Changes in soil C and N stocks and nutrient dynamics 13 years after
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Forest Ecology and Management 255 (2008) 1516–1524 www.elsevier.com/locate/foreco
Changes in soil C and N stocks and nutrient dynamics 13 years after recovery of degraded land using leguminous nitrogen-fixing trees
M.O. Macedo
C.P. Jantalia
, A.S. Resende
, E.F.C. Campello
,
, A.A. Franco
a
Soil Science Department, Federal Rural University of Rio de Janeiro (UFRRJ), Rodovia BR 465, km 7, CEP 23890-000, Serope´dica, RJ, Brazil b
Brazilian Agricultural Research Corporation, National Agrobiology Research Center (Embrapa Agrobiologia),
Rodovia BR 465, km 7, CEP 23890-000, Serope´dica, RJ, Brazil c
Institute of Agronomy, Federal Rural University of Rio de Janeiro (UFRRJ), Rodovia BR 465, km 7, CEP 23890-000, Serope´dica, RJ, Brazil
Received 4 April 2007; received in revised form 9 November 2007; accepted 10 November 2007
Abstract
In tropical forest areas with highly weathered soils, organic matter plays an important role in soil functioning and forest sustainability. When forests are clear-cut, the soil begins almost immediately to lose organic matter, triggering a series of soil degradation processes, the extent and intensity of which depends on soil management. Depending on the level of soil degradation, the rate at which the system can re-establish itself can be slow and may require the use of degraded land restoration techniques. This study aimed at evaluating the potential of pioneer leguminous nitrogen-fixing trees to recuperate degraded land. The area studied – located in the coastal town of Angra dos Reis in the State of Rio de Janeiro,
Brazil – was planted with seven species of fast-growing leguminous nitrogen-fixing trees in 1991. The nutrient concentrations (Ca, Mg, P and K) and N and C stocks in the soil and litter were determined, in addition to the free- and occluded-light fractions of soil organic matter. Soil samples were also collected from two reference areas: (1) an area of undisturbed native forest; and (2) a deforested area spontaneously colonised by Guinea grass ( Panicum maximum ). The nutrient stocks in the litter of the restored area were similar to those found in native forest. The recuperation technique used was able to re-establish the soil C and N stocks after 13 years. C and N increased by 1.73 and 0.13 Mg ha
1 year
1
, respectively.
The free-light fraction was highest in the recuperated area and lowest in the deforested area. The occluded-light fraction of the recuperated area was higher than that of the native forest only in the 0–5 cm layer. Both the free-light and occluded fractions were higher in the native forest and recuperated areas than in the deforested area. Since the free-light and the occluded-light fractions are the result of litterfall and decomposition, these results – combined with the data of litter stocks and soil C and N stocks – indicate that the use of legume trees was efficient in re-establishing the nutrient cycling processes of the systems. These results also show that recovering degraded land with this technique is effective in sequestering carbon dioxide from the atmosphere at high rates.
# 2007 Elsevier B.V. All rights reserved.
Keywords: Atlantic forest; Carbon sink; Climate change; Forest soil; Nutrient cycling; Rehabilitation of degraded land
1. Introduction
Most tropical forests grow on highly weathered soils that contain low activity clays and have low natural fertility and pH
(
Bayer and Mielniczuk, 1999; Whittaker, 1975 ). Because of
this, these systems depend on efficient nutrient cycling based on
litter deposition and decomposition ( Vitousek, 1984 ). In
addition, in these soils, soil organic matter plays an important role in the soil’s cation exchange capacity (CEC), retention of base ions, soil aggregation and is directly related to nutrient
* Corresponding author. Tel.: +55 21 2682 1500; fax: +55 21 2682 1230.
E-mail address: bob@cnpab.embrapa.br
(R.M. Boddey).
0378-1127/$ – see front matter # 2007 Elsevier B.V. All rights reserved.
doi: 10.1016/j.foreco.2007.11.007
availability, especially soil nitrogen (
1999; Craswell and Lefroy, 2001; Six et al., 2002b ). In addition
to being a major factor contributing to good soil functioning,
SOM represents the third largest terrestrial carbon reservoir,
with an estimated global total of 1550 Pg C ( Lal, 2004
). Many studies have shown that tropical forests store large quantities of
C in their biomass and soil ( Brown and Lugo, 1992; Pregitzer and Euskirchen, 2004
). However, the role of forests and soil as sink and/or source of greenhouse gases is still a matter of discussion (
Brown and Lugo, 1992; Hugues et al., 2002;
Bellamy et al., 2005; Keppler et al., 2006 ).
