Journal of Soils and Sediments

https://doi.org/10.1007/s11368-018-2051-y

SEDIMENTS, SEC 4 • SEDIMENT-ECOLOGY INTERACTIONS • RESEARCH ARTICLE

The role of reactive iron in long-term carbon sequestration in mangrove

sediments
Gerald P. Dicen 1,2 & Ian A. Navarrete 1 & Roland V. Rallos 2 & Severino G. Salmo III 1 & Maria Carmela A. Garcia 1

Received: 28 March 2018 / Accepted: 3 June 2018

# Springer-Verlag GmbH Germany, part of Springer Nature 2018

Abstract
Purpose Despite occupying only 0.5% of the global coastal ocean, mangroves play a disproportionately large role in the capture
and retention of atmospheric carbon dioxide as organic carbon (OC) in its sediments. However, the capacity of mangrove
sediments to store high amounts of OC has never been explained mechanistically. This study elucidates the role of reactive iron
(FeR) in long-term carbon sequestration in mangrove sediments.
Materials and methods Sediment samples of up to 1 m in depth were collected from six selected mangrove areas across the
Philippines. The samples were characterized using X-ray diffraction (XRD) and X-ray fluorescence (XRF). A citrate-
bicarbonate-dithionite reduction procedure was employed to extract FeR from the sediments. The OC concentration and δ13C
signatures before and after FeR extraction were determined using a dichromate oxidation technique and isotope ratio mass
spectrometry (IRMS), respectively.
Results and discussion XRD diffractograms showed that the mangrove sediment samples varied in terms of mineralogical
characteristics, which reflected their different parent materials. It was found that the OC concentration increased exponentially
(OC = 8.38e0.37FeR; R2 = 0.88; p < 0.0001) with increasing FeR concentration. δ13C signatures of FeR-associated OC revealed that
FeR preferentially preserved terrestrial over marine-derived organic matter. Finally, FeR was estimated to coprecipitate with up to
5.44 × 1012 g OC in mangrove sediments per year.
Conclusions The findings of this study suggest that FeR is responsible for the preservation of OC, thus making mangrove
sediments a Bgiant rusty sponge^ for carbon. This mechanistic understanding of the long-term carbon storage in mangrove
sediments could help draft better strategies for blue carbon initiatives that include the mangrove ecosystems.

Keywords Carbon sequestration . Mangrove sediments . Organic matter preservation . Reactive iron . Stable isotope

1 Introduction economic and ecological services. These ecosystems function

Mangrove ecosystems are one of the most important ecosys-
tems along continental margins that provide valuable
Responsible editor: Haihan Zhang
Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s11368-018-2051-y) contains supplementary
material, which is available to authorized users.
* Ian A. Navarrete
inavarrete@ateneo.edu
1
Department of Environmental Science, School of Science and
Engineering, Ateneo de Manila University, Loyola Heights,
1108 Quezon City, Philippines
2
Agriculture Research Section, Atomic Research Division, Philippine
Nuclear Research Institute, Diliman, Quezon City 1101, Philippines
as nursery grounds and food source for both terrestrial and
aquatic fauna, support livelihoods, and provide protection to
coastal areas against disasters caused by typhoons, hurricanes,
and tsunamis. As true ecotones, mangrove forests have ele-
ments of terrestrial and marine habitats as well as ecological
characteristics that are unique (Alongi 2009). These forests are
unique not only in ecology but also in biogeochemistry, being
perpetually affected by animal activities, floods, and tides,
which fluctuate daily (Ovalle et al. 1990; Alongi 2009).
Among tropical wetlands, mangrove forests have the highest
carbon stock (Phang et al. 2015), and 49–98% of this carbon
stock is stored in their sediments (Donato et al. 2011). Despite
occupying only 0.5% of the global coastal ocean, mangrove
forests contribute 14% to the global carbon burial (Duarte et
al. 2005). This is in part due to the high net primary produc-
tivity of mangroves, which is comparable to that of tropical

