PRIMARY RESEARCH PAPER
Vegetation and soil characteristics as indicatorsof restoration trajectories in restored mangroves
Severino G. Salmo III • Catherine Lovelock •
Norman C. Duke
Received: 19 November 2012 / Revised: 10 July 2013 / Accepted: 19 July 2013 / Published online: 7 August 2013
� Springer Science+Business Media Dordrecht 2013
Abstract We investigated the restoration trajectories
in vegetation and soil parameters of monospecific
Rhizophora mucronata stands planted 6, 8, 10, 11, 12,
17, 18, and 50 years ago (restored system). We tested
the hypothesis that the changes in vegetation character-
istics, with progressing mangrove age, are related to the
changes in soil characteristics. The vegetation and soil
parameters were compared across this restoration
sequence using a reference system comprising mature,
natural mangrove stands of unknown age. Rapid
increases in leaf area index and aboveground biomass,
and declines in tree density and size (in terms of tree
diameter and height) occurred with increasing stand
age. Soil organic matter, total nitrogen, and soil redox
potential increased, and soil temperature decreased as
stands aged. These patterns tended to stabilize at
approximately the 11th year, indicating the probable
age that restoration plots tend toward forest maturity.
The time for the restored systems to reach forest
maturity, attaining characteristics similar to the refer-
ence system, is estimated at 25 years, which is relatively
slow compared to forest regeneration trajectories esti-
mated for natural mangroves. Our study describes the
trajectory patterns for planted mangroves, which are
important for the assessment of both the progress and
success of mangrove rehabilitation programs.
Keywords Mangroves � Restoration � Soil
carbon � Rhizophora � Space-for-time
substitution � Philippines
Introduction
Mangrove rehabilitation programs have been imple-
mented to restore forest cover and habitat functionality
of extirpated mangrove habitats (Kaly & Jones, 1998;
Field, 1999; Katon et al., 2000; Barbier, 2006). Massive
mangrove planting programs have been undertaken in
Southeast Asia since the early 1990s (Tabuchi, 2004)
Electronic supplementary material The online version ofthis article (doi:10.1007/s10750-013-1617-3) contains supple-mentary material, which is available to authorized users.
Handling editor: I.A. Nagelkerken
S. G. Salmo III (&)
Department of Environmental Science, Ateneo de Manila
University, Loyola Heights, 1108 Quezon City,
Philippines
e-mail: [email protected]
S. G. Salmo III � C. Lovelock
School of Biological Sciences, The University of
Queensland, St Lucia, QLD 4072, Australia
S. G. Salmo III
College of Agriculture, Central Luzon State University,
3120 Science City of Munoz, Nueva Ecija, Philippines
N. C. Duke
Centre for Tropical Water and Aquatic Ecosystem
Research, James Cook University, Townsville,
QLD 4811, Australia
123
Hydrobiologia (2013) 720:1–18
DOI 10.1007/s10750-013-1617-3
and may further continue as planting becomes part of
community rural development programs (Evans, 1999;
Salmo et al., 1999). Among SE Asian countries,
mangrove planting is a popular management tool
(Walters, 2004; Salmo et al., 2007) that has long been
practiced in the Philippines (Primavera & Esteban,
2008). Recently, mangrove rehabilitation programs
have been considered in climate change adaptation
and mitigation strategies because of their likely role both
in the sequestration of atmospheric CO2 (Bouillon,
2011; Donato et al., 2011; Mcleod et al., 2011) and in
enhancing sediment surface elevation with predicted
sea-level rise (McKee, 2011).
While some researchers estimated that the planted
mangroves might approach the biomass, stand structure,
and productivity of natural forests within 20 years (see
for example Colonello & Medina, 1998; Twilley et al.,
1998; McKee & Faulkner, 2000), empirical data to
support such claims are limited. One of the key
parameters that determine the progress or success of
mangrove planting programs is the rate at which the
forest structure and biomass return to those of mature,
natural mangroves (cf. Ellison, 2000). Such parameter
may be used as indicator for forest maturity in planted
mangroves. Another indicator of forest maturity is the
decline and stability of growth rate with stand age
(Jimenez et al., 1985), which for the case of a
Rhizophora apiculata plantation in Thailand, was
estimated to start on the 13th year (Aksornkoae, 1996).
Mangrove recovery from highly localized disturbances,
such as lightning strikes, has been shown to occur
between 10 and 15 years in the process of gap regen-
eration (see Duke, 2001). However, planted mangroves
offer an unusual case where forests are growing on soils
that have often been greatly altered from the original
condition, which may slow growth and development.
The role of soil in the establishment and growth of
mangrove forests has been reported in several studies
(Boto & Wellington, 1984; Thom, 1987; Clarke, 1995;
Cohen et al., 1999 among others). Boto (1984)
proposed that soil parameters are the most important
factors that have direct influence on forest stands,
providing essential nutrients for growth and the
physical structure for anchorage and stability. Aside
from nutrients, other soil parameters that may affect
mangrove growth are soil grain size, salinity, redox
potential, and temperature (Pernetta, 1993; Feller,
1995; McKee, 1995; Chen & Twilley, 1998; Duarte
et al., 1998).
Most mangrove restoration programs are located in
coastal fringes (Primavera & Esteban, 2008; Samson
& Rollon, 2008) where nutrients may be inherently
low and where plants may be exposed to several
additional stresses including inundation with high
salinity water and exposure to erosion due to wind and
waves during storms. The growth and survival of the
planted mangroves will therefore be affected by the
soil characteristics prevailing in a given locality.
Alternatively, the development of soil maturity (sensu
Alongi, 2009) may also be related to the mangrove
vegetation. The inter-relationship between mangrove
vegetation and soil characteristics has been proposed
by Ukpong (1994) and is similar to that described for
tropical forests (Vitousek & Reiners, 1975; Hooper &
Vitousek, 1997). As vegetation structure and produc-
tivity increases with mangrove age, the production of
litter and organic detritus also increases. These
materials are deposited in the forest floor and within
the soil profile, and after degradation and mineraliza-
tion, facilitate the enhancement and accumulation of
organic matter. The large organic matter content of
soils has been proposed to exert an influence on
nutrient regeneration as well as other factors such as
pH and redox potential of the soils (Cardona & Botero,
1998). While there is some understanding of the
relationship between vegetation and soil in natural
mangroves (Chen & Twilley, 1998), studies of the
relationship between growth in planted mangroves and
soil characteristics are still rare, yet, knowledge of
these relationships will assist in determining the value
and delivery of ecosystem services in restored systems
(Lewis, 2005; Bosire et al., 2008; Osland et al., 2012).
