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Temporal and spatial distribution of harmful algal bloom (HAB) species in coastal waters of Kota Kinabalu, Sabah, Malaysia
Harmful Algae 10 (2011) 495–502
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Harmful Algae journal homepage: www.elsevier.com/locate/hal
Temporal and spatial distribution of harmful algal bloom (HAB) species in coastal waters of Kota Kinabalu, Sabah, Malaysia Aimimuliani Adam a, Normawaty Mohammad-Noor a,*, Ann Anton a,b, Ejria Saleh a, Shahbudin Saad c, Sitti Raehanah Muhd Shaleh a a b c
Borneo Marine Research Institute, Universiti Malaysia Sabah, Jalan UMS, 88400 Kota Kinabalu, Sabah, Malaysia Biotechnology Research Institute, Universiti Malaysia Sabah, Jalan UMS, 88400 Kota Kinabalu, Sabah, Malaysia Kulliyah of Science, International Islamic University Malaysia, Jalan Istana, Bandar Indera Mahkota, 25200 Kuantan, Pahang, Malaysia
A R T I C L E I N F O
A B S T R A C T
Article history: Received 23 April 2010 Received in revised form 8 December 2010 Accepted 23 March 2011 Available online 6 April 2011
Development of harmful algal blooms (HABs) in coastal waters of Kota Kinabalu, Malaysia, is a recurring problem. The blooms are caused by Pyrodinium bahamense var. compressum and Cochlodinium polykrikoides. Recently, another potential HAB species, Gymnodinium catenatum, was identified. The occurrence of these species is known to be related to a range of factors, including seasonal monsoons, nutrients, physical parameters and geomorphology. To understand the occurrence and distribution of the three species, extensive samplings were carried out over a period of one year, including the South West Monsoon (SWM), North East Monsoon (NEM) and Inter-Monsoon (IM) periods, at 5 stations located in 3 different bays off Kota Kinabalu. Cell density of the three HAB species and in situ physical parameters (salinity, pH and temperature) were recorded. Secondary data such as rain fall and wind speed were obtained from the Meteorology Department, Kota Kinabalu. C. polykrikoides and G. catenatum occurred year-round with the highest cell densities of 1.54 107 cells L 1 and 1.24 106 cells L 1 in December (NEM). P. bahamense var. compressum was found in low numbers with maximum cell density of 2 104 cells L 1 in August (SWM). The absence of P. bahamense var. compressum during the highest peak of C. polykrikoides and G. catenatum was related to nutrient concentrations and composition. The three species tended to occur at stations near the river and in a sheltered area. The results of the study indicate that the coastal area of Kota Kinabalu may continue to experience HAB problems, unless environmental conditions change significantly. ß 2011 Elsevier B.V. All rights reserved.
Keywords: Cochlodinium polykrikoides Gymnodinium catenatum Harmful algal bloom Pyrodinium bahamense var. compressum Monsoon Sabah
1. Introduction Harmful algal blooms (HABs) are causing problems in many parts of the world. In some cases, the abundance of cells is sufficiently high to discolor the sea surface. Blooms may adversely affect many marine organisms (e.g. Boesch et al., 1997). In coastal waters of Kota Kinabalu, three HAB species have been reported, viz. Pyrodinium bahamense var. compressum, Cochlodinium polykrikoides and Gymnodinium catenatum. P. bahamense var. compressum was first reported in 1976 along a 300-km long stretch south of Kota Kinabalu (Roy, 1977), while the first evidence of C. polykrikoides caused red discolorations of coastal waters in Sepanggar Bay in January 2005 (Anton et al., 2008). Since the first occurrence, P. bahamense var. compressum has been reported to cause mortalities and many types of illness (Ting and Joseph, 1989). C. polykrikoides is a fish killer and its occurrence has coincided with fish mortality in
* Corresponding author. Tel.: +60 88 320000x2591; fax: +60 88 320261. E-mail address: [email protected] (N. Mohammad-Noor). 1568-9883/$ – see front matter ß 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.hal.2011.03.006
aquaculture (Anton et al., 2008). G. catenatum, a species that causes paralytic shellfish poisoning (PSP), was first found in low numbers of Sepanggar Bay during 2003 (Mohammad-Noor et al., 2010). So far, no PSP incidence has been reported. HABs develop almost all year-round on the west coast of Sabah (Wang et al., 2008), especially in Kota Kinabalu coastal areas. Being the capital of Sabah, Kota Kinabalu is bustling with anthropogenic activities – shipping, human settlements and industries, and the impact on coastal marine environments is obvious. HABs may be linked to some of these factors. HAB occurrences have been linked to a number of factors such as nutrient concentrations, to weather conditions impacting on water parameters such as salinity, temperature and currents, to monsoonal winds causing up- and downwellings (Tan et al., 2006), to the geomorphology of the location (Tilstone et al., 1994), etc. A combination of some of these factors probably provides optimal conditions for HAB species, resulting in blooms. Asian tropical monsoons may be divided into three parts, i.e. the Northeast Monsoon (NEM) from November to March, the Southwest Monsoon (SWM) from May to September, and Inter-
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Monsoon periods (April and October). In the South China Sea, the NEM is mainly characterized by strong winds from the northeast (Azanza et al., 2008). The wind breaks the thermocline and causes mixing of the water column, thus bringing up nutrients to the surface and triggering phytoplankton growth. In the eastern Malacca Straits, the NEM has been suggested to cause upwellings resulting in high concentrations of chlorophyll a. During the SWM, the wind causes downwellings, resulting in low concentrations of chlorophyll a (Tan et al., 2006). In the present study, one year monitoring of C. polykrikoides, G. catenatum and P. bahamense var. compressum in the Kota Kinabalu coastal water was carried out to determine their occurrence and distribution. The results were used to identify the influence of seasonal monsoons and physical parameters recorded in situ. This information is expected to help locating more accurately the possible sites of HAB species and to facilitate a knowledge-based management of the recurring HAB problem in Kota Kinabalu. 2. Methodology 2.1. Study area The coastal marine area off Kota Kinabalu in eastern Malaysia was chosen for study. The area consists of 3 bays known as Sepanggar Bay, Likas Bay and Gaya Bay, and is shielded by several coastal islands (Gaya Island, Sepanggar Island, Uda Besar Island,
Uda Kecil Island and Peduk Island) (Fig. 1). Five sampling stations were selected to represent different environmental conditions: Station 1 was situated near Kota Kinabalu Shipping Port, in Likas Bay. Stations 3 and 5 were located in Gaya Bay and Sepanggar Bay, respectively. Stations 2 and 4 were located at the mouths of river Inanam and river Menggatal, respectively. 2.2. Sampling schedule Samples were collected twice monthly January–December 2007. The sampling periods covered the Northeast Monsoon (January–March and November–December), the Southwest Monsoon (May–September) and the inter-monsoon periods (April and October). 2.3. Sample collection At each station, 250-ml seawater samples were collected at 0.5 m depth using a 1-L Van Don water sampler, and immediately preserved with Lugol’s solution (Saraceni and Ruggiu, 1974) for phytoplankton quantification. Species identification was performed using a Carl Zeiss light microscope at 400 and 1000 magnification. Cells of C. polykrikoides, G. catenatum and P. bahamense var. compressum were counted using a Sedgwick Rafter chamber at 400 magnification. Physico-chemical parameters of surface seawater such as salinity, temperature and pH were
Fig. 1. Location of the five sampling stations in Kota Kinabalu coastal waters.