When tropical forests are clear-cut, the deforested soil begins almost immediately to lose organic matter. Depending
M.O. Macedo et al. / Forest Ecology and Management 255 (2008) 1516–1524 on how the soil is managed, the loss of organic matter can be
fast ( Tiessen et al., 1994 ) and trigger a series of soil degradation
processes. Depending on the level of soil degradation, the rate at which the system can be re-established can be slow (
Vitousek et al., 1989; Brown and Lugo, 1992; Guariguata and Ostertag,
2001 ). This occurs because the regeneration of forest
ecosystems depends on different factors, including seed fall,
the intensification of degradation processes. Thus, depending on the level of soil degradation, the use of degraded land restoration techniques is indicated to re-establish the plant community. In the case of nutrient availability, studies indicate that depending on the previous use of degraded land, nitrogen is probably the most important limiting factor to the reestablishment of forest communities (
Tilman, 1985; Vitousek et al., 1989
).
After investing many years of research to identify tropical legume trees that form efficient N
2
-fixing symbioses (
Faria et al., 1984, 1987; Faria, 1995
) and respond well to inoculation
with arbuscular mycorrhizal fungi ( Monteiro, 1990 ), research
scientists at Embrapa Agrobiologia began to conduct experiments using these species in association with these organisms to rehabilitate degraded areas (
). Because of the effectiveness of these associations, legume trees species were selected that not only can establish under harsh conditions, but also produce high biomass yields of low C:N ratio (
Franco and Faria, 1997; Costa et al., 2004; Macedo et al.,
2006 ). In this way, it is expected that after a few years, organic
matter and nitrogen will be incorporated into the soil, contributing to the establishment of new and more demanding plant species.
The objective of this study was to examine the effect of this technique of soil rehabilitation using leguminous nitrogen-fixing trees on the recovery of nutrient cycling processes and soil C and
N stocks 13 years after planting. Since soil is a large C reservoir and considering the fact that very large extensions of degraded land are located in the Atlantic forest region of the country, the potential of these areas to serve as a sink for atmospheric CO
2 with the use of this technology was also examined.
2. Material and methods
2.1. Study area
The study area was located in the town of Angra dos Reis, along the western coast of the State of Rio de Janeiro,
23 8 02
0
30
00
S and 44 8 11
0
30
00
W, 100–200 m above sea level, within the limits of the Atlantic Forest biome. Before European colonisation in the early sixteenth century, the Atlantic Forest biome occupied approximately 100 million ha (Mha) (
). However, satellite surveys showed that the area of native forest had been reduced to only 165,000 ha, or 8% of the original forest area by 1990. According to Ko¨ppen’s method, the climate of Angra dos Reis is classified as Af, moist tropical forest. Average annual precipitation and temperature are
2300 mm and 22.5
8 C, respectively, without a distinct dry
1517
). The area is steeply sloping and the soil is classified as a Ferrosol (Red Yellow Argisol according to the
Brazilian Soil Classification System 1999).
In 1991, when the area was dominated by grass vegetation, the topsoil was removed from the site and used for the foundations of a shopping mall. Exposure of the soil to rain led to severe soil erosion, which after a short period of time resulted in the formation of erosion gullies. The area was restored by planting seedlings of Acacia mangium , Acacia auriculiformis ,
Enterolobium contortisiliquum , Gliricidia sepium , Leucaena leucocephala , Mimosa caesalpiniifolia , and Paraserianthes falcataria , all of which inoculated with rhizobia and arbuscular mycorrhizal fungi. The recovered area was approximately 1 ha in size.
To prepare the seedlings, the dormancy of the seeds was broken with hot water at 80 8 C. After the hot water pretreatment, the seeds were soaked in water for 24 h. Next, the seeds were inoculated with rhizobia strains (
) produced by Embrapa Agrobiologia. Subsequently the seeds were planted in plastic bags containing 150 cm
3 of a mixture of
10% phosphate rock, 30% cow manure, 30% sand and 30% clay. The rhizobium inoculant consisted of a sterilized mixture of peat, CaCO
2 and live rhizobia bacteria grown on a culture medium. Small holes (3 cm 3 cm 3 cm) were made in the plastic bags and portions of 1 g of arbuscular mycorrhizal fungi inoculant were introduced through the holes into the substrate prior to planting the seeds. This arbuscular mycorrhizal fungi inoculant consisted of a mixture of two different fungi species,
Glomus clarum and Gigaspora margarita , both of which are produced by Embrapa Agrobiologia. This inoculant consisted of colonized roots of Brachiaria decumbens , spores and soil from culture pots. The seedlings were transferred to the field after they had reached a height of approximately 30 cm and planted in holes (20 cm 20 cm 20 cm) at a spacing of
2 m 2 m between the plants. One litre of chicken manure was applied to each hole. To avoid further erosion, when the seedlings were planted, bamboo stems were anchored
Table 1
