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Article

Recovery of Soil Processes in Replanted Mangroves: Implications for Soil Functions

by
Laís Coutinho Zayas Jimenez
1,
Hermano Melo Queiroz
1,
Gabriel Nuto Nóbrega
2,
Danilo Jefferson Romero
1,
Youjun Deng
3,
Xosé Luis Otero
4 and
Tiago Osório Ferreira
1,*
1
Department of Soil Science, Luiz de Queiroz College of Agriculture, University of São Paulo (ESALQ-USP), Av. Pádua Dias 11, Piracicaba 13418-900, SP, Brazil
2
Department of Geochemistry, Graduate Program in Earth Sciences (Geochemistry), Federal Fluminense University, Niterói 24020-141, RJ, Brazil
3
Department of Soil and Crop Sciences, Texas A&M University, College Station, TX 77843, USA
4
CRETUS, Department of Soil Science and Agricultural Chemistry, School of Biology, University of Santiago de Compostela, 15705 Santiago de Compostela, Spain
*
Author to whom correspondence should be addressed.
Forests 2022, 13(3), 422; https://0-doi-org.brum.beds.ac.uk/10.3390/f13030422
Submission received: 28 December 2021 / Revised: 20 February 2022 / Accepted: 3 March 2022 / Published: 8 March 2022
(This article belongs to the Special Issue Mangrove Wetland Restoration and Rehabilitation)
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Abstract

:
Mangrove revegetation is a vital strategy to recover ecosystem services (e.g., climate regulation and pollutants retention) provided by these ecosystems. Although soils are directly or indirectly responsible for diverse ecosystem services in mangrove ecosystems, few studies have focused on the recovery of soil functions (e.g., carbon sequestration) after mangrove replanting. This study aimed to evaluate the recovery of soil processes associated with Fe, S, and C dynamics and its implications for the restoration of soil functions. Two mangrove sites under replanting initiatives were studied along the Brazilian coast (i.e., NE and SE). The study was conducted in 3- and 7-year-old replanted mangrove forests, and a comparison was made with degraded and mature mangroves. Particle size, soil C stocks, Fe forms, total Fe and S contents, degrees of pyritization of Fe, and mineralogical assemblages were assessed. Seven years after replanting, soil C stocks increased by 42% and 29% in mangrove soils from the NE and SE sites, respectively. In addition, significant increases were observed in fine particles, reactive Fe, and pyrite contents in replanted plots. These new conditions promoted organic matter accumulation, stabilization, and potential metal retention. Our findings highlight the potential of revegetation programs for recovering soil processes and essential soil functions.

1. Introduction

Mangroves are recognized as one of the most valuable ecosystems due to their wide range of ecosystem services, whose worth is estimated at USD 24 trillion per year [1]. Among the ecosystem services provided by mangroves, those associated with soil processes (e.g., carbon sequestration and pollutant immobilization) [2,3,4,5] are currently among the most addressed. Accordingly, mangrove preservation and restoration programs that guarantee the proper functioning of their soils are vital to ensure ecosystem services [6,7].
In mangrove ecosystems, the soil functions are associated with their unique geochemical conditions. These forests are subjected to daily water saturation, leading to low O2 diffusion into soil pores [8,9,10]. After total O2 consumption by aerobic respiration, facultative and obligate anaerobic microorganisms progressively use oxidized species (NO3−, Mn4+, Fe3+, SO42−, CO2, and N2) as electron acceptors for soil organic matter decomposition [11,12]. In mangrove soils, microbial-mediated reductions of Fe3+ and SO42− are the main metabolic pathways for soil organic matter decomposition [13,14]. These anaerobic pathways contribute to low decomposition rates and, consequently, to a high accumulation of organic matter in mangrove soils, recognized as natural carbon sinks [12,15]. Additionally, the Fe3+ and SO42− metabolic pathways release Fe2+ and sulfides, which may precipitate as pyrite, mackinawite, and acid-volatile sulfides [14,16]. These sulfides represent one of the most stable sinks for potentially toxic elements [17,18].
In this sense, organic matter accumulation and pollutant immobilization are two key services directly controlled by the soils of mangrove forests through their unique soil biogeochemical processes [14,19,20]. In recent decades, the recognition of mangrove forests’ relevance has stimulated the restoration of initiatives worldwide, which occurs mainly through seedling plantation [21,22,23]. Recent studies have reported a negative effect of short-term mangrove degradation on soil functioning [22,24,25]. Loss of soil carbon contents and increased greenhouse gas emissions are the consequences of mangrove loss and degradation [26,27,28,29]. However, to our knowledge, no studies have directly assessed the capacity of revegetation to restore natural soil processes in mangrove forests. Thus, this study aimed to assess the recovery of soil functions (e.g., sink for carbon and trace metals) and correlated ecosystem services in two mangrove forests under revegetation programs in the Brazilian northeastern and southeastern coast.

