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Article

Spatiotemporal Variability in Soil Properties and Composition in Mangrove Forests in Baía de Todos os Santos (NE Brazil)

by
Monica Arlinda Vasconcelos Ramos
1,2,
Augusto Pérez-Alberti
1,*,
Gabriel Nuto Nóbrega
3 and
Xosé Luis Otero
1,4
1
CRETUS, Departamento de Edafoloxía e Química Agrícola, Facultade de Bioloxía, Universidade de Santiago de Compostela, 15705 Santiago, Spain
2
Centro de Ciências Agrárias, Ambientais e Biológicas (CCAAB), Universidade Federal do Recôncavo da Bahia, Cruz das Almas 44380-000, Brazil
3
Departamento de Ciências do Solo, Centro de Ciências Agrárias (CCA), Universidade Federal do Ceará, Fortaleza 60020-181, Brazil
4
Rede de Estación Bioloxicas, Rede de Estacións Biolóxicas da Universidade de Santiago de Compostela, Estación de Bioloxía Mariña da Graña (Ferrol), 15590 Ferrol, Spain
*
Author to whom correspondence should be addressed.
Land 2023, 12(7), 1392; https://doi.org/10.3390/land12071392
Submission received: 16 June 2023 / Revised: 4 July 2023 / Accepted: 6 July 2023 / Published: 12 July 2023
(This article belongs to the Section Soil-Sediment-Water Systems)

Abstract

:
Soil properties and components in mangrove ecosystems influence their geochemical processes and services. Despite the extensive mangrove areas present in Brazil, few studies focusing on these themes are under development. In this sense, this work aimed to investigate the spatial variability in soil attributes and composition, the geochemistry of Fe, and the isotopic characteristics of organic matter in mangroves in Baía de Todos os Santos (Cacha Prego, Ponta Grossa, Ilha de Maré, Pitinga), which constitutes Brazil’s second largest bay. The soils investigated showed spatial and temporal changes affecting their properties (pH, Eh) and composition (TOC, Fe fractions), as well as clear spatial changes in the redox potential values (+30–+188 mV), with higher values in PT. Soil textures ranged from predominantly sandy (CP, PT, PG: sand, >70%) to a finer granulometry (IM: sand, 33–64%). These characteristics influenced Fe partitioning and organic matter content, with higher TOC and pyrite values observed in IM (FeS2: 2720–9233 mg kg−1; TOC: 4.4–6.6%) and lower sulfide values found in PT, mainly in the dry season (FeS2: 85–235 mg kg−1). The soil δ13C and N/C ratios seem to suggest a mixed origin of organic matter.

1. Introduction

Mangrove forests are complex ecological assemblages composed of trees and shrubs adapted to grow in intertidal environments along tropical and subtropical coasts. Despite the wide consensus about their economic and societal value, more than 50% of the world’s mangroves have already been destroyed [1,2]. A considerable portion of the ecosystem services attributed to mangrove forests are closely linked with soil properties and composition, such as their ability to act as CO2 sinks or to regulate coastal water composition and quality [3,4,5].
Intertidal soils often show water saturation, high organic matter contents, fine textures, near-neutral pH, and redox conditions varying from suboxic to anoxic [6,7,8]. However, small variations in topography and in hydrological conditions lead to complex spatial variability in terms of the composition and properties of soils and sediments in these environments [9,10]. Additionally, these properties and compositions show significant seasonal changes in these environments, sometimes affecting soil and water quality, since these changes can increase the bioavailability of potentially toxic elements and substances [11,12].
Mangroves in Brazil occur along a coastline over 7000 km long, from the equatorial Amazon coast to the southern coast, showing variable forest patterns due to climatic and geologic variations [10,13,14]. Among the different Brazilian states, the state of Bahía has the longest coastline (932 km of coastline) and harbors the second largest bay in the country, Baía de Todos os Santos (BTS), 178 km2 of which is occupied by mangrove forests [15,16].
Studies carried out in the BTS have demonstrated the importance of mangroves for the maintenance of biodiversity, the production of coastal biomass, and the economy, promoting the development of fishing and shellfish-harvesting activities and tourism in its vicinity [17,18,19]. However, due to the intense industrialization and urbanization on their margins, these environments are threatened by chemical pollution by trace elements and organic pollutants [20,21,22]. A considerable number of publications have been devoted to studying mangroves in the BTS [15,17,18,19,21,22], but few works have addressed soil heterogeneity and seasonal changes [23,24], and to our knowledge, no studies have approached the spatiotemporal variability in mangrove soils in the BTS, and very few have focused on this aspect in the whole of Brazil. In this sense, this work aimed to investigate the spatial and temporal variability in soil composition, properties, Fe geochemistry, pyrite stability, and isotopic analyses of C and N in mangrove soils of the BTS.

