Ecological Applications, 14(4) Supplement, 2004, pp. S263–S279
q 2004 by the Ecological Society of America
RIVERINE ORGANIC MATTER COMPOSITION AS A FUNCTION OF LAND
USE CHANGES, SOUTHWEST AMAZON
MARCELO C. BERNARDES,1,4 LUIZ A. MARTINELLI,1 ALEX V. KRUSCHE,1 JACK GUDEMAN,2
MARCELO MOREIRA,1 REYNALDO L. VICTORIA,2 JEAN P. H. B. OMETTO,1 MARIA V. R. BALLESTER,1
ANTHONY K. AUFDENKAMPE,3 JEFFREY E. RICHEY,2 AND JOHN I. HEDGES2
1Laboratório
de Ecologia Isotópica, Centro de Energia Nuclear na Agricultura, Universidade de São Paulo,
CEP 13400-970, Piracicaba, SP, Brazil
School of Oceanography, University of Washington, Box 355351, Seattle, Washington 98195 USA
3Stroud Water Research Center, 970 Spencer Road, Avondale, Pennsylvania 19311 USA
2
Abstract. We investigated the forms and composition of dissolved and particulate organic matter in rivers of the Ji-Paraná Basin, which is situated at the southern limit of the
Amazon lowlands and has experienced extensive deforestation in the last three decades
(;35 000 km2). Our objective was to investigate how extensive land-use changes, from
forest to cattle pasture, have affected river biogeochemistry. We measured a series of
chemical, biochemical, and isotopic tracers in three size classes of organic matter within
five sites along Ji-Paraná River and eight more sites in six tributaries. The results were
compared with C4 leaf and pasture soils end members in order to test for a pasture-derived
signal in the riverine organic matter. The coarse size fraction was least degraded and derived
primarily from fresh leaves in lowland forests. The fine fraction was mostly associated with
a mineral soil phase, but its ultimate source appeared to be leaves from forests; this fraction
was the most enriched in nitrogen. The ultrafiltered dissolved organic matter (UDOM)
appeared to have the same source as the coarse fraction, but it was the most extensively
degraded of the three fractions. In contrast to Amazon white-water rivers, rivers of the JiParaná Basin had lower concentrations of suspended solids with a higher carbon and nitrogen
content in the three size fractions. However, principal component analyses showed a correlation between areas covered with pasture and the d13C values of the three size fractions.
The highest d13C values were observed in the ultrafiltered dissolved organic matter of the
Rolim-de-Moura and Jarú rivers, which have the highest areas covered with pasture. The
lower the order of the streams and the higher the pasture area, the greater is the possibility
that the C4-derived organic matter signal will be detected first in the faster-cycling fraction
(UDOM). The large change in land use in the Ji-Paraná Basin, replacement of primary
forests by C4 pastures for cattle feeding, that has taken place in the last 30–40 yr, has
already changed the characteristics of the composition of the riverine organic matter.
Key words: Amazon rivers; black water; deforestation; isotopes; land use; lignin; organic matter;
pasture; principal component analyses; white water.
INTRODUCTION
Of the states located in the Amazon region, the state
of Rondônia in the southern Amazon has experienced
the fourth highest rate of deforestation (Instituto Nacional de Pesquisas Espaciais [INPE] 2001). In this
region, large areas of rainforest have been replaced by
pasture for cattle in the last 30 years (INPE 2001). Of
the total deforested area in the Amazon until 1999,
almost 10% (58 000 km2) has been in Rondônia (INPE
2001). The increase in the land use is concentrated
along highway BR-364 within the limits of the Ji-Paraná River basin. As a consequence, in 1986, of all the
deforested areas in Rondônia, 59% were located in the
Manuscript received 2 November 2001; revised 30 November
2002; accepted 31 December 2002; final version received 29 January 2003. Corresponding Editor: J. M. Melack. For reprints of
this Special Issue, see footnote 1, p. S1.
4 E-mail: [email protected]
Ji-Paraná River basin, with the most intensive land cover changes in the central part of this basin (Fig. 1).
The conversion of large areas of primary forests into
grasslands leads to profound modifications in the structure and functioning of terrestrial ecosystems in the
Amazon. Several studies have shown that the introduction of C4 grasses alters carbon and nitrogen stocks
and dynamics in soil organic matter (Desjardin et al.
1994, Trumbore et al. 1995, Neill et al. 1997, Camargo
et al. 1999). However, these studies do not address
whether these changes in organic matter cycling have
effects beyond the local site of deforestation. Streams
are natural transporters in landscapes, and their flowing
waters reflect the biogeochemistry of their watersheds.
Thus, higher order streams and rivers are considered
to be good integrators of both natural and anthropogenic processes in their drainage basins, and they have
the potential to offer a broad view of the magnitude of
biogeochemical changes over a landscape.
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MARCELO C. BERNARDES ET AL.
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FIG. 1.
Ecological Applications
Special Issue
Study area and sample locations in Rondônia, Brazil.
Few studies have addressed the consequences of
land-use changes on aquatic environments in the Amazon Basin (e.g., Williams and Melack 1997, Neill et
al. 2001, Biggs et al. 2002). None of these studies
investigated possible changes in the compositional
characteristics of organic material of river systems. On
the other hand, the forms and composition of differentsized classes of organic matter transported by whitewater rivers in largely unaltered basins of the Amazon
have been investigated (Hedges et al. 1986, 1994, 2000,
Richey et al. 1990, Quay et al. 1992, Devol and Hedges
2001). These studies have analyzed an array of elemental (carbon and nitrogen concentrations), biochem-
ical (lignin, carbohydrate, and amino acid), stable isotope (d13C, d15N), and radioisotope (D14C) compositions
in riverine organic matter. These measurements were
carried out in three size fractions: coarse (.63 mm)
and fine (,63 mm to 0.1 mm) particulate and ultrafiltered dissolved organic matter (UDOM). The composition and fates of these three fractions throughout the
Amazon Basin are consistently distinct, although they
share the same ultimate source—the leaves of C3 forest
trees. The coarse fraction is the least degraded and
resembles relatively undecomposed tree leaves. The
dissolved products of the decomposition of tree leaves
percolate through the soil column, where nitrogen-rich
August 2004
ORGANIC MATTER OF AMAZON LOWLAND RIVERS
S265
FIG. 2. Daily variability of the discharge
from 1999 to 2001 in the following rivers: Comemoração River (COM-2), Pimenta Bueno River (PB-2), and Ji-Paraná River (JIP-2 and JIP4). Arrows indicate seven times at which water
samples were collected.
compounds are sorbed and stabilized by soil mineral
particles (Aufdenkampe et al. 2001). Consequently, the
fine fraction is the richest in nitrogen and enters the
river systems primarily via soil erosion. Finally, the
dissolved organic fraction is most degraded, being
composed of organic, nitrogen-poor substances that are
not sorbed onto mineral surfaces. Another important
feature is the constancy over time and space of the
compositional characteristics of the size classes of riverine organic matter. From first-order Andean tributaries to the major rivers of the Amazon Basin, no major
differences were observed for a given size fraction
(Hedges et al. 2000).
In the present study, we investigated the forms and
composition of riverine organic matter of the Ji-Paraná
Basin. We sampled the Ji-Paraná River at five different
sites along its main stem. We also sampled several
tributaries, with drainage basins exhibiting a range of
sizes and extents of deforestation. Our main objective
was to compare the composition of the organic matter
in rivers of the Ji-Paraná Basin with other rivers of the
Amazon Basin. Most previous studies of riverine organic matter composition in the Amazon Basin have
focused on turbid white-water systems, which have a
considerable portion of their headwaters in the Andes.
In contrast, rivers of the Ji-Paraná Basin have their
watersheds in lowland areas, carrying a much lower
load of suspended particles than their white-water
counterparts (Martinelli et al. 1993).
Our second objective was to investigate whether the
extensive land-use changes in the Ji-Paraná Basin over
the last 30 yr have altered the organic matter composition of its rivers. In rivers of the Piracicaba Basin,
located in the southeast region of Brazil, land-use
changes that occurred 70–80 yr ago have left their
‘‘imprint’’ in the dissolved and fine fractions of rivers
of that basin (Martinelli et al. 1999). In contrast, most
of the changes in land use in the Ji-Paraná Basin started
just 30–40 yr ago. Studies with soils under pastures of
different ages have shown that after 3–5 yr of pasture
cultivation the signal of C4-derived organic matter from
pasture grasses is detectable in the soil organic matter
(Neill et al. 1997). Therefore, it is possible that the
composition of organic matter in the Ji-Paraná River
network might reflect these new organic matter sources.