rainforests. Their structure and location in depositional areas
also make them effective traps of organic matter inputs from
the terrestrial and marine environments. Mangrove ecosys-
tems are efficient carbon sinks due to their high capacity for
long-term carbon sequestration through the burial of OC in
sediments. However, the mechanisms of the burial of OC in
mangrove sediments remain poorly understood and thus re-
main elusive (Alongi 2014).
Over 90% of organic matter in sediments cannot be phys-
ically separated from its mineral matrix (Hedges and Keil
1995). This mineral matrix is composed of silicate minerals
and metal oxides such as iron oxides, which are related to the
persistence of organic matter in sediments (Lalonde et al.
2012). Organic matter and iron oxides have been demonstrat-
ed to have a unique interaction. On the one hand, organic
matter inhibits the crystallization of iron oxides and deter-
mines the nature and properties of iron oxides to be formed
(Schwertmann 1966; Chen et al. 2015), while synthetically
prepared iron-bound organic matter was shown to resist deg-
radation (e.g., Boudot et al. 1989). These interactions have
long been documented in soils. Although only recently ex-
plored in sediments (Lalonde et al. 2012; Riedel et al. 2013;
Shields et al. 2016), these previously observed interactions
hold clues to the fate of carbon in mangrove sediments. In
marine sediments, the concentrations of iron and carbon were
found to covary (Berner 1970). However, whether this rela-
tionship was caused by either each element having high affin-
ity for the same particle surfaces or if they were directly asso-
ciated is unknown (Lalonde et al. 2012). Recent synchrotron-
based techniques have shown that organic matter is directly
bound to FeR through inner-sphere covalent interactions
(Barber et al. 2017). FeR is defined as the fraction of iron in
marine sediments which readily reacts with dissolved sulfide
to form various iron sulfide minerals (Canfield 1989) and
exists as ferrihydrite, goethite, or lepidocrocite nanophases
(van der Zee et al. 2003). FeR-bound organic matter acquires
marked stability and prolonged resistance to microbial attack
(e.g., Barber et al. 2014), resulting in the preservation of OC
over long periods of time because FeR is metastable over geo-
logical timescales.
Mangrove forests are considered indispensable in climate
regulation because they sequester significant amounts of car-
bon to help counterbalance anthropogenic carbon emissions
(McLeod et al. 2011; Siikamaki et al. 2012). For this reason,
mangrove restoration and rehabilitation is included in climate
change mitigation strategies such as Reducing Emissions from
Deforestation and Forest Degradation in Developing
Countries (REDD+; Friess 2013; IPCC 2007) and voluntary
carbon markets (Ullman et al. 2013; Locatelli et al. 2014).
However, the stability of mangrove OC stock has not been
included in REDD+ initiatives (Donato et al. 2011; Ajonina
et al. 2014) nor is the influence of its mineral environment
explicitly incorporated in carbon models (Lehmann and
J Soils Sediments
Kleber 2015; Keil 2017). This study was conducted to under-
stand the role of FeR on the preservation of organic matter in
mangrove sediments. The aim of the study is to (1) analyze the
relationship between FeR and OC in mangrove sediments; (2)
quantify the amount of OC that is directly bound to FeR; and
(3) determine if there is preferential binding between OC and
FeR.
2 Materials and methods
2.1 Site description
Six mangrove areas across the Philippines were selected for
this study (Fig. 1). These included mangrove areas in
Zambales (Masinloc and Subic), Palawan (Bogtong and
Calauit in Busuanga), and Cebu (Kodia and Oboob in
Bantayan Island). The sampling sites in Zambales are natural
mangrove forests dominated by Avicennia marina, Sonneratia
alba, Rhizophora mucronata, and R. stylosa. These mangrove
forests are located within marine protected areas facing the
West Philippine Sea and comanaged by local government
units and indigenous people. The sampling sites in Palawan
are also natural mangrove forests dominated by R. apiculata
and R. stylosa that are more than 50 years old. The sampling
sites in Bantayan Island, Cebu, are a mix of natural (Kodia)
and planted (Oboob) R. mucronata, R. stylosa, A. marina, and
S. alba mangrove species.
2.2 Sample collection and characterization
A sediment corer (100 cm length and 6.5 cm diameter) was
used to obtain the samples. Sampling was done at day time
during low tide. One-meter sediment core samples were col-
lected from the mangrove areas in Zambales and Palawan,
while the mangrove areas from Bantayan Island, Cebu, which
had a shallow sediment layer due to the absence of sediment-
carrying tributaries, were sampled up to the maximum depths
of 40 cm for Oboob and 75 cm for Kodia. Sediment core
samples were divided into six subsamples (0–5 cm, 5–
10 cm, 10–20 cm, 20–40 cm, 40–60 cm, 60–100 cm) and
were then stored in zip plastic bags with core ID labels and
kept at −4 °C within 24 h of sampling. Roots, stones, shells,
and any visibly large particles were also removed from the
samples. The samples were air-dried, pulverized using a mor-
tar and pestle, and sieved through a 0.5 mm sieve.
X-ray diffraction (XRD) analysis was performed on pow-
dered samples (~ 10 μm) mounted on a XRD holder to max-
imize the intensity of signals from all crystalline faces. The
samples were subjected to a full-scan XRD analysis set at 3.0°
to 40° 2θ angle. X-ray beams were generated from a Cu Kα
radiation source (40 kV; 30 mA) with wavelength of 1.54 Å.
The resolution for the analysis was set at 0.02°, with scan
J Soils Sediments
118°0’0” 119°0’0” 120°0’0” 121°0’0”
15°0’0”
14°0’0”
13°0’0”
12°0’0”
Masinloc
Subic
11°0’0”
Bogtong
Calauit
Kodia
Oboob
Fig. 1 Sampling locations across the Philippines
speed maintained at 2° per minute. Mineralogy was evaluated
and checked manually using the PDF-4+ database of the
International Centre for Diffraction Data (ICDD), Mineral
Database (Materials Data Inc., 1988–2004) and RRUFF™
Project. To provide reference for mineral identification, total
elemental composition of sediment samples was analyzed
using a Horiba XGT-7200 micro-XRF analyzer. About 1.0 g
of each sample was mounted into a sample holder, and tripli-
cate samples were analyzed and the mean values were report-
ed (Navarrete et al. 2017).
2.3 FeR and OC analyses
The OC concentration in the mangrove sediment samples was
determined using a dichromate oxidation technique (Tinsley
1950). The δ13C values for all samples were determined using
an isotope mass ratio spectrometer (IRMS). Prior to analysis,
the samples were decarbonated by acidification (Kennedy et
al. 2005; Brodie et al. 2011) to remove inorganic carbon that
will otherwise have a confounding influence on the δ13C
122°0’0” 123°0’0”
N
Km
0 40 80 160
signature. About 7.5 mg of oven-dried samples was weighed
into open silver capsules and placed in the wells of a microtiter
plate. Repeated additions of 30 μL of 2 M HCl were done,
with oven-drying at 60 °C in between additions. The proce-
dure was repeated until no visual evidence of effervescence
was observed, and the capsules were further dried before they
were crimped. δ13C was measured using a Sercon 20-22 con-
tinuous flow IRMS following combustion at 1000 °C in
Sercon GSL elemental analyzer (Sercon Limited, UK).
Results of 13C isotope analysis were reported in delta notation
(δ) as per mil (‰) relative to international standards of Pee
Dee Belemnite (13C/12C, PDB). Analytical precision of mea-
surement was higher than 0.2‰.
Following the determination of OC concentration and δ13C
signatures, FeR was extracted from mangrove sediment sam-
ples using a modified citrate-bicarbonate-dithionite extraction
procedure (Mehra and Jackson 1958). This procedure is
known to extract reactive phases of iron while being gentle
with clay minerals (Lalonde et al. 2012). About 0.25 g of dry
sediment samples was weighed into 50-mL centrifuge tubes,

