Humus form in ecosystems of the Atlantic Forest, Brazil

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1 Geoderma 108 (2002) Humus form in ecosystems of the Atlantic Forest, Brazil Andreia Kindel a, *, Irene Garay a,b a Departamento de Botânica, Instituto de Biologia, CCS, Universidade Federal do Rio de Janeiro (UFRJ), Ilha do Fundão, , Rio de Janeiro, Brazil b Centre National de Recherche Scientifique, Paris, France Received 6 July 2000; received in revised form 23 November 2001; accepted 1 February 2002 Abstract In order to describe the humus forms present in different ecosystems of the Atlantic Forest (Brazil), a morpho-functional criterium was adopted. Samples were collected from eight sites: three sites in the Tabuleiro Forest, four sites in the Restinga, and one site in Tijuca Forest. Soil samples were sorted in L, F, and H horizon and the A horizon. A horizon was analysed for ph, total C and N, available P, and exchangeable bases. Our results include the recognition of an A interface horizon beneath the holorganic layer as well as aggregates 2 10 mm in diameter in the A horizon. Accumulation of organic matter was found to be related to both nitrogen content in litterfall and soil type. In the Tabuleiro Forest Tropical Mesotrophic Mull, Tropical Oligotrophic mull and Eumoder humus forms were found. Here the soil types, Ultisol and a Spodosol, explained in part the variation in humus form. In the Restinga, a wide range of humus forms was also observed including Moder Mull, Dysmoder, Mesotrophic Mull and Eumoder; humus form was found to be related to the C:N ratio of the litterfall or to the soil substrate. At the Tijuca Forest, beneath an holorganic layer typical of a Moder (presence of the H horizon), an A horizon with a low C:N ratio typical of Mull was encountered. From the eight sites described, the Atlantic Forest biome can be said to be characterised by a great diversity of humus forms, which is a reflection of the complex environmental conditions found there. D 2002 Published by Elsevier Science B.V. Keywords: Decomposition; Litter; Nutrients; Organic matter; Rain forest; Restinga; Soil; Tropical forest * Corresponding author. addresses: (A. Kindel), (I. Garay) /02/$ - see front matter D 2002 Published by Elsevier Science B.V. PII: S (02)00126-X

2 102 A. Kindel, I. Garay / Geoderma 108 (2002) Introduction At the regional scale, due to the effects of temperature and moisture, climate is the best predictor for the decomposition rate and consequently for the formation of humus forms; however, within a particular climatic region, differences found in the decomposition process may be attributed to factors operating at a finer scale of resolution (Aerts, 1997; Anderson et al., 1983; Meentemeyer, 1978; Melillo et al., 1982). This is undoubtedly the case within the Atlantic Forest that stretches over a broad range of latitudes and altitudes, allowing high geomorphologic and biologic diversity. In forest ecosystems, the major trends of decomposition process can be synthesised by the humus form. Thus, the structure of organic materials accumulated in the soil surface, represented by different horizons of decomposing organic matter, result in a succession of interactive processes between vegetation inputs, and microbial and faunal components; indeed, considering humus form, it is necessary to take into account pedological characteristics of the A horizon, like structure, exchangeable bases and mineral composition (Babel, 1975; Barros et al., 1994; Brethes et al., 1995; Garay et al., 1995; Green et al., 1993; Klinka et al., 1990; Lavelle et al., 1993; Ponge, 1999; Ponge et al., 1999; Swift et al., 1979). In the present work, we analyse the humus form considering the morphological structure and the amount of the holorganic layers (L, F and H horizon) associated with the A horizon chemical properties (base saturation, C:N ratio and ph), as suggested by the morpho-functional classification of Berthelin et al. (1994), following the nomenclature used by the French Association of Soil Science. The presence/absence of the H horizon related to the C:N ratio and fertility of the A horizon is the basis for the differentiation between Mull and Moder (Berthelin et al., 1994; Brethes et al., 1995; Garay et al., 1995; Takahashi, 1997). Nevertheless, the description and classification of the humus forms in the Atlantic Forest was adapted to include some features of tropical forest soil, like the presence of an A i (interface) horizon and aggregates 2 10 mm in diameter, found in the soil matrix. Thus, the main objective of our study was to identify and describe humus forms encountered at eight sites in Atlantic Forest and to comment on how their form was a reflection of ecosystem processes. 2. Study sites The Atlantic Forest is located on Brazil s coast between 5j and 30jS latitude and covers altitudes from sea level to 2000 m, and though not as well known as the Amazon Forest it is home to similar biodiversity (Gentry, 1992). Three ecosystems within the Atlantic Forest were investigated: Restinga, Tabuleiro Forest and Tijuca Forest Restinga Restingas are found on Quaternary sandy plains located between the sea and the mountains of Brazil s eastern seaboard. These plains resulted from successive marine transgressions and regressions, which occurred during the Holocene and Pleistocene

3 periods (Muehe, 1983, 1984, 1994; Perrin 1984). The climate is warm and humid with an average annual temperature of 22 jc and precipitation of 1200 mm; the wet season lasts from November to March and there is no pronounced dry period (Ururahy et al., 1983). Restingas are characterised by a high diversity of sclerophyllous shrubs, tree species and palms, not to mention the Cactaceae and Bromeliaceae (Araujo, 1992; Araujo and Henriques, 1984; Rizzini, 1997). Three out four Restinga sites (R1, R2 and R3) were sampled from the Maricá Restinga in the State of Rio de Janeiro (22j55VS, 42j50VW). The soil in R1 site was taken from the sand plain on which shrubs 4 to 8 m in height formed a mosaic of sclerophyllous thickets. R2 soil was taken beneath a swampy shrub tree forest 10 m in height, this site was located on Cardosa Island in Maricá saline lagoon, and R3 soil was collected beneath a shrub tree forest 10 to 15 m in height covering the upper part of the hills on Cardosa Island (Ramos et al., 2001). The fourth Restinga site Grumari R4 (23j03VS, 43j32VW) was soil taken from forest 10 to 20 m in height that lies between the sclerophyllous thickets and the Rain Forest of Serra do Mar. At sites R1, R2 and R4, the soils are classified as Areias Quartzosas Alicas (Psamments, FAO classification), R4 is further distinguished by the presence of a podzolic B horizon (Spodosol, FAO classification). At the R3 site, the soil is a Podzólico Vermelho- Amarelo (Ultisol, FAO classification) (Camargo, 1979; Camargo and Palmieri, 1979; EMBRAPA, 1980) Tijuca Forest The Tijuca Forest (TJ) site is located within Tijuca National Park, in the city of Rio de Janeiro (22j55VS, 43j10VW). Tijuca Forest covers the steep sloped mountains ( m) that dominate the cityscape. The forest is very rich in epiphytes, woody evergreen species and palms. The predominance of Myrtaceae and Leguminosae in the arboreal stratum is one of its main characteristics (Peixoto and Gentry, 1990; Lima and Guedes- Bruni, 1997). In this mountain region, the average annual temperature is of 23 jc and the rainfall reaches almost 2500 mm (CIDE, 1994). The soil at this site was classified as a Litossolo with an AC sequence (Litosol, FAO classification) (Camargo and Palmieri, 1979). Here, geological, edaphic, climatic and also phyto-physiognomic characteristics distinguish this part of the Atlantic Forest from that found at the Tabuleiro land and the Restingas Tabuleiro Forest A. Kindel, I. Garay / Geoderma 108 (2002) The study of humus form in the Tabuleiro Forest was carried out in the Natural Reserve of Vale do Rio Doce (19j12VS, 39j82VW). Here three different sites were studied: the Tabuleiro Forest site, the Tabuleiro Forest neighbouring a stream site and the Mussununga Forest site. The Tabuleiro Forest lies over flat hills that rise m and are covered with tertiary sediments from the Barreira Formation, whereas the valleys and alluvial plains are filled with quaternary sand sediments (Meis, 1976; Suguio et al., 1982). The climate is marked by a dry period in the winter and by an increase in precipitation from October to March.