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recorded in situ using a multiprobe (Cyberscan PH 300 and Ecoscan Portable Meter SALT 6). 2.4. Secondary data
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annual cell abundance. The Kruskal–Wallis test was used to determine the significance of the differences of HAB cell densities between months (temporal) and between stations (spatial), using SPSS (Statistical Package for the Social Sciences) Volume 15.
Secondary data of monthly amount of rainfall and wind speed were obtained from the Meteorology Department, Kota Kinabalu. The data were used to evaluate the HAB pattern.
3. Results
2.5. Data analyses
Kota Kinabalu received heavy rain in the SWM compared to the NEM. The average monthly rainfall was 205.4 mm, with the highest in November (502.7 mm) and the lowest in February (28.2 mm) (Fig. 2). Mean wind speed recorded during the SWM was 14.7 m s 1, which is slightly higher than during NEM
Data on temporal distribution are presented as twice per month, with average cell densities at 5 sampling stations. For spatial distribution, data presented are average cell densities of
3.1. Total amount of rainfall and wind speed in Kota Kinabalu in 2007
Fig. 2. Monthly rainfall (mm) in Kota Kinabalu during 2007.
Fig. 3. Monthly mean wind speed (m/s) in Kota Kinabalu during 2007.
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(13.0 m s 1). The overall average wind speed in the study area was 15.8 m s 1 (Fig. 3). 3.2. Temporal distribution of HABs The three HAB species were found in all samples (Figs. 4–6). Two peaks of C. polykrikoides were observed in February and December with cell densities of 7.86 106 cells L 1 and 1.54 107 cells L 1, respectively. These high cell numbers were observed during the NEM (Fig. 4). Statistical analysis showed significant differences between monthly cell densities of C. polykrikoides (p < 0.05) except between February and December. Cell densities of C. polykrikoides started declining in March and continued decreasing until July in the SWM (Fig. 4). During the
Fig. 4. Cell abundance (cells L
Fig. 5. Cell abundance (cells L
highest peak of C. polykrikoides (December), salinity, temperature and pH were 26.4, 29 8C and 8.31, respectively. The concentration of G. catenatum cells fluctuated throughout the year. The highest cell density of 1.24 106 cells L 1 was observed in December (Fig. 5), which coincides with the highest peak of C. polykrikoides. There were significant differences in G. catenatum cell densities between December and other months (p < 0.05). The cell numbers of P. bahamense var. compressum were very low compared to those of C. polykrikoides and G. catenatum (Fig. 6). The highest cell density was recorded in August at 2.0 104 cells L 1 (Fig. 6). Sea surface salinity, temperature and pH measured during that month were 30.6, 30.9 8C and 8.4, respectively. Significant monthly differences were observed (p < 0.05) except in August and July.
1
) of C. polykrikoides January–December 2007 (log scale).
1
) of G. catenatum January–December 2007 (log scale).
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Fig. 6. Cell abundance (cells L
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1
) of P. bahamense var. compressum January–December 2007 (log scale).
Mean salinity, temperature and pH in 2007 (Fig. 7) were 29.8 (2.1), 30.2 8C (1.1) and 8.4 (0.3), respectively. There were no significant monthly differences in salinity, temperature and pH (p > 0.05). 3.3. Spatial distribution of HABs The cell densities of C. polykrikoides and G. catenatum were high at station 2 (located in front of Inanam River, Fig. 8). Cell numbers for C. polykrikoides and reached 9.4 105 cells L 1 4 7.0 10 cells L 1 for G. catenatum. The sea surface salinity, temperature and pH recorded at station 2 were 29.6, 30.3 8C
and 8.30, respectively. The lowest cell density of C. polykrikoides (2.6 105 cells L 1) was at station 3 (Gaya Bay, Fig. 8), and the lowest cell density of G. catenatum (2.2 103 cells L 1) was at station 1 (Sepanggar Bay, Fig. 8). Significant differences were found between cell densities of C. polykrikoides at each station (p < 0.05), and significant differences also recorded for G. catenatum (p < 0.05). The highest cell density of P. bahamense var. compressum (1.2 103 cells L 1) was at station 5 (Sepanggar Bay, Fig. 8), and the lowest (208 cells L 1) at station 4 (Fig. 8). Significant differences were noticed between cell densities at each station (p < 0.05). The sea surface salinity, temperature and pH recorded at station 5 were 30, 30.1 8C and 8.40, respectively.
Fig. 7. Mean salinity, temperature (8C) and pH January–December 2007.
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Fig. 8. Spatial distribution of C. polykrikoides, G. catenatum and P. bahamense var. compressum in Kota Kinabalu coastal areas (log scale).
