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Harmful Algae 7 (2008) 523–531

Temporal changes in the cyst densities of Pyrodinium bahamense var.

compressum and other dinoflagellates in Manila Bay, Philippines

Fernando P. Siringan a,b,*, Rhodora V. Azanza a, Neil John H. Macalalad b,Peter B. Zamora a,b, Ma. Yvainne Y. Sta. Maria a,b

a Marine Science Institute, University of the Philippines, Diliman, Quezon City 1101, Philippinesb National Institute of Geological Sciences, University of the Philippines, Diliman, Quezon City 1101, Philippines

Received 31 July 2007; received in revised form 16 August 2007; accepted 26 November 2007

Abstract

Temporal variation in the type and abundance of dinoflagellate cysts in Manila Bay, Philippines, is established using 210Pb-dated sediment

cores. At least 17 dinoflagellate cyst species, including those of the toxic species, Pyrodinium bahamense var. compressum, were identified. P.

bahamense may have been present in the area since at least the 1920s. Total cyst density has increased beginning about 1988 to 1998 coinciding

with records of P. bahamense blooms in the area. Heterotrophs have always dominated the cysts assemblage. These changes in the dinoflagellate

record and the P. bahamense blooms in recent years may have been induced by the interplay of warmer temperatures, high rainfall leading to higher

river discharge and less turbulent waters due to passage of few tropical cyclones.

# 2008 Elsevier B.V. All rights reserved.

Keywords: Climate; Dinoflagellate cyst; Harmful algal blooms; Manila Bay; Pyrodinium bahamense var. compressum; Toxic dinoflagellate

1. Introduction

Manila Bay is one of the areas heavily affected by harmful

algal blooms in the Philippines. Recurring annual blooms of the

toxic dinoflagellate Pyrodinium bahamense var. compressum

blooms were observed in Manila Bay from 1988 to about 2000.

Blooms typically start during the onset of the rainy season at the

end of May and terminate from July to August (Bajarias and

Relox, 1996; Azanza et al., 1998). More recently, P. bahamense

blooms have not been reported in the area, instead blooms of

Noctiluca scintillans have taken place (Jacinto et al., 2006;

Azanza et al., 2007 unpublished).

P. bahamense forms non-motile resting forms, cysts, or

hypnozygotes (Azanza, 1997; Usup and Azanza, 1998), which

are deposited onto the sediments and serve as inoculum for later

blooms (Dale, 1983; Anderson, 1984; Corrales and Crisostomo,

1996). Previous studies have shown that high concentrations of

cysts in the sediments may act as ‘‘seed beds’’ for future blooms

* Corresponding author at: Marine Science Institute, University of the

Philippines, Diliman, Quezon City 1101, Philippines. Tel.: +63 433 6063;

fax: +63 433 6063.

E-mail address: fpsiringan@upmsi.ph (F.P. Siringan).

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

doi:10.1016/j.hal.2007.11.003

(Anderson, 1984; Azanza et al., 2004) or become preserved in the

sediments for long periods (Dale, 1983). Villanoy et al. (2006)

postulated that if cysts from sediments initiate P. bahamense

blooms in Manila Bay, it would require wind-induced vertical

mixing of the water column, as well as tidal currents to produce

the needed bottom velocities to resuspend cysts. The wave field

during the southwest monsoon significantly contributes to

bottom current velocities in the southeastern coast of Manila Bay

(Cavite). Analyzing the vertical distribution of cyst assemblage

in sediment cores may provide long-term records of dino-

flagellate blooms. Moreover, some water properties and geologic

events may also be reflected in the sediments that could allow

correlations with P. bahamense bloom events.

Furio et al. (1996) showed that the sediment surface of the

western part of Manila Bay (Bataan) contained high

concentrations of P. bahamense cysts. A recent study of

Azanza et al. (2004) correlated horizontal dinoflagellate cyst

distribution with sediment properties, and indicated that

sediments characterized by high clay content, high wet bulk

density, but moderate water content, low total organic matter,

low N and P flux and low total organic carbon contain the

highest concentrations of P. bahamense cysts.