In order to answer these questions, we analyzed a
series of chemical, biochemical, and isotopic tracers in
the three size classes of organic matter from rivers
within the Ji-Paraná Basin and compared them with
values obtained in previous studies in the Amazon Basin. In addition, we compared these results with C4
plants and pasture soil sources to test for a signal in
the riverine organic matter traceable to introduced grass
species.
METHODS
Sampling sites
The Ji-Paraná Basin, with a drainage area of 75 000
km2, is located in Rondônia state in the southwestern
Amazon Basin (Fig. 1). The headwaters of the Ji-Paraná
River are formed by the confluence of the Comemoração and Pimenta Bueno rivers. The Ji-Paraná River
channel has a total length of 972 km and varies in width
from 150 to 500 m, whereas the channel widths of the
major tributaries range from 30 to 200 m (Table 1).
The high and low water periods for these rivers range
from December to May, and from June to November,
respectively.
Water samples were collected seven times between
1999 and 2001 (Fig. 2). Samples were collected at five
sites along the main channel of the Ji-Paraná River, at
the mouths of six major tributaries, and at two headwater sites, for a total of 13 sampling stations (Fig. 1).
The first four sites were located on the Comemoração
(COM-1 and COM-2) and Pimenta Bueno (PB-1 and
PB-2) rivers; below their junction there were five sampling sites (JIP-1 to JIP-5). Along its course, the JiParaná receives contributions from four main tributaries that were also sampled: the Rolim de Moura (ROL),
Urupá (URU), Jarú (JAR), and Machadinho (MAC)
rivers. The drainage area above each sampling site was
delineated and individually characterized in terms of
total cumulative area, population density, river order,
land use, and soil textural characteristics using a digital
library built using the Arc/Info geographic information
system (ESRI, Redlands, California, USA) (Table 1).
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FIG. 3. Compositional averages of the coarse suspended solids fraction of rivers of the Ji-Paraná Basin. Error bars represent
61 SD. Site identities: 1, COM1; 2, COM-2; 3, PB1; 4, PB2; 5, JIP1; 6, JIP2; 7, JIP3; 8, JIP4; 9, JIP5; 10, ROL; 11, URU;
12, JAR; 13, MAC.
Sample collection and preparation
At each site, 50–100 L of water were collected from
the river in the middle of the channel at 60% of the
total depth using an electric pump. The water sample
was sieved (.63 mm) in field in the order to separate
the coarse suspended solid (CSS) fraction, which was
immediately preserved with HgCl2, to a final concentration of 100 mM. The fine suspended solid (FSS)
fraction (,63 mm and .0.1 mm) and ultrafiltered dissolved organic matter (UDOM) fraction (,0.1 mm and
.1000 daltons) were isolated in the laboratory with a
Millipore tangential flow ultrafiltration system (model
Pellicon-2; Millipore, Billerica, Massachusetts, USA),
using membrane cartridges having a nominal 0.1-mm
pore size (model Durapore VVPP; Millipore) and a
1000-daltons molecular weight nominal cut off (model
PLAC; Millipore), respectively. After filtration, the
material was roto-evaporated and then dried to constant
mass in an oven, both at 508C. The average percentage
recovery of organic matter in all samples during ultrafiltration was 98 6 8%, of which an average of 20 6
6% was recovered as UDOM, from both forested and
pasture drainage areas.
Lignin oxidation, elemental, and isotopic analysis
Lignin analyses were made according to the CuO
oxidation procedure of Hedges and Ertel (1982) as
modified by Goñi and Hedges (1990). Briefly, between
30 to 300 mg of dry sample was oxidized at 1558C for
3 h with CuO under basic (8% NaOH) conditions. The
reaction solution was spiked with a nine-compound gas
chromatography recovery standard mixture (in pyri-
ORGANIC MATTER OF AMAZON LOWLAND RIVERS
August 2004
S267
FIG. 4. Compositional averages of the fine suspended solids fraction of rivers of the Ji-Paraná Basin. Error bars represent
61 SD. Station codes are as for Fig. 3.
TABLE 1.
Sites
COM-1
COM-2
PB-1
PB-2
JIP-1
JIP-2
JIP-3
JIP-4
JIP-5
ROL
URU
JAR
MAC
Characteristics of the studied drainage areas of the southwest Amazon Basin.
Area (km2) Q (m3/s) Width (m)
132
5894
152
10 118
17 843
32 793
39 461
60 494
64 294
1349
4209
7275
3250
···
161
···
205
···
641
···
1332
···
···
···
···
···
8
71
16
86
115
239
214
259
329
37
95
68
52
Population Density (no.
(3 102) inhabitants/km2)
5
269
6
219
680
1516
2509
2973
3155
148
492
793
182
3.8
4.6
3.9
2.2
37.1
13.5
14.0
10.5
9.8
11.0
11.7
10.9
5.6
River
order
Pasture
(%)
3
5
3
6
6
6
6
7
7
5
5
6
5
13
28
8
32
31
39
33
40
40
66
43
53
22
Forest
(%)
Sand (%) Clay (%)
47
65
90
60
62
54
53
53
53
26
50
36
68
44
73
76
66
69
68
67
65
64
64
67
60
41
48
21
19
25
24
24
25
26
27
27
23
30
51
Notes: ‘‘Area’’ is the cumulative drainage area. Population numbers are from 1996. Q is the annual mean discharge from
1999 to 2001. Pasture (%) and forest (%) are the cumulative percentages of pasture and forest; sand (%) and clay (%), are
percentage of sand and clay content in soils (Ballester et al. 2003). Sample site codes are delineated in Methods.
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MARCELO C. BERNARDES ET AL.
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Special Issue
FIG. 5. Compositional averages of the ultrafiltered dissolved organic matter (UDOM) fraction of rivers of the Ji-Paraná
Basin. Error bars represent 61 SD. Station codes are as for Fig. 3.
dine), acidified and extracted with diethyl ether. The
lignin extract was diluted in pyridine, mixed with regisil plus an absolute recovery standard, and analyzed
on a Hewlett Packard 5890 series II gas chromatograph
(Agilent Technologies, Palo Alto, California, USA) fitted with a DB-1 fused-silica capillary column (J&W
Scientific, Folsom, California, USA). Identities of all
phenols were confirmed by mass spectrometry of selected samples vs. commercial standards. The average
analytical precision was 610% for the reported lignin
phenols. Organic carbon and nitrogen concentrations
were determined using a Carlo Erba CHN analyzer
(Thermoquest, Rodano, Italy). Isotope measurements
were performed with a Finnigan Delta-E mass spectrometer (ThermoFinnigan, Bremen, Germany) fitted
with dual inlet and dual collector systems. Results are
expressed in d13C and d15N relative to Pee Dee Belemnite (PDB) and atmospheric N2 standard, respectively defined as d13C or d15N (‰) 5 ([Rsam/Rstd] 2 1)
3 1000, where Rsam and Rstd are the 13C:12C or 15N/14N
of the sample and standard, respectively. Samples were
analyzed at least in duplicate with a maximum difference of 0.2‰ between replicates.
Statistical analysis
Most of our data did not follow a normal distribution.
Accordingly we used nonparametric statistical tests. To
test for differences among sampling sites we used the
Mann-Whitney U test. Principal component analyses
(PCA) were performed in order to examine sources of
August 2004
ORGANIC MATTER OF AMAZON LOWLAND RIVERS
S269
RESULTS
Spatial variability
FIG. 6. Plot of organic carbon vs. fine suspended sediments (FSS) for Ji-Paraná rivers (filled circles), Amazon River (open circles), white-water tributaries (open diamonds),
and black-water tributaries (filled diamonds). Values for the
Amazon River and white- and black-water tributaries are from
Hedges et al. (1986, 2000).
variability in the data. Prior to PCA analyses, we unit
normalized our data to have an average of zero and a
standard deviation of one, since they did not follow a
normal distribution. PCA with Varimax rotation was
used to investigate the relationships among basin characteristics, such as altitude, slope, area covered with
pasture and forest, soil texture (percentage of sand, silt,
and clay), and compositional characteristics ( d13C,
d15N, percentage of organic carbon, percentage of total
nitrogen) of the three size fractions. Only variables with
,20% of missing values were considered in the analysis.
