Iron Reduction and Soil Phosphorus Solubilization in Humid Tropical Forests Soils: The Roles
of Labile Carbon Pools and an Electron Shuttle Compound
Author(s): Noemi Chacon, Whendee L. Silver, Eric A. Dubinsky and Daniela F. Cusack
Source: Biogeochemistry, Vol. 78, No. 1 (Mar., 2006), pp. 67-84
Published by: Springer
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? Springer 2006
Biogeochemistry (2006) 78: 67-84
DOI 10.1007/s10533-005-2343-3
Iron reduction and soil phosphorus solubilization
in humid tropical forests soils: the roles of labile
carbon pools and an electron shuttle compound
NOEMI CHACON*, WHENDEE L. SILVER, ERIC A. DUBINSKY
and DANIELA F. CUSACK
Ecosystem Sciences Division, Department of Environmental Science, Policy andManagement, 137
Mulford Hall 3114, University of California, Berkeley, CA 94720, USA; *Authorfor correspondence:
Lab. Ecologia de Suelos, Centro de Ecologia, Instituto Venezolano de InvestigacionesCientificas
Carretera
(IVIC),
Km.
Panamericana,
11, Apdo.
Caracas
21827,
1020
Venezuela
A,
(e-mail:
[email protected],nchacon(nature.berkeley.edu; Fax: + 1-58-212-5041088)
Received 21 April 2005; accepted in revised form 22 August 2005
Key words: Acetate, Anaerobic soils, AQDS, Glucose, Highly weathered soils, Nutrient cycling,
Phosphorus limitation, Soil redox
Abstract. The affinity of iron oxides and hydroxides for phosphorus is thought to contribute to
phosphorus limitation to net primary productivity in humid tropical forests on acidic, highly
weathered soils. Perennially warm, humid conditions and high biological activity in these soils can
result in fluctuating redox potential that in turn leads to considerable iron reduction in thepresence
of
labile
carbon
combination
shuttle
and
with
on
compound
cose or acetate
humic
was
substances.
of
the addition
iron reduction
labile
We
substrates
and phosphorus
to soils as a single dose
added
the effects
investigated
carbon
release
of
acetate)
and
in a humid
tropical
forest
at the beginning
in
conditions
reducing
and
(glucose
of the experiment,
an electron
soil. Glu
and as pulsed
inputs over time,which more closely mimics patterns in labile carbon availability. Iron reduction
and phosphorus
the addition
additions
mobilization
were weakly
of the electron
produced
shuttle
a significant
increase
by a single
stimulated
or without
with
compound
in soil pH,
low level addition
added
soluble
carbon.
of carbon,
Pulsed
iron, and phosphorus
and
labile carbon
concentrations.
Pulsed labile carbon inputs also promoted the precipitation of ferrous hydroxide complexes which
could
increase
exceeded
for released
coupled
P,
with
soil phosphorus
for P sorption,
the capacity
Plant
re-adsorption.
limiting
periodic
and microbial
although
the role of P re-adsorption.
carbon
mobilization,
our results
P demand
inputs
can
stimulate
which
may
provide
suggest
are also
Our
likely
results
iron reduction
a source
that rates of P solubilization
to serve as an important
suggest
that reducing
and a corresponding
of phosphorus
to plants
sinks
conditions
increase
in
and microor
ganisms previously undocumented in these ecosystems.
Introduction
Highly weathered, humid tropical forest soils are often characterized by a
dominance
of iron (Fe)-rich
minerals,
high
rates of carbon
(C) cycling,
and
variable or fluctuating redox conditions. These characteristics lead to the
for rapid rates of Fe reduction and re-oxidation.
potential
Old, wet tropical
forest soils also tend to have low concentrations
of labile phosphorus
(P) due in
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68
large part to minerals with high P sorption capacities
(Sanchez 1976). Crys
talline and non-crystalline
oxides of Fe and aluminum
(Al) are considered
the
in acidic soils (Parfitt et al. 1975; Hsu
sinks of phosphate
main geochemical
1977; Lopez-Hern'andez 1977; Schwertmann and Taylor 1977; Parfitt 1978);
Fe and Al oxides
non-crystalline
tend to control
soil sorption reactions due to
P extraction procedures
their large specific surface area (Parfitt 1989). Standard
conducted under aerobic conditions often yield low labile inorganic P pools
et al. 2003), and have led to the assumption
of their P from soil organic matter
the majority
et al. 1994; Chacon
(Herrera et al. 1978; Jordan 1982; Tiessen
and Dezzeo
2004). The organic P pool is generally small in relation to the inorganic P pool
the amount of the inorganic P in
(Cross and Schlesinger
1995); for example,
from tropical
forests
soils (Johnson
that tropical
forests
obtain
resistant
form
typically
ranges between
40 and 80% of the total P in the soil
(Tiessen et al. 1994).