This paper presents the temporal distribution of autotrophic

and heterotrophic dinoflagellate cysts, particularly the

F.P. Siringan et al. / Harmful Algae 7 (2008) 523–531524

autotrophic P. bahamense in the sediments of Manila Bay.

These distributions are compared to climate data in order to

evaluate the impacts of recent temporal trends on cyst’

abundance.

2. Materials and methods

2.1. The study site

Manila Bay is a semi-enclosed bay on the southwestern part

of Luzon Island between 148150–148500N and 1208300–1218000E (Fig. 1). It covers an area of 1800 km2 with a

coastline of approximately 190 km, and an average depth of

25 m. The width varies from 19 km at the mouth to 56 km

inside the bay. The provinces of Bataan, Pampanga, Bulacan,

and Cavite together with Metro Manila enclose the bay. The

rivers from these areas drain about 800 m3/s of fresh water into

Manila Bay with Pampanga River and Pasig River contributing

49 and 21%, respectively, to the input. Smaller rivers contribute

26%, with net precipitation supplying 4% of the total fresh

water input (EMB, 1992). The hydrodynamics of the bay is

characterized by a two-gyred circulation pattern emanating

from the western and eastern coasts of the Bay, which in turn,

feeds the two main sources of bloom formation in the Bay,

respectively, from Bataan to Bulacan (western-northwestern)

and Cavite-Paranaque (southeast-eastern) areas (Villanoy et al.,

2006).

Fig. 1. Location of core sites in Manila Bay including co

2.2. Cyst examination

Four sediment gravity cores, designated 8, 14, 16 and 23,

were acquired from Manila Bay in September to November

2000 (Fig. 1), and cut longitudinally. Sub-samples were taken

using a 5-ml syringe at every two cm in the upper 8 cm and

every other cm for the lower core. The samples were stored in

small containers and kept in dark plastic bags at temperatures

which prevent cyst germination. Replicates were also obtained

and archived. The sub-samples were diluted with filtered

seawater and manually disaggregated using a stirrer. Further

disaggregation was done by sonication for 2 min at 5 mA. The

samples were then sieved through 125-mm over 25-mm pans.

Sediments on the 25-mm sieve were diluted to 10 ml with

seawater. A 1-ml aliquot was placed on a Sedgwick-Rafter

chamber and viewed under a light microscope at 100�–400�magnification. Taxonomic analysis for cysts followed the

method by Matsuoka and Fukuyo (2000). Cyst density is

reported in terms of number of cysts per gram of dry sediments,

unless indicated otherwise.

For diatom counting, 5-ml sub-samples were taken every

2 cm up to 20 cm depth and every 10 cm thereafter. Sub-

samples were sieved through 500-mm mesh. Particles retained

in the sieve were collected, washed repeatedly, and diluted to

40 ml. An aliquot of 1 ml mounted on a Sedgwick-Rafter

chamber grid slide was analyzed under a light microscope at

200� magnification. Fragments that were still intact and not

res taken by Yniguez (2000) and Furio et al. (1996).

F.P. Siringan et al. / Harmful Algae 7 (2008) 523–531 525

macerated in appearance were also considered in the counting.

Sediment age was calculated from the sedimentation rates

according to Sombrito et al. (2001, 2004), from 210Pb profiles of

the same cores. Depth-to-time conversion was applied until

1850, in the absence of any other age control.