Rhizobia strains inoculated onto seedlings of legume tree species used to recover degraded areas
Name
Acacia auriculiformis
Rhizobia strain
Acacia mangium
BR 3465
BR 3609
BR 3609
BR 6009
Enterolobium contortisiliquum
Gliricidia sepium
Leucaena leucocephala
Mimosa caesalpiniifolia
Paraserianthes falcataria
BR 4406
BR 4407
BR 8801
BR 8803
BR 827
BR 825
BR 3407
BR 3446
BR 5609
BR 5612
1518 M.O. Macedo et al. / Forest Ecology and Management 255 (2008) 1516–1524
Table 2
Bulk density and texture in the soil profile at different depth increments (total depth 0–60 cm) of recovered, native forest and deforested areas, in Angra dos
Reis, RJ ( n = 3)
Areas Depth
(cm)
Bulk density
(g cm
3
)
Sand
(g kg
1
)
Silt Clay
Native forest
Recovered
Deforested
0–5
5–10
10–20
20–30
30–40
40–60
0–5
5–10
10–20
20–30
30–40
40–60
0–5
5–10
10–20
20–30
30–40
40–60
1.11
1.34
1.37
1.35
1.43
1.52
1.23
1.19
1.28
1.51
1.55
1.59
1.21
1.37
1.35
1.52
1.55
1.52
668
591
536
539
533
523
643
501
519
545
524
546
509
508
509
494
469
486
132
122
131
114
100
84
164
226
191
182
183
174
151
145
138
146
177
167
253
287
333
347
367
393
193b
273
280
273
293
280
340
347
353
360
353
347
. Soil samples were analysed for the following parameters: pH in water; exchangeable Al, Ca and Mg extracted with 1 M KCl, P and K extracted with a double acid solution (0.025 M sulphuric acid and 0.05 M hydrochloric acid
– Mehlich-1 extractant) according to the standard methods of
Embrapa (1997) . Total N was determined using semi-micro
Kjeldahl digestion followed by distillation and titration using a
Kjeltec auto distillation–titration unit (
Samples for total C analysis were ground very finely
( < 100 mesh) using a roller mill and measured using a LECO
CHN-600 analyser after total combustion. The soil C and N stocks were calculated from the C and N concentrations measured at each depth interval multiplied by the respective bulk density and the thickness values of the corresponding soil layer. These soil C and N stocks were then corrected for differences in bulk density between the soil of the study area and the soil under the native forest according to the method described by
. The objective of this soil mass correction was to avoid overestimation of C and N stocks that would result from directly comparing soils with different degrees of compaction.
2.3. Physical fractionation of soil organic matter crosswise in the erosion channels or gullies to slow down the rainwater running down the slope.
The samples were collected from the two reference areas and the area rehabilitated with legume trees. One of these reference areas was a fragment of native forest (Atlantic Forest), with few signs of human presence or disturbance, while the other consisted of 2 ha of deforested land. These three areas are located in close proximity to each other on the same hillside.
The deforested area is approximately 0.5 ha in size and overgrown with Panicum maximum . The topsoil of this area was not completely removed as in the case of the rehabilitated area.
The soils of the reference and study areas were slightly different
in terms of bulk density and texture ( Table 2 ). Based on the
results of texture analysis of the samples, the soil of the areas is classified as clay loam (
).
2.2. Soil analysis
In September 2004, soil samples were collected from the following depth intervals: 0–5, 5–10, 10–20, 20–30, 30–40 and
40–60 cm. The samples were collected from three replicate trenches excavated to a total depth of 70 cm and spaced 4 m apart. Soil bulk density was estimated from samples collected using volumetric rings at each depth interval. Four soil bulk density samples were used. Additional samples were taken from each depth interval for chemical analyses. To perform the chemical analyses, three sub samples were collected. Three samples were utilised for each area.
The bulk density samples were dried at 105 8 C for > 72 h, weighed and then discarded. The samples for analysis of texture, nutrient and C concentration were air-dried and sieved to 2 mm. Soil texture was determined by the densimeter method developed by
as adapted by
Physical fractions of soil organic matter were separated from soil samples taken at the 0–5, 5–10, 10–20 and 20–30 depth intervals. The free-light fraction was obtained by flotation in a sodium iodide solution (NaI) at a density of 1.80 g cm
3 as proposed by
and modified by
(2002) . Five grams of air-dried soil was added to 40 ml NaI
solution and the mixture gently stirred for 30 s and left to stand for 48 h at room temperature. Next, the supernatant was vacuum filtered (Aseptic Sterefil System. 47 mm – Millipore) through glass-fibre filters (diameter 47 mm; 2 m m – Whatman type GF/A). The material retained by the filter – the free-light fraction – was washed with distilled water to rinse out the NaI, dried for 48 h at 65 8 C, and weighed. Once the free-light fraction had been collected, the soil sample suspended in the
NaI solution was gently stirred and then dispersed ultrasonically with an energy input of 400 J ml
1
, for three minutes
(Branson Sonifer 250). The suspension was left to stand at room temperature for 48 h, after which the floating material was removed and filtered as described above to obtain the free light fraction. The material retained by the filter, the ‘‘occluded light fraction’’, was washed with distilled water, dried at 65 8 C for
48 h, and weighed.