4. Discussion 4.1. Total amount of rainfall and wind speed in Kota Kinabalu in 2007 The seasonal variation in rainfall in Malaysia is determined by the seasonal wind regime and by local topography. During the NEM, the northern coast of Sabah experiences heavy rain (Malaysian Meteorology Department, 2010). However, Kota Kinabalu, which is located on the west coast of Sabah, receives less rain. This situation, which has been reported since 1975 (Usup and Yu, 1991), is caused by the Crocker Range mountains blocking humid wind from reaching Kota Kinabalu. During the SWM, the heavy rain is due to a tail effect of the typhoons during the typhoon season (June–November) in neighbouring countries such as the Philippines. In 2007, the monthly rainfall in Kota Kinabalu ranged by a factor of nearly 18, from 28.2 to 502.7 mm, and similar differences have been reported elsewhere (Usup and Yu, 1991; Malaysian Meteorology Department, 2010). During the SWM, the heavy rainfall brings nutrients to the study area by river run-off. The three bays of the study area are shallow with a maximum depth of 22 m, and at the mean wind speed of 15.8 m s 1, the Ekman layer (the wind-affected depth) extends to the bottom. This creates a well-mixed homogeneous water column which brings up nutrients from the sediments and results in minor differences in salinity, temperature and pH during the year. 4.2. Temporal distribution of HAB species in Kota Kinabalu The blooms of C. polykrikoides persisted almost throughout the year, with high peaks during the NEM (February and December). A previous study has reported the occurrence of this species in the bay during the SWM (March and May 2005) and in June 2006, but not during the NEM (September 2005–April 2006) (Anton et al., 2008). Obviously, this species may occur anytime regardless of the monsoon seasons, but with different cell densities. However, the heavy rainfall during the SWM contributes high amounts of nutrients, which support the growth of C. polykrikoides. The importances of nutrients have been identified by several studies (Lee and Lee, 2006; Tomas and Smayda, 2008). The capability of C. polykrikoides to utilize multiple nitrogen sources (Kudela et al., 2008) allows populations to establish very quickly. Other
contributing factors are mixotrophy (Jeong et al., 2004), the capability of high-speed swimming, and the ability to withstand sinking due to chain-formation (Fraga et al., 1988). These attributes provide competitive strategy to other phytoplankton as well and are keys to successful competition at different habitats (Kudela et al., 2008), including Sabah. When compared to previous studies, the present investigation is more comprehensive and covered more sampling stations at a wider geographical area, and we conclude that there has been an increase in the number of C. polykrikoides blooms in the area. The almost monthly occurrence in 2007 suggests that the species is well established in coastal waters of Kota Kinabalu, and that the conditions of the area favour proliferation. Cell numbers of G. catenatum fluctuated during both the NEM and the SWM, but the highest peak occurred in December, concomitant with C. polykrikoides. G. catenatum has been found in temperate (Mee et al., 1986; Carrada et al., 1991) as well as tropical regions (Holmes et al., 2002), indicating a wide range of temperature and salinity tolerance. The highest density in December occurred at a temperature and salinity of 29.1 8C and 26.4, respectively. G. catenatum in Singapore waters has been reported to grow at temperatures ranging from 15 8C to 25 8C (Holmes et al., 2002). In temperate G. catenatum, the optimal growth temperature has been recorded as ranging between 12 and 28 8C (Blackburn et al., 1989). Numerous annual blooms of P. bahamense var. compressum have been reported in the area since 1980. They mostly occur in June– July (SWM) and December–January (NEM) except in 1988 and 1989 (Usup et al., 1989). Eight years of data from Kimanis and Kota Kinabalu show P. bahamense var. compressum occurring both during the NEM and the SWM (Usup and Yu, 1991). In the present study P. bahamense var. compressum was found in low numbers only, and mostly during the SWM. Wang et al. (2008) reported more than 200 blooms of P. bahamense var. compressum on the western coast of Sabah during 1991–2003. However, from mid2005 to early 2006, it was absent in samples collected in the same bay (Sepanggar Bay, Jaffar-Sidik et al., 2008). P. bahamense var. compressum was absent for several months during the NEM, when C. polykrikoides and G. catenatum dominated. Its absence during C. polykrikoides blooms was also reported from the Philippines (Azanza et al., 2008). Suppression of P.
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bahamense var. compressum during the C. polykrikoides and G. catenatum blooms is believed to be due to a range of factors. Since the three species can occur together, salinity, temperature and pH may not be limiting factors, rather a combination effect of these factors. In the Philippines, the absence of P. bahamense var. compressum and its replacement by other phytoplankton species was believed to be caused by changes in nutrient availability (Villanoy et al., 2006). A point to consider in our study is the high cell concentrations observed in coastal water of Kota Kinabalu. This may be linked to effluents, mostly from domestic wastes, which changes the nutrient composition and concentration. C. polykrikoides and G. catenatum are both highly tolerant to nutrient increases, P. bahamense var. compressum much less so, leading to reduced concentrations of P. bahamense var. compressum and its eventual disappearance. The high tolerance of C. polykrikoides and G. catenatum is also indicated by the wide geographical distribution of these species in temperate and tropical region, while P. bahamense var. compressum is restricted to the Indo-Pacific countries, including Indonesia (Wiadayana et al., 1996), Papua New Guinea (MacLean, 1989) and the Philippines (Bajarias and Relox, 1996). Azanza and Taylor (2001) found P. bahamense var. compressum to be a tropical species, which requires a specific range of high temperatures to reproduce (Wang et al., 2008). The origin of the three HAB species in coastal bays of Sabah is unknown. P. bahamense var. compressum was first detected in 1976 at Putatan, which is located south of the study area (Roy, 1977), while the other two species were found more recently, G. catenatum in 2003 and C. polykrikoides in 2005, both in Sepanggar Bay. Since all three species form resting cysts, transportation of cysts in ballast water and discharges from cargo ships into the study area from other parts of Sabah or from other countries may have occurred, Kota Kinabalu is one of the main shipping ports in Sabah. The introduction of toxic dinoflagellates, including G. catenatum, by ballast water has been addressed in detail elsewhere (e.g. Hallegraeff and Bolch, 1992; Bolch and de Salas, 2007). Another possible source of introduction and spreading is ocean currents (Lee and Lee, 2006). Azanza et al. (2008) found C. polykrikoides blooms to be transported by ocean currents and wind from the western part of Sabah to Palawan, Philippines. However, in a study by Iwataki et al. (2008), based on LSU rDNA sequences, C. polykrikoides from Kota Kinabalu grouped with C. polykrikoides from the Pacific and the Atlantic coasts of North America and the Caribbean, rather than with East Asia and the Philippines. The complexity of the spreading therefore needs to be addressed further. 4.3. Spatial distribution of HABs species in Kota Kinabalu High cell densities of C. polykrikoides and G. catenatum were found at station 2, which is located near Inanam river mouth. A study by Toha (2008) at the same station in 2007 reported that the river supplied high concentrations of phosphate (1.64 mM L 1), especially in January and February 2007. As described earlier, the water column of the study area is homogenous and nutrients from the sediments and river discharge are therefore believed to trigger cells to form blooms. High cell densities of P. bahamense var. compressum, however, were recorded at station 5, which is located in a semi-enclosed and sheltered bay, and we believe that nutrients from the sediments support high cell density. Previous studies by Usup and Yu (1991) and Estim (1999) found P. bahamense var. compressum to require a stable water column to develop. 5. Conclusions C. polykrikoides and G. catenatum were found during both the NEM and the SWM. High cell density of P. bahamense var.