2. Materials and Methods

2.1. Study Sites

Two mangrove forests under revegetation programs were sampled along the Brazilian coast: a mangrove forest at the Guanabara Bay (Rio de Janeiro state, SE-Brazil) and another mangrove forest at the Cocó river (Ceará state, NE-Brazil; Figure 1). Plots at different stages of revegetation (i.e., 3- and 7-year-old plantations) were found at both sites, thus allowing for a temporal analysis of the effects of revegetation and their comparison with degraded plots and adjacent mature mangrove forests. The Cocó river estuary in Ceará has constituted a conservation unit of the Environmental Protection Area of Sabiaguaba since 2006. During this period, mangrove replanting initiatives have been carried out [30]. The Guanabara Bay in Rio de Janeiro is located within a Permanent Preservation Area (PPA) that covers more than 1300 ha [31]. The PPA was created in 1984 to preserve mangrove forests and support reforestation programs [31,32].
According to the time elapsed since replanting, the studied plots were divided into three categories: well-established, mature mangrove forests (RJ-MM and CE-MM), 3-year-old mangrove plantations (RJ-3Y and CE-3Y), and 7-year-old mangrove plantations (RJ-7Y and CE-7Y). Additionally, replanted and mature mangroves were compared with degraded plots within each site.
In Ceará, degraded mangrove (CE-DM) is mainly impacted by urban occupation and deforestation; thus, it is characterized by a total absence of vegetation [33]. In Rio de Janeiro, there is a long history of degradation in Guanabara Bay (e.g., deforestation, informal housing, and sewage and industrial waste disposals) [34]. Previous studies reported that degraded areas are commonly colonized by Acrostichum aureum, a typical species associated with mangrove forests in the tropics [35,36]. These plants may present vigorous growth in cleared mangrove areas and can interfere with the success of mangrove forest regeneration processes [37].
In the state of Ceará (northeastern Brazil), the climate is semi-arid (BSh, Köppen climate classification; Table 1), with mean annual precipitation under 900 mm and with well-defined rainy (February to May) and dry (June to January) seasons [38,39]. Mangrove forests are surrounded by dunes and by the sandy–clayey soils from the Barreiras geological formation, dominated by quartz and kaolinite, with minor amounts of Fe oxyhydroxides [40,41,42]. Mangrove soils are subjected to a daily mesotidal regime, ranging from 0.75 to 3.25 m (Table 1) [43], with redox potentials (Eh) ranging between +16 and +450 mV and pH values ranging from 6.3 to 7.7 (Table 1). Mature mangroves are composed of Avicennia germinans (L.) L., Laguncularia racemosa (L.) C. F., and Rhizophora mangle L. Revegetation was carried out using Rhizophora mangle L propagules.
The climate in Guanabara Bay (southeastern Brazil) is classified as tropical humid (Af, Köppen climate classification; Table 1), with a rainfall regime varying between 1100 and 2100 mm, well-distributed throughout the year. Granitic–gneissic rocks from the Serra do Mar outcrop surround the Guanabara Bay, showing clayey soils composed of large amounts of gibbsite, kaolinite, and Fe oxyhydroxides in the clay fraction [44]. The region has low hydrodynamic activity, with a semidiurnal microtidal regime ranging from 0.1 to 1.2 m (Table 1) [45]. Mangrove soils are marked by Eh values ranging between +250 and +408 mV and pH values close to neutrality (ranging from 6.9 to 7.3; Table 1). The predominant plant species in mature and replanted mangrove forests are Avicennia germinans (L.) L., Laguncularia racemosa (L.) C. F., and Rhizophora mangle L.

2.2. Soil Sampling

Within both coastal sites, soil samples were collected from plots at different stages of vegetative growth (3- and 7-year-old plantations), degraded, and mature mangrove forests (Figure 1). In both sites, soil sampling was carried out during low tide within 1 × 1 m sampling points within each study plot, using polyvinyl chloride tubes attached to a stainless-steel sampler for flooded soils in order to obtain undeformed soil samples. After sample collection, tubes were hermetically sealed and transported to the laboratory in vertical position under refrigerated conditions; all soil samples were removed from the tubes and divided into sections at the following depth intervals: 0–10, 10–20, 20–30, and 30–40 cm.
Redox potential (Eh) and pH were measured in the field using portable meters. Eh was determined using a platinum electrode, and the final readings were corrected to a calomel reference electrode (+244 mV). pH values were measured using a glass electrode calibrated with standard solutions (pH 4.0 and 7.0).