for P is thought
The high affinity of soil Fe and Al minerals
to be a primary
mechanism responsible for P limitation of net primary productivity (NPP) in
humid tropical forests (Vitousek 1984;Vitousek and Sanford 1986). This no
et al. 2000;
C density
tion contrasts with high aboveground
(Mackensen
Dezzeo
and Chacon 2005), large P pools in forest soils and vegetation
(Scatena
et al. 2000), and high
et al. 1993; Silver 1994; Silver et al. 1996; Mackensen
et al. 2004) reported for these forests. Although
rates of P cycling (McGroddy
P retention by Fe and Al oxides has been considered
a process of low revers
ibility in highly weathered tropical soils (Gijsman et al. 1996), undoubtedly the
amounts of P from this appreciable
transfer of even modest
pool to the soil
soil P bioavailability.
solution can play an important role in maintaining
There are several mechanisms
that could result in the release of P from
geochemical pools under low redox conditions, including reduction of Fe(III)
of Fe and Al phosphates,
and release of
hydrolysis and dissolution
and Patrick 1978;
clay-associated
phosphates
1972; Gambrell
(Ponnamperuma
et al. 2005). Under
Baldwin
and Mitchell
2000; Chacon
reducing conditions
the oxidation of organic matter
bacteria obtain energy for growth by coupling
to the reduction of different electron acceptors
(Quantin et al. 2002; Stemmler
and Berthelin 2003; Weiss et al. 2004). Manganese
and Fe oxides are among the
phosphates,
main
electron
acceptors
in soils under anaerobic
condition
(Lovley
and Phillips
et al. 2002). As Fe(II) production
anions
1986; Quintin
occurs, phosphate
to Fe(III) oxides are released (Baldwin and Mitchell
associated
chemically
2000).
These
processes
fluctuating
are likely to be stimulated
redox conditions
associated
with
by the availability of labile C and
and warm perhumid
high NPP,
conditions
typical of wet tropical forests (Figure 1). Iron reduction is fueled by
the availability of organic acids of low-molecular weight such as acetate (Kuisel
et al. 2002). More complex organic substrates such as glucose can also be used
it has been suggested
that less than 5% of the
by Fe(III) reducers, however,
are transferred
to Fe(III), while most of the glucose
is
reducing equivalents
degraded by fermentation
(Lovley 1991). Humic substances can affect patterns
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69
of Fe
reduction
and
in soils.
re-oxidation
Several
studies
have
shown
that
Geobacter metallireducens and Shewanella alga can use humic substances and
quinones to transfer electrons between electron donors and acceptors (Lovley
et al. 1996, 1998). For example, experiments with anthraquinone-2,6-disulfo
acid, have shown that it can increase the
(Fredrickson
et al. 1998; Zachara et al.
nate (AQDS), an analog to the humic
rate and amount of Fe(III) reduction
1998).
In this studywe conducted a laboratory experiment to investigate the effects
on Fe reduction and soil P release in a humid tropical
of reducing conditions
forest soil. We examined
the effects of changes in redox alone, and in combi
nation with the addition of an easily fermentable C substrate (acetate), a less
fermentableC substrate (glucose), and an electron shuttle compound (AQDS)
with and without
an additional C substrate. We added glucose and acetate as a
single dose and as a pulsed input over time. Pulsed inputs of organic substances
to the soil are likely to have a different impact on microbial
processes
and
biogeochemical cycling than static inputs, particularly if inputs effectively
replenish resources depleted by biological or biogeochemical processes. In
humid tropical forests, inputs of labile C tend to be pulsed, as opposed
to
constant over time or strongly seasonal and are driven by patterns in rainfall,
(Lodge et al. 1994). We
wind, and plant and microbial
growth and mortality
hypothesized themicrobial reduction of Fe(III) can be an importantmecha
nism for increasedbioavailability of soil P due to frequent reducing conditions,
and abundant
labile C and Fe minerals.
)
gh Rainfall
~~~~~2 ~
High clay content
organic mafter
and/or
c
~
o
CD
CD
,
\
\
b
~~~~~Lifter
Fe" + P04
I
Low soil oxygen
iron
Dissimilatory
reducing bacteria
Figure
1.
