International Journal on Algae, 2008, 10(2):141-162
141
Changes in relative abundance of phytoplankton in arsenic contaminated waters at the Ron Phibun district of Nakhon Si Thammarat province, Thailand∗ W. MEEINKUIRT1, W. SIRINAWIN2, S. ANGSUPANICH3 & P. POLPUNTHIN1 1
Department of Biology, Faculty of Science, Prince of Songkla University, Hat Yai, 90112 Songkhla, Thailand 2 Division of Environmental Science, Faculty of Science, Ramkhamhaeng University, Bangkapi, 10240 Bangkok, Thailand 3 Department of Aquatic Science, Faculty of Natural Resources, Prince of Songkla University, Hat Yai, 90112 Songkhla, Thailand e-mail:
[email protected] ABSTRACT
This research project examines the changes in relative abundance of phytoplankton in arsenic contaminated waters at the Ron Phibun district of Nakhon Si Thammarat Province during July 2004 to June 2005. The chosen locations were four dredg ponds (abandoned tin mines) at Ron Phibun and Hintok sub-districts and two in dug ponds for community use at Saothong and Khuankoey subdistricts. The dominant phytoplankton in all study locations were cyanobacteria except for one location in the Saothong sub-district. The results demonstrated that there were major seasonal variations in phytoplankton abundance and in dominant genera associated with all sampling locations, and these were particularly evident during the rainy period. In general, all sampling locations showed a decrease in total abundance during the rainy season, but changes to the dominant population at any one location were different from all the others.
KEYWORDS: phytoplankton, arsenic contaminated waters, dominant species, Thailand.
INTRODUCTION
As Thailand becomes more industrialized and increased pressure to improve productivity and yields of agricultural products occurs, the use of chemical fertilizers, pesticides, and toxic organic compounds causes adverse environmental effects. As a result, the country
∗ Originally published in Algologia, 2008, 18(2), pp. 153-175
ISSN 1521-9429 ©Begell House Inc., 2008
142
W. MEEINKUIRT et al.
faces increasing problems related to water pollution and environmental degradation (Chaibu, 2000). Surface and groundwater in the Ron Phibun district have been contaminated with arsenic and the source of the contamination is the consequence of old mining activities that continue to cause arsenic contamination of the environment. Background arsenic concentrations in these waters are usually measured at the µg/L (ppb) level with levels being generally higher in contaminated areas (Jianjun, 2000; JICA, 2000). The waters in the Ron Phibun district contaminate aquatic organisms, particularly phytoplankton, thereby allowing arsenic to enter the food chain (Suwanmanee, 1991). There have been many studies that have attempted to present a comprehensive overview of arsenic contamination of air, water, and soil and their specific sources. Arsenic contamination may be a result from either point sources from anthropogenic activities or natural processes (Duker et al., 2005). Arsenic is one of the toxic elements widely distributed in marine, freshwater, and soil environments. It is found naturally in rocks and soil, surface water, groundwater, aquatic animals, agricultural products, and especially in phytoplanktons (Boonchalermkit et al., 1996; Chaffin, 2003; Pinto et al., 2003; Thirunavukkarasu et al., 2003; Katsoyiannis & Zouboulis, 2004). Phytoplanktons absorb and accumulate arsenic in their cells resulting in bioaccumulation in the food chain (Chen et al., 2000). Additionally, there are numerous laboratory studies dealing with the effects of arsenic on phytoplankton (Sanders & Windom, 1980; Riedel, 1993; Sanders & Riedel, 1993; Howard et al., 1995; Fujiwara et al., 2000). Some species of microalgae such as Chlorella, Cryptomonas, Hymenomonas, Synechococcus, Phormidium, and Anabaena have been reported to be resistant to concentrations of arsenic that are greater than those found in natural waters (Bottino et al., 1978; Planas & Healey, 1978; Budd & Craig, 1981; Csonto et al., 2004). However, changes in phytoplankton communities resulting from arsenic contamination are not particularly understood because of the lack of prior information on the initial composition of these communities. This research project is designed to examine the changes of phytoplankton communities in arsenic contaminated waters in the Ron Phibun district of Nakhon Si Thammarat province. MATERIALS AND METHODS
Ron Phibun district is located approximately 800 km south of Bangkok adjacent to the shore of the gulf of Thailand on the east side of the Peninsula Thailand. It is one of the 23 districts in Nakhon Si Thammarat province and composed of six sub-districts, i.e., Hintok, Sao Thong, Ron Phibun, Kuan Chum, Kuan Phang, and Khuan Koey. It has an area of 504.76 km3. The Ron Phibun sub-district is situated between longitude 99° 46′-99° 54′ E and latitude 8° 04′-8° 15′ N. It consists of 16 villages, and at one time, was the center of a tin
CHANGES IN RELATIVE ABUNDANCE OF PHYTOPLANKTON
143