and approximately 15 mL solution containing a buffer
(NaHCO 3 , pH 7.3) and a metal ion complexing agent
(Na3C6H5O7·2H2O) were added. The centrifuge tubes were
then heated to 80 °C in a water bath, and a reducing agent
(0.25 g Na2S2O4) was added to the mixture, which was then
maintained at 80 °C for 15 min. Following the treatment, the
supernatant was separated from the solid fraction by centrifu-
gation at 3000g for 10 min. The solid fraction was rinsed three
times with artificial seawater to ensure that bicarbonate and
citrate did not contaminate the samples with adventitious OC.
The rinse water and supernatant were combined, acidified,
filtered, and diluted 10 times. Finally, the concentration of
FeR in the solutions was analyzed by an atomic absorption
spectrophotometer (Shimadzu AA-6300, Tokyo, Japan).
The percentage of OC bound to FeR in mangrove sedi-
ments and its δ13C signature were obtained by reanalyzing
the residue from the extraction procedure using a dichromate
oxidation technique and IRMS, as described above. To pre-
vent overestimation of the amount of OC bound to FeR, con-
trol experiments were also conducted for all samples, simul-
taneously. Control samples were extracted under the same
conditions as the reduction method but with the replacement
of Na3C6H5O7·2H2O and Na2S2O4 with NaCl at an equivalent
ionic strength because it had been observed that heating can
cause a significant amount of OC to be extracted from the
samples (Lalonde et al. 2012). This was done since the control
did not have Na2S2O4 the active ingredient in extracting FeR
to correct for the FeR and OC that might be extracted.
2.4 Statistical analyses
Statistical analyses were carried out using a JMP (version 11;
SAS Institute, Cary, NC, USA) software package. Analysis of
variance (ANOVA) was used to determine if there are signif-
icant differences in the measured parameters across sites.
Tukey’s honest significant difference (HSD) test was used to
determine which among the mangrove areas were significant-
ly different. Regression analysis was done to determine the
predictive relationship between FeR and OC concentrations.
The level of significance was set at p < 0.05 for all statistical
analyses.
3 Results
3.1 Sediment characteristics
The XRD diffractograms (see Electronic Supplementary
Material, Fig. S1) of bulk samples from Masinloc and Subic
have very pronounced peaks of plagioclase feldspar (3.18 and
6.41 nm) and amphibole (8.45 nm). The XRD diffractograms
of mangrove sediments from Subic revealed the presence of
halloysite (7.20 nm), whereas in sediment samples from
J Soils Sediments
Oboob and Kodia were dominated with aragonite (2.37 nm)
and calcite (3.03 nm). While peaks of amphibole and feldspar
were observed in the XRD diffractograms of sediments from
Kodia, quartz peaks (3.34 nm) are dominant. Quartz (4.26 and
3.34 nm) and illite (2.54 nm) were dominant in mangrove
sediments collected from Bogtong and Calauit, with quartz
being the most pronounced peak.
3.2 OC concentration and δ13C signature
The bulk OC concentration in mangrove sediments generally
increased from surface to bottom (Fig. 2a). Across sites, Kodia
had the highest OC concentration (81 ± 20 g kg−1), while
Subic and Oboob had the lowest (11 ± 4 and 12 ± 2 g kg−1,
respectively) (Table 1). The δ13C signatures obtained from the
surface sediments generally varied (Fig. 2c), with values rang-
ing from − 24.2 to − 30.1‰. However, the variation in δ13C
values diminished as depth increased, with five of the man-
grove areas (i.e., Bogtong, Calauit, Kodia, Masinloc, and
Subic) approaching the terrestrial δ13C signature of approxi-
mately − 27‰.
3.3 FeR concentration
The concentration of FeR generally increased from the surface
sediments down to the bottom (Fig. 2b). Of the six sampling
sites, Oboob had the lowest Fe R concentration (0.5 ±
0.1 g kg−1), while Subic had the highest (10 ± 3 g kg−1).
Subic and Oboob represent the highest and the lowest FeR
concentrations, respectively, but both have the lowest OC con-
centrations among all sites (Table 1).
3.4 FeR-associated OC concentration and δ13C
signature
Analyses of OC concentrations between bulk mangrove sed-
iment samples and post-FeR extraction samples quantified the
amount of OC that is lost upon the removal of FeR from the
sediments, or the amount of OC that is directly bound to FeR.
The percentage of OC bound to FeR was highest in the man-
grove sediments from Masinloc (25 ± 9%) and lowest in
Kodia (10 ± 2%) (Table 1). On average, it was estimated that
15 ± 7% of OC in the sediments from six mangrove areas is
directly bound to FeR. The δ13C signatures between the bulk
OC (− 27.6 ± 1.7‰) and FeR-associated OC (− 27.3 ± 2.3‰)
in mangrove sediments did not have any significant difference
(p > 0.05). The downcore profile of δ13C signatures of FeR-
associated OC (Fig. 2d) shows that in the surface sediments,
the δ13C signatures of organic matter sorbed onto FeR signif-
icantly varied (p < 0.05).
J Soils Sediments