4 104 A. Kindel, I. Garay / Geoderma 108 (2002) Annual rainfall is around 1100 mm and both temperature (23 jc) and relative humidity of air (83%) are constant throughout the year (Garay et al., 1995). The Tabuleiro Forest (T1) is a well-protected forest with no record of logging and burning (Jesus, 1987). It is a semi-deciduous forest characterised by a great diversity of trees, dominated by the families Leguminosae, Myrtaceae and Sapotaceae (Rizzini et al., 1997). The Tabuleiro Forest neighbouring a stream was the second site studied (T2). Here the forest is influenced by the fluctuating water regime, notably in the rainy summer when the stream water level rises. It is important to note that the forest near this watercourse is not flooded, but the proximity to an open area, where the stream flows, offers intense luminosity that increases the number of Moraceae and Arecaceae (Rizzini et al., 1997). The third site within the Tabuleiro region is the Mussununga Forest (MF), which is restricted to the mosaic of quaternary sediments covering the valleys. The MF site is less diverse and the tree strata are lower than in the T1 site (Jesus, 1987). According to the Brazilian classification, the soils in T1 and T2 sites belong to a Podzólico Vermelho-Amarelo Distrófico (Ultisol), while the MF lies over a Hydromorphic Podzol (Spodosol) (Garay et al., 1995). Although, there is a slight difference between the soil at T1 and T2 sites, in T2 the relief is gently rolling due to the existence of a shallow valley slope, at the bottom of which there is a stream. In this situation the erosive process can be more accentuated (Santos, pers. comm.) Materials and methods 3.1. Field sampling Ten samples of L (comprised of recently fallen litter), F (comprised of fragmented leaves and fine organic matter smaller than 2 mm) and H (comprised mostly of fine organic matter < 2 mm inter-woven by fine roots and associated with some leaf residues) horizons, and of A horizon were collected in the Restingas, Tijuca Forest, Mussununga Forest, and Tabuleiro Forest, in 1990 (Babel, 1975; Malagon et al., 1989). In 1993, a more detailed study was performed in T1 and T2 sites, and 12 and 16 samples were collected in each site in summer and winter, respectively. A metal frame cm was used to collect the holorganic layers and also the A i horizon when present. A cylindrical core (10 cm in diameter, and 10 cm height) was used to collect the A horizon. The A i (A interface ) horizon constitutes a mineral horizon that varies from 0 to 2 cm in thickness located between the holorganic layers and the A horizon. It has a loose structure and is black coloured, because of the high amount of organic matter Sample treatment and analysis Twigs, seeds, and fine roots were separated from every horizon. Sorting was done using a 2-mm mesh sieve, enabling the quantification of the organic matter fine fractions. All 1 Raphael David dos Santos. Empresa Brasileira de Pesquisa Agropecuária-Centro Nacional de Pesquisa de Solos (EMBRAPA-CNPS), Jardim Botânico, 1024, Jardim Botânico, , Rio de Janeiro.

5 this material was dried at 60 jc, and weighed. The organic matter content of the holorganic layers was estimated by combustion and the nitrogen content was estimated on composite samples (three sub-samples) using a TECATOR Kjeltec Auto 1030 Analyzer. The surface foliar weight (SFW) was calculated by the following formula: SFW = DW/A, where DW is the mean of the dry weight of 30 leaf units of 1 cm in diameter, and A is the area of this unit. This physical analysis was done only for the L horizon because of the integrity of the leaves. The A i and A horizon samples were dried at 40 jc, sieved and separated into two categories: soil smaller than 2 mm (soil fine fraction) and very stable aggregates 2 to 10 mm in diameter (soil aggregate fraction). Analysis of carbon, nitrogen, nutrients and physical properties of the fine and aggregate (composite samples of three or four subsamples) fraction was carried out using methods developed by the Centro Nacional de Pesquisa de Solos of the Empresa Brasileira de Pesquisa Agropecuária (EMBRAPA, 1979). For details of soil analysis, see Garay et al. (1995) Statistical analysis A. Kindel, I. Garay / Geoderma 108 (2002) Comparisons between seasons in the Tabuleiro Forest (T1 and T2) were made using Student s t-tests. When data were not normally distributed, they were square root transformed before analysis. In the case of small sample numbers, as for the soil aggregate fraction (n = 3 and 4), the Mann Whitney U-test was chosen to perform comparisons (Siegel, 1975). 4. Results and discussion 4.1. Description of humus forms Maricá Restinga (R1): Dysmoder L, F, H, A The litter sequence in the sclerophyllous thickets humus form is the following: L (4 t ha 1 ), F (7 t ha 1 ) and H (15 t ha 1 ) horizon. At this site the H horizon accounts for almost 60% of the organic matter found in the holorganic layers (Table 1). The analysis of the A horizon showed that it was dominated by sand particles ( > 92%, Table 3), showing so a particulate structure with no kind of aggregation. The low ph (4.6) and base saturation (28%) added to the high C:N ratio (22) evidenced also the Dysmoder (Table 1). A parallel research, made by our study group, on edaphic mesofauna showed that ants dominated the soil community (unpublished data). Considering that enchytraeids are usually very abundant in Dysmoder of temperate region (Schaefer and Schauermann, 1990), their absence in this study site is a peculiarity of the soil fauna community Cardosa Island (R2): Mesotrophic Mull L, F, (H), A The Restinga situated on the island shore (R2) possesses the smallest accumulation of organic matter in the holorganic layers (LFH: 9.7 t ha 1 ), with the H horizon restricted to as little as 2 t ha 1 (Table 1). Smaller stocks of organic matter are a reflection of faster decomposition. The A horizon of this humus form showed base saturation of 44%, similar