Most of the sites had low concentrations of bulk
coarse suspended solids, generally ,3 mg/L. Samples
from site PB-1 were the exception (no. 3, Fig. 3), with
a statistically higher average concentration of 8 mg/L.
Concentrations of bulk fine suspended solids averaged
15–35 mg/L at most sites. The 5 mg/L average at COM1 (no. 1, Fig. 4) was the exception and was statistically
lower than the highest concentrations found at ROL
(no. 10, Fig. 4). The mass percentages of organic carbon (OC%) in the coarse fraction varied from 6.3%
(JIP-5; no. 9, Fig. 3) to 11.8% (PB-2; no. 4, Fig. 3),
but no significant statistical difference among sampling
sites was detected, partially because the variability at
each sampling site was large (Fig. 3). The same was
true for the ultrafiltered-dissolved organic matter fraction. There was a variation from 2.7% (URU; no. 11,
Fig. 5) up to 14% (JIP-2; no. 6, Fig. 5), but the variability at each sampling site was also large.
The variability of the OC% levels in the fine fractions
at each sampling site was smaller than in the coarse
and ultrafiltered-dissolved fractions with no statistical
difference among sampling sites (Fig. 4). An inverse
relationship was observed between the OC% in the fine
fraction and fine suspended solids concentrations (Fig.
6). The mass percentages of total nitrogen (TN%) in
all size fractions did not vary significantly among sampling sites, and the variability at each sampling site
was smaller in the fine fraction than in the coarse and
ultrafiltered-dissolved fractions (Figs. 3–5). The C:N
atomic ratio of the coarse fraction varied from 11 (JAR;
no. 12, Fig. 3) to 28 (MAC; no. 13, Fig. 3), with most
values between 15 and 20 (Fig. 3). In spite of this large
variability among sampling sites, no statistical difference was detected among them. The C:N ratios of the
fine fraction were less variable (9.5–12.5) among sam-
TABLE 2. Compositional averages of the coarse and fine fractions of organic matter of rivers of the Ji-Paraná Basin in
comparison with the Solimões/Amazon main channel, and their white- and black-water tributaries.
Rivers
Ji-Paraná
Solimões/Amazon†
White-water tributaries†
Black-water tributaries†
Ji-Paraná
Solimões/Amazon
White-water tributaries
Black-water tributaries
Size
fraction
d13C
coarse
coarse
coarse
coarse
fine
fine
fine
fine
229.1
228.0
228.0
···
228.1
226.9
227.7
228.5
Organic
C
Total N
(mass %) (mass %) C:N
8.92
1.08
0.87
1.29
8.04
1.15
1.39
2.32
0.53
0.04
0.04
···
0.72
0.10
0.16
0.23
18.0
24.5
20.6
···
11.5
11.1
8.9
10.2
Suspended
L
sediments (mg/100 g
(Ad/
(mg/L) organic C) cin:van syr:van Al)v
2.3
69.6
36.4
1.5
20.5
262.3
179.1
14.3
7.81
7.37
6.41
7.99
2.48
2.15
1.74
1.46
0.12
0.07
0.06
0.07
0.16
0.10
0.11
0.09
0.94
0.78
0.69
0.85
0.71
0.84
0.86
0.79
0.27
0.24
0.28
0.25
0.72
0.43
0.55
0.54
Notes: Values reported for d13C are the deviations (‰) of the 13C:12C of the samples from the same ratio for the PDB
standard; cin:van is the ratio of the sum of cinnamyl phenols to vanillyl phenols; syr:van is the ratio of the sum of syringyl
phenols to vanillyl phenols; L is the total yield of lignin-derived phenols normalized to 100 mg of organic carbon in the
sample; (Ad/Al)v is the acid-to-aldehyde ratio of vanillyl phenols. White-water tributaries are the rivers Iça, Juruá, Japurá,
Purus, and Madeira. Black-water tributaries are the rivers Jutaı́ and Negro.
† Data from J. E. Richey (unpublished data).
TABLE 3.
Ecological Applications
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MARCELO C. BERNARDES ET AL.
S270
Compositional averages (61 SD) of the organic matter size fractions of the rivers of the Ji-Paraná Basin (Rondônia).
Measure
COM-1
COM-2
PB-1
PB-2
JIP-1
JIP-2
Coarse
L (mg/100 g organic C)
(Ad/Al)v
4.83
0.42
8.58
0.28
7.46
0.3
8.33
0.25
8.36 6 4.17
0.26 6 0.01
8.73 6 1.66
0.24 6 0.01
Fine
L (mg/100 g organic C)
(Ad/Al)v
ND
ND
2.3
0.83
ND
ND
2.51
0.85
2.51 6 0.06
0.71 6 0.12
2.82 6 0.13
0.63 6 0.13
UDOM
L (mg/100 g organic C)
(Ad/Al)v
ND
ND
ND
ND
ND
ND
ND
ND
0.77
2.07
0.83
2.07
Notes: L is the total yield of lignin-derived phenols normalized to 100 mg of organic carbon in the sample; (Ad/Al)v is
the acid-to-aldehyde ratio of vanillyl phenols; ND, not determined. Sample site and size fraction codes are delineated in
Methods. Standard deviation was not computed when N , 3. UDOM is ultrafiltered dissolved organic matter.
pling sites with no statistical differences among them
(Fig. 4). Finally, the C:N ratios of the ultrafiltered fraction had a large variability at each sampling site and
among sampling sites, with no statistical differences
among them (Fig. 5).
The suspended solids concentrations in rivers of the
Ji-Paraná Basin were significantly smaller than the suspended solids concentrations found in the Amazon River and their white-water tributaries, and similar to the
concentrations found in black-water tributaries (Negro
and Jutaı́) of the Amazon River (Table 2). As a consequence, the organic carbon transported in the particulate form was low. Most of the organic carbon (average 72%) was transported in a dissolved form
(UDOM): 26% as fine particulate carbon, and only 2%
in the coarse fraction.
The d13C average values of the coarse fraction varied
only 2.5‰ between the highest (228.5‰; URU; no.
11, Fig. 3) and the lowest (231.0‰; MAC; no. 13,
Fig. 3) values, and no statistical differences were observed among sampling sites. The variability at each
sampling site was not large, with exception of the MAC
(no. 13, Fig. 3). For the fine fraction the same trend
was found, the d13C varied between 226.7‰ (URU;
no. 11, Fig. 4) and 230.7‰ (MAC; no. 13, Fig. 4).
With the exception of two high d13C values of the
UDOM (221.8‰ at ROL; no. 10, Fig. 5; and 223.4‰
at JAR; no. 12, Fig. 5), the remainder of the values
varied from 226 to 228‰ (Fig. 5).
Due to low suspended-sediment concentrations in
some tributaries of the Ji-Paraná River, the biochemical
composition (lignin-derived phenols) could not be determined in every sample (Table 3). The carbon normalized yields of total lignin-derived phenols (L, mg/
100 mg organic C) of the coarse fraction varied between 7 and 9 mg/100 mg organic C, with the exception
of COM-1, where the average concentration was ;5
mg/100 mg organic C (Table 3). However, this lower
value was not statistically different than the others. The
average L values of the fine fraction were smaller than
the coarse fraction and varied from 2 to 3 mg/100 mg
organic C (Table 3). Finally, the acid:aldehyde ratio of
vanillyl phenols, (Ad/Al)v, of the coarse fraction varied
from 0.24 to 0.30 (Table 3). The exception was a value
of 0.42 found in the COM-1 sampling site. The (Ad/
Al)v of the fine fraction was generally higher than the
coarse fraction, varying from 0.63 to 0.83 (Table 3).
The biochemical composition (L and [Ad/Al]v) of the
UDOM fraction was determined only for the sampling
sites JIP-1 throughout JIP-4 and only for one sampling
period (Table 3). Therefore, it was not possible to test
for differences between these sampling sites.
Seasonal variability
In order to test for seasonal differences we grouped
the data in high water period (February, March, and
May) and in low water period (June, September, and
November) (Fig. 2). In addition, as we did not, in general, find significant differences among sampling sites,
we also grouped samples collected along a river under
the same name in order to have enough statistical power
to run the statistical test. Therefore, we included in this
comparison only rivers with more than one sampling
site, as Comemoração, Pimenta Bueno, and Ji-Paraná
(Table 4).