2.3. Rainfall data and proxies

Annual precipitation data were obtained from Philippine

Atmospheric, Geophysical and Astronomical Services Admin-

istration (PAGASA) stations within the watershed of Manila

Bay, including Ninoy Aquino International Airport (1956–

2000), Port Area (1949–2000) and Science Garden (1962–

2000) in Metro Manila; and Sangley Point (1976–2000) in

Cavite. Earlier precipitation records for a station in Manila,

dating back to the mid-1800s, were downloaded from the

website of the International Research Institute for Climate and

Society at the Columbia University through the IRI/LDEO

Climate Data Library. The sediment record reflects the net

effect of all interacting factors and processes that influence a

particular basin, and thus the annual precipitation levels for the

different stations were averaged. The resulting mean annual

and seasonal precipitation (October–March, and April–

September) were plotted against dinoflagellate cyst and

diatom densities.

Indices of sea surface temperature (SST) anomalies for Nino

3.4 region [5S–5N, 170W–170E] were obtained from the IRI/

LDEO Climate Data Library. The Integrated Global Ocean

Services System (IGOSS) website provided data of sea surface

temperature, centered at 14.58E and 120.58N, from 1981 to

2000. To extend the SST records, air temperatures of PAGASA

Fig. 2. Vertical distribution of dinoflagellate cyst densitie

stations (Science Garden in Quezon City and Port Area in

Manila), and from the IRI/LDEO Climate Data Library were

used as proxies for sea surface temperature. Frequency of

tropical cyclones crossing within 50-km radius of the bay was

generated from Joint Typhoon Warning Center’s web-available

tropical cyclone tracks since 1945.

3. Results

3.1. Dinoflagellate cysts and diatoms

Twenty-four dinoflagellate species were identified in the

core samples, with core 8 having the highest number of species.

Heterotrophs dominate the dinoflagellate cyst assemblage

comprising between 63% (core 14) and 92% (core 8) of the total

cyst count. Autotrophic species consisted mainly of Lingulo-

dinium polyedrum, Gonyaulax sp., Pyrophacus steinii, Proto-

ceratium reticulatum, and P. bahamense var. compressum while

heterotrophs were predominantly represented by Protoperidi-

nium spp. and Diplopsaloid spp. At least ten protoperidinoids

were recognized in the assemblage.

All cores show vertical variations in cyst density, with an

overall increase towards the top of the cores (Fig. 2). Cyst

densities in the uppermost portions of the cores ranged from 61

to 1266 cysts/g. Below 20 cm, cysts densities ranged from 2 and

600 cysts/g. The average cyst density over the length of cores

16, 14, and 23 ranged from 113 to 238 cysts/g, whereas core 8

had the highest mean cyst density of 355 cysts/g. Peak cyst

counts mostly occurred in the upper sections of the cores with

461 cysts/g in core 16, 443 cysts/g in core 23, 1266 cysts/g in

core 8, and 619 cysts/g in core 14.

s: (a) total cyst, (b) heterotrophs, and (c) autotrophs.

Fig. 3. Time-adjusted vertical distribution of dinoflagellate cyst densities: (a) total cysts, (b) heterotrophs, and (c) autotrophs. Calculated sedimentation rates were

used to estimate age until 1850, in the absence of any other age control.

Fig. 4. Time-adjusted vertical plots of diatom counts. Calculated sedimentation

rates were applied until 1850 in the absence of any other age control.

F.P. Siringan et al. / Harmful Algae 7 (2008) 523–531526

Sediment ages, from the sedimentation rates according to

Sombrito et al. (2001, 2004), indicate that the transition from

low to high cyst counts occurred around the mid to late 1980s

(Fig. 3), which coincides with the first reported toxic algal

bloom of P. bahamense in 1988. High cyst abundance was

maintained from the mid-1980s to the late 1990s, followed by

a large decrease in the uppermost portion of the core,

consistent with the disappearance of P. bahamense blooms,

and perhaps other cyst-forming dinoflagellates. Relatively

high cyst densities were also observed towards the bottom of

the cores, corresponding to the late 1800s to early 1900s.

During the latter time period, heterotrophs consisted

predominantly of Protoperidinium spp., while autotrophs

were predominantly Gonyaulax sp., L. polyedrum and

Pyrophacus. These autotrophs could have been present in

the Bay long before P. bahamense first appeared and

dominated this assemblage until the first recorded P.

bahamense bloom in the late 1980s.