2. Materials and Methods

This study was performed in Baía de Todos os Santos, characterized by a humid tropical climate with a mean annual temperature of 25.2 °C and a mean rainfall of 1900 mm/year. There is a dry season during the months of January to March (<150 mm/month), when maximum temperatures reach 30 °C and mean values are around 27 °C, while during the rainy season (April, May, and June), mean temperatures are around 24 °C and rainfall exceeds 300 mm/month [25,26]. A total of four mangrove forest sites were selected in Baía de Todos os Santos (BTS, Figure 1): two located at the entrance of the bay (Cacha Prego, CP, and Ponta Grossa, PG), in areas with a low degree of anthropic impact; another one located in the northeastern region (Ilha de Maré, IM), close to industrial areas and maritime ports; and another one in the northern region (Pitinga, PT), an area with a history of metal pollution associated with past metallurgical activity [21].
The selected sites showed different hydrodynamic conditions, with the IM site located in the middle of the BTS, in a more sheltered area with a lower degree of exposure to hydraulic energy. Mangrove sites CP and PG, located in Itaparica Island, were subjected to a higher influence of marine currents due to the higher speed of tidal currents at the entrance of Baía de Todos os Santos [27]. Finally, mangrove site PT, despite being located at the northern end of the BTS, far away from the Atlantic Ocean, is included within an estuarine area subjected to the influence of the Subaé River [27].
Mangroves in sites IM and CP were composed of single-species Rhizophora mangle (L.) forests, while PT and PG showed mixed forests composed of R. mangle and Laguncularia racemosa (L.). These sites were selected in order to cover different sections of the BTS to analyze potential spatial variations due to the different forest compositions and hydrodynamic characteristics of each site.
Soil and mangrove leaf samples were collected at low tide during the dry season (DS), between December 2020 and February 2021, and during the rainy season (WS), in the months of June and July 2021. For each site and season, 12 samples were collected from the soil surface layer (0–5 cm) and from the deep layer (15–30 cm); each sample was, in turn, composed of 3 subsamples, collected using stainless-steel corers. Additionally, twelve leaf samples were collected at each site; considering the representative species within each forest site, samples collected at CP and IM consisted of R. mangle leaves, while those collected at PG and PT consisted of R. mangle and L. racemosa leaves. Each composite sample consisted of 12 leaves from three different individual trees for each species.
Soil samples were characterized in terms of pH and Eh using an HI8424 portable pH meter (Hanna Instruments). The pH electrode was previously calibrated using pH 4 and pH 7 standards, while the Eh meter was tested using a 220 mV standard redox solution. Granulometry was determined by sifting through a 2 mm sieve to obtain the fine earth fraction, followed by a 0.05 mm sieve to separate the fine sand from the fine fraction (silt and clay particles) [28]. To calculate the water content, 5 g of each wet soil sample was dried in an oven at 60 °C for 48 h, following the method adapted from [29].
In soil and plant samples, total organic carbon (TOC%) and total nitrogen (TN%) were determined using an elemental analyzer (FlashEA1112), while isotopic ratios for carbon (δ13C) and nitrogen (δ15N) were determined using an elemental analyzer (FlashEA1112) coupled to a Delta V Advantage isotopic ratio mass spectrometer (ThermoFinnigan). Samples were weighed in tin capsules using a UMX-2 scale (Mettler Toledo), and the results for δ15N and δ13C were expressed in ‰ relative to atmospheric N air and VPDB (Vienna Pee Dee Belemnite), respectively. For each analytical sequence, the following secondary patterns were used for δ15N: USGS 40 (−4.52‰), USGS41a (+47.55‰), IAEA-N-1 (+0.4‰), IAEA-N-2 (+20.3‰), and USGS-25 (−30.4‰). For δ13C, the following were used: USGS 40 (−26.39‰), USGS41a (+36.55‰), NBS 22 (−30.031‰), and USGS 24 (−16.049‰). To evaluate the precision (standard deviation), acetanilide was used as a standard, yielding a value of ±0.15‰ (n = 10). All soil samples had been previously subjected to an acid attack using 10 mL HCl (1N) to remove carbonates. After adding the acid solution, samples were shaken for 1 h, then centrifuged to remove HCl, washed five times in deionized water, and dried in an oven at 60 °C, following the method adapted from [30]. Leaf samples were washed in distilled water several times to remove all adhered material. All the analyses were performed by the Research Support Services (Servizos de Apoio á Investigación, SAI) of the University of A Coruña.
Fe content was determined using 0.5 g of ground sample, digested using 9 mL nitric acid (HNO3 65%) and 3 mL ultrapure hydrochloric acid (HCl 37.5%) in a closed-system microwave digestor (Milestone; ETHOS EASY); determination was carried out on an atomic absorption spectrometer (Perkin Elmer, Waltham, MA, USA). The analytical method employed was validated using a certified reference material for soil (SO-3, Canadian Certified Reference Material Project, Canada), with an iron recovery rate of over 87%. Sequential extraction of metallic phases was performed using the BCR method [31] and the sequence proposed by [32], as described below:
-
F1, soluble fraction, exchangeable and associated with carbonates (ExCa): Briefly, 30 mL acetic acid (0.11 mol L−1; pH = 4.5) was added to each sample (2 g wet sample); samples were then shaken at 25 °C for 16 h. After shaking, samples were centrifuged to remove the supernatant (fraction 1), washed in ultrapure deoxygenated water with bubbling N2 for 10 min, and then centrifuged again, a procedure that was repeated before each subsequent stage.
-
F2, fraction associated with amorphous iron oxides (Am): Briefly, 20 mL of solution containing 20 g ascorbic acid +50 g sodium citrate +50 g bicarbonate +1 L ultrapure deoxygenated H2O and N2 at pH 8 was added to the residue of the previous fraction. Samples with the solution were shaken at 25 °C for 24 h and were subsequently centrifuged to collect the washed extract.
-
F3, fraction associated with crystalline iron oxyhydroxides (Cri): briefly, 20 mL of solution containing 73.925 g sodium citrate +9.24 g NaHCO3 in 1 L ultrapure H2O and 3 g sodium dithionite was added to each sample, then shaken for 30 min at 75 °C, and finally centrifuged to collect the washed extract.
-
F4, reduced forms associated with organic matter and oxidizable sulfides (Red): Briefly, 10 mL of H2O2 (8.8 M) was added to each sample and warmed in a bath at 85 °C until evaporation down to 3 mL, followed by a second addition of 10 mL of H2O2. Samples were kept warm (in a bath at 85 °C) until evaporation down to 1 mL, at which point 50 mL of AcNH4 solution was added and samples were shaken for 16 h at 25 °C.
The residual fraction (FR) value was calculated from the difference between the total concentration after microwave digestion and the sum of bioavailable fractions (∑ F1 → F4). Contents in each fraction were analyzed via atomic absorption spectrometry (AAS).
To extract pyrite, 10 g of wet soil sample from each site was freeze-dried for 48 h and then gently disaggregated using an agate mortar [33]. Pyrites were separated by density inside a fume hood using bromoform (ρ = 2.89 g cm−3) and subsequently washed in acetone and analyzed under a field-emission scanning electron microscope (FESEM, Ultra-Plus, Zeiss, Jena, Germany).
The results were analyzed using descriptive statistics (Sigmaplot 12.0), and a Kruskal–Wallis non-parametric test was applied at a p < 0.05 level of significance (XLSTAT 2014) to compare the results obtained from the different study sites. This non-parametric test was selected due to its higher robustness and lower statistical assumption requirements [34].