Most of the seasonal differences were found in the
Ji-Paraná River. As expected, the bulk coarse average
suspended solids concentration was higher in the high
water period than in the lower water period. The same
was true for the bulk fine average concentration, but
in this case the averages were not statistically different
(Table 4). The OC% and TN% levels were higher in
the low-water period in the three fractions. However,
only for the fine fraction was OC% level statistically
different, and only for the coarse and fine fractions was
the TN% statistically different (Table 4). The average
C:N ratios of the three fractions were smaller during
the low water, but only in the fine fraction was the
difference statistically significant. For each of the three
rivers, average d13C values of the fine fraction were
statistically lower in the low-water period than in the
high-water period. Finally, the average d15N value of
the coarse fraction of the Ji-Paraná River was statistically higher during the low water (Table 4).
August 2004
TABLE 3.
ORGANIC MATTER OF AMAZON LOWLAND RIVERS
S271
Extended.
JIP-3
JIP-4
JIP-5
ROL
URU
JAR
MAC
7.46 6 0.38
0.24 6 0.01
6.97 6 2.35
0.26 6 0.01
7.87
0.25
8.87
0.23
8.17
0.27
ND
ND
ND
ND
2.76 6 0.50
0.70 6 0.16
2.07 6 0.84
0.78 6 0.22
2.36 6 0.22
0.68 6 0.07
ND
ND
ND
ND
ND
ND
ND
ND
0.73
2.72
0.58
2.2
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
Compositional differences among size fractions
The bulk fine suspended solids concentrations were
statistically higher than the bulk coarse concentrations
(Table 5). The average OC% and TN% levels were only
statistically higher in the UDOM fraction. The C:N
average ratio of the fine fraction was statistically smaller than the ratios of the coarse and UDOM fractions
(Table 5). The d13C values statistically increased with
decreasing size fraction, with a difference of ;2.5‰
between the coarse and UDOM fraction. The average
d15N value of the UDOM fraction was statistically higher than the coarse and fine fractions. The carbon normalized yields of total lignin-derived phenols (L, mg/
100 mg organic C) statistically decreased with decreasing size fraction and the (Ad/Al)v statistically increased with decreasing size fraction (Table 5).
Sources of organic matter to rivers of the
Ji-Paraná Basin
We compared elemental composition (OC% and
N%), stable isotopes characteristics (d13C and d15N),
and biochemical composition (L and [Ad/Al]v) of the
size fractions of the Ji-Paraná Basin rivers with potential end members. Based on previous work of Hedges
et al. (1986, 2000) and Martinelli et al. (1999), we
selected as potential organic-matter sources forest soil
organic matter, pasture soil organic matter, tree leaves
(C3 type), and grass leaves (C4 type). As there were no
significant differences between sampling sites, we
grouped Ji-Paraná sites together and focused on compositional differences between the three size fractions.
The fine and the coarse fractions of the Ji-Paraná Rivers
were characterized by high concentrations of carbon
and nitrogen. A plot of these two parameters produced
significant correlation coefficients for the particulate
organic matter (r2 5 0.74 for coarse and r2 5 0.72 for
fine) and no correlation for the ultrafiltered organic
matter (Fig. 7, UDOM data not shown). Both lines have
a small positive intercept in the OC% axis that is not
statistically different from zero, indicating that most of
the nitrogen was in an organic form (Hedges et al.
1986). The three fractions had, in general, higher carbon and nitrogen concentrations than Rondônia soils
and smaller concentrations than found in leaves (Fig.
7). The d13C and d15N values of the fine and coarse
fractions were similar to values found in the soil organic matter of Rondônia forest soils. The coarse fraction had the most negative d13C values, which places
this fraction nearest to tree leaves compositionally (Fig.
8). The UDOM fraction had higher d13C and d15N values
than the particulate fractions, and the d13C average value was higher than values found in the soil organic
matter (Fig. 8). None of the three fractions had d13C
values similar to C4 leaves; consequently, the three
fractions plotted distant from the C4 leaves average in
Fig. 8. The same occurred when d13C values were plotted as a function of N:C ratios (the inverse of the conventional C:N is required so that both axes are mathematically independent; Fig. 9). The fine and UDOM
fractions plotted near forest soils, whereas the coarse
fraction plotted between tree leaves and forest soils,
but both fractions plotted far from soil organic matter
of pastures of different ages (Fig. 9). High syringyl:
vanillyl and cinnamyl:vanillyl ratios, specific phenols
from lignin, were measured in coarse size fractions
followed by the fine size fractions. Similar values were
found for Amazon rivers and its tributaries (Table 2
and Fig. 10).
Organic degradation
The acid to aldehyde ratio of lignin vanillyl phenols,
(Ad/Al)v, is a robust indicator of lignin decomposition,
with values increasing with progressive degradation by
fungi and bacteria (Hedges et al. 1988, Opsahl and
Benner 1995). For samples from the Ji-Paraná, the (Ad/
Al)v ratio increases from the larger to the smaller size
fraction, corresponding to a decrease of total yields of
lignin-derived phenols (Fig. 11A). This trend indicates
a progressive loss of lignin during the degradation process, as was observed for the coarse and fine fractions
of the Amazon River (Fig. 11A; Ertel et al. 1986). Fig.
11B shows that as the riverine fractions become more
degraded (coarse , fine , UDOM) there was a progressive increase in d13C. Such a trend is expected for
a standard isotope effect in which carbonaceous residues became progressively 13C enriched, as less strongly bonded 12C carbons are preferentially lost.
Ecological Applications
Special Issue
MARCELO C. BERNARDES ET AL.
S272
TABLE 4. Compositional averages (61 SD) of the three organic matter size fractions of the rivers Comemoração, Pimenta
Bueno, and Ji-Paraná, grouped according the water level.
Pimenta
Bueno
Comemoração
High
Low
High
Coarse
N
d13C
d15N
Organic C (mass %)
Total N (mass %)
C:N
Suspended sediments (mg/L)
Measure
4
229.0 6 0.4
3.8 6 0.4
9.9 6 6.9
0.54 6 0.37
19 6 2.1
2.88 6 2.11
6
229.1 6 0.3
4.4 6 0.2
8.4 6 2.8
0.43 6 0.15
19.4 6 1.2
1.34 6 0.68
4
229.2 6 0.1
3.5 6 0.6
12.5 6 7.5
0.59 6 0.39
21.0 6 1.7
7.50 6 3.60
Fine
N
d13C
d15N
Organic C (mass %)
Total N (mass %)
C:N
Suspended sediments (mg/L)
3
227.7a 6 0.5
4.4 6 4.2
8.7 6 6.4
0.81 6 0.64
11.3 6 2.2
27.6 6 26.9
5
228.6b 6 0.4
3.9 6 0.8
10.7 6 2.3
0.80 6 0.20
13.6 6 1.3
8.05 6 8.92
3
227.6a 6 0.4
3.2 6 1.2
7.4 6 3.1
0.69 6 0.29
10.9 6 1.1
25.4 6 23.1
UDOM
N
d13C
d15N
Organic C (mass %)
Total N (mass %)
C:N
1
227.6
7.5
14
0.35
40.1
3
227.2 6 0.9
9.7 6 2.3
3.5 6 1.7
1.72 6 1.44
5.6 6 7.4
1
227.2
9.3
10.6
0.42
25.3
Notes: Values reported for d13C are the deviations (‰) of the 13C:12C of the samples from the same ratio for the PDB
standard; d15N are the deviations (‰) of the 15N:14N of the samples from the same ratio for the atmospheric N2 stable isotope
standard. Standard deviation was not computed when N , 3. ‘‘High’’ denotes the high-water period (February–May) and
‘‘Low’’ denotes the low-water period (June–November). UDOM is ultrafiltered dissolved organic matter. Different letters
indicate statistically significant differences between averages.
Principal component analysis
The communality for each variable, which represents
the fraction of each variable that is explained by the
retained factor, were typically higher than 65%. The
last lines of Tables 6–8 express the percentages of variance explained by each factor. For the coarse fraction,
PCA explained 80.6% of the variability of the data.