Diatom densities ranged from 42 to 458 cells/g for core

16, and 9 to 101 cells/g for core 23 (Fig. 4). The highest

diatom density in core 16 (Cavite) occurred around 1995

while small peaks at Pampanga (core 23) corresponded to

1911 and 1999 (Fig. 5). Diatom densities in core 16 remained

relatively constant until 1980. After 1980, diatom densities at

core 16 showed variability and doubled around 1983, 1987

and 1995. Core 23 shows a different trend, with a peak

occurring in the lower section around 1910, then leveling out

before peaking again in the topmost section of the core

around 1999.

Fig. 5. Vertical profile of Pyrodinium bahamense var. compressum cyst density (1900–2000): (a) depth-controlled and (b) time-adjusted. The appearance of P.

bahamense in the 1920s indicates that this species had been present in Manila Bay long before the 1988 blooms.

Table 1

Calculated sedimentation rates (from Sombrito et al., 2001, 2004)

Core number Depth (cm) Sedimentation rates (cm/yr)

Core 8 Upper 20 2

20–50 0.4

Core 16 Upper 40 1

40–65 0.4

Core 14 0–36 0.98

Core 23 0–70 1

F.P. Siringan et al. / Harmful Algae 7 (2008) 523–531 527

3.2. Cysts of P. bahamense var. compressum

The vertical profile of P. bahamense cysts showed an

increasing trend towards the top in all of the cores (Fig. 5). P.

bahamense cyst counts ranged from 0 to 204 cysts/g. The

highest densities were found in the top portions of cores 8 and

23, which are located in the western side of Manila Bay. The

deepest record of P. bahamense cyst was at 58 and 44 cm

respectively in cores 16 and 23, corresponding to the 1920s and

1950s (Fig. 5).

4. Discussion

4.1. Dinoflagellate cysts and P. bahamense bloom record

Previously reported peak cyst densities in sediments vary

within Manila Bay: 420 � 73 cysts/cm3 at 14–16 cm in the

central part of the Bay (Furio et al., 1996), almost 20,000 cysts/

g at 30-cm depth in a core from Canacao Bay (Eastern side),

more than 4000 cysts/g at the top of a core near Upper Western

side (Pampanga) (Yniguez et al., 2000, unpublished), and

869 cysts/cm3 in surface sediments off Bataan (Azanza et al.,

2004). This variation can be due to differences in the local

conditions in the water column and sea floor where the cores

were taken. For example, the cores used by Yniguez et al.

(2000) were acquired in a relatively protected site and is within

the area where blooms originate and persist (Corrales and

Crisostomo, 1996; Bajarias and Relox, 1996), which explains

the relatively higher cyst density.

In the current study, core 8, off Bataan coast, yielded the

highest cyst count, and is also a region characterized by the

highest sedimentation rates, at 2 cm/yr (Sombrito et al., 2004).

Other core sites have similar sedimentation rates, at 1 cm/yr

(Table 1; Sombrito et al., 2001, 2004). The high count in core 8

is likely due to its proximity to the site where dinoflagellate

blooms frequently occur (Corrales and Crisostomo, 1996). The

high total cyst densities observed on both the western and

eastern sides of Manila Bay (Fig. 4) indicate the presence of

potential seed beds even early in the 20th century, similar to the

observations of Corrales and Crisostomo (1996) and Azanza

et al. (2004) in the surface sediments. Possible cyst and

germinated cell dispersal from these seed beds have been

modeled by Villanoy et al. (2006). Total cyst counts in the lower

segment of the cores show total dinoflagellate cyst concentra-

tions that are similar to period of bloom occurrences without a

major P. bahamense cyst presence. A bloom is traditionally

defined as a significant population increase that may lead to a

Fig. 6. Vertical profiles of P. bahamense and other autotrophic species (1900–2000). P. bahamense dominated the autotrophic assemblage during the algal bloom that

lasted from 1988 to 1998.