Forest age is suggested as an important factor in
determining soil maturity (Alongi, 2009). Predictable
changes in soil characteristics may be expected as
mangrove stand age increases. Unfortunately, criteria
for evaluating soil in mangrove restoration programs
are limited. Ellison (2000) suggested that the mea-
surements of nutrient export and hydrologic patterns
were the key components in assessing the success of
restoration programs. But, evaluation of soils may
provide more suitable indicators because of its linkage
to macrofaunal recruitment and nutrient cycling
(Kathiresan & Bingham, 2001; Chapman & Tolhurst,
2007; Nagelkerken et al., 2008).
While it is perceived that planted mangroves may
show similar growth trajectory patterns as natural
mangroves (under Intermediate Disturbance
2 Hydrobiologia (2013) 720:1–18
123
Hypothesis; cf. Connell, 1978), it is not clear, how-
ever, if planted mangroves have the same rate of
growth and forest recovery to that of natural man-
groves after disturbances (Duke, 2001). Moreover, the
lack or absence of monitoring activities in almost all
mangrove planting programs have been widely criti-
cized since the late 1990s (see for example Kaly &
Jones, 1998; Ellison, 2000; Bosire et al., 2003; Crona
& Ronnback, 2005 among others). Despite the high
level of investment in plantings, it is not clear if these
planting programs are successful or not.
In this study, we evaluated the restoration trajectory
patterns (cf. Ruiz-Jaen & Aide, 2005) in forest and soil
development of planted mangroves over stands of
different ages (referred to as the restored system) and
provided estimates of the time when planted man-
groves approach or match the characteristics observed
within mature, natural mangrove forests (referred to as
the reference system). We tested the hypothesis that
the progression in vegetation characteristics, with
mangrove forest age, is related to changes in soil
characteristics. Such progression of changes with
mangrove age can serve as possible indicator param-
eters for evaluating the progress or success of man-
grove restoration programs. The study contributes
knowledge in setting indicators for assessing forest
maturity in planted mangroves.
Materials and methods
Experimental design
We used existing mangrove plantations of known
different ages to establish space-for-time (SFT)
sequence of mangrove growth and development
trajectory following restoration. Data gathered from
planted mangroves (referred to as the restored system)
were compared with data from natural mangroves
(referred to as the natural system) that served as a
proxy trajectory endpoint of restoration. Our sampling
design used a SFT substitution approach that infers
temporal trends from different aged sites to generate
patterns in the trajectory of the restored system (cf.
Pickett, 1989). Such an approach has been used in
similar studies in restoration ecology where an optimal
sampling design (i.e., the presence of experimental
controls and age replicates within one site) may not be
available (cf. Michener, 1997).
Site description
The main study sites were located in Lingayen Gulf,
northwestern Philippines (between 16�230 and
16�390N latitude; 119�530 and 120�190E longitude;
Fig. 1). Remnant stands of mangrove forests in
Lingayen Gulf consist largely of secondary growth
of the genera Avicennia, Sonneratia, and Rhizophora
in coastal fringes with Nypa swamps in some riverine
areas. The largest and oldest mangrove plantation site
is located in the municipality of Bani (42 ha; 18 years)
and is co-managed by the municipal government and
local communities since 1990. The community-man-
aged mangrove planting projects in the municipalities
of Bolinao and Anda started in 1997 and 1999,
respectively, while the mangroves in Alaminos were
planted in 2000. The youngest plantation is located in
Anda (Tondol), which was planted in 2002. Among
these sites, only the mangrove forest in Bani has a
formal management regime as it was declared a
Marine Protected Area in 2001.
We utilized the planted R. mucronata mangroves
located in Tondol, Anda (6-year); Mona, Alaminos (8-
year); Imbo, Anda (10-year); Pilar, Bolinao (11-year);
and Bangrin, Bani (18-year; Fig. 1). Sites in Alami-
nos, Anda, and Bolinao are more exposed to coastal
currents since they face the Lingayen Gulf while
mangroves in Bani are located in sheltered areas in
Tambac Bay and receive freshwater and sediment
inputs from the Bani River. Additional mangrove
plantations from Central Philippines were included,
these are: 12- and 17-year-old plantations from
Buswang, Kalibo (Panay Island, central Philippines),
and 50-year-old plantation from Banacon Island
(Getafe, Bohol, central Philippines). The mangrove
forest in Banacon is considered one of the earliest and
largest mangrove plantations in Asia (at least 50 years,
400 ha). Most of the early planted forests were
subjected to rotational harvesting (Walters, 2005)
with a small patch (*5–10 ha) spared by the locals
from cutting. These remnant pseudo-protected man-
grove stands were used as the sampling site for the
50-year-old forest.
Three natural mangrove forests were used as refer-
ence sites (Fig. 1): Buenavista in Bohol (Nx; central
Philippines; 10�5036.0300N latitude, 124�7017.9400E lon-
gitude), and Masinloc (Ny; 15�29028.2900N latitude,
119�53030.3100E longitude) and Palauig (Nz;
15�29013.1900N latitude, 119�54015.0200E longitude) in
Hydrobiologia (2013) 720:1–18 3
123
Zambales (north-northwestern Philippines). These nat-
ural forests are dominated by Rhizophora species and
are protected by national environmental laws. The
variation in the age of the planted mangroves provided
an opportunity to describe restoration trajectories and
predict the time that it takes for planted forests to
achieve similar vegetation and soil characteristics as the
reference system.
The average depth of tidal water at high tide across
study sites was estimated at 2 m. Most of the forests were
exposed at low tide particularly during September to
February. All sites received precipitation of more than
1,700 mm year-1. Under the modified Corona classifi-
cation system, the climate in Lingayen Gulf and
Zambales is classified as Type I (with two pronounced
seasons: dry from November to April and wet from May
to October) while Aklan is categorized as Type III (no
pronounced maximum rain period, with 1–3 months dry
season). The climate in Bohol falls under Type IV, which
has no pronounced wet and dry seasons (Table 1).
Fig. 1 Location of study sites. Numbers indicate the age of
plantation. Planted mangroves are located in northwestern
Lingayen Gulf (top left); Kalibo, central Philippines (top right);
and Getafe, central Philippines (bottom right). Natural man-
grove stands are located in Masinloc and Palauig (north-
northwestern Philippines; bottom left) and Buenavista, central
Philippines (bottom right). The ages of natural mangroves are
unknown (inset map of the Philippines). P planted mangroves,
N natural mangroves
4 Hydrobiologia (2013) 720:1–18
123
Vegetation
Mangrove forests were measured from December
2008 to March 2010. Mangrove plantations in Ling-
ayen Gulf were assessed in December 2008, May
2009, July 2009, December 2009, and March 2010
while the plantations in Kalibo (12- and 17-year) and
Bohol (50-year and Nx) were measured in January
2009, June 2009, and January 2010. The natural
mangroves in Zambales (Ny and Nz) were measured
in December 2008, May 2009, December 2009, and
February 2010. Our sampling approach allowed
assessment of three to five temporal data points in
the restoration trajectory of each stand.
