Marine Pollution Bulletin 119 (2017) 460–464

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Marine Pollution Bulletin

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Baseline

High fragility of the soil organic C pools in mangrove forests MARK

a,⁎ a b b a c
X.L. Otero , A. Méndez , G.N. Nóbrega , T.O. Ferreira , M.J. Santiso-Taboada , W. Meléndez ,
F. Macíasa
a
Departamento de Edafoloxía e Química Agrícola, Facultade de Bioloxía, Universidade de Santiago de Compostela, 15782, Spain
b
Departamento de Ciência do Solo, Universidade de São Paulo, 13418-900 Piracicaba, SP, Brazil
c
Instituto de Ciencias de la Tierra, Facultad de Ciencias, Universidad Central de Venezuela, Caracas, Venezuela

A R T I C L E I N F O A B S T R A C T

Keywords: Mangrove forests play an important role in biogeochemical cycle of C, storing large amounts of organic carbon.
Blue carbon However, these functions can be controlled by the high spatial heterogeneity of these intertidal environments. In
Dead mangrove this study were performed an intensive sampling characterizing mangrove soils under different type of
Soil organic C pools vegetation (Rhizophora/Avicennia/dead mangrove) in the Venezuelan coast. The soils were anoxic, with a
ENSO
pH ~7; however other soil parameters varied widely (e.g., clay, organic carbon). Dead mangrove area showed a
significant lower amounts of total organic carbon (TOC) (6.8 ± 2.2%), in comparison to the well-preserved
mangrove of Avicennia or Rhizophora (TOC = 17–20%). Our results indicate that 56% of the TOC was lost within
a period of 10 years and we estimate that 11,219 kg m− 2 of CO2 was emitted as a result of the mangrove death.
These results represent an average emission rate of 11.2 ± 19.17 tCO2 ha− 1 y− 1.

Mangrove forests occur along tropical and subtropical coastlines,
covering > 70% of the intertidal zones (FAO, 2003; Spalding et al.,
1997; Giri et al., 2011; Donato et al., 2011; Kauffman and Donato,
2012; Kauffman et al., 2014). These ecosystems play an important role
in the regulation of biogeochemical cycling of C and nutrients (such N
and P) (Chmura et al., 2003; Kristensen et al., 2008a; Suarez-Abelenda
et al., 2014; Nóbrega et al., 2014). However, the ability of these
ecosystems to perform such functions depends on the degree of
development and conservation of the forests, which in turn may
influence the composition and properties of their soils (Lee et al.,
2014; Nóbrega et al., 2014). Mangrove soils are generally characterized
by reducing conditions and highly variable soil salinity (Mitsch and
Gosselink, 1993; Sherman et al., 1998). However, recent studies
reported a great heterogeneity in relation to soil properties (pH, Eh,
electrical conductivity) and composition (clay mineralogy, organic
matter and metal concentration), implying that the physiographical
position of mangroves within the estuary greatly affects soil attributes
and environmental functions (e.g. Souza-junior et al., 2008; Bouillon
et al., 2008a, 2008b; Ferreira et al., 2010; McKee, 2011; Krauss et al.,
2014; Li et al., 2014; Lunstrum and Chen, 2014). Nevertheless, the
degradation of mangrove forests by direct (e.g., deforestation and wood
removal) or indirect anthropogenic actions (eutrophication, climatic
changes) promotes changes in the soil properties stimulating organic
matter decomposition and increases in CO2 and/or CH4 fluxes to the
atmosphere (Kristensen et al., 2008b; Suarez-Abelenda et al., 2014;
Chauhan et al., 2015).
The main objective of this study was evaluated the loss of soil
organic carbon induced by non-anthropogenic causes (e.g. El Niño
Southern Oscillation -ENSO). For this purpose it have been selected two
mangrove forests on the Venezuelan coast: La Restinga lagoon National
Park on Margarita Island and the Golfete de Cuare wildlife refuge, part
of which is located in the Morrocoy National Park (Falcón state)
(Fig. 1A and B). Both locations are natural environments that have
been protected since 1974, representing two well-preserved coastal
ecosystems. Rhizophora mangle and Avicennia germinans predominate in
both mangrove forests (Barreto, 2004, 2008). However, a massive
mangrove mortality, previously vegetated with Avicennia germinans,
was observed after the very strong event of El Niño Southern Oscillation
(ENSO) (Barreto, 2008). Mangrove mortality has been related to
progressive increase in the porewater salinity (73 to 88 ppt) in the A.
germinans zone due changes in hydrological and sedimentary patterns
(Barreto, 2008). Similar results were also observed in Micronesian
mangroves (Drexler and Ewel, 2001). The sampling points were
selected based on the distribution of plant species, physiographical
position and degree of conservation of the mangrove forest (well-
preserved or dead), to cover the variability within and between the
different mangrove systems.
This coast is characterized by a semi-arid, sub-humid dry climate.
The mean annual temperature ranges between 27 and 29 °C and the
mean annual rainfall varies between 362 mm on Margarita Island (data

