Marine Pollution Bulletin 109 (2016) 734–743

Contents lists available at ScienceDirect

Marine Pollution Bulletin

journal homepage: www.elsevier.com/locate/marpolbul

Damage and recovery assessment of the Philippines' mangroves

following Super Typhoon Haiyan
Jordan Long a,⁎,2, Chandra Giri b, Jurgenne Primavera c, Mandar Trivedi d
a
InuTeq 1, Sioux Falls, SD 57198, USA
b
U.S. Geological Survey EROS Center, Sioux Falls, SD 57198, USA
c
Zoological Society of London, 48 Burgos Street, La Paz, 5000 Iloilo City, Philippines
d
Zoological Society of London, Regent's Park, London, NW1 4RY, United Kingdom

a r t i c l e i n f o a b s t r a c t

Article history: We quantified mangrove disturbance resulting from Super Typhoon Haiyan using a remote sensing approach.
Received 20 November 2015 Mangrove areas were mapped prior to Haiyan using 30 m Landsat imagery and a supervised decision-tree clas-
Received in revised form 15 June 2016 sification. A time sequence of 250 m eMODIS data was used to monitor mangrove condition prior to, and follow-
Accepted 22 June 2016
ing, Haiyan. Based on differences in eMODIS NDVI observations before and after the storm, we classified
Available online 7 July 2016
mangrove into three damage level categories: minimal, moderate, or severe. Mangrove damage in terms of ex-
Keywords:
tent and severity was greatest where Haiyan first made landfall on Eastern Samar and Western Samar provinces
Philippines mangrove and lessened westward corresponding with decreasing storm intensity as Haiyan tracked from east to west
Landsat across the Visayas region of the Philippines. However, within 18 months following Haiyan, mangrove areas clas-
eMODIS sified as severely, moderately, and minimally damaged decreased by 90%, 81%, and 57%, respectively, indicating
NDVI mangroves resilience to powerful typhoons.
Super Typhoon Haiyan © 2016 Elsevier Ltd. All rights reserved.
Mangrove disturbance

1. Introduction have resulted in extensive deforestation and degradation. Brackish-

Mangroves are highly productive coastal ecosystems found within
the intertidal zones of the tropics and subtropics ranging from 35° N
to 40° S latitude (Giri et al., 2011b). Mangroves provide numerous eco-
system goods and services that support human livelihoods and well-
being, and are critically important to nature and society (Alongi, 2002;
Duke et al., 2007). Mangroves have traditionally been used by coastal
populations for construction materials, food, fuel, and medicine
(Walters, 2005). In addition to providing suitable breeding and feeding
grounds for numerous aquatic and avian species, undisturbed man-
grove ecosystems provide coastal protection from erosion, tropical cy-
clones, and tsunamis (Alongi, 2008; Chmura et al., 2003; Lee et al.,
2014); are closely coupled to neighboring ecosystems (e.g., sea grasses
and coral reefs) (Mumby et al., 2004); and store carbon (McLeod et
al., 2011; Siikamäki et al., 2012; Twilley et al., 1992).
Despite the well-understood importance of mangroves, this biome
has become among the most threatened in the past half century (Van
Lavieren et al., 2012). Globally, pressures from land use competition
⁎ Corresponding author.
E-mail address: Jordan.Long.ctr@usgs.gov (J. Long).
1
Contractor to the U.S. Geological Survey (USGS) Earth Resources Observation and
Science (EROS) Center.
2
Work performed under U.S. Geological Survey contract G13PC00028.
water aquaculture, agriculture, salt production, infrastructure develop-
ment, and forest extraction are among the leading drivers of mangrove
loss, worldwide (Food and Agriculture Organization of the United
Nations, 2007; Primavera, 1995; Primavera, 2005a). Natural distur-
bances such as high water surge, tropical cyclones, tsunamis, and
wave action have also contributed to mangrove loss (Cornforth et al.,
2013; Giri et al., 2008; Paling et al., 2008); however, mangroves are gen-
erally more resilient to natural perturbations than to human-induced
disturbances (Jimenez et al., 1985).
Typhoon Haiyan, known as “Super Typhoon Yolanda” in the Philip-
pines, made landfall in Eastern Samar, Philippines, on November 8,
2013. According to the Saffir-Simpson hurricane wind scale (SSHWS),
Haiyan was rated as a category 5 hurricane with maximum sustained
winds of over 251 km/h and wind gusts greater than 300 km/h
(Fig. 1). The inordinately powerful typhoon damaged 1.1 million hous-
ing structures, displaced 4.1 million people, and caused over 6000
deaths (National Disaster Risk Reduction and Management Council,
2013; United States Agency for International Development, 2014). In
the aftermath of Typhoon Haiyan, the Philippines' Environment Secre-
tary announced plans for mangrove replanting and rehabilitation
throughout the Philippines to provide bio-protection from future natu-
ral disasters similar to Haiyan (Department of Environment and Natural
Resources, 2013). Effective mangrove restoration requires precise infor-
mation on the geographic distribution as well as extent and severity of