6 106 Table 1 Means and standard deviations (in parentheses) of holorganic layers (L, F and H horizons) and A horizon Tabuleiro Forest Tijuca Forest Restinga Forest T1 (n = 10) T2 a MF (n = 10) TJ (n = 10) R1 (n = 10) R2 (n = 10) R3 (n = 10) R4 (n = 10) Holorganic layers L 2.20 (0.17) 1.52 (0.12) 2.85 (0.35) 0.85 (0.12) 4.00 (0.90) 3.15 (0.38) 1.29 (0.19) 2.51 (0.33) F residues 2.46 (0.22) 2.51 (0.13) 2.73 (0.23) 4.52 (0.70) 4.39 (0.48) 3.13 (0.67) 3.46 (0.51) 3.37 (0.48) F fine fraction 1.23 (0.21) 0.74 (0.09) 0.80 (0.16) 0.39 (0.12) 0.81 (0.06) 0.09 (0.04) 1.19 (0.60) 0.42 (0.14) H residues 0.50 (0.18) 3.55 (0.71) 5.86 (1.69) 1.98 (0.47) 1.21 (0.47) 3.41 (1.02) 3.60 (0.65) H fine fraction 1.01 (0.44) 11.9 (2.2) 5.35 (1.01) 15.1 (3.9) 2.13 (0.66) 8.97 (2.55) 4.86 (0.94) LFH 5.89 (0.46) 6.28 (0.64) 21.8 (2.8) 17.0 (2.3) 26.3 (4.7) 9.71 (1.41) 18.3 (3.4) 14.8 (1.2) A horizon C (%) 0.86 (0.12) 1.21 (0.06) 1.16 (0.27) 2.63 (0.49) 2.00 (0.57) 1.09 (0.19) 2.82 (0.31) 1.82 (0.20) N (%) 0.07 (0.01) 0.09 (0.00) 0.07 (0.01) 0.27 (0.05) 0.08 (0.02) 0.08 (0.01) 0.20 (0.02) 0.09 (0.01) C:N 12.6 (0.6) 13.1 (0.4) 16.9 (1.1) 10.1 (0.5) 22.0 (1.9) 14.2 (0.8) 13.6 (0.6) 19.5 (1.0) P (ppm) 2.80 (0.25) 5.61 (0.41) 3.0 (0.4) 4.5 (0.8) 3.30 (0.67) 6.80 (1.47) 7.20 (0.59) 4.50 (0.62) EB (meq 100 g 1 ) b 2.29 (0.36) 0.89 (0.06) 0.96 (0.16) 1.6 (0.4) 2.66 (0.76) 2.33 (0.74) 1.33 (0.16) 1.40 (0.31) Ca 2+ (meq 100 g 1 ) 1.73 (0.32) 0.30 (0.03) 0.38 (0.16) 0.84 (0.23) 1.69 (0.63) 1.50 (0.58) 0.26 (0.05) 0.69 (0.28) BS (%) 46.3 (5.0) 14.3 (1.0) 16.3 (2.8) 10.9 (1.4) 28.5 (4.6) 43.8 (4.2) 9.50 (0.90) 29.7 (6.3) ph H 2 O 5.6 (0.1) 4.5 (0.0) 4.6 (0.1) 4.4 (0.1) 4.6 (0.1) 5.2 (0.1) 4.3 (0.1) 5.0 (0.3) T1: Tabuleiro Forest, T2: Tabuleiro Forest neighbouring a stream, MF: Mussununga Forest, TJ: Tijuca Forest, R1: Maricá Restinga, R2: Cardosa Island (shore), R3: Cardosa Island (hill) and R4: Grumari Restinga. EB: exchangeable base; BS: base saturation. a The data presented for T2 corresponds to the mean of both seasons studied, summer (n = 12) and winter (n = 16) of Fig. 1 and Table 1. b The value of exchangeable bases corresponds to the sum of Ca 2+,Mg 2+,Na + and K +. A. Kindel, I. Garay / Geoderma 108 (2002)

7 A. Kindel, I. Garay / Geoderma 108 (2002) to the Mull from the Tabuleiro Forest described below; the amount of phosphorus (P) was twice (6.8 ppm) that of R1 site (3.3 ppm). The ph was 5.2 and the C:N ratio Cardosa Island (R3): Moder Mull L, F, H, A The transition between the F and H horizon was progressive: 3.4 t ha 1 of leaf fragments (F h ) were found adhering to the roots of the H horizon. The H horizon itself contributes to 50% of the total holorganic layers (18 t ha 1 ). Parallel to this accumulation, the A horizon was also rich in organic matter (2.8%) and nitrogen concentration (0.2%) with a C:N ratio of 14. The ph was 4.3 and the base saturation very low (9.5%). On one hand this humus form should be an Oligotrophic Mull, on the other hand the conspicuous discontinuity between the litter layers and the A horizon, represented by a thick H horizon, characterises a Moder (Table 1). Termites and ants dominated the mesofauna community too (unpublished data). Some termites were found inside the aggregates that constituted almost 50% of the weight of the A horizon. The aggregate fraction of this study site was not analysed Grumari Restinga (R4): Eumoder L, F, H, A The F horizons form a continuous transition toward the H horizon: 3.6 t ha 1 of leaf fragments (F h ) were found adhered to the root of the H horizon. The stock of organic matter in the H horizon (4.9 t ha 1 ) was three times less than that of the Dysmoder described for R1 and the double of that in R2. The chemical characteristics of the A horizon confirms the Eumoder humus form: both the ph (5) and the base saturation (30%) had low values while the C:N ratio was 19 (Table 1). The A horizon was structureless Tijuca Forest (TJ): Moder Mull L, F, H, A The humus profile was rich in organic matter, so that the L and F, F h and H horizon comprised 5.4, 5.9 and 5.4 t ha 1, respectively (Table 1). Accompanying these values, the carbon content of the A horizon was also high (2.6%), despite this the C:N ratio of the soil was low (10). Thus, in this forest we noticed another puzzling humus form. Under large amounts of superficial litter, with presence of the H horizon, typical of a Moder, we found an A horizon with low C:N ratio, typical of a Mull (see also Barros et al., 1994). The paucity of nutrients and the low ph reflected soil poverty Tabuleiro Forest (T1): Tropical Mesotrophic Mull L, F, A i,a In Table 1 we present the results of the research carried out in 1990, while Fig. 1 and Table 2 show data of the detailed study that was performed in this forest (1993), Tabuleiro Forest (T1) and Tabuleiro Forest neighbouring a stream (T2) in In the T1, the accumulation of organic matter (Fig. 1) and the soil fine and aggregate fraction carbon, nitrogen and exchangeable bases (Table 2) were similar between the wet summer and the dry winter, showing stability of the humus forms in this undisturbed system (Table 1; see also Garay et al., 1995). These results are in accordance with the statement of Duchaufour and Toutain (1985) that humus forms are stable in systems not disturbed by man. A second interesting feature is the presence of very stable soil aggregates. These aggregates correspond to 10% to 30% of the total weight of soil in both horizons A i and A. The aggregates are recognisable to the naked eye (2 to 10 mm in size) and are comprised