a OC Concentraon (g kg-1)
b FeR Concentraon (g kg-1)
0 30 60 90 120 0 5 10 15
Legend:
-5 -5 Bogtong
Calauit
Subic
Masinloc

Depth (cm)
-25 -25 Kodia
Oboob

-45 -45

-65 -65

-85 -85

c Bulk δ13C (‰) d FeR-associated δ13C (‰) e OC:FeR (m/m)

-31 -26 -21 -35 -30 -25 -20 0 5 10 15 20 25

-5 -5 -5
Depth (cm)

-25 -25 -25

-45 -45 -45

-65 -65 -65

-85 -85 -85

Fig. 2 Profiles of a OC concentration, b FeR concentration, c bulk δ C signature, d FeR-associated δ13C signature, and e OC/FeR molar ratios in
13

mangrove sediments

3.5 Relationship between OC and FeR
Results revealed two trends between OC and FeR concentra-
tions (Fig. 3). An exponential relationship (OC = 8.38e0.37FeR;
R2 = 0.88; p < 0.0001) emerged between OC and FeR in five
mangrove areas, including Bogtong, Calauit, Kodia,
Masinloc, and Oboob. It was found that the OC/FeR molar
ratios for these areas remained high throughout the sediment
column (Fig. 2e). In this cluster of data points comprising the
five mangrove areas in Fig. 3, the mean OC/FeR molar ratio
was 8.7 ± 4.6. On the other hand, a linear relationship (OC =
− 2.29 + 1.31FeR; R2 = 0.69; p < 0.05) between OC and FeR
was observed in the sediments collected from Subic. The OC/
FeR molar ratio also did not greatly vary throughout the col-
umn and had a mean value of 0.8 ± 0.5.
4 Discussion
4.1 OC across mangrove areas
The increasing OC concentration with depth (Fig. 2a) indicates
that OC is accumulating with depth and is also an evidence of
the efficient burial of OC in mangrove sediments (Breithaupt et
al. 2012). Kodia, which had the highest OC concentration, had
about three times more OC at the bottom sediments (60–75 cm
 J Soils Sediments

Table 1 Depth-integrated means (±SD) of OC and FeR analyses for all sites

Mangrove OC FeR OC- δ13C δ13C-FeR OC/FeR

FeR
Area (g kg−1) (g kg−1) (% OC) (‰) (‰) (m/m)