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compressum was observed during the SWM rather than during the NEM. The suppression of P. bahamense var. compressum during C. polykrikoides and G. catenatum blooms is believed to be due to a change in nutrient concentrations and composition, rather than to pH, temperature and salinity. The spatial distribution of C. polykrikoides and G. catenatum was high at station 2, which may have received nutrients from the Inanam river. Concentrations of P. bahamense var. compressum were high at station 5, located in a semi-enclosed area. The observations reported during the present study indicate the importance of nutrients in the triggering blooms. We conclude that Kota Kinabalu coastal area will continue to experience HAB problems as long as nutrient concentrations remain high in the area. Acknowledgements We thank the staff of Borneo Marine Research Institute, Universiti Malaysia Sabah, for providing field assistance and to Prof. Øjvind Moestrup, Prof. Saleem Mustafa and Assoc. Prof. Than Aung for critically revising the manuscript. The efforts of the anonymous reviewers to improve the quality of the manuscript are highly appreciated. This study was supported by a MOSTI Sciencefund (Grant code: SF0014 and SF0019).[SS] References Anton, A., Teoh, P.L., Mohd-Shaleh, S.R., Mohammad-Noor, N., 2008. First occurrence of Cochlodinium blooms in Sabah, Malaysia. Harmful Algae 7, 331–336. Azanza, R.V., Taylor, F.J.R.M., 2001. Are Pyrodinium blooms in the Southeast Asian region recurring and spreading? A view at the end of the Millennium. Ambio 30, 356–364. Azanza, R.V., David, L.T., Borja, R.T., Baula, I.U., Fukuyo, Y., 2008. An extensive Cochlodinium bloom along the western coast of the Palawan, Philippines. Harmful Algae 7, 324–330. Bajarias, F.F.A., Relox, J.R., 1996. Hydrological and climatological parameters associated with the P. bahamense blooms in Manila Bay, Philippines. In: Yasumoto, T., Oshima, Y., Fukuyo, Y. (Eds.), Harmful and Toxic Algal Blooms. IOC of UNESCO, Paris, pp. 49–52. Blackburn, S.I., Hallegraeff, G.M., Bolch, C.J., 1989. Vegetative reproduction and sexual life cycle of the toxic dinoflagellate Gymnodinium catenatum from Tasmania, Australia. J. Phycol. 25, 577–590. Boesch, D.F., Anderson, D.M., Horner, R.A., Shumway, S.E., Tester, P.A., Whitledge, T.E., 1997. Harmful Algal Blooms in Coastal Waters; Options for Prevention, Control and Mitigation. NOAA Coastal Ocean Program. Decision Analysis Series No. 10. Bolch, C.J.S., de Salas, M.F., 2007. A review of the molecular evidence for ballast water introduction of the toxic dinoflagellates Gymnodinium catenatum and the Alexandrium ‘tamarensis complex’ to Australasia. Harmful Algae 6, 465–485. Carrada, G.C., Casotti, R., Modigh, M., Saggiomo, V., 1991. Presence of Gymnodinium catenatum (Dinophyceae) in a coastal Mediterranean Lagoon. J. Plankton Res. 13, 229–238. Estim, A., 1999. Study of nutrients and its effects on the occurrences of red tide in Sabah coastal waters (in Malay). Unpublished Master of Science Thesis. Fraga, S., Anderson, D.M., Bravo, I., Reguera, B., Steidinger, K.A., Yentsch, C.M., 1988. Influence of upwelling relaxation on dinoflagellates and shellfish toxicity in Ria de Vigo, Spain. Estuar. Coast. Shelf Sci. 27, 349–361. Hallegraeff, G.M., Bolch, C.J., 1992. Transport of diatom and dinoflagellate resting spores in ships’ ballast water: implications for plankton biogeography and aquaculture. J. Plankton Res. 14, 1067–1084. Holmes, M.J., Bolch, C.J.S., Green, D.H., Cembella, A.D., Teo, S.L.M., 2002. Singapore isolates of the dinoflagellate Gymnodinium catenatum (Dinophyceae) produce a unique profile of paralytic shellfish poisoning toxins. J. Phycol. 38, 96–106. Iwataki, M., Kawami, H., Mizushima, K., Mikulski, C.M., Doucette, G.J., Relox Jr., J.R., Anton, A., Fukuyo, Y., Matsuoka, K., 2008. Phylogenetic relationships in the harmful dinoflagellate Cochlodinium polykrikoides (Gymnodiniales, Dinophyceae) inferred from LSU rDNA sequences. Harmful Algae 7, 271–277. Jaffar-Sidik, M., Rashed-Un-Nabi, M., Hoque, M.A., 2008. Distribution of phytoplankton community in relation to environmental parameters in cage culture area of Sepanggar Bay, Sabah, Malaysia. Estuar. Coast. Shelf Sci. 80, 251–260. Jeong, H., Yoo, Y., Kim, J., Kim, T., Kim, J., Kang, N., Yih, W., 2004. Mixotrophy in the phototropic harmful alga Cochlodinium polykrikoides (Dinophyceae): prey species, the effects of prey concentration, and grazing impact. J. Eukaryot. Microbiol. 51, 563–569. Kudela, R.M., Ryan, J.P., Blakely, M.D., Lane, J.Q., Peterson, T.D., 2008. Linking the physiology and ecology of Cochlodinium to better understand harmful algal bloom events: a comparative approach. Harmful Algae 7, 278–292. Lee, Y.S., Lee, S.Y., 2006. Factors affecting outbreaks of Cochlodinium polykrikoides blooms in coastal areas of Korea. Mar. Pollut. Bull. 52, 626–634.