mining area of Primary Tin-Wolfram-Arsenic (Sn-W-As) deposits and secondary placer tin deposits that were exploited 100 years ago. The weather patterns were considered according to the seasonal periods. They can be divided into three seasonal periods depending on rain intensity. The early rainy period is considered to be May, June, July, August, and October. The rainy period is November, December, and January. Lastly, the dry period in 2005 was February, March, and April. Both surface and groundwater drainage systems are water sources in Ronphibun. Surface drainage systems flow predominantly west to east, with headwaters in the Ron NaSuang Chan Mountains. Groundwater drainage systems include two types of aquifers: a shallow aquifer with a depth of less than 10 m consists of unconsolidated alluvial gravel, sand, and clay, typically yielding 20-50 m3 ⋅ h-1 and a deeper carbonate-rich aquifer at a depth of more than 15 m. This aquifer generally yields 10-20 m3 ⋅ h-1 with an easterly or southeasterly hydraulic gradient. Hydraulic interaction between the two aquifers is strictly limited due to an intervening clay bed, which acts as an efficient aquiclude. The principal bedrock mining areas of the Ron Phibun district occupy the headwaters of the Huai Ron Na River, which flows southeastward from the granite massif through areas of alluvial mining to the north of the town of Ron Phibun. The principal alluvial mining areas of the district are drained by the Klong Sak, Klong Rak Mai, and Klong Nam Khun systems. All surface drainage from the area is slow flowing and extensively canalized to the east of the main Nakhon Si Thammarat highway (Williams et al., 1996). Phytoplankton samples were taken monthly between July 2004 and June 2005 at the Ron Phibun district of Nakhon Si Thammarat province. Investigations were carried out at four locations in dredging ponds at the Ron Phibun and Hin Tok subdistricts and two locations in dug ponds used by the local community at the Sao Thong and Khuan Koey sub-districts (Figure 1). Water samples (35 liters) were filtered with the use of a 20 µm plankton net at the water surface. The sample was fixed with 5-10% formaldehyde. For the determination of species type and abundance of phytoplankton, a micropipette was used to add the phytoplankton samples into a Sedgwick-Rafter chamber and specimens were identified and counted with an Olympus CH-2 compound microscope. The identification of algal species was carried out according to the procedures described in the literature (Whitford & Schumacher, 1973; Croasdale & Flint, 1986a-c; Komarek & Anagnostidis, 1999; Wongrat, 2001; John et al., 2002; Peerapornpisal, 2005). At each sampling location, a GPS was used to collect positioning data in order to allow accurate mapping of our sites. The map of the study is shown in Figure 1. These locations were selected based upon the following criteria: 1) the latest survey’s findings; 2) the arsenic contamination tested areas; 3) recommended areas by research papers such as Williams et al. (1996), Bunnag (2000), JICA (2000).
144
W. MEEINKUIRT et al.
Figure 1. The six sampling locations along the Ron Phibun district of Nakhon Si Thammarat Province, Thailand.
TABLE 1. Some environmental variables from six sampling locations along the arsenic
contaminated waters in the Ron Phibun district of Nakhon Si Thammarat province, Thailand, measured during the sampling period from June 2004 to July 2005 Location
Chl a, µg/L
BOD5
DO
NO3--N
NH3-N
PO43--N
mg/L
Conductivity, µS/cm
1
3.7-58.7
0.90-3.36
2.02-6.67
0.01-0.23
*ND-0.08
0.03-0.06
58.17-134.10
2
5.0-17.0
0.63-3.48
3.67-7.56
0.01-0.07
*ND-0.06
0.01-0.03
21.17-50.50
3
3.0-71.0
0.70-3.84
3.20-6.91
0.01-0.12
*ND-0.06
0.02-0.05
46.73-114.50
4
2.0-8.0
0.20-3.39
4.98-7.38
0.01-0.08
*ND-0.05
0.01
38.10-89.33
5
1.0-11.3
0.40-3.61
4.03-7.30
0.01-0.20
*ND-0.08
0.01-0.10
84.50-214.40
6
11.3-39.0
0.63-5.18
4.50-7.86
0.01-0.24
*ND-0.09
0.01-0.02
119.13-275.80
* ND – non-detection.
CHANGES IN RELATIVE ABUNDANCE OF PHYTOPLANKTON
145
Some environmental variables were measured during the sampling period (Table 1). Chlorophyll a (Chl a) was extracted by 90% acetone and then determined by spectrophotometer, biochemical oxygen demand (BOD5) and dissolved oxygen (DO) were determined by Winkler method, nitrate-nitrogen (NO3––N) was determined by colori-metric method after cadmium reduction, ammonia-nitrogen (NH3–N) was determined by phenate method and dissolved phosphorus (PO43 ––N) was determined by ascorbic acid method. These environmental variables were analyzed using the methodology in APHA, AWWA, and WEF (1998). In addition, conductivity was determined by YSI model 30/10 FT during sampling. RESULTS AND DISCUSSION
This study found that the phytoplankton communities consist of highly diversified flora as compared to another study on heavy metal contaminated wetlands (Yan, 1979). A total of 78 phytoplankton genera, belonging to the Cyanophyta, Chlorophyta, Bacillariophyta, Pyrrophyta, Euglenophyta, Chrysophyta, and Xanthophyta were identified. The list of phytoplankton genera found during the sampling times is given in Table 2. In this study, species diversity of Chlorophyta was much higher than that of other groups. This is apparently consistent with another study by Bunnag (2000) and Chankaew et al. (2007) whose observation locations were close to these study areas. The study in mine drainage areas showed that metals decreased the diversity of phytoplankton flora. Also, it was found that the Cyanophyta and Bacillariophyta were generally less tolerant than members of the Chlorophyta (South & Whittick, 1987). The relative abundance of phytoplankton assemblages at each sampling location studied was variable. It varied from 0% to 99.66% among the Cyanophyta, from 0.04% to 98.65% for Chlorophyta, from 0% to 59.94% for Pyrrophyta, from 0% to 91.85% for Bacillariophyta, from 0% to 18.63% for Euglenophyta, and from 0% to 98.18% for the Chrysophyta. In most of the samples taken, Cyanophyta were the most abundant group, representing 77.55% of the total phytoplankton assemblages (Figures 2-7). Cyanophyta contributed a relatively high proportion at all sampling locations and sampling times, except location 4 and during the rainy period. In location 4, Chlorophyta were generally found to be the most abundant group during several months (except October, November, and June), and accounted for more than 50% of the total.