Anaerobic
Schematic
model
decomposition
of Fe(III)
-
Inputs of labile
organic C
reduction
and P release
Electron
transfer
in humid
tropical
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Fe"'-O-PO4
forests
soils.
70
Materials andmethods
Study area
The study was conducted with soils sampled from the Bisley Research
Watersheds, part of the NSF-Sponsored Long Term Ecological Research
Program in the Luquillo Experimental Forest (LEF) in northeastern Puerto
Rico
(18?18' N,
550 m
above
65?50' W).
sea level,
The
receive
Bisley Watersheds
approximately
between
350 and
of rainfall
per year
occur
3500 mm
relatively evenly distributed throughout the year, and have an average annual
temperature
of 23 ?C with
little seasonal
variation
(Brown
et al. 1986; Scatena
1989). Soils in the LEF are derived from volcanic sedimentswith Tertiary-age
intrusions of the Rio Blanco stock (Frizano et al. 2002). Soils at
quartz-diorite
as acidic with high clay, Al, and Fe content.
the study sites are characterized
The labile P fraction considered most
accessible
to plant roots (Cross and
in these soils, while the moderately
Schlesinger
1995) was not detectable
labile
NaOH-extractable pool and the recalcitrant concentrated HCl-extractable
of the total P in the soil (McGroddy
in the Humatus-Cristal
pool represent the 20 and 67% respectively
and Silver 2000). These soils are classified
as Ultisols
Zarzal series.
Soil sample and incubation
We collected a composite
soil sample (about 10 kg) from the 0-10 cm depth.
to U.C. Berkeley and maintained
at room
The sample was shipped immediately
in order to avoid detrimental
temperature
impacts to microbes
(Verchot 1999).
removed and the samples were evenly split
Upon arrival, roots were manually
into seven treatments with 35 replicates each (Table 1). Our additions of labile
to 0.09 mg C g dry soil-'. This represents only a small percentage
C amounted
as reported inMcGroddy
and
of the total labile C pool (4.7 mg C g dry soil-)
Silver (2000). Our goal here was to add small pulses of labile C typical of
C inputs
weekly
Table
1.
Description
to the soil.
of
the experimental
treatments.
Treatment
Description
Control
Without additional C source
Acetate
1mM
sodium
acetate
added
at a rate of 0.960 mg
Acetate-3T
1mM
sodium
acetate
added
in three
0.33 mM
Glucose
glucose
Glucose-3T
0.33 mM
AQDS
0.10 mM
AQDS
0.10 mM
AQDS
AQDS
+
glucose
plus
glucose
0.33 mM
added
added
added
added
glucose
installments
at a rate of 0.959 mg
in three
installments
C/20
C/20
at a rate of 0.672 mg
C/20
at a rate of 0.959 mg
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g fresh
g fresh
on days
at a rate of 0.672 mg
added
C/20
on days
soil
0, 2 and
g fresh
soil
g fresh
soil
C/20
soil
0, 2 and
g fresh
7
soil
7
71
The
incubated as a slurry in amber 100 ml serum vials (n = 5
total n = 245), using a 2:1 water to soil ratio. Anoxic conditions
samples were
per treatment,
were
created by flushing the vials for several minutes with 100% N2. Incuba
tions were conducted at 25 ?C for a period of 13 days. At selected times (0, 1, 2,
3, 6, 10, 13 days) five replicate samples from each treatment were destructively
harvested
in a glove box for gas production
and chemical
or consumption
determinations.
We measured
the production
of carbon dioxide
(CO2) and
(CH4) as indices of microbial
methane
activity.
Chemicalmeasurements
We measured
It was
acid-extractable
used here as a measure
Fe(II) using 0.5 N HCl (Chao and Zhou 1983).
of the total extent of reduction (Fe 2+ produc
tion). Ferrous iron (Fe(II)) in the acidified extract was determined using the
ferrozine assay (Lovley and Phillips 1987). Oxalate-extractable
Fe and Al and
the associated P pool were extracted using 0.2 M ammonium
oxalate at pH 3 in
the dark (McKeague
and Day 1966). In reduced soils, oxalate extracts have
been shown to extract poorly crystalline ferrous hydroxides compounds
Fe(OH)2, ferrosoferric hydroxide, ferrous carbonate and soluble Fe(II) (Willet
in the oxalate extract was determined
fol
1978). Phosphorus
lowing Szilas et al. (1998) to avoid interference of the oxalate reagent. A 10 ml
at
aliquot of extract was combined with 5 ml concentrated HNO3, evaporated
in 2 ml 0.3 M H2SO4. Phos
100 ?C, and digested. The residue was dissolved
and Higgings
phorus concentrations were measured using a colorimetric method (Murphy
and Riley 1962) after adjusting the solution to pH 4 using p-nitrophenol.