3. Results

3.1. Physicochemical Characterization of Soils

Sand contents ranged from 43.7% to 89.8%, with soils from IM (silt + clay: 52.4 ± 8.6%; Figure 2) showing a significantly finer texture than the remaining sites both in the surface and deep layers (Figure 2). Site CP (fine fraction: 22.6 ± 3.1%) showed a significantly finer texture in the deep layer than the remaining two sites: PT (11.9 ± 3.6%) and PG (10.6 ± 2.4%).
The water content varied between 24% and 153%, with significantly higher values in IM (85–153%, mean: 109 ± 16%) than in the remaining sites during both the dry and rainy seasons (Figure 3). No common patterns related to depth or seasonality were observed for the water content.
During the dry season (DS), pH varied between 4.5 and 7.4 (Figure 4), with PT soils ranging from highly to moderately acidic (range: 4.5–6.2), while values in the remaining areas were near-neutral, ranging between 6.9 and 7.4. In the rainy season (WS), pH varied between 6.6 and 7.7, with mean values approaching neutrality in all sites (Figure 4). Variations according to depth were observed during the rainy season in the PT mangrove and in the two seasons in IM, with the lowest pH values found in the surface soil layer. As for seasonality, only PT showed significant differences, with more acidic values in the dry than in the rainy season.
Eh during the rainy season ranged from +92 mV to +188 mV (Figure 4), with mean values typical of suboxic soils in all the mangroves (generally Eh < 300 mV) [35] except for IM, where the conditions in the deep soil layer were predominantly anoxic (+93 ± 6 mV). Eh values during the rainy season were generally lower than those observed during the dry season (range: 30 to 155 mV), mainly corresponding to suboxic conditions in the surface layer and anoxic conditions in the deep layer in IM, PG, and CP (IM: 93 ± 27 mV; PG: 96 ± 15 mV; CP: 90 ± 31 mV). Seasonal differences were observed both for the surface and deep soil layers in IM, while for PT, they were only observed in the deep layer. Vertical variations were only observed in IM, with the highest values found in surface soils for both seasons. Eh showed significant spatial differences, with the highest values in the PT mangrove in both seasons.

3.2. Soil Composition: Total Organic Carbon (TOC), Total Nitrogen (TN), C/N Ratio, and Isotopic Ratios

Value ranges for TOC and TN were 0.75–6.59% and 0.03–0.35%, respectively, with the highest contents in IM soils; these parameters showed a strong positive correlation (r = 0.84; p < 0.001) (Table 1). No seasonal differences or variations according to depth were observed, except in the case of IM during the dry season, where the highest contents were found in surface soils (TOC: 6.01 ± 0.58%; TN: 0.32 ± 0.03%). C/N ratios varied between 17.3 and 31.6, with no seasonal or spatial differences. Differences according to depth were only observed in IM during the dry season, with higher values in the deep layer.
The values for δ13C ranged from −28.4‰ to −25.6‰, with no seasonal differences but with significant spatial variations for the two periods. Thus, during the dry season, values in PT soils (15–30 cm depth: −27.40 ± 0.54‰) were significantly lower than in PG (−26.16 ± 0.16‰). During the rainy season, the contents in surface soils were also lower in PT than in PG, as well as being lower than those observed in the deep soil layer of the remaining sites. Differences between depths were only observed in IM during the rainy period, with the lowest values in the surface soil layer.
The isotopic ratio for δ15N ranged between 0.3‰ and 3.8‰. The values observed in PG during the dry season in the surface soil layer and during the rainy season in the deep soil layer were significantly lower than those found in the remaining sites. No differences between depths or seasonal variations were found.

3.3. Leaf Composition: Total C, TN, C/N, δ13C, and δ15N

The C and N contents in plants ranged from 36.7% to 42.5% and from 0.7% to 1.4% (Table 2), respectively, with no spatial variations. However, they showed significant differences between species in PT, with Rhizophora mangle leaves (total C: 41.5 ± 0.5%; total N: 1.3 ± 0.2%) showing significantly higher values than Laguncularia racemosa leaves (total C: 40.5 ± 0.3%; N total 1.0 ± 0.2%). C/N ratios ranged from 30 to 54 and showed no differences among sites, but they did show variations between species in PT, with significantly higher values for L. racemosa.
δ13C and δ15N ratios varied between −30.6‰ and −28.6‰ and between 0.4‰ and 3.3‰, respectively, again with differences between species in the PT mangrove, where δ13C values were higher for R. mangle, while δ15N was higher for L. racemosa.
The values for δ13C in R. mangle showed spatial variations, with poorer levels in IM and CP, while the opposite pattern was observed for δ15N. As for L. racemosa leaves, differences among sites were only observed for δ15N, with the values in PT (2.93 ± 0.32‰) being significantly higher than those in PG (1.83 ± 0.12‰).

3.4. Total Fe and Geochemical Partitioning in Soils

Total Fe varied between 0.10% and 2.8% and showed no differences according to soil depth (Figure 5), but it did show significant spatial variations, with the highest values corresponding to IM soils, both during the dry (0–5 cm: 2.3 ± 0.5%; 15–30 cm: 2.6 ± 0.1%) and the rainy season (0–5 cm: 2.3 ± 0.5%; 15–30 cm: 2.6 ± 0.1%). Contents in CP during the rainy season (0–5 cm: 1.3 ± 0.3%; 15–30 cm: 1.2 ± 0.2%) were also higher than those found in PT and PG for both depth levels. Seasonal differences were only observed for the deep soil layer in sites IM and CP, where the contents were higher during the rainy season.
The majority of non-residual Fe was present in the form of crystalline oxyhydroxides (FeCri) and associated with the reduced fraction (FeRed), except in PT during the dry season, where the contents were similarly distributed among fractions FeAm, FeCri, and FeRed (Table 3). The FeExCa and FeAm contents ranged from 2.40 to 133 mg kg−1 and from 0.30 to 944 mg kg−1, respectively, and were higher in IM and CP, while the FeCri contents were generally higher in IM except for the values observed in the surface soil layer during the rainy season in this site, which did not differ from the concentrations found in CP and PG. FeRed was higher in IM and CP, with the exception of the surface soil layer during the dry season.
Seasonal variations were only observed in the CP mangrove, where the FeExCa concentrations in the deep layer were higher during the dry season. Regarding depth, differences were observed for the FeAm (rainy season) and FeCri (dry season) contents in IM, where the values found in surface soils (FeAm: 356 ± 90 mg kg−1; FeCri: 1828 ± 181 mg kg−1) were higher than those in deep soils (FeAm:107 ± 53 mg kg−1; FeCri: 1154 ± 76.8 mg kg−1), as well as being higher than the FeRed contents in PT (rainy season), which were significantly higher in the deep layer (1721 ± 853 mg kg−1).