146
W. MEEINKUIRT et al.
TABLE 2. Spatial occurrence of taxa registered from sampling locations in the arsenic
contaminated waters
Taxon
Dredging ponds
Dug ponds
1
2
3
Cyanophyta Anabaena spp.
1, 2, 3, 5
4, 6
Anabaenopsis sp.
5
4, 6
Anacystis sp.
-
6
1, 2, 3
4, 6
2, 5
-
Chroococcus spp.
1, 2, 3, 5
4, 6
Cylindrospermopsis sp.
1, 2, 3, 5
4, 6
Cylindrospermum sp.
1, 2, 3, 5
4, 6
Gloeocapsa sp.
1, 2, 3, 5
4, 6
Microcystis spp.
1, 2, 3, 5
4, 6
Merismopedia spp.
1, 2, 3, 5
4, 6
Oscillatoria spp.
1, 2, 3, 5
4, 6
Phormidium spp.
1, 2, 3, 5
4, 6
Raphidiopsis sp.
1, 2, 3, 5
4, 6
1, 2, 3
6
Aphanocapsa sp. Calothrix sp.
Spirulina sp. Synechococcus sp. Tolypothrix sp. Trichodesmium sp.
1
6
1, 5
6
1, 3, 5
-
Chlorophyta Ankistrodesmus spp. Botryococcus sp.
1, 2, 3, 5 2, 3, 5
4, 6 4
Chlorella sp.
1, 2, 3, 5
4, 6
1, 2, 5
4, 6
1
4
Chlorococcum sp. Chodatella sp. Clamydomonas sp.
1
6
Closterium sp.
1, 2, 3, 5
4, 6
Coelastrum spp.
1, 2, 3, 5
6
Cosmarium spp.
1, 2, 3, 5
4, 6
Crucigenia spp.
1, 2, 3, 5
4, 6
Crucigeniella sp.
1, 2, 3
4
Cylindrocystis sp.
1, 2
4, 6
Dictyosphaerium sp.
1, 3
4
-
4
Elakatothrix sp. Continued on next page
CHANGES IN RELATIVE ABUNDANCE OF PHYTOPLANKTON
TABLE 2 – End 1 Euastrum sp. Eudorina sp.
2
3
1, 2
6
1, 5
6
Gloeocystis sp.
2, 3, 5
4, 6
Golenkinia sp.
1, 2, 3, 5
4, 6
Gonatozygon sp. Micractinium sp. Monoraphidium spp. Mougeotia spp. Nephrocytium sp. Netrium sp. Oedogonium spp. Oocystis spp. Pandorina sp. Pediastrum spp. Penium sp. Scenedesmus spp. Spirogyra sp. Spirotaenia sp. Staurastrum spp. Staurodesmus spp. Tetraedron spp. Tetralantos sp. Treubaria sp. Ulothrix sp. Zygnema spp. Pyrrophyta Ceratium sp. Peridinium spp. Bacillariophyta Caloneis sp. Cymbella sp. Diatomella sp. Fragilaria sp. Gomphonema spp. Gyrosigma sp./Pleurosigma sp. Navicula spp. Nitzchia spp. Phaeodactylum sp. Pinnularia sp. Surirella spp. Synedra sp. Euglenophyta Euglena spp. Lepocinclis spp. Phacus spp. Trachelomonas spp. Chrysophyta Dinobryon spp. Xanthophyta Centritractus sp. Isthmochloron sp.
1 1, 2, 3 1, 2, 3, 5 1, 2, 3, 5 3 5 1, 2, 3, 5 1, 2, 3, 5 1, 2, 3 1, 2 1,5 1, 2, 3, 5 1, 2, 3 1 1, 2, 3, 5 1, 2, 5 1, 2, 3, 5 1, 2 3 1 1, 2
4 4 4, 6 6 4, 6 4, 6 4, 6 4, 6 4, 6 4, 6 4, 6 4 4 -
2, 5 1, 2, 3, 5
4, 6 4, 6
2 1, 2, 3 1, 2, 3, 5 1, 2, 3, 5 1, 2, 3, 5 2, 5 1, 2, 3, 5 1, 2, 3, 5 1, 2 1, 2, 3, 5 1, 2, 3, 5 2, 3, 5
4, 6 4, 6 4, 6 4, 6 4, 6 4, 6 6 4, 6 4 4
1, 2, 3, 5 1, 2, 3, 5 1, 2, 3, 5 1, 2, 3, 5
4, 6 4, 6 4, 6 4, 6
1, 2, 3, 5
4, 6
1, 2, 3, 5 1, 2, 3, 5
4, 6
147
148
W. MEEINKUIRT et al.
Also, note that the changes in relative abundance occasionally occurred during the rainy period (mainly from November to December). During the rainy period, several phytoplankton groups were recorded with a relative high abundance such as the Chrysophyta in location 1 (98.14% in November), Chlorophyta in locations 2, 4, and 5 (98.65% in November, 72.57% in December and 79.55% in November, respectively), and Bacillariophyta in location 3 (91.85% in December). There were remarkable differences in relative abundance among sampling locations, although Cyanophyta seemed to be present in higher numbers in many sampling locations as compared to other phytoplankton groups. Nutrient addition might have affected species composition of the phytoplankton communities (Seppala et al., 1999). Many studies have stated that Cyanophyta made up a large portion of assemblages in the epilimnion lake, which might have sheltered species that could have adapted to quite different ecosystems (Round, 1984).
Figure 2. Changes in phytoplankton densities (a) and relative abundance (b) of phytoplankton assemblages in location 1 at the arsenic contaminated waters, during the period July 2004 to June 2005.