In each planted and natural mangrove stand, three
permanent monitoring plots were randomly estab-
lished. Plots had 3-m radius for plantations less than
17-year-old and 5-m radius for the more mature sites.
The difference in plot sizes was made to accommodate
differences in size of trees and tree density and thus
standardize the number of trees measured from each
plot. Leaf area index (LAI) was measured twice from
the center of the plot using CI-110 (Plant Canopy
Imager, CID Bio-Science, Washington, USA). Each
individual within the plot was tagged and measured
throughout the sampling period. Tree diameter of all
individuals in the plot was measured 2–3 cm above the
highest prop root using a measuring tape and total tree
height was measured using a telescoping pole. In each
plot, the number of seedlings and saplings were also
measured. Tree density was computed from the
number of trees per plot scaled up to per hectare.
The aboveground biomass (AGB) was computed
using the allometric equation for Rhizophora species.
We used the equation Y = 0.235 DBH2.42, where
Y = biomass (in kg) and DBH = diameter at breast
height (in cm), derived from Matang mangroves in
Perak, Malaysia (Ong et al., 2004). We are not aware
of published allometric equation for Philippine man-
groves. Hence, from the available Southeast Asian
mangrove data, we chose the allometric equation from
the Matang mangroves because it has closer agro-
meteorological resemblance to that of the mangrove
sites used in this study.
Soil
From each vegetation plot, three replicate soil samples
were randomly collected during low tide. Samples
were collected to 10 cm depth using a soil corer
(diameter: 6.5 cm) made from PVC. From the inter-
stitial waters, salinity was measured with a hand-held
refractometer (HT211-ATC, HT Tech, Jiangsu,
China). The pH, redox potential of soils, and temper-
ature, were measured using Aqua-pH Waterproof pH-
mV-temperature meter (Aqua pH 2.2, TPS, Brisbane,
Australia). The salinity, pH, redox potential, and
temperature were measured three times in each plot.
Soil samples were analyzed within 24–48 h after
sampling at the Bureau of Soils and Water
Table 1 Physical and climatic description of the study sites
Stand age/
stage
Location Latitude, �N Longitude, �E Study
area (ha)
Elevation (m) Mean annual
temp.a (�C)
Total annual
rainfalla (mm)
6 Tondol (Lingayen Gulf) 16.3151 120.0101 6 -0.12 ± 0.02 27.1 ± 0.3 2,904 ± 84
8 Pangapisan (Lingayen Gulf) 16.2023 119.9875 6 0.14 ± 0.01 27.1 ± 0.3 2,904 ± 84
10 Imbo (Lingayen Gulf) 16.3208 120.0019 8 -0.22 ± 0.03 27.1 ± 0.2 2,904 ± 84
11 Pilar (Lingayen Gulf) 16.3711 119.9638 8 -0.13 ± 0.01 27.1 ± 0.3 2,904 ± 84
12 Buswang (Panay Is.) 11.7188 122.3895 10 0.12 ± 0.01 27.2 ± 0.2 2,597 ± 32
17 Buswang (Panay Is.) 11.7185 122.3912 10 0.07 ± 0.01 27.2 ± 0.2 2,597 ± 32
18 Bangrin (Lingayen Gulf) 16.2432 119.9303 42 0.20 ± 0.01 27.1 ± 0.3 2,904 ± 84
50 Banacon (Bohol) 10.2010 124.1659 10 -0.23 ± 0.03 27.6 ± 0.2 1,775 ± 15
Nx Buenavista (Bohol) 10.0876 124.1191 8 0.10 ± 0.01 27.6 ± 0.2 1,775 ± 15
Ny Masinloc (Zambales) 15.4937 119.9234 8 -0.13 ± 0.01 27.2 ± 0.3 3,049 ± 85
Nz Palauig (Zambales) 15.4921 119.9205 5 -0.09 ± 0.01 27.2 ± 0.3 3,049 ± 85
Nx, Ny, and Nz are natural mangroves of unknown ages. Elevation was estimated based on mean tidal levela Extrapolated from 30-year climate normals from FAO 2001
Hydrobiologia (2013) 720:1–18 5
123
Management laboratory (Quezon City, Philippines)
for the analysis of sand, silt, organic matter (OM), total
nitrogen (TN), and available phosphorus (AP) con-
tents. Soil organic matter was measured by Walkley–
Black method (Walkley & Black, 1934), total nitrogen
by digestion method (Nelson & Sommers, 1972), and
available phosphorus by the Bray 2 method (Bray &
Kurtz, 1945).
Data analysis
Data were analyzed using one-way repeated measures
ANOVA, correlation analyses, and multivariate sta-
tistics. For the three natural mangrove stands, data
were pooled since there was no statistically significant
difference among these stands. For the 11- and 18-year
stands in Lingayen Gulf, only the December 2008 data
were included in the analyses as these sites suffered
high mortalities caused by Typhoon Chan-hom on 7th
May 2009.
One-way repeated measures ANOVA was used to
determine if the LAI, tree density, and AGB varied
with time in each stand. The assumptions for ANOVA
were evaluated using Levene’s test without data
transformation. Post hoc comparisons were made
using Tukey’s test to determine pairwise differences
between sampling periods. The relationships among
vegetation and soil characteristics with mangrove
stand age were assessed using correlation analyses.
Multivariate tests were conducted to visualize vege-
tation and soil development patterns with mangrove
stand age. For vegetation, LAI data was untransformed
while the tree density and AGB data were log-
transformed and then normalized to create a resem-
blance matrix based on Euclidean Distance. For soils,
all soil variables except redox potential were log-
transformed, and then normalized to create a resem-
blance matrix based on Euclidean Distance. Principal
component analysis (PCA) plots were then created for
vegetation and soil. From the resemblance matrix, an
analysis of similarity (ANOSIM) test was conducted
to compare differences among stand ages.
To test the relationship between the soil and
mangrove vegetation, a stepwise multiple regression
analyses were applied to a correlation matrix. The
BEST-BIOENV procedure was used to compare
the rank-similarity matrices for the soil with matrices
created from the vegetation variables on 999
permutations. We used the R Statistical Software
(R Development Core Team, 2012) for ANOVAs and
correlation analyses, while PRIMER (version 6;
Clarke & Gorley, 2006) was used for multivariate
tests.