2.3. Soil Chemical and Physical Analyses

Particle size distribution was determined by the densimeter method after both mechanical dispersion (agitation for 12 h) and chemical dispersion using a 0.15 mol L−1 sodium hexametaphosphate and 1 mol L−1 sodium hydroxide solution [46]. Before analysis, samples were pretreated with hydrogen peroxide (30% solution) to remove soil organic matter.
Soil organic carbon (OC) was determined by dry combustion in an elemental analyzer (LECO SE-144 DR). Prior to analysis, all soil samples were treated with HCl mol L−1 for carbonate removal [47]. Soil carbon stocks (SCS) were quantified to a depth of 40 cm following Equation (1) [47]:
SCS = soil bulk density × depth × OC
Solid-phase Fe partitioning was performed to assess the recovery of soil processes associated with Fe and S dynamics in the studied mangrove soils [48,49]. This method has been largely used in mangrove soil studies [14,17,39,50] and allows the obtainment of six distinct, operationally defined Fe fractions:
  • F1—exchangeable and soluble Fe, extracted by 1 mol L−1 MgCl2 solution at pH 7, agitated for 30 min;
  • F2—carbonate-associated Fe, extracted by 1 mol L−1 NaOAC solution at pH 5 (adjusted using acetic acid), agitated for 5 h;
  • F3—Fe in ferrihydrite, extracted by 0.04 mol L−1 hydroxylamine + 25%acetic acid (v/v) solution at 30 °C, agitated for 6 h;
  • F4—Fe in lepidocrocite, extracted by a 0.04 mol L−1 hydroxylamine + 25% acetic acid (v/v) solution at 96 °C, agitated for 6 h;
  • F5—Fe in crystalline oxyhydroxides, extracted by a 0.25 mol L−1 Na3C6H5O7 (sodium citrate) + 0.11 mol L−1 NaHCO3 (sodium bicarbonate) and 3g Na2S2O4 (sodium dithionite) solution at 75 °C, agitated for 30 min;
  • F6—Fe in pyritic forms (extracted after previous removal of silicates using 10 mol L−1 hydrofluoric acid, followed by agitation for 16 h and removal of organic matter using concentrated sulfuric acid, agitated for 2 h), using a concentrated nitric acid solution.
Between each step and the next, samples were centrifuged (6000 RPM for 30 min) to separate the extract, then washed with ultrapure water and centrifuged again.
Following the determination of pyritic Fe, the degree of Fe pyritization was calculated (DOP; Equation (2)), which determines the portion of the pseudo-total Fe content (i.e., the sum of F1 to F6) that is incorporated into pyrite (F6) (Berner, 1970; Ferreira et al., 2007). In addition, the sum of F1 to F5 was considered as reactive Fe.
DOP = [F6/(ΣF1→F6)] × 100
Moreover, total Fe and total S were determined by X-ray fluorescence spectrometry (XRF). Prior to analysis, all samples were dried at 105 °C and finely ground using an agate mill.

2.4. Mineralogical Characterization by X-ray Diffraction (XRD) and Scanning Electron Microscopy (SEM)

Mineralogical composition was assessed by X-ray diffraction (XRD) analysis using a Rigaku Miniflex II with CuKα radiation. XRD analysis was carried out using nonoriented powder samples (i.e., bulk samples) scanned from 3 to 60° 2θ, at 0.02° 2θ step size and 3s step−1 count time. To remove organic matter, soil samples were previously treated with 9% sodium hypochlorite [51].
Scanning electron microscopy was used to obtain photomicrographs of soil minerals. All images were obtained using a SU8010 cold-field emission scanning electron microscope (FESEM, Hitachi, Japan) equipped with energy-dispersive X-ray spectroscopy (EDS, AMETEK-EDAX, Mahwah, NJ, USA) for elemental analysis.

2.5. Statistical Analysis

A nonparametric statistical test with a 5% significance level was carried out to assess differences in soil parameters among the different scenarios (i.e., 3- and 7-year-old, degraded, and mature mangrove forests) within both sites (Ceará and Rio de Janeiro). As each study site is subjected to contrasting climate and geological surroundings, statistical analyses were performed independently. Relationships among soil parameters were assessed by multivariate discriminant analysis [52], which contributed to identifying the main variables that distinguish stages of revegetation and allowed us to make inferences on the recovery of soil processes. All statistical tests were performed using the XLSTAT software version v.2014.5.03.

3. Results

3.1. Particle Size Distribution

Soils from the CE site were dominated by sand and were predominantly classified as having a sandy–loam texture (CE-7Y, sand: 63%, silt: 29%, and clay 8%; CE-3Y, sand: 65%, silt: 27%, and clay 8%; CE-DM, sand: 68%, silt: 25%, and clay 7%), except for CE-MM (sand: 29%, silt: 52%, and clay 19%; Figure 2a), which showed a loam texture. On the other hand, soils from the RJ site showed a higher presence of fine particles with a silty–clay texture in RJ-MM (sand: 2%, silt: 43%, and clay 56%), RJ-7Y (sand: 5%, silt: 49%, and clay 46%), and RJ-DM (sand: 6%, silt: 51%, and clay 44%), and a silty–clay–loam texture in RJ-3Y (sand: 4%, silt: 48%, and clay 49%; Figure 2b).
In addition, in both sites (Figure 2c,d), there was a significant increase in fine particle (silt + clay) contents in replanted (3- and 7-year-old) plots in comparison with degraded mangroves. In CE-DM, CE-3Y, CE-7Y, and CE-MM, fine particle contents were 32 ± 1%, 35 ± 3%, 37 ± 8%, and 71 ± 16%, respectively (Figure 2c). In the Rio de Janeiro site, fine particle contents in RJ-DM, RJ-3Y, RJ-7Y, and RJ-MM were 94 ± 2%, 96 ± 3%, 95 ± 3%, and 98 ± 0.1%, respectively (Figure 2d).