Iron
in the oxalate extract were measured
on an inductively
and Al concentrations
coupled plasma spectrophotometer
(Thermal Jarrel Ash, Framingham, MA) at
in 0.10 N NaOH
U.C. Berkeley. A second soil subsample was extracted
and
to
for
and
analyzed
P04 according
Murphy
Riley (1962). Soil pH was obtained
in a 1:1 soil to water ratio.
Gas production
The
of each jar was sampled before harvesting
headspace
of CO2 and the production
and/or consumption
to estimate
production
of CH4
the
as an
integratedmeasure of microbial activity. Twenty-five milliliters of gas samples
were
collected
with
geomicrobial
from each vial, transferred to 22 ml serum bottles and sealed
septa and silicon. Carbon dioxide and CH4 were analyzed
on a SRI 8610C gas chromatograph
simultaneously
using a thermal conduc
of
tivity detector
(CO2) and a flame ionization detector
(CH4) at University
of 100 ppm CO2 and 10 ppm CH4 were run
California,
Berkeley. Standards
every
10 samples
to check
for instrument
drift.
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72
Statistical analyses
6.0
Statistical analyses were performed using STATISTICA for Windows
to
of variance
(ANOVA)
analysis
used a one-way
2001). We
(Statistica
if treatments differed in pool sizes or rates. Data were log-trans
determine
We used a
for ANOVA.
to meet
the assumptions
formed when necessary
non
test as a means separation procedure. We used a Kruskal-Wallis
Tukey's
(pH, HCl
that did not meet assumptions
for ANOVA
linear
correlations
Simple
Fe
and
P,
and
index).
Fe, oxalate-extractable
Psat
between
and pH.
Fe(II) production
were used to assess the relationship
=
=
+ bx)
=
m
(y
ln(x)) and linear (y
(y
ex), logarithmic
Exponential
parametric
test on data
and
between Fe(II) production
were used to assess the relationship
Fe. In each case the model with the highest r2 value was
oxalate-extractable
data. The relationship between Fe(II)
selected as the best fit to the experimental
and CO2 or CH4 effluxes was analyzed using Pearson correlation
production
at the 95% level.
coefficients. All the correlations were tested for significance
models
Results
of labile carbon and an electron
Effects
shuttle compound
with
labile C and AQDS
alone and in combination
anoxic headspace
in HCl
immediate
increase
in a small, but significant
resulted
additions
P (Table 2). Oxalate
extractable
Fe
extractable Fe(II) and oxalate-extractable
increased in all treatments except the control and single dose
and NaOH-Pi
and pH increased in all treatments except the single dose
glucose addition,
this initial phase (day 3) HCl
additions
acetate and AQDS
(Table 2). After
to increase
Fe continued
extractable Fe (II), soil pH, and oxalate-extractable
with the pulsed C inputs, but did not show a similar pattern in controls or with
An
Table
2.
for ANOVAs
F-statistics
of changes
in Fe, P and pH pools
over
the first 3 days
of
the
anaerobic soil incubation.
Studied parameters
Treatment
Control
Acetate
Acetate-3T
Glucose
Glucose-3T
AQDS
AQDS + glucose
*p < 0.05;
**p < 0.01;
Pox
Feox
NaOH-Pi
HCl-Fe(II)
pH
3.83*
4.28*
3.39*
5.14*
9.58**
5.39*
4.02*
ns
3.39*
17.28***
ns
15.49***
3.45*
7.03**
ns
7.19**
9.48**
ns
9.27**
8.86**
4.23*
11.90***
34.42***
31.73***
3.61*
27.78***
13.94***
12.37***
8.67**
ns
8.23**
5.70**
8.06**
ns
10.86***
***p
< 0.001.
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73
single-dose C additions
(Figures 2 and 3). A short term increase in oxalate
Fe
the 6th and 10th day after a single acetate
extractable
occurred between
no
was
effect
of a single dose of glucose. Soil pH was
addition
and there
in the pulsed C
correlated
with
concentrations
strongly positively
Fe(II)
8000- (a)
^
*> 7000
.L 6000
0)
5000
4m 2000
x
-
I9 1000
2
0
4
6
8
10
12
14
-
7
(b)
6
2
0
|4--Control
Figure
2.