Results
Vegetation structure and biomass
As mangrove forests aged, the tree size (diameter and
height; Fig. 2), LAI (Fig. 3A), and AGB (Fig. 3C)
increased logarithmically while tree density decreased
(Fig. 3B). The smallest diameter (2.20 ± 0.20 cm)
and shortest tree height (2.0 ± 0.45 m) were observed
in the youngest plantation, which steadily increased as
stand age increased. Such patterns tended to stabilize
in the 18-year stands (diameter: 9.31 ± 0.91 cm;
height: 10.53 ± 1.05 m). Maximum sizes were mea-
sured from the natural mangroves with tree diameter
of 12.03 ± 1.81 cm and tree height of 11.10 ±
0.60 m (Fig. 2). Seedlings were observed only in the
50-year-old plantation (of the species R. mucronata)
and natural mangroves (composed of R. mucronata,
Avicennia marina, Bruguiera gymnorrhiza, and Son-
neratia sp.). The seedling abundance was significantly
higher in the 50-year-old plantation (20 ± 2 seedlings
0
5
10
15
0.00 0.05
Diameter, m
Hei
ght,
m
0.10 0.15
Fig. 2 Tree diameter and height distribution in planted and
natural mangroves (n = 30 per stand). The younger mangroves
(6- and 8-year) have homogenous size distribution, which
tended to become more variable as plantation matures. Legend:
unfilled circle (6-year), filled circle (8-year), unfilled triangle
(10-year), filled triangle (11-year), unfilled diamond (12-year),
filled diamond (17-year), unfilled rectangle (18-year), filled
rectangle (50-year), and x, *, ? (natural mangroves Nx, Ny, and
Nz of unknown age, respectively)
6 Hydrobiologia (2013) 720:1–18
123
100 m-2) compared with the three natural mangrove
stands which had similar abundance of 12 ± 3
seedlings 100 m-2.
The rate of tree diameter increment was highest in the
youngest plantation (6-year; 0.77 ± 0.02 cm year-1),
slowed as age increased (8- to 12-year-old plantations),
and was almost constant in the 17- and 18-year-old
plantations (0.20–0.22 cm year-1; Table 2). Similarly,
the rate of tree height increment was high in the younger
plantations (0.35 ± 0.01 m year-1), and slowed at
10- to 12-year-old until it became almost constant in
the 18-year plantations (0.03 ± 0.00 m year-1;
Table 2). The 6-, 8-, 10-, and 11-year-old plantations
had significantly higher rates in both diameter and
height increment compared to the 12- and 17-year
stands, and the 18-year, 50-year, and natural stands.
The LAI (R2 = 0.74; P \ 0.001; q = 0.76;
Fig. 3A) was positively correlated, while tree density
(R2 = 0.56; P \ 0.001; Fig. 3B) was negatively cor-
related (q = -0.52), with age of mangrove stands.
Lowest LAI values were recorded in the youngest
plantation and LAI steadily increased as stand age
increased. The rate of increases in LAI (0.24 ±
0.01 m2 m-2 year-1; Appendix Table 1a in Elec-
tronic Supplementary Material) was higher in B10-
year-old plantations compared to[11-year-old stands
(LAI: 0.09 ± 0.02 m2 m-2 year-1). The natural
stands had almost constant LAI (-0.04 ±
0.03 m2 m-2 year-1) over the study period.
The AGB was positively correlated with age of
mangrove stands (R2 = 0.89; P \ 0.001; q = 0.79;
Fig. 3C). Lowest AGB value was recorded in the
youngest plantation and AGB steadily increased as
stand age increased. The rate of increases in AGB
(9.27 ± 0.99 T ha-1 year-1; Appendix Table 1c in
Electronic Supplementary Material) was higher in
Naturalmangroves,
unknown age
0
2
4
6
0
2,000
4,000
6,000
8,000
10,000
0
50
100
150
200
0 10 20 30 40 50
LA
I,m
2m
-2
Tre
eD
ensi
ty,
nha
-1A
bove
-Gro
und
Bio
mas
s,t h
a- 1
Stand Age, yr
A
B
C
Fig. 3 Changes in A Leaf Area Index (LAI), B tree density, and
C aboveground biomass (AGB) with mangrove stand age. There
were significant relationships in LAI, tree density, and AGB
with mangrove stand age and were expressed in the equations
Y = 1.86 ln(x) - 2.32 (r2 = 0.74), Y = -1,828 ln(x) ? 7,722;
(r2 = 0.56), and Y = 62.35 ln(x) - 97.76 (r2 = 0.89),
respectively
Table 2 Differences in rates of tree diameter and height
increment (mean ± standard deviation; n = 30 per stand age)
with age of mangrove stands
Stand age (years) Diameter
(cm year-1)
Height (m year-1)
6 0.77 ± 0.02a 0.23 ± 0.01a
8 0.57 ± 0.02b 0.35 ± 0.01a
10 0.43 ± 0.04c 0.26 ± 0.00a
11 0.41 ± 0.02c 0.25 ± 0.01a
12 0.37 ± 0.02c 0.16 ± 0.01b
17 0.22 ± 0.01d 0.12 ± 0.01b
18 0.20 ± 0.01d 0.03 ± 0.00c
50 0.21 ± 0.01d 0.01 ± 0.00c
Natural (unknown age) 0.21 ± 0.02d 0.01 ± 0.00c
df 8 8
MS treatment 0.13 0.05
MS residual 0.00 0.00
F ratio 294.2 645.9
P *** ***
Different letters between age groups denote significant
difference between stand ages. Significance at *** P \ 0.001
Hydrobiologia (2013) 720:1–18 7
123
B10-year-old plantations compared to [11-year-old
stands (AGB: 7.71 ± 0.57 T ha-1 year-1). The nat-
ural stands had almost constant AGB
(0.55 ± 0.18 T ha-1 year-1) over the study period.
The tree density declined with age of the stands.
Among stands, only the youngest plantation had
significant variation in tree density with time
(930 ± 206 stems ha-1 year-1; Appendix Table 1b in
Electronic Supplementary Material). Older stands had
slower rates of change in tree density over the sampling
periods (8- to 12-year stands, mean of 332 ± 74 stems
ha-1 year-1), and tree density was relatively stable in
the plantations[12-year and natural mangrove forests
(mean loss of 58 ± 43 stems ha-1 year-1).