8 108 A. Kindel, I. Garay / Geoderma 108 (2002) Fig. 1. Organic matter stock in holorganic layers, L, F and H horizons, in the Tabuleiro Forest (T1) and in the Tabuleiro Forest neighbouring a stream (T2). n = 12 in the summer (s) and 16 in the winter (w). mainly of mineral particles, e.g., textural composition of aggregates of the Ai horizon in T1, clay: 26%, silt: 34.3%, fine sand: 14.4% and coarse sand: 25.3%. The remainder of the soil matrix was particulate and structureless (in this work named fine fraction). Another peculiarity is the existence of an interface mineral A i horizon of only 0 2 cm or 0 3 cm between the litter layers and the A horizon, where most of the nutrients and organic carbon are concentrated. An example is the quantity of carbon, which is four to five times greater in the A i horizon than in the A horizon (Table 2). Phosphorous (P), nitrogen (N) and calcium (Ca 2+ ) follows the same pattern. The aggregate fraction is also richer in carbon and nutrients, so that a fertility gradient can be described: the greatest values of C, N and exchangeable bases are found in A i horizon aggregates, followed by the A i horizon fine fraction and A horizon aggregates, with A horizon fine fraction exhibiting the smallest amounts of these elements (Table 2) (see also Garay et al., 1995; Kindel et al., 1999). Physical analyses reveals that despite the sandy texture of the A horizon fine fraction, containing only around 10% of clay (Table 3), the aggregate fraction is richer in fine particles (from 18% to 30% of clay). These data probably explains the higher fertility (expressed by the base saturation) observed, since clays are, together with humified organic matter, responsible for the soil cation exchange capacity (CEC). At the T1 site, Ca 2+ (Table 2) is the most important base, contributing to almost 80% of the sum of exchangeable bases. For this reason, the other bases (magnesium, potassium and sodium) were not considered in our analyses. In conclusion, a morphological discontinuity marks the transition between the leaf remains and the hemiorganic layer with absence of an H horizon, as a result of the fast decomposition. The A horizon is rich in exchangeable bases, so that the base saturation approaches 70% and 56% in the A i and A horizon, respectively. The ph is 6.0 and the C:N ratio ranges from 8 to only 12, indicating a well-humified organic matter. These results in the humus form being considered as a Tropical Mesotrophic Mull. This Mull was considered tropical, because of the presence of the A i horizon and the aggregates. In Mull humus forms of temperate regions, the A horizon is characterised by

9 Table 2 Means and standard deviations (in parentheses) of properties of the hemiorganic layers in the Tabuleiro Forest and in the Tabuleiro Forest neighbouring a stream Soil fine fraction Soil aggregate fraction A i horizon A horizon A i horizon A horizon Summer (n = 12) Winter (n = 16) t test Summer (n = 12) Winter (n = 16) t test Summer (n =3) Winter (n =4) U test Summer (n =3) Tabuleiro Forest C (%) 2.94 (0.46) 3.71 (0.48) o 0.75 (0.09) 0.71 (0.07) o 6.98 (1.22) 8.28 (0.62) o 1.49 (0.29) 1.79 (0.25) o N (%) 0.28 (0.04) 0.31 (0.04) o 0.09 (0.01) 0.08 (0.01) o 0.61 (0.12) 0.63 (0.03) o 0.17 (0.03) 0.20 (0.02) o P (ppm) 9.83 (1.01) 14.3 (1.63) * 2.25 (0.18) 2.50 (0.27) o 22.0 (1.73) (1.53) o 5.50 (0.87) 3.75 (0.25) o Ca 2+ (meq 100 g 1 ) 8.84 (1.46) 8.64 (1.23) o 2.13 (0.41) 1.55 (0.27) o 18.0 (3.25) 17.5 (2.16) o 4.40 (1.35) 3.53 (0.39) o EB (meq 100 g 1 ) 10.7 (1.7) 11.1 (1.5) o 2.8 (0.4) 2.1 (0.3) o 23.1 (3.9) 23.4 (3.1) o 5.4 (1.4) 4.6 (0.5) o CEC 14.0 (1.6) 15.9 (1.8) o 4.5 (0.4) 3.8 (0.4) o 29.4 (4.2) 34.2 (4.1) o 7.8 (1.6) 8.2 (0.5) o BS 72.8 (4.3) 68.0 (2.1) o 58.8 (5.2) 53.5 (2.8) o 77.5 (3.3) 68.1 (1.0) o 65.7 (5.5) 56.2 (3.0) o C:N 10.7 (0.5) 12.0 (0.2) * 8.3 (0.4) 9.4 (0.5) o 11.6 (0.4) 13.1 (0.5) o 8.9 (0.2) 9.1 (0.3) o ph H 2 O 6.3 (0.2) 5.9 (0.1) * 5.9 (0.2) 5.7 (0.1) o 6.3 (0.2) 5.8 (0.0) * 6.2 (0.2) 5.8 (0.1) o Clay (%) 8.2 (0.6) 7.2 (0.4) 26.0 (2.4) 24.0 (0.8) o 17.5 (0.0) 20.5 (0.7) Tabuleiro Forest neighbouring a stream C (%) 3.42 (0.24) 5.71 (0.68) *** 1.08 (0.07) 1.31 (0.08) * 5.58 (0.47) 5.29 (0.19) o 2.49 (0.21) 2.79 (0.48) o N (%) 0.23 (0.02) 0.35 (0.04) ** 0.09 (0.00) 0.09 (0.01) o 0.41 (0.04) 0.39 (0.01) o 0.21 (0.01) 0.20 (0.01) o P (ppm) 12.8 (0.76) 26.6 (2.72) *** 3.92 (0.36) 6.88 (0.46) *** 18.2 (2.81) 17.0 (2.04) o 9.50 (0.96) 9.00 (1.22) o Ca 2+ (meq 100 g 1 ) 2.43 (0.39) 3.99 (0.53) * 0.29 (0.04) 0.31 (0.05) o 3.03 (0.86) 2.70 (0.31) o 0.56 (0.15) 0.45 (0.05) o EB (meq 100 g 1 ) 4.5 (0.6) 7.3 (0.8) ** 0.8 (0.1) 0.9 (0.1) o 6.1 (1.4) 5.7 (0.5) o 1.6 (0.4) 1.4 (0.1) o CEC 14.3 (1.0) 21.0 (1.9) *** 6.1 (0.3) 6.6 (0.3) o 21.4 (1.6) 22.6 (0.7) o 11.2 (0.7) 12.5 (0.4) o BS 32.1 (4.0) 35.1 (2.7) o 14.0 (1.5) 14.6 (1.5) o 28.3 (6.2) 25.4 (2.9) o 14.3 (4.0) 11.3 (1.0) o C:N 14.9 (0.4) 14.8 (0.5) o 11.9 (0.5) 13.9 (0.4) *** 13.7 (0.3) 13.5 (0.3) o 11.8 (0.4) 13.5 (1.4) o ph H 2 O 4.8 (0.1) 4.6 (0.1) o 4.5 (0.1) 4.4 (0.1) o 4.6 (0.2) 4.5 (0.1) o 4.4 (0.1) 4.4 (0.1) o Clay (%) 11.7 (1.3) 10.2 (0.5) 30.7 (0.8) 28.5 (0.7) o 24.2 (1.1) 25.5 (0.7) o EB: exchangeable base; CEC: cation exchange capacity; BS: base saturation. t: parametric Student test; U: nonparametric Mann Whitney test. Winter (n =4) U test A. Kindel, I. Garay / Geoderma 108 (2002)