3.5. Pyrite Morphology

A total of 51 pyrites of different morphologies were identified via FESEM. Pyrite crystals were present in soils in three main morphologies (Figure 6): isolated euhedral crystals, forming framboids (aggregations of pyrite crystals), and polyframboids (aggregations of framboids). Isolated crystals were generally smaller than 1 µm (mean size: 1.1 ± 0.9 µm; range: 0.10–2 µm); most framboids were 10–25 µm in size; and polyframboids showed markedly larger sizes, generally between 50 and 75 µm (Figure 7, Figure 8 and Figure 9).
Individual pyrite crystals (28 occurrences) showed a predominantly octahedral habit (Figure 7E–G) in all mangrove sites, with truncated octahedral crystals only found in IM (Figure 7C,D). Isolated crystals with signs of degradation were identified in PT and PG, including the presence of perforations and poorly defined vertices (Figure 7F–H).
Framboids were mainly spherical in shape, although subspherical shapes were also recorded, as well as some aggregates with an undefined shape, mostly constituted by uniformly sized crystals. However, one framboid found in PT showed microcrystals of different sizes from those of crystals forming the aggregate; these microcrystals were present on the surface and had an undefined habit (Figure 8D). Crystals present in framboids showed variable habits: octahedral, truncated octahedral, and cubic (Figure 8). Except for IM, framboids with signs of degradation were observed in all mangrove sites, including alterations in shape (Figure 9A), the presence of perforations, and poorly defined vertices (Figure 9B–D).

4. Discussion

4.1. Spatiotemporal Heterogeneity in Mangrove Soils

Intertidal environments are considered highly dynamic biogeochemical environments whose acid–base and redox conditions can oscillate widely from hyperacidic (pH < 3.5) to neutral (pH~6.5), and from anoxic (Eh < 100 mV) to oxic (Eh > 400 mV) [10]. In mangrove soils, these changes are mainly driven by hydroperiod dynamics, which encompass all components of the water budget (rainfall, evaporation, and subsurface and surface flow). Seasonal changes are one of the main environmental factors in terms of their influence on edaphic and biogeochemical processes in soils of intertidal environments such as mangrove forests [10,11]. In tropical and subtropical areas, two seasons (dry and rainy) can mainly be differentiated, with the drastic changes in temperature and rainfall between them substantially affecting water availability in ecosystems; such is the case of the BTS [25,26].
Consistent with the complex interaction among factors regulating sedimentary and biogeochemical processes in coastal environments, soils in the BTS showed spatial differences affecting both their composition and their properties. A granulometric composition is a clear example of spatial variability, with differences in particle size according to the different sedimentary conditions along the coastal area [36,37]. Mangroves in PT and PG are close to river mouths, while CP is close to the Atlantic Ocean; both are high-energy environments, which can explain the higher proportion of the sand fraction in these areas [27,37]. Conversely, IM is located in the middle of the BTS and is therefore more sheltered from wave action and marine and river currents [27].
Acid–base conditions showed spatial and seasonal changes. Acidic conditions in mangrove soils during the rainy season were close to neutrality, which is consistent with the reduction processes that are typical of flooded soils, leading to the consumption of protons, particularly associated with the reduction of Fe oxyhydroxides and sulfates (Reactions 1 and 2) [6,8].
4FeOOH + CH2O + 7H+ → 4Fe2+ + HCO3− + 6H2O
CH3-COOH + SO42− + H+ → 2CO2 + 2H2O + HS
Conversely, a different spatial pattern was observed during the dry season, with significant differences among mangrove sites and with soils ranging from highly acidic in PT to neutral in the remaining sites. The higher acidity and Eh in PT soils are consistent with their lower water saturation (Figure 3), which promotes soil aeration. Additionally, the more sandy texture observed in PT soils, together with the higher relief related to the riverbed, promotes faster drainage and higher levels of soil aeration, with the subsequent oxidation of Fe sulfides according to Reactions 3 and 4, leading to proton release and decreased pH [9,13]. Moreover, the small size observed for many isolated pyrite crystals (<1 µm, Figure 7) provides them with a large specific surface area and a high reactivity, promoting their rapid oxidization.
FeS2 + H2O + 7/2 O2 → Fe2+ + 2SO42− + 2H+
FeS2 + O2 + 3/2 H2O → Fe2+ + SO42− + 2H+
The presence of a large number of degraded pyrites with signs of alteration in this mangrove site, as well as the low contents of Fe associated with the reduced fraction (FeRed) during the dry season, confirmed the pattern observed for pH and Eh and suggested a higher oxidative dissolution of sulfates (FeS and FeS2) in this area, mainly during the period with lower water availability (Reactions 3 and 4) [6,33].

4.2. Variation in Organic Matter Composition in Mangrove Soils

Mangrove soils are currently recognized as one of the marine ecosystems that store the greatest amounts of organic C (over 900 Mg ha−1), known as blue carbon [3]. In our case, the content of organic C stored in mangrove soils showed great spatial variability, with mean TOC values ranging from 1.0% to 6.0% (Table 1). The high spatial variability systematically observed in the organic C content in mangrove soils is particularly relevant to estimating the global C stock stored in marine ecosystems [10,38].
However, the origin of organic C stored in mangrove soils and sediments is still poorly known. Depending on local conditions, organic carbon entering mangrove soils is either produced autochthonously or imported by tidal currents and/or rivers. Mangrove litter and benthic microalgae are usually the most important autochthonous carbon sources, while phytoplankton and seagrass detritus imported by tidal currents may represent a significant supplementary carbon input in other circumstances [5,39].
Our results agree with those obtained by previous studies in that the specific characteristics of each study area play an essential role in organic C contents in mangrove soils. Thus, the highest TOC values observed in the IM site (6.0 ± 0.5%) are consistent with an environment with a high sedimentary rate due to its lower energy promoting the deposition of fine particles (silt and clay) and presumably also organic matter [3,27]; at the same time, minerals in the clay fraction exert a protective effect against the microbial degradation of organic matter [40].
Comparing the TOC contents with the results observed in other mangrove forests in Brazil, the mean values in IM were higher than the mean contents found in northeastern Brazil (2.2 ± 1.5%) [11], but lower than those found in southeastern Brazil (4.0–25% [6]), (6.9± 7.1% [13]), as well as being lower than the values recorded for mangroves in other regions of the world, such as New Caledonia (2–17%) [41], Indonesia (16.4 ± 2.1) [42], and Venezuela (14.5 ± 0.71%) [43]. This is consistent with the fact that the organic matter content in mangrove forests depends on a wide range of factors (coastal morphology, type of vegetation, soil properties and composition, etc.) that define the coastal environmental setting [38,44].
In our case, the observed TOC contents also showed differences depending on forest composition, with the highest contents in areas colonized by R. mangle (IM and CP) compared with areas occupied by mixed mangrove forests (PG and PT). Differences in TOC values according to the species composition of mangrove forests have also been observed in other studies, with enriched contents in soils occupied by R. mangle [41,43], which could be associated with the more developed root system of this species [41], as well as differences in biomass and in carbon transformation processes [43,45,46].
Most of the organic C contained in mangrove soils is generally associated with autochthonous sources, such as detritus from mangroves and roots, as well as benthic microalgae [5,47]. δ13C values in the soil (δ13C: −26.9 ± 0.6‰) were higher than those observed in plants (δ13C: −29.4 ± 0.5‰), unlike the C/N ratios (soil: 22.8 ± 3.4; leaves: 40.9 ± 6.8), which were higher in the leaf tissue. The observed differences suggest a progressive 13C enrichment of organic matter and C depletion in CO2 [48,49]. On the other hand, the joint analysis of the δ13C and C/N ratios suggests that part of the organic matter could have an allochthonous origin, mainly associated with terrestrial plants with C3 metabolism (Figure 10) [42,50,51].
Phytoplankton and marine algae are more enriched in the heaviest C isotope (13C), leading to a higher δ13C ratio, with values ranging from −23‰ to −17‰; this is due to the origin of the C used in marine photosynthesis, both from CO2 (lower δ13C) and from HCO3- (higher δ13C), while terrestrial plants use only atmospheric CO2, therefore showing lower δ13C values [50,51]. Isotope patterns and N/C ratios in soils from the BTS were similar to those found in Tanzania [47] and India [52], but different from the patterns observed in Saudi Arabia [53], where organic matter showed a greater contribution from phytoplankton and C4 plants (Figure 10).