CHANGES IN RELATIVE ABUNDANCE OF PHYTOPLANKTON
149
Figure 3. Changes in phytoplankton densities (a) and relative abundance (b) of phytoplankton assemblages in location 2 at the arsenic contaminated waters, during the period July 2004 to June 2005.
Referring to the classifications modified by the Applied Algal Research Laboratory, Chiang Mai University (Peerapornpisal et al., 2002), by altering the amounts of DO, BOD, conductivity, nitrate-nitrogen, ammonia-nitrogen, dissolved phosphorus and chlorophyll a, all sampling locations seem to have similar limnological behavior. According to the magnitude of those parameters, locations 3 and 5 could be classified as having an oligo-mesotrophic status, whilst other locations showed some differences in water quality at several sampling periods (Table 3). In fact, many Cyanophyta have been frequently associated with high trophic environments (Harrer, 1992; Huszar & Reynolds, 1997), but they are also important components of phytoplankton in oligo- and mesotrophic waters (Hecky & Kling, 1987; Canfield et al., 1989; Blomqvist et al., 1994; Huszar & Caraco, 1998). Chlorophyta were also significant in location 4, mainly due to desmids, which were less importance in other locations. The preponderance of desmids for location 4, probably caused by lower nutrient loading and pH than at other locations, supports Yan’s study (Yan, 1977).
150
W. MEEINKUIRT et al.
Figure 4. Changes in phytoplankton densities (a) and relative abundance (b) of phytoplankton assemblages in location 3 at the arsenic contaminated waters, during the period July 2004 to June 2005.
Certain dominant genera of Cylindrospermopsis sp. and Microcystis spp., for example, synthesized hepatoxic alkaloids and peptides, respectively, whereas, Cylindrospermum sp. synthesized neurotoxin. Cyanobacterial toxins were commonly classified according to their toxicological effect from cyanobacterial toxins (Beasley et al., 1989). They can occur within the cyanobacterial cell or be released into the water after cell lysis. A possible biological function of cyanotoxins, such as microcystins, is that they might provide cyanobacteria an advantage by reducing the losses associated with grazing and competition. Because grazing and competition pressures are not constant, the production of cyanotoxins could be induced or promoted only when necessary to avoid dispensable costs. Several cyanobacterial genera and strains can be examined on induced chemical (toxin production) and morphological (colony formation) defenses when exposed to grazers or competitors. Several functional groups on the cyanobacteria surface can interact with metals and play a major role in heavy metal contaminated waters (Ledin, 2000).
CHANGES IN RELATIVE ABUNDANCE OF PHYTOPLANKTON
151
Figure 5. Changes in phytoplankton densities (a) and relative abundance (b) of phytoplankton assemblages in location 4 at the arsenic contaminated waters, during the period July 2004 to June 2005.
Location 1 In location 1, generally the Cyanophyta were the dominant group in all sampling periods, except in November (Figure 2). The highest total abundance was attained in May with growth of Raphidiopsis sp. comprising 97.16% of the total. Minor peaks occurred in September and March, due to a large number of Cylindrospermum sp. in those periods, constituting about 62.77% and 53.37% of the total, respectively. However, the pattern in the rainy period (November and December) was very different. A significant number of phytoplankton flora was detected during the rainy period. In subsequent periods, the total abundance decreased with a fall in the numbers of mostly phytoplankton assemblages.
152
W. MEEINKUIRT et al.
Figure 6. Changes in phytoplankton densities (a) and relative abundance (b) of phytoplankton assemblages in location 5 at the arsenic contaminated waters, during the period July 2004 to June 2005.
During November, Chrysophyta in the genus Dinobryon spp. were most conspicuous with a relatively high abundance of 98.14% of the total. In December, phytoplankton assemblages seemed to decrease distinctly as the rain intensity decreased slightly. The population of dinoflagellates dominated with only small quantities of Peridinium spp., found (21.41%). When rain intensity sharply increased, the phytoplankton identified was mostly dominated by Cyanophyta. Phytoplankton rich waters in those periods were generally dominated by Oscillatoria spp.
Location 2 In location 2, different phytoplankton groups alternated dominance in each period. Cyanophyta were dominant in July, August, February, April and May, and a small number were also found in December. Chlorophyta were dominant in November, January, and March and Chrysophyta in September (Figure 3). The investigations showed that the lowest
CHANGES IN RELATIVE ABUNDANCE OF PHYTOPLANKTON
153
density was observed in December. Microcystis spp. dominated but with only small quantities, or 37.67% of the total. In the following month, January, the highest numbers were observed with Botryococcus sp. achieving 61.17% of the total.
Figure 7. Changes in phytoplankton densities (a) and relative abundance (b) of phytoplankton assemblages in location 6 at the arsenic contaminated waters, during the period July 2004 to June 2005.
In general, all sampling locations had their highest cell density in the early rainy period. However, it was found that the highest cell density occurred in location 2 during the rainy period, mainly in January. The Meteorological Department of Thailand has reported that the annual rain intensity was not high during the study period and when compared with previous investigations.
International Journal on Algae, 2008, 10(2):141-162
154
TABLE 3. Water quality status of sampling locations in arsenic contaminated waters determined from July 2004 to June 2005 Month
Location 1
Location 2
Location 3
Location 4
Location 5
Location 6
July
Mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
August
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
September
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
October
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
November
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligotrophic
Oligo-mesotrophic
Oligo-mesotrophic
December
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
January
Oligo-mesotrophic
Oligotrophic
Oligo-mesotrophic
Oligotrophic
Oligo-mesotrophic
Oligo-mesotrophic
February
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
March
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Mesotrophic
April
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligotrophic
Oligo-mesotrophic
Oligo-mesotrophic
May
Mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Mesotrophic
June
Mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Oligo-mesotrophic
Mesotrophic
TABLE 4. Dominant phytoplankton genera in each location of arsenic contaminated waters at the Ronphibun district of Nakhon Si Thammarat province, Thailand, during July to December 2004 Location
Year 2004 July
August
September
October
November
December
1
Cylindrospermopsis sp.