Bogtong 76 (2)ab 5.6 (0.1)b 14 (4)b − 28.1 (0.2)cd − 25.8 (0.6)a 8.8 (2.5)ab
Calauit 28 (10)cd 4.0 (1.6)b 11 (4)b − 29.4 (0.5)e − 29.3 (2.5)b 3.5 (1.2)cd
Kodia 81 (20)a 5.6 (0.6)b 10 (2)b − 26.2 (0.7)b − 25.5 (2.1)a 6.8 (1.7)bc
Masinloc 50 (27)bc 4.3 (1.4)b 25 (9)a − 27.3 (0.2)c − 25.1 (1.5)a 12.7 (4.8)a
Oboob 12 (2)d 0.5 (0.1)c 12 (2)ab − 22.7 (0.9)a − 30.8 (1.4)b 14.6 (3.5)a
Subic 11 (4)d 10.3 (2.8)a 15 (9)ab − 28.4 (0.5)d − 29.0 (1.6)b 0.8 (0.5)d

Means not sharing common letter in a column are significantly different at p < 0.05
OC-FeR FeR-associated OC concentration, δ13 C-FeR δ13 C signature of FeR-associated OC

in depth) than at the surface. Calauit and Masinloc had three
and seven times more OC at the bottom, respectively, while the
rest of the mangrove areas almost have a uniform distribution of
OC concentrations from the surface to the bottom sediments.
The apparent accumulation of OC in deeper sediments in this
study implies that the carbon stock of mangrove forests, which
is commonly measured to a depth of 1 m only, may be much
higher than previously thought. This could influence global
estimates of carbon stocks (Scharlemann et al. 2014), as well
as the estimates of potential greenhouse gas emissions from
mangrove deforestation. Several studies (Donato et al. 2011;
Hamilton and Friess 2018) reported that mangrove deforesta-
tion results in total carbon loss over time.
Contrary to studies in other mangrove areas across the Asia
Pacific (Donato et al. 2011; Murdiyaso et al. 2015; Nam et al.
2016) which found no significant difference between the OC
concentration of natural and planted mangrove areas, the natu-
ral mangrove areas in Bogtong, Calauit, Kodia, and Masinloc
120
0.37Fe
OC = 8.38e
R2 = 0.88; p < 0.0001
100
OC:FeR = 8.65 ± 4.56
OC Concentraon (g kg-1)
have higher OC concentrations than the planted mangrove area
in Oboob. The mangroves in Oboob were planted on a former
seagrass area, whose sediment conditions may not be suited for
storing OC from mangroves and other terrestrial inputs. While
not significantly different (p > 0.05), the natural mangrove area
in Subic had a slightly lower OC concentration than Oboob.
However, preliminary evaluation of sedimentation rates in
Philippine mangrove forests using 210Pb dating technique
showed that Subic had an anomalously high sediment accretion
rate of 12 ± 3 mm year−1 (Lim et al. 2015), which falls above
the global average of 1.9–3.9 mm year−1 for mangrove areas
(Breithaupt et al. 2012), and was considered an outlier. The
high sediment accretion rate in the Subic site was due to vol-
canic ash deposition from the eruption of Mt. Pinatubo in 1991
(Wilson 1999), as confirmed by the presence of halloysite in the
samples (see Electronic Supplementary Material, Fig. S1).
Small variations in the ratio of two stable isotopes of car-
bon (13C and 12C) can indicate whether photosynthesized or-
ganic matter was mainly derived from either terrestrial or ma-
rine ecosystems. Since marine plants use dissolved inorganic
Mangrove Area
Bogtong carbon as their source of carbon (δ13C = 0‰) and terrestrial
Calauit
Kodia plants use carbon dioxide in air (δ13C = −7‰), there will be
Masinloc
differences in the final isotopic signatures of resulting OC