10 110 Table 3 Means and standard deviations (in parentheses) of some characteristics of the humus forms studied Tabuleiro Forest Tijuca Forest Restinga Forest T1 T2 a MF TJ R1 R2 R3 R4 L horizon N (%) 1.74 (0.02) 1.29 (0.05) 1.70 (0.14) 1.60 (0.08) 0.79 (0.11) 1.53 (0.34) 1.21 (0.05) 1.16 (0.12) C:N ratio 26.7 (0.3) 37.4 (1.1) 28.5 (2.2) 30.0 (1.4) 61.4 (6.5) 32.5 (5.0) 39.7 (1.2) 42.5 (3.5) SFW (mg cm 2 ) 7.8 (0.2) 8.7 (0.2) 8.9 (0.6) 8.1 (0.4) 14.3 (0.5) 7.6 (0.4) 8.1 (0.9) 8.9 (0.5) Soil properties Clay + silt (%) 11.6 (0.6) 15.3 (0.7) 8.3 (0.8) 11.6 (1.9) 7.2 (1.2) 7.3 (0.8) 22.5 (1.2) 4.8 (0.4) Soil type Podzólico (Ultisol) Podzólico (Ultisol) Podzol (Spodosol) Litossolo (Litosol) Ar. Quar. Al. (Psamments) Podzólico (Ultisol) Ar. Quar. Al. (Psamments) Podzol (Spodosol) Classification Tropical Tropical Eumoder Moder Mull Dysmoder Mesotrophic mull Moder Mull Eumoder Mesotrophic Mull Oligotrophic Mull T1: Tabuleiro Forest, T2: Tabuleiro Forest neighbouring a stream, MF: Mussununga Forest, TJ: Tijuca Forest, R1: Maricá Restinga, R2: Cardosa Island (shore), R3: Cardosa Island (hill) and R4: Grumari Restinga. SFW: Surface Foliar Weight. a The data presented for T2 corresponds to the mean of both seasons studied, summer and winter. A. Kindel, I. Garay / Geoderma 108 (2002)

11 A. Kindel, I. Garay / Geoderma 108 (2002) the presence of well developed clay mineral complex (represented by the microaggregates, not seen to the naked eye), and in this way it has a granular or occasionally blocky structure (Green et al., 1993; Berthelin et al., 1994). In the current literature of humus form classification, an A i horizon is not described (Green et al., 1993; Berthelin et al., 1994; Brethes et al., 1995), but something similar has been reported by Furch and Klinge (1989). These authors observed that the topsoil concentrates much more nutrients than the next deeper horizon in soils of the Terra Firme Amazon Forest. Despite the development of a Mull humus form in this forest, earthworms generally favoured by Mull soil conditions in temperate regions (Schaefer and Schauermann, 1990; Toutain, 1981) are not present; in fact, social insects dominated the soil macroarthropod communities (ants + termites: 2420 individuals m 2 ; total community: 4340 individuals m 2 ) (Pellens and Garay, 1999). As stated by Lavelle (1988), in environments where the dry season last more than 5 months, earthworms are replaced by termites Tabuleiro Forest neighbouring a stream (T2): Tropical Oligotrophic Mull L, F, (H), A i,a When the T2 site was analysed, some differences from the T1 site became evident (Fig. 1, Table 2). There is a higher accumulation of organic matter: both the holorganic (2.0 t ha 1 higher in T2 than in T1) and the hemiorganic layers (e.g., 3.7% in T1 vs. 5.7% in T2 in A i horizon in the winter) have higher carbon quantities in T2 than in T1 site. In the holorganic layers, the higher accumulation is due to larger amounts of L and to the presence of a thin H horizon (1.0 t ha 1 ), mainly in the winter. The seasonal stability observed in the A i and A horizons of T1 site did not occur for the soil in T2 site, e.g., C, N and exchangeable bases are about 60% higher in winter than in summer for the A i horizon (Table 2). As in the native forest, Ca 2+ is the most important exchangeable base, although at lower concentrations. Here the quantities of Ca 2+ can be seven times lower than in T1 (see also Kindel and Garay, 2001). In view of the more gradual transition from the holorganic to the hemiorganic layer reflected by the thin H horizon, and of the poor nutritional soil condition (the base saturation varies from 14 in the A to 35 in the A i horizon), the low C:N ratios and the ph of 5, humus form in the T2 site was considered as Tropical Oligotrophic Mull (Table 2). Here the A i horizon and some aggregates were also found. The textural composition of these aggregates is similar to that given for T1 (aggregates of the A i horizon, clay: 30.7%, silt: 16.3%, fine sand: 28.3%, coarse sand: 24.7%) Mussununga Forest (MF): Eumoder L, F, H, A A stock of about 22 t ha 1 of organic matter at different stages of decomposition was found deposited over the A horizon (Table 1). More than half of this quantity belonged to the H horizon. Attached to this horizon, a high amount of leaf fragments was found, contributing also to this important quantity of organic matter. In contrast to the other sites of the Tabuleiro region, MF site was not rich in Ca 2+ and so the concentrations of exchangeable bases were also very low (Table 1). Aggregates and the A i horizon were absent. The humus form at this site was considered as an Eumoder because of successive stages of litter layers, high C:N ratio (17), low base saturation (16%), and an A horizon dominated by loose material (see also Garay et al., 1995).