Cylindrospermopsis sp.
Cylindrospermum sp., Oscillatoria spp.
Raphidiopsis sp.
Dinobryon spp.
2
Cylindrospermopsis sp.
Cylindrospermopsis sp.
Dinobryon spp., Botryococcus sp.
Botryococcus sp., Dinobryon spp.
Botryococcus sp.
Peridinium spp., Dinobryon spp., Oscillatoria spp. Microcystis spp.
3
Cylindrospermopsis sp.,Microcystis spp., Raphidiopsis sp
Microcystis spp., Raphidiopsis sp., Oscillatoria spp.
Raphidiopsis sp., Fragilaria sp., Peridinium spp.
Anabaena spp.
Fragilaria sp.
Staurastrum spp.
CHANGES IN RELATIVE ABUNDANCE OF PHYTOPLANKTON
4
Cosmarium spp.
5
Raphidiopsis sp., Oscillatoria spp., Anabaena spp., Chroococcus sp.
6
Cylindrospermopsis sp. Peridinium spp., Oscillatoria spp.
Botryococcus sp.
Cylindrospermopsis sp.
Cylindrospermopsis sp.
Cosmarium spp., Staurastrum spp., Gloeocapsa sp., Chroococcus spp.
Raphidiopsis sp., Gloeocapsa sp.
Microcystis spp., Oscillatoria spp., Botryococcus sp.
Staurastrum spp., Ankistrodesmus spp.
Cylindrospermopsis sp. Oscillatoria spp., Dinobryon spp.
Oscillatoria spp.
Botryococcus sp.
Phormidium spp., Fragilaria sp.
Cylindrospermopsis sp.
Peridinium spp., Oscillatoria spp.
Cylindrospermopsis sp. Phormidium spp., Chroococcus sp., Cylindrospermum sp.
Chlorella sp., Gomphonema sp., Trachelomonas spp.
TABLE 5. Dominant phytoplankton genera in each location of arsenic contaminated waters at the Ronphibun district of Nakhon Si Thammarat province, Thailand, during January to June 2005 Location
Year 2005 January
Febuary
March Cylindrospermum sp.,
1
Oscillatoria spp.
Oscillatoria spp.
Oscillatoria spp., Phormidium spp.
2
Botryococcus sp.
Oscillatoria spp., Cylindrospermopsis sp.
Botryococcus sp.
3
Dinobryon spp.
Oscillatoria spp.
4
Peridinium spp., Cosmarium spp.
Botryococcus sp.
5
Dinobryon spp.
Dinobryon spp., Oscillatoria spp.
Oscillatoria spp., Botryococcus sp. Ankistrodesmus spp., Oscillatoria spp. Oscillatoria spp., Dinobryon spp.
6
Cylindrospermopsis sp. Oscillatoria spp.
Oscillatoria spp.
Oscillatoria spp.
April
May
June
Oscillatoria spp., Phormidium spp.
Raphidiopsis sp., Phormidium spp.
Oscillatoria spp.
Oscillatoria spp., Cylindrospermopsis sp. Raphidiopsis sp., Oscillatoria spp.
Oscillatoria spp.
Dinobryon spp., Oscillatoria spp. Peridinium spp., Oscillatoria spp. Oscillatoria spp., Anabaenopsis sp. Oscillatoria spp., Dinobryon spp., Raphidiopsis sp.
Botryococcus sp. Oscillatoria spp., Raphidiopsis sp., Dinobryon spp. Cylindrospermopsis sp., Cylindrospermum sp.
Cylindrospermopsis sp., Oscillatoria spp. Chroococcus sp., Ankistrodesmus sp. Oscillatoria spp., Peridinium spp. Oscillatoria spp., Cylindrospermopsis sp.
Cylindrospermopsis sp.
155
International Journal on Algae, 2008, 10(2):141-162
156
Location 3 Cyanophyta were the most abundant group of phytoplankton in location 3 in August, October and March, whereas Chlorophyta were the most abundant in January (Figure 4). Each sampling period above had one dominant genera of phytoplankton with the highest peak observed in March when Oscillatoria spp. accounted for 88.91% of the total. Other genera dominated at other times. Thus, Raphidiopsis sp. was dominant in October and Microcystis spp. was dominant in August, whereas Dinobryon spp. was dominant in January. In addition, there was a noticeable decrease in the total cell densities of phytoplankton assemblages during the rainy period (November and December). In December, cell densities were at their lowest level, whereas Fragilaria sp. was dominant at 79.94% of the total at that time. Location 4 Compared with the other sampling locations, location 4 had a dominant phytoplankton group that differed from the other locations. Generally, Chlorophyta were the dominant phytoplankton group at all sampling periods, except for October and November (Figure 5). In October and November, Cyanophyta were occasionally dominant and they alternated in dominance during the following months. The highest peak of phytoplankton abundance was in August, with Botryococcus sp. making up 79.82% of the total. A small peak of the same genus was found in February, with 79.82% of the total. In December, again this had the lowest total population. At that time, the phytoplankton was dominated by Staurastrum spp., accounting for 40.12% of the total. In January Pyrrophyta in the genus Peridinium spp. and Chlorophyta in the genus Cosmarium spp. had small increases. In particular, the phytoplankton present during the remaining months in 2005 was frequently characterized by the presence of Chlorophyta and Cyanophyta, such as Botryococcus sp., Ankistrodesmus spp. and Oscillatoria spp. Location 5 During the early rainy period in location 5, except for February, Cyanophyta played an important role in the phytoplankton population (Figure 6). In August Cylindrospermopsis sp. accounted for 90.90% of the total, whilst Oscillatoria spp. and Dinobryon spp. (in particular) were dominant in October. Cell density declined distinctly during the rainy period (November and December) and then seemed to increase when the rain intensity decreased slightly in January. In those sampling periods, many different groups were found to be dominant such as Chlorophyta in November (mainly Botryococcus sp.), Cyanophyta in December (mainly Phormidium spp.)
