Are mangrove forest substrates sediments or soils? A case study in southeastern Brazil

Catena 70 (2007) 79 – 91 www.elsevier.com/locate/catena

Are mangrove forest substrates sediments or soils? A case study in southeastern Brazil T.O. Ferreira a , P. Vidal-Torrado b , X.L. Otero c,⁎, F. Macías c a

Depto. de Ciências do Solo, CCA/UFC, Fortaleza, Brazil Depto. de Ciência do Solo, Universidade de São Paulo, ESALQ, M.B. 9, Piracicaba-SP, 13418-900, Brazil Depto. Edafoloxía e Química Agrícola, Facultade de Bioloxía, Universidade de Santiago de Compostela 15782, Santiago de Compostela, Spain b

c

Received 11 March 2005; received in revised form 27 July 2006; accepted 31 July 2006

Abstract Morphological and analytical data corresponding to several profiles from two mangrove systems in the Brazilian state of São Paulo were examined for evidence of pedogenetic processes. Plant activity exerted a strong effect on the processes occurring in mangrove substrates, especially on the intensity of these processes and, therefore, constitutes one of the major factors involved in the differentiation of sediments and soils. Colonization of substrates by vascular plants leads to drastic changes in physicochemical conditions. The redox processes were much more diverse in the soil than in the sediment (substrate without vegetation); in the former they varied with depth, with oxic or suboxic conditions being observed at the surface and anoxic conditions observed below 30 cm, whereas in the sediment, anoxic conditions were observed throughout. Likewise, the acid–base conditions were more variable in the soils, ranging from strongly acid to neutral, and in the sediment they were close to neutral. Furthermore, different pedogenetic processes were identified: (1) addition of organic matter by accumulation of vegetable debris and dead roots, with formation – in some cases – of a histic epipedon, (2) transfer of soluble iron (Fe2+) towards the surface and precipitation in the form of Fe oxyhydroxide, and transfer of the mineral particles due to the bioturbation caused by activity of crabs, (3) transformation of elements such as iron (gleization) and sulphur (sulphidization). Changes undergone in the mangrove substrates were also characterized by simultaneity and intergradations between pedogenesis and diagenesis, especially in the lowermost layers in which authigenesis appears to intensify. Thus, the presence of smectite minerals in the clay fraction may be attributed to authigenic processes that take place in both soils and sediments. © 2006 Elsevier B.V. All rights reserved. Keywords: Mangrove sediments; Mangrove soils; Pedogenesis; Diagenesis

1. Introduction Mangrove forests are very important tropical coastal tidal ecosystems and grow on nutrient-rich muddy substrates that are low in oxygen and that undergo variations in salinity (Shaeffer-Novelli, 1999). The important functional role of mangrove forest communities and their transitional position between marine and terrestrial environments have led to these ecosystems being the object of study within a variety of scientific disciplines such as biology, ecology, geology, oceanography and pedology. However, scientists, including ⁎ Corresponding author. Tel.: +34 981 5631x13346; fax: +34 981 566904. E-mail address: [email protected] (X.L. Otero). 0341-8162/$ - see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.catena.2006.07.006

pedologists, often refer to the substrate on which mangrove vegetation develops as sediment rather than as soil (Corredor and Morrell, 1994; Clark et al., 1998; Tam and Wong, 1998). As far as Brazilian mangrove forests are concerned, classification of estuarine substrates as sediments is largely attributed to the fact that there exist very few studies on the genesis and classification of estuarine soils in Brazil (Lima and Costa, 1975; Prada-Gamero et al., 2004) or other countries (Ukpong, 1994). Sediments are defined as deposits of solid material on the earth's surface, from any medium (air, water, ice) (Krumbein and Sloss, 1963), whereas a recent definition of the word ‘soil’ (Soil Survey Staff, 2003) considers that it is ‘a natural body comprised of solids, liquid and gases that occurs at the

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earth's surface, occupies space, and has one or both of the following characteristics: (1) is organized into horizons or layers that are distinguishable from the initial material as a result of additions, losses, transfers, and transformations of energy and matter and/or (2) is capable of supporting rooted plants in a natural environment’. The definition considers soils as all natural bodies that contain living matter and are capable of supporting rooted plants although they do no have genetically differentiated parts (layers and horizons). Thus, a soil must contain living matter (Soil Survey Staff, 1993). On the other hand, the term ‘soil’ as defined by Soil Taxonomy was modified in 1998 to include soils permanently submersed by water columns of up to 2.5 m in depth (subaqueous soils) and that support submerged aquatic vegetation (SAV). The change in definition was based on the existence of pedogenetic processes (Demas and Rabenhorst, 1999; Demas and Rabenhorst, 2001; Bradley and Stolt, 2003). The main objectives of the present study therefore were to document features associated with the pedogenetic processes occurring in two mangrove forest substrates in São Paulo state (Brazil) and to provide data that will help in reaching a decision about whether these substrates should be denominated as soil. We demonstrate in this study that in these two estuarine systems active pedogenetic processes have led to modification of the substrates to soil.