12 112 A. Kindel, I. Garay / Geoderma 108 (2002) Factors influencing humus form development In the four Restinga studied, both the litter quality and specific soil peculiarities are responsible for the distinct humus forms observed. The C:N ratio of the fallen leaves that constitutes the L horizon varies from 32 in R2 to 61 in R1. Thus, in the Restinga with the lowest availability of nitrogen in the fresh fallen leaves (R1 = 0.79%), a Dysmoder was recognised, while the one situated on the island shore, with the highest content of this nutrient (R2 = 1.53%), presented a Mull. The Restingas with intermediate values of nitrogen in the L leaves, the one on the island hill (R3 = 1.21%) and the dry remnant forest of Grumari (R4 = 1.16%), presented a Moder Mull and an Eumoder, respectively (Table 3). As in temperate regions and other tropical areas, low availability of nitrogen in the leaf litter inputs induces slow decomposition rates, with consequent accumulation of organic matter (Grubb et al., 1994; Medina and Cuevas, 1989; Swift et al., 1979). For example, Wesemael and Veer (1992), in a study carried out in different Mediterranean forests, including sclerophyllous ones, found a relationship between decreasing organic matter amounts in the holorganic layers and an increase in the N content of litter (0.57% to 0.93%), together with an increase in the decay constant k, that ranged from 0.07 to The decay constant is expressed as k = I/X, where I is the annual input to the forest floor and X is the mean litter standing crop (Olson, 1963). The humus forms described by these authors belonged to the Moder. For R1 site the decay constant is of 0.14, considering an input of 3.7 t ha 1 year 1 (Ramos and Pellens, 1994) and an accumulation of 25.6 t ha 1 (Table 1). Furthermore, surface foliar weight (SFW), considered as an index of sclerophylly (Medina et al., 1990; Rizzini, 2000), is in general positively correlated with lignin content and negatively with nitrogen concentration (Medina et al., 1990; Turner, 1994). The physical analyses made in our study corroborate this tendency. The SFW of fresh fallen leaves was inversely correlated to their nitrogen content, so that the weight of the leaves in R1 (14.3 mg cm 2 ) was the greatest, decreasing to 7.6 mg cm 2 in R2, which had the highest N content of the Restingas studied (Table 3). Considering the eight study sites, this correlation was also significant (r = 0,77, a = 0.03, n = 8). It seems that besides the litter quality, the soil chemical and physical properties also played an important role in humus form development. R1 and R4 sites have similar soil types, with a texture comprising more than 90% coarse particles (Table 3). The associated slow decomposition process (Moder humus forms, see Table 1) and the development of a considerable mat of roots in the H horizon (Fig. 2) could act as a mechanism against nutrient loss and was suggested by Herrera et al. (1978) for the poor and sandy Amazonian soils. Otherwise, in R2 and R3 sites, soil moisture, physical and nutrient conditions were better than in R1 and R4. The appearance of a Mesotrophic Mull in R2 can be explained by high amounts of P, and due to its topographic position near a beach resulting in increased moisture. In R3 site the development of a Moder Mull was possible because of higher clay and silt content in the A horizon (20%, Table 3). The presence of fine particles encourages good soil structure resulting in the formation of aggregates, enhancing soil moisture and aeration, and so favours specific faunal development and a consequent Mull

13 A. Kindel, I. Garay / Geoderma 108 (2002) Fig. 2. Amounts of roots in the H A horizon. n = 10 (T1, MF, TJ, R1, R2, R3 and R4); n = 28 (T2) and n =5 (because of stones in the A horizon we collected only five samples with roots in TJ). For legend see Table 1 or 3. humus form (Duchaufour and Toutain, 1985). On the other hand, low nutrient conditions (base saturation: 9.7%, Table 1) may lead to an interruption of the decomposition process with accumulation of organic matter in the H horizon. Here the root mat reached almost 3 t ha 1 (Fig. 2). A puzzling humus form was also found in TJ site: associated with a thick H horizon (Table 1 and Fig. 2), we found the lowest C:N ratio (10) recorded for all studied sites. Taking into account that the N content in the whole leaves, used as an indicator of litter quality, was high (1.6%), the quality of the litter was not the limiting factor for the decomposition process, reflected in the accumulation observed (LFH: 17 t ha 1 ). In fact, in this forest, the presence of a humus form with characteristics of both a Moder (presence of H horizon) and a Mull (low C:N ratio in the A horizon) must be related to the unfavourable properties of the Litosol: low fertility, revealed in the poor amounts of exchangeable bases (1.6 meq 100 g 1 ) and base saturation (11%), and the absence of fine sediments ( < 12%). In this case only the soil conditions seem to limit the decomposition process. Humus form with a double functioning pattern as those observed in R3 and TJ site have been described by Brethes et al. (1995) and named as Amphimull. In this humus form, the holorganic layer can be described morphologically as a Moder, while the A horizon is chemically like a Mull. But in the classification of Brethes et al. (1995), a crumb structure made by clay humus complexes characterised the A horizon. In our study sites, these structures were not found, and so we decided to use the term Moder Mull to identify this type of humus form in the Atlantic Forest. When the Tabuleiro Forest complex is analysed, it can be noted that the soil type played a decisive role in the decomposition process. Situated on a Ultisol and a Spodosol, the humus type at T1 and MF site were Mull and Eumoder, respectively, despite similar nitrogen content in the L horizon. The main difference between these two soil types is the presence of a Bt horizon in the Ultisol, with higher amounts of clay, probably used in the

14 114 A. Kindel, I. Garay / Geoderma 108 (2002) aggregates formation. In effect, the aggregate fraction is a very important sink of carbon and nutrients, since they accumulate these elements in relation to the A horizon fine fraction (Table 2). The presence of an interface A i horizon, between the holorganic horizons and the A horizon, rich in carbon and exchangeable bases, is evidence for the discrepancy between tropical Mull humus forms and temperate ones: in the tropics the nutrient cycle may be characterised by a surfacial functioning. Burnham (1989) designated as closed the nutrient cycle present in tropical forests, where there is little input of nutrients from the weathering of parent materials. In MF site, there was neither nutrient availability nor fine elements that might create condition favourable for the development of a Mull. The proximity of T2 site to a watercourse demonstrates that even natural disturbances can change the decomposition pathway. Louzada et al. (1997) measured the litterfall in T1 (5.0 t ha 1 year 1 ) and in T2 (3.9 t ha 1 year 1 ) site, and found that in the former, leaf input is almost 35% higher. Albeit smaller litterfall inputs T2 site showed accumulation of organic matter with development of a thin H horizon. The decomposition quotient k confirms the slower decomposition rate in T2. The quotient was calculated using the amount of carbon stock constituting all holorganic layers (L, F and H) presented in Table 2. The following values were estimated: 1.28 year 1 in T1 and 0.63 year 1 in T2. The soil nutrient condition linked to smaller L nitrogen concentration (T1: 1.74% vs. T2: 1.29%; a = 0.001) and to thicker leaves (T1: 7.8 mg cm 2 vs. T2: 8.8 mg cm 2 ; a = 0.002) certainly induced the modification of a Mesotrophic Mull in T1 site to an Oligotrophic Mull with litter accumulation in T2 site (Table 2). Rizzini (2000) found that the lignin:n ratio for the green leaves were two units greater in T2 site (9.8) than in T1 site (7.8) and that the SFW was correlated to the N content as to the C:N and lignin:n ratios. The diversity of humus form described in our work shows that humus forms are good indicator of ecosystem function, reflecting with accuracy the intimate relationship between soil and vegetation. Thus, management practices should consider humus form alteration in the light of natural process; e.g., T1 site analysed in this work, and its answers to disturbance caused by man s activities (Kindel et al., 1999; Garay and Kindel, 2001; Kindel and Garay, 2001). These authors, in a study carried out in Tabuleiro secondary forests submitted to selective logging or to slash and burn, showed that the decomposition process was substantially altered by these actions, resulting in the accumulation of organic matter and increase in soil fertility in one case and accumulation of organic matter and decrease in soil fertility in the other. 5. Conclusion In the Atlantic forest, the vegetation, soil, and microclimate conditions are very diverse. Similarly, the patterns of decomposition process reflected in humus form are highly variable. In the Atlantic Forest, we found six different humus forms at eight sites. The analysis of the humus forms and sites revealed that humus form could be a reliable and useful indicator of tropical forests decomposition processes.