4.3. Spatiotemporal Variability in Geochemical Forms of Fe in Mangrove Soils

Mangroves are located in the transition zone between terrestrial and marine environments, and despite the narrow strip they occupy within coastal areas, they experience spatial changes in their characteristics, particularly in those affected by flooding, such as redox processes, which in turn affect the geochemical forms of redox-sensitive elements (e.g., Fe, S). Geochemical Fe partitioning revealed clear differences among sites, with higher values for all fractions in IM. The high contents found in IM could be explained by the lower energy of the system, which promotes the deposition of small-sized particles (clay and silt) and metal and organic colloids [54,55]. The anoxic conditions also promote Fe precipitation and sulfate formation, mainly as pyrite [8].
The results showed clear spatial differences in the concentrations of the different forms of Fe, while seasonal differences were not as evident, particularly in the deep layer. At the spatial level, it is worth highlighting that crystalline Fe oxyhydroxides and pyritic Fe were the dominant forms of Fe across all mangrove sites, accounting for 23.6 ± 3.8% and 70.0 ± 3.8%, respectively, of potentially reactive Fe in CP, PG, and IM. Meanwhile, the distribution pattern in PT was different during the dry season, with reactive Fe mainly present in the amorphous oxyhydroxide (38.5 ± 10.5%) and crystalline oxyhydroxide phases (41.0 ± 14.7%), while pyritic Fe accounted for 17.3 ± 10.4% of non-residual Fe.
Pyrite shows high stability under reduced conditions [8]; however, the observed redox conditions and the presence of degraded pyrites in most mangrove sites suggest their instability and oxidization to Fe oxyhydroxides (Figure 11). In intertidal environments, Fe sulfates, and especially pyrite, are subjected to intense recycling as a result of the alternating oxic and anoxic conditions experienced by these soils due to seasonal changes affecting water availability in the system, as well as biological activity [35].
Amorphous Fe oxyhydroxides represent less than 9% of reactive Fe, with a clear decrease during the rainy season, consistent with the lower thermodynamic stability of this fraction under prolonged flooding conditions, as well as the rapid microbial reduction of these Fe forms in suboxic and anoxic environments compared with crystalline Fe oxyhydroxides [56,57,58,59]. Crystalline Fe oxyhydroxides, in turn, experience an increase during the dry period as a result of pyrite oxidization, a process that initially leads to amorphous oxyhydroxides, with the subsequent generation of crystalline forms within a relatively short period [56].
Soluble or exchangeable Fe forms (range: 12.4–133.0 mg kg−1) represented 2.1 ± 1.9% of the non-residual content. This fraction corresponds to Fe2+, which is highly unstable in mangrove soils due to fluctuations in redox conditions, being rapidly consumed under oxic conditions and precipitating as Fe (III) oxyhydroxides, while under anoxic conditions, it is consumed to form sulfates as a result of the predominance of sulfate and Fe reduction pathways [58,59]. The Eh–pH conditions observed for most samples suggest a higher stability of Fe oxyhydroxides, with the most stable Fe2+ found in the PT mangrove, where the system reaches highly acidic conditions (Figure 11). The higher Fe2+ values observed in IM could correspond to low-crystallinity FeS forms solubilized during the first extraction step, according to the reaction
FeS +H+ → Fe2+ + HS
The mainly suboxic redox conditions observed in these mangrove forests are consistent with the results obtained for mangroves within the BTS [24] and in other regions in northeastern Brazil [13], and these can be related to climatic conditions [33], as well as the shallow depth at which the samples were collected (0–30 cm), where bioturbation associated with plants and crabs contributes to soil oxygenation, leading to pyrite destruction [5,33,35].
Pyrites occurred mainly as framboids and isolated crystals, consistent with the results found in other reducing marine environments [33,58,60], with crystals showing a mainly octahedral habit and generally being found in soils with high sulfur contents [61]. Crystals of a cubic habit were only observed in IM, which could be associated with the higher Fe content in soils of this area [62]. Octahedral, pyritohedral, and cubic habits are among the most commonly observed in pyrites, which can also occur in intermediate forms, such as the truncated octahedral form found in IM. Differences in habits are associated with differences in pyrite growth conditions, which vary among mangrove forests and are influenced by granulometry, organic matter content, and nutrient availability [63].
A large portion of pyrites showed signs of degradation, including perforations, shape alterations, and poorly defined crystal vertices, with smaller framboid sizes (1.9 ± 1.9 µm) than those observed in other coastal systems in Brazil [64] and worldwide [33,60], which may suggest alternating redox conditions during their formation and growth periods [65]. Moreover, the presence of these alterations indicates the occurrence of degradation by oxidization in these areas, associated with the role of tidal fluctuations and bioturbation in the alteration of redox conditions [33,35].
The lower stability of pyrites in these mangroves in the face of oxidative processes could also have been favored by their small size, which leads to higher reactivity. In addition, the presence of a large proportion of crystals of an octahedral habit supports their greater instability, as they are subjected to weathering to a greater degree due to their mineral facet {111}, compared with faceted crystals {100}, such as cubic ones [66].
Figure 11. Eh–pH diagram showing the mineral stability of the Fe-S-O-H system in mangroves in the BTS [67].
Figure 11. Eh–pH diagram showing the mineral stability of the Fe-S-O-H system in mangroves in the BTS [67].
Land 12 01392 g011