2. Materials and methods 2.1. Study areas The sampling sites were in a mangrove forest in the Crumahú River (Site 1 – S1) close to the urban areas of Morrinhos and Vila Zilda (Baixada Santista region, Guarujá county, São Paulo) and in a mangrove forest on the Island of Pai Matos (Cananéia county, São Paulo) (Site 2 – S2) (Figs. 1 and 2). The overall average air temperature for the region fluctuates between 10 and 35 °C and rainfall ranges from 1700 to 2000 mm year− 1. The study areas consist of coastal plains within a littoral relief region of lowlands, tidal flats and meandering fluvial systems enclosing plains covered with mangrove forests (Rossi, 1999). The geological substrate consist of fluvial–marine deposits, limited to the west by alluvial, colluvial and marine deposits and to the east by the granite–gneiss Serra do Mar scarps. Site S1 is mainly dominated by the mangrove species Rhizophora mangle and Avicennea schaueriana, especially at sites distant from the urban areas of Morrinhos and Vila Zilda. Within the urban areas, a considerable part of the mangrove forest has been irregularly reclaimed for human occupation and the Crumahú River receives untreated effluents from people living in Morrinhos and Vila Zilda; untreated domestic sewage is discharged directly into the river causing

Fig. 1. Location of study area, showing in detail the location of the transects and profiles selected (A, B, C, D) in site S1.

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Fig. 2. Location of the profiles studied at 2 (S2) on the Island of Pai Matos: (A) vegetated with Spartina alterniflora and (B) non-vegetated.

eutrophication and affects the fauna (especially crabs) and mangrove species. The vegetation at sites close to the effluent discharge is dominated by the fern Acrostichum aureum (Pteridaceae, order Filicales), which is one of the few species that can grow in the transitional environment between mangrove forests and terrestrial ecosystems (Lamberti, 1966). A. aureum is also associated with anthropogenically-affected mangrove systems such as the Crumahú River forest. At S2 an intertidal mudflat vegetated by Spartina alterniflora and non-vegetated areas were studied to evaluate the effect of biological (i.e. plant) activity on the intensity of some soil-forming processes. The sites (vegetated and non-vegetated) were close to one another (b3 m) (Fig. 2). 2.2. Sampling and laboratory procedures At S1 samples were collected along two transects of length 150 m. Samples were collected every 10 m (15 sampling points) along transect 1, which is situated upstream and every 30 m (5 sampling points) along transect 2, situated downstream. Fifteen further profiles were sampled and analyzed for better control of spatial variation in the substrate (Fig. 1). However, in the present study, only the data corresponding to 4 profiles (A, B, C, D) that we consider representative, are provided. All cores were drilled at low tide with a special sampler for flooded sediments, which consists of a 0.9 m long stainless-steel tube of 0.07 m diameter; samples were taken at 0–0.2, 0.3–0.5 and 0.6– 0.8 m depth. At S2, six samples were collected with PVC tubes (0.05 m i.d. and 0.5 m in length) from both sampling sites (vegetated and non-vegetated substrates). The cores were taken from

within an area of 1 m radius, in order to minimize spatial variation. The tubes were sealed, stored at approximately 4 °C and transported in a vertical position to the laboratory where they were cut into sections (0–0.03 m, 0.03–0.06 m, 0.06–0.1 m, 0.1–0.15 m, 0.15–0.2 m, 0.2–0.25 m, 0.25– 0.3 m, 0.3–0.35 m) and stored frozen until analysis. All core samples were collected at low tide. The redox potential (Eh) and pH of all samples were measured in the field after equilibrating the cores and electrodes for several minutes (∼2 min). The Eh values were determined using an oxidation–reduction potential (ORP) platinum electrode and the final readings were corrected by adding the potential (+ 244 mV) of a calomel reference electrode; the pH was measured using a glass electrode (Model MP120; Mettler Toledo) calibrated at pH 4.0 and 7.0. The samples were air-dried, crushed and sieved; electrical conductivity (EC) was measured in saturated extracts, with a conductivity meter. Before chemical analysis, samples were washed with 60% (v/v) aqueous ethanol to remove salts (Embrapa, 1997). A combined glass–calomel electrode was used to determine the pH of aqueous suspensions (1:2.5 solid/liquid ratio). Total organic carbon (TOC) was determined by dry combustion, in an elemental analyzer (Leco CNH-1000). A mixed ion exchange resin pre-saturated with 0.5 M NaHCO3 buffered at pH 8.5 was used for Ca, K and Mg extraction (Raij et al., 1986) from which the cations were extracted with acidified (0.2 M HCl) NH4Cl and determined by flame photometry (K) and atomic absorption spectrophotometry (Ca and Mg). Potential acidity (H + Al) was determined by extraction with a 1 mol L− 1 Ca acetate solution at pH 7 (Quaggio et al., 1985). Cation exchange capacity (CEC) was calculated as the sum of exchangeable cations (Ca, Mg, K, Na and H + Al) (Sumner and Miller,

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1996). The hydrometer method (Gee and Bauder, 1986) was used for particle-size analysis, preceded by oxidation of organic matter with H2O2 by using a combination of physical (overnight shaking) and chemical (0.015 M (NaPO3)6 + 1.0 M NaOH) dispersal methods. The mineralogy of the clay fraction (b 2 mm) was studied using XRD in a Philips X'pert System (Philips, São Paulo, Brazil). Clay samples were prepared according to Jackson's (1969) method, and analyzed under five different conditions (K saturated, Mg saturated, ethylene–glycol solvation, and heating to 110, 350 and 550 °C for 2 h). Scanning electron microscopy (SEM) of the samples was performed with a JEOL-5600LV scanning electron microscope fitted with a Noran Voyager X-ray microanalysis energy dispersive spectrum (EDS) analysis system. Iron was sequentially extracted in two samples using methods of Tessier et al. (1979), Fortin et al. (1993) and Huerta-Díaz and Morse (1990) as follows: F1 – Exchangeable iron: 30 min with 30 mL of a 1 M MgCl2 solution at pH 7.0 (Tessier et al., 1979). In this step and the following, the extract was centrifuged at 10,000 rpm (4 °C) for 30 min. Table 1 Profile descriptions of two representative cores from Site 1 (S1) Horizon

Depth

Profile C – Histic Sulfaquent O 0–20 cm

Cg1

20–50 cm

Cg2

50–80 cm

Profile D – Typic Sulfihemist Oe1 0–20 cm

Oe2

20–50 cm

Cg1

50–80 cm

F2 – Carbonatic iron: 30 mL of a 1 M NaOAc, at solution pH 5.0, agitated for 5 h (Tessier et al., 1979). F3 – Ferrihydrite: 30 mL of a 0.04 M hydroxylamine + acetic acid 25% (v/v) solution; agitated for 6 h at 30 °C (Fortin et al., 1993). F4 – Lepidocrocite: 30 mL of a 0.04 M hydroxylamine + acetic acid 25% (v/v) solution; agitated for 6 h at 96 °C (Fortin et al., 1993). F3 and F4 would also extract iron from manganese oxides (Chester and Hughes, 1967). F5 – Goethite and hematite: 20 mL of a 0.25 M sodium citrate + 0.11 M sodium bicarbonate solution with 3 g of sodium dithionite; agitated for 30 min at 75 °C (Fortin et al., 1993). Before the extraction of pyrite, samples were subjected to treatment with 10 M HF for 16 h under agitation, to remove iron associated with the silicate, followed by treatment with concentrated H2SO4 to remove organic matter associated iron. F6 – Pyrite: 10 mL of concentrated HNO3; samples were agitated for 2 h at RT and then washed with 15 ml of ultrapure water (Huerta-Díaz and Morse, 1990). Between each extraction step samples were washed with 20 mL of deaerated ultrapure water. The % of iron in pyrite (DOP) was calculated as follows (Berner, 1970): DOP ð%Þ ¼ ½ðPyrite FeÞ=ðReactive Fe þ Pyrite FeÞ  100

Description Brownish black (2,5Y 3/1) moist; 2% medium distinct reddish brown (5YR 4/6) mottles; clay loam; structureless; slightly sticky; nonplastic; many fine and very fine roots, common medium and few course roots Black (GLEI N 2/) moist; clay loam; structureless; sticky; plastic; few fine and very fine roots Dark gray (GLEI N 2/) moist; clay; structureless; very sticky; plastic

Brownish black (2,5Y 3/1) moist; 2% medium distinct reddish brown (5YR 4/6) mottles; sandy clay loam; structureless; nonsticky; nonplastic; many fine and very fine roots, common medium and course roots; moderate fiber content 32% (hemic) Brownish black (2,5Y 3/1) moist; 1% medium distinct reddish brown (5YR 4/6) mottles; sandy clay loam; structureless; slightly sticky; nonplastic; many fine and very fine roots, common medium and few course roots; moderate fiber content 32% (hemic) Black (2,5Y 2/1) moist; clay; structureless; sticky; plastic; few fine and very fine roots

We calculated the DOP by considering the reactive iron (i.e. that can react with sulphide to form pyrite) as the iron extracted in the first four steps (Otero and Macías, 2003). Root biomass and necromass was determined after sieving (0.5 mm mesh) core slices and washing them with water. The living roots were separated from dead roots by visual inspection and dried at 80 °C until constant weight. To classify the profiles according to the Soil Survey Staff method (Soil Survey Staff, 2003), Munsell colour, fibre content and sulphidic materials (FeS2) were determined after incubation at RT under moist aerobic conditions for up to 8 weeks (Soil Survey Staff, 2003). The sodium pyrophosphate index (Lyn et al., 1974) was also determined. This involves determining the colour developed on chromatographic paper strip placed in a suspension of the sample in a saturated solution of sodium pyrophosphate. The pyrophosphate index is the difference between the Munsell value and chroma on the paper strip. The greater amounts of humic and fulvic acids dissolved in the solution, the darker the colour developed, indicating greater decomposition. Pyrophosphate index values greater than or equal to 5 indicate that the material is poorly decomposed or not decomposed, and that fibrous material dominates; values of less than or equal to 3 indicate highly decomposed organic matter, with sapric material dominating; intermediate values indicate hemic material. Four representative profiles from site S1 (A, B, C and D) were chosen based on the morphological and physicochemical data (Fig. 1).

Table 2 Chemical properties and classification of the representative profiles A, B, C and D from site S1 Horizons Depth (m)

pH (H2O)

Na (cmolc kg− 1)

K (cmolc kg− 1)

Ca (cmolc kg− 1)

Mg (cmolc kg− 1)

Al (cmolc kg− 1)

H + Al (cmolc kg− 1)

SB (cmolc kg− 1)

CEC (cmolc kg− 1)

ECEC (cmolc kg− 1)

V (%)

ESP (%)

EC (dS m− 1)

A – Typic Sulfihemist Oe1 0–0.2 5.7 Oe2 0.3–0.5 5.4 Oe3 0.6–0.8 5.7

19 17 19

11.0 12.2 7.00

0.9 1.1 1.0

6.3 7.1 5.1

4.4 4.6 4.5

nd 0.1 1.0

10.0 10.9 8.8

22.7 25.0 17.6

32.7 35.9 26.4

22.7 25.1 18.6

69 70 67

34 34 26

21.56 20.27 20.68

B – Histic Sulfaquent 0–0.2 5.8 O1 O2 0.3–0.5 6.3 Cg1 0.6–0.8 6.0

16 17 14

13.0 12.0 13.0

1.2 1.1 1.0

7.3 6.9 6.1

4.6 4.7 4.4

1.0 1.0 nd

7.9 7.8 7.8

26.1 24.7 24.5

34.0 32.5 32.3

27.1 25.7 24.5

77 76 76

38 37 40

22.40 23.73 24.04

C – Histic Sulfaquent O 0–0.2 5.5 0.3–0.5 5.4 Cg1 0.6–0.8 6.4 Cg2

16 7 4

8.20 16.4 6.70

1.2 1.4 1.2

7.1 6.6 6.0

4.6 4.8 4.6

2.0 1.0 nd

9.3 8.7 2.7

21.1 29.2 18.5

30.4 37.9 21.2

23.1 30.2 18.5

69 77 87

27 43 32

23.92 22.56 20.07

D – Typic Sulfihemist Oe1 0–0.2 6.2 0.3–0.5 6.1 Oe2 Cg1 0.6–0.8 6.3

25 24 14

15.4 14.8 12.0

0.9 0.8 1.1

7.4 5.7 6.4

4.3 4.1 4.6

nd nd nd

8.0 7.0 7.3

28.0 25.4 24.1

36.0 32.4 31.4

28.0 25.4 24.1

78 78 77

42 46 38

25.62 25.13 24.02

Horizons

Depth (m)

Clay (%)

Textural classes

Color (Munsell)

Fiber (after rubbing (%))

Color (Napyrophosphate)

A – Typic Sulfihemist 0–0.2 Oe1 0.3–0.5 Oe2 Oe3 0.6–0.8

33 39 48

Sandy clay loam Clay loam Clay

2,5Y 2,5/1 GLEI N 2,5/ GLEI N 2,5/

40 39 39

B – Histic Sulfaquent 0–0.2 O1 0.3–0.5 O2 Cg1 0.6–0.8

37 61 73

Clay loam Clay Clay

2,5Y 3/1 2,5 Y 3/1 5Y 2,5/1

C – Histic Sulfaquent O 0–0.2 0.3–0.5 Cg1 0.6–0.8 Cg2

36 37 45

Clay loam Clay loam Clay

D – Typic Sulfihemist Oe1 0–0.2 Oe2 0.3–0.5 0.6–0.8 Cg1

26 27 48

Sandy clay loam Sandy clay loam Clay

Sulfidic materiala

pH dropb

Initial pH

Final pH

pHi − pHf

10YR 7/2 10YR 7/1 –

5.0 4.8 6.4

4.3 3.9 5.0

0.7 0.9 1.4

– – –

– – –

5.8 5.6 6.4

5.2 4.0 5.7

0.6 1.6 0.7

2,5Y 3/1 GLEI N 2/ GLEI N 3/

– – –

– – –

5.5 6.4 6.4

5.5 5.8 4.0

– 0.6 2.4

2,5Y 3/1 2,5Y 3/1 2,5Y 2/1

32 32 –

10YR 8/1 10YR 8/1 –

5.4 5.1 5.9

4.5 4.8 5.2

0.9 0.3 0.7

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TOC (%)

TOC: total organic carbon; SB: sum of base cations; CEC: cation exchange capacity; ECEC: effective cation exchange capacity; V%: base saturation (V% = 100 × sum of bases/cation exchange capacity); ESP: exchangeable sodium percentage; EC: Electrical conductivity of saturation extract. a See Methods. b Difference in pH = initial (in situ pH) − final pH (after 8 weeks of incubation). 83

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2.3. Statistical analysis The differences between non-vegetated and vegetated sites were tested using one-way ANOVA. Statistically significant differences between groups were assessed using Tukey's comparison test. The relationships between Fe and root biomass were determined by calculating Spearman's coefficients of correlation. All analyses were carried out using a SYSTAT 5.0 computer program (Systat INC, 1992). 3. Results 3.1. Morphological data and soil classification The morphological characteristics and chemical and analytical data of selected profiles from S1 were used to classify the soils taxonomically (Tables 1 and 2). All four representative profiles showed intense accumulation of organic debris from the mangrove vegetation and this, along with dead roots and the high groundwater level promoted the formation of characteristic histic epipedons in all four profiles. In profile B and C organic material was equally accumulated but not sufficient to make it a Histosol (Soil Survey Staff, 2003). The total organic carbon (TOC) content ranged between 4% and 25%, with the highest values of 25% in profile D. The matrix colours were bluish to greenish-grey in all profiles at all depths, the chroma were 1 or less and colour values less than 4, with red (5YR 4/6) and black mottles (5GB 2/1), presumably due the presence of Fe monosulphides (soluble in HCl, Souza-Silva, 2005). The EC

values ranged from 20.1 to 25.6 dS m− 1 with the highest values corresponding to substrate profile D and the lowest to profile A (Table 1). The EC values generally decreased with depth. Despite the high EC values, it was not possible to confirm a salic horizon (EC ≥ 30 dS m− 1; Soil Survey Staff, 2003). Sulphidic material was another common characteristic of the profiles. The pH decreased by at least 0.5 units when the samples were incubated under moist aerobic conditions (Table 2), which indicated the presence of sulphidic material and justified the classification of profiles A and D as Typic Sulfihemists and profiles B and C as Histic Sulfaquents (Tables 1 and 2). The SEM and EDS spectra also indicated the presence of characteristic pyrite framboids (Fig. 3), which may be the main component of sulphidic material in this environment. In fact, the presence of acid volatile sulphides (AVS = ∑HS−, FeS, Fe3S4) has previously been observed in these substrates, but at lower concentrations than those observed for pyrite (Crumahú: pyrite 400 ± 100 μg− 1; AVS 1.0 ± 1.2 μg− 1) (Souza-Silva, 2005). 3.2. Particle size distribution and mineralogical data Sand predominated in the upper layers and decreased with depth (Table 2). The XRD patterns of all 4 profiles from S1 showed the same clay mineralogy, with presence of kaolinite, a mica and smectite (Fig. 4A). Some peaks corresponded to jarosite, which was probably formed by pyrite oxidation during the removal of organic matter with hydrogen peroxide. Vertical profiles of clay samples treated with ethylene-glycol (Fig. 4B) showed a clear increase in the intensity of smectite peaks with increasing depth of sample. The scanning electron micrographs and energy dispersive spectra show the characteristic smectitic honeycomb morphology and intense peaks that correspond to silicon peaks in relation to the aluminium peaks (Fig. 5). 3.3. Physicochemical parameters

Fig. 3. Framboidal morphology of a pyritic mineral phase and EDS spectrum showing intense iron and sulphur peaks.

For all layers of the S1 profiles, in situ values of pH ranged between slightly acidic and neutral (6.1 to 7.0), with the pH increasing slightly with depth (Fig. 6). The Eh values generally decreased with depth for all the profiles, and ranged between −100 and 120 mV in the uppermost layer to between ∼− 50 and − 150 mV at depth. The maximum Eh values at S1 occurred in substrate profile A, particularly in the superficial layers. On the other hand, redox potential and pH values showed clear differences between vegetated and non-vegetated substrates (S2). The Eh values recorded in non-vegetated substrates were always close to 75 mV, whereas in vegetated substrate the Eh varied within a wider interval, ranging between oxic conditions in the uppermost layer (Eh: 356 mV) and strongly reduced conditions at depth (Eh: − 56 mV). There was also a significant difference (P b 0.05) between the pH values for these two sites, which varied from pH 7.9 ± 0.4 (non-vegetated) to pH 7.5 ± 0.3 (vegetated).

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Fig. 4. (A) XRD pattern of a superficial (0–0.2 m) clay sample from profile C (Site 1) (M = mica; SM = smectite; KK = kaolinite). (B) Downward variations in the ethylene-glycolated XRD pattern in the clay fraction of representative profile C.

3.4. Iron speciation The highest concentrations of iron species, especially reactive-Fe (∑F1, …, F4), occurred in vegetated substrates (173.7 μM at 0–3 cm), decreased with depth (31.7 μM at 40–45 cm) (Fig. 7a, b) and showed a strong correlation with root biomass (r = 0.933, P b 0.001; Fig. 8). The DOP data is evidence of a more intense degree of Fe pyritization in vegetated substrate (28.4 ± 6.8%) than in non-vegetated substrate (20.8 ± 4.3%). 4. Discussion 4.1. Characterization of the physicochemical environment The more acidic pH values found in the surface layers of the S1 profiles (Fig. 6) may be attributed to the oxidation of iron sulphides promoted by the release of O2 from plant, especially in surface layers (Marchand et al., 2003). Thus, the decrease in the redox potential with depth may be related

to a lower density of plant roots in deeper layers. Previous findings suggest that mangrove species are able to alter the redox potential (i.e. by oxidation) of sediments by translocating oxygen absorbed on above-ground root structures to below-ground roots (Mckee et al., 1988; Mckee, 1993) and that different species, with different types of root structures, may not be equally capable of oxidizing the rhizospheres (Gleason et al., 2003). In the present study, the highest values in profile A, especially in superficial layers, are assumed to be due to the presence of the fern A. aureum, which has a highly ramified aerial root system that probably has a greater oxidizing capacity than species such as R. mangle. At S2 the effect of plants on the physicochemical conditions of the substrates became even more evident when comparing the Eh and pH of the vegetated and non-vegetated substrate. The presence and activity of plants resulted in the appearance of more oxidative and acid conditions (Fig. 6), since both areas present the same physical conditions of flushing and percolation. The presence of plants also led to the appearance of a clear redox zonation at the vegetated

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Fig. 5. Honeycomb morphology of the smectite and EDS spectrum showing the presence of iron and potassium at the mineral structure.

substrate, with oxic (0.1 m), suboxic (0.3 m) and anoxic (N0.5 m) conditions in the same profile (Fig. 6). On the other hand, in the non-vegetated profile, redox conditions remained anoxic in all layers, with homogeneous patterns within depths. These results indicate that the acid base and redox conditions are strongly affected by the presence of vegetation and therefore contribute to establishing initial differentiation between sediment and soil. 4.2. Pedogenetic processes 4.2.1. Additions Pedogenetic additions may consist of minerals received through alluvial and colluvial transport (cumulization) and/ or addition of organic matter (Simonson, 1959). This process was recently studied in estuarine environments by Demas

and Rabenhorst (1999) who observed mineral, organic and biogenic additions to the sediment. The present results indicate clearly higher accumulation of organic matter in the soils than in the sediments. This process appears to be related to the accumulation of dead roots. The mass of dead roots obtained from several depths in three different sites colonized by R. mangle was approximately 10 t ha− 1. This high net productivity of roots may be one of the major factors leading to the genesis of histic horizons (Table 2). On the other hand, the higher TOC content in profile D (Table 2) may be related to more highly developed Rhizophora vegetation at this site, because this site was far from wastewater contamination and also near to the entrance pathway for seawater where water fluxes are intense and there is a higher concentration of nutrients that favours development of vegetation (Citrón and Schaeffer-Novelli, 1983).

Fig. 6. pH and redox variation for all profiles. A, B, C, D are the profiles selected from S1.

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Fig. 7. Fe fractions from Site 2, showing different iron species distribution: (A) vegetated site and distribution of fresh roots; (B) non-vegetated profile and (C) degree of Fe pyritization (DOP) in non-vegetated and vegetated substrate.

4.2.2. Translocations Translocation occurred in the vegetated profile, as indicated by the high concentration of Fe in the surface layer. The results show a clear enrichment of iron (mainly oxyhydroxide iron) in the surface layers (249 ± 14 μmol g− 1) of the substrate vegetated by Spartina relative to the lowest layers (123 ± 72 μmol g− 1) and the adjacent non-vegetated profile (585 ± 9 μmol g− 1) (Fig. 7). Spartina can generate a considerable water flow towards its roots, through evapotranspiration (see e.g. Dacey and Howes, 1984). During this process dissolved Fe2+, present in the interstitial water, is mobilized towards the rhizosphere where existing oxidizing conditions favour its precipitation as iron oxyhydroxide (Sundby et al., 1998). The highly significant correlation between iron oxyhydroxide species and root biomass is consistent with this hypothesis (Fig. 8). By contrast, in the non-vegetated site the concentrations of iron, and its species, do not vary with depth and are homogeneous in all profiles. Bioturbation is another pedogenetic translocation process. According to Simonson (1959), bioturbation is among the most common natural pedogenetic translocations occurring in soils. The velocity of water flow is variable in mangrove forests, and this may cause variations in grain size distributions within a single area; however, because mangrove forests commonly occur along protected shorelines, where both the hydraulic energy and sedimentation rates are low, the transport and deposition of mineral material in such environments generally involves clay and silt fractions (Citrón and Schaeffer-Novelli, 1983). The higher proportion of sand observed in superficial layers in the present study may have been generated by a combination of bioturbation and erosional winnowing (selective transport by water). The

