Short communication

Implications of iron solubilization on soil phosphorus release in seasonally

flooded forests of the lower Orinoco River, Venezuela

Noemi Chacon *, Saul Flores, Ana Gonzalez

Centro de Ecologıa, Instituto Venezolano de Investigaciones Cientıficas, Apdo. 21827, Caracas 1020 A, Venezuela

Received 19 April 2005; received in revised form 7 October 2005; accepted 26 October 2005

Available online 4 January 2006

Abstract

The microbial reduction of Fe oxides is thought to contribute with the release of P in sedimentary environments. However, secondary reactions

of the bioproduced Fe(II) with P in solution, can lead to a decrease in the soluble P concentration. In this study, we examined how the reduction of

Fe(III) affects the soluble P concentration, when the soils of a seasonally flooded forest gradient are subjected to anaerobic conditions. Soil

samples were collected during the dry season from two zones subjected to different flooding intensity: MAX andMIN zones that were inundated 8

and 2 months per year, respectively. When anaerobic conditions were applied to soils from both zones, a clear stimulatory effect on the Fe(III)

reduction was observed. However, bioproduced Fe(II) underwent secondary chemical reactions, masking the extend of Fe(III) reduction of these

soils. Iron was reduced mainly during the first 15 days of the anaerobic incubation and it was stimulated by a pulse of labile carbon. Iron

dissolution did not lead to an increase of the soluble P content. However, in both zones P was high and positively correlated with Fe(II), implying

that soil P mobilization was linked to Fe dissolution. In the MIN zone, soluble P concentration decreased, probably as a consequence of the

secondary reactions of solubilized P with other non-redox sensitive soils elements. Fe solubilization also had an effect on the activity of acid

phosphatase and consequently in the solubilization of P from the organic pool. In conclusion, the P cycle in these soils is strongly coupled to C and

Fe cycles.

q 2005 Elsevier Ltd. All rights reserved.

Keywords: Anaerobic soils; Iron dissolution; Phosphorus mobilization

Extensive areas of river watersheds in the tropics are

covered with forests, some of which are seasonally flooded

(Kubitzky, 1989). These forests are characterized by annual

oscillations between aquatic and terrestrial phases (Junk et al.,

1989). The productivity of these forests in the humid tropics is

thought to be limited by the phosphorus (P) supply (Vitousek,

1984). Soils in this region are nearly depleted of primary

P-containing minerals and most of this element is found pre-

dominantely chemisorbed on amorphous minerals and some is

also found on crystalline iron (Fe) and aluminum (Al) oxides

(Lopez-Hernandez, 1977; Hsu, 1977; Schwertmann and

Taylor, 1977; Parfitt, 1978; Parfitt and Smart, 1978). For

these ecosystems, soil P mobilization has been associated with

the biogeochemistry of Fe (Gambrel and Patrick, 1978;

Baldwin and Mitchell, 2000; Chacon et al., 2005a).

Water in soil restricts gas diffusion and limits the oxygen

availability in soil (Smith and Tiedje, 1979), with a consequent

0038-0717/$ - see front matter q 2005 Elsevier Ltd. All rights reserved.

doi:10.1016/j.soilbio.2005.10.018

* Corresponding author. Tel.: C58 212 5041415; fax: C58 212 5041088.

E-mail address: nchacon@oikos.ivic.ve (N. Chacon).

decrease in the soil redox potential (Gambrel and Patrick,

1978). Under such circumstances, microbial dissolution of

Fe(III) oxides can take place (Lovley et al., 1991; Baldwin

et al., 1997; Baldwin and Mitchell, 2000) and the phosphate

anion chemically sorbed to these iron oxides surfaces can be

released (Baldwin and Mitchell, 2000). Indeed, several studies

have found that P concentration increases when soils become

waterlogged (Moore et al., 1992; Szilas et al., 1998; Ferrando

et al., 2002). However, Fe(II) produced by the reduction of

Fe(III) oxides may undergo chemical transformations, affect-

ing the concentration of P in solution. For example, ferric

hydrous oxides can be reduced to amorphous ferrous hydroxide

gel complexes (Fe(OH)2) (Ponnamperuma et al., 1967), with a

greater surface area than the original ferric compound (Holford

and Patrick, 1979). This results in an increase in P sorption

capacity (Patrick and Khalid, 1974; Willet and Higgins, 1978;

Holford and Patrick, 1979; Phillips and Greenway, 1998).