F.P. Siringan et al. / Harmful Algae 7 (2008) 523–531528

peak (Smayda, 1997a). Periods where these peaks in

dinoflagellate cysts were observed included 1900, 1930 and

1950 in core 8, and 1860 and 1964 in core 16. Core 14, on the

other hand, did not register values higher than 300 cysts/g in the

lower core segment, but had minor peaks occurring around

1908–1916 and the mid-1890s. Thus, periods where potential

bay-wide bloom events might have occurred appear to be

restricted to the late 1800s to early 1900s, and the late 1900s. As

early as 1908, red tide had been reported along the Bataan coast

where a fishkill event was attributed to Peridinium blooms

(Smith, 1908). Other bloom events may have gone undetected

due to their limited spatial distribution. Nevertheless, the

temporal trends of cyst concentrations for the different cores

show relative coherence. Thus, slight variations in the timing of

highs and lows can be due to local variability within the Bay.

Variations in cyst abundance of the cores are interpreted as

indicative of changes in the population densities of dino-

flagellates in the Bay through time. The finding that

heterotrophs predominate in the sediments of Manila Bay is

similar to the result of Wang et al. (2004) in Daya Bay, South

China Sea where more than half of the cyst types were

heterotrophs. Reflective of the phytoplankton communities,

cyst composition in a bay with predominating heterotrophic

dinoflagellates also indicate abundance of diatoms on which

these types of dinoflagellates could feed on (Matsuoka, 1999;

Dale, 2001; Wang et al., 2004). However, such relationship

between heterotrophs and diatoms is not resolvable due to

different sampling resolution.

The first appearance of P. bahamense cysts in the sediments

is from the 1920s at core 16 in the eastern side of the bay and

around 1956 in the Western side (Bataan, core 23). The high

concentrations of cysts, exceeding 300 cysts/g of sediment, in

the upper section of all cores starting in the mid-1980s

coincided with higher frequency of recorded blooms of P.

bahamense during this period (MacLean, 1989) (Fig. 4). The

average density of P. bahamense cysts coinciding with the

bloom periods is about 27 cysts/g. As water circulation has not

significantly changed in the last century in Manila Bay, as the

Bay’s morphology has not changed much (Siringan and Ringor,

1997), these values indicate that P. bahamense blooms occurred

only from the mid-1980s to the late-1990s, since there are no

values higher than 27 cysts/g before this period (Fig. 6).

By the mid-1980s to the late 1990s, peaks of P. bahamense

cyst coincided with peaks of heterotrophic assemblages, but dips

of other autotrophs such as Gonyaulax sp. and L. polyedrum,

showing their predominance over the autotrophs during this

period (Fig. 6). These peaks of P. bahamense cysts also coincided

with the bloom of their vegetative cells in overlying waters

(Bajarias and Relox, 1996; Azanza and Miranda, 2001). This

implies that blooms of P. bahamense can occur simultaneously

with or right before the bloom of a heterotrophic dinoflagellate

species. Thus, factors that influence heterotrophic dinoflagellate

blooms may also influence P. bahamense. Alternatively, it could

be possible that before a bloom of P. bahamense, significant

densities of heterotrophic dinoflagellates could control the

expansion of P. bahamense populations. Species interactions

within dinoflagellate groups have been studied experimentally.

Grazing experiments have shown that N. scintillans feed on P.

bahamense cells and that one N. scintillans cell can contain

several P. bahamense cells simultaneously (Hansen et al., 2004).

Moreover, the ingestion and growth rates of N. scintillans

increase with increasing P. bahamense cell concentration,

suggesting that P. bahamense make a suitable food source. This

means that multiplication of P. bahamense cells could be limited

by N. scintillan grazing, thereby controlling the potential for

blooms. Field reports have shown that N. scintillans succeeded P.

bahamense blooms in Manila Bay (Azanza and Miranda, 2001).