⁎
Corresponding author at: Departamento de Edafoloxía e Química Agrícola, Facultade de Bioloxía, Universidad de Santiago de Compostela, 15782 Santiago de Compostela, Spain.
E-mail address: xl.otero@usc.es (X.L. Otero).

http://dx.doi.org/10.1016/j.marpolbul.2017.03.074
Received 1 February 2017; Received in revised form 23 March 2017; Accepted 31 March 2017
Available online 06 April 2017
0025-326X/ © 2017 Elsevier Ltd. All rights reserved.
X.L. Otero et al.
Fig. 1. A) Map showing the location of the study area and the sampling points; B) Detail of sample distribution in transect 4; C) Area with dead mangrove in the Golfete de Cuare estuary.
recorded between 1967 and 1977) and 1000 mm in the Golfete de
Cuare (data recorded between 1961 and 2000; Monente, 1978; MARNR
- Ministério del Ambiente y del Recursos Naturales Renovables, 1991;
Barreto, 2008). At La Restinga lagoon, 12 surface soil samples
(0–20 cm) were obtained under well-preserved R. mangle (n = 5) and
A. germinans (n = 5) and dead mangrove (n = 2) (Fig. 1A). In the
Golfete de Cuare estuary 23 surface soil samples (0–20 cm) were
collected: 14 samples were collected under a well-preserved mangrove
forest with two-different mangrove species, R. mangle (n = 6) and A.
germinans (n = 8), and 9 soil samples were collected in a dead
mangrove forest. All sampling points were selected based on the plant
species and degree of conservation of the mangrove forest (well-
preserved or dead), to cover the variability within and between
different mangrove systems.
Soil samples were collected at low tide during the dry period (April)
in 2008. Core samples were collected in triplicate using 20-cm depth
PVC tubes (5 cm diameter). The samples were immediately combined to
461
Marine Pollution Bulletin 119 (2017) 460–464
make a composite soil sample. The composite soil samples and were
sealed and placed in a portable cooler at ~5 °C. The pH (pHField) and
redox potential (Eh) were measured in the field, at 5–10 cm depth, with
a glass and a platinum electrode, respectively. The final Eh readings
were corrected by adding the potential (+244 mV) of a calomel
reference electrode. In the laboratory, sub-samples were dried for the
determination of particle size distribution, bulk density, total carbon
(TC), total organic carbon (TOC), total nitrogen (TN), total sulphur (TS)
contents. The particle size distribution was determined by the pipette
method, with sodium hexametaphosphate as dispersant (Gee and
Bauder, 1986), after removal of the organic matter with hydrogen
peroxide (15%). Dry bulk density (DBD) was determined from the mass
of the sample dried at 105 °C to constant weight and its original volume
(100 cm3) (Howard et al., 2014). The TC, TOC (after removing
carbonates with HCl 1 M) and TN contents were determined in a
TruSpec CHNS analyzer (LECO Corp., St Joseph, MI, USA), while TS
was measured in an SC-144DR analyzer.
X.L. Otero et al.
Soil C pools were determined by adopting a widely used field
protocol for mangrove ecosystem C stocks assessment (Kauffman and
Donato, 2012; Howard et al., 2014). Soil organic C pools and were
calculated for the studied sites (type of mangroves, including dead
mangrove) and sites, according to Eq. (1). In order to compare soil C
stocks for the same soil mass among different vegetation types, the
Equivalent Soil organic C pool was calculated considering an equivalent
depth (Zeqv). For the calculations, an equivalent depth is obtained
using a reference DBD (in this study, the DBD from the Avicennia forest)
and the DBD from other mangrove type (dead mangrove and Rhizo-
phora) (Eq. (2)). Thus, the Equivalent Soil organic C pool (EQV-Cpool)
is calculated as presented in Eq. (3) and the CO2 emission resulting from
the mangrove death was estimated (for more details see Kauffman and