CHANGES IN RELATIVE ABUNDANCE OF PHYTOPLANKTON
157
and Chrysophyta in January (mainly Dinobryon spp.). In addition, Dinobryon spp. was also the dominant phytoplankton in February during the early part of the rainy period. During the dry period, in which there was a considerable increase in the total amount of arsenic, the cell density of phytoplankton increased compared to the previous months, and Cyanophyta were the dominant group. Generally, filamentous cyanobacteria and Chrysophyta were the abundant organisms during the dry periods, such as Oscillatoria spp. and Dinobryon spp. Location 6 In location 6, Cyanophyta were always the dominant group with filamentous cyanobacteria as the major genera (Figure 7). At the beginning of the sampling period, phytoplankton abundance steadily increased from July to August and then decreased immediately in September. However, phytoplankton abundance increased again slightly in October. The main genus found in those periods was Cylindrospermopsis sp. with the highest peak occurring with 94.98% of the total population. A later peak was found in May, and the present study also shows filamentous cyanobacteria still the dominant genera with Oscillatoria spp. and Cylindrospermopsis sp. constituting 46.10% and 44.43% of the total, respectively. During November and December, the proportion of phytoplankton assemblages seemed to have changed considerably, and the phytoplankton density also declined compared with other months. Many other genera were encountered during November and December in small numbers such as Pyrrophyta, Chlorophyta, Cyanophyta, and Euglenophyta. In the genus Peridinium spp. a member of the Pyrrophyta were dominant in November, accounting for 31.87% of the total, whilst Chlorophyta in the genus Chlorella sp. were dominant in December, accounting for 30.19% of the total. Most previous investigations on natural tropical waters have reported that higher phytoplankton populations occur in dry rather than in rainy periods (Egborge, 1979; Zhang et al., 2006). However, this was not the case for all the ecosystems in this study. However, the highest phytoplankton population was found at location 3 during the dry period. At this time, there was an increase in temperature, and light intensity was high. This was consistent with Ghavzan and Gunale’s study (2007) on one hand. On the other hand, at other locations the mean total phytoplankton population density during the early rainy period was significantly higher than that in the dry period. This is also consistent with the observation of Nweze (2006). This finding can probably be correlated with initial rains, causing run-off containing increased quantities of nutrients from the surrounding agricultural land, which induced the phytoplankton growth. The observation that phytoplankton species numbers and densities dramatically decreased as the rainy season progressed (November to December) at all sampling locations might be attributable to reduced water transparency,
158
W. MEEINKUIRT et al.
wind effects, cloud cover, and the dilution effects of the rain (Evurunobi, 1984; Gurung et al., 2006). From November to December, heavy rains occurred in the sampling ponds, resulting in large volumes of water being added over a short period of time. This increased water volume might have diluted the phytoplankton in the sampling locations, and the rate of basin flushing restricts the flora to small, fast-growing, and invasive species with a faster growth rate allowing them to resist dilution from the waters (Reynolds & Lund, 1988; Melo & Huszar, 2000). During such a period of time, the water ponds cool from November to December, so low phytoplankton abundance coincides with low temperatures and light. Therefore light and temperature conditions are of great importance in controlling phytoplankton growth (Bleiker & Schanz, 1989; Perez et al., 1999). Needoba and Harrison (2004) have stated that the light regime influences the relative uptake, assimilation, and efflux rates of nitrate, whilst a decrease in phytoplankton density with falling water temperatures was probably due to slow reproduction rather than to an increased death rate (Biswas, 1992). In the meantime, genera number and densities apparently increased in January. This could be due to a steadily decreasing level of precipitation with little monsoon effect from the northeast as compared to previous years. Thus, the observation that climatic events and seasonal impacts have a strong influence on hydrodynamics and on the structure of aquatic communities in ponds support Cowan et al. (1999), who have suggested that this due mainly through interference with nutrient balances (Anneville et al., 2005). CONCLUSIONS
The phytoplankton population in the arsenic contaminated waters of Ron Phibun district are associated with highly diversified flora. This investigation of water samples taken from dredging ponds and dug ponds has shown the presence of a cosmopolitan phytoplankton community making a significant contribution to the richness of phytoplankton biodiversity in arsenic contaminated surface freshwater. All the different sampling points lie in the same geographical area; they are subjected to identical climate and, on the average, to the same seasonal metereological variability (Jianjun, 2000). However, some sampling locations may have slight differences but enough to alter the response of the phytoplankton especially during the rainy period. A distinctive change in phytoplankton communities was observed in December at all sampling locations. There is no field or experimental evidence that offers a clear mechanism for the responses in richness and abundance that have been observed along the arsenic contaminated waters. This study is among the first to explore regional phytoplankton richness and abundance with respect to a major well-documented seasonal impact.