Oboob

80
Subic (Farquhar et al. 1989). Organic matter loadings in marine en-
Dominant Binding vironments via sediment transport is characterized by aliphatic
Mechanism
Adsorpon organic compounds like lignin, a class of phenolic compounds
60 Coprecipitaon
found exclusively in vascular plants, which are also used as
tracers of terrestrial organic matter. Organic matter produced
40 OC=−2.29+1.31FeR
in situ, on the other hand, has high amino acids, sugars, and
R2 = 0.69; p = 0.04
lipids from phytoplankton, the end-member for marine organ-
OC:FeR = 0.75 ± 0.49
20 ic matter (Burdige 2007). Therefore, terrestrial organic matter
has a δ13C signature of approximately − 27‰, while marine-
derived organic matter has a δ13C signature of approximately
0
0 5 10 15 − 20‰ (Wang et al. 1998; Lalonde et al. 2012). Kristensen et
FeR (g kg-1) al. (2008) reported that measurements which have δ13C values
Fig. 3 Scatterplot of OC concentration vs. FeR concentration with
more depleted than − 25‰ in mangrove sediments indicate a
exponential and linear fits for sites with coprecipitation and adsorption significant contribution of mangrove litter (δ13C ≈ − 27 to −
as dominant binding mechanisms, respectively 29.4‰) (Bouillon et al. 2008) to the mangrove OC pool, while
J Soils Sediments
δ13C values between − 17 and − 23‰ indicate a large contri-
bution of imported or local 13C-enriched carbon sources like
phytoplankton, seagrasses, or microphytobenthos.
The δ13C values in the surface sediments encompassed
both terrestrial and marine carbon signatures (Fig. 2c). These
results indicate that the δ13C signatures of the bulk OC were
characteristic of the organic matter deposited into mangrove
sediments from different sources. As depth increased, the de-
viation among the values decreased and approached the δ13C
signature of terrestrially derived organic matter, indicating a
preference in the bulk organic matter that is preserved and
accumulated in deeper sediments. Sediments from all man-
grove areas except Oboob had δ13C values which are more
depleted than − 25‰. This implies that terrestrial organic mat-
ter is a primary contributor of OC in the sample mangrove
areas. It is clear from the δ13C values of sediments from
Oboob that the bulk OC was derived from marine photosyn-
thetic organisms, particularly seagrasses, which is native to the
area as revealed by the increasing enrichment of δ13C values
with depth. The site in Oboob has wide seagrass extent.
4.2 FeR as primary control of OC concentration
Similar to the trend in OC concentration, FeR concentration
also increased from the surface sediments to the bottom (Fig.
2b), which suggests that efficient OC burial is associated with
the burial of FeR. The differences in FeR concentration across
sites are attributed to the differences in total iron concentration
in the sediments derived from the parent material (see XRF
data in the Electronic Supplementary Material 2). Mangrove
sediments collected from Oboob, for example, which were
mostly made up of calcareous minerals (e.g., calcite), had
the least iron concentration. However, those collected from
Subic, which were derived from recently exposed volcanic
materials and had very dominant XRD peaks of iron-bearing
minerals like amphibole, had the highest concentration (see
Electronic Supplementary Material 1, Fig. S1). Iron undergoes
through diagenetic transformation at the redox interface of
sediments (Riedel et al. 2013), and its interaction with organic
matter determines the fate of OC.
The mangrove forest floor easily absorbs and releases wa-
ter like a giant sponge (Alongi 2009). Being in the interface of
land and ocean, tides heavily affect the porewater chemistry of
mangrove forest floors (Ovalle et al. 1990; Marchand et al.
2004). During flood tides, oxygen concentration decreases
(anoxic) at the forest floor as it is submerged, and oxygen
concentration increases (oxic) during ebb tides as it is exposed
to air (Skelton and Allaway 1996; Kitaya et al. 2002). Under
anoxic conditions, iron in the sediments is reductively dis-
solved, and it is reprecipitated into its oxidized state once
exposed to oxygen. In the oxidation process, organic matter
may be chelated or coprecipitated with iron, leading to the
formation of FeR-organic matter complexes (Riedel et al.
2013). It had also been observed through long-term incubation
experiments that FeR not only directly preserves organic mat-
ter (Boudot et al. 1989), but actively participates in its shut-
tling from solution to the solid phases of deep marine sedi-
ments during early diagenesis as well (Barber et al. 2014). The
dynamic and sponge-like characteristic of the mangrove forest
floor thus allows for the enhanced coupling of organic matter
and FeR in the sediments. The mechanism observed by Barber
et al. (2014) manifests significantly in mangrove sediments,
thus resulting in OC concentrations being controlled by FeR
(Fig. 3). Together, these results suggest that FeR plays a pri-
mary role in the efficient burial and preservation of organic
matter in the carbon-rich substrate of mangrove systems.
Strong correlations between OC and FeR concentrations had
also been observed in sediments from four diverse river (r =
0.72) and glacial (r = 0.88) systems (Poulton and Raiswell
2005). However, the exponential relationship observed in this
study highlights the unique redox conditions of mangrove
systems that govern the interaction between OC and FeR.
4.3 Direct association between FeR and OC
The association between OC and FeR occurs mainly through
two binding mechanisms, adsorption and/or coprecipitation.
Adsorption occurs when OC is simply attached onto discrete
iron oxide particles or surfaces of aluminosilicate minerals.
Coprecipitation occurs when reduced iron migrating through
anoxic porewaters is oxidized in the presence of dissolved
organic matter at the redox interface, forming FeR-organic
matter complexes (Riedel et al. 2013; Chen et al. 2015). A
study reported that the maximum sorptive capacity of the re-
active phases of iron was found to be 0.22 g OC per g FeR
(OC/FeR = 1) (Kaiser and Guggenberger 2000). An OC/FeR
molar ratio of 1 or less indicates adsorption as the dominant
binding mechanism, while an OC/FeR of 6–10 indicates
coprecipitation (Shields et al. 2016).
The exponential relationship between OC and FeR in the
samples from Bogtong, Calauit, Kodia, Masinloc, and Oboob
(Fig. 3), in which coprecipitation is the dominant binding
mechanism (OC/FeR molar ratio = 8.7 ± 4.6), is reflective of
coprecipitation interaction. This result is consistent with the
findings of Chen et al. (2014), wherein higher OC concentra-
tion is obtained with increasing FeR concentration than can be
obtained with simple adsorption. Furthermore, this exponen-
tial relationship, which has never been observed in other en-
vironments, is also reflective of the growth of metastable
onion-like structures of organic matter bound together by
inner-sphere covalent bonds with FeR (Mackey and Zirino
1994; Barber et al. 2017). The linear relationship between
OC and FeR concentrations for mangrove sediments collected
from Subic, in which adsorption was the dominant binding
mechanism (OC/FeR molar ratio = 0.8 ± 0.5), had a different
environment and hydrodynamics among the sample areas