Donato, 2012; Howard et al., 2014).
Soil organic C pool (Mg C ha−1) = DBD (g cm −3) × TOC (%) × depth (cm)
(1)
Zeqv=(DBDAVICENNIA DBDSITE) × 20 cm (2)
Equivalent Soil C pool (Mg C ha−1) = DBDSITE (g cm −3) × TOC (%)
× Zeqv (cm) (3)
As the natural event of ENSO affected a Avicennia forest (Barreto,
2008), the differences in soil organic C pools among a previous
preserved condition (used the Avicennia soil organic C pool) and the
actual dead mangrove condition were quantified, assuming a conver-
sion maxima of 90% of the soil carbon to CO2 as a result of changes of
the vegetation, according to the criteria stablished in previous man-
groves studies (Murray et al., 2011; Siikamäki et al., 2012). The value
of C loss was converted to CO2 by multiplying 3.67, (ratio of molecular
weights between carbon dioxide (44) and carbon, (12) (Kauffman and
Donato, 2012)).
All Statistical analysis were performed using SSPS 19.0 (Inc.,
Chicago, USA). The normality of the data was checked using the
Kolmogorov-Smirnov test. Non-normally distributed variables were
transformed to natural logarithms, except for the percentage data,
which were subjected to an arcsine transformation, more appropriate to
this type of data (Zar, 1996). Differences in soil variables were analysed
by two-way ANOVA (SPSS 19.0; Inc., Chicago, USA) followed by a
Tukey test, with the sampling area (Golfete de Cuare and La Restinga
lagoon) and type of mangrove-forest (Rhizophora, Avicennia and dead
mangrove) as fixed factors.
Dry bulk density showed significant differences between sites and
among forest types, with the higher mean values in the dead mangrove
soils (0.50 ± 0.11 g cm− 3, Table 1) followed by Avicennia
(0.33 ± 0.01 g cm− 3) and Rhizophora (0.22 ± 0.02 g cm− 3). Redox
potential did not differ between the study areas (mean values:
141 ± 112 mV and 154 ± 119 mV at Golfete de Cuare and La
Restinga lagoon, respectively; Table 1). However, a clear difference
(p < 0.001) between Rhizophora (179 ± 99 mV) and Avicennia
(60 ± 62 mV) was evidenced. Unfortunately, the Eh values for the
dead mangrove site were not obtained during the same sampling
campaign. However, in a posterior study realized at the same sampling
site, Mendez (2016) observed similar Eh values at the dead mangrove
sites and Rhizophora site (dead mangrove: Eh: 177 ± 77 mV;
pH = 6.4 ± 0.2), which indicate an average increment of 117 mV
with respect to Avicennia mangrove soils. The pHField values were close
to neutral (6.1 ± 0.6 at Golfete de Cuare and 6.5 ± 0.3 at La Restinga
lagoon) and did not differ between the study sites or plant species
(Table 1). The particle size distribution, TC, TOC and TS contents did
not differ between sites, but did between forest types (Fig. 2, Table 1).
The clay content was significantly higher in the dead mangrove area
(30.7 ± 1.4%; Table 1). The values of variables associated with the
organic matter content (TC, TOC, TN) were significantly lower in the
dead mangrove area (e.g. mean TOC values for Rhizophora = 14.8 ±
8.0%, Avicennia = 15.5 ± 4.5% and dead mangrove = 6.8 ± 2.2%;
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Marine Pollution Bulletin 119 (2017) 460–464
Table 1, Fig. 2).
The high productivity of mangrove forests, the addition of high
amounts of organic matter and the frequent tidal flooding promote
anoxic conditions (Eh < 200 mV; Table 1) (Alongi, 2012; Vidal-
Torrado et al., 2010). Under these conditions, microbial metabolism
is less efficient degrading simple organic molecules, such as low
molecular weight organic acids (Jørgensen, 2000; Chmura, 2009). This
leads to an increase in the soil organic carbon (SOC) contents,
characterizing these ecosystems as efficient C sinks, denominated Blue
Carbon Sinks (Nellemann et al., 2009; Otero and Macías, 2010; Howard