5. Conclusions

The soil parameters and components showed spatial heterogeneity, with differences affecting soil attributes and composition. The environments identified within the BTS ranged from strongly reduced ones, associated with low-energy areas with higher deposition of finer fractions and organic matter, to mangroves with a predominantly sandy texture, which promotes aeration and favors the stability of Fe (III) oxyhydroxides to the detriment of pyrite. On the other hand, the physicochemical conditions of soils, results from sequential extraction, and electron microscopy images seem to suggest that pyrites are found in conditions of instability, with the exception of those in Ilha de Maré (IM), where pyrites showed well-developed habits.
Organic matter in mangrove soils seems to have a mixed origin, both associated with local (autochthonous) and allochthonous terrestrial production, with a low contribution from phytoplankton and seaweed. Seasonal changes also contribute to increasing the heterogeneity and complexity of geochemical processes in mangrove soils within the BTS, while no clear general pattern can be observed for all the study sites.
The seasonal differences in soil properties and composition did not show any common pattern. However, the clear spatial variations indicate different edaphic conditions in the studied mangroves, suggesting different capacities to provide ecosystem services, mainly those associated with carbon sequestration and storage, and with pollutant immobilization.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/land12071392/s1, Figure S1: Surface chemical composition of pyrite from mangrove soils of Ilha de Maré; Table S1: Physicochemical attributes and soil composition in mangroves in Ilha de Maré, Ponta Grossa, Pitinga and Cacha Prego.

Author Contributions

Conceptualization, M.A.V.R., A.P.-A., G.N.N., and X.L.O.; methodology, M.A.V.R., A.P.-A., G.N.N., and X.L.O.; software, not applicable; validation, M.A.V.R., A.P.-A., G.N.N., and X.L.O.; formal analysis, M.A.V.R., A.P.-A., G.N.N., and X.L.O.; investigation, M.A.V.R., A.P.-A., G.N.N., and X.L.O.; resources, M.A.V.R., A.P.-A., G.N.N., and X.L.O.; data curation, M.A.V.R., A.P.-A., G.N.N., and X.L.O.; writing—original draft preparation, M.A.V.R., A.P.-A., G.N.N., and X.L.O.; writing—review and editing, M.A.V.R., A.P.-A., G.N.N., and X.L.O.; visualization, M.A.V.R., A.P.-A., G.N.N., and X.L.O.; supervision, X.L.O.; project administration, X.L.O.; funding acquisition, X.L.O. All authors have read and agreed to the published version of the manuscript.

Funding

This research was co-funded by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) do Ministério da Ciência, Tecnologias e Inovações do Brasil, project titled “Desenvolvimento do Índice de Qualidade das Florestas de manguezais na Baía de Todos Santos (BTS), Bahia” (n° 441389/2017-1), and the Consellería de Educación, Universidade e Formación Profesional-Xunta de Galicia (Axudas á consolidación e estruturación de unidades de investigación competitivas do SUG do Plan Galego IDT, Ambiosol Group ref. ED431C; 2022/40).

Data Availability Statement

Most of the results are presented in the tables of the manuscript and in the Supplementary Material. The results with which the figures have been elaborated can be requested directly from the corresponding author (augustoperezalberti@gmail.com) or from M.A.V.R. (monica.ramos@ufrb.edu.br).

Acknowledgments

Thanks are due to María José Santiso for her assistance with the laboratory work.