The first two factors explained 24.5% and 24.1% of the
data variability, respectively. The third and fourth factors explained 17.5% and 14.5%, respectively. The first
factor had significant loadings for d15N and soil clay
content (Table 6). The second factor had high loading
for d13C and pasture area and soil silt content. The third
factor is loaded with OC% and TN% and fourth factor
with forest area, altitudes, and slopes. For the fine fraction, PCA explained 78.3% of the variability of the
data. The first factor alone explains almost 29% of the
variability and had significant loadings for d13C and
d15N with pasture area and silt (Table 7). The second
factor, which explains 25% of the variability had significant loadings especially for soil sand and clay contents. The third factor explains ;15% of the variability
and significant loads are OC% and TN%. The fourth
factor explains only 10% of the variability and links
mainly forest area, and altitudes and slopes. Finally,
the UDOM explained 78.8% of the data variability. The
first factor explains 23.5% of the variability, and had
significant loadings again for d13C and pasture area
(Table 8). The second factor had high loadings only
for soil clay content. The third factor had high loadings
for d15N, OC%, and TN%. The fourth factor had high
loadings for forest area, altitude, and slopes.
DISCUSSION
The rivers of the Ji-Paraná Basin originate mostly in
the lowlands of the Rondônia State and drain mainly
the Precambrian Brazilian Shield (Fig. 1). Consequently, these rivers have lower sediment concentrations
than white-water rivers of the Amazon Basin that have
their headwaters in the Andes or in the Andes foothills,
and are more similar to other black-water tributaries of
the Amazon system such as the Negro and the Jutaı́.
This geomorphological context has important implications for the source of organic matter to rivers in the
Amazon. For instance, because of the increase in the
d13C composition of C3 plants with increasing elevation, the vegetation of the Andes is a source of 13Crich particulate matter to the Amazon main channel
(Quay et al. 1992). Progressively, this 13C-rich organic
matter is replaced and diluted by 13C-poor organic matter produced in the Amazon lowlands. Consequently,
the d13C values of the fine and coarse organic matter
ORGANIC MATTER OF AMAZON LOWLAND RIVERS
August 2004
TABLE 4.
Extended.
Pimenta
Bueno
Ji-Paraná
Low
High
Low
6
228.9 6 0.3
4.2 6 0.8
8.1 6 3.8
0.43 6 0.21
19.0 6 1.4
4.47 6 6.21
14
228.9 6 0.4
4.8a 6 1.1
7.3 6 4.2
0.40a 6 0.23
18.3 6 2.1
3.42a 6 1.80
19
228.9 6 0.9
6.5b 6 1.1
9.4 6 3.5
0.63b 6 0.25
15.2 6 2.9
0.85b 6 0.58
5
228.6b 6 0.5
4.4 6 0.9
6.5 6 1.8
0.54 6 0.17
12.3 6 1.2
19.7 6 12.5
14
227.5a 6 0.5
5.2 6 1.5
6.8a 6 1.0
0.54a 6 0.09
12.6a 6 1.0
25.8 6 7.1
19
228.4b 6 1.1
5.5 6 0.8
8.3b 6 1.1
0.80b 6 0.21
10.8b 6 2.4
21.5 6 10.3
3
225.7 6 3.5
11.2 6 5.8
5.4 6 2.4
1.06 6 0.85
8.7 6 6.9
10
227.1 6 0.8
7.6 6 1.0
11.4 6 5.8
0.58 6 0.18
21.7 6 11.8
13
226.9 6 1.7
6.6 6 2.1
12.6 6 7.5
1.08 6 1.12
19.4 6 10.0
become more negative downstream (Quay et al. 1992,
Hedges et al. 2000). This is one of the major changes
in the composition of the particulate organic matter of
the entire Amazon Basin, and sharply contrasts with
the elemental and biochemical uniformity of the lower
main stem which experiences few changes over a river
reach of ;2000 km (Hedges et al. 1992). The same
lack of pronounced changes in the bulk composition
of the riverine organic matter was observed within size
fractions sampled over a stretch of the Beni River, extending from its headwater near to the city of La Paz
(first order streams) to its confluence with the Madre
de Dios River in the southeast Amazon region (Hedges
et al. 2000). Investigating a 970-km stretch of the JiParaná River we reached the same conclusion. Differences in the elemental, biochemical, and stable isotope
composition were not very different among the main
TABLE 5.
Compositional averages (61
SD )
Fraction
d13C (‰)
d15N (‰)
Coarse
Fine
UDOM
229.1 6 1.0
228.1b 6 1.2
226.7c 6 1.8
5.4 6 1.7
5.0a 6 1.5
7.9b 6 2.6
8.9 6 4.4
8.0a 6 2.3
9.8b 6 6.7
a
a
channel or subject to significant downstream changes.
On the other hand, we observed compositional differences among the fine, coarse, and dissolved organic
fractions from the same water samples. Another important similarity between the Ji-Paraná River and the
major rivers of the Amazon Basin is that both appear
to share common organic-matter sources. The three size
fractions appear to have a common source: tree leaves
and soil organic matter from the tropical rainforest. We
reached this conclusion for the Ji-Paraná Basin based
on the fact that the three fractions exhibit compositions
near those of the tree leaf and soil organic-matter end
members (Figs. 3, 4, and 5). Secondly, the Ji-Paraná
size fractions plotted near the Amazon River particles,
suggesting that both systems have similar organic-matter sources. The organic degradation stages of the size
fractions in the Ji-Paraná Basin also appear to be similar to what has been found in other Amazonian and
South American rivers (Martinelli et al. 1999, Hedges
et al. 2000, Devol and Hedges 2001, Krusche et al.
2002). The coarse fraction of the Ji-Paraná River appears to be the least degraded and resembles the remains of tree leaves (Fig. 11A). The relatively high
syringyl/vanillyl and cinnamyl/vanillyl ratios measured
in coarse and fine size fractions indicate that an important amount of lignin in Ji-Paraná Basin originates
from non-woody angiosperm plants (Fig. 10). The fine
fraction is more degraded than the coarse fraction and
during this process there was a loss of lignin-derived
phenols and an increase in the d13C values (Fig. 11).
Although the fine fraction is more degraded, this fraction is richer in nitrogen (Figs. 7 and 9). This characteristic was also found in other rivers of the Amazon
(Hedges et al. 2000) and also in rivers of southeast
Brazil (Krusche et al. 2002). This N enrichment is probably due to the fact that nitrogenous organic matter
selectively accumulates in the fine fractions with time
by preferential sorption on soil minerals before they
are eroded into aquatic systems (Hedges et al. 2000,
Aufdenkampe et al. 2001). In addition, nitrogen-rich
remains of microbial fauna tend to concentrate in finegrain minerals (Hedges and Oades 1997, Amelung et
al. 1999). Finally, the most degraded fraction appears
to be the ultrafiltered dissolved organic material
(UDOM; Fig. 11).
of the three organic matter size fractions.
Organic C
(mass %)
a
S273
Total N
(mass %)
C:N
0.53 6 0.27
0.72a 6 0.25
0.85b 6 0.88
18 6 7
12b 6 2
18a 6 11
a
a
Suspended
sediments
(mg/L)
L (mg/100 g
organic C)
(Ad/Al)v
2.3 6 2.9
7.81 6 1.71 0.27a 6 0.05
20.5b 6 12.5 2.48b 6 0.72 0.72b 6 0.14
0.73c 6 2.27 2.27c 6 0.31
a
a
Notes: Values reported for d13C are the deviations (‰) of the 13C:12C of the samples from the same ratio for the PDB
standard; d15N are the deviations (‰) of the 15N:14N of the samples from the same ratio for the atmospheric N2 stable isotope
standard; L is the total yield of lignin-derived phenols normalized to 100 mg of organic carbon in the sample; (Ad/Al)v is
the acid-to-aldehyde ratio of vanillyl phenols. UDOM is ultrafiltered dissolved organic matter. Different letters indicate
statistically significant differences between averages.
S274
MARCELO C. BERNARDES ET AL.
Ecological Applications
Special Issue
and its major white-water tributaries (Table 2), including the Beni Basin (Hedges et al. 2000). Even the heavily sewage-contaminated rivers of the Piracicaba Basin
had lower carbon and nitrogen concentration in these
fine and coarse fractions (Krusche et al. 2002). We do
not have a good explanation for these much higher C
and N concentrations in the coarse and fine fractions
of Ji-Paraná rivers. One possible explanation independent of recent land-cover alterations would be that rivers of the Ji-Paraná Basin drain mainly lowland forests,
which constitute a continuous source of organic matter
with little diluting mineral matter. The suspended solids
concentration is an order of magnitude smaller in the
Ji-Paraná Basin in comparison to the Solimões/Amazon
River and its white-water tributaries (Table 2). This
explanation is consistent with lower d13C values found
in the coarse and fine particles of Ji-Paraná rivers in
relation to the white-waters Amazon rivers, which drain
high altitude regions of the Andean mountains that are
a source of 13C-enriched organic matter (Quay et al.
1992, Hedges et al. 2000). A similar situation occurs
in the Jutaı́ and Negro rivers (black-water tributaries)
that drain exclusively Amazonian lowlands and combine lower OC% and TN% levels with lower d13C values than white-water rivers (Table 2). The fine fractions
of the Ji-Paraná rivers follow the classic inverse relationship between OC% and suspended solids concentrations (Fig. 6). The majority of the particulate organic
matter in the Amazon main stem is associated with
mineral grains and is a direct function of the total sur-
FIG. 7. (A) Plot of organic carbon vs. total nitrogen for
Ji-Paraná coarse fractions (open squares), fine fractions (open
circles), leaf end members (rectangles representing the distribution of C4 leaves from pastures and C3 leaves from forests), and soils of Rondônia (filled circles). (B) Zoom of
region outlined in (A). (C) Plot of organic carbon vs. total
nitrogen for the Amazon River coarse (open square) and fine
(open circle) fractions. Values are from the following sources:
tree leaves, L. A. Martinelli and J. E. Ehleringer (unpublished
data); Rondônia soils, M. V. Ballester (unpublished data);
Manaus and Santarém soils, E. V. Telles (unpublished data);
Amazon River coarse and fine fractions, Hedges et al. (1986).
In general, the compositional differences between
the Ji-Paraná River, the Amazon River, and the Amazon
major tributaries were not large enough to indicate different organic matter sources among the rivers. The
exception is the higher carbon and nitrogen concentrations in the coarse and fine fractions of rivers of the
Ji-Paraná Basin in comparison with the Amazon River
FIG. 8. Plot of d15N vs. d13C for the three size fractions
(coarse, fine, and ultrafiltered dissolved organic matter
[UDOM]; error bars represent 61 SD) and the following end
members: C4 leaves from pastures; C3 leaves from forests,
and C3 leaves from soil organic matter (boxes represent the
distribution of all points). Values are from the following
sources: C4 leaves from pasture were collected in Santarém
(L. A. Martinelli and J. E. Ehleringer, unpublished data); tree
leaves were collected in Ji-Paraná, Santarém, and Manaus (L.
A. Martinelli and J. E. Ehleringer, unpublished data); forest
soil organic matter was collected in forests near Manaus and
Santarém (E. V. Telles, unpublished data).
August 2004
ORGANIC MATTER OF AMAZON LOWLAND RIVERS
S275
FIG. 9. Plot of N:C ratio vs. d13C for the
three size fractions (coarse, fine, and ultrafiltered dissolved organic matter [UDOM]; error
bars represent 61 SD) and the following end
members: tree leaves from forests; forest soil;
soil covered with a pastures of age 3–5 yr, 7–
13 yr, 20 yr, and 80 yr (boxes represent the
distribution of all points). Tree leaves were collected in Ji-Paraná, Santarém, and Manaus (L.
A. Martinelli and J. E. Ehleringer, unpublished
data); forest soil organic matter was collected
in forests near Manaus and Santarém (E. V.
Telles, unpublished data); pasture soils were
collected at several sites in the Rondônia State
(Neill et al. 1997).
face area of suspended sediment particles, i.e., proportionately more carbon is attached to smaller particles (Keil et al. 1994). If the same association holds
for the Ji-Paraná Basin, it is likely that, in addition to
the lack of dilution of the particulate organic matter by
higher suspended particles concentrations, a higher
proportion of the particulate organic matter load is
transported by smaller particles, with proportionately
more surface area than the Amazon main stem and its
white-waters tributaries.
The land cover of the Rondônia State, and especially
of the Ji-Paraná Basin, has experienced significant
changes in the last 30–40 yr. Approximately 35% of
the area of the Ji-Paraná Basin has been altered, the
main change being the replacement of the original forest by pastures, which in 1999 occupied 30% of this
basin (Ballester et al. 2003). In some sub-basins, such
as the Rolim de Moura, the area covered with pastures
reaches almost 70% (Table 1). In the basins of the rivers
FIG. 10. Plot of syringyl:vanillyl ratio vs. cinnamyl:vanillyl ratio for the three size fractions (coarse, fine, and ultrafiltered dissolved organic matter [UDOM]; error bars represent 61 SD); coarse and fine fractions of the Amazon River
(boxes represent the distribution of all points); and forest tree
leaves as end members (boxes represent the distribution of
all points). Values for the Amazon coarse and fine fractions
and leaf end members are from Hedges et al. (1986).
Urupá and Jarú, approximately half of the forest has
been replaced by pasture (Table 1). Less-altered areas
are located primarily in the lower portions of the basin,
which includes the sub-basins of the rivers Machadinho, JIP-4, and JIP-5 (Table 1).
The fact that essentially all pastures in the Ji-Paraná
Basin are cultivated with C4 grass species provides an
opportunity to test whether large land-use changes have
FIG. 11. Plots of acid:aldehyde ratio of vanillyl phenols
((Ad/Al)v) vs. (A) carbon-normalized yields of total ligninderived phenols (L) and (B) d13C for the three size fractions
(coarse, fine, and ultrafiltered dissolved organic matter
[UDOM]; error bars represent 61 SD), the coarse and fine
fractions of the Amazon River (boxes represent the distribution of all points), and forest tree leaves as end members
(boxes represent the distribution of all points). Values for the
Amazon coarse and fine fractions and leaf end members are
from Hedges et al. (1986).
Ecological Applications
Special Issue
MARCELO C. BERNARDES ET AL.
S276
TABLE 6. Matrix of component loading of principal component analysis for the coarse organic
matter fraction.
Variable
d13C
d15N
Organic C (%)
Total N (%)
Forest (%)
Pasture (%)
Sand (%)
Clay (%)
Silt (%)
Altitude
Slope
Variance (%)
Factor 1
Factor 2
Factor 3
0.79
Factor 4
Communalities
(%)†
0.25
82
77
95
86
87
86
86
85
86
86
86
80.6
0.69
0.96
0.87
0.31
0.81
0.81
0.85
0.45
24.5
0.30
0.78
24.1
17.5
0.79
0.92
14.5
Note: Only factors larger than 0.2 are shown.
† The percentage of variance accounted for by the current number of factors.
already affected the compositional characteristics of
the organic-matter size fractions carried into this basin.
This is because C4 grasses have d13C values varying
between 211 and 214‰, while forest C3 leaves in the
tropics have characteristically low d13C values, varying
from 228 to 234‰ (Farquhar et al. 1989, Martinelli
et al. 1998). In ecosystems where C4 grasses naturally
occur, their presence can be detected either in the soil
(Cerri and Volkoff 1987) or in river particles (Mariotti
et al. 1991, Bird et al. 1994, 1998). In agricultural
ecosystems, where an original C3 forest has been replaced by some kind of C4 plants, the C4-derived organic matter quickly becomes incorporated into the surface soil layers (Cerri et al. 1985, Vitorello et al. 1989,
Moraes et al. 1996, Neill et al. 1996, 1997). For instance, the d13C value of the surface soil layer sampled
at the Fazenda Nova Vida, 120 km north of the city of
Ji-Paraná, changed from 228.1‰ to 224.7‰,
220.6‰, and 218.3‰ after 3, 9, and 20 yr of pasture
cultivation, respectively (Neill et al. 1996, 1997). Newly introduced C4 material appears also to be quickly
incorporated in the aquatic systems. A preliminary in-
vestigation in this cattle ranch (Fazenda Nova Vida)
on the stable isotopic composition of riverine organic
matter size fractions of a first order stream, suggests
that changes start in small streams. We found a change
in the d13C of the fine fraction from 227.2‰ to
220.5‰ when a small stream (;3 m width) leaves the
forest and enters in a pasture in a reach of only 100
m, (L. F. Charbel, unpublished data). The same riverine
organic matter dynamic was observed in rivers of the
Piracicaba River basin, where the introduction of C4
agricultural fields occurred 70–80 year ago and an increase in the d13C values of the size fractions was detected (Martinelli et al. 1999). This replacement, from
forest to sugar cane or pasture, was mainly associated
with faster cycling fraction (UDOM), while the original
vegetation remains were mainly associated with slower
cycling fractions (CSS and FSS) (Krusche et al. 2002).
In the Amazon River and in the Beni River, areas covered mainly by C4 grasses had the UDOM fraction with
the heaviest d13C values in relation to the fine and
coarse fraction (Hedges et al. 1986, 2000). Conversely,
TABLE 7. Matrix of component loading of principal component analysis for the fine organic
matter fraction.
Variable
Factor 1
Factor 2
d13C
d15N
Organic
Total N
Forest
Pasture
Sand (%)
Clay (%)
Silt (%)
Altitude
Slope
Variance (%)
0.85
0.61
0.40
Factor 3
Factor 4
Communalities
(%)†
0.37
0.97
0.95
0.79
0.85
0.33
0.98
0.97
0.83
28.5
25.0
14.6
0.85
0.78
10.2
Note: Only factors larger than 0.2 are shown.
† The percentage of variance accounted for by the current number of factors.
85
75
94
94
80
84
97
96
84
81
75
78.3
ORGANIC MATTER OF AMAZON LOWLAND RIVERS
August 2004
S277
TABLE 8. Matrix of component loading of principal component analysis for the unfiltered
dissolved organic matter (UDOM) fraction.
Variable
Factor 1
d13C
d15N
Organic
Total N
Forest
Pasture
Sand (%)
Clay (%)
Silt (%)
Altitude
Slope
Variance (%)
0.83
Factor 2
Factor 3
0.27
0.40
0.80
0.81
0.70
Factor 4
Communalities
(%)†
0.88
0.93
0.74
23.5
0.99
0.30
20.1
19.8
0.91
0.79
15.4
79
75
79
77
83
91
99
98
78
86
83
78.8
Note: Only factors larger than 0.2 are shown.
† The percentage of variance accounted for by the current number of factors.
in areas where C4 grasses are not important, the d13C
of the UDOM fraction was lightest.
Comparisons of d13C average values for the three
size fractions with those of tree leaves and forest soils
(Figs. 8 and 9) did not allow us to detect a major signal
of the presence of C4-derived organic matter in the main
channel of the Ji-Paraná River. The average deforestation extent of the all sampled basins is relatively low
(;30%), which may alone account for the low riverine
signal. On the other hand, the PCA developed with all
data showed correlations between the areas covered
with pasture and the d13C values of the three size fractions (Tables 6–8). In addition, the highest d13C values
of our results were observed in the UDOM of the Rolim-de-Moura and Jarú rivers, which have among the
highest areas covered with pasture (Table 1). The lower
the order of the streams and the higher the pasture area,
greater is the possibility that the C4-derived organic
matter signal will be detected first in the faster-cycling
fraction (UDOM).
The fact that we found a strong correlation between
pasture area and d13C values of the three size fractions
suggests that the large-scale deforestation in Rondônia
State, started in early 1970, is affecting the origin of
the carbon in the Ji-Paraná River basin. The extent of
changes in the carbon isotopic composition of size fractions in the Ji-Paraná Basin should be investigated in
more detail. However, the strong association among
d13C values, pasture area and soils texture, suggests
that soil texture may have a strong influence on how
the C4 signal moves from the terrestrial to the aquatic
system. In the Congo River Basin, Mariotti et al. (1991)
noticed that, in areas where there was a predominance
of sandy soils, the d13C of riverine size fractions was
controlled mainly by riparian vegetation. In contrast,
in areas of the basin where clay-texture soils predominate, the entire vegetation cover of the basin was the
most important factor. Riparian vegetation in Rondônia
rivers has a predominance of forests with C3 plants. A
preliminary survey of the soil texture of the A horizon
in Rondônia State revealed a high percentage of sand
in several sub-basins of the Ji-Paraná Basin (Table 1).
Therefore, depending on the soil texture, riparian forest
vegetation could be more important than the area of
the basin covered with pasture (Mariotti et al. 1991,
McClain et al. 1997).
CONCLUSIONS
Most of the earlier studies in the Amazon Basin rivers focused on rivers that had their headwaters in the
Andes or sub-Andean regions (Hedges et al. 1986,
1994, 2000). These rivers are characterized by high
suspended solids concentrations (white-water rivers),
and their riverine organic matter has two geographically distinct allochthonous sources, the Andean region
and the Amazon lowlands. The rivers that we investigated in this study have their drainage basin almost
exclusively in the Amazon lowlands, draining mainly
the Precambrian shield. These clear to black-water rivers have a lower concentration of suspended solids, and
lowlands are their only sources of allochthonous organic matter. Therefore, the results of this study extend
our knowledge about the composition and dynamics of
size fractionated organic matter over South America
river types that have not been extensively investigated
in the past.
The principal differences that were observed for the
Ji-Paraná river system included higher carbon and nitrogen concentration found in the three size fractions
of Ji-Paraná rivers in comparison with Amazon whitewater and black-water tributaries (Table 3). We do not
have a definite explanation for these differences.
However, some of the characteristics of organic matter from white-water rivers were similar for rivers of
the Ji-Paraná Basin. For instance, we observed compositional differences between the three size fractions
that suggested substantial differences in the stages of
degradation between size fractions despite similar organic matter sources. The coarse fraction is the least
degraded and its main source appears to be leaves from
MARCELO C. BERNARDES ET AL.
S278
lowland forests (Devol and Hedges 2001). The fine
fraction is mostly associated with a mineral soil phase,
but its ultimate source appears also to be leaves from
forests. This fraction was also enriched in nitrogen as
for other rivers of the Amazon. The ultrafiltered-dissolved organic fraction appears to have the same source
as the coarse fraction, but this is the most degraded
fraction.
Although the organic matter transported throughout
the main channel of the Ji-Paraná River seems to share
the same sources as the Amazon Rivers, principal component analysis showed high communality for factors
explained by the variables d13C and pasture area in all
three size fractions. The highest d13C values were observed in the UDOM of the sub-basins with the highest
areas covered by pasture.
Finally, the large change in land-use in the Ji-Paraná
Basin, replacement of primary forests by C4 pastures
for cattle feeding, that has taken place in the last 30–
40 yr, has already changed the composition of the riverine organic matter size fractions. Any attempt to understand those changes must take into account the faster-cycling fraction (UDOM) and the low-order streams.
ACKNOWLEDGMENTS
We thank John Melack, Trent Biggs, and one anonymous
reviewer for providing valuable comments and discussion to
the manuscript. This work was supported by FAPESP (Proc.
01/07580-5 and Projeto Temático 99/01159-4) and by NASA–
LBA Ecology (CD-06 and ND-09).
LITERATURE CITED
Amelung, W., R. Bol, and C. Friedrich. 1999. Natural C-13
abundance: a tool to trace the incorporation of dung-derived
carbon into soil particle-size fractions. Rapid Communications in Mass Spectrometry 13:1291–1294.
Aufdenkampe, A. K., J. I. Hedges, J. E. Jeffrey, A. V. Krusche, and C. A. Llerema. 2001. Sorptive fractionation of
dissolved organic nitrogen and amino acids onto fine sediments within the Amazon Basin. Limnology and Oceanography 46(8):1921–1935.
Ballester, M. V., D. C. Victoria, A. V. Krusche, R. Coburn,
R. L. Victoria, J. E. Richey, M. G. Logsdon, E. Mayorga,
and E. Matricardi. 2003. A remote sensing/GIS-based
physical template to understand the biogeochemistry of the
Ji-Paraná river basin (Western Amazonia). Remote Sensing
of Environment 87:429–445.
Biggs, T. W., T. Dunne, T. F. Domingues, and L. A. Martinelli.
2002. Relative influence of natural watershed properties
and human disturbance on stream solute concentrations in
the southwest Brazilian Amazon Basin. Water Resources
Research 38(8):1150.
Bird, M. I., P. Giresse, and A. R. Chivas. 1994. Effect of
forest and savanna vegetation on the carbon-isotope composition of sediments from the Sanaga River, Cameroon.
Limnology and Oceanography 39:1845–1854.