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Harmful Algae journal homepage: www.elsevier.com/locate/hal
Temporal and spatial distribution of harmful algal bloom (HAB) species in coastal waters of Kota Kinabalu, Sabah, Malaysia Aimimuliani Adam a, Normawaty Mohammad-Noor a,*, Ann Anton a,b, Ejria Saleh a, Shahbudin Saad c, Sitti Raehanah Muhd Shaleh a a b c
Borneo Marine Research Institute, Universiti Malaysia Sabah, Jalan UMS, 88400 Kota Kinabalu, Sabah, Malaysia Biotechnology Research Institute, Universiti Malaysia Sabah, Jalan UMS, 88400 Kota Kinabalu, Sabah, Malaysia Kulliyah of Science, International Islamic University Malaysia, Jalan Istana, Bandar Indera Mahkota, 25200 Kuantan, Pahang, Malaysia
A R T I C L E I N F O
A B S T R A C T
Article history: Received 23 April 2010 Received in revised form 8 December 2010 Accepted 23 March 2011 Available online 6 April 2011
Development of harmful algal blooms (HABs) in coastal waters of Kota Kinabalu, Malaysia, is a recurring problem. The blooms are caused by Pyrodinium bahamense var. compressum and Cochlodinium polykrikoides. Recently, another potential HAB species, Gymnodinium catenatum, was identified. The occurrence of these species is known to be related to a range of factors, including seasonal monsoons, nutrients, physical parameters and geomorphology. To understand the occurrence and distribution of the three species, extensive samplings were carried out over a period of one year, including the South West Monsoon (SWM), North East Monsoon (NEM) and Inter-Monsoon (IM) periods, at 5 stations located in 3 different bays off Kota Kinabalu. Cell density of the three HAB species and in situ physical parameters (salinity, pH and temperature) were recorded. Secondary data such as rain fall and wind speed were obtained from the Meteorology Department, Kota Kinabalu. C. polykrikoides and G. catenatum occurred year-round with the highest cell densities of 1.54 107 cells L 1 and 1.24 106 cells L 1 in December (NEM). P. bahamense var. compressum was found in low numbers with maximum cell density of 2 104 cells L 1 in August (SWM). The absence of P. bahamense var. compressum during the highest peak of C. polykrikoides and G. catenatum was related to nutrient concentrations and composition. The three species tended to occur at stations near the river and in a sheltered area. The results of the study indicate that the coastal area of Kota Kinabalu may continue to experience HAB problems, unless environmental conditions change significantly. ß 2011 Elsevier B.V. All rights reserved.
Keywords: Cochlodinium polykrikoides Gymnodinium catenatum Harmful algal bloom Pyrodinium bahamense var. compressum Monsoon Sabah
1. Introduction Harmful algal blooms (HABs) are causing problems in many parts of the world. In some cases, the abundance of cells is sufficiently high to discolor the sea surface. Blooms may adversely affect many marine organisms (e.g. Boesch et al., 1997). In coastal waters of Kota Kinabalu, three HAB species have been reported, viz. Pyrodinium bahamense var. compressum, Cochlodinium polykrikoides and Gymnodinium catenatum. P. bahamense var. compressum was first reported in 1976 along a 300-km long stretch south of Kota Kinabalu (Roy, 1977), while the first evidence of C. polykrikoides caused red discolorations of coastal waters in Sepanggar Bay in January 2005 (Anton et al., 2008). Since the first occurrence, P. bahamense var. compressum has been reported to cause mortalities and many types of illness (Ting and Joseph, 1989). C. polykrikoides is a fish killer and its occurrence has coincided with fish mortality in
* Corresponding author. Tel.: +60 88 320000x2591; fax: +60 88 320261. E-mail address: [email protected] (N. Mohammad-Noor). 1568-9883/$ – see front matter ß 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.hal.2011.03.006
aquaculture (Anton et al., 2008). G. catenatum, a species that causes paralytic shellfish poisoning (PSP), was first found in low numbers of Sepanggar Bay during 2003 (Mohammad-Noor et al., 2010). So far, no PSP incidence has been reported. HABs develop almost all year-round on the west coast of Sabah (Wang et al., 2008), especially in Kota Kinabalu coastal areas. Being the capital of Sabah, Kota Kinabalu is bustling with anthropogenic activities – shipping, human settlements and industries, and the impact on coastal marine environments is obvious. HABs may be linked to some of these factors. HAB occurrences have been linked to a number of factors such as nutrient concentrations, to weather conditions impacting on water parameters such as salinity, temperature and currents, to monsoonal winds causing up- and downwellings (Tan et al., 2006), to the geomorphology of the location (Tilstone et al., 1994), etc. A combination of some of these factors probably provides optimal conditions for HAB species, resulting in blooms. Asian tropical monsoons may be divided into three parts, i.e. the Northeast Monsoon (NEM) from November to March, the Southwest Monsoon (SWM) from May to September, and Inter-
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Monsoon periods (April and October). In the South China Sea, the NEM is mainly characterized by strong winds from the northeast (Azanza et al., 2008). The wind breaks the thermocline and causes mixing of the water column, thus bringing up nutrients to the surface and triggering phytoplankton growth. In the eastern Malacca Straits, the NEM has been suggested to cause upwellings resulting in high concentrations of chlorophyll a. During the SWM, the wind causes downwellings, resulting in low concentrations of chlorophyll a (Tan et al., 2006). In the present study, one year monitoring of C. polykrikoides, G. catenatum and P. bahamense var. compressum in the Kota Kinabalu coastal water was carried out to determine their occurrence and distribution. The results were used to identify the influence of seasonal monsoons and physical parameters recorded in situ. This information is expected to help locating more accurately the possible sites of HAB species and to facilitate a knowledge-based management of the recurring HAB problem in Kota Kinabalu. 2. Methodology 2.1. Study area The coastal marine area off Kota Kinabalu in eastern Malaysia was chosen for study. The area consists of 3 bays known as Sepanggar Bay, Likas Bay and Gaya Bay, and is shielded by several coastal islands (Gaya Island, Sepanggar Island, Uda Besar Island,
Uda Kecil Island and Peduk Island) (Fig. 1). Five sampling stations were selected to represent different environmental conditions: Station 1 was situated near Kota Kinabalu Shipping Port, in Likas Bay. Stations 3 and 5 were located in Gaya Bay and Sepanggar Bay, respectively. Stations 2 and 4 were located at the mouths of river Inanam and river Menggatal, respectively. 2.2. Sampling schedule Samples were collected twice monthly January–December 2007. The sampling periods covered the Northeast Monsoon (January–March and November–December), the Southwest Monsoon (May–September) and the inter-monsoon periods (April and October). 2.3. Sample collection At each station, 250-ml seawater samples were collected at 0.5 m depth using a 1-L Van Don water sampler, and immediately preserved with Lugol’s solution (Saraceni and Ruggiu, 1974) for phytoplankton quantification. Species identification was performed using a Carl Zeiss light microscope at 400 and 1000 magnification. Cells of C. polykrikoides, G. catenatum and P. bahamense var. compressum were counted using a Sedgwick Rafter chamber at 400 magnification. Physico-chemical parameters of surface seawater such as salinity, temperature and pH were
Fig. 1. Location of the five sampling stations in Kota Kinabalu coastal waters.