Conflicts of Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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Figure 1. Map showing the locations of sampling sites in mangroves within Baía de Todos os Santos (BTS). Sites IM and CP correspond to single-species Rhizophora mangle forests, while PT and PG are mixed R. mangle and Laguncularia racemosa forests.
Figure 1. Map showing the locations of sampling sites in mangroves within Baía de Todos os Santos (BTS). Sites IM and CP correspond to single-species Rhizophora mangle forests, while PT and PG are mixed R. mangle and Laguncularia racemosa forests.
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Figure 2. Percentages of sand and fine fraction (silt and clay) in mangrove soils from Ponta Grossa (PG, n = 6), Cacha Prego (CP, n = 6), Ilha de Maré (IM, n = 6), and Pitinga (PT, n = 6). For each depth ((A): 0–5 cm; (B): 15–30 cm), lowercase letters indicate significant differences (p < 0.05) in granulometric composition among sites, while (*) indicates significant differences between depths within the same site (p < 0.05); ns indicates that variations between depths within the same site were not significant (p > 0.05).
Figure 2. Percentages of sand and fine fraction (silt and clay) in mangrove soils from Ponta Grossa (PG, n = 6), Cacha Prego (CP, n = 6), Ilha de Maré (IM, n = 6), and Pitinga (PT, n = 6). For each depth ((A): 0–5 cm; (B): 15–30 cm), lowercase letters indicate significant differences (p < 0.05) in granulometric composition among sites, while (*) indicates significant differences between depths within the same site (p < 0.05); ns indicates that variations between depths within the same site were not significant (p > 0.05).
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Figure 3. Water content in mangrove soils from Pitinga (PT), Ilha de Maré (IM), Ponta Grossa (PG), and Cacha Prego (CP) in the surface (n = 12; 0–5 cm) and deep (n = 12; 15–30 cm) soil layers during the dry (DS) and rainy (WS) seasons. For each season (DS and WS), different letters indicate significant differences among sites and between depths (p < 0.05), while (*) indicates significant differences between depths within the same site (p < 0.05). Black balls represent outliers.
Figure 3. Water content in mangrove soils from Pitinga (PT), Ilha de Maré (IM), Ponta Grossa (PG), and Cacha Prego (CP) in the surface (n = 12; 0–5 cm) and deep (n = 12; 15–30 cm) soil layers during the dry (DS) and rainy (WS) seasons. For each season (DS and WS), different letters indicate significant differences among sites and between depths (p < 0.05), while (*) indicates significant differences between depths within the same site (p < 0.05). Black balls represent outliers.
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Figure 4. Spatial and seasonal variations in pH and Eh (PT: Pitinga; IM: Ilha de Maré; PG: Ponta Grossa; CP: Cacha Prego) in the surface (0–5 cm) and deep (15–30 cm) soil layers. For each season (dry season, DS, and rainy season, WS), different letters indicate spatial differences both between depths and among sites, while (*) indicates significant seasonal differences within each site and depth.
Figure 4. Spatial and seasonal variations in pH and Eh (PT: Pitinga; IM: Ilha de Maré; PG: Ponta Grossa; CP: Cacha Prego) in the surface (0–5 cm) and deep (15–30 cm) soil layers. For each season (dry season, DS, and rainy season, WS), different letters indicate spatial differences both between depths and among sites, while (*) indicates significant seasonal differences within each site and depth.
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Figure 5. Total Fe content (%) in surface (0–5 cm) and deep (15–30 cm) mangrove soils in the BTS, both during the dry (DS) and rainy (WS) seasons. For each season, different letters indicate differences among sites (p < 0.05), while (*) indicates seasonal variations.
Figure 5. Total Fe content (%) in surface (0–5 cm) and deep (15–30 cm) mangrove soils in the BTS, both during the dry (DS) and rainy (WS) seasons. For each season, different letters indicate differences among sites (p < 0.05), while (*) indicates seasonal variations.
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Figure 6. Distribution of different pyrite morphologies in mangrove soils in the BTS.
Figure 6. Distribution of different pyrite morphologies in mangrove soils in the BTS.
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Figure 7. Isolated pyrite crystals from mangrove soils in the BTS.
Figure 7. Isolated pyrite crystals from mangrove soils in the BTS.
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Figure 8. Microphotographs of pyrite framboids from mangrove soils in the BTS: (A,B) individual framboids composed of octahedral crystals from the Ponta Grossa and Ilha de Maré sites; (C) individual framboid from the Ponta Grossa site, with a poorly defined shape, composed of octahedral crystals; (D) framboid from the Pitinga site, with the presence of microcrystals; (E) subspherical framboid from Ilha de Maré, composed of octahedral crystals; (F) individual framboid from Ilha de Maré, composed of cubic crystals.
Figure 8. Microphotographs of pyrite framboids from mangrove soils in the BTS: (A,B) individual framboids composed of octahedral crystals from the Ponta Grossa and Ilha de Maré sites; (C) individual framboid from the Ponta Grossa site, with a poorly defined shape, composed of octahedral crystals; (D) framboid from the Pitinga site, with the presence of microcrystals; (E) subspherical framboid from Ilha de Maré, composed of octahedral crystals; (F) individual framboid from Ilha de Maré, composed of cubic crystals.
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Figure 9. Microphotographs of framboid clusters: (A,B) microphotographs of framboid clusters from the Cacha Prego site; (C,D) truncated octahedral crystals from Ilha de Maré.
Figure 9. Microphotographs of framboid clusters: (A,B) microphotographs of framboid clusters from the Cacha Prego site; (C,D) truncated octahedral crystals from Ilha de Maré.