Recent monitoring data also show that P. bahamense blooms

have not been observed in the area since 1999 (Azanza and

Miranda, 2001; Azanza et al., 2007 unpublished). These species

F.P. Siringan et al. / Harmful Algae 7 (2008) 523–531 529

interactions within the dinoflagellate group should be further

studied to elucidate how and up to what extent they can influence

succession in the field and the occurrence of harmful algal

blooms.

4.2. Possible role of climate variables on the 1988 P.

bahamense bloom

The timing and occurrences of some common PSP-causing

dinoflagellates such as P. bahamense, Alexandrium and

Gymnodinium spp. have been attributed to both regional

weather (e.g., ENSO events, warmer SSTs) and local

environmental conditions (e.g., high runoff, eutrophication,

storm resuspension of resting cysts) that promote dinoflagellate

blooms (e.g., MacLean, 1989; Usup and Azanza, 1998; Dale,

2001; Mudie et al., 2002; Azanza et al., 2004; Phlips et al.,

2006). MacLean (1989), for instance, suggested that the timing

of P. bahamense blooms between 1972 and 1988 in Southeast

Asia coincided with El Nino events, although the mechanism

by which El Nino influences bloom dynamics was not clear. In

Manila Bay, the first recorded bloom of P. bahamense in 1988

also coincided with an El Nino event. In fact, the period during

which the blooms persisted was characterized by more frequent

and prolonged El Nino occurrences (Fig. 7). However, this

coincidence between dinoflagellate blooms and El Nino

occurrences is not reflected in the older sediments.

Salinity and temperature have also been found to influence the

abundance of dinoflagellate species. The growth and reproduc-

tion of different dinoflagellates species is optimal at certain

salinity and temperature ranges (Corrales et al., 1995; Reigman,

1996; Burkholder et al., 2006), therefore certain species may

dominate the assemblage at different times depending on

ambient environmental conditions. Previous blooms of P.

bahamense var. compressum in Southeast Asia, for instance,

Fig. 7. Comparison of long-term records of P. bahamense cyst density and climate

rainfall, and (d) frequency of tropical cyclone. Sources of data: (a) http://ing

iridl.ldeo.columbia.edu/SOURCES/.IGOSS/.nmc/Reyn_SmithOIv2/ while air temp

PAGASA and IRI/LDEO Climate Data Library (http://iridl.ldeo.columbia.edu/SOUR

50 km of Manila Bay from Joint Typhoon Warning Center (http://205.85.40.22/jtw

occurred in waters with salinity between 24.7 and 36.8 ppt, and

within a temperature range of 25–31 8C (e.g., MacLean, 1989;

Usup and Azanza, 1998). Since the 1980s, both sea surface and

air temperatures within the vicinity of Manila Bay have steadily

increased (Fig. 7), thus creating a suitable environment for the

motile population of autotrophs, such as P. bahamense, to

proliferate. P. bahamense cells, in laboratory culture, reached

optimum growth at 28 8C (Usup, 1995, cited in Usup and

Azanza, 1998), which is within the temperature range of sea

surface waters during blooms in Southeast Asia.

Other factors that might have contributed to the P.