2.4. Litter stocks
The amount of standing litter on the soil surface and its Ca,
Mg, P, K and N content were determined on samples from the recovered and native forest areas. Five samples were collected during the dry (September 2004) and rainy season (March
2005). The samples were taken using a steel quadrant frame
(0.25 m
2
). The collected samples were dried at 65 8 C, and weighed. The material was divided into leaf, shoot and decomposed litter (i.e. decaying material the nature of which
2.5. Statistical analysis
The results were submitted to normality analysis (Lilliefors.
1%) and error variance homogeneity (Cochran 1%). Once the variance analysis presuppositions were attained, or at least the variance homogeneity errors, analysis of variance (5%) was performed, followed by the Bonferroni ‘ t ’ test (5%). When the variance analysis presuppositions were not attained, the data were transformed by ln( x ). When the variance presuppositions were not attained, even after transformation of the results, the nonparametric Wilcoxon test was used. To verify the correlation between soil carbon and soil nitrogen, Pearson’s correlation analysis was applied.
M.O. Macedo et al. / Forest Ecology and Management 255 (2008) 1516–1524 could not be identified), weighed and ground prior to chemical analysis. Total N was determined on 200 mg samples as described above for the soil samples. Total P, K, Ca and Mg were determined after digestion in a nitric acid/perchloric acid mixture (
). The concentration of phosphorus (P) was determined by the molybdate blue method using ascorbic
acid as reducing agent ( Braga and Defelipo, 1974
), potassium
(K) by flame photometry and calcium (Ca) and magnesium
(Mg) with atomic absorption spectrophotometry. Nutrient stocks were calculated by multiplying the nutrient concentration (g kg
1
) by the litter mass (kg ha
1
).
1519
Table 3
C and N concentration and C:N ratio in the soil profile at different depth increments (total depth 0–60 cm) of recovered, native forest and deforested areas in Angra dos Reis, RJ ( n = 3)
Recovered Native forest Deforested Depth (cm)
C (g kg
1
)
0–5
5–10 ns
10–20
20–30 ns
30–40 ns
40–60 ns
N (g kg
0–5
5–10
10–20
1
20–30
30–40 ns
40–60 ns
)
C:N
0–5 ns
5–10 ns
10–20 ns
20–30 ns
30–40 ns
40–60 ns
18.5a
15.0
13.6ab
11.2
1.7
9.6
1.3
6.0
1.68a
1.37a
1.22a
1.04a
0.69
0.52
11
11
11
10
14
11
0.4
1.4
0.8
0.8
0.15
0.14
0.11
0.11
0.07
0.04
0.8
2.0
1.6
1.3
2.3
1.0
17.5ab
16.0
16.1a
2.4
1.6
1.8
10.5
2.7
10.9
2.9
10.2
1.90a
1.69a
1.33a
1.04a
0.82
0.76
9
10
12
10
145
16
4.3
0.12
0.11
0.10
0.13
0.14
0.18
1.0
0.3
1.0
3.5
6.3
9.1
11.0b
9.9
9.3b
0.4
0.1
0.3
6.8
1.5
6.2
1.9
6.2
0.99b
0.76b
0.73b
0.61b
0.62
0.65
12
13
12
11
10
9
2.1
0.17
0.06
0.05
0.06
0.01
0.03
2.4
0.8
1.4
3.0
3.1
3.1
Numbers followed by the same letter are not significantly different according to the Bonferroni ‘‘ t ’’ test (5%).
standard error; ns, not significant.
3. Results
3.2. The free and occluded-light fraction
3.1. Soil C and N concentrations and stocks
The free-light fraction of the areas investigated exhibited differences only in the 0–5 cm soil depth interval, with the recovered area having the highest and the deforested area the lowest concentration (
Table 5 ). The occluded-light fraction
concentration of the recovered area was higher than the native forest in the 0–5 cm soil depth, but the reverse was observed in the 5–10 cm depth interval. It was not possible to measure the occluded-light fraction of the soil of the deforested area because the values were too low.
The C and N concentrations in the soil of the recuperated area were higher than in the soil of the deforested area, and
similar to C and N values of the native forest soil ( Table 3
). The
C:N ratio did not differ among the three areas investigated and remained constant for all depths (
).
shows that the
N concentration correlated closely with the C concentration
(Pearson correlation).
The three areas exhibited no significant differences in soil C and N stocks at the individual depth intervals, in addition to having similar total soil C stocks across the 0–60 cm depth
range ( Table 4 ). However, although the total soil C stocks of the
0–60 cm depth range were similar between the areas, it is possible to conclude that the recovered areas were actually in the process of recovery. Assuming that the C stock of the deforested area is equivalent to the C stock of the recovered area prior to planting the legume trees, it may be concluded that the soil C stock increased by 23 Mg ha
1 in 13 years.
