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: ssalmo@ateneo.edu

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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