because of its anomalously high sediment accretion rate (Lim
et al. 2015). In areas of high clastic sedimentation rates, OC
and FeR are expected to be associated through adsorption
(Shields et al. 2016), and this is consistent with our findings
on the mangrove sediments from Subic. But since Subic,
which experienced volcanic ash deposition, had an anoma-
lously higher sediment accretion rate, the association between
OC and FeR in its sediments is non-representative of man-
grove areas worldwide. Together, these results suggest that
coprecipitation is the dominant binding mechanism in man-
grove sediments forming FeR-organic matter complexes
(Riedel et al. 2013; Chen et al. 2015).
Coprecipitation allows the formation of covalent bonds be-
tween iron and organic matter, which then leads to the forma-
tion of FeR-organic matter complexes that are metastable over
geologic timescales (~ 400 ky) (Haese et al. 1997). On aver-
age, it was estimated that approximately 15.01 ± 7.35% of OC
in mangrove sediments is directly bound to FeR and ~ 14.7 ±
8.0% of this OC is bound through coprecipitation. This esti-
mate is lower than that of Lalonde et al. (2012) for sediments
from various depositional areas (21.5 ± 8.6%), but comparable
to the value reported by Shields et al. (2016) for deltaic sedi-
ments (15 ± 2.6%). However, it is important to note that the
OC concentration reported by both studies were significantly
lower than the OC concentration in mangrove sediments re-
ported in this study. Using the global OC burial rate in man-
grove sediments, it was estimated in this study that FeR pre-
serves organic matter by coprecipitation of up to 5.44 × 1012 g
OC year−1. Together, these results indicate a direct interaction
between OC and FeR in mangrove sediments and that the
covariation between the iron and OC is not just a result of
the high affinity of these species for solid and fine-grained
particles (Berner 1970; Lalonde et al. 2012). Based on the
downcore profiles of OC/FeR molar ratios (Fig. 2e), the inter-
action between OC and FeR in mangrove sediments remains
active even up to a depth of 1 m, as opposed to what was
previously observed in other coastal systems (Shields et al.
2016).
4.4 Preferential sorption of terrestrial OC
It was hypothesized that FeR preferentially binds with OC of
terrestrial origin in mangrove sediments. That is, the FeR-as-
sociated OC will have a depleted δ13C value, regardless of the
bulk OC signature. In all the sample mangrove areas except
Oboob, both the δ13C value of the bulk and FeR-associated
OC (Table 1) reflect the signature of organic matter derived
from the terrestrial environment. In Oboob, even if the bulk
δ13C values reflect marine-derived organic matter, the FeR-
associated OC have depleted δ13C values.
These results suggest that FeR in mangrove sediments pref-
erentially traps and preserves organic matter delivered in
mangrove forests from terrestrial environments. These
J Soils Sediments
support the findings of Shields et al. (2016) and Riedel et al.
(2013) that FeR plays a significant role in the delivery of
terrestrial organic matter into sediments. Since iron plays a
significant role in the capture and retention of OC in mangrove
sediments, and since it is affected by the redox regimes that
result from the sponge-like characteristic of the mangrove
forest floor, this study proposes that mangrove sediments
function as a Bgiant rusty sponge^ for carbon.
4.5 Implications for mangrove restoration
and rehabilitation
Mangrove restoration and rehabilitation are critical compo-
nent of climate change mitigation due to the capacity of man-
groves to sequester large amounts of carbon (Alongi 2014).
Recent environmental tragedies such as the Indonesia tsunami
in 2004 and super typhoon Haiyan in 2013 showed the impor-
tance to our environmental and coastal resilience. Hence,
mangrove restoration and rehabilitation have gained public
awareness in the last 15 years. The increasing storm frequency
and intensity associated with climate change have also
highlighted the coastal protection function of mangrove for-
ests (Salmo et al. 2014). However, some important measures
for the selection of restoration and rehabilitation areas and
site-specific matching were disregarded. In addition, while
the significant increase in awareness is generally beneficial,
it reached the point where mangrove rehabilitation had also
been carried out seaward in seagrass beds and mudflats
(Primavera et al. 2012), as was the case with the Oboob area.
This is not only ecologically misguided as it will disturb the
distinct seagrass ecosystem, but will also unlikely serve the
climate change mitigation function of mangroves. This study
emphasizes that the capacity of mangroves to sequester carbon
in sediments is inextricably linked to its ecology, particularly
its unique redox conditions (Gleason et al. 2003; Kristensen
2008; Salmo et al. 2013), which enhance the coupling of iron
and OC, resulting in the long-term preservation of the latter.
Interestingly, it was also suggested that large amounts of OC
in mangrove sediments also facilitate conducive redox poten-
tials needed for optimum nutrient cycling (Cardona and
Botero 1998; Salmo et al. 2013).
While FeR in the sediments retained terrestrial OC (Fig. 2d),
low FeR concentration caused the bulk δ13C signature to be
reflective of marine-derived OC. It was established that FeR
preferentially preserves terrestrial OC, and because of the low
FeR concentration in Oboob, it is unlikely that the total OC
concentration in its sediments will significantly increase over
time. This demonstrates that initiatives on increasing the carbon
stock in mangrove forests must incorporate a mechanistic un-
derstanding of how OC persists in the sediments. This under-
standing can support how mangrove forests can be sustainably
managed and valued as it will inform decisions on maximizing
the ecological and economic benefits of mangrove ecosystems.
J Soils Sediments
It is projected that the sea level will increase by 0.5 to 1.4 m
above the 1990 level (Rahmstorf 2007), which in turn will alter
environmental conditions of the mangrove areas such as salinity.
Different mangrove species have marked preference for different
levels of salinity and are thus found at specific distances and
elevations that reflect specific degrees of tidal and freshwater
mixing (Field 1995). Mangroves can adjust to this change only
if the rates of sediment accretion exceed that of sea-level rise, a
problem for mangroves in limestone islands such as Bantayan
Island, Cebu (i.e., Kodia and Oboob sites), where sediment input
is low (Ellison and Stoddart 1991). However, climate change and
other anthropogenic activities have led to the decrease in the
delivery of sediments, and therefore of iron-bearing minerals
and organic matter, from the terrestrial environment to the ocean
(Syvitski et al. 2005; Keil 2017). The damming of rivers, for
example, which already decreased sediment delivery by 30%
to the coastal regions (Syvitski and Milliman 2007), remains a
threat to the survival of mangroves. All these can result in a
snowball feedback on the atmospheric carbon dioxide concen-
tration and therefore call for mangrove rehabilitation programs
and research on carbon in coastal wetlands to consider these
future scenarios.
5 Conclusions
The interaction between OC and FeR in mangrove sediments
occurs mainly through coprecipitation, which happens when
dissolved iron in the sediments is oxidized in the presence of
organic matter to form FeR-OC complexes. This mechanism
allows for a greater amount of OC to be bound to FeR, shown
to be metastable and exhibit a preservative effect on OC, than
can be obtained by its adsorption to mineral surfaces in sedi-
ments. Moreover, it was observed that FeR preferentially traps
terrestrial OC in the sediments. This implies that FeR aids the
incorporation of riverine OC in the sediments, explaining why
terrestrially derived organic matter composes over 60% of the
carbon budget of mangrove sediments and why it disappears
in marine sediments. Finally, this study found that FeR expo-
nentially controls the concentration of OC in mangrove sedi-
ments. FeR plays a significant role in the burial and eventual
preservation of OC in sediments and is an essential driver of
the global biogeochemical cycles of oxygen and carbon. This
mechanistic understanding of the long-term carbon storage in
mangrove systems could help draft better strategies for blue
carbon initiatives.
Funding information This study was supported by the Department of
Science and Technology Accelerated Science and Technology Human
Resource Development Program—National Science Consortium
(DOST ASTHRDP-NSC); the Philippine Nuclear Research Institute
Graduate Student Research Grant Program (PNRI GSRGP), with funding
from the Philippine Council for Industry, Energy and Emerging
Technologies (PCIEERD); and the United States Agency for
International Development (USAID) through the Partnership for
Enhanced Engagement in Research (PEER) of the National Science
Foundation (NSF; Project 3-191). The University Research Council of
Ateneo de Manila University has granted a research faculty fellowship to
Ian A. Navarrete during the preparation of the manuscript.
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