, T. (2016). “In situ effects of biochar on aggregation, water retention and porosity in light textured tropical soils,” Soil and Tillage Research 155, 35-44. DOI: 10.1016/j.still.2015.08.002
O’Connor, D., Peng, T., Zhang, J., Tsang, D. C. W., Alessi, D. S., Shen, Z., Bolan, N. S., and Hou, D. (2018). “Biochar application for the remediation of heavy metal polluted land: A review of in situ field trials,” Science of The Total Environment 619–620, 815-826. DOI: 10.1016/j.scitotenv.2017.11.132
Oliveira, F. R., Patel, A. K., Jaisi, D. P., Adhikari, S., Lu, H., and Khanal, K. (2017). “Environmental application of biochar: Current status and perspectives,” Bioresource Technology 246, 110-122. DOI: 10.1016/j.biortech.2017.08.122
Oyarzo-Miranda, C., Latorre, N., Meynard, A., Rivas, J., Bulboa, C., and Contreras-Porcia, L. (2020). “Coastal pollution from the industrial park Quintero bay of central Chile: Effects on abundance, morphology, and development of the kelp Lessonia spicata (Phaeophyceae),” PLOS One 15(10), 1-24. DOI: 10.1371/journal.pone.0240581
Palansooriya, K. M., Shaheen, S. M., Chen, S. S., Tsang, D. C. W., Hashimoto, Y., Hou, D., Bolan, N. S., Rinklebe, J., and Ok, Y. S. (2020). “Soil amendments for immobilization of potentially toxic elements in contaminated soils: A critical review,” Environment International 134, article ID 105046. DOI: 10.1016/j.envint.2019.105046
Pardo, J., Mondaca, P., Celis-Diez, J. L., Ginocchio, R., Navarro-Villarroel, C., and Neaman, A. (2018). “Assessment of revegetation of an acidic metal(oid)-polluted soil six years after the incorporation of lime with and without compost,” Geoderma 331, 81-86. DOI: 10.1016/j.geoderma.2018.06.018
Parra, S., Bravo, M. A., Quiroz, W., Querol, X., and Paipa, C. (2015). “Distribution and pollution assessment of trace elements in marine sediments in the Quintero Bay (Chile),” Marine Pollution Bulletin 99(1), 256- 263. DOI : 10.1016/j.marpolbul.2015.07.066
Rachou, J., Gagnon, C., and Sauvé, S. (2007). “Use of an ion-selective electrode for free copper measurements in low salinity and low ionic strength matrices,” Environmental Chemistry 4(2), 90-97. DOI: 10.1071/EN06036
Rees, F., Germain, C., Sterckeman, T., and Morel, J. L. (2015). “Plant growth and metal uptake by a non-hyperaccumulating species (Lolium perenne) and a Cd-Zn hyperaccumulator (Noccaea caerulescens) in contaminated soils amended with biochar,” Plant and Soil 395(1), 57-73. DOI: 10.1007/s11104-015-2384-x
Roberts, D. A., Paul, N. A., Bird, M. I., and Nys, R. (2015a). “Bioremediation for coal-fired power stations using macroalgae,” Journal of Environmental Management 153, 25-32. DOI: 10.1016/j.jenvman.2015.01.036
Roberts, D. A., Paul, N. A., Cole, A. J., and de Nys, R. (2015b). “From waste water treatment to land management: Conversion of aquatic biomass to biochar for soil amelioration and the fortification of crops with essential trace elements,” Journal of Environmental Management 157, 60-68. DOI: 10.1016/j.jenvman.2015.04.016
Roberts, D. A., Cole, A. J., Paul, N. A., and de Nys, R. (2015c). “Algal biochar enhances the re-vegetation of stockpiled mine soils with native grass,” Journal of Environmental Management 161, 173-180. DOI: 10.1016/j.jenvman.2015.07.002
Rotter, A., Bacu, A., Barbier, M., Bertoni, F., Bones, A. M., Cancela, M. L., Carlsson, J., Carvalho, M. F., Cegłowska, M., Dalay M. C., et al. (2020). “A new network for the advancement of marine biotechnology in Europe and beyond,” Frontiers in Marine Science 7, article 278. DOI: 10.3389/fmars.2020.00278