3.2. Soil Carbon Stocks

In the Ceará site, mean SCS values were significantly higher (k = 23.48; p < 0.001) in mature (CE-MM: 20.2 ± 6.4 Kg m−2) than in replanted mangroves (CE-7Y: 11.5 ± 3.1 Kg m−2; CE-3Y: 10.5 ± 4.9 Kg m−2) and in degraded plots (CE-DM: 6.1 ± 1.7 Kg m−2; Figure 3a). No significant differences were observed between the replanted plots (CE-3Y and CE-7Y), while significantly lower SCS values were observed in CE-DM (Figure 3a).
In Rio de Janeiro, significantly higher SCS values (k = 14.12; p = 0.002) were observed in RJ-7Y (59.6 ± 15.2 Kg m−2), while the lowest values were found in RJ-3Y (21.5 ± 0.6 Kg m−2; Figure 3b). In RJ-DM and RJ-MM, SCS values were 33.5 ± 0.9 and 25.6 ± 2.2 Kg m−2, respectively (Figure 3b).

3.3. Fe Partitioning and Total Contents of Fe and S

In the Ceará site, sequential extraction showed a predominance of Fe associated with oxyhydroxides (i.e., F3, F4, and F5) in all plots (Figure 4a). Most Fe was associated with low-crystallinity fractions (i.e., F3 and F4), especially in both replanted plots. Contrastingly, in CE-MM, there was a sharp increase in Fe associated with the pyritic fraction compared with degraded and replanted plots. Regarding DOP values, the highest values were observed in CE-MM (42.8 ± 22.9%), but no significant differences were observed between CE-DM (0.8 ± 0.3%), CE-3Y (1.0 ± 0.2%), and CE-7Y (1.8 ± 2.1%; Figure 4c).
In the Rio de Janeiro site, in RJ-DM and RJ-3Y, sequential extraction showed a dominance of Fe associated with both low- and high-crystallinity Fe oxyhydroxides (i.e., F3, F4, and F5) and a sharp increase in Fe associated with pyrite (i.e., F6) with revegetation (Figure 4b). In RJ-7Y, the content of pyritic Fe (74,300 ± 60,130 mg kg−1) was ~4-fold higher than in RJ-DM (8500 ± 4800 mg kg−1) and 2-fold higher than in RJ-3Y (see Figure 4b). DOP values in all RJ plots ranged from 37% to 61%, and no significant differences were observed between plots (Figure 4d).
Regarding total Fe and S content, in the Ceará site, mean Fe contents were significantly higher in replanted plots (CE-MM: 19,700 ± 10,800 mg kg−1; CE-3Y: 7120 ± 6800 mg kg−1; CE-7Y: 4900 ± 1700 mg kg−1) compared with the degraded plot (CE-DM: 2000 ± 830 mg kg−1; Figure 5a). On the other hand, mean total S content in CE-MM (9200 ± 1300 mg kg−1) was significantly higher than those in replanted and degraded mangroves, and no significant differences were observed among CE-3Y, CE-7Y, and CE-DM (Figure 5a).
In the Rio de Janeiro coastal site, no significant differences were observed regarding total Fe and S contents among the studied plots (Figure 5a). Mean total Fe content in Rio de Janeiro ranged from 30,000 ± 5400 mg kg−1 in RJ-DM to 57,400 ± 16,900 mg kg−1 in RJ-7Y (Figure 5b). Total S contents varied between 10,000 ± 5900 (RJ-DM) and 29,300 ± 30,200 mg kg−1 (RJ-7Y; Figure 5b).

3.4. Mineralogical Characteristics (XRD and SEM Analyses)

The XRD diffractograms indicated that the mineralogical assemblage in mangrove soils from Ceará was mainly composed of quartz, whereas mangrove soils from Rio de Janeiro were mainly composed of quartz and kaolinite (Figure 6).
SEM micrographs of mangrove soils from Ceará revealed arrangements of poorly crystalline isolated microcrystals of authigenic euhedral pyrites in the replanted plots (represented by CE-7Y; Figure 7a). On the other hand, in the mature mangrove (CE-MM), authigenic framboidal pyrites were densely packed and homogeneous. Furthermore, the EDS spectra corroborated the presence of pyrite with chemical signals from Fe and S (Figure 7c,d).
In the Rio de Janeiro site, in RJ-MM, SEM micrographs showed the presence of smooth spherical authigenic pyrite framboids (Figure 8a) along with irregularly shaped kaolinite particles (Figure 8b). The SEM-EDS analysis corroborated this mineralogical assemblage by elemental composition (Fe, S, Si, O, Al, and K; Figure 8c–e).

3.5. Discriminant Analysis

The discriminant analysis revealed contrasting effects of revegetation in the study sites (Figure 9). In Ceará, there was an increase in SCS, DOP, fine particles (silt and clay), and S and Fe contents in mature and replanted mangrove plots (Figure 9a,b). In fact, these variables explained 81.91% of data variance, while Eh values and pyritic Fe explained only 12.80%. Conversely, in Rio de Janeiro, no apparent effects of revegetation were observed (Figure 9c,d). Nevertheless, the pyritic Fe, SCS, and DOP vectors in data from RJ-7Y indicated a higher value of these parameters in this plot than in others.