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recorded in situ using a multiprobe (Cyberscan PH 300 and Ecoscan Portable Meter SALT 6). 2.4. Secondary data
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annual cell abundance. The Kruskal–Wallis test was used to determine the significance of the differences of HAB cell densities between months (temporal) and between stations (spatial), using SPSS (Statistical Package for the Social Sciences) Volume 15.
Secondary data of monthly amount of rainfall and wind speed were obtained from the Meteorology Department, Kota Kinabalu. The data were used to evaluate the HAB pattern.
3. Results
2.5. Data analyses
Kota Kinabalu received heavy rain in the SWM compared to the NEM. The average monthly rainfall was 205.4 mm, with the highest in November (502.7 mm) and the lowest in February (28.2 mm) (Fig. 2). Mean wind speed recorded during the SWM was 14.7 m s 1, which is slightly higher than during NEM
Data on temporal distribution are presented as twice per month, with average cell densities at 5 sampling stations. For spatial distribution, data presented are average cell densities of
3.1. Total amount of rainfall and wind speed in Kota Kinabalu in 2007
Fig. 2. Monthly rainfall (mm) in Kota Kinabalu during 2007.
Fig. 3. Monthly mean wind speed (m/s) in Kota Kinabalu during 2007.
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(13.0 m s 1). The overall average wind speed in the study area was 15.8 m s 1 (Fig. 3). 3.2. Temporal distribution of HABs The three HAB species were found in all samples (Figs. 4–6). Two peaks of C. polykrikoides were observed in February and December with cell densities of 7.86 106 cells L 1 and 1.54 107 cells L 1, respectively. These high cell numbers were observed during the NEM (Fig. 4). Statistical analysis showed significant differences between monthly cell densities of C. polykrikoides (p < 0.05) except between February and December. Cell densities of C. polykrikoides started declining in March and continued decreasing until July in the SWM (Fig. 4). During the
Fig. 4. Cell abundance (cells L
Fig. 5. Cell abundance (cells L
highest peak of C. polykrikoides (December), salinity, temperature and pH were 26.4, 29 8C and 8.31, respectively. The concentration of G. catenatum cells fluctuated throughout the year. The highest cell density of 1.24 106 cells L 1 was observed in December (Fig. 5), which coincides with the highest peak of C. polykrikoides. There were significant differences in G. catenatum cell densities between December and other months (p < 0.05). The cell numbers of P. bahamense var. compressum were very low compared to those of C. polykrikoides and G. catenatum (Fig. 6). The highest cell density was recorded in August at 2.0 104 cells L 1 (Fig. 6). Sea surface salinity, temperature and pH measured during that month were 30.6, 30.9 8C and 8.4, respectively. Significant monthly differences were observed (p < 0.05) except in August and July.
1
) of C. polykrikoides January–December 2007 (log scale).
1
) of G. catenatum January–December 2007 (log scale).
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Fig. 6. Cell abundance (cells L
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1
) of P. bahamense var. compressum January–December 2007 (log scale).
Mean salinity, temperature and pH in 2007 (Fig. 7) were 29.8 (2.1), 30.2 8C (1.1) and 8.4 (0.3), respectively. There were no significant monthly differences in salinity, temperature and pH (p > 0.05). 3.3. Spatial distribution of HABs The cell densities of C. polykrikoides and G. catenatum were high at station 2 (located in front of Inanam River, Fig. 8). Cell numbers for C. polykrikoides and reached 9.4 105 cells L 1 4 7.0 10 cells L 1 for G. catenatum. The sea surface salinity, temperature and pH recorded at station 2 were 29.6, 30.3 8C
and 8.30, respectively. The lowest cell density of C. polykrikoides (2.6 105 cells L 1) was at station 3 (Gaya Bay, Fig. 8), and the lowest cell density of G. catenatum (2.2 103 cells L 1) was at station 1 (Sepanggar Bay, Fig. 8). Significant differences were found between cell densities of C. polykrikoides at each station (p < 0.05), and significant differences also recorded for G. catenatum (p < 0.05). The highest cell density of P. bahamense var. compressum (1.2 103 cells L 1) was at station 5 (Sepanggar Bay, Fig. 8), and the lowest (208 cells L 1) at station 4 (Fig. 8). Significant differences were noticed between cell densities at each station (p < 0.05). The sea surface salinity, temperature and pH recorded at station 5 were 30, 30.1 8C and 8.40, respectively.
Fig. 7. Mean salinity, temperature (8C) and pH January–December 2007.
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Fig. 8. Spatial distribution of C. polykrikoides, G. catenatum and P. bahamense var. compressum in Kota Kinabalu coastal areas (log scale).