bahamense bloom in the late 1980s are the infrequent passage

of typhoons near Manila Bay, and a general increase in seasonal

rainfall. Web-available tropical cyclone tracks since 1945 show

that no typhoon crossed within 50-km radius of Manila Bay

between 1984 and 1988 (Fig. 7), indicating relatively calmer

conditions within the bay. The lack of turbulence, which

adversely affects cell growth and survival of seed population of

dinoflagellates (Smayda, 1997b), probably promoted the

growth of P. bahamense cells in the water column. Despite

fewer typhoons crossing the Bay during the bloom period,

rainfall coinciding with the southwest monsoon (April to

September), and to some extent, annual rainfall appears to have

steadily increased although at levels lower than those of the

earlier decades (Fig. 7). Nevertheless, increased rainfall would

trigger higher land-based discharge, which would then lead to

an environment that is less saline and more enriched in nutrients

like P and N. Incidentally the year prior to the 1988 bloom was

marked with relatively intense rainfall that exceeded 3000 mm,

which would have resulted in elevated nutrient levels within the

bay. Blooms of P. bahamense in Malaysia seem to coincide with

periods of elevated rainfall and nutrient-rich runoff (Anton

et al., 2000, cited in Phlips et al., 2004) similar to the conditions

that triggered the Atlantic strain, P. bahamense var. bahamense

variables: (a) Nino 3.4 index, (b) sea-surface and air temperatures, (c) seasonal

rid.ldgo.columbia.edu/SOURCES/.KAPLAN/.Indices/; (b) SST from http://

erature (b) and precipitation (c) are reconstructed using historical data from

CES/.NOAA/.NCDC/.GCPS/.MONTHLY/.STATION/); (d) TCs passing within

c/best_tracks/) and number of TCs making landfall from PAGASA.

F.P. Siringan et al. / Harmful Algae 7 (2008) 523–531530

to bloom in the Indian River Lagoon in Florida, after a period of

drought (Phlips et al., 2004).

The interplay of warmer temperatures, higher rainfall and

less turbulence due to few tropical cyclones in 1988 could have

supported more stable and perhaps prolonged water column

stratification than what had been seasonally observed by

Villanoy et al. (2006). Monthly phytoplankton collection and

hydrographic surveys between 1992 and 1994 demonstrated

that P. bahamense red tides occurred at the onset of the rainy

season after a warm dry period that increased thermal

stratification and vertical stability of the water column (Bajarias

and Relox, 1996). A decrease in vertical mixing leading to

persistent stratification might increase the probability of a

bloom by giving P. bahamense more time to multiply in the

upper layer (Villanoy et al., 2006). Moreover, Smayda (1997b)

points out that stratified waters are microhabitats wherein

entrained populations of dinoflagellates can persist until the

nutrients are used up or increased turbulence is encountered.

The stability of the water column, coupled with higher nutrient

flux caused by increasing rainfall, and warmer temperatures

likely promote the growth of P. bahamense cells, resulting in

blooms. Blooms can persist for a long time owing to the

presence of motile population and seed beds which serve as

inoculum for recurring blooms until the population is controlled

by and eventually superseded by other species, such as N.

scintillans (Azanza and Miranda, 2001), which can graze on P.

bahamense.

4.3. Source of the P. bahamense cysts

Our core records show that P. bahamense cysts have been

present in Manila Bay sediments, at least by the 1950s on the

Bataan side (core 8) and by the 1920s on the Cavite side (core

16) of Manila Bay, much earlier than reported by Furio et al.

(1996) for a core from Canacao Bay (also in the Cavite side).

Furio et al. (1996) found P. bahamense cysts at 50–52 cm

depths dated back to around 1958–1959. Our results indicate

the presence of P. bahamense in Manila Bay long before the

1988 blooms. The occurrence of P. bahamense cysts around the

1920s (58 cm) weakens the hypothesis that the 1988 toxic

bloom was caused by the introduction of cysts to Manila Bay

through the release of ballast waters of huge marine vessels

from other parts of Southeast Asia (Seliger, 1989), where toxic

algal blooms were first reported. The bloom of 1988 was

probably initiated from small and disperse populations of P.

bahamense cells, which multiplied to bloom proportions when

conditions became favorable.

Acknowledgements

The authors wish to acknowledge the International Atomic

Energy Agency (IAEA) and the Philippine Council for Aquatic

and Marine Research and Development (PCAMRD) for their

research support. We appreciate the help of Iris Baula and

Edison Macusi in the preparation of the manuscript as well as

the constructive comments and suggestions of our anonymous

reviewer.[SS]

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