Soil characteristics
As mangrove forests aged, the OM, TN, AP, and redox
potential of soils increased logarithmically while soil
temperature decreased (Fig. 4). There was no correla-
tion between the age of mangrove stands and grain size
(sand and silt), salinity, and pH. Low OM values were
observed from \10-year-old stands (P6 = 1.02 ±
0.15%; P8 = 1.49 ± 0.13%) and increased in 10- to
12-year stands (mean = 5.39 ± 0.78%). The rates of
change in OM were 0.20 ± 0.06% year-1 in 6- and
8-year stands, which peaked in the 12-year stands
(0.46 ± 0.09% year-1) and was lower in mature
plantations (0.10 ± 0.01% year-1) and natural man-
groves (0.07 ± 0.01% year-1).
Low TN and AP values were measured from the 6-
and 8-year stands (TN: 0.04 ± 0.004%; AP: 9.65 ±
1.39 ppm), which slightly increased in 10- to 12-year
stands (TN: 0.07 ± 0.009%; AP: 21.58 ± 1.99 ppm),
and in 17-, 18-, and 50-year stands (TN 0.09 ± 0.007%;
AP: 21.96 ± 1.35 ppm), and was highest in the natural
stands (TN: 0.18 ± 0.01%; AP: 24.86 ± 2.60 ppm).
There were no significant variations in TN and AP over
the course of the study in any of the stands (P [ 0.05).
The redox potential of soils was significantly
correlated with mangrove stand age (q = 0.67; P \0.001; Fig. 4E). The young plantations had more
anoxic soils (6- and 8-year; mean: -26.83 ± 3.08 mV),
slightly oxidized in 10- to 12-year stands (mean:
4.59 ± 1.78 mV), and more oxidized in mature stands
(mean: 17.63 ± 2.01 mV) and natural stands (mean:
26.67 ± 3.04 mV). There were no significant differ-
ences in redox potential over the course of the study in
0
50
100
0
5
10
15
0.00
0.05
0.10
0.15
0.20
0
10
20
30
40
-40
-20
0
20
40
20
25
30
35
40
0 10 20 30 40 50
silt sand
OM
,%
Tota
lN,
%A
vail.
P,pp
mR
edox
Pote
ntia
l,m
VT
empe
ratu
re, °
CG
rain
Siz
e,%
Stand Age, yr Naturalmangroves,
unknown age
A
B
C
D
E
F
Fig. 4 Changes in A grain size (sand and silt content),
B organic matter (OM), C total nitrogen (TN), D available
phosphorus (AP), E redox, and F temperature with mangrove
stand age. There were no correlations between grain size,
salinity, and pH with mangrove age. There were significant
relationships in organic matter, TN, AP, redox, and temperature
with mangrove stand age and were expressed in the equations
Y = 4.276 ln(x) - 5.804 (r2 = 0.83), Y = 0.067 ln(x) - 0.103
(r2 = 0.82), Y = 7.727 ln(x) ? 0.22 (r2 = 0.55), Y = 18.287
ln(x) - 46.343 (r2 = 0.57), and Y = -1.79 ln(x) ? 36.403
(r2 = 0.62), respectively
8 Hydrobiologia (2013) 720:1–18
123
any of the stands (Appendix Table 2h in Electronic
Supplementary Material).
Soil temperature was warmest in the youngest
plantation (36.10 ± 1.00�C) and coolest in the natural
mangrove stands (28.87 ± 0.09�C). The soil tempera-
ture in 11- and 12-year stands (31.05 ± 0.19�C)
appeared to be almost similar with the more mature plan-
tations (30.48 ± 0.12�C) and natural stands (30.28 ±
0.38�C). Changes in soil temperature through time were
more apparent in young stands (6-, 8-, and 10-year;
mean: -1.50 ± 0.22�C year-1) compared to the rela-
tively more stable rates in mature plantations ([10-year;
mean: -0.008 ± 0.004�C year-1) and natural man-
grove stands (mean: -0.003 ± 0.001�C year-1;
Appendix Table 2i in Electronic Supplementary
Material).
Vegetation and soil development patterns
There was a clear trajectory pattern in forest vegeta-
tion development with age of the mangrove stands
(Fig. 5A). The PCA plot showed four major stand age
groupings: 6- and 8-year (group 1), 10-, 11-, and
12-year (group 2), and 17-, 18-, and 50-year (group 3),
and natural mangroves (group 4). The PC1 and PC2
accounted for 81.5 and 10.3% of the variation where
AGB (0.54) and number of seedlings (0.86) had the
highest correlation coefficients in PC1 and PC2,
respectively. Each age group was significantly differ-
ent from each other as revealed by the ANOSIM test
(Global R = 0.87; P \ 0.001).
There was also a progression of changes in soil
characteristics with age of the stands (Fig. 5B). In the
PCA plot, PC1 and PC2 accounted for 71.6 and 14.7%
of the variation where OM (0.42) and silt (0.69)
contents had the highest correlation coefficients in
PC1 and PC2, respectively. Similar groupings in the
vegetation were also observed in the PCA soil plots: 6-
and 8-year (group 1), 10-, 11-, and 12-year (group 2),
17-, 18-, and 50-year (group 3), and natural mangroves
(group 4). Each group was significantly different from
each other (ANOSIM test; Global R = 0.66;
P \ 0.001).
The BIOENV test revealed significant relationship
between the mangrove vegetation and soil character-
istics (q = 0.70; P \ 0.001). The combination of soil
OM, N, redox potential, and soil temperature had the
highest correlation coefficients (0.69). Similarly, the
mangrove vegetation was significantly correlated with
the soil characteristics (q = 0.65; P \ 0.001) where
LAI and AGB had the highest correlation (q = 0.63).
Discussion
The growth and development of restored mangrove
stands reported in our study followed typical patterns
in the structure of terrestrial forest communities
through time (referred to as forest stand dynamics
and gap-phase dynamics; sensu Oliver & Larson,
1996) and for mangroves (Fromard et al., 1998;
Alongi, 2009). Even-aged monospecific mangrove
plantations with initially homogenous tree sizes
Fig. 5 PCA plots of A vegetation and B soil patterns in
different mangrove stand ages. Four distinct groupings can be
inferred and classified based on age and development stage of
the stands as: young (6- and 8-year), intermediate (10-, 11-, and
12-year), mature (17-, 18-, and 50-year), and natural stands. The
planted stands are referred to as the restored system whereas the
natural stands are referred to as the reference system, which
represents the proxy endpoint of restoration. Stand age legend
same as Fig. 2. Legend: dashed ellipse grouping per stand age,
solid ellipse grouping per development stage
Hydrobiologia (2013) 720:1–18 9
123
follow development patterns similar to those
described in classical literature of forest stand dynam-
ics where stands undergo colonization, early develop-
ment, maturity, and senescence (see for example
reviews in Guariguata & Ostertag, 2001; Chazdon,
2003). During the initial growing period, the growth of
individual trees appeared to be synchronized until
tree-to-tree competition and self-thinning occurs,
resulting in variation in tree size. Similarly, the
attainment of soil maturity (through the accumulation
of organic matter) along with vegetation development
with increasing age of the stands has been reported in
other tropical forests (Chazdon, 2003) and more
recently in restored mangroves in Florida, USA
(Osland et al., 2012). Substantial changes in forest
communities and soils occur early in the ecosystem
development stage of mangrove plantations similar to
the forest development dynamics proposed by Kellner
et al. (2011).