Phosphorus concentration may also decrease during flooding

due to the precipitation of ferrous phosphate (vivianite,

Fe3(PO4)2$8H2O) (Zachara et al., 1998).

In a previous study, along a flooded gradient, Chacon et al.

(2005a) found that both labile and moderately labile soil P

Soil Biology & Biochemistry 38 (2006) 1494–1499

www.elsevier.com/locate/soilbio

Fig. 1. Fe(II) production (a) and soluble P concentration (b) in the acidified

extract. Mean valuesGSD. MAX, maximum flooding zone; MIN, minimum

flooding zone. Lowercase letters denote significant differences over time within

a zone (P!0.05).

N. Chacon et al. / Soil Biology & Biochemistry 38 (2006) 1494–1499 1495

concentrations were strongly associated with the amount of

crystalline Fe oxides, when the soils were under aerobic

condition. Based on this previous study, we hypothesized that

any change occurring in the behavior of Fe oxides during the

anoxic period, may affect the size of the labile P pool.

Therefore, in this study, we examined how the reduction of

Fe(III) affects the soluble P concentration when seasonally

flooded tropical soils are subjected to anaerobic conditions.

The soil samples were collected from the floodplain of the

Mapire River located in south-east Venezuela, between 78

30 0–88 30 0N and 648 30 0–658 00 0W. This river is a northern

tributary of the lower Orinoco River, and its basin constitutes

a region of low relief covered by the Pleistocene Mesa

Formation (Carbon and Schubert, 1994). The Mapire river

has been classified as a black-water river due to its brown

color and its oligotrophic character in terms of nutrient,

sediment load and primary productivity (Vegas-Vilarrubia,

1988). According to the climatic diagram of the region

(Vegas-Vilarrubia and Herrera, 1993), the annual mean

temperature is 27.4 8C and the annual precipitation averages

1333 mm, with the dry season between November and April

and the rainy season from May to October. Forests

communities of the Mapire river are related to longitudinal

and perpendicular gradients of flooding depth and duration,

which are associated with local topography.

Soil samples were collected from two zones of a flooded

gradient perpendicular to the course of the Mapire River: a low

zone close to the river margin where the flood reaches a

maximum of 12 m and lasts up to 8 months (from May to

December) (MAX zone), and a high zone where the flood

reaches a maximum of 1 m for 2 months (from July to

September) (MIN zone). In each zone, the surface mineral

horizon (0–10 cm) was sampled in six points arranged into

three transects with two sampling points in each one. A total of

six samples per zone were taken with an auger during the dry

season (March 2003). The soil samples were air-dried and

passed through a 2-mm sieve.

From each soil sample, four subsamples were taken for

the incubation experiment (nZ24 per zone). Dry soil was

placed in glass jars of 500 mL and a slurry was prepared,

using a 2.5:1 water/soil ratio. Anoxic condition was created

using 100% N2. Soil samples were then incubated at 25 8C

for a period of 2 months. In order to ensure anaerobic

conditions, the jars were flushed with N2 gas every 2 days.

At selected times (i.e. 0, 15, 30 and 60 days), six replicate

samples from each zone were analyzed for pH, HCl-

extractable-Fe (HCl–Fe(II)) and associated inorganic P

(HCl–Pi), soil organic carbon (SOC), and acid phosphatase

activity (APA). pH was measured in a soil–water mixture at

a 1:2.5 soil:water ratio. Acid-extractable Fe(II) was obtained

using 0.5 N HCl (Fredrickson et al., 1998) and was

considered a measure of the total extent of reduction (Fe2C

production). Iron content was determined by absorption

atomic spectroscopy and it was assumed that all was ferrous

iron. Inorganic P concentration in the acidified extract was

determined using the colorimetric method of Murphy and

Riley (1962) after adjusting to pH 4 using p-nitrophenol.

Soil organic carbon was obtained using the Walkley and

Black (1934) wet oxidation method. The acid phosphatase

activity (APA) was determined using p-nitrophenylphosphate

(p-NPP) as substrate at a temperature of 37 8C (Tabatabai

and Bremner, 1969).