4. Discussion 4.1. Total amount of rainfall and wind speed in Kota Kinabalu in 2007 The seasonal variation in rainfall in Malaysia is determined by the seasonal wind regime and by local topography. During the NEM, the northern coast of Sabah experiences heavy rain (Malaysian Meteorology Department, 2010). However, Kota Kinabalu, which is located on the west coast of Sabah, receives less rain. This situation, which has been reported since 1975 (Usup and Yu, 1991), is caused by the Crocker Range mountains blocking humid wind from reaching Kota Kinabalu. During the SWM, the heavy rain is due to a tail effect of the typhoons during the typhoon season (June–November) in neighbouring countries such as the Philippines. In 2007, the monthly rainfall in Kota Kinabalu ranged by a factor of nearly 18, from 28.2 to 502.7 mm, and similar differences have been reported elsewhere (Usup and Yu, 1991; Malaysian Meteorology Department, 2010). During the SWM, the heavy rainfall brings nutrients to the study area by river run-off. The three bays of the study area are shallow with a maximum depth of 22 m, and at the mean wind speed of 15.8 m s 1, the Ekman layer (the wind-affected depth) extends to the bottom. This creates a well-mixed homogeneous water column which brings up nutrients from the sediments and results in minor differences in salinity, temperature and pH during the year. 4.2. Temporal distribution of HAB species in Kota Kinabalu The blooms of C. polykrikoides persisted almost throughout the year, with high peaks during the NEM (February and December). A previous study has reported the occurrence of this species in the bay during the SWM (March and May 2005) and in June 2006, but not during the NEM (September 2005–April 2006) (Anton et al., 2008). Obviously, this species may occur anytime regardless of the monsoon seasons, but with different cell densities. However, the heavy rainfall during the SWM contributes high amounts of nutrients, which support the growth of C. polykrikoides. The importances of nutrients have been identified by several studies (Lee and Lee, 2006; Tomas and Smayda, 2008). The capability of C. polykrikoides to utilize multiple nitrogen sources (Kudela et al., 2008) allows populations to establish very quickly. Other
contributing factors are mixotrophy (Jeong et al., 2004), the capability of high-speed swimming, and the ability to withstand sinking due to chain-formation (Fraga et al., 1988). These attributes provide competitive strategy to other phytoplankton as well and are keys to successful competition at different habitats (Kudela et al., 2008), including Sabah. When compared to previous studies, the present investigation is more comprehensive and covered more sampling stations at a wider geographical area, and we conclude that there has been an increase in the number of C. polykrikoides blooms in the area. The almost monthly occurrence in 2007 suggests that the species is well established in coastal waters of Kota Kinabalu, and that the conditions of the area favour proliferation. Cell numbers of G. catenatum fluctuated during both the NEM and the SWM, but the highest peak occurred in December, concomitant with C. polykrikoides. G. catenatum has been found in temperate (Mee et al., 1986; Carrada et al., 1991) as well as tropical regions (Holmes et al., 2002), indicating a wide range of temperature and salinity tolerance. The highest density in December occurred at a temperature and salinity of 29.1 8C and 26.4, respectively. G. catenatum in Singapore waters has been reported to grow at temperatures ranging from 15 8C to 25 8C (Holmes et al., 2002). In temperate G. catenatum, the optimal growth temperature has been recorded as ranging between 12 and 28 8C (Blackburn et al., 1989). Numerous annual blooms of P. bahamense var. compressum have been reported in the area since 1980. They mostly occur in June– July (SWM) and December–January (NEM) except in 1988 and 1989 (Usup et al., 1989). Eight years of data from Kimanis and Kota Kinabalu show P. bahamense var. compressum occurring both during the NEM and the SWM (Usup and Yu, 1991). In the present study P. bahamense var. compressum was found in low numbers only, and mostly during the SWM. Wang et al. (2008) reported more than 200 blooms of P. bahamense var. compressum on the western coast of Sabah during 1991–2003. However, from mid2005 to early 2006, it was absent in samples collected in the same bay (Sepanggar Bay, Jaffar-Sidik et al., 2008). P. bahamense var. compressum was absent for several months during the NEM, when C. polykrikoides and G. catenatum dominated. Its absence during C. polykrikoides blooms was also reported from the Philippines (Azanza et al., 2008). Suppression of P.
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bahamense var. compressum during the C. polykrikoides and G. catenatum blooms is believed to be due to a range of factors. Since the three species can occur together, salinity, temperature and pH may not be limiting factors, rather a combination effect of these factors. In the Philippines, the absence of P. bahamense var. compressum and its replacement by other phytoplankton species was believed to be caused by changes in nutrient availability (Villanoy et al., 2006). A point to consider in our study is the high cell concentrations observed in coastal water of Kota Kinabalu. This may be linked to effluents, mostly from domestic wastes, which changes the nutrient composition and concentration. C. polykrikoides and G. catenatum are both highly tolerant to nutrient increases, P. bahamense var. compressum much less so, leading to reduced concentrations of P. bahamense var. compressum and its eventual disappearance. The high tolerance of C. polykrikoides and G. catenatum is also indicated by the wide geographical distribution of these species in temperate and tropical region, while P. bahamense var. compressum is restricted to the Indo-Pacific countries, including Indonesia (Wiadayana et al., 1996), Papua New Guinea (MacLean, 1989) and the Philippines (Bajarias and Relox, 1996). Azanza and Taylor (2001) found P. bahamense var. compressum to be a tropical species, which requires a specific range of high temperatures to reproduce (Wang et al., 2008). The origin of the three HAB species in coastal bays of Sabah is unknown. P. bahamense var. compressum was first detected in 1976 at Putatan, which is located south of the study area (Roy, 1977), while the other two species were found more recently, G. catenatum in 2003 and C. polykrikoides in 2005, both in Sepanggar Bay. Since all three species form resting cysts, transportation of cysts in ballast water and discharges from cargo ships into the study area from other parts of Sabah or from other countries may have occurred, Kota Kinabalu is one of the main shipping ports in Sabah. The introduction of toxic dinoflagellates, including G. catenatum, by ballast water has been addressed in detail elsewhere (e.g. Hallegraeff and Bolch, 1992; Bolch and de Salas, 2007). Another possible source of introduction and spreading is ocean currents (Lee and Lee, 2006). Azanza et al. (2008) found C. polykrikoides blooms to be transported by ocean currents and wind from the western part of Sabah to Palawan, Philippines. However, in a study by Iwataki et al. (2008), based on LSU rDNA sequences, C. polykrikoides from Kota Kinabalu grouped with C. polykrikoides from the Pacific and the Atlantic coasts of North America and the Caribbean, rather than with East Asia and the Philippines. The complexity of the spreading therefore needs to be addressed further. 4.3. Spatial distribution of HABs species in Kota Kinabalu High cell densities of C. polykrikoides and G. catenatum were found at station 2, which is located near Inanam river mouth. A study by Toha (2008) at the same station in 2007 reported that the river supplied high concentrations of phosphate (1.64 mM L 1), especially in January and February 2007. As described earlier, the water column of the study area is homogenous and nutrients from the sediments and river discharge are therefore believed to trigger cells to form blooms. High cell densities of P. bahamense var. compressum, however, were recorded at station 5, which is located in a semi-enclosed and sheltered bay, and we believe that nutrients from the sediments support high cell density. Previous studies by Usup and Yu (1991) and Estim (1999) found P. bahamense var. compressum to require a stable water column to develop. 5. Conclusions C. polykrikoides and G. catenatum were found during both the NEM and the SWM. High cell density of P. bahamense var.