http://dx.doi.org/10.1016/j.marpolbul.2016.06.080
0025-326X/© 2016 Elsevier Ltd. All rights reserved.
 J. Long et al. / Marine Pollution Bulletin 109 (2016) 734–743
Fig. 1. Typhoon Haiyan path and category in the Philippines (Hurrevac, 2014).
damage. Time-series remotely sensed measurements coupled with in
situ observations are needed to monitor mangrove damage and recov-
ery at a large spatial scale. Typically, studies of storm impacts on man-
groves have used either remote sensing (Wang and D'Sa, 2009; Wang,
2012) or re-surveys of forest plots (Kauffman and Cole, 2010; Smith et
al., 2009); however, neither on their own provide a complete assess-
ment. Therefore, the aim of this study is to use remote sensing, coupled
with ground observations, to map and quantify change in mangrove
condition resulting from Typhoon Haiyan and monitor the subsequent
temporal pattern of recovery. The data and information from this
work are useful for developing rehabilitation and conservation strate-
gies and providing baseline information for future monitoring.
2. Materials and methods
2.1. Study area
The Republic of the Philippines is an archipelago of 7107 islands lo-
cated off the southeastern coast of Asia. With an extensive coastline
comprising numerous low-wave energy intertidal bay areas and a trop-
ical climate, the Philippines provides ideal environmental conditions for
mangrove growth. In 2010, the total mangrove area of the Philippines
735
was approximately 240,000 ha, with the greatest extent located in the
provinces of Palawan, Sulu, and Siargao Island, Surigao del Norte
(Long et al., 2013). Mangrove biological diversity is relatively high
with 35 true mangrove species (Food and Agriculture Organization of
the United Nations, 2007); however, mangrove diversity is threatened
and declining throughout the Philippines (Garcia et al., 2014; Richards
and Friess, 2016). The Philippines' total mangrove area decreased nearly
11% from 1990 to 2010 (Long et al., 2013; Long and Giri, 2011). The
principal threats are anthropogenic, with aquaculture and forest extrac-
tion among the leading drivers of loss in recent decades (Primavera and
Esteban, 2008). Within the next century, mangrove loss and degrada-
tion is expected to continue as human populations increase and concen-
trate in coastal regions. The impacts of climate change, sea level rise, and
increased storm strength and frequency also contribute to expected
mangrove loss in the Philippines (Gilman et al., 2008).
The Philippines has one of the highest disaster risk rankings in the
world due to its constant exposure to droughts, earthquakes, floods,
landslides, typhoons, and volcanic eruptions (UNU-EHS, 2014). Ty-
phoons are the most frequently occurring natural disaster in the Philip-
pines, historically impacting the greatest number of people and causing
the greatest amount of property damage (Bankoff, 2012). On average,
6.5 tropical typhoons make landfall in the Philippines per year (Joint
736 J. Long et al. / Marine Pollution Bulletin 109 (2016) 734–743
Typhoon Warning Center, 2008). The northern Luzon and central
Visayas regions are the most frequently impacted during the wet season
from June to November, while typhoons impacting the southern Minda-
nao region are less frequent. Mangroves in Luzon and Visayas make up
68% of the Philippines total mangrove area, and are exposed to recurrent
disturbances such as high winds and tropical storms (Long et al., 2013).
Tropical cyclones potentially have long-term influences on the distribu-
tion and composition of mangroves. Wind effects can range from minor
defoliation to catastrophic uprooting of entire mangrove stands, while
prolonged hydro-period and increased sediment deposition resulting
from storm surge can result in mortality from suffocation (Smith et al.,
2009). Frequently disturbed mangroves are typically young succession-
al forests and have a lower biomass than mature old growth mangroves,
but still provide important ecosystem goods and services (Twilley et al.,
1992).
2.2. Landsat mangrove classification
Landsat 30 m resolution satellite imagery was used to map man-
grove areas in the storm-affected region prior to Typhoon Haiyan
(Fig. 2). Typhoon Haiyan transected 5 Landsat path/row footprints
(Fig. 3). Images from the Landsat 7 Enhanced Thematic Mapper Plus
(ETM+) and Landsat 8 Operational Land Imager (OLI) sensors captured
Fig. 2. Methods workflow for mapping impact of Typhoon Haiyan on the Philippines' mangrove forests.
within 8 months prior to Haiyan's passing were selected from the U.S.
Geological Survey Earth Resources Observation and Science (USGS
EROS) Center archive through the Global Visualizing Viewer (GloVis)
(U.S. Geological Survey, 2016b) for 5 Landsat footprints (Table 1).
Once Landsat imagery were visually selected, surface reflectance
Landsat imagery were downloaded from the USGS EROS Science Pro-
cessing Architecture (ESPA) on demand interface (U.S. Geological
Survey, 2016d). Surface reflectance data provided via ESPA are generat-
ed from the Landsat Ecosystem Disturbance Adaptive Processing Sys-
tem (LEDAPS). The LEDAPS software applies the 6S radiative transfer
model (Kotchenova et al., 2006) to Level-1 Landsat data products.
Landsat sensors have a relatively low temporal resolution with a
combined revisit time every 8 days, so regions of the world that are per-
sistently cloudy such as the Philippines, particularly during the rainy
season (i.e., June through November), can be difficult to monitor with
single-date Landsat imagery. Therefore, several Landsat images were re-
quired per Landsat path/row footprint for complete mangrove classifi-
cation because of partial cloud cover. Landsat image pre-processing
included stacking, masking cloudy pixels and cloud filling, and Normal-
ized Difference Vegetation Index (NDVI) transformation (Fig. 2). Cloudy
pixels were identified using the Fmask algorithm (Zhu and Woodcock,
2012) and filled using a Spectral Similarity Grouping (SSG) approach
with secondary Landsat imagery (Jin et al., 2013).
 J. Long et al. / Marine Pollution Bulletin 109 (2016) 734–743 737

Fig. 3. Landsat path/row footprints over Typhoon Haiyan eye transect.

Mangrove areas were mapped using a supervised decision-tree clas-
sification applied to a multilayer data stack. The mapped region of inter-
est included approximately 17.5% (42,098 ha) of the Philippines' total
mangrove area (Fig. 3). Several studies have obtained high mangrove
land cover classification accuracy using a supervised decision-tree ap-
proach applied to Landsat imagery and vegetation indices (Giri et al.,
2011a; Heumann, 2011b; Long et al., 2013; Zhang, 2011). For example,
a 2010 national mangrove land cover map for the Philippines used a de-
cision-tree classification approach and has a reported overall accuracy
of 93% (Long et al., 2013). Training data of known land cover samples
for three target classes: i) mangrove ii) water and iii) terrestrial non-
mangrove, were collected from very high resolution imagery and
Landsat imagery. Very high resolution satellite data with a spatial reso-
lution of 5 m or less were downloaded from the USGS EROS Hazards
Data Distribution System (HDDS) Explorer (U.S. Geological Survey,
2016c) and the National Geospatial Agency's (NGA) Web-based Access
and Retrieval Portal (WARP) (National Geospatial-Intelligence Agency,
2014). Very-high resolution data sensors included WorldView-2,
IKONOS-2, and QuickBird-2. The decision-tree ‘rule set’ was generated
using See5 commercial software (Rulequest Research, 2011). Indepen-
dent variables in the multilayer stack included Landsat spectral bands
1, 2, 3, 4, 5, and 7 for ETM+ sensor and 2, 3, 4, 5, 6, and 7 for OLI sensor,
a 30 m Digital Elevation Model (DEM) derived from Shuttle Radar To-
pography Mission (SRTM) (Farr et al., 2007), a Slope index generated
from the 30 m DEM, NDVI index, and a 30 m 2010 mangrove land
cover map consisting of three thematic classes: i) mangrove ii) water
and iii) terrestrial non-mangrove (Long et al., 2013). Band ratios, such
as NDVI, potentially increase spectral separability of mangrove from
non-mangrove vegetation cover (Heumann, 2011a) and DEMs poten-
tially increase separability of low-lying mangrove from upland forest
(Jones et al., 2014; Lee et al., 2004). Following classification, we per-
formed a chi-squared test to determine which variables the decision-
tree classifier used the most and found that the Landsat surface reflec-
tance bands were the highest used variables, followed by elevation
data layers, the 2010 mangrove land cover map, and NDVI (Table 2). It
is likely that NDVI values of mangrove were similar to other land
cover types (e.g., upland forest and agriculture areas) and were ineffec-
tive to the decision-tree classifier in this case study. Additionally, the
thematic mangrove classification independent variable was not highly
utilized by the classifier likely because of differences in dependent
class labels and the independent class labels, most notably in the terres-
trial non-mangrove and water classes.
2.3. Mangrove classification accuracy assessment

Table 1 An accuracy assessment was performed using a total of 250 random

Landsat imagery acquired for mangrove mapping analysis. points: 50 points for mangrove class, 100 points for terrestrial non-
Landsat path/row Satellite sensor Date acquired Table 2
P112 OLI 4/13/2013 Rank order of independent variables used by decision-tree classifier.
R52 OLI 4/29/2013
Rank Variable
P113 OLI 5/22/2013
R52 OLI 7/25/2013 1 ETM+ Band 1 OLI Band 2
OLI 8/10/2013 2 ETM+ Band 3 OLI Band 4
P114 ETM+ 4/3/2013 3 ETM+ Band 2 OLI Band 3
R52 OLI 9/2/2013 4 ETM+ Band 7 OLI Band 7
P115 ETM+ 8/16/2013 5 ETM+ Band 5 OLI Band 6
R52 OLI 7/7/2013 6 ETM+ Band 4 OLI Band 5
OLI 9/9/2013 7 SRTM DEM
P116 ETM+ 3/16/2013 8 DEM Slope
R52 ETM+ 4/1/2013 9 Mangrove 2010
ETM+ 5/19/2013 10 NDVI
738 J. Long et al. / Marine Pollution Bulletin 109 (2016) 734–743
Table 3
Error matrix for 2013 mangrove land cover classification.
Reference
Predicted
Mangrove Land Water Total
Mangrove 45 1 0 46
Land 5 99 0 104
Water 0 0 100 100
Total 50 100 100
Producer's % 90 99 100
Overall
mangrove class, and 100 points for water class. The randomly generated
points were overlaid and compared with high resolution imagery from
Google Earth Pro™. High resolution imagery used in assessment were
captured on 2/29/2012, 5/23/2012, 3/31/2013, 4/30/2013, 5/17/2013,
6/30/2013, and 8/26/2013. An error matrix was constructed to cross
tabulate the observed data with the reference data (Table 3)
(Congalton, 1991). The accuracy assessment indicates high classifica-
tion accuracy, with an overall accuracy of 97%, a producer accuracy of
90% and a user accuracy of 97% for mangrove cover (Table 3). The ma-
jority of misclassification errors occurred where mangrove areas were
incorrectly mapped as terrestrial non-mangrove (i.e., land).
2.4. Time-series eMODIS
Expedited Moderate Resolution Imaging Spectroradiometer
(eMODIS) data were used to monitor and quantify changes in mangrove
condition resulting from Haiyan. The eMODIS collection is derived from
250 m MODIS data (Jenkerson et al., 2010). MODIS provides surface re-
flectance data with a higher temporal resolution than Landsat, revisiting
once to twice per day, while Landsat combined sensor (ETM+ and OLI)
revisit time is every 8 days. The higher temporal resolution of MODIS is
particularly advantageous in obtaining timely information and quality
cloud-free observations in tropical regions like the Philippines, which
is not possible with Landsat data. Moderate resolution eMODIS data
were downloaded through EarthExplorer (U.S. Geological Survey,
2016a). The eMODIS datasets include acquisition, quality, and NDVI in-
formation at 250 m spatial resolution.
NDVI is one of the most widely applied proxies used to measure and
monitor plant growth, vegetation cover, and biomass production and
has been extensively used for vegetation monitoring, crop yield assess-
ment, and drought detection (Ill et al., 1997; Peters et al., 2002;
Pettorelli, 2013; Tucker, 1979). NDVI exploits the contrasting character-
istics of the red and near-infrared (NIR) spectral bands and is calculated
using the following formula:NDVI = (NIR − RED)/(NIR + RED). Values
for NDVI range from −1.0 to 1.0, where densely vegetated areas (e.g.,
closed canopy tropical forest) generally yield high NDVI values (0.6 to
0.9), sparsely vegetated areas (e.g., open shrub and grasslands) yield
moderate values (0.2 to 0.3), and non-vegetated surfaces (e.g., bare
rock, water, and snow) yield lower NDVI values (0.1 and lower) (U.S.
Geological Survey, 2015). Dense and healthy mangrove forests typically
have NDVI values greater than 0.7 year round (Fig. 4). NDVI of man-
grove forests remains high year round because they are largely ever-
green plants. Several studies have employed repeated measures of
NDVI to monitor mangrove vegetation response from varying distur-
bances (Giri et al., 2011a; Satyanarayana et al., 2011), but few have ap-
plied this approach to monitor mangrove disturbance from tropical
cyclones (Wang, 2012).
The eMODIS products available for our study region included 10-day
composited data sets. NDVI can be sensitive to atmospheric scattering
and absorption, as well as variations in the illumination and viewing
conditions (Kerekes, 1994); however, the eMODIS composite selection
process minimizes these artifacts by filtering through input surface re-
flectance data and flagging poor quality pixels with negative values,
clouds, snow cover, low view angles, or low sun angle and labeling
User's %
97
95
100
97
Fig. 4. Phenology of mangrove area located in Palawan, Philippines (12°16′10.38″N, 119°
54′48.28″E). Monthly NDVI observations derived from 250 m 16-day MODIS NDVI
products. NDVI remained between 7.5 and 9.5 during the 2-year observation period
(2011–2012).
these pixels in a quality band (Jenkerson et al., 2010). We further pre-
processed the standard 10-day eMODIS data to generate NDVI time se-
ries composites prior to, and three time periods following, Typhoon
Haiyan: 6 months prior (April 15, 2013–November 4, 2013) (B); 1 to
6 months after (November 21, 2013–May 26, 2014) (A1); 7 to
12 months after (June 5, 2014–November 6, 2014) (A2); and 12 to
18 months after (November 6, 2014 – May6, 2014) (A3). Our eMODIS
pre-processing algorithm took raw 10-day eMODIS data and performed
data stacking, poor quality pixel removal based on the image quality
data provided, and calculated the median NDVI value per pixel to pro-
duce a smoothed cloud-free NDVI composite for each of the three
time periods. Only data with known high quality indicated in the quality
layer were analyzed. Next, the 30 m mangrove map derived from
Landsat imagery was resampled to 250 m resolution using a nearest
neighbor resampling method and applied to mask areas where only
mangrove are located for all eMODIS time series composites (B, A1,
A2, and A3). The differences of B and A1, B and A2, and B and A3 NDVI
composites were calculated to create NDVI change maps of mangrove
areas for the three time periods following Haiyan. Finally, we classified
mangrove change into three damage level categories. Mangrove areas
where NDVI decreased by 0.2 to 0.3, 0.3 to 0.5, and 0.5 or greater were
classified into Minimal (i.e., mostly intact, minor defoliation), Moderate
(i.e., branches broken, tree trunks partially broken, but still standing and
mostly defoliated), or Severe damage (i.e., trees uprooted or trunks bro-
ken at base and completely defoliated) level categories, respectively.
2.5. Ground referencing
Mangrove change maps were quality checked with independently
collected field photos and field notes. Two field teams conducted field
observations of mangrove damage from Haiyan in Eastern Samar and
Leyte over a total of 7 days in January and March of 2014. With coordi-
nation by the Zoological Society of London (ZSL), the teams comprised
17 participants from non-governmental organizations (NGOs), univer-
sities, and the Philippine government. The locations surveyed included
Quinapondan, Guiuan (Bagongbanwa Island), Salcedo (Maliwaliw Is-
land and Abejao), General MacArthur, Hernani, and Lawaan in Eastern
Samar, and Ormoc City, Palompon, Isabel, Merida, Carigara, Palo, and
Tacloban City in Leyte. Mangrove damage and recovery potential were
assessed for 39 plots using two methods. First, counts of live seedlings,
saplings, and trees were made in 10 × 10 m or 4 × 4 m plots. Second,
the degree of defoliation and other damage of trees was classified as
minimally damaged (i.e., intact), partially damaged (i.e., branches bro-
ken, tree trunks partially broken but still standing and with or without
sprouts), or totally damaged (i.e., trees uprooted or trunks broken at
the base without sprouts). Mangrove damage maps produced from
this study were quality checked with ground observations by overlaying
georeferenced ground observations points over mangrove damage
 J. Long et al. / Marine Pollution Bulletin 109 (2016) 734–743
maps and comparing field note damage level classifications and
georeferenced photos with mapped damage level category.
3. Results
We found general patterns of mangrove damage with the greatest
decreases in NDVI values, indicating increasing severity of mangrove
disturbance, occurring in proximity to Typhoon Haiyan's eye transect.
According to Chen et al. (Chen et al., 2013), most tropical storms cause
the greatest damage severity on the right and front side of the eye
track, where wind and wave stress can be up to 25% greater than on
the left. Consistent with most tropical storms (Dahal et al., 2014), the
greatest extent of moderately and severely damaged mangrove oc-
curred on the right side (i.e., north side of Haiyan transect) of the
storm eye track and generally decreased with increasing distance from
the eye path (Fig. 5); however, non-linear spatial patterns of mangrove
damage were observed in some areas. For example, mangroves in
Southwestern Matarinao Bay were less-severely damaged compared
with mangroves further north from the eye transect in Northern
Matarinao Bay and near Hernani (Fig. 6). This non-linear damage likely
resulted from variations in storm surge intensity, bathymetry and to-
pography, wind speed and direction, and type and condition of the
existing mangrove vegetation. Additionally, damaged mangrove extent
ranging from 0 to 10 km north of Haiyan was relatively low because
mangrove extent is relatively low in this region (i.e. less than
1500 ha.). Overall, mangrove damage was greatest in extent and sever-
ity 20 to 30 km north of Hiayan's eye path where Haiyan first made
landfall in the eastern Philippines and lessened corresponding with de-
creasing storm intensity as Haiyan tracked from east to west (Fig. 5).
Total mangrove area initially impacted (i.e., mangrove experiencing
NDVI decreases greater than or equal to 0.2 during time period A1) by
Haiyan was 8568 ha, about 3.5% of the Philippines' total mangrove
area or 20.4% of the region of interest's total mangrove area. Nearly
870 ha of mangrove were severely damaged, 1820 ha were moderately
damaged, and 5900 ha were minimally damaged during this time peri-
od (Fig. 7).
Fig. 5. Mangrove damage observed at 1 degree longitude intervals (A) and 10 km intervals
north and south of Haiyan's eye path (B) during time period A1.
739
The majority of severely and moderately damaged mangrove was
identified in Eastern Samar, Western Samar, and Leyte provinces, in-
cluding mangrove areas along Matarinao Bay north to Hernani and
from Guiuan west to Balangiga (Fig. 6). As Haiyan tracked east to west
it impacted mangroves in Leyte province, from Ormoc City west to
Isabel, and north to Tabango. Haiyan crossed the northern tip of Cebu,
causing moderate damage to mangroves. Haiyan also caused moderate
damage to mangroves in northern Iloilo, northern Capiz, and northern
Aklan, although damage was minimal in extent because mangroves in
this region are highly fragmented from aquaculture development and
mangrove area is relatively small. Haiyan's intensity lessened to a cate-
gory 4 before passing over northern Palawan (Fig. 1); minimal and
moderate mangrove damage was detected here, but was negligible in
terms of area compared with mangroves in the Eastern Samar, Western
Samar, and Leyte provinces.
Severely, moderately, and minimally damaged mangrove respec-
tively decreased by 90%, 81%, and 57% within 18 months following
Haiyan (Fig. 7). Very high R-squared values near 1.0 indicate mangrove
damage recovered near linearly for all damage level (Fig. 7). Based on
linear extrapolation, if the remaining damaged mangrove continues to
recover at constant rates, minimally damaged mangrove could poten-
tially recover completely within 12 months following time period A3
and moderately and severely damaged mangrove could potentially re-
cover completely within 6 months following time period A3; although,
Wang (Wang, 2012) reported that mangrove recovery following a cate-
gory 5 hurricane disturbance in southern Florida did not recover linearly
and recovery was greatest in the first year, slowed in the second year,
and was minimal in the third year.
A complete statistical validation was not performed on the man-
