Hydrobiologia
DOI 10.1007/s10750-013-1766-4
BIODIVERSITY IN ASIAN COASTAL WATERS
Assessment of vegetation and soil conditions in restored
mangroves interrupted by severe tropical typhoon
‘Chan-hom’ in the Philippines
Severino G. Salmo III • Catherine E. Lovelock
Norman C. Duke
Received: 1 March 2013 / Accepted: 23 November 2013
Ó Springer Science+Business Media Dordrecht 2013
Abstract Using a space-for-time substitution
approach, we investigated the effects of a typhoon
on the vegetation and soil development trajectories
of monospecific stands of Rhizophora mucronata
mangroves of different ages (6-, 8- 10-, 11-, 12-, 17-,
18- and 50-year stands). The vegetation and soil
parameters were compared to a reference system
comprised of mature, natural mangrove stands. Pre-
typhoon measures of vegetation and soil parameters
were compared with 1-mo, 7-mo and 9-mo post-
typhoon. Prior to the occurrence of the typhoon,
there were clear patterns of vegetation and soil
development with age of the stands. The
Guest editors: M. Tokeshi & H. T. Yap / Biodiversity in
Changing Coastal Waters of Tropical and Subtropical Asia
S. G. Salmo III (&)
Department of Environmental Science, Ateneo de Manila
University, 1108 Quezon City, Philippines
e-mail: ssalmo@ateneo.edu
S. G. Salmo III  C. E. 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,
Science City of Munoz 3120, Nueva Ecija, Philippines
N. C. Duke
Centre for Tropical Water and Aquatic Ecosystem
Research, James Cook University, Townsville,
QLD 4811, Australia
•
development trajectory was however interrupted
by the occurrence of the typhoon. Severe damage
was more apparent in older mangrove stands (11-
and 18- year stands) with very low to no damage in
the younger stands. The typhoon-impacted sites
experienced a number of changes, including: com-
plete defoliation; reduced living tree densities of
61–69 %; decreased above-ground biomass of
70–79 %; increased soil nutrient levels of
40–60 %; more waterlogged soils by at least
113 % and increased soil temperature of 8–10 °C.
Cumulative tree mortality, compounded by the lack
of seedling recruits and unfavourable soil condi-
tions may limit long-term recovery of the typhoon-
impacted stands.
Keywords Mangroves  Restoration 
Rhizophora mucronata  Typhoon damage 
Post-typhoon recovery  Philippines
Introduction
Mangrove rehabilitation programmes have been
implemented to increase forest cover and restore the
ecosystem functionality of mangrove forests of the
tropical coasts (Fortes, 1995; Kaly & Jones, 1998;
Field, 1999; Katon et al., 2000; Barbier, 2006). Many
of these planted mangroves are mono-specific (Walt-
ers, 2004; Lewis, 2005) with stunted growth and poor
survival (Samson & Rollon, 2008) raising doubts as to
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whether these plantations effectively restore ecosys-
tem functionality. Unfortunately, monitoring activi-
ties are rarely undertaken to document the success (or
failure) of these planting programmes (Ellison, 2000).
While some researchers estimated that planted man-
groves may approach the biomass, stand structure and
productivity of natural forests within two decades (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 success of mangrove
planting programmes is the rate and time at which a
stand attains the forest structure and biomass of a
mature, natural mangroves (cf. Ellison, 2000).
The role of soil characteristics in influencing the
establishment and growth of mangrove forest has been
reported in several studies (Boto & Wellington, 1984;
Thom, 1987; Clarke, 1995; Cohen et al., 1999 among
others). Predictable changes in soil characteristics may
be expected as mangrove forest age increases (Alongi,
2009). Boto (1984) proposed that soil parameters are the
most important factors that have direct influence on
forest stands, providing essential nutrients for growth,
the physical structure for anchorage and stability and
substrate for a wide range of fauna. Aside from nutrients,
other soil parameters that may affect mangrove growth
are soil grain size, salinity, redox and temperature
(Pernetta, 1993; Feller, 1995; McKee, 1995; Chen &
Twilley, 1998; Duarte et al., 1998). Most mangrove
restoration programmes 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 known stresses (i.e. being
periodically inundated and drained, with rapid, daily
fluctuations in desiccation, salinity and temperature).
The growth and survival of the planted mangroves will
therefore be affected by the soil characteristics prevail-
ing in a given locality. Additionally, the development of
soil maturity (sensu Alongi, 2009) may also be related to
the development of mangrove vegetation.
The inter-relationship between mangrove vegetation
and soil characteristics was proposed by Ukpong (1994)
to be similar to that observed in tropical terrestrial forests
(Vitousek & Reiners, 1975; Hooper & Vitousek, 1997).
As vegetation structure and productivity increases with
mangrove age, the production of litter and organic
detritus production also increases. These materials are
deposited in the forest floor, and after degradation and
mineralization, facilitate the enhancement and
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Hydrobiologia
accumulation of organic matter. The large organic matter
content in mangroves has been proposed to exert a strong
influence on nutrient regeneration as well as other factors
such as redox potential of soils (Cardona & Botero,
1998).
Mangroves are vulnerable to typhoons because of
their position in the coastal zone (Hogarth, 2007). The
frequency and severity of typhoon shapes the popula-
tion structure and forest dynamics of mangroves that
could define their resilience, survival and regeneration
patterns over longer periods (Ellison & Farnsworth,
1996; Cahoon et al., 2003). Most studies of the effects
of intense storms on mangroves are from the Caribbean
region (although see Smith et al., 2009). There are very
few reports of typhoon effects on mangroves from SE
Asia where typhoons are prevalent. While it is likely
that planted mangroves may show similar develop-
mental trajectory patterns as natural mangroves (e.g.
Fromard et al., 1998; Alongi, 2009), it is not clear if
planted mangroves will have the same rate of forest
recovery as natural mangroves if they are disturbed.
The low biodiversity of planted mangroves (often
mono-cultures) and less well-developed soils may
result in delayed recovery compared to natural forests.
The Philippines is a tropical archipelagic country
known as one of the most disaster-prone country in the
world (Gaillard et al., 2007). An average of 20
typhoons per year visits the country (Velasco &
Cabanilla, 2003). In the last 30 years, the number of
typhoons has increased. Such increased frequency
appears to be associated with increases in sea-surface
temperatures (Webster et al., 2005). With prevailing
climate change, several simulations suggest that the
frequency of typhoons would decrease, but their
severity may increase (Kubota & Chan, 2009). The
occurrence of high intensity typhoons in the Philip-
pines threaten the growth, development and regener-
ation of both planted and natural mangroves.
Studies of the restoration ecology and post-distur-
bance regeneration in mangroves are rare because, in
most cases, a reference system within restored sites is
absent (Cairns & Heckman, 1996) or each planted
mangrove stand has a different management system.
Fortunately, in Lingayen Gulf, northwestern Philip-
pines, planted monospecific Rhizophora mangroves of
known different ages (6-, 8-, 10-, 11- and 18-year old
plantations) exist, with comparable planting and man-
agement systems (e.g. similar species, planting density
and planting location), thus providing a rare opportunity
 Table 1 Biological and physical description of the study sites (modified from Salmo III et al., 2013)
Stand Location Study Biological Physical
age/ area
stage (ha) Species Tree density Above-ground Tree height, DBH, m Tree height Mean Total annual Elevation, Exposure
Hydrobiologia