Our study showed a clear trajectory of mangrove
forest and soil development patterns from a series of
progressing ages of planted mangroves. Despite a
wide range of plots spread over a large area of the
Philippines, the LAI, tree density, and AGB in the
vegetation, and the soil OM, N, P, redox potential, and
temperature in the soils showed a clear trajectory of
development with forest age. There were clear patterns
of increases in the LAI, AGB, soil OM, TN, AP, and
redox potential, and decreases in tree density and soil
temperature with stand age. These parameters stabi-
lized at the 11th year indicating the probable age that
the recovery trajectory tends toward forest maturity.
From the PCA plots (Fig. 5A, B), three distinct
groupings can be inferred and classified based on the
development stage of the restored stands, as: group 1
(young stands: \10-year), group 2 (intermediate
stands: 10- to 17-year), and group 3 (mature stands:
[17-year). The vegetation and soil patterns in 17-,
18-, and 50-year stands are comparable with that of the
reference system indicating that at 17 years, the
restored system may achieve vegetation and soil
maturity that is comparable to the vegetation and soil
characteristics of the reference system (natural
stands).
In younger plantations (e.g.,\11-year), mangroves
have homogenous tree sizes (in terms of tree diameter
and height; Fig. 2) and have high density. Homoge-
nous tree sizes are commonly observed in young tree
plantations where planted seedlings are not yet
exposed to strong competition (see for example Niklas
et al., 2003). But as planted mangroves grow (in this
case [11-year), space and light for tree growth
becomes less available. At this time, tree competition
slows growth rates and paves way for self-thinning and
size variability (Analuddin et al., 2009). The rapid
decline in tree density in young plantations is due to
high mortality rates, which are common in most
mangrove planting projects in the country (Primavera
& Esteban, 2008). In the Philippines, seedling survival
is very low (10–40%; Samson & Rollon, 2008).
Nonetheless, the decline in tree density with mangrove
stand age was similar to published tree density values
from other planted and natural Rhizophora mangroves
in SE Asia (Table 3).
The forest canopies in the younger plantations are
still open and started to close only at the 10th year. The
LAIs of young plantations were still low. Forest gap
filling (sensu Duke, 2001) in a regenerating canopy is
initially slow in 6- to 8-year stands then peaked in
10-year stands. In the 10-year-old stands, the LAI
started to increase. Older plantations (e.g.,[11 years)
and natural mangroves had full canopy cover with LAI
ranging from 4.13 to 4.54 m2 m-2. The gap filling
process with stand age observed in this study is
consistent with the forest canopy regeneration concept
of Duke (2001) who proposed that gap filling in a
regenerating forest can be completed in 10 years. Our
values for LAI in developing forests are similar to
published LAI values from other planted and natural
Rhizophora mangroves in the region despite differ-
ences in methods used (Table 4).
The AGB exponentially increased with stand age
(Fig. 3C) showing a clear development pattern from
young to intermediate stands and then through the
mature stands. Young plantations initially have low
AGB but rapidly increased in 12-year-old stands and
then tend to asymptote beginning at the 17th year.
Thus, it will take at least 18 years for the planted
mangroves to approach the biomass of the reference
natural mangroves used in this study. However, the
AGB reported here for the 50-year and natural
mangrove stands (130–150 T ha-1) are relatively
low and approximately half of AGB values in
published reports for other natural mangroves in SE
Asian countries (Komiyama et al., 2008; Table 5).
This may be a consequence of the Philippine man-
groves being frequently exposed to disturbances such
as typhoons which may constrain mangroves from
10 Hydrobiologia (2013) 720:1–18
123
Table 3 Tree density among planted mangroves of different ages and natural mangroves (unknown ages)
Location Species Age Tree density, n (ha-1) References
Lingayen Gulf, Philippines R. mucronata 6 7,780 This study
Central Java, Indonesia R. mucronata 7 3,287 Sukardjo & Yamada (1992)
Can Gio, Vietnam R. apiculata 8 6,450 Hong (1996)
Lingayen Gulf, Philippines R. mucronata 8 4,244 This study
Can Gio, Vietnam R. apiculata 10 5,200 Hong (1996)
Matang, Malaysia R. apiculata 10 3,000 Chan (1996)
Lingayen Gulf, Philippines R. mucronata 10 2,387 This study
Lingayen Gulf, Philippines R. mucronata 11 1,886 This study
Trat, Thailand R. apiculata 12 2,900 Ishii & Tateda (2004)
Kalibo, Philippines R. mucronata 12 2,122 This study
Can Gio, Vietnam R. apiculata 15 3,950 Hong (1996)
Kalibo, Philippines R. mucronata 17 1,532 This study
Lingayen Gulf, Philippines R. mucronata 18 1,358 This study
Matang, Malaysia R. apiculata 20 1,560 Chan (1996)
Matang, Malaysia R. apiculata 22 3,000 Clough et al. (1997)
Matang, Malaysia R. apiculata 30 940 Chan (1996)
Bohol, Philippines R. mucronata 50 1,231 This study
Ranong, Thailand R. apiculata Natural 1,777 Imai et al. (2006)
Zambales, Philippines R. mucronata Natural 1,499 This study
Bohol, Philippines R. mucronata Natural 1,442 This study
Ranong, Thailand R. apiculata Natural 1,351 Tamai & Iampa (1988)
Table 4 LAI among planted Rhizophora mangroves of different ages and natural mangroves (unknown ages)
Location Species Age LAI (m2 m-2) Method References
Lingayen Gulf, Philippines R. mucronata 6 0.15 CI-110 Canopy Imager This study
Lingayen Gulf, Philippines R. mucronata 8 0.29 CI-110 Canopy Imager This study
Lingayen Gulf, Philippines R. mucronata 10 2.00 CI-110 Canopy Imager This study
Lingayen Gulf, Philippines R. mucronata 11 2.80 CI-110 Canopy Imager This study
Kalibo, Philippines R. mucronata 12 2.81 CI-110 Canopy Imager This study
Mekong, Vietnam R. apiculata 5–12 3.3–4.9 LAI-2000 Clough et al. (2000)
Trat, Thailand R. mucronata 6–12 4.1–5.5 LAI-2000 Ishii & Tateda (2004)
Kalibo, Philippines R. mucronata 17 3.91 CI-110 Canopy Imager This study
Lingayen Gulf, Philippines R. mucronata 18 4.13 CI-110 Canopy Imager This study
Matang, Malaysia R. apiculata 22 5.10 LAI-2000 Clough et al. (1997)
Bohol, Philippines R. mucronata 50 4.54 CI-110 Canopy Imager This study
Hinchinbrook Is., Australia R. apiculata Natural 3.10 LAI-2000 Clough (1998)
Bohol, Philippines R. mucronata Natural 4.50 CI-110 Canopy Imager This study
Zambales, Philippines R. mucronata Natural 4.51 CI-110 Canopy Imager This study
SW Florida, USA R. mangle Natural 3.90 Remote Sensing Ramsey and Jensen (1996)
British West Indies R. apiculata Natural 4.00 Remote Sensing Green et al. (1997)
SE Florida, USA R. mangle Natural 4.30 LI-COR LI-190SA Araujo et al. (1997)
Hydrobiologia (2013) 720:1–18 11
123
attaining taller and larger diameter trees. Nonetheless,
planted mangroves at 18th year can have biomass of
115 T ha-1. Assuming that 50% of forest biomass is
composed of carbon (see for example Masera et al.,
2003), the gain in AGB of planted mangroves can
positively contribute to carbon sequestration with at
least 55–60 T C ha-1 gained over the 18 years of
forest growth.