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Figure 10. Carbon isotope (δ13C) and N/C ratios in soils and plants (Rhizophora mangle and Laguncularia racemosa) from the BTS and potential sources of organic matter for mangroves in IM, PT, PG, and CP in relation to other mangrove forests in Brazil and worldwide [47,52,53].
Figure 10. Carbon isotope (δ13C) and N/C ratios in soils and plants (Rhizophora mangle and Laguncularia racemosa) from the BTS and potential sources of organic matter for mangroves in IM, PT, PG, and CP in relation to other mangrove forests in Brazil and worldwide [47,52,53].
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Table 1. TOC, TN, δ13C (‰), δ15N (‰), and C/N ratio in mangrove soils (n = 3). For each season, different uppercase letters indicate significant differences (p < 0.05) among sites. For each site, different lowercase letters indicate differences according to depth.
Table 1. TOC, TN, δ13C (‰), δ15N (‰), and C/N ratio in mangrove soils (n = 3). For each season, different uppercase letters indicate significant differences (p < 0.05) among sites. For each site, different lowercase letters indicate differences according to depth.
DepthCOT (%)TN (%)C/Nδ13C (‰)δ15N (‰)
Dry season (DS)
IM0–5 cm6.0 ± 0.5 Aa0.32 ± 0.03 Aa19.1 ± 1.3 Ab−26.98 ± 0.24 Aa2.76 ± 0.53 Aa
15–30 cm4.8 ± 0.3 Ab0.21 ± 0.02 Ab22.8 ± 1.1 Aa−26.58 ± 0.13 ABa2.20 ± 0.45 Aa
PT0–5 cm1.3 ± 0.4 Ba0.07 ± 0.04 Ba19.9 ± 3.7 Aa−27.35 ± 0.21 Aa1.97 ± 0.52 Aa
15–30 cm1.1 ± 0.3 Ba0.05 ± 0.01 Ba20.2 ± 3.2 Aa−27.40 ± 0.54 Ba2.63 ± 0.51 Aa
CP0–5 cm2.5 ± 0.4 Ba0.10 ± 0.02 Ba24.7 ± 2.9 Aa−27.18 ± 0.26 Aa2.13 ± 0.41 Aa
15–30 cm3.2 ± 0.5 Ba0.12 ± 0.04 Ba26.7 ± 4.2 Aa−26.77 ± 0.27 ABa2.18 ± 0.46 Aa
PG0–5 cm1.3 ± 0.7 Ba0.06 ± 0.04 Ba23.5 ± 3.2 Aa−26.43 ± 0.49 Aa1.12 ± 0.93 Aa
15–30 cm1.4 ± 0.0 Ba0.06 ± 0.00 Ba24.9 ± 0.7 Aa−26.16 ± 0.16 Aa0.94 ± 0.39 Ba
Rainy season (WS)
IM0–5 cm5.9 ± 0.9 Aa0.30 ± 0.06 Aa19.6 ± 1.3 Aa−26.90 ± 0.16 ABb2.56 ± 0.29 Aa
15–30 cm4.8 ± 0.3 Aa0.23 ± 0.01 Aa21.1 ± 1.7 Aa−26.39 ± 0.21 Aa2.26 ± 0.69 Aa
PT0–5 cm1.5 ± 0.4 Ca0.06 ± 0.01 Ba23.2 ± 4.3 Aa−27.83 ± 0.33 Ba3.10 ± 0.63 Aa
15–30 cm2.1 ± 0.6 Ba0.08 ± 0.02 Ba25.7 ± 1.6 Aa−28.00 ± 0.34 Ba2.37 ± 0.30 Aa
CP0–5 cm3.4 ± 0.8 Ba0.15 ± 0.04 Ba22.4 ± 2.4 Aa−27.04 ± 0.33 ABa2.63 ± 0.04 Aa
15–30 cm2.5 ± 0.4 Ba0.11 ± 0.03 Ba23.0 ± 1.7 Aa−26.51 ± 0.18 Aa2.74 ± 0.24 Aa
PG0–5 cm1.0 ± 1.2 Ca0.05 ± 0.03 Ba21.0 ± 4.4 Aa−26.09 ± 0.70 Aa1.20 ± 0.66 Ba
15–30 cm1.9 ± 1.2 Ba0.07 ± 0.04 Ba26.9 ± 2.3 Aa−26.50 ± 0.07 Aa1.12 ± 1.13 Aa
Table 2. Total contents of C and N, and δ13C, δ15N, and C/N ratios in Rhizophora mangle and Laguncularia racemosa leaves from mangroves in the BTS (n = 3). Different letters indicate spatial differences within the same species (p < 0.05).
Table 2. Total contents of C and N, and δ13C, δ15N, and C/N ratios in Rhizophora mangle and Laguncularia racemosa leaves from mangroves in the BTS (n = 3). Different letters indicate spatial differences within the same species (p < 0.05).
C (%)N (%)C/Nδ13C (‰)δ15N (‰)
R. mangle
IM41.6± 0.8 a1.0 ± 0.2 a43.5 ± 7.2 a−29.7 ± 0.4 bc2.7 ± 0.4 a
CP40.4 ± 0.9 a1.0 ± 0.1 a38.7 ± 1.8 a−30.3 ± 0.3 c2.2 ± 0.1 a
PT41.5 ± 0.5 a1.3 ± 0.1 a32.8 ± 2.7 b−28.7 ± 0.1 a0.9 ± 0.2 b
PG41.1 ± 1.0 a1.0 ± 0.2 a40.6 ± 7.2 a−29.4 ± 0.4 ab1.1 ± 0.6 b
L. racemosa
PT40.5 ± 0.3 b1.0 ± 0.2 b41.0 ± 4.1 a−29.3 ± 0.1 b2.9 ± 0.3 a
PG38.5 ± 1.6 a1.0 ± 0.2 a48.2 ± 7.2 a−29.2 ± 0.2 a1.8 ± 0.1 b
Table 3. Mean concentration (with standard deviation in parentheses) of geochemical fractions of Fe (mg kg−1) in soils from Ilha de Maré, Pitinga, Ponta Grossa, and Cacha Prego during the dry (DS) and rainy (WS) seasons (n = 3). Different uppercase letters indicate differences among sites within the same season, while lowercase letters indicate differences according to depth within the same site. * indicates significant seasonal differences (p < 0.05).
Table 3. Mean concentration (with standard deviation in parentheses) of geochemical fractions of Fe (mg kg−1) in soils from Ilha de Maré, Pitinga, Ponta Grossa, and Cacha Prego during the dry (DS) and rainy (WS) seasons (n = 3). Different uppercase letters indicate differences among sites within the same season, while lowercase letters indicate differences according to depth within the same site. * indicates significant seasonal differences (p < 0.05).
DepthFeExCaFeAmFeCriFeRed
DSWSDSWSDSWSDSWS
Ilha de Maré (IM)
S77.9 Aa
(21.3)
68.0 Aa
(22.9)
355 Aa
(163)
356 Aa
(90.2)
1828 Aa
(181)
2154 Aa
(816)
5074 Aa
(3329)
5855 Aa
(1580)
P63.3 Aa
(17.5)
69.5 Aa
(8.9)
196 Aa
(68.1)
107 ABb
(53.2)
1155 Ab
(76.8)
1243 Aa
(65.5)
7200 Aa
(2662)
6819 Aa
(1437)
Pitinga (PT)
S39.6 Aa
(18.0)
40.3 Aa
(11.3)
613 Aa
(335)
136 Aa
(167)
568 Ba
(368)
346 Ba
(170)
140 Aa
(7.9)
313 Bb
(184)
P22.1 Aa
(5.8)
14.9 Aa
(2.4)
340 Aa
(241)
12.3 Ba
(5.7)
279 Ba
(138)
196 Ca
(50.1)
160 Ba
(106)
1722 Ca
(853)
Cacha Prego (CP)
S55.2 Aa
(10.3)
85.1 Aa
(41.9)
223 Aa
(30.4)
513 Aa
(381)
577 Ba
(73.1)
1255 ABa
(773)
2488 Aa
(1044)
3621 Aa
(689)
P73.8 Aa*
(4.1)
55.2 Aa*
(5.1)
224 Aa
(108)
325 Aa
(152)
575 Ba
(63.3)
630 Ba
(126)
3782 ABa
(1828)
4321 Ba
(851)
Ponta Grossa (PG)
S32.8 Aa
(27.5)
33.8 Aa
(8.9)
112 Aa
(46.5)
54.5 Aa
(38.8)
562 Ba
(633)
629 ABa
(573)
1163 Aa
(1348)
467 Ba
(471)
P35.0 Aa
(25.2)
30.9 Aa
(15.1)
46.5 Aa
(65.5)
29.1 Ba
(26.5)
395 Ba
(206)
317 Ca
(43.3)
881 Ba
(246)
1082 Ca
(417)
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Vasconcelos Ramos, M.A.; Pérez-Alberti, A.; Nuto Nóbrega, G.; Otero, X.L. Spatiotemporal Variability in Soil Properties and Composition in Mangrove Forests in Baía de Todos os Santos (NE Brazil). Land 2023, 12, 1392. https://doi.org/10.3390/land12071392

AMA Style

Vasconcelos Ramos MA, Pérez-Alberti A, Nuto Nóbrega G, Otero XL. Spatiotemporal Variability in Soil Properties and Composition in Mangrove Forests in Baía de Todos os Santos (NE Brazil). Land. 2023; 12(7):1392. https://doi.org/10.3390/land12071392

Chicago/Turabian Style

Vasconcelos Ramos, Monica Arlinda, Augusto Pérez-Alberti, Gabriel Nuto Nóbrega, and Xosé Luis Otero. 2023. "Spatiotemporal Variability in Soil Properties and Composition in Mangrove Forests in Baía de Todos os Santos (NE Brazil)" Land 12, no. 7: 1392. https://doi.org/10.3390/land12071392

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