(stems ha-1) biomass (T m to DBH annual rainfalla, m to

ha-1) ratio temp.a,°C mm wave &
coastal
current

6 Tondol 6 Rm 7,780 13.58 2.01 ± 0.44 0.025 ± 0.001 80.40 27.1 2,904 -0.12 Exposed
(Lingayen ± 0.3 ± 84 ± 0.02
Gulf)
8 Pangapisan 6 Rm 6,450 18.21 3.66 ± 0.34 0.040 ± 0.004 91.50 27.1 2,904 0.14 Protected
(Lingayen ± 0.3 ± 84 ± 0.01
Gulf)
10 Imbo 8 Rm 2,387 38.45 4.14 ± 0.33 0.045 ± 0.003 92.00 27.1 2,904 -0.22 Exposed
(Lingayen ± 0.2 ± 84 ± 0.03
Gulf)
11 Pilar 8 Rm 1,886 43.29 5.32 ± 0.59 0.050 ± 0.007 106.40 27.1 2,904 -0.13 Exposed
(Lingayen ± 0.3 ± 84 ± 0.01
Gulf)
12 Buswang 10 Rm, Ra 2,122 51.43 6.41 ± 0.66 0.060 ± 0.006 106.83 27.2 2,597 0.12 Protected
(Panay Is.) ± 0.2 ± 32 ± 0.01
17 Buswang 10 Rm, Ra 1,532 101.80 8.96 ± 0.92 0.080 ± 0.01 112.00 27.2 2,597 0.07 Protected
(Panay Is.) ± 0.2 ± 32 ± 0.01
18 Bangrin 42 Rm 1,358 115.62 10.51 ± 0.98 0.090 ± 0.009 116.78 27.1 2,904 0.20 Protected
(Lingayen ± 0.3 ± 84 ± 0.01
Gulf)
50 Banacon 10 Rm, Rs 1,231 132.18 10.36 ± 0.78 0.100 ± 0.014 103.60 27.6 1,775 -0.23 Exposed
(Bohol) ± 0.2 ± 15 ± 0.03
Nx Buenavista 8 Rm, Ra, 1,442 147.60 9.11 ± 0.97 0.090 ± 0.034 101.22 27.6 1,775 0.10 Protected
(Bohol) Am, Sa, ± 0.2 ± 15 ± 0.01
Bg, Nf
Ny Masinloc 8 Rm, Ra, 1,485 142.79 10.08 ± 0.79 0.100 ± 0.026 100.80 27.2 3,049 -0.13 Exposed
(Zambales) Am, Sa, ± 0.3 ± 85 ± 0.01
Bg
Nz Palauig 5 Rm, Ra, Sa 1,399 137.98 11.76 ± 0.96 0.115 ± 0.029 102.26 27.2 3,049 -0.09 Exposed
(Zambales) ± 0.3 ± 85 ± 0.01

Nx, Ny and Nz are natural mangroves of unknown ages. Elevation was estimated based on mean tidal level. Species are listed based on order of dominance. Species legend: Am—Avicennia
marina; Bg—Bruguiera gymnorrhiza; Nf—Nypa fruticans; Ra—Rhizophora apiculata; Rm—R. mucronata; Rs—R. stylosa; Sa—Sonneratia alba
a
Extrapolated from 30-year climate normals (FAO, 2001)