4. Discussion

4.1. Particle Size Distribution and Soil Carbon Stocks in the Different Replanted Plots

In the Ceará site, the dominance of sand in all plots is related to the surrounding soils and geological materials (i.e., sedimentary deposits from the Barreiras Formation), mainly with a sandy–clayey texture [40].
However, our results reveal a significant increase in fine particles from CE-DM to CE-7Y, with the highest contents observed in CE-MM (Figure 2). This increase in fine particles (clay + silt) with forest development is related to a higher particle trapping capacity by aerial roots, decreasing hydrological energy and favoring deposition [53,54]. This increase in fine particles was also significantly correlated to a gradual increase in SCS upon replanting (Figure 3a), which indicates an organic carbon accumulation promoted by an interaction with fine-grained mineral particles (silt and clay). Previous works have suggested that the sorption of organic matter to the surfaces of fine-grained minerals directly controls the accumulation and preservation of soil organic matter in coastal environments. These organic matter–mineral interactions are a product of the high surface areas of the mineral matrix [55,56]. This mechanism is corroborated by the discriminant analysis that shows a positive relation between vectors of fine particles and SCS (Figure 9).
On the other hand, in the Rio de Janeiro site, all mangrove soils showed naturally high contents of fine particles (clay and silt; Figure 2b) and SCS (Figure 3b). The absence of a gradual rise in fine particles associated with SCS in this site may be related to the presence of invasive species Acrostichum aureum (especially in the degraded and replanted plots). Acrostichum aureum is known for its dense root zone and, thus, for promoting both trapping of mineral particles and high organic matter inputs into soils [37,57]. Moreover, the Guanabara Bay is geographically constrained and marked by low hydrodynamic energies, decreasing dissolved carbon exportation towards the ocean [58,59].
The higher presence of fine particles in all plots in the Rio de Janeiro site also reflects the characteristics of the surrounding soils of the Serra do Mar scarps, which originate from granite–gneiss rocks and are rich in authigenic fine-grained minerals (silt and clay), such as kaolinite, gibbsite, and Fe oxyhydroxides [60]. This environmental context favors clay-rich mangrove soils (>50%), which contrast with those in the Ceará coast [44,61]. Indeed, XRD results (Figure 6) and SEM micrographs (Figure 8) of mangrove soils from Rio de Janeiro corroborate the higher presence of clay minerals in both degraded and revegetated plots. Furthermore, in Guanabara Bay, the semidiurnal tidal regime, with a range of 0.7 m (i.e., low hydrodynamic energy), favors fine particle deposition (e.g., clay minerals) and promotes the low export of suspended materials to adjacent areas [62,63]. However, in the Rio de Janeiro site a gradual increase of SCS was not observed, with no significant differences between RJ-MM and RJ-DM and higher values at the RJ-7Y plot (Figure 3). In mature mangroves, fauna activity plays a key role in the soil carbon dynamic [64,65]. Fauna activity, mainly macro- and mesofauna, acts on organic matter decomposition, firstly promoting the fragmentation of organic matter decreasing the contact area for subsequent decomposition by the microbiota [66]. In addition, fauna activity favors the O2 diffusion in mangrove soils through channels and burrows, which enhances the most energy-efficient aerobic decomposition of organic matter [65]. Indeed, the RJ-MM recorded the higher Eh values (+424 ± 197 mV; Table 1) among Rio de Janeiro plots.