CHANGES IN RELATIVE ABUNDANCE OF PHYTOPLANKTON
159
From this study, Cyanophyta were the most dominant genera of phytoplankton. The high relative abundance was made up of coccal and filamentous forms such as Microcystis, Oscillatoria, Cylindrospermopsis, and Phormidium, all belonging to the Cyanophyta. Moreover, manipulative analyses are needed to verify cause and affect relationships between environmental factors and phytoplankton communities. We foresee that more accurate and sensitive descriptions of the variability of biodiversity in phytoplankton communities can be obtained at different locations if, in future studies, more physical and chemical characteristics are included in addition to phytoplankton communities so that we can show how a limnological characterization related to phytoplankton communities of arsenic contaminated waters may allow for a more scientific planning process for the use of the waters. ACKNOWLEDGMENTS This work was carried out with the aid of a grant from the TRF/BIOTEC Special Program for Biodiversity Research and Training grant T 348014 and by the financial support of Graduate School, Prince of Songkla University, Thailand. We also thank Dr. Brian Hodgson for assistance with the manuscript. REFERENCES
Anneville, O., S. Gammeter & D. Straile. 2005. Phosphorus decrease and climate variability: mediators of synchrony in phytoplankton changes among European perialpine lakes. Freshwat. Biol. 50: 1731-1746. APHA, AWWA, WEF. 1998. American Public Health Association, American Water Works Association and Water Environment Federation. Standard methods for the examination of water and wastewater. Amer. Publ. Health Ass., Washington, DC. Beasley, V.R., A.M. Dahlem, W.O. Cook et al. 1989. Diagnostic and clinically important aspects of cyanobacterial (blue-green algae) toxicoses. J. Vet. Diagn. Invest. 1: 359-365. Biswas, S. 1992. Phytoplankton periodicity in Ogelube Lake, Anambra State, Nigeria during 1979-1980. Hydrobiologia 246(2): 169-172. Bleiker, W. & F. Schanz. 1989. Influence of environmental factors on the phytoplankton spring bloom in lake Zurich. Aquat. Sci. 51(1): 47-58. Blomqvist, P., A. Petterson & P. Hyenstrand. 1994. Ammonium-nitrogen: A key regulatory factor causing dominance of non nitrogen-fixing Cyanobacteria in aquatic systems. Arch. Hydrobiol. 132: 141-164. Boonchalermkit, S., J. Wongsanoon & M. Fukuda. 1996. A study of arsenic contamination in Pak Pa-Nang Bay Nakhon Sri-Tammaraj Province, Thailand. Proc. of the ASEAN-Canada Technical. Conf. on Mar. Sci., 24-28 June 1996, Penang (Malaysia).
160
W. MEEINKUIRT et al.
Bottino, N.R., R.D. Newman, E.R. Cox et al. 1978. The effects of arsenate and arsenite on the growth and morphology of the marine Unicellular algae Tetraselmis chui (Chlorophyta) and Hymenomonas carterae (Chrysophyta). J. Exp. Mar. Biol. Ecol. 33(2): 153-168. Budd, K. & S.R. Craig. 1981. Resistance to arsenate toxicity in the blue-green alga Synechococcus leopoliensis. Can. J. Bot. 59: 1518-1521. Bunnag, P. 2000. Removal of arsenic from water by freshwater algae. M.Sc. Thesis. Mahidol Univ., Bangkok (Thailand). Canfield, D.E.Jr., E. Philips & C.M. Duarte. 1989. Factors influencing the abundance of blue-green algae in Florida lakes. Can. J. Fish. Aquat. Sci. 46: 1232-1237. Chaffin, J.L. 2003. The Influence of Elevated Arsenic Concentrations from an Abandoned Mine on Stream Biota and Leaf Breakdown in a Headwater Stream. M.Sc. Thesis. The Virginia Polytechnic Inst. and State Univ., Virginia. Chaibu, P. 2000. Potential use of trichoptera as water pollution biomonitoring in Ping river, Chiangmai. Abstr. Ph.D. (Biol.) Thesis. Chiangmai. Chankaew, W., S. Chankaew & N. Sugsai. 2007. Diversity of phytoplankton in Sago palm forest in Ronphibun district, Nakhon Si Thammarat province: The 3rd nat. conf. on algae and plankton, faculty of sci., Chulalongkorn Univ. 21-23 March 2007. Chen, C.Y., R.S. Stemberger, B. Klaue et al. 2000. Accumulation of heavy metals in food web components across of lakes. Limnol. Oceanogr. 45: 1525-1536. Cowan, V.J., K. Lorenzen & S.J. Funge-Smith. 1999. Impact of culture intensity and monsoon season on water quality in Thai commercial shrimp ponds. Aquat. Res. 30: 123-133. Croasdale, H. & E.A. Flint. 1986a. Flora of New Zealand Desmids. Vol. I. Gover. Print., Wellington. Croasdale, H. & E.A. Flint. 1986b. Flora of New Zealand Desmids. Vol. II. Gover. Print., Wellington. Croasdale, H. & E.A. Flint. 1986c. Flora of New Zealand Desmids. Vol. III. Gover. Print., Wellington. Csonto, J., J. Kadukova & M. Polak. 2004. Artificial life simulation of living alga cells and its Sorption mechanisms. J. Med. Syst. 25(3): 221-231. De Philipplis, R. & M. Vincenzini. 1998. Exocellular polysaccharides from cyanobacteria and their possible applications. FEMS Microbiol. Rev. 22(3): 151-175. Duker, A.A., E.J.M. Carranza & M. Hale. 2005. Arsenic geochemistry and health. Environ. Int. 31: 631-641. Egborge, A.B.M. 1979. The seasonal distribution of phytoplankton of the lake Asejire – a new impoundment in Nigeria: Proc. of Intern. Conf. on Kainji Lake and River Basins Development in Africa, 11-17 Dec. 1977, Ibadan (Nigeria). Fujiwara, S., I. Kobayashi, S. Hoshino et al. 2000. Isolation and characterization of arsenate-sensitive and resistant mutants of Chlamydomonas reinhardtii. Plant Cell Physiol. 41: 77-83. Evurunobi, N.O. 1984. The phytoplankton and some physicochemical aspects of Ogelube lake, Nigeria during May 1981-May 1982. M.Sc. Thesis. Univ. of Nigeria, Nsukka. Geesey, G. & L. Jang. 1990. Extracellular polymers for metal binding. Pp. 223-247. In: Microbial mineral recovery. McGraw-Hill Publ. Company, New York.