123

to study restoration ecology in planted mangroves. The
plantations were exposed to Typhoon Chan-hom on 7th
May 2009. The typhoon event provided a rare oppor-
tunity to investigate the effects of a typhoon on the
restoration trajectory of planted mangroves. Here, using
a range of planted forests of different ages and mature
forests (referred to as the restored system), we tested
whether planted mangroves recover in a similar way to
natural mangrove stands (referred to as the reference
system) after an intense typhoon.
Materials and methods
Experimental design
We used existing mangrove plantations of known
different ages to establish a space-for-time (SFT)
sequence of mangrove growth and development trajec-
tory following restoration and disturbance. Data gath-
ered from planted mangroves (referred to as the restored
system) were compared with data from natural man-
groves (referred to as the reference system) that serve as
a proxy trajectory endpoint. Our sampling design used
the SFT substitution approach that inferred temporal
trend from different age stands to generate patterns in
the trajectory of the restored system (cf. Pickett, 1989).
We acknowledged the limitations of SFT substitution
approach particularly the role of localized confounding
factors such as topography, elevation and exposure to
waves (Table 1). However, such an approach has been
used in similar studies in restoration ecology where
optimal sampling designs (i.e. presence of experimental
controls and age replicates within one site) may not be
available (cf. Michener, 1997).
Site description
The main study sites are located in Lingayen Gulf,
northwestern Philippines (between 16°230 and 16°390 N
latitude; 119°530 –120°190 E longitude). This study uti-
lized the planted Rhizophora mucronata mangroves
located in Tondol, Anda (6 years); Mona, Alaminos
(8 years); Imbo, Anda (10 years); Pilar, Bolinao
(11 years); and Bangrin, Bani (18 years; Fig. 1). Sites
in Alaminos, 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 inputs from Bani
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Hydrobiologia
Fig. 1 Location of the study sites. Numbers indicate the age of c
plantation. P—planted mangroves, N—natural mangroves.
Planted mangroves are located in: northwestern Lingayen Gulf
(top left); Kalibo, central Philippines (mid right) and Getafe,
central Philippines (bottom right). Natural mangrove stands are
located in Masinloc, Palauig (north-northwestern Philippines;
bottom left) and Buenavista, central Philippines (bottom right).
The age of natural mangroves are unknown. The dashed lines
indicate the estimated trajectory of Typhoon Chan-hom
(adapted from Kitamoto, 2009)
River. Detailed information on each stand and site can
be found in Salmo III et al. (2013). Additional man-
grove plantations from the 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 (Bohol,
central Philippines). The mangrove forests in Banacon
are 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, 2004) with a small patch
(*5–10 ha) spared from cutting by the local people.
This remnant pseudo-protected area of mangroves was
used as the sampling site for the 50-year old forest.
Three natural mangrove forests were used as
reference sites (Fig. 1): Buenavista in Bohol (Nx;
central Philippines); and Masinloc (Ny) and Palauig
(Nz) in Zambales (north-northwestern Philippines;
15°330 N latitude, 119°570 E longitude). These natural
forests are dominated by Rhizophora species and are
protected by national environmental laws.
The average depth of tidal water across study sites
is estimated as 2 m during high tide, but forests are
generally exposed at low tide particularly during
September to February. All sites receive precipitation
of more than 1,700 mm year-1. Under the modified
Corona climate classification system, the climate in
the 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 II (no dry season, but pronounced
wet season from December to February). The climate
in Bohol falls under Type IV, which has no pro-
nounced wet and dry seasons.
Typhoon Chan-hom
Typhoon Chan-hom (known locally as Typhoon Emong)
was the fifth typhoon that entered the Philippines in the
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2009 season. There were four other typhoons that crossed
the Lingayen Gulf (Nangka, Ketsana, Parma and Miri-
nae) in that season. However, these typhoons had lower
wind speeds and did not pass as close to the study sites.
Typhoon Chan-hom was formed near SE Vietnam in the
West Philippine Sea and crossed the Philippine Area of
Responsibility (PAR) on 3rd May 2009. It had strong
winds of 85–150 km h-1 and was categorized as
Typhoon 2 under the Saffir-Simpson Scale. The eye of
the typhoon first crossed land at Cape Bolinao on 7th May
2009 (see dashed lines in Fig. 1) bringing with it strong
winds, heavy rains (at least 200 mm in 24 h), and
flooding which directly affected the mangroves in
northwestern Lingayen Gulf. We estimated the distance
of the plots to the published path of the typhoon
(Kitamoto, 2009). Plots P6, P8, P10, P11 and P18 were
within 5 km of the path of the typhoon (Fig. 1). The
farthest distance from the northernmost and southern-
most mangrove plots is \20 km. P12 and P17 were
approximately\3 km from the path of the typhoon. Ny
and Nz were approximately 100 km from the typhoon
path, while P50 and Nx were 800 km from the path. Sites
that were [80 km from the path were considered to be
unaffected by the typhoon.
Sampling
Prior to the typhoon, measurements of trees and soils
in experimental plots were carried out in December
2008. Subsequent samplings were made at 1-mo and
7-mo post-typhoon in May and December 2009,
respectively. Additional measurements were made
for Lingayen Gulf sites at 9-mo post-typhoon (March
2010) to further establish patterns of damage and
regeneration in typhoon-affected sites. Additional
sampling was also carried out in natural mangrove
sites in Zambales (Ny and Nz) at 9-mo post-typhoon
(March 2010) to provide comparison of non-typhoon
affected sites with those affected by the typhoon.
Vegetation and soil characteristics
At each of the planted and natural sites, three circular
permanent monitoring plots were established. Plots
had 3-m radius for plantations less than 17 year-old
and 5-m radius for the more mature sites. The
differences in plot sizes were made to standardize
the number of trees measured from each plot. Leaf
area index (LAI) was measured twice from the centre
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Hydrobiologia
of the plot using a CI-110 Plant Canopy Imager (CID
Bio-Science, Washington, USA). The Plant Canopy
Imager captures a 150° image of the canopy then
calculates LAI through the solar beam transmission
coefficients, or the fraction of the sky visible from
beneath the plant canopy. Each individual within the
plot was tagged and measured repeatedly throughout
the sampling period. All individuals within the plot
were recorded by measuring tree diameter (at 2–3 cm
above the highest prop root using a measuring tape)
and total tree height (using a telescoping pole). Tree
density and aboveground biomass were then later
computed using allometric equations (Komiyama
et al., 2008). The number of seedlings (\2.5 cm
diameter) and saplings (2.5–5 cm diameter) in each
plot were also measured. The diameter of each
seedling and sapling was measured 2–3 cm above
the first node.
From each vegetation plot, three replicate soil
samples were randomly collected during low tide to
10 cm depth using a soil corer (diameter 6.5 cm).
From the interstitial waters, salinity was measured
with a hand-held refractometer (HT211-ATC, HT
Tech, Jiangsu, China). The pH, redox and temperature,
were measured using a TPS Aqua-pH portable instru-
ment (Aqua pH 2.2, TPS, Brisbane, Australia). Soil
samples were collected and submitted within 24–48 h
of sampling to the Bureau of Soils and Water
Management (BSWM) laboratory in Quezon City,
Philippines for the analysis of sand and silt particle
size composition, organic matter (OM), total nitrogen
(TN) and available phosphorus (AP) contents. 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 analyses
One-way repeated measures ANOVA was used to
determine if the vegetation and soil variables varied with
time (pre-typhoon vs. post-typhoon) in each stand. Data
from the three natural mangrove sites were pooled. The
assumptions for ANOVA were evaluated using Le-
vene’s test without data transformation (a = 0.05). Post
hoc comparisons were made using Tukey’s test to
determine pair-wise differences between sampling
periods. To compare the change in forest and soil
Hydrobiologia
variables with time, Analysis of Covariance
(ANCOVA) was used with stand age as the covariate.
The slope of the pre-typhoon regression line was
compared with the slopes of 1-mo, 7-mo and 9-mo
post-typhoon regression lines. Data for natural man-
groves were pooled. Data were log transformed prior to
ANCOVA test to conform to assumptions of normality.
Multivariate tests were conducted to visualize
forest and soil development patterns with age of the
stands and between sampling periods (pre-typhoon vs.
post-typhoon). The variables used in multivariate tests
were LAI, density, AGB and the number of seedlings
and saplings for the vegetation and the proportion of
sand and silt, OM, TN, AP, salinity, pH, redox and
temperature in the soils. Post-typhoon data were
pooled and then compared with the pre-typhoon data.
LAI data was untransformed, while the tree density
and AGB data were log-transformed and then nor-
malized to create a resemblance matrix based on
Euclidean Distance. Principal Component Analysis
(PCA) plots were then created. 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 that of the
mangrove vegetation, a stepwise multiple regression
analysis was applied to a correlation matrix (Sokal &
Rohlf, 1997). The BEST-BIOENV procedure was
used to compare the rank-similarity matrices for the
soil with matrices created from the vegetation vari-
ables on 999 permutations. All ANOVA and
ANCOVA tests were run in R Statistical Software
(R Development Core Team, 2012), while multivar-
iate tests were conducted in PRIMER (version 6;
Clarke & Gorley, 2006).
Results
Pre- versus post-typhoon vegetation development
Leaf area index (LAI)
The LAI increased logarithmically with age of the
stands (Y = 1.86 ln (x) - 2.32; r2 = 0.74; Fig. 2A).
The lowest LAI values were observed from the
youngest plantations (P6 = 0.15 ± 0.01 m2 m-2;
P8 = 0.29 ± 0.01 m2 m-2), increased in the interme-
diate stands (P10–P12, mean = 2.54 ± 0.02 m2 m-2)
and then peaked at P50 (4.54 ± 0.18 m2 m-2). The 17-
and 18-year old plantations (4.02 ± 0.01 m2 m-2) had
comparable LAI values with P50 and natural mangrove
stands (4.54 ± 0.05 m2 m-2). The typhoon resulted in
the total defoliation of the 11- and 18-year old stands in
Lingayen Gulf. The ANCOVA test showed significant
differences between pre-typhoon and all post-typhoon
LAI (Table 2A). After the typhoon, the 11-year
old plantation had faster refoliation rate (Y =
1.313x - 14.504, r2 = 0.52) compared to the 18-year
old plantation (Y = 0.629x - 11.581, r2 = 0.87).
Tree density
Prior to the occurrence of the typhoon, the tree density
decreased logarithmically with age, Y = -1,828 ln
(x) ? 7,722 (r2 = 0.46; Fig. 2B). The highest density
was observed from the youngest plantation
(7,780 ± 770 trees ha-1), rapidly decreased in inter-
mediate age stands (P10; 2,387 ± 115 trees ha-1) and
then tended to stabilize at P11 (1,886 ± 156 trees
ha-1). The 12-, 17- and 18-year old stands
(1,671 ± 321 trees ha-1) had comparable densities
as the P50 (1,231 ± 42 trees ha-1) and the natural
mangrove stands (1,499 ± 76 trees ha-1). The occur-
rence of the typhoon resulted in a decline in tree
densities in the 11- and 18-year old stands in Lingayen
Gulf. At 9-mo post-typhoon, tree densities were
reduced by 61 and 69 % in P11 and P18, respectively
(Fig. 2B). The ANCOVA test showed significant
difference between pre-typhoon and that of the 7-mo
and 9-mo post-typhoon slopes (Table 2A).
Aboveground biomass (AGB)
The aboveground biomass (AGB) increased logarith-
mically with age of mangrove stands (Y = 62.35 ln
(x) - 97.76; r2 = 0.89; Fig. 2C). Lowest AGB was
recorded from the youngest plantation (13.59 ± 1.56
T ha-1) and steadily increased as stand age increased.
The 17- and 18-year old plantations had 30–40 %
lower AGB compared with the natural mangroves. The
50-year old plantation (132.18 ± 3.18 T ha-1) had
comparable biomass to the natural mangroves
(150.66 ± 3.57 T ha-1). The typhoon caused AGB
reductions in the 11- and 18-year old plantations in
Lingayen Gulf by 70 and 79 %, respectively (Fig. 2C).
There was a significant difference between pre-
typhoon and that of the 7-mo and 9-mo post-typhoon
slopes (ANCOVA Test; Table 2A).
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Fig. 2 Changes in: A LAI,

B tree density and
C aboveground biomass
with age of the mangrove
stands and with sampling
periods (pre- vs. post-
typhoon). Prior to the
occurrence of the typhoon,
there was a significant
relationship between LAI
(Y = 1.86 ln (x) - 2.32;
r2 = 0.74), tree density
(Y = -1,828 ln
(x) ? 7,722 (r2 = 0.46) and
aboveground biomass
(Y = 62.35 ln (x) - 97.76;
r2 = 0.89) with age of the
stands. The typhoon caused
complete defoliation,
reduction of tree density (by
61–69 %) and aboveground
biomass (by 70–79 %) of
the typhoon-affected sites
(see arrows and encircled
dashed lines in the plot).
Legend: unfilled circles
(pre-typhoon), grey circles
(1-mo post-typhoon),
triangles (7-mo post-
typhoon) and solid dashed
lines (9-mo post-typhoon)

Seedling and sapling abundance
Seedlings were present in the 50-year old plantation
and natural mangroves, but none in plantations \20-
year old. The seedling abundance was significantly
higher in the 50-year old plantation (20–25 seedlings
100 m-2) compared to the three natural mangroves
that had similar abundances of 12–15 seedlings
100 m-2. Seedlings had homogeneous girth (mean
0.75 ± 0.05 cm) and height (mean 0.75 ± 0.01 m)
and were more abundant at pre-typhoon and 7-mo
post-typhoon than at the other sampling periods. Very
few saplings were observed and were only present in
the natural stands (3–5 saplings 100 m-2).
Pre- versus post-typhoon soil development
Organic matter, total nitrogen and available
phosphorus
Prior to the typhoon, only the OM and TN contents had
significant relationships with the age of the mangrove
stands (OM: Y = 4.456 ln (x) - 6.543; r2 = 0.75;
Fig. 3C; TN: Y = 0.067 ln (x) - 0.103, r2 = 0.82;

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 Table 2 Results of 1-way repeated measures ANOVA on: changes of (A) vegetation and (B) soil parameters across sampling periods (pre- vs. post-typhoon) of the typhoon-
affected sites
Time LAI, m2m-2 Tree density, n ha-1 AGB, T ha-1
Hydrobiologia

P11 P18 Slope P11 P18 Slope P11 P18 Slope

Pre-typhoon 2.80a 4.13a -0.269xa 1,886a 1,532a 0.001xa 45.37a 115.62a 0.057xa
(0.01) (0.05) (156) (170) (12.36) (3.97)
1-mo post-typhoon 0.00b 0.00b -0.119xb 891ab 848ab -0.009xa 12.86b 52.18b 0.005xa
(0.01) (0.00) (127) (212) (4.34) (1.21)
7-mo post-typhoon 1.50c 0.51c -0.0006xb 806bc 764bc 0.051xb 13.66b 23.28bc -0.004xb
(0.17) (0.01) (194) (124) (4.90) (1.64)
c c b bc bc b b
9-mo post-typhoon 1.77 0.63 -0.084x 733 424 -0.028x 13.01 22.80d -0.046xb
(0.15) (0.02) (147) (42) (7.25) (1.13)
Source
MS 4.02 10.76 78.76 1.71 9 106 5.91 9 105 2.97 7.78 9 108 9.69 9 109 5.51
df 3 3 3 3 3 3 3 3 3
F-ratio 429.10 302.85 6.38 6.38 16.61 4.83 20.67 194.60 6.36
P *** *** *** * ** * ** *** ***
Time OM, % Total N, % Avail. P, ppm ORP, mV Temp., °C
P11 P18 Slope P11 P18 Slope P11 P18 Slope P11 P18 Slope P11 P18 Slope

Pre-typhoon 7.53a 7.99a 0.037xa 0.08a 0.09a 0.0001x 22.37a 22.37a 1.52xa 8.00a 14.67a 0.142xa 30.87a 30.70a 0.001xa
(0.97) (1.27) (0.01) (0.01) (4.66) (4.66) (0.79) (3.29) (0.25) (0.22)
1-mo post-typhoon 4.54b 3.74b -0.036xb 0.14b 0.08ab -0.0003x 35.73b 29.33b 1.73xb -10.00b -0.67b 0.078xb 37.60b 38.63b -0.001xb
(0.35) (0.34) (0.04) (0.01) (2.42) (2.78) (0.35) (4.03) (0.62) (0.89)
b b a a b ab b b a a b b
7-mo post-typhoon 5.46 3.55 0.005x 0.08 0.06 -0.0003x 34.80 27.63 -1.25x 11.33 14.33 0.322x 35.80 34.60c 0.001xb
(0.37) (1.01) (0.00) (0.01) (5.92) (2.91) (0.37) (2.05) (0.82) (0.67)
9-mo post-typhoon 6.51a 3.49b 0.007xa 0.08a 0.05b 0.0005x 30.40ab 25.43b -1.72b 8.67a 14.67a 0.101xa 32.63a 33.73c -0.001xb
(0.63) (0.62) (0.00) (0.02) (1.48) (0.26) (0.63) (5.25) (0.73) (0.42)
Source
MS 4.81 14.44 76.89 0.003 0.01 9107 0.01 22.04 18.47 222.96 21.46 17.46 178.45 27.68 159.3 212.91
df 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3
F-ratio 10.43 17.90 3.39 4.76 6.39 2.03 4.59 5.78 3.83 4.45 7.87 3.67 41.65 343.20 6.75

123
 Hydrobiologia

Slope

The slopes are derived from the ANCOVA values (using stand age as covariate) to determine the differences in vegetation and soil trajectories between pre- and post-typhoon
Fig. 3D). The occurrence of the typhoon resulted in

***
the immediate reduction of soil OM contents by 40 and
53 % in P11 and P18, respectively (Table 2B).
However, the two typhoon-impacted sites showed
P18

***
different post-typhoon recovery trends. The P11
Temp., °C

plantation appeared to recover the soil OM content

at 7-mo post-typhoon, while P18 in contrast, showed a
P11

***

continuous decline in soil OM even at 9-mo post-

typhoon (Table 2B). The slope of pre-typhoon regres-
sion line was significantly different from the 1-mo
Slope

post-typhoon line, but not from the slopes of 7-mo and

*

9-mo post-typhoon periods (Table 2B).

For TN, the typhoon-impacted sites showed
P18

**

increases of 60 and 33 % for P11 and P18, respectively

ORP, mV

at 1-mo post-typhoon (Fig. 3D; Table 2B). This trend

was no longer evident for P11 at 7-mo and 9-mo post-
P11

typhoon. However, P18 showed continuous decreased

*

from 1-mo post-typhoon to 7-mo and 9-mo post-

typhoon. There was no significant difference between
Slope

pre-typhoon and post-typhoon changes on TN with age

*

of the stands. In terms of AP, the typhoon-impacted

sites showed increases of 38 and 23 % for P11 and P18,
P18
Avail. P, ppm

respectively at 1-mo post-typhoon (Fig. 3E; Table 2B),

*

but no significant difference from initial pre-typhoon

values at 7- and 9-mo post-typhoon.
P11

sampling periods. Different letters denote significance between sampling periods

Redox and soil temperature

Slope

The occurrence of typhoon caused the soils of typhoon-

impacted sites to become more anoxic (P11 =
ns

P denote significance at \0.05 (*), \0.01 (**) and \0.001 (***)

-10.00 ± 0.35 mV; P18 = -0.67 ± 4.03 mV, at

0.5-mo post-typhoon; Table 2B). Both stands tended
P18

to return to pre-typhoon redox values at 7-mo post-

Total N, %

typhoon. The ANCOVA test showed significant

difference in redox potential with forest age between
P11

pre-typhoon, 1-mo and 7-mo post-typhoon, but a return

to pre-typhoon values at 9-mo post-typhoon.
Slope

There was an increase in soil temperature by

8–10 °C in P11 and P18 after the typhoon (Table 2B).
*

Both impacted sites showed that temperatures at 9-mo

post-typhoon were still 3–4 °C warmer compared to the
P18

**

pre-typhoon data. The ANCOVA test showed signifi-

cant differences between pre-typhoon and post-typhoon
Table 2 continued
OM, %

in the relationship between soil temperature and stand

P11

**

age. The pre-typhoon slope of the relationship was

significantly different from pre-typhoon to 1-mo post-
typhoon, but was similar to the pre-typhoon relationship
Time

at 7-mo and 9-mo post-typhoon (Table 2B).

123
Hydrobiologia

Fig. 3 Changes in A sand

content, B silt content,
C organic matter, D total
nitrogen, E available
phosphorus, F salinity,
G pH, H oxidation–
reduction potential and
I temperature in the soil with
age of the mangrove stands
and with sampling periods
(pre- vs. post-typhoon).
Prior to the occurrence of the
typhoon, only the OM
(Y = 4.456 ln (x) - 6.543;
r2 = 0.75) and TN
(Y = 0.067 ln (x) - 0.103,
r2 = 0.82) have significant
relationship with age of the
mangrove stands. At 1-mo
post-typhoon, there was a
reduction of OM (by
40–53 %), and sudden
increase of TN (by 43 %)
and AP (by 23–38 %) in the
typhoon-affected sites (see
arrows and encircled
dashed lines in the plot). The
soils also became more
waterlogged (by at least
113 %) and warmer by
8–10 °C. Legend: unfilled
circles (pre-typhoon), grey
circles (1-mo post-typhoon),
triangles (7-mo post-
typhoon) and solid dashed
lines (9-mo post-typhoon)

Pre-typhoon versus post-typhoon vegetation
and soil development patterns
Prior to the occurrence of the typhoon, there was a
clear vegetation and soil development pattern with age
of the stands (Fig. 4A). The result of Principal
Component Analysis showed three major stand age
groupings: P6 and P8 (group 1), P10 and P11 (group
2), and P12, P17, P18, P50 and natural mangroves
(group 3). The PC1 and PC2 accounted for 91.3 and

123
 Hydrobiologia

Fig. 4 PCA plots of

vegetation and soil
parameters A pre-typhoon
and B post-typhoon. Prior to
the typhoon, 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 (see also
Salmo III et al., 2013). The
typhoon caused the
impacted sites (grey circles)
to retract from their pre-
typhoon groupings and
moved to the category of the
younger stands (see arrow).
Legend: dashed ellipse—
grouping per stand age; solid
ellipse—grouping per
development stage

6.1 % of the variation where LAI and tree density had
the highest correlation in PC1 and PC2, respectively.
These groupings showed progression in forest devel-
opment with age approaching maturity as was
observed in natural mangroves. These groupings were
significantly different from each other as revealed by
the ANOSIM test (Global R = 0.84, P \ 0.001).
There was no significant differences between sites
within the age groups. The BIOENV test revealed a
significant relationship between the forest vegetation
and soil characteristics (q = 0.68, P \ 0.01) where
the combination of OM, TN, redox and soil temper-
ature had the highest correlation (q = 0.67). Simi-
larly, the mangrove vegetation is strongly correlated
with the soil characteristics (q = 0.64, P \ 0.01)
where LAI had the highest correlation (q = 0.63). The
relationship between mangrove vegetation and soils
were significantly correlated in all sampling periods
(1-mo post-typhoon: r = 0.60, P \ 0.01; 7-mo post-
typhoon: r = 0.57, P \ 0.01; 9-mo post-typhoon:
r = 0.56, P \ 0.01).
These patterns were, however, disrupted by the
typhoon (Fig. 4B). The PC1 and PC2 accounted for 68.6
and 28.1 % of the variation. The reductions in tree
density (q = 0.67) and AGB (q = 0.89) had the highest
correlation with PC1 and PC2, respectively. The
ANOSIM test revealed significant difference between
pre-typhoon and post-typhoon groupings (Global
R = 0.80, P \ 0.01). The typhoon-affected sites sepa-
rated from their pre-typhoon groupings at 1-mo post-
typhoon and remained different at 7-mo and 9-mo post-
typhoon (see arrow in Fig. 4B), although the variables
that caused the differences at different sampling periods
varied. The two most heavy typhoon-affected sites were
grouped together and were significantly different from
the less affected sites in all post-typhoon sampling
periods. The summary of BEST-BIOENV correlations
are presented in Tables 3A and 3B. At 1-mo post-
typhoon, the combination of increased in soil temper-
ature (0.57) and the reduction in redox potential (0.56)
and OM (0.42) were related to the changes in mangrove
vegetation (q = 0.57, P \ 0.01). Soil temperature