4.2. Responses of Fe, C, and S Geochemistry to Revegetation: Implications for Soil Functions

Fe partitioning indicates evident changes in Fe and S geochemistry as the forest developed in both study sites. In mangrove soils from Ceará, the increase in total Fe contents and low-crystallinity Fe oxyhydroxides in replanted plots (CE-3Y and CE-7Y; Figure 4) favors pyritization, as corroborated by vectors of F6, DOP, and total Fe in replanted and mature mangroves (Figure 9a,b). Additionally, poorly crystalline Fe oxyhydroxides are more susceptible to reductive dissolution, a process coupled to pyritization [67,68,69,70]. The effects of a higher availability of Fe (e.g., reactive Fe) or Fe oxyhydroxides favoring pyritization have been widely reported in previous studies [71,72]. Although F6 contents were low in replanted plots compared with CE-MM, a significant increase was observed in DOP compared with the degraded plot (CE-DM; Figure 4c). The recovery of pyritization plays a key role in immobilizing contaminants in mangrove soils [17]. Pyrite is an important trace metal-binding phase within mangrove soils [16,17]; therefore, its presence is directly associated with the regulating pollutant removal service [73].
In addition, higher total Fe and Fe oxyhydroxide contents (within the fine particle fraction) directly affect SCS in replanted plots. This assumption is supported by the positive correlation among vectors of fine particles, total Fe, and SCS shown by the discriminant analysis (Figure 9b). Several recent studies have reported that poorly crystalline Fe oxyhydroxides (e.g., ferrihydrite and lepidocrocite) play an important role in preserving and accumulating soil organic matter in mangrove soils [74]. These works reported the formation of stable complexes between the functional groups in organic matter and those in poorly crystalline Fe oxyhydroxides [75,76,77]. In fact, a recent study conducted in this revegetated area revealed how the content of organic matter in degraded and newly replanted mangroves depends on organomineral interactions [78], probably with Fe oxyhydroxides.
Furthermore, annual SCS increases in replanted plots in Ceará (Figure 3a) are higher than values reported in other studies along the Brazilian coast, for example in Cananéia (1.9 Mg ha−1 year−1) [79] and Ilha Grande (2.0 Mg ha−1 year−1) [80]. Our findings also reveal a higher potential for carbon sequestration than the average estimates for mangroves reported by previous studies at different locations; e.g., 2.3 Mg ha−1 year−1 [81], 1.4 Mg ha−1 year−1 [82], 2.0 Mg ha−1 year−1 [83], and 3.0 Mg ha−1 year−1 [84]. Thus, SCS values in the Ceará replanted plots provide strong evidence for the recovery of geochemical processes and its impact on Fe, S, and C dynamics.
Similarly, in mangrove soils from Rio de Janeiro, an increase in Fe contents was observed as plants developed, mainly related to increases in low-crystallinity Fe oxyhydroxide (i.e., F3 + F4) and pyrite (i.e., F6; Figure 4b) contents. Despite the absence of significant differences in DOP values (Figure 4d), the higher pyritization in Rio de Janeiro (~50%) is probably related to the higher contents of reactive Fe available for reaction with dissolved sulfide (HS−) [85]. The high contents of pyrite-associated Fe (i.e., F6) indicate that sulfate reduction is the main anaerobic metabolism related to soil organic matter degradation at Rio de Janeiro [8,39,86]. In fact, in mangrove soils, microbial-mediated sulfate reduction is widely reported as a significant respiration pathway that favors soil organic matter accumulation [8,15]. Previous studies have shown that the high availability of reactive Fe forms favors pyritization and enhances soil organic matter contents [33,48,87].
Since sulfate reduction has a lower energy yield compared to other respiration pathways (e.g., reduction of NO3−, Mn3+, and Fe3+) [12,15], the rate of decomposition is considerably lower than the rate of organic matter input, leading to carbon-rich soils [77]. Furthermore, mangrove soils from Rio de Janeiro are mostly composed of clay minerals (e.g., kaolinite; Figure 6 and Figure 8), which have been reported to physically protect soil organic matter against microbial decomposition [76,88]. This physical protection and preservation of organic matter explain the high SCS in RJ-DM. In fact, the role of phyllosilicates in preserving soil organic matter has been previously reported and related to the establishment of organomineral associations [89]. In this case, phyllosilicates, such as kaolinite, and iron oxyhydroxides provide surface charges (both permanent and variable) and high-surface areas (>>in Fe oxyhydroxides) that contribute to organic matter adsorption (e.g., innersphere, outersphere, and H-bonding), resulting in its physical protection against decomposition [90]. Therefore, these mechanisms may be responsible for the high SCS recorded in the Rio de Janeiro site. In fact, the SCS in RJ-7Y (59.6 ± 15.2 Kg m−2; Figure 3b) was higher than the mean SCS reported for mangrove soils (up to 100 cm depth) in 15-year-old (48.3 Kg m−2) [91] and 20-year-old replanted plots (25.8 Kg m−2) [92].
In the Rio de Janeiro site, a combination of geoenvironmental settings (i.e., geology, geomorphology) and biological factors has led to the recovery of soil geochemical processes (e.g., sulfate reduction) and of SCS, positively impacting the soil functions of metal immobilization and carbon sequestration.

5. Concluding Remarks

Our findings suggest that mangrove reforestation initiatives are an effective strategy for recovering soil functions (i.e., carbon sequestration and metal retention) and their related ecosystem services (i.e., climate regulation and filtering of pollutants). Although soil response was variable in both study sites, increases in reactive Fe, pyrite, DOP, and SCS were observed in mangrove soils after replanting. The recovery of key soil processes (related to Fe, S, and C) directly affected the ability of these replanted mangroves to accumulate organic matter and potentially control bioavailability of pollutants (e.g., trace metals; Figure 10). In this sense, specific protocols for mangrove restoration initiatives [93,94,95] should consider the variability of factors such as soil texture, climate conditions, and geological surroundings, since these features directly affect the recovery of soil functions.
Understanding how the recovery of soil functions impacts the restoration of ecosystem services in replanted mangroves may help guide future restoration programs as a nature-based solution for achieving net-zero emission targets.

Author Contributions

T.O.F., G.N.N., D.J.R., L.C.Z.J. and H.M.Q. designed the field study. L.C.Z.J., D.J.R., H.M.Q., Y.D. and G.N.N. collected samples and performed laboratory analyses. L.C.Z.J. and H.M.Q. analyzed data. L.C.Z.J., H.M.Q., T.O.F., G.N.N., D.J.R. and X.L.O. wrote the paper. All authors participated in editing the paper. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Finance Code 001), National Council for Scientific and Technological Development (CNPQ; grant numbers 305996/2018-5 and 430010/2018-4 to TOF and 409593/2018-4 to GNN), the São Paulo Research Foundation (FAPESP; grant number 2021/00221-3 to HMQ), and the Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (grant number E-26/202.757/2019 to GNN).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