3T =
labile C added
Effect
4
-U-- Acetate
installments.
8
days
Acetate
on Fe(II)
of labile C source
in three
A
6
Harvest
3T---
10
14
12
Glucose -1-
Glucose 3T
production
(a) and pH (b). Acetate-3T
are means
i 1 standard deviation.
and glucose
Values
70
cm
on 60
u_ 50
40
30
x
9) 20
a)
0010
x
IS
2
0
-
Figure
3.
glucose-3T
Control
-
4
Acetate
I
I
I
6
8
10
- Acetate-3T
I
14
12
- Glucose
Effect of labile C source on the content
of oxalate-extractable
= labile C added in three installments.
+
are means
Values
)K Glucose-3T
Fe. Acetate-3T
1 standard
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deviation.
and
74
treatments (Table 3). In all the treatments, oxalate-extractable
Fe was
and positively
correlated with Fe(II)
(Figure 4). With
pulsed C
the relationship
approached
saturation near 2000 ,ug g-1 Fe(II) and
addition
strongly
additions
Table
was
3.
Relationship
pH and Fe(IJ)
between
at the 95%
determined
in experimental
production
treatments
Treatment
R2
Significance level
Equation
Control
Acetate
Acetate-3T
Glucose
Glucose-3T
AQDS
AQDS + glucose
0.32
0.18
0.83
0.14
0.83
0.10
0.48
0.001
0.05
0.001
0.05
0.001
ns
0.001
pH
pH
pH
pH
pH
pH
pH
ns
(significance
level).
=
=
=
=
=
=
=
3.96
4.48
4.53
4.15
4.25
4.14
4.13
+
+
+
+
+
+
+
0.0004Fe(II)
0.0002Fe(II)
0.0002Fe(II)
0.0002Fe(II)
0.0002Fe(II)
0.0002Fe(II)
0.0003Fe(II)
not significant.
Acetate
Control
25
20
y
15
10 -
0
O-
wb,
v
250
0
+
500
750
~
~
~
1250
y = 2.649eO002X
= 0.843
6-
Glucose
60 50 -40
1000
~
~
*40
y = 3.095e?002x
R2 = 0. 860
0
50
40 30
201
10
3.026e?o00'x
R2 = 0.656
* *
_
~~~~~~~~0?
0
250
500
1000 1250 1500 17-50 2000
750
Acetate
3T
60
50 -*
y =13.801lLn(x) - 70.699
20-30C)
LL
?)
,-)
201-
10
0
0
30-
20
22002.00
1000
5000
400
2
000
R=2
0
*
Glucose 3T
4000
6000
8000
10000
302
y = 2.319e0002x
AQDS
60
d 40
(
(U
X
o
20
-
y =17.309Ln(x) -90.882
=0.952
_
*0
0
50~~~~~~~~~~~~~3
60
0
2000
4000
*
6000
I
8000
20 F
r
0
30 0
500
1000
1500
AQDS+Glucose
60 50 40 30 20 -
2
R
=0010.814
*R=.1
10
0
Figure
1000
4.
2000
Relationships
3000
between
I
Fe(II) Production
(gig g-1)
4000
Fe(11)
production
and oxalate-extractable
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Fe.
2000
75
40 g kg-1 oxalate-extractable
Fe (Figure
4), while
in the control,
single C dose,
and AQDS treatments oxalate-extractable Fe increased linearly.
in the behavior of Fe oxides were reflected in the soil P fractions.
Changes
Fe
P followed
the same trend as oxalate-extractable
Oxalate-extractable
(Figure 5a) with the largest effect in the pulsed C treatments after the 3rd day
of soil incubation and little or no significant effect from a single dose of glucose
inorganic P fraction (NaOH-Pi) was only
or acetate. The alkaline-extractable
sensitive to the pulsed glucose additions (Figure 5b); this fraction is associated
P on amorphous
and some crystalline Al and Fe
with the strongly chemisorbed
phosphates (Tiessen et al. 1983).
The molar ratio of oxalate-extractable P:(oxalate-extractable Fe + oxalate
extractable Al) can be used as an index of the P saturation
(Psat) status of soils.
High values of Psat are indicative of a low P sorption capacity where P can be
released after dissolution of Fe oxides and resorbedunder oxidizing conditions
(Szilas et al. 1998). In this study, the Psat index range from 0.005 to 0.001.