123
Hydrobiologia

Table 3 Summary of BEST-BIOENV results showing corre- early establishment phase, and with self-thinning as
lation coefficients between soil characteristics (A) and vege- they approach the stabilization stage at the 11th year.
tation (B) for each sampling period
In the Philippines, most plantations have stunted
Variables Time growth and very low survival (10–40 %; Primavera &
Pre- 1-mo post- 7-mo post- 9-mo post- Esteban, 2008; Samson & Rollon, 2008).
typhoon typhoon typhoon typhoon These parameters stabilized at the 11th year
indicating that many characteristics of the planted
A. Soil
forests are similar to natural forests. Similar trends in
Sand 0.21 0.09 0.03 0.21
canopy closure and stem density have been observed
Silt 0.27 0.22 0.15 0.36
OM 0.76 0.42 0.42 0.47
in plantations in Malaysia (Clough et al., 1997; Alongi
Total N 0.59 0.17 0.12 0.30
et al., 1998) and also in natural forests in French
Avail. P 0.37 0.20 0.21 0.21
Guiana (Fromard et al., 1998). The time to maturity is
Salinity 0.37 0.11 -0.13 -0.12
estimated at 25 years, which is relatively slow com-
pH 0.29 0.11 -0.07 -0.04
pared to the gap regeneration process in natural
Redox 0.59 0.56 0.05 0.19 mangroves (Duke, 2001), but similar to that observed
Temp. 0.52 0.57 0.56 0.22 in other plantations and natural forests (Fromard et al.,
q 0.76 0.57 0.56 0.47 1998; Alongi, 2009).
P ** ** ** ** From the PCA plot (Fig. 4A), three distinct group-
B. Vegetation ings can be inferred and classified based on the
LAI 0.64 0.55 0.52 0.49 vegetation and soil development stage of the restored
Tree density 0.40 0.24 0.18 0.21 stands. These are: Group 1 (young stands: \10-year),
AG biomass 0.52 0.54 0.35 0.29 Group 2 (intermediate stands: 10- to 11-year) and
q 0.64 0.55 0.53 0.49 Group 3 (mature stands: [12-year). The vegetation
P ** ** ** ** and soil characteristics in 17-, 18- and 50-year stands
are comparable with that of the reference system
The variables that have high correlation coefficients are in bold
fonts (natural stands). Following the evolutionary model of
P denote significance at \0.01 (**) mangrove forest development (cf. Fromard et al.,
1998), mangrove plantations reported here that are less
than 12 years old are comparable to the early devel-
(0.56) and OM (0.42) remained the main contributing opment stage, while plantations that are 17- and
variables that were associated with the vegetation at 18-years old are similar to the young development
7-mo post-typhoon (q = 0.56, P \ 0.01), but at 9-mo stage, and the 50-years old are comparable with the
post-typhoon, only OM (0.47) maintained a high mature stage.
correlation coefficient with vegetation (q = 0.47, As mangrove stands mature, the change in vegeta-
P \ 0.01). tion contributes to the attainment of soil maturity. The
relationship between mangrove vegetation and soil
characteristics has been reported in previous studies
Discussion which suggest linkage of vegetation structure and
productivity with redox potential of soils (Sherman
Pre-typhoon restoration trajectory et al., 1998; Rivera-Monroy et al., 2004), and nutrient
availability particularly nitrogen and phosphorus
Our study showed a clear trajectory of mangrove (Boto & Wellington, 1984; Ukpong, 1994). The
forest and soil development patterns from a series of relationship between soil temperature and forest
ages of planted mangrove stands (see also Salmo development is related to the surrounding mangrove
III et al., 2013). There were increases in the LAI, canopy cover that regulates absorption of solar
AGB, OM, TN, AP and redox potential, and decreases radiation (Bosire et al., 2005; Tolhurst & Chapman,
in tree density and soil temperature with stand age. In 2007), while the relationship of nitrogen is likely
young plantations, the rapid decline in tree density caused by the enhancement of litter degradation and
with stand age is due to high mortality rates during the organic matter decomposition (Bosire et al., 2005).

123

Table 4 Reductions in tree density and basal area (BA) reported in typhoon-damaged mangroves
Location Age/stage Density reduction, %
Lingayen Gulf, Philippines 11 61
Lingayen Gulf, Philippines 18 70
Bluefields, Nicaragua Natural 36
SW Florida, USA Natural 40
SW Florida, USA Natural 60
Guadeloupe, French West Indies Natural 59
Dominican Republic Natural 48
SW Florida, USA Natural 47
In this study, BA was derived from tree diameter measurements
The accumulation of OM in the soils may be attributed
to the increases in belowground root expansion with
stand age (which is correlated with LAI from BEST-
BIOENV results in this study) that may have lead to
the rapid deposition of litter and organic detritus in the
soil (see for example Saenger, 2002; Morrisey et al.,
2003; McKee, 2010). The significant correlation of
mangrove aboveground vegetation with soil OM is
similar to the findings of Alongi (2009) for the Matang
forests. Moreover, Cardona & Botero (1998) proposed
that the large pool of OM might also affect nutrient
availability as well as other variables such as pH and
redox potential.
Impacts of typhoon on vegetation and soil
development trajectory pattern
We acknowledged the unbalanced nature of our
experimental design. In assessing the effects of typhoon
in restoration trajectory, the comparisons we made
between and among mangrove stands relative to the
track of the typhoon and the differences in ages of the
stands (including that of planted vs. natural stands) are
confounded. Like other natural disasters however,
typhoons are unexpected events with heterogenous
effects, and therefore do not comply with optimal
ecological experimental designs. Nevertheless, our
study documented the effects of typhoon in young
growing mangrove plantations of different ages.
We observed that Typhoon Chan-hom caused
severe damage to mangrove plantations in Lingayen
Gulf, although the damage was not homogeneous over
all mangrove stands. Similar to published reports, the
damage from a typhoon within a forest stand or even at
a landscape level are heterogeneous and may be
123
Hydrobiologia
BA reduction, % Reference
60 This study
80 This study
68 Roth (1992)
54 Doyle et al. (1995)
– McKoy et al. (1996)
68 Imbert et al. (1996)
42 Sherman et al. (2001)
– Milbrandt et al. (2006)
attributed to gradients of wind speed over the path of
the typhoon and localized site gradients such as
position relative to shoreline, tidal elevation, soil type
and tree height (see for example Everham & Brokaw,
1996; Busby et al. 2008). The path of the typhoon,
which followed an arc, led to more severe damage in
the 11- and 18 year old stands. Consistent with
published reports, trees with taller heights and larger
diameters had higher mortality than smaller trees
(Roth, 1992; Smith et al., 1994; Baldwin et al., 2001).
The trees that died had stem diameter [8 cm and
height [7 m in the 11-year old plantation, and stem
diameter [10.5 cm and height [10 m in 18-year old
plantation. Similar to other tropical forest types,
mangrove plantations are perceived to be more
vulnerable to typhoons compared to natural stands
(Everham & Brokaw, 1996) because of the lower
structural complexity and lower wind firmness (sensu
Gardiner & Quine, 2000) as defined by high height to
DBH ratio (Ancelin et al., 2004). The typhoon-
damaged 11- and 18-year old stands were relatively
tall with height to DBH ratios of 106.40 and 116.78,
respectively (Table 1). Given the high frequency and
severity of typhoons prevailing in the area, such size
classes could be the maximum size that these
mangroves may reach and it is possible that damage
from typhoons could be responsible for the relatively
low biomass reported for Philippine mangrove forests
(see for example Gevaña & Pampolina, 2009).
The reductions in tree density and basal area in
Lingayen Gulf after the typhoon are comparable to
losses described in other published reports (Table 4).
Tree mortalities continued even after 9 months post-
typhoon and may even persist for at least two more
years, also similar with other published reports (Smith
Hydrobiologia
et al., 1994; Sherman et al., 2001). The sudden
reduction in LAI, tree density and AGB in the 11- and
18-year stands effectively retarded the restoration
trajectory by five to ten years.
The occurrence of the typhoon also caused signif-
icant changes in soil characteristics in the typhoon-
affected sites (Fig. 4B). Changes to soils after intense
storms have also been reported from other typhoon-
disturbed sites (Craighead & Gilbert, 1962; Smith
et al., 1994; Ellison, 1998; Rivera-Monroy et al.,
2004). In this study, among the immediate and easily
discernable post-typhoon changes are the reductions in
OM (40–53 %), more anoxic soils (-10 mV) and
increase in nutrients (TN by 30–60 %; AP by
30–40 %), salinity (4–10 ppt) and soil temperature
(8–10 °C). Increases in soil temperature can be
attributed to the removal of canopy shading that
exposes the soil to solar radiation (Bosire et al., 2003).
The increases in temperature after defoliation may
also cause increases in salinity due to higher evapo-
ration and decreases in redox potential through
enhanced microbial activity. The increase in nutrient
availability after the typhoon may be explained by the
influx of fine-grained materials during the typhoon
surge that were deposited on the forest floor (pers.
obs.), but also could be explained by the mortality of
roots and release of nutrients in the biomass to the soil.
The deposition of material within the forests during
intense storms was observed at other sites (Craighead
& Gilbert, 1962; Smith et al., 1994; Ellison, 1998)
where 50–100 % increases in soil N and P were
reported (Castaneda-Moya et al., 2010). The observed
reduction in soil OM in this study could be due to
enhanced decomposition of organic matter due to
increased nutrient availability (Bianchi, 2011),
although this hypothesis requires further assessment.
The changes to the soil environment were closely
linked with the continuous decline in mangrove
vegetation after the typhoon (as revealed from BIO-
ENV results; Tables 2A, 2B). While post-typhoon
salinity (33 ppt) falls within the normal range of
mangrove conditions, the 4–10 ppt increase (above 20
ppt from pre-typhoon) may cause reductions in tree
growth and slow forest recovery. Abrupt increases in
soil salinity have caused massive mangrove mortality
in the Caribbean coast of Colombia (Cardona &
Botero, 1998). The increase in nutrient availability,
particularly of phosphorus is known to contribute to
changing vegetation characteristics (Chen & Twilley,
1998; Castaneda-Moya et al., 2010), which may have
long-term effects on the structure and function of
forests (Smith et al., 2009).
Prospects for post-typhoon regeneration
Reports of the recovery of mangroves after a cata-
strophic typhoon are highly variable (Saenger, 2002).
There is a general consensus that recovery could be
very slow or may even be uncertain (Milbrandt et al.,
2006; Smith et al., 2009) since delayed tree mortalities
may still occur more than 10 years post-typhoon and
species differ in both their susceptibility to storm
damage and their recovery (Baldwin et al., 2001). The
mangrove plantations in the Lingayen Gulf are
exclusively composed of Rhizophora species that do
not coppice or resprout (Tomlinson, 1994; Imbert
et al., 1996). In the Lingayen Gulf, the only visible
sign of recovery 9 months after the typhoon was that
the typhoon-impacted sites began to refoliate.
In Nicaraguan mangroves, signs of recovery (i.e.
refoliation, resprouting, coppicing and seedling
growth) were manifested 5 years after a typhoon and
trees that recovered were those with low initial tree
diameter and height (Roth, 1992). Models of regen-
eration pathways (sensu Everham & Brokaw, 1996)
predict that the primary mode for recovery of the
typhoon-affected mangroves in Lingayen Gulf, would
be through seedling colonization, as reported in other
sites (Roth, 1992; Smith et al., 1994; Baldwin et al.,
1995; McKoy et al., 1996; Imbert et al., 1996; Baldwin
et al., 2001). Rapid seedling recruitment and growth
was observed in the mangroves in Nicaragua and
Dominican Republic at 17- and 18-months post-
typhoon, respectively (Roth, 1992; Sherman et al.,
2001). But the planted mangroves in Lingayen Gulf
have very few seedlings prior to the typhoon which is a
consequence of very high density plantings that
inhibits seedling recruitment and growth (Salmo
III & Duke, 2010). With a limited source of regener-
ation, it is not clear if the typhoon-affected planted
mangroves will recover without management inter-
vention (i.e. replanting).
It is apparent that most soil and vegetation variables
measured had returned to pre-typhoon state at 7-mo
and 9-mo post-typhoon. However, the two most
typhoon-affected sites had contrasting patterns of
recovery. Based on pre-typhoon values of soil OM,
nutrients, redox potential and soil temperature, the
123

11-year old stands showed some degree of recovery at
7-mo post-typhoon, but this was less obvious in the
18-year old stands. The younger stands may be able to
refoliate more rapidly because their epicormic buds
are still functional than that of the mature stands.
While the vegetation continued to show delayed
mortality in the 11- and 18-year old stands at 9-mo
post-typhoon, the improvements in the soil environ-
ment may contribute to post-typhoon seedling growth
and recruitment.
Acknowledgments We are grateful to Ford Foundation-
International Fellowship Program (FORD-IFP) and 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. SS thank the Ateneo de Manila University for
providing conference support grant, which facilitated the
presentation of this manuscript to the international symposium
‘Biodiversity in Changing Coastal Waters of Asia and Subtropical
Asia’ in Amakusa, Japan in November 2012.
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