The authors would like to acknowledge the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), National Council for Scientific and Technological Development, São Paulo Research Foundation, and the Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro for their funding and scholarships.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Location of the studied mangrove forests in Ceará (NE-Brazil) (a) and Rio de Janeiro (SE-Brazil) (b). Different colored plots indicate the different studied scenarios, i.e., degraded and mature mangrove forests and plots at different stages of revegetation (3- and 7-year-old plantations). Satellite images were obtained with Google Earth ProTM.
Figure 1. Location of the studied mangrove forests in Ceará (NE-Brazil) (a) and Rio de Janeiro (SE-Brazil) (b). Different colored plots indicate the different studied scenarios, i.e., degraded and mature mangrove forests and plots at different stages of revegetation (3- and 7-year-old plantations). Satellite images were obtained with Google Earth ProTM.
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Figure 2. Particle size distribution in mature mangroves, degraded plots, and 3- and 7-year-old plantations in Ceará (a) and Rio de Janeiro (b). (c) Fine particle (silt + clay) contents in degraded, mature, and replanted mangrove forests from the Ceará and (d) Rio de Janeiro sites. Different lowercase letters indicate significant differences among fine particle contents found by the Kruskal–Wallis test at the 5% probability level, and k values above the critical k (7.8147) indicate statistical differences.
Figure 2. Particle size distribution in mature mangroves, degraded plots, and 3- and 7-year-old plantations in Ceará (a) and Rio de Janeiro (b). (c) Fine particle (silt + clay) contents in degraded, mature, and replanted mangrove forests from the Ceará and (d) Rio de Janeiro sites. Different lowercase letters indicate significant differences among fine particle contents found by the Kruskal–Wallis test at the 5% probability level, and k values above the critical k (7.8147) indicate statistical differences.
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Figure 3. Soil carbon stocks for the different stages of revegetation (DM; 3Y; 7Y; MM) in the Ceará (a) and Rio de Janeiro (b) mangrove forests. Different lowercase letters indicate significant differences among variables found by the Kruskal–Wallis test at the 5% probability level, and k values above the critical k (7.8147) indicate statistical differences.
Figure 3. Soil carbon stocks for the different stages of revegetation (DM; 3Y; 7Y; MM) in the Ceará (a) and Rio de Janeiro (b) mangrove forests. Different lowercase letters indicate significant differences among variables found by the Kruskal–Wallis test at the 5% probability level, and k values above the critical k (7.8147) indicate statistical differences.
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Figure 4. Fe partitioning (a,b) and degree of Fe pyritization, DOP (c,d) in all studied plots. Different lowercase letters indicate significant differences among variables found by the Kruskal–Wallis test at the 5% probability level, and k values above the critical k (7.8147) indicate statistical differences.
Figure 4. Fe partitioning (a,b) and degree of Fe pyritization, DOP (c,d) in all studied plots. Different lowercase letters indicate significant differences among variables found by the Kruskal–Wallis test at the 5% probability level, and k values above the critical k (7.8147) indicate statistical differences.
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Figure 5. Total Fe and S contents in all studied plots in Ceará (a) and Rio de Janeiro (b). Different lowercase letters indicate significant differences among variables found by the Kruskal–Wallis test at the 5% probability level, and k values above the critical k (7.8147) indicate statistical differences.
Figure 5. Total Fe and S contents in all studied plots in Ceará (a) and Rio de Janeiro (b). Different lowercase letters indicate significant differences among variables found by the Kruskal–Wallis test at the 5% probability level, and k values above the critical k (7.8147) indicate statistical differences.
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Figure 6. XRD data of nonoriented soil samples from both degraded and mature mangroves in the Ceará (a,b) and Rio de Janeiro (c,d) sites. Qz: quartz, K: kaolinite.
Figure 6. XRD data of nonoriented soil samples from both degraded and mature mangroves in the Ceará (a,b) and Rio de Janeiro (c,d) sites. Qz: quartz, K: kaolinite.
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Figure 7. SEM photomicrographs of pyrites found in mangrove soils from CE-7Y (* represents the exact surface from where the EDS spectra were obtained) (a) and CE-MM (b) and their corresponding EDS spectra (c–e). In CE-7Y (a), the SEM-EDS photomicrographs revealed arrangements of poorly crystalline isolated authigenic euhedral pyrites. Contrastingly, in CE-MM, the SEM-EDS photomicrographs revealed the presence of authigenic framboidal pyrites.
Figure 7. SEM photomicrographs of pyrites found in mangrove soils from CE-7Y (* represents the exact surface from where the EDS spectra were obtained) (a) and CE-MM (b) and their corresponding EDS spectra (c–e). In CE-7Y (a), the SEM-EDS photomicrographs revealed arrangements of poorly crystalline isolated authigenic euhedral pyrites. Contrastingly, in CE-MM, the SEM-EDS photomicrographs revealed the presence of authigenic framboidal pyrites.