Rueda-Holgado, F., Calvo-Blázquez, L., Cereceda-Balic, F., and Pinilla-Gil, E. (2016). “Temporal and spatial variation of trace elements in atmospheric deposition around the industrial area of Puchuncaví-Ventanas (Chile) and its influence on exceedances of lead and cadmium critical loads in soils,” Chemosphere 144, 1788-1796. DOI: 10.1016/j.chemosphere.2015.10.079
Tag, A. T., Duman, G., Ucar, S., and Yanik, J. (2016). “Effects of feedstock type and pyrolysis temperature on potential applications of biochar,” Journal of Analytical and Applied Pyrolysis 120, 200-206. DOI: 10.1016/j.jaap.2016.05.006
Tawfik, A., Niaz, H., Qadeer, K., Qyyum, M. A., Liu, J. J., and Lee, M. (2022). “Valorisation of algal cells for biomass and bioenergy production from wastewater: Sustainable strategies, challenges, and techno-economic limitations,” Renewable and Sustainable Energy Reviews 157, article ID 112024. DOI: 10.1016/j.rser.2021.112024
Ullah, N., Ditta, A., Khalid, A., Mehmood, S., Rizwan, M. S., Ashraf, M., Mubeen, F., Imtiaz, M., and Iqbal, M. M. (2020). “Integrated effect of algal biochar and plant growth promoting rhizobacteria on physiology and growth of maize under deficit irrigations,” Journal of Soil Science and Plant Nutrition 20, 346-356. DOI: 10.1007/s42729-019-00112-0
Ulriksen, C., Ginocchio, R., Mench, M., and Neaman, A. (2012). “Lime and compost promote plant re-colonization of metal-polluted, acidic soils,” International Journal of Phytoremediation 14, 820-833. DOI: 10.1080/15226514.2011.628716
Schiel, D. R., and Foster, M. S. (2015). The Biology and Ecology of Giant Kelp Forest, University of California Press, Oakland, CA, USA.
Shi, S., Xu, G., Yu, H., and Zhang, Z. (2018). “Strategies of valorization of sludge from wastewater treatment,” Journal of Chemical Technology and Biotechnology 93, 936-944. DOI: 10.1002/jctb.5548
Wallender, W. W., and Tanji, K. K. (2011). Agricultural Salinity Assessment and Management (Report N° 71), American Society of Civil Engineers (ASCE), Reston, VA, USA.
Wang, G. J., Xu, Z. W., and Li, Y. (2016). “Effects of biochar and compost on mung bean growth and soil properties in a semi-arid area of northeast China,” International Journal of Agriculture & Biology 18(5), 1056-1060. DOI: 10.17957/IJAB/15.0210
Wu, S., He, H., Inthapanya, X., and Yang, C. (2017). “Role of biochar on composting of organic wastes and remediation of contaminated soils — A review,” Environmental Science and Pollution Research 24, 16560-16577. DOI: 10.1007/s11356-017-9168-1
Xu, X., Zhao, Y., Sima, J., Zhao, L., Mašek, O., and Cao, X. (2017). “Indispensable role of biochar-inherent mineral constituents in its environmental applications: A review,” Bioresource Technology 241, 887-899. DOI: 10.1016/j.biortech.2017.06.023
Yanes, A., Botero, C. M., Arrizabalaga, M., and Vásquez, J. G. (2018). “Methodological proposal for ecological risk assessment of the coastal zone of Antioquia, Colombia,” Ecological Engineering 130, 242-251. DOI: 10.1016/j.ecoleng.2017.12.010
Yu, K. L., Lau, B. F., Show, P. L., Ong, H. C., Ling, T. C., Chen, W. H., Ng, E. P., and Chang, J. S. (2017). “Recent developments on algal biochar production and characterization,” Bioresource Technology 246, 2-11. DOI: 10.1016/j.biortech.2017.08.009
Zar, J. H. (1984). Biostatistical Analysis, Prentice-Hall, Englewood Cliffs, NY, USA.
Zhai, T., Wang, J., Fang, Y., Qin, Y., Huang, L., and Chen, Y. (2020). “Assessing ecological risks caused by human activities in rapid urbanization coastal areas: Towards an integrated approach to determining key areas of terrestrial-oceanic ecosystems preservation and restoration,” Science of The Total Environment 708, article ID 135153. DOI: 10.1016/j.scitotenv.2019.135153
Article submitted: February 21, 2023; Peer review completed: April 8, 2023; Revised version received and accepted: May 12, 2023; Published: May 17, 2023.
DOI: 10.15376/biores.18.3.4637-4656