Pulsed C additions quickly led to low values of Psat (after the 3rd day of soil
90
3'.880(a)
80
-
70
E
~60
(D
50
_
40
30
x
q20
? 10
45
0)30
E 25
20
40
Z
-
15
10
2
0
4
6
Harvest
4
Figure
5.
Acetate-3T
Effect
Control
of
T
Acetate
A
Acetate-3T
8
10
12
-0
Glucose
)K Glucose-3T
P (a) and
the labile C source on oxalate-extractable
= labile C added in three installments.
Values
and glucose-3T
14
days
alkali-extractable
are means
deviation.
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?
P (b).
1 standard
76
incubation),
while
in the other
experiment
(days
10 and 13).
treatments
Psat decreased
only at the end of the
The addition of AQDS alone did not produce significant changes in Fe(II),
or pH with
Fe,
oxalate-extractable
respect
to the control
(Figure
6a and b;
Table 3). Glucose + AQDS increased Fe(II) and oxalate-extractable Fe, but
did not result in a significant
7a and b).
Fe dissolution
NaOH-Pi
release of oxalate-extractable
P or
(Figure
Biodegradation of organicmatter
in
peaked during the 1st day of soil incubation
Both CO2 and CH4 production
rates of CO2
the 2nd day of soil incubation,
all treatments
(Figure 8). After
production decreased and stayed relatively constant throughout the rest of the
declined after the
production
(2 and 6 ,ug g dw-1 day-'). Methane
experiment
in the pulsed C
and then increased significantly
1st day in all treatments,
(Figure 8b). The increase was
treatments after the 6th day of soil incubation
Fluxes of CO2
than in the acetate additions.
greater in the glucose additions
3000
(a)
-
2500
E
2000
1500
_
-
_1000
x _500
00
2
0
50-
',
4
6
8
14
12
10
(b)
45 40
35
U-
-
30
=
25
20
*x 15
4) 1
x
(~5
lo
Q
0
2
6
4
8
12
10
14
Harvest days
|*
Figure
6.
extractable
Effect
Fe
of AQDS
(b). Values
Control
Glucose
-r-aAQDS
-A
AQDS+G
on HCl-extractable
+ glucose
and AQDS
+ 1 standard
deviation.
Fe
are means
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(a)
and
oxalate
77
and CH4 were negatively correlatedwith Fe(II) production in the control and
a single dose of labile C (Table 4).
following
Discussion
of added C and AQDS
Effects
on Fe and P dynamics
Humid tropical forest soils are often characterized by heterogeneous physio
chemical environments (Lodge et al. 1994),where the availability of soil oxygen
short temporal scales (hours to
to meters)
(Silver et al. 1999;
(02), C, and electron couples fluctuate over
days) and small spatial scales (centimeters
Pett-Ridge and Firestone 2005). Periodic depletion of soil 02 availability
coupled to high Fe content and inputs of labile C are likely to make to these
suitable sites for bacterial Fe(III) reduction, which can increase the
ecosystems
solubility of P associated with Fe oxides.
In this study, the decline in soil 02 availability
alone and in combination
led to Fe(III) reduction
with the addition of C or an electron shuttle compound
this initial period, pulsed C
during the first 3 days of soil incubation. After
inputs in combination with reducing conditions were necessary to increase
-
50
,
(a)
En
-
-40
30
= 20
a
o 10
0
x
0
e
-
c
2
4
6
8
2
4
6
8
10
12
14
(b)
~,40
E 30
20
Z
Cu
I
0
0
Harvest
-4-Control
Figure
7.
extractable
Effect
--Glucose
-ri-
10
12
14
days
AQDS
-i--
AQDS+G
+ glucose
on oxalate-extractable
of AQDS
and AQDS
+ 1 standard deviation.
are means
P (b). Values
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P
(a)
and
alkali
78
12
-(a)
10 -
x
0
2
0
0
4
2
4
6
8
10
14
12
(b)
c3
x
0
2
0
4
6
8
10
12
14
Harvest days
|
Figure
3T =
8.
Effect
Control
Acetate
of
C
labile C added
labile
in three
source
A
Acetate-3T
on CO2
installments.