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Figure 8. SEM photomicrographs of pyrite and kaolinite in mangrove soils from a mature mangrove (RJ-MM) in Rio de Janeiro (a,b) and their corresponding EDS spectra (c–e), (* represents the exact surface from where the EDS spectra were obtained). In RJ-MM, the SEM-EDS photomicrographs revealed morphologies of poorly crystalline smooth spherical authigenic pyrite framboids (a). In addition, the SEM-EDS photomicrographs showed the presence of irregularly shaped kaolinite particles (b).
Figure 8. SEM photomicrographs of pyrite and kaolinite in mangrove soils from a mature mangrove (RJ-MM) in Rio de Janeiro (a,b) and their corresponding EDS spectra (c–e), (* represents the exact surface from where the EDS spectra were obtained). In RJ-MM, the SEM-EDS photomicrographs revealed morphologies of poorly crystalline smooth spherical authigenic pyrite framboids (a). In addition, the SEM-EDS photomicrographs showed the presence of irregularly shaped kaolinite particles (b).
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Figure 9. Discriminant analysis data for the studied soil variables in the Ceará (a,b) and Rio de Janeiro (c,d) sites. The squares on the right represent the correlations among the soil parameters that compose the two discriminant functions. Fine particles: Σclay and silt; SCS: soil carbon stock; DOP: degree of pyritization.
Figure 9. Discriminant analysis data for the studied soil variables in the Ceará (a,b) and Rio de Janeiro (c,d) sites. The squares on the right represent the correlations among the soil parameters that compose the two discriminant functions. Fine particles: Σclay and silt; SCS: soil carbon stock; DOP: degree of pyritization.
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Figure 10. Schematic summary showing a conceptual model for the recovery of the studied soil functions upon mangrove revegetation. The development of mangrove forests led to an increase in organic matter input from vegetation and fine particle trapping (e.g., phyllosilicates and Fe oxyhydroxides), which contributed to increasing SCS. An increase in reactive Fe favors pyritization and, thus, the potential for pollutant immobilization. The recovery of these soil functions shows high potential for restoring the ecosystem services of climate regulation and filtering of pollutants.
Figure 10. Schematic summary showing a conceptual model for the recovery of the studied soil functions upon mangrove revegetation. The development of mangrove forests led to an increase in organic matter input from vegetation and fine particle trapping (e.g., phyllosilicates and Fe oxyhydroxides), which contributed to increasing SCS. An increase in reactive Fe favors pyritization and, thus, the potential for pollutant immobilization. The recovery of these soil functions shows high potential for restoring the ecosystem services of climate regulation and filtering of pollutants.
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Table
Table 1. Location, geoclimatic and physicochemical (pH and Eh) characteristics, tidal regime, and forest structure of studied mangrove forests from each plot.
Table 1. Location, geoclimatic and physicochemical (pH and Eh) characteristics, tidal regime, and forest structure of studied mangrove forests from each plot.
PlotLocation (UTM)Climate *Geological SurroundingsEhpHTidal RegimeForest Features
Ceará
DM562,638.15 m E
9,582,935.79 m S		BShSedimentary deposists+425 ± 28 mV7.0 ± 0.2Mesotidal
(0.75 to 3.25 m)		No vegetation
3Y562,577.33 m E
9,582,811.95 m S		BShSedimentary deposits+450 ± 16 mV7.0 ± 0.1Mesotidal
(0.75 to 3.25 m)		RM
7Y562,624.41 m E
9,582,661.79 m S		BShSedimentary deposists+437 ± 22 mV7.7 ± 0.3Mesotidal
(0.75 to 3.25 m)		RM
MM562,669.31 m E
9,582,785.29 m S		BShSedimentary deposists+21 ± 163 mV6.3 ± 0.1Mesotidal
(0.75 to 3.25 m)		AG, LR, and RM.
Rio de Janeiro
DM705,619.57 m E
7,486,388.30 m S		AfGranitic–gneissic rocks+250 ± 25 mV6.9 ± 0.2Microtidal
(0.1 to 1.2 m)		AG, LR, and RM.
3Y708,610.57 m E
7,487,890.50 m S		AfGranitic–gneissic rocks+340 ± 53 mV6.9 ± 0.1Microtidal
(0.1 to 1.2 m)		AG, LR, and RM.
7Y708,487.00 m E
7,488,109.00 m S		AfGranitic–gneissic rocks+408 ± 147 mV7.3 ± 0.3Microtidal
(0.1 to 1.2 m)		AG, LR, and RM.
MM707,915.30 m E
7,487,394.68 m S		AfGranitic–gneissic rocks+424 ± 197 mV7.2 ± 0.2Microtidal
(0.1 to 1.2 m)		AG, LR, and RM.
* According to Köppen climate classification. DM: degraded mangrove. 3Y: 3-year-old mangrove. 7Y: 7-year-old mangrove. MM: mature mangrove forests. BSh: semi-arid. Af: tropical humid. Avicennia germinans (L.) L.: AG. Laguncularia racemosa (L.) C. F.: LR. Rhizophora mangle L: RM.
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Jimenez, L.C.Z.; Queiroz, H.M.; Nóbrega, G.N.; Romero, D.J.; Deng, Y.; Otero, X.L.; Ferreira, T.O. Recovery of Soil Processes in Replanted Mangroves: Implications for Soil Functions. Forests 2022, 13, 422. https://0-doi-org.brum.beds.ac.uk/10.3390/f13030422

AMA Style

Jimenez LCZ, Queiroz HM, Nóbrega GN, Romero DJ, Deng Y, Otero XL, Ferreira TO. Recovery of Soil Processes in Replanted Mangroves: Implications for Soil Functions. Forests. 2022; 13(3):422. https://0-doi-org.brum.beds.ac.uk/10.3390/f13030422

Chicago/Turabian Style

Jimenez, Laís Coutinho Zayas, Hermano Melo Queiroz, Gabriel Nuto Nóbrega, Danilo Jefferson Romero, Youjun Deng, Xosé Luis Otero, and Tiago Osório Ferreira. 2022. "Recovery of Soil Processes in Replanted Mangroves: Implications for Soil Functions" Forests 13, no. 3: 422. https://0-doi-org.brum.beds.ac.uk/10.3390/f13030422

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