15 A. Kindel, I. Garay / Geoderma 108 (2002) Furthermore, some characteristics, such as the interface A i horizon and the aggregate fraction, found in the hemiorganic horizons, were considered peculiar to the forests studied. Thus, we suggest that these features should be considered in the identification of the humus forms in Atlantic Forest ecosystems. Acknowledgements This research was financed by Fundacßão de Amparo a Pesquisa do Estado do Rio de Janeiro (FAPERJ), Universidade Federal do Rio de Janeiro (UFRJ), Fundacß ão José Bonifácio (FUJB) and Conselho Nacional de Pesquisa (CNPq) and started in the framework of Centre National de Recherche Scientifique (CNRS) CNPq (France Brazil) international cooperation program. It is also part of the National Program for Conservation and Restoration of the Biological Diversity, sub-project Conservation and Restoration of the Tabuleiro Atlantic Forest based on the Functional Evaluation of Biodiversity in Linhares, ES, which is financed by Global Environmental Facility-Banco Interamericano de Desenvolvimento/Ministério do Meio Ambiente-CNPq-FUJB. We wish to thank the Centro Nacional de Pesquisa de Solos (EMBRAPA-CNPS) for assistance in the soil analyses. We are especially grateful to the ex-students in the Laboratório de Ecologia de Solos of UFRJ (Andréa Callipo, Luis A. Santos, Luis G. Santos, Maria E.O. Barros) and to Andrew Macrae and Roseli Pellens for their help with the English language. We are also very grateful to Dr. Karel Klinka and Dr. Jean-Francßois Ponge for their useful comments on the manuscript. References Aerts, R., Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos 79, Anderson, J.M., Proctor, J., Vallack, H.W., Ecological studies in four contrasting lowland rain forests in Gunung Mulu National Park, Sarawak: III. Decomposition processes and nutrient losses from leaf litter. J. Ecol. 71, Araujo, D.S.D., Vegetation types of sandy coastal plains of tropical Brazil: a first approximation. Coastal Plant Communities of Latin America. Academic Press, New York, pp Araujo, D.S.D., Henriques, R.P.B., Análise florística das Restingas do Estado de Rio de Janeiro. In: Lacerda, L.D., Araujo, D.S.D., Cerqueira, R., Turcq, B. (Eds.), Restingas. Origem, Estrutura, Processos. CEUFF, Niterói, pp Babel, U., Micromorphology of soil organic matter. In: Gieseking, J.E. (Ed.), Soil Components. Organic Components, vol. 1 Springer, New York, pp Barros, M.E.O., Kindel, A., Garay, I., Formas de húmus em ecossistemas de Mata Atlântica. III Simpósio de Ecossistemas da Costa Brasileira. Academia de Ciências de São Paulo, São Paulo, vol. 2, pp Berthelin, J., Leyval, C., Toutain, F., Biologie des sols: rôle des organismes dans l alteration et l humification. In: Bonneau, M., Souchier, B. (Eds.), Pédologie, vol. 2. Constituants et propiétés du sol. Masson, Paris, pp Brethes, A., Brun, J.J., Jabiol, B., Ponge, J.F., Toutain, F., Classification of forest humus forms: a French proposal. Ann. Sci. For. 52, Burnham, C.P., Pedological processes and nutrient supply from parent material in tropical soils. In: Proctor, J. (Ed.), Mineral Nutrients in Tropical Forest and Savanna Ecosystems. Blackwell, Oxford, pp

16 116 A. Kindel, I. Garay / Geoderma 108 (2002) Camargo, M.N., Legenda preliminar de identificacßão de solos do Estado do Rio de Janeiro e critérios para separacßão de unidades de solos e fases. Reunião de classificacßão, correlacßão e interpretacßão de aptidão agrícola de solos, I, Anais. CNPS-EMBRAPA e SBCS, Rio de Janeiro, pp Camargo, M.N., Palmieri, F., Correlacßão aproximada das classes de solos da legenda preliminar do Estado de Rio de Janeiro com os sistemas FAO-UNESCO e Soil Taxonomy. Reunião de classificacßão, correlacßão e interpretacßão de aptidão agrícola de solos, I, Anais. CNPS-EMBRAPA e SBCS, Rio de Janeiro, pp Centro de informacßões e dados do Rio de Janeiro (CIDE), Anuário estatístico do estado do Rio de Janeiro. Governo do Estado do Rio de Janeiro (Secplan), Rio de Janeiro. Duchaufour, P., Toutain, F., Apport de la pédologie à l étude des écosystèmes. Bull. Ecol. 17, 1 9. EMBRAPA, Manual de métodos de análise de solos. EMBRAPA-CNPS, Rio de Janeiro, p EMBRAPA, Levantamento semidetalhado e aptidão agrícola dos solos do Município do Rio de Janeiro, RJ. Boletim Técnico CNPS-EMBRAPA, Rio de Janeiro. Furch, K., Klinge, H., Chemical relationships between vegetation, soil and water in contrasting inundation areas of Amazonia. In: Proctor, J. (Ed.), Mineral Nutrients in Tropical Forest and Savanna Ecosystems. Blackwell, Oxford, pp Garay, I., Kindel, A., Diversidade funcional em fragmentos de Floresta Atlântica. Valor indicador das formas de húmus florestais. In: Garay, I., Dias, B. (Eds.), Conservacßão da Biodiversidade em Ecossistemas Tropicais: Avancßos conceituais e revisão de novas metodologias de avaliacßão e monitoramento. Ed. Vozes, Petrópolis, pp Garay, I., Kindel, A., Jesus, R.M., Diversity of humus forms in the Atlantic Forest ecosystems (Brazil). The Table-land Atlantic Forest. Acta Oecol. 16, Gentry, A.H., Tropical forest biodiversity: distributional patterns and their conservational significance. Oikos 63, Green, R.N., Trowbridge, R.L., Klinka, K., Towards a taxonomic classification of humus forms. For. Sci. Monogr. 29, Grubb, P.J., Turner, I.M., Burslem, D.F.R.P., Mineral nutrient status of coastal hill dipterocarp forest and adinandra belukar in Singapore: analysis of soil, leaves and litter. J. Trop. Ecol. 10, Herrera, R., Jordan, C.F., Klinge, H., Medina, E., Amazon ecosystems. Their structure and functioning with particular emphasis on nutrients. Interciencia 3, Jesus, R.M., Mata Atlântica de Linhares: aspectos florestais. Seminário sobre desenvolvimento econômico e impacto ambiental em áreas de trópico úmido brasileiro a experiência da CVRD. Anais do Seminário, Rio de Janeiro, pp Kindel, A., Garay, I., Caracterizacßão de ecossistemas da Mata Atlântica de Tabuleiros por meio das formas de húmus. R. Bras. Ci. Solo 25, Kindel, A., Barbosa, P.M.S., Pérez, D.V., Garay, I., Efeito do extrativismo seletivo de espécies arbóreas da Floresta Atlântica de Tabuleiros na matéria orgânica e outros atributos do solo. R. Bras. Ci. Solo 23, Klinka, K., Wang, Q., Carter, R.E., Relationships among humus forms, forest floor nutrients properties, and understory vegetation. For. Sci. 36, Lavelle, P., Assessing the abundance and role of invertebrates communities in tropical soils: aims and methods. J. Afr., Lavelle, P., Blanchart, E., Martin, A., Martin, S., Spain, A., Toutain, F., Barois, I., Schaefer, R., A hierarchical model for decomposition in terrestrial ecosystems: application to soil of the humid tropics. Biotropica 25, Lima, H.C., Guedes-Bruni, R.R., Plantas arbóreas da Reserva Ecológica de Macaé de Cima. In: Lima, H.C., Guedes-Bruni, R.R. (Eds.), Serra de Macaé de Cima: diversidade florística e conservacßão em Mata Atlântica. Jardim Botânico, Rio de Janeiro, pp Louzada, M.A.P., Curvello, A., Barbosa, J.H.C., Garay, I., O aporte de matéria orgânica ao solo: quantificacßão, fenologia e suas relacßões com a composicßão específica em área de Floresta Atlântica de Tabuleiros. Leandra 12, Malagon, D., Sevink, J., Garay, I., Methods for soil analysis. In: Van der Hammen, T., Müeller-Dombois, D., Little, M.A. (Eds.), Manual of Methods for Mountain Transect Studies. Comparative Studies of Tropical Mountain Ecosystems. IUBS, Paris, pp