CHANGES IN RELATIVE ABUNDANCE OF PHYTOPLANKTON
161
Ghavzan, N.J. & V.R. Gunale. 2007. Seasonal dynamics of phytoplankton and their relationship with the environment in the Pavana and Mutha rivers (Pune, India). Intern. J. Algae 9(1): 64-80. Gurung, T.B., R.P. Dhakal & J.D. Bista. 2006. Phytoplankton primary production, chlorophyll a and nutrient concentrations in the water column of mountainous Lake Phewa, Nepal. Lakes Reserv. Res. Manag. 11: 141-148. Harrer, D. 1992. Eutrophication of freshwater: Princicles, problems and restroration. Chapman & Hall, London. Hecky, R. & H.J. Kling. 1987. Phytoplankton ecology of the great lakes in the rift valleys of central Africa. Arch. Hydrobiol. 25: 197-228. Howard, A.G., S.D.W. Comber, D. Kifle et al. 1995. Arsenic speciation and seasonal changes in nutrient availability and microplankton abundance in Southampton Water, U.K. Estuar. Coast. Shelf. Sci. 40: 435-450. Huszar, V.L.M & N. Caraco. 1998. The relationship between phytoplankton composition and physical-chemical variables: a comparison of taxonomic and morphological-functional approaches in six temperate lakes. Freshwat. Biol. 40: 1-18. Huszar, V.L.M. & C.S. Reynolds. 1997. Phytoplankton periodicity and sequencesof dominance in an Amazonian flood-plain lake (Lago Botata, Para, Brazil): responses to gradual environmental change. Hydrobiologia 346: 169-181. Japan International Cooperation Agency (JICA). 2000. The environmental management planning survey for arsenic contaminated area of the Nakhon Si Thammarat province in the Kingdom of Thailand: Final report. Jianjun, Z. 2000. GIS application on arsenic considering toxicological aspect in an old Tin Mining Area, Thailand. Abstr. Ph.D. (Biol.) Thesis. Pathumthani. John, D.M., B.A. Whitton & A.J. Brook. 2002. The freshwater algal flora of the British Isles. Cambridge Univ. Press, Cambridge. Katsoyiannis, I.A. & A.I. Zouboulis. 2004. Application of biological processes for the removal of arsenic from groundwaters. Water Res. 38: 17-26. Komarek, J. & K. Anagnostidis. 1999. Cyanoprokaryota. 1. Teil: Chroococcales. Gustav Fischer, Germany. Ledin, M. 2000. Accumulation of metals by microorganisms-processes and importance for soil systems. Earth. Sci. Rev. 51: 1-31. Melo, S.D. & M. Huszar. 2000. Phytoplankton in an Amazonian flood-plain lake (Lago Batata, Brasil): diel variation and species strategie. J. Plankton. Res. 22(1): 63-76. Needoba, J.A. & P.J. Harrison. 2004. Influence of low light and a light: Dark cycle on NO3- uptake, intracellular NO3- and nitrogen isotope fractionation by marine phytoplankton. J. Phycol. 40(3): 505-516. Nweze, N.O. 2006. Seasonal variations in phytoplankton populations in Ogelube Lake, a small natural West African Lake. Lakes Reserv. Res. Manag. 11: 63-72. Peerapornpisal, Y. 2005. Freshwater Algae in Northern Thailand. Chotana Print Co. Ltd. Chiang Mai. Perez, M.C., S. Bonilla & G. Martinez. 1999. Phytoplankton community of a polymictic reservoir, La Plata River basin, Uruguay. Rev. Brasil. Biol. 59(4): 535-541.
162
W. MEEINKUIRT et al.
Pinto, E., T.C.S. Sigaud-Kutner, M.A.S. Leitao et al. 2003. Heavy metal-induced oxidative stress in algae. J. Phycol. 39: 1008-1018. Planas, D. & F.P. Healey. 1978. Effect of arsenate on growth and phosphorus metabolism of phytoplankton. J. Phycol. 14: 337-341. Reynolds, C.S. & J.W.G. Lund. 1988. The phytoplankton of an enriched, soft-water lake subject to intermittent hydraulic flushing (Grasmere, English lake district). Freshwat. Biol. 19: 379-404. Riedel, G.F. 1993. The annual cycle of arsenic in a temperate estuary. Estuaries 16: 533-540. Round, F.E. 1984. The ecology of algae. Cambridge Univ. Press, Cambridge. Ruangsomboon, S., A. Chidthaisong, B. Bunnag et al. 2006. Lead (Pb2+) removal from wastewater by the cyanobacterium Calothrix marchica. Kasetsart J. (Nat. Sci). 40: 784-794. Sanders, J.G. & G.F. Riedel. 1993. Trace element transformation during the development of an estuarine algal bloom. Estuaries 16: 521-532. Sanders, J.G. & H.L. Windom. 1980. The Uptake and Reduction of Arsenic Species by Marine Algae. Estuar. Coast. Mar. Sci. 10: 555-567. Seppala, J., T. Tamminen & S. Kaitala. 1999. Experimental evaluation of nutrient of phytoplankton communities in the Gulf of Riga. J. Mar. Syst. 23: 107-126. South, G.R. & A. Whittick. 1987. Introduction to phycology. Black. Sci. Publ. Inc, California. