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Harmful Algae 7 (2008) 324–330

An extensive Cochlodinium bloom along the western

coast of Palawan, Philippines

Rhodora V. Azanza a,*, Laura T. David a, Roselle T. Borja a,Iris U. Baula a, Yasuwo Fukuyo b

a The Marine Science Institute, University of the Philippines, Diliman, Quezon City 1101, Philippinesb Asian Natural Environmental Science Center, The University of Tokyo, Yayoi 1-1-1 Bunkyo-ku, Tokyo 113-8657, Japan

Received 13 October 2006; received in revised form 10 April 2007; accepted 3 December 2007

Abstract

A massive fish kill and water discoloration were reported off the western coast of Puerto Princesa, Palawan, Philippines in March 2005.

Phytoplankton analysis revealed a near monospecific bloom of the dinoflagellate, Cochlodinium polykrikoides, with cell concentrations ranging

from 2.5 � 105 to 3.2 � 106 cells per liter. Ground truth data were supplemented by processed satellite images from MODIS Aqua Level 2 data

(1 km resolution) from January to April 2005, which revealed high surface chlorophyll-a levels (up to 50 mg/m3) offshore of west and southwest

Palawan as early as February 2005. The bloom extended 310 km in length and 80 km in width at its peak in March off the central coast (Puerto

Princesa). By April, the bloom declined in intensity, but was still apparent along the northern coast (El Nido). Fluctuations in chlorophyll levels off

the western coast of Sabah, Malaysia and Brunei during this time period suggested that the bloom was not limited to the coast of Palawan. Satellite

imagery from Sabah in late January revealed a plume of chl-a that is believed to be the source of the C. polykrikoides bloom in Palawan. This plume

drifted offshore, advected northward via the basin-wide counterclockwise gyre, and reached nutrient-rich, upwelled waters near Palawan (due to a

positive wind stress curl) where the dinoflagellate bloomed and persisted for 2 months from March to April 2005.

# 2008 Elsevier B.V. All rights reserved.

Keywords: Cochlodinium polykrikoides; Fish kills; Philippines; Remote sensing

1. Introduction

The unarmored, chain-forming, gyrodinioid dinoflagellate

species, Cochlodinium polykrikoides Margalef is characterized

by having a conical epitheca and a bilobed hypotheca with

single cells being ellipsoidal having a displaced cingulum. This

species commonly occurs in warm-temperate and tropical

waters (Steidinger and Tangen, 1997). In Asia, C. polykrikoides

is notorious for causing fish kills in Japan, Korea and China. For

example, Kim (1997) reported that damages to Korean fisheries

due to blooms of this organism totaled USD $95.5 million in

1995. More recently, red tides caused by C. polykrikoides have

been documented in Southeast Asia, and particularly in the

Philippines (Vicente et al., 2002; Relox and Bajarias, 2003),

Sabah, Malaysia (Anton et al., 2006) and Brunei (S. Taha, pers.

comm.).

* Corresponding author. Tel.: +63 2 9215967; fax: +63 2 9215967.

E-mail address: rhod@upmsi.ph (R.V. Azanza).

1568-9883/$ – see front matter # 2008 Elsevier B.V. All rights reserved.

doi:10.1016/j.hal.2007.12.011

The mechanism(s) by which C. polykrikoides kills fish has

been and continues to be a topic of extensive investigation.

Reactive oxygen species such as superoxide anion and

hydrogen peroxide produced by C. polykrikoides have been

recognized as factors likely involved in fish mortalities. Such

reactive oxygen species destroy gill cells as well as induce

excessive mucus secretion from gill epithelia, which can lead to

suffocation (Kim et al., 1999).

The aim of the present paper is to document the extensive

bloom of C. polykrikoides along the west coast of Palawan,

Philippines from February to May 2005 as tracked by field

observations and processed satellite data, including ocean color

(i.e., surface chl-a), sea surface temperature, and wind stress.

Evidence suggesting that blooms observed in the coastal waters

of Palawan may be related to those that occurred in the

neighboring countries of Sabah, Malaysia and Brunei is also

presented. These findings are discussed in relation to better

understanding the origin and transport of Cochlodinium blooms

in this region.

Table 1

Sampling sites, temperature, and salinity recorded along the western coast of

Palawan, Philippines from March to May 2005

Date of

collection

Station Longitude

(8N)

Latitude

(8E)

Temperature

(8C)

Salinity

(ppt)

16 March 2005 PP1 118.4949 9.8068 – –

8 April 2005 EN1 119.3245 11.1462 33 35

8 April 2005 EN2 119.3272 11.1513 36 36

8 April 2005 EN3 119.3260 11.1608 35 36

8 April 2005 EN4 119.3005 11.1435 36 35

8 April 2005 EN5 119.2740 11.1639 33 33

8 April 2005 EN6 119.2730 11.1970 31 35

26 May 2005 EN1 119.3245 11.1462 – –

26 May 2005 EN3 119.3260 11.1608 – –

R.V. Azanza et al. / Harmful Algae 7 (2008) 324–330 325

2. Materials and methods

2.1. Study location and date

The island of Palawan is located in the western part of the

Philippines, lying in the southeastern part of South China Sea

(Fig. 1A). It is about 650 km long and only about 50 km north

of Sabah, Malaysia (lat 5858060N; long 1168400E).

Reddish coloration of the sea surface was sighted along the

southern part of Palawan in February 2005 by local fishermen

and government officials. However, sampling for phytoplank-

ton and fish, and collection of other ground truth data were

performed only from March to May 2005 in the northern

(Fig. 1B) and central (Fig. 1C) parts of the island, following a

request for assistance by government officials. Temperature

was measured with a hand-held thermometer and salinity was

determined using a refractometer. Satellite data were collected

during the period January–April 2005 for the entire length of

Palawan and as far south as Sabah, Malaysia.

2.2. Phytoplankton sampling and analysis

Samples were taken during March–May 2005 along the

western coast of Palawan (Table 1), including six stations in El

Fig. 1. (A) Map of the Philippines showing island of Palawan; (B) west coast of north

of central Palawan (Puerto Princesa) with location of one sampling station.

Nido towards the north (Fig. 1B) and from one station in Puerto

Princesa located in the center of the island (Fig. 1C). A plankton

net with 20-mm mesh having 40.6 cm mouth diameter was used

to collect water samples at 3-m depth. Plankton samples were

preserved with Lugol’s iodine solution and observed under a

Zeiss Axioskop II light microscope at 100� to 1000�magnification. Cell counts were done using a Sedgewick-

Rafter counting chamber and cell concentration was generated

using the formula from Relox (2002): cell density = (number of

ern Palawan (El Nido) with locations of six sampling stations and; (C) west coast

R.V. Azanza et al. / Harmful Algae 7 (2008) 324–330326

cells in 1 mL sample � total volume of sample where 1 mL

aliquot was taken)/(area of mouth of plankton net � hauling

depth). Phytoplankton species were identified according to the

morphological criteria given by Steidinger and Tangen (1997).

2.3. Remote sensing

Ocean color spectra were gathered daily by the MODIS

(Moderate Resolution Imaging Spectroradiometer) instrument

on-board the NASA satellite Aqua, and processed using the

OC3 algorithm to derive estimates of chlorophyll-a (O’Reilly

et al., 2000) and sea surface temperature (SST). The processed

data at 1 km resolution is freely available via the OceanColor

website (http://oceancolor.gsfc.nasa.gov). Chlorophyll-a and

SST data for waters surrounding Palawan and Sabah were

downloaded for the period January–April 2005. However,

complete daily data were not available for this entire period due

to extensive cloud cover in most of the images. Therefore, a 2-

week average was constructed out of 6–12 daily images,

yielding a composite time series with a temporal resolution of

15 days. The limitations associated with this binned approach

are acknowledged, yet unavoidable. It should also be noted that

while humic loading can interfere with the interpretation of

ocean color data from coastal waters, Palawan is devoid of

large rivers, which are a major source of such compounds.

Further, the Palawan west coast experiences a pronounced dry

season from November to April, such that even effects of

groundwater and small rivers would be negligible during the

study period.

Wind stress data were gathered by the SeaWinds instrument

deployed on the QuikSCAT satellite. SeaWinds is a radar

device that measures near-surface wind velocity and wind stress

from the backscatter of microwave pulses transmitted to the

earth. Processed data at 25 km resolution are freely available

through the Physical Oceanography Distributed Active Archive

Center website (http://podaac.jpl.nasa.gov). Daily wind data

were downloaded for the entire South China Sea from July 2004

to June 2005. Wind stress curl was then computed to identify

upwelling areas that could possibly support a dense population

of bloom-forming phytoplankton. Wind stress curl is a

legitimate proxy for surface water divergence, hence, upwel-

ling, in the absence of ocean current data. This can be explained

by the inverse barometer effect, which occurs when the

direction of the wind changes in a counterclockwise (positive)

Table 2

Phytoplankton cell counts (cells per mL) during 2005 from Puerto Princesa (PP) a

Sampling date (station)

16 March

(PP1)

8 April

(EN1)

8 April

(EN2)

8

(

Cochlodinium polykrikoides 3022 1714 1644 1

Other dinoflagellates 4 7 11

% Cochlodinium polykrikoides 99.9 99.6 99.0

Diatoms 0 0 4

Cyanobacteria 0 0 0

Total 3026 1721 1659 1

direction. This wind movement creates a low pressure area over

the sea surface and, by the mechanism of Ekman pumping, lifts

deeper water and channels it upward to establish an upwelling

condition. Wind data were analyzed by calculating the daily

wind stress curl from the wind stress data and summarizing the

frequency of positive curls for a period of 2 weeks.

3. Results

3.1. Phytoplankton, fish, and ground truth physical data

From March to April 2005, near monospecific blooms of C.

polykrikoides (Table 2) were recorded along the western coast

of Palawan (Fig. 1). Those fish affected included reef fish such

as ‘suno’ (Plectropomus leopardus), parrotfish (Scarus sp.),

chinese emperor (Letrinus haematopterus), moray eels

(Gymnothorax undulates), and ‘suran’ (Naso brevirostris), all

of which were seen floating dead off the coast of Palawan.

In El Nido to the north, sampling sites were intensely

discolored similar to the waters in Puerto Princesa more

towards the center of the island. C. polykrikoides comprised

almost 100% of the phytoplankton population in April 2005 in

both areas (Table 2), with maximum cell counts of

3.2 � 106 cells per liter. Sea surface temperature ranged from

31 to 36 8C and salinity from 33 to 36 ppt (Table 1). By May

2005, approximately 60% of the phytoplankton assemblages

were made up of C. polykrikoides (Table 2). The remainder of

the phytoplankton consisted of dinoflagellates (e.g., Ceratium

furca, Akashiwo sanguinea, Peridinium quinquecorne, Pro-

rocentrum lima, Prorocentrum micans, Protoperidinium spp.,

Pyrophacus horolgium, Scrippsiella trochoidea), diatoms

(Bacteriastrum spp., Chaetoceros spp., Coscinodiscus spp.,

Cylindrotheca closterium, Navicula spp., Rhizosolenia spp.),

and cyanobacteria.

3.2. Remote sensing data

Satellite chlorophyll data revealing the extent of the bloom

are shown in Fig. 2. In late February, patches of high chl-a

concentrations (up to 171.44 mg/m3) were noticeable offshore

of southwestern Palawan and approaching the coast of the

southernmost tip of the island (Fig. 2 Box a). This was followed

by a general north-eastward movement of the bloom parallel to

the coast, lasting until early April. The bloom covered a

nd El Nido (EN) in Palawan, Philippines

April

EN3)

8 April

(EN4)

8 April

(EN5)

8 April

(EN6)

26 May

(EN1)

26 May

(EN3)

124 1365 2613 207 0 251

1 0 4 2 76 53

99.7 99.7 99.7 96.3 0.0 59.6

2 4 4 6 42 7

0 0 0 0 0 10

127 1369 2621 215 118 421

Fig. 2. Time series images of surface chl-a concentrations along the Sabah and Palawan coasts from January to April 2005.

R.V. Azanza et al. / Harmful Algae 7 (2008) 324–330 327

distance approximately 500 km from the southern to the

northern tip of mainland Palawan. In addition, very high chl-a

concentrations were evident along the western coast of Sabah,

Malaysia throughout this period beginning as early as January.

A particularly interesting feature noted was a plume of high chl-

a (up to 187 mg/m3) seen in late January and extending from the

Sabah coast into adjacent offshore waters (Fig 2 Box b).

In February, the SST data showed a prominent cold water

tongue that developed off the northwestern tip of the Sabah

coast (Fig. 3). A highly positive wind stress curl frequency was

observed along the coastal areas of Sabah and Palawan in

December (Fig. 4), which is projected to result in upwelling

events leading to nutrient enrichment of surface waters during

the ensuing months (discussed below).

4. Discussion

The Cochlodinium bloom in Palawan was estimated to cover

310 km by 80 km, which compared with previous blooms of

this dinoflagellate in other areas of the Philippines, was

considerably more widespread. In Iligan Bay where Cochlo-

dinium bloomed in March 2002, the bloom spanned 2 km by

0.5 km (Vicente et al., 2002), while in Balayan Bay, Batangas

the bloom covered 7 km by 0.3 km during June of the same year

(Relox and Bajarias, 2003). Temperatures recorded during the

C. polykrikoides bloom in Palawan ranged from 31 8C to 36 8C.

These values are higher than the range of 29–31 8C reported in

the Gulf of California, Mexico for a bloom of the same

organism (Garate-Lizarraga et al., 2004), suggesting a wide

temperature tolerance of this species.

In Palawan, the bloom coincided with mass mortalities of

reef fish, which were the same fish species affected in Balayan

Bay, Batangas in 2002. By comparison, the bloom in Iligan Bay

was associated with demersal and pelagic fish kills (Vicente

et al., 2002), and included the same species affected in

Singapore during the first reported Cochlodinium bloom in

Southeast Asia (Cheong et al., 1984). Other countries in

Southeast Asia that have reported Cochlodinium blooms

include Malaysia (in 2003, 2004, and 2005) and Brunei (in

2004). Interestingly, Pyrodinium bahamense var. compressum,

a species causing paralytic shellfish poisoning (PSP) was found

to co-occur with Cochlodinium in Malaysia (S. Taha, pers.

comm.; Anton et al., 2006).

The spatial and temporal variation in chl-a as detected

through remote sensing coincided with reported bloom events

in situ, both in Palawan and in Sabah, Malaysia. Prior to the

2005 event, no C. polykrikoides bloom had been documented in

Palawan coastal waters. Thus, the origin and mechanism for

development of the bloom described herein is a matter of local

concern. Certainly the role of nearby sources for bloom

initiation (e.g., possible cyst beds in the Philippines and other

adjacent countries) should be considered in attempting to

identify the origin of C. polykrikoides blooms in Palawan.

However, given that in the preceding years blooms of this

species have been reported in the neighboring countries to the

south (i.e., Malaysia and Brunei in 2003, 2004 and 2005), it is

Fig. 3. Time series images of sea surface temperature along the Sabah and Palawan coasts from January to April 2005. Note the difference in scale to emphasize the

tongue of colder water located off the northwest coast of Sabah during February.

Fig. 4. Wind stress curl along the Sabah and Palawan coasts from December 2004 to March 2005, showing a highly positive wind stress curl frequency along the

western coasts of Sabah and Palawan in December 2004.

R.V. Azanza et al. / Harmful Algae 7 (2008) 324–330328

R.V. Azanza et al. / Harmful Algae 7 (2008) 324–330 329

likely that development of the bloom in Palawan was influenced

to some extent by a larger, regional scale forcing.

The East Asian Monsoon exerts a prominent influence over

the entire South China Sea (SCS) region and its bordering

countries. In the SCS, this monsoon period is characterized by

changing wind patterns over a year, with two distinct seasonal

components: the Northeast monsoon, lasting from November to

March is marked by strong winds blowing from the northeast,

creating a single counterclockwise gyre over the entire basin;

and, the Southwest monsoon, lasting from June to September is

characterized by weaker winds out of the southwest, creating a

second gyre in the lower half of the basin moving in a clockwise

direction (Wyrtki, 1961; Hu et al., 2000; Wu et al., 1998; Liu

et al., 2001).

Strong winds along coastal areas have the potential to

generate upwelling or deep mixing, bringing nutrient-rich

water from below the thermocline to the surface and thus

promoting phytoplankton growth. For example, Tang et al.

(2004) have documented the occurrence of a yearly algal bloom

in direct response to coastal upwelling off Vietnam during the

peak of the Southwest monsoon. A similar phytoplankton

growth response has been documented in the northeastern SCS

during the peak of the Northeast monsoon; however, in this

case, winds from the northeast passing over northern Luzon

move in a counterclockwise direction and create a positive wind

stress curl that generates an upwelling event offshore (Udarbe-

Walker and Villanoy, 2001).

In the month of December, a high frequency of positive wind

stress curl was recorded along the coasts of Sabah and Palawan,

which should promote the occurrence of upwelling in these

areas. However, a modeling study by Chu et al. (1998) using the

Princeton Ocean Model demonstrated a 1–3-month lag time

between positive wind stress curl and the manifestation of

surface upwelling in the SCS. Therefore, the occurrence of a

positive wind stress curl in December would be predicted to

result in an upwelling response in January and February. In

addition, an earlier study by San Diego-McGlone et al. (1995)

on the chemical hydrography of the Kalayaan Island Group

(KIG; see Fig. 1), near the site of the present C. polykrikoides

bloom, showed that waters below 100 m are considerably richer

in nutrients compared to the surface. Thus, an upwelling event

could potentially enhance surface nutrient levels enough to

support the growth and accumulation of C. polykrikoides cells.

Indeed, chl-a images following this upwelling event showed

large patches of high chl-a concentrations near the Palawan

coast in late February and during March.

The series of satellite images coupled with prior studies

indicating a cyclonic, basin-wide circulation provides: (1) a

time-series record of the build-up of chl-a along the Sabah and

Palawan coasts, and (2) a temporal association between the C.

polykrikoides blooms in both Sabah and Palawan. However,

because these images are limited only to the region between

Sabah and Palawan, they remain insufficient for identifying the

source of the bloom’s seed population. It has been noted by

Kudela et al. (2008) that this species is present at background

concentrations in the Pacific, Atlantic, and Indian oceans, and

may also exist in offshore sediments as dormant cysts capable

of forming a bloom when triggered by favorable environmental

conditions. Nonetheless, considering that a bloom of C.

polykrikoides was reported earlier in nearby Sabah, we

contend that the cells responsible for initiating the bloom in

Palawan were likely transported from the existing population

off of Sabah. In January 2005 Anton et al. (2006) reported

blooms of Cochlodinium in Sepanggar Bay off Kota Kinabalu,

with maximum densities exceeding 104 cells per liter. The

conspicuous plume of chl-a observed in late January off the

northern coast of Sabah probably transported some of the

dinoflagellate cells into offshore waters. The mixotrophic

capabilities of this species (Jeong et al., 2004) and its high

tolerance to warm salty water (Kim et al., 2004) increase the

likelihood of it survival in these waters. Following their

entrainment into the nutrient-rich, upwelled water near

Palawan, rapid growth of the C. polykrikoides cells may have

lead to development of the bloom. Blooms of Cochlodinium

were again reported in Sabah during 2006 (Anton et al., 2006).

However, northward movement of the bloom population and

its establishment in Palawan did not occur, indicating that

prevailing local conditions were not consistent with those

required for the successful transport of blooms in this region.

Acknowledgements

The help extended by the local residents and municipal

heads of concerned areas in Palawan (especially Puerto

Princesa and El Nido) in the collection of in situ data is greatly

appreciated with special mention to Mayor Edward Hagedorn,

Ms. Mariglo Laririt and Ten Knots Development Corp.

Chlorophyll and wind data from Oceancolor and Physical

Oceanography Distributed Active Archive Center websites,

respectively, are also acknowledged. This study was funded by

the Department of Science and Technology as an ancillary

study of the research program Application of Nuclear

Techniques to Address Specific Harmful Algal Bloom

Concerns Phase II: Development and Application of Predict-

ing, Controlling and Mitigating (PCM) Techniques for

Harmful Algal Blooms (HABs) in Selected Mariculture Sites

in the Philippines; City Government of Puerto Princesa and El

Nido. The help of Ms. Vanessa Mercee D. Vargas in the

incorporation of the revisions of the manuscript is also

recognized.[SES]

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