17 A. Kindel, I. Garay / Geoderma 108 (2002) Medina, E., Cuevas, E., Patterns of nutrient accumulation and release in Amazonian forests of the upper Rio Negro basin. In: Proctor, J. (Ed.), Mineral Nutrients in Tropical Forest and Savanna Ecosystems. Blackwell, Oxford, pp Medina, E., Garcia, V., Cuevas, E., Sclerophylly and Oligotrophic environments: relationships between leaf structure, mineral nutrient content, and drought resistance in tropical rain forests of the upper Rio Negro region. Biotropica 22, Meentemeyer, V., Macroclimate and lignin control of litter decomposition rates. Ecology 59, Meis, M.R.M., Contribuicßão ao estudo do Terciário superior e Quaternário da baixada da Guanabara. Tese de Doutorado, UFRJ, Rio de Janeiro. Melillo, J.M., Aber, J.D., Muratore, J.F., Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63, Muehe, D., Consequências higroclimáticas das glaciacßões quaternárias no relevo costeiro a leste da Baía de Guanabara. Rev. Bras. Geocienc. 13, Muehe, D., Evidências do recuo dos cordões litorâneos em direcßão ao continente no litoral de Rio de Janeiro. In: Lacerda, L.D., Araujo, D.S.D., Cerqueira, R., Turcq, B. (Eds.), Restingas. Origem, Estrutura, Processos. CEUFF, Niterói, pp Muehe, D., Lagoa de Araruama: geomorfologia e sedimentacßão. Caderno Geocienc. 10, Olson, J., Energy storage and the balance of producers and decomposers in ecological systems. Ecology 44, Peixoto, A.L., Gentry, A., Diversidade e composicßão florística da Mata de Tabuleiro na Reserva Florestal de Linhares (Espírito Santo, Brasil). Rev. Bras. Bot. 13, Pellens, R., Garay, I., Edaphic macroarthropod communities in fast-growing plantations of Eucalyptus grandis Hill ex Maid (Myrtaceae) and Acacia mangium Wild (Leguminosae) in Brazil. Eur. J. Soil Biol. 35, Perrin, P., Evolucßão da costa fluminense entre as Pontas de Itacoatiara e Negra: Preenchimentos e restingas. In: Lacerda, L.D., Araujo, D.S.D., Cerqueira, R., Turcq, B. (Eds.), Restingas. Origem, Estrutura, Processos. CEUFF, Niterói, pp Ponge, J.F., Heterogeneity in soil animal communities and the development of humus forms. Going Underground, Ecological Studies in Forest Soils, Ponge, J.F., Patzel, N., Delhaye, L., Devigne, E., Levieux, C., Beros, P., Wittebroodt, R., Interactions between earthworms, litter and trees in an old-growth beech forest. Biol. Fertil. Soils 29, Ramos, M.C.L., Pellens, R., Producßão de serapilheira em ecossistemas de Restinga em Maricá, Rio de Janeiro. Anais do Simpósio sobre Ecossistemas da Costa Brasileira, vol. 3. Acad. Sci. São Paulo, São Paulo, pp Ramos, M.C.L., Pellens, R., Lemos, L.C., Perfil florístico de dois trechos de mata litorânea no município de Maricá -RJ. Acta Bot. Bras. 15, Rizzini, C.T., Tratado de fitogeografia do Brasil, aspectos sociológicos e florísticos, vol. 2. Hucitec-Edusp, São Paulo, p Rizzini, C.M., Diversidade funcional do estrato arbóreo como indicador do status da biodiversidade em Floresta Atlântica de Tabuleiros (Linhares-ES). Tese de Doutorado, UFRJ, Rio de Janeiro. Rizzini, C.M., Aduan, R.E., Jesus, R.M., Garay, I., Contribuicßão ao conhecimento da Floresta Pluvial de Tabuleiros, Linhares, ES, Brasil. Leandra 12, Schaefer, M., Schauermann, J., The soil fauna of beech forests: comparison between a mull and a Moder soil. Pedobiologia 34, Siegel, S., Estatística não paramétrica para as ciências do comportamento. McGraw-Hill, Brasil, p Suguio, K., Martin, L.E., Dominguez, J.M.L., Evolucßão da planície costeira do Rio Doce (ES) durante o Quaternário: influência das flutuacßões do nível do marsimpósio do Quaternário no Brasil, vol. 4, pp Swift, M.J., Heal, O.W., Anderson, J.M., Decomposition in Terrestrial Ecosystems. Blackwell, Oxford, p Takahashi, M., Comparison of nutrient concentrations in organic layers between broad-leaved and coniferous forests. Soil Sci. Plant Nutr. 43, Toutain, F., Les humus forestiers. Structures et modes de fonctionnement. R. For. Fr. 33,

18 118 A. Kindel, I. Garay / Geoderma 108 (2002) Turner, I.M., Sclerophylly: primarily protective? Func. Ecol. 8, Ururahy, J.C.C., Collares, J.E.R., Santos, M.M., Barreto, R.A.A., As regiões fitoecológicas, sua natureza e seus recursos econômicos. Estudo fitogeográfico. Projeto Radam Brasil. Levantamento de Recursos Naturais, vol. 32. Ministério de Minas e Energia, Brasília. Wesemael, B., Veer, A.C., Soil organic matter accumulation, litter decomposition and humus forms under Mediterranean-type forests in southern Tuscany, Italy. J. Soil Sci. 43,

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