macrofauna of mangrove forests (mainly crabs) has an important effect on the physical characteristics of mangrove substrates, as activity of the organisms causes movement of particles to superficial layers (Iribarne et al., 2000; Nielsen et al., 2003). Chasmagnathus granulata and Uca species are included among the most common crab species present along the Southwest Atlantic coast, and are considered to be the most important disturbers of coastal sediments because of their high density and their ability to build channels 0.25 to 0.4 m deep that are used for mating or for taking refuge from predators. These species also have the capacity to remove large amounts of subsurface sediment particles, up to 5 kg m− 2 day− 1 in the case of Uca species, forming surface

Fig. 8. Relationship between reactive-Fe and fresh roots in vegetated profile from S2.

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Fig. 9. Schematic model representing the relationships between unconsolidated sediment, pedogenesis, diagenesis and their gradual boundaries.

mounds (Uca sp.) and pellets (C. granulata), with a low organic matter content, which are formed during low tide and are disintegrated during high tides (Botto and Iribarne, 2000). The development of coarser surface layers observed in the present study would have been generated by bioturbation by crabs, leading to physical soil mixing and a net removal of fines from the surface by erosional winnowing, which preferentially removes the smallest, lightest particles (clays). Previous studies of the formation of vertical textures contrasts (VTC) have suggested that the combination of these two factors is one of the major factors involved in transforming profiles into coarser-over-finer sequences (Phillips, 2004). 4.2.3. Transformations Simonson (1959) states that pedogenetic transformations consist of changes in mineral and organic material from one form to another within a body of soil. In the mangrove substrates studied here, three kinds of pedogenetic transformations occurred: transformation of ferric iron to ferrous iron (gleization), reduction of SO42− to metal sulphides, mainly pyrite, (sulphidization), and neo-formation of 2:1 minerals. Gleization refers to the reduction of iron under anaerobic waterlogged conditions, and the production of bluish to greenish grey matrix colours (Munsell colours) observed here indicated the presence of reduced forms of Fe (Schwertmann, 1992) (Table 2). The compounds that give rise to these colours remain poorly characterized. In this sense, Breemen (1988) refers to a poorly defined material denominated “green rust”. This material is constituted by mixed Fe 2+ and Fe3+ hydroxides of variable Fe2+/Fe3+ ratio ranging between 0.8 and 3.6. The excess of positive charge may be neutralized by anions such as Cl−, SO42=, CO32= (Schwertmann, 1992). Recently, Bourrié et al. (1999) stated that these compounds have the following formula [Fe2+1−x–Fe3+x(OH)2]+x [x/z Az−]−x; where A− may represent Cl−, SO42−, CO32−, or OH−, with x oscillating between 0 and 1. Troulard and Bourrié (1999) established the first relations between these iron oxides and the redox sequences occurring in soils. Their findings indicated

that at pH values close to 7 the medium may be saturated with some forms of “green rust” when Pe values are higher than 6. In estuarine environments strongly affected by tidal fluctuations (generally located below mean sea level), such as S2, sulphate reduction is the main process involved in the biogeochemical cycles of sulphur and iron (Howarth, 1984). This process consists of the reduction of sulphate to sulphide by sulphate-reducing bacteria, and posterior synthesis of pyrite, which is thermodynamically the most stable end product of the sulphate reduction process (Berner, 1984). The results corresponding to S2 can be explained by the long periods of flooding to which these substrates are subjected every day which cause, along with the oxidizing effect of plants, anoxic and suboxic conditions in the subsurface and surface layers, respectively. In superficial layers, the highest concentrations of pyrite and DOP were found in the substrate colonized by Spartina. These results may be explained by the effect of plants in anoxic soils, where root exudates favour the activity of the sulphate-reducing bacteria (SRB) and in addition facilitate the partial oxidation of the sulphides generated by the SRB, giving rise to the formation of polysulphides that allow rapid formation of pyrite, according to reaction (1) (Giblin and Howarth, 1984). − 2− þ Fe2þ þ S2− 5 þ HS →FeS2 þ S4 þ H

ð1Þ

Finally, synthesis or neo-formation of mineral species is another transformation process that may occur in mangrove substrates. The study site is close to the Serra do Mar mountain range and the soils on the foothills of these mountains mainly consist of residual and poorly weathered minerals such as quartz, along with secondary minerals such as gibbsite, kaolinite, goethite and hematite (Furian et al., 2002). However, the clay diffractograms showed the presence of a smectitic 2:1 clay mineral (Fig. 4A). Although the existing evidence indicates that continental accretions exert a major influence on the clay mineral assembly, the smectite must be of authigenic origin. The formation of new minerals within the substrates appears to increase with depth, as shown in Fig. 4B.