Bird, M. I., P. Giresse, and S. Ngos. 1998. A seasonal cycle
in the carbon-isotope composition of organic carbon in the
Sanaga River, Cameroon. Limnology and Oceanography
43:143–146.
Camargo, P. B., S. Trumbore, L. A. Martinelli, E. A. Davidson, D. C. Nepstad, and R. L. Victoria. 1999. Soil carbon
dynamics in regrowing forest of eastern Amazonia. Global
Change Biology 5:693–702.
Ecological Applications
Special Issue
Cerri, C., C. Feller, J. Balesdent, R. Victoria, and A. Plenecassagne. 1985. Particle-size fractionation and stable carbon isotope distribution applied to the study of soil organic
matter dynamics. Comptes Rendus de la Academie des Sciences Serie II 300:423–428.
Cerri, C., and B. Volkoff. 1987. Carbon content in a yellow
latsol of central Amazon rain-forest. Acta Oecologica–Oecologia Generalis 8:29–42.
Desjardins, T., F. Andreux, B. Volkoff, and C. C. Cerri. 1994.
Organic carbon and 13C content in soils and soil size-fractions, and their changes due to deforestation and pasture
installation in eastern Amazonia. Geoderma 61:103–118.
Devol, A. H., and J. I. Hedges. 2001. Organic matter and
nutrients in the main stem Amazon River. Pages 275–306
in M. E. McClain, R. L. Victoria, and J. E. Richey, editors.
The biogeochemistry of the Amazon Basin. Oxford University Press, Oxford, UK.
Ertel, J. R., J. I. Hedges, A. H. Devol, J. E. Richey, and M.
D. G. Ribeiro. 1986. Dissolved humic substances of the
Amazon River system. Limnology and Oceanography 31:
739–754.
Farquhar, G. D. 1989. Models of integrated photosynthesis
of cells and leaves. Philosophical Transactions of the Royal
Society of London Series B-Biological Sciences 323:357–
367.
Goñi, M. A., and J. I. Hedges. 1990. Cutin-derived CuO
reaction products from purified cuticles and tree leaves.
Geochimica et Cosmochimica Acta 54:3065–3072.
Hedges, J. I., R. A. Blanchette, K. Welihy, and A. H. Devol.
1988. Effects of fungal degradation on the CuO oxidation
products of lignin: a controlled laboratory study. Geochimica et Cosmochimica Acta 52:2717–2726.
Hedges, J. I., W. A. Clark, P. D. Quay, J. E. Richey, A. H.
Devol, and U. D. Santos. 1986. Compositions and fluxes
of particulate organic material in the Amazon River. Limnology and Oceanography 31:717–738.
Hedges, J. I., G. L. Cowie, J. E. Richey, P. D. Quay, R. Benner,
M. Strom, and B. R. Forsberg. 1994. Origins and processing of organic matter in the Amazon River as indicated
by carbohydrates and amino acids. Limnology and Oceanography 39:743–761.
Hedges, J. I., and J. R. Ertel. 1982. Characterization of lignin
by capillary gas chromatography of cupric oxide oxidation
products. Analytical Chemistry 54:174–178.
Hedges, J. I., P. G. Hatcher, J. R. Ertel, and K. J. Meyersschulte. 1992. A comparison of dissolved humic substances
from seawater with Amazon River counterparts by C-13NMR spectrometry. Geochimica et Cosmochimica Acta 56:
1753–1757.
Hedges, J. I., et al. 2000. Organic matter in Bolivian tributaries of the Amazon River: a comparison to the lower
mainstream. Limnology and Oceanography 45:1449–1466.
Hedges, J. I., and J. M. Oades. 1997. Comparative organic
geochemistries of soils and marine sediments. Organic
Geochemistry 27:319–361.
INPE (Instituto Nacional de Pesquisas Espaciais). 2001.
Monitoring of the Brazilian Amazon forest by satellite
1999–2000. Instituto Nacional de Pesquisas Espaciais, São
José dos Campos, SP, Brazil.
Keil, R. G., D. B. Montluçon, F. G. Prahl, and J. I. Hedges.
1994. Sorptive preservation of labile organic matter in marine sediments. Nature 370:549–552.
Krusche, A. V., L. A. Martinelli, R. L. Victoria, M. C. Bernardes, P. B. Camargo, and S. Trumbore. 2002. Composition of particulate organic matter in a disturbed basin of
southeast Brazil (Piracicaba River basin). Water Research
36:2743–2752.
Mariotti, A., F. Gadel, P. Giresse, and Kingamouzeo. 1991.
Carbon isotope composition and geochemistry of particulate organic-matter in the Congo River (Central-Africa)—
August 2004
ORGANIC MATTER OF AMAZON LOWLAND RIVERS
application to the study of quaternary sediments off the
mouth of the river. Chemical Geology 86:345–357.
Martinelli, L. A., S. Almeida, I. F. Brown, M. Z. Moreira, R.
L. Victoria, L. S. L. Sternberg, C. A. C. Ferreira, and W.
W. Thomas. 1998. Stable carbon isotope ratio of tree
leaves, boles and fine litter in a tropical forest in Rondônia,
Brazil. Oecologia 114:170–179.
Martinelli, L. A., M. V. R. Ballester, A. V. Krusche, R. L.
Victoria, P. B. Camargo, M. Bernardes, and J. P. H. B.
Ometto. 1999. Landcover changes and 13C composition of
riverine particulate organic matter in the Piracicaba River
basin (southeast region of Brazil). Limnology and Oceanography 44:1826–1833.
Martinelli, L. A., R. L. Victoria, J. L. I. Demate, J. E. Richey,
and A. H. Devol. 1993. Chemical and mineralogical composition of Amazon River floodplain sediments, Brazil. Applied Geochemistry 8:391–402.
McClain, M. E., J. E. Richey, J. A. Brandes, and T. P. Pimentel. 1997. Dissolved organic matter and terrestrial-lotic
linkages in the central Amazon Basin of Brazil. Global
Biogeochemical Cycles 11:295–311.
Moraes, J. F. L., B. Volkoff, C. C. Cerri, and M. Bernoux.
1996. Soil properties under Amazon forest and changes
due to pasture installation in Rondônia, Brasil. Geoderma
70:63–81.
Neill, C., L. A. Deegan, S. M. Thomas, and C. C. Cerri. 2001.
Deforestation for pastures alters nitrogen and phosphorus
in small Amazon streams. Ecological Applications 11:
1817–1828.
Neill, C., B. Fry, J. M. Melillo, P. A. Steudler, J. F. L. Moraes,
and C. C. Cerri. 1996. Forest and pasture-derived carbon
S279
contributions to carbon stocks and microbial respiration of
tropical pasture soils. Oecologia 107:113–119.
Neill, C., J. M. Melillo, P. A. Steudler, C. C. Cerri, J. F. L.
Moraes, M. C. Piccolo, and M. Brito. 1997. Soil carbon
and nitrogen stocks following forest clearing for pasture in
the southwestern Brazilian Amazon. Ecological Applications 7:1216–1225.
Opsahl, S., and R. Benner. 1995. Early diagenisis of vascular
plant-tissue—lignin and cutin decomposition and biogeochemical implications. Geochimica et Cosmochimica Acta
59:4889–4904.
Quay, P. D., D. O. Wilbur, J. E. Richey, J. I. Hedges, A. H.
Devol, and R. Victoria. 1992. Carbon cycling in the Amazon River—implications from the C-13 compositions of
particles and solutes. Limnology and Oceanography 37:
857–871.
Richey, J. E., J. I. Hedges, A. H. Devol, P. D. Quay, R.
Victoria, L. Martinelli, and B. R. Forsberg. 1990. Biogeochemistry of carbon in the Amazon River. Limnology and
Oceanography 35:352–371.
Trumbore, S. E., E. A. Davidson, P. B. Camargo, D. C. Nepstad, and L. A. Martinelli. 1995. Below ground cycling of
carbon in forests and pastures of eastern amazonia. Global
Biogeochemical Cycles 9:515–528.
Vitorello, V. A., C. C. Cerri, A. Andreaux, C. Feller, and R.
L. Victoria. 1989. Organic matter and natural carbon-13
distribution in forested and cultivated oxisols. Soil Science
Society American Journal 53:773–778.
Williams, M. R., and J. M. Melack. 1997. Solute export from
forested and partially deforested catchments in the central
Amazon. Biogeochemistry 38:67–102.