et al., 2014; Nóbrega et al., 2016). In this study, the TOC contents were
high (mean value for type of vegetation: 14.8–8.7%; median value
17.6–9.7%) in comparison with the median reference value (median
2.2; Kristensen et al., 2008a) and the results found in some areas from
Asia (Tue et al., 2014: TOC = 1.3–2–9%; Alongi et al., 2016: TOC
~1–5%), but similar to those found in Central America mangroves
(Kauffman et al., 2014: TOC > 26%, Bhomia et al., 2016; TOC:
11–20%).
On the other hand, SOC pools, calculated to the first 20 cm of the soil,
showed significant differences among type of vegetation (Fig. 3). The lowest
values were found for the Rhizophora forest (65.1 ± 41.1 Mg C ha− 1),
followed by the dead mangrove soils (68.8 ± 37.0 Mg C ha− 1) and
Avicennia forest (102.3 ± 32.8 Mg C ha− 1). When compared the soil C
pool for the same soil mass, using the soil mass of the Avicennia forest as a
reference, the Rhizophora soil C pool increased to 97.7 ± 55.8 Mg C ha− 1,
whereas the C pool for the dead mangrove decreased to
44.9 ± 15.9 Mg C ha− 1. This SOC loss at the dead mangrove site is in
accordance to the higher redox potential, since the shift from anoxic
condition (Eh < 100 mV) to suboxic (100–300 mV) may lead to a higher
efficiency mineralization process and a SOC loss (Lovelock et al., 2011).
Mangrove soils represent the single largest pool of SOC in these
ecosystems (Bhomia et al., 2016), however, carbon dynamics in
mangrove ecosystems is still far from having an integrated view of
the overall ecosystem functioning in terms of organic matter processing
(Bouillon et al., 2008a). In this respect, the present results indicate a
high fragility of the SOC pools in mangrove forests. If one considers that
the dead mangrove areas correspond to a former Avicennia forest
affected by a severe El Niño Southern Oscillation (ENSO) which
occurred during 1997–1998 (Barreto, 2008), it can be assumed that
56% of the TOC was lost within a period of 10 years. Similar results
were obtained in a study evaluating the impact of deforestation on the C
stored in mangrove soils, in which Granek and Ruttenberg (2008)
recorded losses of 50% of the C stored in the soil 8 years after clearing.
If we consider that the dead mangrove areas correspond to old
Avicennia mangrove forests (Barreto, 2008), with similar environmental
characteristics to the area currently occupied by Avicennia, and that
90% of the soil carbon stock in mangrove forest was released into the
atmosphere as CO2 after land conversion (Murray et al., 2011;
Siikamäki et al., 2012; Pendleton et al., 2012), we may estimate (using
the stock-difference method: Kauffman et al., 2014; Howard et al.,
2014; IPCC [Intergovernmental Panel on Climate Change], 2003) that
11,219 kg m− 2 of CO2 (mass) was emitted as a result of the death of the
mangroves. This represents an average emission rate of
11.2 ± 19.17 tCO2 ha− 1 yr− 1, similar to rates measured in tropical
mangroves in Kenya (Lang'at et al., 2014) and Belize (Lovelock et al.,
2011). However, the emissions measured in Africa and in Central
America included the effects of clearing mangroves on soil emission
from the entire soil profile, whereas our estimation are based only for
the first 20 cm of the soil. Since organic C may reach depths of > 1 m
(Donato et al., 2011; Kauffman et al., 2011, 2014) and considering that
the upper 1 m will be the most affected layer (Siikamaki et al., 2013;
Murray et al., 2011; Donato et al., 2011), the actual emissions in the
study areas may be at least 5 times higher than the estimated values.
Moreover, as the clearance of mangrove forests results in rapid erosive
processes (Lang'at et al., 2014), the loss of mangrove soil particles
would also result in further CO2 emissions far from the study site
X.L. Otero et al. Marine Pollution Bulletin 119 (2017) 460–464