grove damage maps because of inadequate reference data across the
study area; however, georeferenced field photos collected during inde-
pendent field surveys following Haiyan indicate our results are consis-
tent with on-the-ground mangrove condition observations (Primavera
et al., 2016). Fig. 8 (A) illustrates a mangrove area on Anahaw Island,
Eastern Samar, in Matarinao Bay where our change analysis indicated
mangrove damage was minimal during time period A1. Ground obser-
vations showed mangrove cover remained intact and the field team
measured minimal observable defoliation or blowdown. Fig. 8 (B) illus-
trates a mangrove area on Tubabao Island, Guiuan, in the Leyte Gulf that
we classified as moderately damaged (NDVI decreased by 0.4) during
time period A1; consistent with field observations, Haiyan caused mod-
erate damage in this area. Fig. 8 (C) shows a mangrove area on Tubabao
Island, Guiuan, in the Leyte Gulf that we classified as severely damaged;
ground observation were consistent with damage maps indicating se-
vere damage to mangrove. Such field surveys found that the majority
severely damaged mangroves were plantations of Rhizophora while
most natural mangrove stands were recovering from minimal and mod-
erate damage (Primavera et al., 2016).
4. Discussion
Tropical storms are a frequently occurring phenomenon in the Phil-
ippines and greatly influence mangrove forest dynamics. Similar to
most mangroves worldwide, mangroves in the Philippines are mostly
located in remote and inaccessible regions, making it difficult, if not im-
possible, to conduct a comprehensive impact assessment from field sur-
veys alone. Remote sensing offers consistent, timely, and reliable
measurements that allow disturbance monitoring across large areas.
The results from this study indicate that a hybrid remote sensing ap-
proach using a combination of medium-resolution Landsat and time-se-
ries eMODIS data is effective for identifying storm damage severity and
recovery response of mangrove ecosystems. These findings are support-
ed by ground-referencing using field surveys at impacted sites. Our
analysis found that nearly 3.5% of the Philippines' total mangrove area
was initially impacted by Haiyan. There was a high degree of spatial var-
iation in mangrove damage with damage found to be greatest in extent
740 J. Long et al. / Marine Pollution Bulletin 109 (2016) 734–743
Fig. 6. Mangrove damage across the Philippines. Mangrove damage was greatest in severity and extent in Eastern Samar where Haiyan made first landfall in the Philippines.
and severity in the Eastern Samar, Western Samar, and Leyte provinces
where Haiyan initially made landfall. Of the total impacted mangrove
area, approximately 868 ha of mangrove experienced severe damage,
with Eastern Samar experiencing the majority of severe and moderate
mangrove damage.
Despite the initial damage caused to 3.5% of the Philippines' total
mangrove area, the majority of damaged mangrove recovered within
18 months following Super Typhoon Haiyan and, in the absence of fur-
ther typhoons or other perturbations. These findings demonstrate the
value of remote sensing as an ongoing monitoring tool to assess damage
and document recovery, and also indicate that some of the initial dam-
age was likely due to defoliation rather than mortality. Additionally,
ground referencing surveys provide an important validation of the
true status of mangroves post-typhoon and need to be integrated into
Fig. 7. Total mangrove area impacted by Typhoon Haiyan. Time periods after Haiyan: 1–
6 months (A1), 7–12 month (A2), and 13–18 months (A3).
any remote sensing methodology. These findings have implications for
government policy. The immediate response of the Philippine govern-
ment to Haiyan was to allocate approximately 350 million Philippine
pesos (US $7.4 million dollars) to re-plant mangroves in thousands of
hectares along hundreds of kilometers of coastline (Department of
Environment and Natural Resources, 2013). The present results suggest
that mangrove recovery should be surveyed as late as 1.5 years
(18 months) following a category 5 typhoon to determine if mangrove
areas require rehabilitation. This study suggests that natural recovery
and regeneration would be a more economically and ecologically viable
strategy.
The high mangrove recovery rates we observed in a relatively short
amount of time (1.5 years) further demonstrate the resilience of man-
groves to inordinately powerful tropical cyclones. These findings are
consistent with several studies affirming mangroves resilience and
high rate of recovery shortly following natural perturbations across
the globe (Alongi, 2008; Aung et al., 2013; Ayyappan et al., 2016;
Herbert et al., 1999; Wang, 2012). The resilience of the Philippines'
mangroves, and hence their ability to act as an important buffer for
coastal communities, could be enhanced through domestic policies
and measures to reduce recent rates of loss (i.e., 10.5% total mangrove
loss from 1990 to 2010) primarily resulting from anthropogenic activi-
ties (Long et al., 2013). Dating back to the 1970s, the Philippine green-
belt laws require mangrove buffer zones of 50–100 m facing open seas
and 20–50 m along riverbanks (e.g., Presidential Decree (PD) 705 of
1975, PD 953 of 1976, PD 1067, MNR Administrative Order (AO) 42 of
1986, DENR AO 76 of 1987), but these laws have been observed more
in the breach than in the compliance (Primavera, 2000). In the wake
of the 2004 tsunami, Primavera (Primavera, 2005b) called for their im-
plementation by planting mangrove greenbelts. Nearly a decade later
with the added urgency from the damage to life and property caused
by Typhoon Haiyan, this advocacy has resulted in the filing of the Na-
tional Coastal Greenbelt Bill in the Philippine Senate (National Coastal
Greenbelt Act of 2014, 2014), that mandates a 100 m wide band of man-
grove vegetation. Remote sensing observations, as applied in this study,
can be a viable approach to documenting how effectively this legislation
 J. Long et al. / Marine Pollution Bulletin 109 (2016) 734–743 741

Fig. 8. (A) Mangrove area on Anahaw Island, Matarinao Bay in Eastern Samar where change analysis indicated minimal mangrove damage (NDVI decreased by 0.1 from B to A1 time
periods). Ground observation agreed with damage maps showing minimal damage to mangrove. (B) Mangrove area on Tubabao Island, Guiuan, in Leyte Gulf where change analysis
indicated moderate mangrove damage (NDVI decreased by 0.4 from B to A1 time periods). Consistent with field observations, Haiyan caused moderate damage (i.e., branches broken,
tree trunks partially broken but still standing and with shoots) in this location. (C) Mangrove area on Tubabao Island, Guiuan, in Leyte Gulf where change analysis indicated severe
mangrove damage (NDVI decreased by 0.6 from B to A1 time periods). Ground observation agreed with damage maps showing severe damage to mangrove. (Photos ZSL/Amado Blanco).

is implemented over time to restore coastal mangrove greenbelts in the
Philippines.
It is vital that mangrove replanting activities are scientifically
based to ensure the correct species are planted in the correct loca-
tions and with the support of local communities to ensure ongoing
maintenance and protection (Primavera et al., 2012). Mangrove
replanting schemes are currently dominated by those resulting in
mono-type plantations (e.g., planting only Rhizophora) often with
low survival rates, or impact on other important habitats such as
mudflats and seagrass beds (Alongi, 2002; Erftemeijer and Lewis,
1999; Field, 1999; Walters, 2000). Further research is needed into
the relative resilience of these mono-type species mangrove planta-
tions versus natural mixed species stands. Small-scale studies in
Panay have shown that severe damage from Typhoon Haiyan was
much higher in mono-type Rhizophora plantations than in diverse
natural mangrove forests (Primavera et al., 2016). Aung et al.
(2013) also observed higher mortality rates (N90%) among mono-
type Rhizophora stands compared with non-Rhizophora stands
(b 20%) following a typhoon disturbance in Myanmar.
The data and findings from this study are useful for developing man-
grove rehabilitation and conservation strategies and provide baseline
information for future monitoring. Long-term monitoring of mangrove
areas impacted by Typhoon Haiyan using ground and remote sensing
observations is needed to fully understand the impacts on the
ecosystem.
Author contributions
All listed authors contributed to study design. Authors Long and Giri
performed analysis and Long prepared figures and wrote the first draft
of the manuscript. Giri, Primavera, and Trivedi revised the draft. Prima-
vera and Filipino colleagues organized the field surveys, with sugges-
tions from Trivedi. All authors read and approved the final version of
the manuscript.
Conflicts of Interest
The authors declare no conflicts of interest.
742 J. Long et al. / Marine Pollution Bulletin 109 (2016) 734–743
Acknowledgments
Any use of trade, firm, or product names is for descriptive purposes
only and does not imply endorsement by the U.S. Government. Work per-
formed under U.S. Geological Survey contract G13PC00028. ZSL gratefully
acknowledge the efforts of the field team including representatives from
Guiuan Development Foundation (GDFI), Environmental Leadership and
Training Initiative (ELTI), Haribon Foundation, Tambuyog Development
Center, Conservation International, University of the Philippines Diliman,
University of the Philippines Tacloban College, Ateneo University, La Salle
University, and the Department of Environment and Natural Resources
(DENR), Region 6. ZSL is also grateful to Christian Aid and the Darwin Ini-
tiative for funding the field surveys and Dr. Primavera. We appreciatively
acknowledge peer and anonymous reviewers.
References
National Coastal Greenbelt Act of 2014 (Ed.), 2014. Senate Bill 2179, First ed.
Alongi, D.M., 2002. Present state and future of the world's mangrove forests. Environ.
Conserv. 29, 331–349.
Alongi, D.M., 2008. Mangrove forests: resilience, protection from tsunamis, and responses
to global climate change. Estuar. Coast. Shelf Sci. 76, 1–13.
Aung, T.T., Mochida, Y., Than, M.M., 2013. Prediction of recovery pathways of cyclone-dis-
turbed mangroves in the mega delta of Myanmar. For. Ecol. Manag. 293, 103–113.
Ayyappan, N., Stephen, A., Muthusankar, G., Jeyakumar, S., Presena, J., 2016. Spatio-tem-
poral changes in fringe mangrove extent in Pondicherry, India after two phenomenal
perturbations: tsunami and cyclone Thane. Trop. Ecol. 57, 361–368.
Bankoff, G., 2012. Cultures of Disaster: Society and Natural Hazard in the Philippines.
Routledge.
Chen, S.S., Zhao, W., Donelan, M.A., Tolman, H.L., 2013. Directional wind–wave coupling in
fully coupled atmosphere–wave–ocean models: results from CBLAST-Hurricane.
J. Atmos. Sci. 70, 3198–3215.
Chmura, G.L., Anisfeld, S.C., Cahoon, D.R., Lynch, J.C., 2003. Global carbon sequestration in
tidal, saline wetland soils. Glob. Biogeochem. Cycles 17, 1111.
Congalton, R.G., 1991. A review of assessing the accuracy of classifications of remotely
sensed data. Remote Sens. Environ. 37, 35–46.
Cornforth, W., Fatoyinbo, T., Freemantle, T., Pettorelli, N., 2013. Advanced Land Observing
Satellite Phased Array Type L-Band SAR (ALOS PALSAR) to inform the conservation of
mangroves: sundarbans as a case study. Remote Sens. 5, 224–237.
Dahal, D., Liu, S., Oeding, J., 2014. The carbon cycle and hurricanes in the United States be-
tween 1900 and 2011. Sci. Rep. 4, 5197.
Department of Environment and Natural Resources, 2013. DENR sets aside P347M for
coastal forest rehabilitation in Eastern Visayas. http://www.denr.gov.ph/news-and-
features/latest-news/1604-denr-sets-aside-p347m-for-coastal-forest-rehabilitation-
in-eastern-visayas.html.
Duke, N.C., Meynecke, J.-O., Dittmann, S., Ellison, A.M., Anger, K., Berger, U., Cannicci, S.,
Diele, K., Ewel, K.C., Field, C.D., 2007. A world without mangroves? Science 317,
41–42.
Erftemeijer, P.L., Lewis, R.R., 1999. Planting Mangroves on Intertidal Mudflats: Habitat
Restoration or Habitat Conversion, Proceedings of the ECOTONE VIII Seminar Enhanc-
ing Coastal Ecosystems Restoration for the 21st Century. Ranong, Thailand,
pp. 23–28.
Farr, T.G., Rosen, P.A., Caro, E., Crippen, R., Duren, R., Hensley, S., Kobrick, M., Paller, M.,
Rodriguez, E., Roth, L., 2007. The shuttle radar topography mission. Rev. Geophys. 45.
Field, C., 1999. Rehabilitation of mangrove ecosystems: an overview. Mar. Pollut. Bull. 37,
383–392.
Food and Agriculture Organization of the United Nations, 2007. The World's Mangroves,
1980–2005: A Thematic Study in the Framework of the Global Forest Resources As-
sessment 2005. Food and Agriculture Organization of the United Nations, Rome.
Garcia, K.B., Malabrigo Jr., P.L., Gevaña, D.T., 2014. Philippines' mangrove ecosystem: sta-
tus, threats and conservation. In: Latiff, A., Hakeem, K.R., Ozturk, M. (Eds.), Faridah-
Hanum, I. Mangrove Ecosystems of Asia, Springer New York, pp. 81–94.
Gilman, E.L., Ellison, J., Duke, N.C., Field, C., 2008. Threats to mangroves from climate
change and adaptation options: A review. Aquat. Bot. 89, 237–250.
Giri, C., Long, J., Tieszen, L., 2011a. Mapping and monitoring Louisiana's mangroves in the
aftermath of the 2010 Gulf of Mexico oil spill. J. Coast. Res. 27, 1059–1064.
Giri, C., Ochieng, E., Tieszen, L.L., Zhu, Z., Singh, A., Loveland, T., Masek, J., Duke, N., 2011b.
Status and distribution of mangrove forests of the world using earth observation sat-
ellite data. Glob. Ecol. Biogeogr. 20, 154–159.
Giri, C., Zhu, Z., Tieszen, L., Singh, A., Gillette, S., Kelmelis, J., 2008. Mangrove forest distri-
butions and dynamics (1975–2005) of the tsunami-affected region of Asia†.
J. Biogeogr. 35, 519–528.
Herbert, D.A., Fownes, J.H., Vitousek, P.M., 1999. Hurricane damage to a Hawaiian forest:
nutrient supply rate affects resistance and resilience. Ecology 80, 908–920.
Heumann, B.W., 2011a. An object-based classification of mangroves using a hybrid deci-
sion tree—support vector machine approach. Remote Sens. 3, 2440.
Heumann, B.W., 2011b. Satellite remote sensing of mangrove forests: Recent advances
and future opportunities. Prog. Phys. Geogr. 35, 87–108.
Hurrevac, 2014. A storm tracking and decision support tool for government emergency
managers, 1.4.2 ed. http://www.hurrevac.com.
Ill, E.W.R., Chappell, D.K., Baldwin, D.G., 1997. AVHRR imagery used to identify hurricane
damage in a forested wetland of Louisiana. Photogramm. Eng. Remote. Sens. 63,
293–297.
Jenkerson, C., Maiersperger, T., Schmidt, G., 2010. eMODIS: A User-friendly Data Source,
in: Survey, U.S.G. (Ed.). Reston, Virginia, p. 10.
Jimenez, J.A., Lugo, A.E., Cintron, G., 1985. Tree mortality in mangrove forests. Biotropica
17, 177–185.
Jin, S., Homer, C., Yang, L., Xian, G., Fry, J., Danielson, P., Townsend, P.A., 2013. Automated
cloud and shadow detection and filling using two-date Landsat imagery in the USA.
Int. J. Remote Sens. 34, 1540–1560.
Center, Joint Typhoon Warning, 2008. Appendix B: Characteristics of Tropical Cyclones Af-
fecting the Philippine Islands (Shoemaker 1991).
Jones, T.G., Ratsimba, H.R., Ravaoarinorotsihoarana, L., Cripps, G., Bey, A., 2014. Ecological
variability and carbon stock estimates of mangrove ecosystems in northwestern
Madagascar. Forests 5, 177–205.
Kauffman, J.B., Cole, T., 2010. Micronesian mangrove forest structure and tree responses
to a severe typhoon. Wetlands 30, 1077–1084.
Kerekes, J.P., 1994. NDVI sensitivity to atmospheric water vapor as a function of spectral
bandwidth, Geoscience and Remote Sensing Symposium, 1994. IGARSS '94. Surface
and Atmospheric Remote Sensing: Technologies, Data Analysis and Interpretation.,
International. IEEE, pp. 1506–1508.
Kotchenova, S.Y., Vermote, E.F., Matarrese, R., Klemm Jr., F.J., 2006. Validation of a vector
version of the 6S radiative transfer code for atmospheric correction of satellite data.
Part I: Path radiance. Applied optics Vol. 45, pp. 6762–6774.
Lee, J., Shuai, Y., Zhu, Q., 2004. Using images combined with DEM in classifying forest veg-
etations, Geoscience and Remote Sensing Symposium, 2004. IGARSS '04. Proceedings.
2004 IEEE International. IEEE, pp. 2362–2364.
Lee, S.Y., Primavera, J.H., Dahdouh-Guebas, F., McKee, K., Bosire, J.O., Cannicci, S., Diele, K.,
Fromard, F., Koedam, N., Marchand, C., Mendelssohn, I., Mukherjee, N., Record, S.,
2014. Ecological role and services of tropical mangrove ecosystems: a reassessment.
Glob. Ecol. Biogeogr. 23, 726–743.
Long, J., Napton, D., Giri, C., Graesser, J., 2013. A mapping and monitoring assessment of
the Philippines' mangrove forests from 1990 to 2010. J. Coast. Res. 260–271.
Long, J.B., Giri, C., 2011. Mapping the Philippines' mangrove forests using Landsat imag-
ery. Sensors 11, 2972–2981.
McLeod, E., Chmura, G.L., Bouillon, S., Salm, R., Björk, M., Duarte, C.M., Lovelock, C.E.,
Schlesinger, W.H., Silliman, B.R., 2011. A blueprint for blue carbon: toward an im-
proved understanding of the role of vegetated coastal habitats in sequestering CO2.
Front. Ecol. Environ. 9, 552–560.
Mumby, P.J., Edwards, A.J., Arias-González, J.E., Lindeman, K.C., Blackwell, P.G., Gall,
A., Gorczynska, M.I., Harborne, A.R., Pescod, C.L., Renken, H., 2004. Mangroves
enhance the biomass of coral reef fish communities in the Caribbean. Nature
427, 533–536.
National Disaster Risk Reduction, Management Council, 2013. NDRRMC Update SitRep
No. 74 Effects of Typhoon “Yolanda” (Haiyan). http://www.ndrrmc.gov.ph/
attachments/article/1125/updsitrep74.pdf.
National Geospatial-Intelligence Agency, 2014. Web-based Access and Retrieval Portal.
https://warp.nga.mil.
Paling, E.I., Kobryn, H.T., Humphreys, G., 2008. Assessing the extent of mangrove change
caused by Cyclone Vance in the eastern Exmouth Gulf, northwestern Australia.
Estuar. Coast. Shelf Sci. 77, 603–613.
Peters, A.J., Walter-Shea, E.A., Ji, L., Vina, A., Hayes, M., Svoboda, M.D., 2002. Drought mon-
itoring with NDVI-based standardized vegetation index. Photogramm. Eng. Remote.
Sens. 68, 71–75.
Pettorelli, N., 2013. The Normalized Difference Vegetation Index. Oxford University Press.
Primavera, J.H., 1995. Mangroves and Brackishwater Pond Culture in the Philippines, Asia-
Pacific Symposium on Mangrove Ecosystems. Springer, pp. 303–309.
Primavera, J.H., 2000. Development and conservation of Philippine mangroves: institu-
tional issues. Ecol. Econ. 35, 91–106.
Primavera, J.H., 2005a. Mangroves, fishponds, and the quest for sustainability. Science
310, 57–59.
Primavera, J.H., 2005b. Tsunamis and Mangrove Greenbelts The Philippine Star.
Primavera, J.H., Cruz, M.D., Montilijiao, C., Consunji, H., Paz, M.D., Rollon, R., Maranan, K.,
Samson, M.C., Blanco, A., 2016. Preliminary Assessment of Post-Haiyan Mangrove
Damage and Reocvery in Eastern Samar, Central Philippines (in Press).
Primavera, J.H., Esteban, J., 2008. A review of mangrove rehabilitation in the Philippines:
successes, failures and future prospects. Wetl. Ecol. Manag. 16, 345–358.
Primavera, J.H., Savaris, J., Bajoyo, B., Coching, J., Curnick, D., Golbeque, R., Henderin, A.G.J.,
Joven, R., Loma, R., Koldewey, H., 2012. Manual on Community-Based Mangrove Re-
habilitation, Mangrove Manual Series No. 1. Zoological Society of London, United
Kingdom, p. 240.
Richards, D.R., Friess, D.A., 2016. Rates and drivers of mangrove deforestation in Southeast
Asia, 2000–2012. Proc. Natl. Acad. Sci. 113, 344–349.
Rulequest Research, 2011. See5/c5.0. http://www.rulequest.com/see5-info.html.
Satyanarayana, B., Mohamad, K.A., Idris, I.F., Husain, M.-L., Dahdouh-Guebas, F., 2011. As-
sessment of mangrove vegetation based on remote sensing and ground-truth mea-
surements at Tumpat, Kelantan Delta, East Coast of Peninsular Malaysia. Int.
J. Remote Sens. 32, 1635–1650.
Siikamäki, J., Sanchirico, J.N., Jardine, S.L., 2012. Global economic potential for reducing
carbon dioxide emissions from mangrove loss. Proc. Natl. Acad. Sci. 109,
14369–14374.
Smith, T.J., Anderson, G.H., Balentine, K., Tiling, G., Ward, G.A., Whelan, K.R.T., 2009. Cu-
mulative impacts of hurricanes on Florida mangrove ecosystems: sediment deposi-
tion, storm surges and vegetation. Wetlands 29, 24–34.
Tucker, C.J., 1979. Red and photographic infrared linear combinations for monitoring veg-
etation. Remote Sens. Environ. 8, 127–150.
 J. Long et al. / Marine Pollution Bulletin 109 (2016) 734–743
Twilley, R.R., Chen, R.H., Hargis, T., 1992. Carbon sinks in mangroves and their implica-
tions to carbon budget of tropical coastal ecosystems. Water Air Soil Pollut. 64,
265–288.
U.S. Geological Survey, 2015. Remote Sensing Phenology. http://phenology.cr.usgs.gov/
ndvi_foundation.php.
U.S. Geological Survey, 2016a. Earth Explorer. http://earthexplorer.usgs.gov.
U.S. Geological Survey, 2016b. Global Visualization Viewer (GloVis). http://glovis.usgs.
gov.
U.S. Geological Survey, 2016c. Hazards Data Distribution Systems Explorer. http://
hddsexplorer.usgs.gov.
U.S. Geological Survey, 2016d. LSDS Science Research and Development. http://espa.cr.
usgs.gov.
United States Agency for International Development, 2014. Philippines - Typoon Yolanda/
Haiyan, FACT SHEET #22. FISCAL YEAR (FY). Vol. 2014, p. 7.
UNU-EHS, 2014. World Risk Report. In: Lars Jeschonnek, M. (Ed.), United Nations Univer-
sity, Institute for Environment and Human Security.
743
Van Lavieren, H., Spalding, M., Alongi, D.M., Kainuma, M., Clüsener-Godt, M., Adeel, Z.,
2012. Securing the future of mangroves.
Walters, B.B., 2000. Local mangrove planting in the Philippines: are fisherfolk and fish-
pond owners effective restorationists? Restor. Ecol. 8, 237–246.
Walters, B.B., 2005. Patterns of local wood use and cutting of Philippine mangrove forests.
Econ. Bot. 59, 66–76.
Wang, F., D'Sa, E.J., 2009. Potential of MODIS EVI in identifying hurricane disturbance to
coastal vegetation in the northern Gulf of Mexico. Remote Sens. 2, 1–18.
Wang, Y., 2012. Detecting Vegetation Recovery Patterns After Hurricanes in South Florida
Using NDVI Time Series.
Zhang, X.-H., 2011. Identification of Mangrove Using Decision Tree Method, Information
and Computing (ICIC). 2011 Fourth International Conference on. IEEE, pp. 130–132.
Zhu, Z., Woodcock, C.E., 2012. Object-based cloud and cloud shadow detection in Landsat
imagery. Remote Sens. Environ. 118, 83–94.