Statistical analysis of the data was carried out by a one-way

ANOVA. Data were log-transformed when necessary to meet

the assumptions for ANOVA. A Tukey honestly significant

difference (HSD) test was used when statistical differences

(P!0.05) were observed. A Kruskal–Wallis non-parametric

test was used on data that did not meet assumptions for

ANOVA. The relationship between HCl-extractable Fe(II) and

inorganic P was analyzed using simple linear regressions and

tested for significance at the 5% level. All statistics were

computed using STATISTICA for Windows 6.0 (Statistical,

2001).

In the studied soils, the anaerobic condition lead to a

decrease in the content of Fe(II), particularly after 15 days of

soil incubation, but the decrease was significant only in the

soils of the MAX zone (Fig. 1a). Along the incubation period,

soil pH increased in both zones, but the increase was slow in

the soil of the MAX zone (Table 1). During the first 4 weeks of

anaerobic incubation a putrefying odor was present in the soils

of the MAX zone. However, at the end of the experiment (day

60), the odor disappeared and the soil pH increased

significantly respect to the soil initial condition (Table 1). In

the soils of the MIN zone the odor was not present, but a green–

blue precipitate, in colloid form, was observed in the early

stage of the experiment. This colloid disappeared at the end of

the experiment. Soils of the MAX zone did not show

precipitate during the incubation period.

In sedimentary environments, two non-enzymatic

mechanisms have been postulated for Fe(III) reduction.

Table 1

Soil properties in two zones of the flooded forest gradient

Soil property Zone Days

0 15 30 60

pH MAX 4.32G0.08a 4.15G0.27a 4.37G0.37ab 4.83G0.36b

MIN 4.43G0.10a 4.83G0.39b 5.38G0.35c 5.64G0.06c

SOC (%) MAX 2.38G0.52b 3.40G0.37c 1.52G0.41a 1.63G0.17a

MIN 1.32G0.21b 2.28G0.29c 1.02G0.10a 0.82G0.14a

APA (mg p-NP gK1 hK1) MAX 32G34a 114G75ab 202G74bc 224G60c

MIN 94G41a 127G70ab 65G12a 173G39b

MAX, maximum flooding zone; MIN, minimum flooding zone; SOC, soil organic carbon; APA, acid phosphatase activity. Day 0 refers to initial condition of soil and

days 15–60 refer to amount of time of anaerobic incubation. Mean valuesGSD followed by the same letter in each line are not different at PO0.05.

N. Chacon et al. / Soil Biology & Biochemistry 38 (2006) 1494–14991496

Sulphate-reducing bacteria (SRB) use sulphate (SO2K4 ) as

an electron acceptor to produce hydrogen sulphide (H2S),

which can reduce iron oxyhydroxides to form insoluble iron

sulphides (FeS) (Ponnamperuma, 1972; Coleman et al., 1993;

Baldwin and Mitchell, 2000; Lovley, 2000). Fe(III)-respiring

microorganisms (FRM) is the another possible mechanism

for non-enzymatic Fe(III) reduction (Lovley, 2000). FRM

use directly Fe(III) oxides and oxyhydroxides as the

terminal electron acceptor (Baldwin and Mitchell, 2000;

Lovley, 2000).

In this study, the increase in the soil pH during the

incubation, suggest that Fe(III) reduction took place, because

the microbial reduction of Fe(III) is proton-consumption

process (Ponnamperuma, 1972; Szilas et al., 1998; Chacon

et al., in press). However, Fe(III) reduction in the soils of the

MAX zone followed a mechanism different from that of the

soils of the MIN zone. In the MAX zone, the temporal

decrease in the Fe(II) content accompanied by the strong

odor until the 30 days of soil incubation, suggest that Fe(III)

was reduced by hydrogen sulphide with the consequent

precipitation of the insoluble FeS. The sudden disappearance

of the strong odor of these soils, at the 60 days of soil

incubation, also suggest that soil bacterial community

changed in this stage of the experiment. Future studies

should investigate the implications of such bacterial changes

on the Fe cycle.

Under anaerobic soil condition biogenerated Fe(II) can

experience secondary chemical reactions, which lead to the

formation of aqueous complexes and/or the precipitation of

ferrous solids as iron sulphide (FeS), magnetite (Fe3O4),

vivianite (Fe3(PO4)2$8H2O), siderite (FeCO3) and green

rusts compounds ½FeIIð1KxÞFeIIIx ðOHÞ2�

xC½ðx=nÞAnKðm=nÞH2O�xK

(Ponnamperuma, 1972; Coleman et al., 1993; Fredrickson

et al., 1998; Zachara et al., 1998; Dong et al., 2000; Lovley,

2000; Baldwin and Mitchell, 2000). Some of these ferrous

minerals have been considered an effective sink for the

bioproduced Fe(II) (Coleman et al., 1993; Dong et al., 2000;

Fredrickson et al., 1998). It is know that the precipitation of

FeS remove high amounts of Fe(II) from anoxic lakes and

muds (Ponnamperuma, 1972).

Due to the fact that soil pH increased quickly in the MIN

zone and no odor was detected, it is likely that in these soils,

Fe(III) was reduced via FRM. From our results we cannot

explain the differences observed in the microbial community

between MAX and MIN zone. However, we suggest that such

differences may be the result of the long of the flood period,

which are subjected these soils in the field.

In the MIN zone, it is probably that secondary chemical

reactions are masking the extent of the Fe reduction. In these

soils we observed the precipitation of a green–blue colloid in

the early stage of the experiment. This suggests that anaerobic

soil condition lead to the Fe(III) reduction in these soils,

however, the bioproduced Fe(II) was probably precipitated as a

biogenic mineral. The precipitation of the ferrous mineral did

not lead to a significant decrease in the Fe(II) content in these

soils, as was observed in the soils of the MAX zone, because

Fe(II) associate to minerals as, siderite, vivianite and green-

rusts compounds, can be extracted in 0.5 N HCl (Fredrickson

et al., 1998). Green-rusts compounds are among the biogenic

minerals that could be precipitating in these soils, because

green–blue color in hydromorphic soils has been frequently

associated with this type of compounds (Trolard et al., 1997).

Green rusts are intermediate compounds between ferrous

hydroxide and ferric oxyhydroxide (Benali et al., 2001). In the

MIN zone, when the soils are exposed to the air, just at the end

of the aquatic phase, dispersed spots of a blue–green color are

observed in the soil.

In both zones, the iron reduction and ferrous iron

precipitation was accompained by a pulse of organic carbon

at the first 15 days of the anaerobic incubation. Later, little

changes in the Fe(II) content was observed, while the

concentration of soil organic carbon (SOC) decreased

(Fig. 1a and Table 1). Rewetting of the dry soil may induce

the mycrobial cell lysis, with the consequent increase in the

microbial-C pool (Kieft et al., 1987; Fierer and Schimel, 2003).

Rewetting process also releases physically protected soil

organic matter, increasing the amount of extractable SOM-C

(Fierer and Schimel, 2003). Both biomass C and non-biomass

SOM-C, contribute with the increase of the labile C pool in

rewetting soil (Fierer and Schimel, 2003). Our studied soils

were previously air-dried and then incubated under anaerobic

condition as a slurry. In this study, the observed increase in the

SOC concentration at the 15 days of soil incubation, could be

then ascribed to the pulse of labile C induced by the rewetting

of the soil. Iron reduction is fueled by the availability of labile

organic carbon, because the biodegradation of labile organic

N. Chacon et al. / Soil Biology & Biochemistry 38 (2006) 1494–1499 1497

matter leads to the production of electrons which can be

microbially transfered to the Fe(III), an important electron

acceptor under anaerobic soil conditions (Lovley and Phillips,

1986; Quantin et al., 2001; 2002; Stemmler and Berthelin,

2003; Chacon et al., in press). The depletion of organic C in the

later stages of the experiment (30–60 days), suggest that Fe(III)

reduction was limited by the supply of labile organic C in this

stage of the experiment.

It has been reported that in waterlogged soils, the

microbial reduction of Fe(III) is greatly stimulated by

organic matter inputs. In natural areas oscillating between

terrestrial and aquatic phases, the microbial reduction of

Fe(III) will primarily be carried out during the initial period

of soil anoxia because pulses of labile C are available during

the aquatic phase as a result of both the leaching of the

accumulated litter during the terrestrial phase and by the

pulse of labile C induced by the rewetting of the soils (Kieft

et al., 1987; Junk, 1997; O‘Connell et al., 2000; Fierer and

Schimel, 2003).

During the first 15 days of anaerobic incubation, the content

of soluble P declined respect to the initial levels in the soils of

the MIN zone, but there was no significant changes in the

content of P in the soils of the MAX zone (Fig. 1b). In both

zones, P content was high and positively correlated with Fe(II)

content (MAX: r2Z0.53, P!0.0001; MIN: r2Z0.41,

P!0.0001). A recent study by Chacon et al. (2005a) suggests

that the microbial reduction of Fe(III) is an important

mechanism for P release in soils subjected to long flooding

periods. Although, we cannot corroborate this hypothesis with

the available data from this study, the positive relationship

between both Fe(II) and P content allow us to suggests that the

P mobilization in the studied soils is linked to Fe(II)

dissolution. However, under anaerobic soil condition Fe and

P undergo secondary chemical reactions that could be

preventing to observe a significant increase in the content of

both elements.

The sharp decrease in the P content in the soils of the MIN

zone could be ascribed to secondary reactions of P with other

non-redox sensitive soil components. In oxidized soil samples

of the MIN zone, Chacon et al. (2005a) reported high contents

of humic–Al-complexes (174.01G19.01 mmol kgK1)

compared to the soils of the MAX zone (99.65G35.36 mmol kgK1). Aluminum is a non-redox sensitive

element and the organo-mineral–Al complexes are considered

active surfaces that control the soil’s sorption capacity (Gerke

and Jungk, 1991; Darke and Walbridge, 2000; Chacon and

Dezzeo, 2004).

Acid phosphatase activity (APA) increased gradually in

the soils of the MAX zone (Table 1). However, in the soils

of the MIN zone, APA showed no significant changes during

the first 30 days of soil incubation, but it increased

significantly at the end of the experiment (Table 1). The

differences in the APA behavior could be explained through

the interaction of this enzyme with various soil components.

According to Chacon et al. (2005b), during the non-flooded

phase, acid phosphatase seems to be adsorbed by minerals of

the fine fraction of the soils (clayCsilt) in the MAX zone

and by organo-mineral–Al–complexes in the MIN zone. As

was previously disscussed, organo-mineral–Al-complexes are

not sensitive to the changes in the soil redox condition.

Therefore, it is logical that APA in the soil of the MIN zone

did not respond to the anaerobic soil condition. The gradual

increases of the enzyme activity as the Fe dissolution took

place in the MAX soils, suggests that probably immobilized

enzyme is being released during the Fe(III) reduction. It has

been reported that the activity of acid phosphatase in solution

is much higher than the activity of the immobilized enzyme

(Rao et al., 1996; Shindo et al., 2002). Even though a net

change in the P content was not observed in the soils of the

MAX zone, it is clear that the increase in the enzimatic

activity, can lead to the transference of P from the organic

pool to the soil solution.

Our findings showed that anaerobic condition coupled with

inputs of labile carbon stimulate iron reduction in the studied

soils. We propose that two different mechanisms are involved

in Fe(III) reduction: in the MAX zone, Fe is indirectly reduced

by the activity of sulphate-reducing bacteria, through the

production of sulphide, while in the MIN zone, Fe is reduced

directly by Fe(III)-respiring microorganisms. Under anoxic

soil condition P mobilization was linked to the Fe dissolution.

However, both biogenerated Fe(II) and the released P,

underwent secondary chemical reactions, which could be

masking the extend of iron reduction and consequently the

transference of P from this pool to the soil solution. Fe

solubilization seems to have a significant effect on the activity

of the immobilized acid phosphatase and consequently in the

solubilization of P from the organic pool. The results in this

study allowed us to suggest a number of hypotheses concerning

the mechanisms that regulate the iron dissolution and

phosphorus release in seasonal flooded forests. However,

future investigations should include long-term studies in the

field in combination with simulations in the laboratory that

allow to understand, the composition and activity of the soil

microbial community, linked to the geochemical

transformations.

Acknowledgements

The authors thank two anonymous reviewers who provided

helpful comments on this manuscript.

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