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4.2.4. Losses Leaching and erosion are amongst the most common processes leading to soil loss that occur in terrestrial soils (Buol et al., 1997), but in mangrove substrates leaching is almost non-existent because of the stagnation of the water and low hydraulic gradient. Demas and Rabenhorst (1999) studied losses in estuary sediments and considered the action of waves and tides as the most common process causing erosion in these environments, although this type of erosion is difficult to detect because of the concomitant occurrence of the deposition of terrigenous material. Previous findings have indicated that this process is not a very important in estuarine sediments in comparison with addition, transfer and transformation processes (Demas and Rabenhorst, 1999). 4.3. Pedogenesis or diagenesis? The pedogenetic evidence presented here may be useful for defining the boundary between diagenesis and pedogenesis, both of which were active in the substrates studied. Diagenesis refers to all of the natural changes that occur in sediments between initial deposition and solidification or metamorphism (Singer and Müller, 1988) and that result in lithification by the gradual compaction and homogenization of the deposited material, whereas pedogenetic changes act in the opposite direction. As previously mentioned, soil forming processes (addition, transfers and transformations) favour the formation of distinguishable horizons and layers within the deposited material. In the substrates examined here the formation of organic rich horizons (H) and gleyed horizons (Cg) is evidence of the differentiation that impedes diagenetic effects; such differentiation also leads to formation of soils. Another aspect that must be taken into account is the role of biological activity in soil formation. At the lowest boundary of soils there is usually a gradual change to the parent material (solid rock or unconsolidated sediment), which is virtually devoid of animals, roots or any sign of biological activity (Soil Survey Staff, 2003). The lowest depth at which biological activity occurs is difficult to determine for most soils and this was also true for the substrates under study here, with the lower boundary being arbitrarily set at 2 m (Soil Survey Staff, 2003). In the uppermost layers of substrates (including those studied here) the presence of large amounts of reactive organic matter favours microbial activity, and the release of oxygen and organic compounds from roots modifies the chemical balance so that they can be considered as independent subsystems in the sediment (Madureira et al., 1997), constituting what we call a soil. The present results also showed that redox reactions in substrates that support rooted plants (soils) are much more diverse than those observed in nonvegetated substrates (sediments). Thus, there exists a redox gradient in the soils, which changes with depth from oxic to suboxic and anoxic conditions within the same profile.

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Furthermore, although redox reactions such as sulphidization may be considered as one of the earliest diagenetic processes that occur in waterlogged substrates (Krumbein and Sloss, 1963; Fairbridge, 1988), in the present case they consist of pedogenetic alterations. The higher degree of pyritization in the substrate colonised by Spartina than in the sediments (Fig. 7C) indicates that this process is strongly favoured by the activity of plants, which exude organic acids through their roots that stimulate the activity of sulphatereducing bacteria (Isaksen and Finster, 1996). In addition, the acid–base conditions generated in the soil (slightly acidic) favour the synthesis of pyrite over other Fe sulphides (Howarth, 1979). Diagenetic alterations, on the other hand, may have led to authigenesis of clay minerals, and the increasing intensity of the XRD peaks of smectite with depth of sample may indeed indicate a gradual imposition of diagenesis over pedogenesis with depth. This is illustrated in Fig. 9, in a schematic model representing the relationships among unconsolidated sediment, pedogenesis, diagenesis and their gradual boundaries. 5. Conclusions The results indicate that the pedogenetic processes of addition, translocation and transformation occurred after the sediments were colonized by vascular plants. The mangrove forest substrate should therefore be considered as a soil rather than sediment. Although this may appear to be purely semantic, consideration of mangrove substrates as sediment leads to an oversimplified picture of the active processes involved, whereas their consideration as soils implies a better understanding of the functioning of the system as a whole. This also implies the use of techniques and methods more appropriate to the study of soils rather than of sediments. Acknowledgments Many thanks are due to Dorival Grisotto, Humberto (IOUSP) and others for their help in the fieldwork. The authors thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação de Amparo á Pesquisa do estado de São Paulo (FAPESP) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for financial support, and the Núcleo de Pesquisa em Geoquímica e Geofísica da Litosfera (NUPEGEL-/USP) for providing laboratory facilities for the SEM/EDS and XRD analysis. Financial aid was also provided by the Spanish government (Dirección General de Universidades del Ministerio de Educación y Ciencia, HBP-2002-0056PC). We thank María Santiso for laboratory assistance, Esther Sierra-Abraín for elaborating Fig. 1, and also two anonymous revisers whose comments helped us to improve the original version of the paper. The authors also thank Prof. Yara Schaeffer-Novelli and Clemente Coelho Júnior for their useful advice and comments.

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