Although structurally mature, a critical component
that is conspicuously missing in the 17- and 18-year-
old plantations are seedling and sapling recruits. The
abundance of seedlings is important in forest regen-
eration should a disturbance occur (Baldwin et al.,
2001; Milbrandt et al., 2006). However, there are no
seedling recruits observed up to the 18-year-old
stands, possibly because conditions are not yet favor-
able for recruitment (for example low propagule
supply). Forest canopies of these stands are noticeably
more closed and dense, limiting the available light and
space needed for the recruitment and growth of
seedlings (Salmo & Duke, 2010). This finding con-
trasts with propositions of facilitated seedling recruit-
ment in rehabilitated mangroves as observed in Gazi
Bay, Kenya (Bosire et al., 2003) and in Leizhou Bay,
China (Ren et al., 2008). The combination of relatively
low AGB (Table 5) and the absence of seedling
recruits may be considered indicative of immaturity in
18-year-old stands.
Results from the BIOENV tests reveal that as
mangrove stands mature, the vegetation also facilitates
the development of the soil similar to the proposition
of Alongi (2009). The relationship between mangrove
vegetation and soil characteristics has been similarly
reported in previous studies, which suggest linkage of
vegetation structure with redox potential (Sherman
et al., 1998; Rivera-Monroy et al., 2004) and nutrient
availability, particularly nitrogen and phosphorus
(Boto & Wellington, 1984; Ukpong, 1994). The effect
of developing forests in reducing soil temperature can
be explained by the development of mangrove canopy
cover that provides shading and thus regulates
absorption of solar radiation (Bosire et al., 2005;
Tolhurst & Chapman, 2007). The relationship of soil
N, P, and redox potential with stand age is likely
caused by the growth of roots, enhancement of litter
degradation, organic matter decomposition, and nutri-
ent regeneration (Bosire et al., 2005).
There was a clear progression of change in soil
characteristics with age of the stands (Fig. 5B) similar
to that observed in the study reported from Leizhou
Bay, China (Ren et al., 2008). The role of mangrove
vegetation in facilitating soil maturity was emphasized
by Alongi (2009) who proposed that maturity is
attained through the accumulation of organic matter
and nutrients particularly nitrogen and phosphorus.
Planted mangroves effectively contribute to nutrient
Table 5 AGB among planted Rhizophora mangroves of different ages and natural mangroves (unknown ages)
Location Species Age AGB (T ha-1) References
Lingayen Gulf, Philippines R. mucronata 6 13.58 This study
Lingayen Gulf, Philippines R. mucronata 8 18.21 This study
Lingayen Gulf, Philippines R. mucronata 10 38.45 This study
Lingayen Gulf, Philippines R. mucronata 11 43.29 This study
Kalibo, Philippines R. mucronata 12 51.43 This study
Kalibo, Philippines R. mucronata 17 101.80 This study
Lingayen Gulf, Philippines R. mucronata 18 115.62 This study
Matang, Malaysia R. apiculata 28 211.80 Ong et al. (1982)
Bohol, Philippines R. mucronata 50 132.18 This study
Matang, Malaysia R. apiculata [80 460.00 Putz and Chan (1986)
Bohol, Philippines R. mucronata Natural 147.60 This study
Zambales, Philippines R. mucronata Natural 150.66 This study
Halmahera, Indonesia R. apiculata Natural 216.80 Komiyama et al. (1988)
S Ranong, Thailand Rhizophora spp. Natural 281.20 Komiyama et al. (1987)
Ranong, Thailand Rhizophora spp. Natural 298.50 Komiyama et al. (1987)
12 Hydrobiologia (2013) 720:1–18
123
enrichment of soils, as well as increasing the redox
potential because of the enhancement of litter degra-
dation and organic matter decomposition (Bosire
et al., 2005). Among soil parameters however, the
most significant contribution of planted mangroves
was the accumulation of soil organic matter. The
18-year-old stands have 8.00 ± 0.89% OM equivalent
to 4.65 ± 0.52% organic carbon. This effectively
translates into a soil carbon stock amounting to
58.59 ± 1.65 T C ha-1 (in the top 10 cm of soil)
confirming the proposition that mangroves store vast
amount of carbon in the soil. Our data indicate that
mangrove rehabilitation programs may play a signif-
icant role in climate change adaptation and mitigation
strategies (Donato et al., 2011; Bouillon, 2011).