The soil N stocks of the three areas exhibited marked differences at some depth intervals. In the soil underneath the recovered and native forest, the N stocks were similar in the 0–
30 cm depth range, and higher than in the corresponding soil
layer of the deforested area ( Table 4
). Similarly to what was observed for the stocks of soil C, the N stocks in the 0–60 cm depth range of the recovered soil were higher than in the deforested soil, but lower than that of the native forest soil. The results of the recovered area showed that the soil N stock had increased by 1.7 Mg ha
1 over 13 years.
Fig. 1. Soil C and N Pearson’s correlation of the areas investigated and located in Angra dos Reis, RJ, Brazil.
1520
3.3. Litter stock
M.O. Macedo et al. / Forest Ecology and Management 255 (2008) 1516–1524
Table 4
C and N stocks (0–60 cm) in the whole soil profile of recovered, native forest and deforested areas in Angra dos Reis, RJ ( n = 3)
Native forest Deforested Depth (cm)
C stock (Mg ha
0–5 ns
5–10 ns
10–20 ns
20–30 ns
30–40 ns
40–60 ns
1
)
0–30 ns
0–60
Recovered
10.9
10.6
19.7
15.9
14.4
21.5
0.2
1.0
1.2
2.4
1.9
2.7
54.8
2.1
88.1ab
0.4
0–5 ns
(Mg ha
5–10 ns
10–20
20–30
30–40 ns
40–60
1
)
0.94
0.08
0.92
0.09
1.67a
0.15
1.41ab
0.14
0.98
0.10
1.75b
0.12
0–30
0–60
5.0a
0.4
7.7ab
0.3
12.0
10.9
21.7
16.8
17.9
34.1
58.3
107.7a
1.27
2.54a
5.4a
9.1a
1.5
1.0
2.5
4.3
4.8
14.4
7.7
22.1
1.17
0.07
1.00
0.06
1.70a
0.12
1.57a
0.18
0.21
0.56
0.2
0.9
7.1
7.2
13.3
11.0
10.1
19.8
35.4
65.1b
0.3
0.1
0.5
2.4
3.0
6.7
1.7
11.2
0.59
0.10
0.52
0.04
0.99b
0.07
0.94b
0.08
0.97
1.96ab
3.0b
6.0b
0.02
0.09
0.1
0.1
Numbers followed by the same letter are not significantly different according to the Bonferroni ‘‘ t ’’ Test (5%).
, standard error; ns, not significant.
*
Data transformed by ln( x ).
during the rainy season, in both areas. The Mg stock of the leaf fraction was higher during the dry season in the recovered area and during the rainy season in the decomposed fraction, in both areas. The P concentration differed between seasons in all fractions. In the leaf and stem fractions, the highest P stocks were observed during the dry season in both areas. The K stocks, similarly to what was observed relative to the N stock, were higher during the rainy season in the decomposed and total litter of both areas. The native forest exhibited the highest
N stock in the decomposed fraction during the dry season.
3.4. Soil fertility
The soils of the investigated areas can be classified as very acid. The native forest area showed the lowest pH values, congruent with the higher Al concentration found ( higher concentration found in the recovered area (
). As the Ca and Mg concentrations were individually very low, they were analysed together. The Ca + Mg concentration only showed differences in the 0–5 cm depth interval, with the
spite of the fact that the P concentrations were very low, the values measured were different between the areas in the respective 0–5 cm, 5–10 cm and 10–20 cm layers. In this case, the highest concentrations were observed in the native forest
and the lowest in the deforested area ( Table 9
). The highest K concentrations were found in the native forest and recovered areas. These areas were found to contain similar concentrations
of K in the two first layers (0–5 cm e 5–10 cm) ( Table 9 ).
The litter stocks of the recovered and native forest areas
were statistically similar for both seasons evaluated ( Table 6
).
However, the results were different when the different litter fractions were considered. The leaf fraction of the recovered area, as well as the decomposed fraction of both areas exhibited differences between the seasons. The largest amounts of leaf litter were observed during the dry season on the recovered area. And the largest amount of decomposed matter during the rainy season on both the recovered and native forest areas.
The nutrient stocks exhibited differences between seasons
(
). The leaf fraction showed the highest values for Ca stock during the dry season, and the decomposed fraction
4. Discussion
4.1. Soil C and N concentrations and stocks
Table 5
Free- and occluded-light fraction in the soil profile at different depth increments
(0–30 cm) of recovered, native Forest and deforested areas in Angra dos Reis,
RJ ( n = 3)
Native forest Deforested Depth (cm) Recovered
Free-light fraction (g kg
0–5
5–10 ns
10–20 ns
20–30 ns
1
18.8a
1.4*
6.1
4.8
3.3
)
0.3
0.9
0.1
Occluded-light fraction (g kg
0–5 5.22a
1
)
1.59
5–10
10–20 ns
20–30 ns
1.60b
1.39
0.75
0.75
0.86
0.18
12.7b
4.5
4.1
2.8
2.40b
2.70a
1.00
0.54
1.3
0.5
1.0
1.6
0.35
1.47
0.53
0.30
6.8c
3.6
2.9
2.6
tr** tr tr tr
0.3
0.8
1.5
1.0
Numbers followed by the same letter are not significantly different according to the Bonferroni ‘‘ t ’’ test (5%).
, standard error; ns, not significant.
**tr trace – too low to be determined.
The soil C and N results showed that the legume trees, in association with the nitrogen-fixing bacteria and arbuscular mycorrhizal fungi, were able to restore the level of these two nutrient elements in a short period of time. Other studies have shown the increase of soil C and N during forest development
(
Brown and Lugo, 1990; Gleason and Tilman, 1990;
). On the other hand, a number of studies did not observe any discernible patterns in mineral soil
C related to or influenced by land use or forest age (
).
Soil N increase is very important in degraded land rehabilitation projects, since, according to
(1994) , it enhances the capacity of the system to support a more
complex community. According to some studies, the availability of higher concentrations of this nutrient element in the course of ecological succession promotes an increase in the number of tree species on plots that are in the sucessional
process ( Davidson et al., 2004; Francis and Read, 1994 ).
observed an increase in biomass during the early stages of the succession process, when nitrogen was added on soil. In addition, the higher N concentrations reduced individual plant mortality during the trial.
The N increase is directly related to C incorporation, as indicated by Pearson’s correlation coefficient (
M.O. Macedo et al. / Forest Ecology and Management 255 (2008) 1516–1524 1521
Table 6
Total nutrient content of different litter fractions on native forest, recovered and deforested areas in Angra dos Reis, RJ, Brazil, collected during the dry and rainy season ( n = 5)
Leaves
Dry Rainy
Stem
Dry Rainy
Decomposed
Dry Rainy
Total
Dry Rainy
Area (kg ha
1
)
Native forest
Recovered
CV (%)
1278
1725
Aa
Aa
855
543
Aa
Ab
1419
1463
Aa
Aa
1088
1935
Aa
Aa
2312
2765
Ab
Ab
3809
4308
Aa
Aa
5009
5954
Aa
Aa
5753
6786
Aa
Aa
44.97
29.47
37.34
A different superscript letter indicates a significant difference between the areas in the same season according to the Bonferroni test ‘‘t’’ p < 0.05. A subscript letter indicates a significant difference between the seasons relative to the same area according to the Bonferroni ‘‘ t ’’ test, p < 0.05.
*
Data transformed by ln( x ).
Table 7
Nutrient content of different litter fractions on native forest and recovered areas located in Angra dos Reis, RJ, Brazil, collected during the dry and rainy seasons
( n = 5)
Area Leaves
Dry Rainy
Stems
Dry Rainy
Decomposed
Dry Rainy
Total
Dry Rainy
Ca (kg ha
1
)
Native forest
Recovered
CV (%)
Mg (kg ha
1
)
Native forest
Recovered
CV (%)
P (kg ha
1
)
Native forest
Recovered
CV (%)
K (kg ha
1
)
Native forest
Recovered
CV (%)
N (kg ha
1
)
Native forest
Recovered
CV (%)
11.0
14.0
4.0
4.8
1.5
1.9
13.2
13.8
a a a a a a
0.21
0.33
b b
61.1
68.1
65.2
6.4
4.1
3.0
1.5
a b a b
0.29
0.22
5.3
4.3
14.4
9.0
a a b b
10.6
10.9
3.1
2.8
1.5
2.0
1.5
1.6
11.6
7.6
a a a b
80.64
83.6
85.7
6.3
10.9
1.6
3.0
0.20
0.36
3.2
8.5
11.9
20.9
a a b b
15.5
12.2
5.6
4.0
2.7
2.9
0.36
0.24
21.7
15.4
b b b b a a b b
Ab
Bb
26.2
36.1
34.9
7.9
27.2
30.1
12.3
12.6
1.6
2.4
20.8
20.8
72.0
80.1
a a a a b a a a
A
A a a
37.7
41.1
12.8
12.1
6.0
7.3
2.3
2.3
46.5
39.4
a a b b b b
36.7
40.8
7.6
6.6
45.0
40.7
19.1
14.2
2.1
2.2
33.4
32.3
89.1
b b a a a
104.08
a
37.7
A different superscript letter indicates a significant difference between the areas in the same season according to the Bonferroni ‘‘ t ’’ test p < 0.05. A subscript letter indicates a significant difference between the seasons relative to the same area according to the Bonferroni ‘‘t’’ test, p < 0.05.
*
Data transformed data by ln( x ).
**
Non-parametric Wilcoxon test.
their ability to fix nitrogen in the soil, legume species have been used as an N source in a series of tropical system development projects, including pastures (
), no-till fields (
Sisti et al., 2004 ), tree-farming (
agroforestry ( Handayato et al., 1995 ). These projects are
aimed not only at incorporating N, but also at raising the organic matter content of the soil. Organic matter is very important in tropical soils since it plays an crucial role in the formation and maintenance of soil structure, fertility, nutrient and water availability (
Bayer and Mielniczuk, 1999; Craswell and Lefroy, 2001; Six et al., 2002b
). The soil C:N ratio remained stable in the three areas studied and was not influenced by different conditions (
.
The degraded land restoration technique investigated in this study was capable of re-establishing the soil C and N stocks in a short period of time (13 years;
exhibited higher C and N stocks than the deforested area, but lower stocks compared to the native forest. Based on the total C and N stocks of the deforested area, it is possible to conclude that there was an increase of, respectively, 24 Mg ha
1 and
1.7 Mg ha
1 in the soil C and N stocks of the recovered area after 13 years. This represents an increase of 35% and 25%, respectively. The C increase (35%) represents an annual increase of 1.73 Mg ha
1
, a finding corroborated by the results obtained by other research groups in tropical areas (
Feldpausch et al., 2004; Silver et al., 2000 ). However, this rate of increase
will inevitably slow down as the soil C concentration increases
1522 M.O. Macedo et al. / Forest Ecology and Management 255 (2008) 1516–1524
Table 8 pH and soil Al in whole soil profile (0–60 cm) of recovered, native forest and deforested areas in Angra dos Reis, RJ ( n = 3)
Recovered Native forest Deforested Depth (cm) pH
H
2
0
0–5
5–10
10–20
20–30
30–40
40–60 ns
Al (cmol c dm
0–5
5–10
10–20
20–30
30–40
40–60
3
)
4.8a
4.6ab
4.6ab
4.6ab
4.6ab
4.5
0.7b
1.2b
1.1b
1.1b
1.1b
1.2ab
0.13
0.09
0.06
0.06
0.06
0.07
0.23
0.12
0.17
0.13
0.13
0.10
4.5b
4.4b
4.3b
4.4b
4.4b
4.5
1.9a
2.1a
2.5a
2.2a
2.1a
1.7a
0.06
0.03
0.07
0.03
0.03
0.07
0.38
0.29
0.29
0.12
0.17
0.21
4.7ab
4.7a
4.7a
4.7a
4.8a
4.7
1.0b
1.1b
1.1b
0.9b
0.9b
0.9b
0.10
0.03
0.06
0.09
0.12
0.15
0.03
0.07
0.06
0.09
0.19
0.15
Numbers followed by the same letter are not significantly different according to the Bonferroni ‘‘ t ’’ test (5%).
, standard error; ns, not significant.
depending on land use prior to re-establishment of secondary vegetation or land recovery, the rate of C and N incorporation can vary. This occurs because the regeneration of forest ecosystems depends on different factors, such as seed fall, seed
bank, nutrient availability and microclimate (
intensification of degradation processes. For that reason, it is expected that in areas from which a large part of the surface layer of the soil is removed, as in this study, re-establishment of the C and N levels will be slower. However, the planting of legume trees, in association with bacteria and fungi, was able to improve the soil C at the same rate as seen in areas submitted to less aggressive management, such as pastures (
4.2. The free and occluded-light fraction
), all of which are seriously affected by the
The free- and occluded-light fractions of samples of recuperated area were similar to the values of the soil samples of the native forest area and higher than those of the deforested area. These results are comparable to the native forest. Some studies have found that the free-light fraction can respond faster
to land use changes than soil C ( Freixo et al., 2002; Bayer et al.,
observed that the freelight fraction was re-established after 12 years under secondary succession, as observed in the present study. According to that study, this is a response to the large biomass production in early secondary forests.
Table 9
Ca + Mg, P and K in whole soil profile (0–60 cm) of recovered, native forest and deforested areas in Angra dos Reis, RJ ( n = 3)
Native forest Deforested Depth (cm) Recovered
Ca + Mg (cmol c dm
0–5
5–10 ns
10–20 ns
20–30 ns
30–40 ns
40–60 ns
3
)
1.9a
0.61
0.8
0.22
0.6
0.18
0.5
0.15
0.4
0.09
0.4
0.09
P (mg dm
0–5
5–10
10–20
20–30 ns
30–40 ns
40–60 ns
3
)
K (mg dm
0–5
5–10
10–20
20–30
30–40 ns
40–60 ns
3
)
2.3a
1.3ab
1.3ab
0.6
0.3
0.0
66a
43a
35ab
20ab
14
7
0.33
0.33
0.33
0.33
0.33
0.00
2.6
6.6
9.0
4.8
2.3
0.88
0.7b
0.5
0.4
0.4
0.3
0.4
2.3a
2.6a
2.0a
0.6
0.3
0.3
66a
52a
38a
28a
19
21
0.12
0.09
0.03
0.03
0.03
0.06
0.33
0.88
0.58
0.33
0.33
0.33
11.0
3.2
0.88
4.41
3.76
1.67
0.5b
0.5
0.4
0.3
0.3
0.3
0.6b
1.0b
0.3b
0.0
0.0
0.0
21b
16b
14b
10b
7
8
0.06
0.03
0.03
0.03
0.00
0.00
0.58
0.33
0.33
0.00
0.00
0.00
2.5
2.3
1.5
1.7
3.2
5.0
Numbers followed by the same letter are not significantly different according to the Bonferroni ‘‘ t ’’ test (5%).
, standard error; ns, not significant.
with time (
Six et al., 2002a; Silver et al., 2000
). According to
, the annual rate of soil C incorporation will be reduced to 0.20 Mg ha
1 year
1 in the next 80 years, after experiencing a higher incorporation rate (1.3 Mg ha
1 year
1
) over the first 20 years. At this point, it is important to emphasize the role of tropical soils as C sink during the first 20–50 years
(
).
However, in order to determine how long a tropical soil can act as C sink, studies of longer duration are needed. In addition,
and
observed that,
4.3. Litter stock and its nutrient content
The recovered and native forest areas presented similar litter stocks. The litter stock contributes decisively to rehabilitating nutrient cycling processes since it is a primary source of nutrients and energy for soil organisms. In addition, the data relative to the soil C and N stocks and the free- and occluded-light fractions indicate that the litter had been decomposed and the organic matter incorporated.
The litter stocks measured for the purpose of this study, ranging between 5.0 and 6.7 Mg ha forest (6.2 Mg ha
1
, are similar to the results reported by
relative to a steady state
1
), and lower than the values observed by
in a 9–10-year-old agroforestry system established on degraded land (8.7 Mg ha
1
).
reported higher litter stocks under a secondary forest
(24.7 Mg ha
1
) than under a primary forest (12.0 Mg ha
1
) in the Brazilian Amazon Region. However, litterfall and litter stock can vary, depending on soil type, weather, composition and age of the plant community (
During the time period evaluated, the litter stocks differed between the dry and the rainy season. The leaf and decomposed fractions were the most sensitive fractions. The decomposed fraction represented 46% of the total litter stock in the dry season and 63–66% in the rainy season. This increase of 20% probably occurs in response to the higher decomposition rate during the rainy season, which, in turn, is the result of heavier
4.4. Soil fertility
M.O. Macedo et al. / Forest Ecology and Management 255 (2008) 1516–1524 deposition combined with higher temperatures during this time of year.
The litter nutrient contents were also different between the seasons studied. The litter N stocks were higher during the rainy season, with the largest portion contained in the decomposed fraction. On the other hand, the P stock in litter was higher during the dry season.
observed that in tropical areas, the litterfall concentrations of P and N are reduced during the dry season and increase during the rainy season, probably as a result of the retranslocation of these nutrients in the plant in the dry season. However, this does not explain the higher P stocks in litter observed during the dry season. Since P is an important limiting nutrient for plant growth in tropical areas (
Vitousek, 1984; Read and Lawrence,
2003 ), it is probably rapidly absorbed by soil microorganisms,
mycorrhizal fungi and plant roots during the rainy season. The litter concentrations of Ca + Mg were not different between the seasons. As these nutrients are essential components of plant tissues, they have low mobility. Thus, senescent leaf tissues tend to contain a higher relative concentration of Ca + Mg than of N, P and K, nutrients that are reabsorbed by the plant when it is subjected to lack of water stress (
).
In memoriam important contribution, will also feel her absence.
Acknowledgements
1523
On the 19th of September 2007, the first author of this paper,
Michele Oliveira Macedo suffered a fatal heart attack, probably brought on by a tick-borne bacterial disease. Michele was only
30 years old and had just successfully defended her PhD thesis at the Universidade Federal Rural do Rio de Janeiro. Her family, friends and colleagues will sorely miss her, but the scientific community to which she had started to make such an
To the PRODETAB Project for providing financial support and CNPq for the fellowship granted to the first author. To the
Soil Science Post Graduation Department – Agronomy/
UFRRJ, and the Brazilian Agricultural Research Corporation,
National Agrobiology Research Centre (Embrapa Agrobiologia) for technical and scientific support. To Dr. Jose´ Carlos
Polidoro of the Brazilian Agricultural Research Corporation,
National Soil Research Center (Embrapa Solos) and Dr. Pedro
L.O.A. Machado of the Brazilian Agricultural Research
Corporation, National rice and bean Research Centre (Embrapa
Arroz e Feija˜o), for the technical support in soil organic matter physical fractioning. And to Carlos Fernando Cunha and Telmo
Felix da Silva for technical assistance in collecting soil samples.
The soil of the native forest area had the lowest pH values and the highest Al concentrations. Wisniewski (unpublished data mentioned by
) observed a slight decrease in pH and an increase in Al concentration as the succession process advanced. The P, Ca and Mg levels were low in all three areas. This low nutrient availability is related to the high degree of soil weathering, resulting in very low availability of base minerals and adsorption of P by Fe and Al oxides
(
Tiessen et al., 1994; Pereira, 1996
). The low availability of soil nutrients along with the higher nutrient concentrations in litter corroborate the hypothesis that in tropical ecosystems, nutrient
availability depends on litterfall and decomposition ( Vitousek,
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