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compressum was observed during the SWM rather than during the NEM. The suppression of P. bahamense var. compressum during C. polykrikoides and G. catenatum blooms is believed to be due to a change in nutrient concentrations and composition, rather than to pH, temperature and salinity. The spatial distribution of C. polykrikoides and G. catenatum was high at station 2, which may have received nutrients from the Inanam river. Concentrations of P. bahamense var. compressum were high at station 5, located in a semi-enclosed area. The observations reported during the present study indicate the importance of nutrients in the triggering blooms. We conclude that Kota Kinabalu coastal area will continue to experience HAB problems as long as nutrient concentrations remain high in the area. Acknowledgements We thank the staff of Borneo Marine Research Institute, Universiti Malaysia Sabah, for providing field assistance and to Prof. Øjvind Moestrup, Prof. Saleem Mustafa and Assoc. Prof. Than Aung for critically revising the manuscript. The efforts of the anonymous reviewers to improve the quality of the manuscript are highly appreciated. This study was supported by a MOSTI Sciencefund (Grant code: SF0014 and SF0019).[SS] References Anton, A., Teoh, P.L., Mohd-Shaleh, S.R., Mohammad-Noor, N., 2008. First occurrence of Cochlodinium blooms in Sabah, Malaysia. Harmful Algae 7, 331–336. Azanza, R.V., Taylor, F.J.R.M., 2001. Are Pyrodinium blooms in the Southeast Asian region recurring and spreading? A view at the end of the Millennium. Ambio 30, 356–364. Azanza, R.V., David, L.T., Borja, R.T., Baula, I.U., Fukuyo, Y., 2008. An extensive Cochlodinium bloom along the western coast of the Palawan, Philippines. Harmful Algae 7, 324–330. Bajarias, F.F.A., Relox, J.R., 1996. Hydrological and climatological parameters associated with the P. bahamense blooms in Manila Bay, Philippines. In: Yasumoto, T., Oshima, Y., Fukuyo, Y. (Eds.), Harmful and Toxic Algal Blooms. IOC of UNESCO, Paris, pp. 49–52. Blackburn, S.I., Hallegraeff, G.M., Bolch, C.J., 1989. Vegetative reproduction and sexual life cycle of the toxic dinoflagellate Gymnodinium catenatum from Tasmania, Australia. J. Phycol. 25, 577–590. Boesch, D.F., Anderson, D.M., Horner, R.A., Shumway, S.E., Tester, P.A., Whitledge, T.E., 1997. Harmful Algal Blooms in Coastal Waters; Options for Prevention, Control and Mitigation. NOAA Coastal Ocean Program. Decision Analysis Series No. 10. Bolch, C.J.S., de Salas, M.F., 2007. A review of the molecular evidence for ballast water introduction of the toxic dinoflagellates Gymnodinium catenatum and the Alexandrium ‘tamarensis complex’ to Australasia. Harmful Algae 6, 465–485. Carrada, G.C., Casotti, R., Modigh, M., Saggiomo, V., 1991. Presence of Gymnodinium catenatum (Dinophyceae) in a coastal Mediterranean Lagoon. J. Plankton Res. 13, 229–238. Estim, A., 1999. Study of nutrients and its effects on the occurrences of red tide in Sabah coastal waters (in Malay). Unpublished Master of Science Thesis. Fraga, S., Anderson, D.M., Bravo, I., Reguera, B., Steidinger, K.A., Yentsch, C.M., 1988. Influence of upwelling relaxation on dinoflagellates and shellfish toxicity in Ria de Vigo, Spain. Estuar. Coast. Shelf Sci. 27, 349–361. Hallegraeff, G.M., Bolch, C.J., 1992. Transport of diatom and dinoflagellate resting spores in ships’ ballast water: implications for plankton biogeography and aquaculture. J. Plankton Res. 14, 1067–1084. Holmes, M.J., Bolch, C.J.S., Green, D.H., Cembella, A.D., Teo, S.L.M., 2002. Singapore isolates of the dinoflagellate Gymnodinium catenatum (Dinophyceae) produce a unique profile of paralytic shellfish poisoning toxins. J. Phycol. 38, 96–106. Iwataki, M., Kawami, H., Mizushima, K., Mikulski, C.M., Doucette, G.J., Relox Jr., J.R., Anton, A., Fukuyo, Y., Matsuoka, K., 2008. Phylogenetic relationships in the harmful dinoflagellate Cochlodinium polykrikoides (Gymnodiniales, Dinophyceae) inferred from LSU rDNA sequences. Harmful Algae 7, 271–277. Jaffar-Sidik, M., Rashed-Un-Nabi, M., Hoque, M.A., 2008. Distribution of phytoplankton community in relation to environmental parameters in cage culture area of Sepanggar Bay, Sabah, Malaysia. Estuar. Coast. Shelf Sci. 80, 251–260. Jeong, H., Yoo, Y., Kim, J., Kim, T., Kim, J., Kang, N., Yih, W., 2004. Mixotrophy in the phototropic harmful alga Cochlodinium polykrikoides (Dinophyceae): prey species, the effects of prey concentration, and grazing impact. J. Eukaryot. Microbiol. 51, 563–569. Kudela, R.M., Ryan, J.P., Blakely, M.D., Lane, J.Q., Peterson, T.D., 2008. Linking the physiology and ecology of Cochlodinium to better understand harmful algal bloom events: a comparative approach. Harmful Algae 7, 278–292. Lee, Y.S., Lee, S.Y., 2006. Factors affecting outbreaks of Cochlodinium polykrikoides blooms in coastal areas of Korea. Mar. Pollut. Bull. 52, 626–634.
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