Similar to the patterns observed in the vegetation,
the soil characteristic in younger stands significantly
changed over time. In contrast, the soil in 50-year and
natural mangrove stands were comparable and less
variable over the sampling periods, which imply that
soil development continues for stands up to 20 years
but stabilizes thereafter. Thus, there appears to be a lag
period in soil development that follows the above-
ground vegetation (which stabilized as early as on the
11th year). Similar development of soil characteristics
among age and stand classes has been observed in the
studies of 8-year-old Rhizophora and Sonneratia
plantations in Gazi Bay, Kenya (Bosire et al., 2005),
natural Avicennia stands of Auckland, New Zealand
(Morissey et al., 2003; Lovelock et al., 2010), and
restored mangroves in Florida, USA (Osland et al.,
2012). In our study, planted mangroves clearly
modified soil conditions, particularly by increasing
OM content as stands develop. We found that while
10–12 years is sufficient for recovery of AGB,
20–25 years is needed for soils to reach a state that
is similar to natural forests.
Restoration trajectories and indicators
In an attempt to increase the number of guidelines for
restoration of mangroves in the region (see for
example Ellison, 2000; Bosire et al., 2008), we
identified vegetation and soil variables that could
serve as potential restoration indicators (sensu SER,
2004). Following approaches from some published
restoration studies, we detected changes and inferred
patterns of changes in the restored system (De Boer,
1983; SER, 2004; Weilhoefer, 2010). The patterns of
changes for each parameter were compared graphi-
cally to show temporal changes and compare the
patterns from restored system relative to that of a
reference system as a proxy endpoint of restoration
trajectory (cf. Morgan & Short, 2002; Nichols &
Nichols, 2003; Ruiz-Jaen & Aide, 2005).
The clear progression of patterns and significant
correlation of vegetation parameters (LAI, tree density
and biomass, seedling and sapling recruits, growth
rate) with age of mangrove stands obviously qualify as
restoration indicators. Clearly at 50 years, the planted
mangroves have the vegetation characteristics that are
similar to natural mangroves. But even before
50 years, the vegetation structure and biomass of the
17- and 18-year-old plantations were already compa-
rable with the mature and natural stands (although the
presence of seedling recruits was not). While there
have been speculations that it will take 20 years for
planted mangroves to fully mature (Colonello &
Medina, 1998; Twilley et al., 1998; McKee &
Faulkner, 2000), empirical data to prove such claims
are lacking. Jimenez et al. (1985) proposed that
maturity is reached when the growth rate of trees
slow down relative to stand age. In this study, growth
rate slows in the 11th year (which is 2 years earlier
compared with the planted mangroves in Thailand;
Aksornkoae, 1996) but is more apparent in the 17- and
18-year-old plantations indicating that mature stages
of forest development in the region are reached in
17 years.
Setting indicators to evaluate soil maturity is
difficult because many processes are interlinked and
there are fluctuating inputs occurring in the coastal soil
environment. Unlike the vegetation component where
most variables can be easily assessed (i.e., tree
diameter and biomass), soil variables are affected by
inherent site-specific conditions that may or may not
be related with the age of mangrove stands. Among the
factors influencing soils are tidal inundation (McKee,
1993), erosion and deposition (Chen & Twilley, 1999;
Saenger, 2002), and geomorphology and rainfall
patterns (Alongi, 2009). The high sensitivity of soils
to environmental variation may be the reason why
when recommending indicators for assessing impacts
of mangrove restoration, Ellison (2000) suggested that
only nutrient export and hydrologic patterns were
suitable indicators. In this study however, we have
found that some soil parameters may serve as resto-
ration indicators.
Hydrobiologia (2013) 720:1–18 13
123
From the measured variables over stands of different
ages and using comparison with natural sites, we found
that OM (Fig. 4B) and N (Fig. 4C) contents were
significantly correlated with forest age. The accumula-
tion of OM in soils can be attributed to the increases in
foliage density and related belowground root expansion
with stand age (which is correlated with LAI from
BEST-BIOENV results) that leads to the rapid deposi-
tion of litter and organic detritus in the soil (see for
example Saenger, 2002; Morissey et al., 2003; McKee,
2010). The significant correlation of mangrove vegeta-
tion with OM is similar to the findings of Alongi (2009;
Fig. 6) and Osland et al. (2012). Moreover, Cardona &
Botero (1998) proposed that the large pool of OM might
also facilitate nutrient enhancement as well as other
variables such as amelioration of redox potential. There
was also a clear separation between the young and
intermediate stands, and the mature and natural stands in
terms of phosphorus, redox potential, and soil temper-
ature which may also serve as potentially useful
restoration indicators. Variation in site-specific condi-
tions may limit the use of soil characteristics as
indicators, but in many cases soil characteristics may
provide a measure of ecosystem maturity that is directly
related to their function and value.
Conclusion
We used a SFT substitution approach to identify
patterns of trajectory for mangrove vegetation and soil
development in the Philippines. Such opportunistic
sampling may not be necessarily optimal (in compar-
ison with the before vs. after and control vs. impacted
approach typical in ecological studies; cf. Green,
1979), however, we were able to document changes in
vegetation and soil patterns within the current age
range of planted mangroves over a range of sites. From
the observed restoration trajectory patterns, this study
shows that the planted mangrove can match the
vegetation and soil characteristics of a mature, natural
mangrove forests. The vegetation development of
planted mangroves can be classified as young (\8-
year), intermediate (10- to 12-year), and mature ([17-
year) stands. Rapid growth rate occurred at the
youngest plantation, slowed in the 11th year, and
becomes relatively constant as they approach matu-
rity. The time to reach forest maturity is estimated at
25 years. There was a clear progression in soil OM, N,
P, redox potential, and temperature among planted
mangroves of different developmental stages (from
young to intermediate, mature, and natural stands)
leading toward soil maturity (sensu Alongi, 2009). The
changes in mangrove vegetation, primarily LAI, had
significant relationship with the changes in soil
characteristics. In addition to vegetation parameters,
we propose that the changes in soil OM, N, P, redox
potential, and soil temperature with mangrove stand
age can be used as indicators in evaluating the progress
or success of mangrove restoration programs.
Acknowledgments We are grateful to Ford Foundation-
International Fellowship Program (FORD-IFP) and
Fig. 6 Comparison of
changes in organic matter
(OM) content with stand
ages. Unfilled circle (this
study; Y = 4.456 ln(x) -
6.543; r2 = 0.75); filled
circle (extrapolated from
Alongi, 2009; Y = 6.098
ln(x) - 3.917; r2 = 0.72).
Dashed regression line
denotes combined data from
this study and Alongi
(2009); Y = 5.299 ln(x) -
5.209; r2 = 0.67
14 Hydrobiologia (2013) 720:1–18
123
International Foundation for Science (IFS; D/4667-1) for
providing financial assistance throughout the study period; the
University of Queensland Research Scholarship Grant for
providing financial support to SS; the Local Government
Units and mangrove managers; and Jack Rengel and Tommy
Conzaga for assisting in the field sampling.
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