EO Glucose
(a) and CH4
Values
are means
)K Glucose-3T|
(b) fluxes. Acetate-3T
+ 1 standard deviation.
and
glucose
rates of Fe(III) reduction. The production
of Fe(II) was positively
correlated
soil pH in most
treatments, due to the general tendency of proton con
reduction of Fe(III)
sumption during microbial
(Ponnamperuma
1972). The
lack of correlation between Fe(II) production
and pH in the AQDS
treatment,
in the control and single dose C additions
and the weak correlations
obtained
that Fe(III)
for organic
reduction was not a significant
suggests
pathway
matter
in those treatments. Our data also suggest
that C
decomposition
with
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79
Table
4.
Pearson
coefficient
correlation
between
C02,
CH4
flux and Fe(II)
production.
Treatment
CO2 flux vs. Fe(II) production
CH4 flux vs. Fe(II) production
Control
Acetate
Acetate-3T
Glucose
Glucose-3T
AQDS
AQDS + glucose
-0.71
- 0.70
ns
- 0.60
ns
-0.51
-0.42
-0.57
-0.63
ns
- 0.57
ns
-0.43
-0.59
ns =
not
significant.
availability
may
have
limited Fe(III)
rates in the control
reduction
and single
dose treatments.
We
can estimate
the potential
for C limitation
to Fe reduction
under natural
conditions using some simplifying assumptions. The amount of labileC added
to our soil is equivalent
to 0.06 Mg C ha-1 (using a bulk density of 0.64, Silver
et al. 1994), and 4.7 Mg C ha-1 y-1 assuming
three pulsed
inputs every
2 weeks. This amount
is similar to the standing stock of labile C reported in
McGroddy
and Silver (2000). In this a seasonal ecosystem, C inputs are dis
tributed throughout
the year; storm events and treefalls could increase C inputs
to the soil surface resulting in large pulses of labile C (Ostertag et al. 2003).
for this experiment
are comparable
to natural C
Thus, the pulsed C additions
inputs at the study site and suggest that Fe(III) reduction under natural soil
we speculate that dis
conditions
is not likely to be C-limited.
Furthermore,
turbance events that result in strong C pulses could result in significant P
release via Fe reduction if coupled with reducing conditions.
Bacterially generated Fe(II) undergoes secondary chemical reactions, which
lead to the precipitation of ferrous Fe solids as viavianite (Fe3(PO4)2.8H20)
et al. 1998; Zachara
et al. 1998; Dong
and siderite (FeCO3) (Fredrickson
et al. 2000). Both minerals
can be an effective sink for Fe(II)
(Dong et al.
in pH or the
either a decrease
2000). In this study we did not observed
formation of purplish-blue precipitate characteristic of vivianite formation. It
is possible that sideritewas formed, particularly given the high concentration
of CO2 during
Future
the later phases of the experiment.
studies should
of siderite formation and implications
for Fe and P
investigate the possibility
cycling.
In addition to the precipitation of Fe(II) minerals, ferrichydrous oxides can
also be reduced
to ferrous
hydroxide
gel complexes
(Ponnamperuma
et al.
1967). Freshly precipitated Fe(OH)2 would be in amorphous form (Shukla
et al. 1971) and have a greater
the original
ferric compound,
surface
area (Holford
potentially
resulting
and Patrick
in greater
1979) than
P sorption
capacity (Patrick and Khalid 1974;Willet and Higgings 1978; Holford and
Patrick 1979). As mentioned
above, oxalate extracts
tract poorly crystalline ferrous hydroxides
compounds
have been shown
such as Fe(OH)2.
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to ex
In this
80
study the observed increase in oxalate-extractable Fe as progressive Fe(III)
reduction
place with
took
C pulses
could
be ascribed
to the extraction
of
freshly precipitated Fe(OH)2 compounds. The relationship between Fe(II) and
oxalate-extractable Fe suggests that the formation of ferrous compounds from
the dissociated
Fe(II)
reached
a saturation
level in the treatments with pulsed C
inputs. This saturation state suggests that the production of Fe(II) surpasses
the precipitation of ferrous hydroxide complexes.