Table 1
Mean ( ± SD) and median values of the physicochemical properties and soil components, and p values corresponding to the ANOVA analysis.

Site Type of mangrove P

GolfeteCuare Restinga Rhizophora Avicennia (n = 12) Dead mangrove Site Type of Interaction
(n = 23) (n = 12) (n = 15) (n = 9) mangrove

Eh (mV) mean ± SD 141 ± 112 154 ± 119 179 ± 99 60 ± 62 na ns < 0.001 ns

Median 81 171 115 66
pH field mean ± SD 6.1 ± 0.6 6.5 ± 0.3 6.3 ± 0.3 6.1 ± 0.8 na ns ns ns
Median 6.8 6.7 6.7 6.4
Bulk density (gr cm− 3), mean ± SD 0.32 ± 0.11 0.37 ± 0.14 0.22 ± 0.02 0.33 ± 0.01 0.50 ± 0.11 0.028 < 0.005 ns
Median 0.30 0.39 0.21 0.27 0.49
Sand (%), mean ± SD 66.9 ± 10.8 46.9 ± 34.7 76.8 ± 16.7 61.3 ± 22.4 45.3 ± 21.3 ns ns 0.017
Median 74.6 46.7 77.1 74.6 47.2
Silt (%), mean ± SD 22.8 ± 11.3 43.8 ± 27.8 19.3 ± 13.3 33.7 ± 17.2 24.0 ± 5.0 ns ns ns
Median 23.1 42.1 17.5 24.4 27.1
Clay (%), mean ± SD 10.2 ± 15.8 9.3 ± 8.1 3.9 ± 4.2 4.9 ± 6.2 30.7 ± 11.4 ns 0.017 ns
Median 3.0 7.9 3.3 2.2 11.6
Total C (%), mean ± SD 16.3 ± 8.6 21.1 ± 5.4 17.4 ± 9.6 20.3 ± 3.8 8.7 ± 1.9 ns 0.017 ns
Median 15.1 23.1 24.2 19.8 10.8
TOC (%), mean ± SD 12.9 ± 6.9 16.4 ± 4.3 14.8 ± 8.0 15.5 ± 4.5 6.8 ± 2.2 ns 0.036 ns
Median 13.3 17.3 17.6 14.6 9.7
Total N (%), mean ± SD 0.8 ± 0.32 1.2 ± 0.2 0.7 ± 0.3 1.1 ± 0.2 0.6 ± 0.1 0.005 0.007 ns
Median 0.84 1.21 1.04 1.01 0.72
Total S (%), mean ± SD 1.7 ± 0.9 1.4 ± 0.3 2.0 ± 1.2 1.6 ± 0.5 1.1 ± 0.3 ns ns ns
Median 1.54 1.43 1.54 1.54 1.27

(Howard et al., 2014; Kauffman et al., 2011).

In conclusion this study revealed that the C stocks in these
environments are very fragile and prone to disturbance. The results
suggest that more than half of the TOC held in soil C stocks may be lost
within a relatively short period of time (10–20 years) if the geochemical
conditions are altered (i.e. Eh-pH conditions), which would also limit
the natural recovery or colonization of the ecosystem.

Acknowledgements

This study was partially supported by a project entitled

“Monitorización dos procesos bioxeoquímicos nas lagoas litorais de
Galicia en relación coa súa calidade ambiental e respuesta ao cambio
climático”, funded by the Consellería de Innovación y Industria-Xunta
de Galicia (PGIDIT08MDS036000PR). The authors (XLOP, AM, MJST, Fig. 3. Soil organic C pool under different type of mangrove forest and different type of
FMV) belong to the CRETUS Strategic Partnership (AGRUP2015/02) environment (gulf and lagoon). Bars indicated with different letters are significantly
co-funded by FEDER (UE). We thank Angel Rivas and Fernando Ramos different to level 5%.
for help during sampling. AMM was supported by a grant from
Fundación Gran Mariscal de Ayacucho (FUNDAYACUCHO), GNN from
São Paulo Research Foundation (FAPESP, grant no 2014/11778-5), TOF
from National Council for Scientific and Development (CNPq).

Fig. 2. Variation in different soils components between vegetation and sites. Rh: Rhizophora, Av: Avicennia, De: dead mangrove.

463
X.L. Otero et al.
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