Pulsed
C
inputs
also
led
to an
increase
in oxalate-extractable
P with
increasing oxalate-extractable Fe, reaching high levels of extractable P by the
end of the experiment. This
labile C and Fe dissolution,
of P, associated with inputs of
high mobilization
in soil P fractions
in
supports observed patterns
this ecosystem (McGroddy and Silver 2000). Moderately
(NaOH-Pi),
and the light C fraction. Soil moisture
to
correlated
soil redox) and labile C availability
increase,
negatively
reduction is enhanced and P is released.
in humid tropical
from the reduction of Fe(III)
high P mobilization
and plant uptake. A
could result in an increase in soil P availability
et al. (2005) showed that the leaf litter P concentrations
study by Wood
positively
(often
Fe(III)
The
forests
recent
labile P fraction
is likely to include P that is sorbed on Fe and Al oxides, was
which
correlated
with
soil moisture
in tropical forestswere positively correlated with rainfall. The authors suggest
that this positive
relationship
could
be a response
to increased
P availability
associated with higher soil moisture.
to
that some of the P released via Fe reduction was re-adsorbed
Fe(OH)2
due to the large reactive surface area of these
precipitated
In this study pulsed C inputs accelerated
the reduction of Fe(III)
compounds.
of P, while at the same time
to ferrous compounds
and the mobilization
increasing the P sorption capacity of the soil evidenced by the decrease in the
P mobilization
increased over time, the rate of P
Psat index over time. Although
P was simultaneous
if some of the mobilized
release may be an underestimate
on Fe surfaces. Several authors have shown a decrease in water
re-adsorbed
on ferrous hydroxide
soils due to P re-adsorption
soluble P04 in anaerobic
gel
and Higgings
and
1978; Holford
1974; Willet
complexes
(Patrick and Khalid
P demand may
Patrick 1981; Phillips and Greenway
1998). Plant and microbial
if re-adsorption
is
compete with P re-adsorption,
particularly
effectively
It is possible
freshly
delayed
as suggested
Biodegradation
by our results.
of C coupled with Fe(III)
reduction
leads to
anoxic soil conditions
the final step of organic C mineralization
or to CO2 production
if
environments
of CH4 in methanogenic
the production
are available.
In this
electron
acceptors
Fe(III),
inorganic
S042-)
(NO3-,
C
utilization
of the easily metabolizable
study, we measured
rapid microbial
the progressive
solubi
substrates and resulting fluxes of CO2 and CH4. With
of CH4 and, to a lesser extent, that of CO2
lization of Fe(II), the production
Under
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81
was
inhibited
in the control
and single C dose
treatments.
This
inhibition
was
corroborated by the negative correlation between Fe(II) production and CO2
or CH4 flux. In the treatments with pulsed C inputs ferric iron reducers and
methanogenic
bacteria were able to utilize the fermentable C substrate,
thus
CH4 efflux increased after the second dose of acetate and glucose without
a
delay in Fe(II) production. Previous studies have shown that ferric iron
reducers can compete with methanogenic bacteria, causing the inhibition of
CH4 production (Lovley and Phillips 1986;Achtnich et al. 1995;Chidthaisong
and Conrad
2000).
Our
data
suggest
that at low
levels of available
C, Fe
reducers inhibitedCH4 production, but at higher levels of substrate availability
CH4 production did not compete with Fe reduction.
Conclusion
Our results suggests that in ferralitic soils characteristic of humid tropical
forests,
soil P availability
is strongly
coupled
to C and Fe cycles. Spontaneous
pulses of organic acids of lowmolecular weight, when coupled with periodic
reducing conditions, are a suitable source of energy to Fe-reducing bacteria.
Microbial
reduction
of Fe(III)
led to the release of P strongly
on the
sorbed
surfaces of Fe oxides. However, under periodic labile C inputs ferric hydrous
oxide can be reduced to ferrous hydroxide gel complexes. High concentrations
of
freshly precipitated
lead to an increase in the P sorption
Fe(OH)2 may
results from our study suggest that P solubilization
capacity,
although
ex
ceeded rates of re-adsorption.
P demand under
High plant and microbial
natural conditions
could also limit rates of P re-adsorption.
Our results high
light the importance of Fe(III) reduction as a potential
source of available P
under short-term anoxic conditions
in humid topical forest soils, and the role
of periodic C inputs to fuel the process in these highly productive
ecosystems.
Phosphorus
release via Fe reduction
is likely to provide an important
and
source of labile P in highly weathered
poorly documented
tropical soils and
may in turn contribute to the high NPP observed in these ecosystems.
Acknowledgements
This
research was financially
supported
by a grant from
toW.L. Silver, M.K. Firestone
and G. Sposito.
Foundation
the A.W.
Support
Mellon
was
also
provided by Grant No. BSR-8811902 from theNational Science Foundation
as part of the Long Term Ecological Research Program,
Institute of Tropical Forestry
in Puerto Rico, and was
and the International
done
under
the Cali
forniaAgricultural Experiment Station projects # 7069-MS (WLS).We would
like thank toAndy Thompson and Amy Silverberg for their technical support.
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82
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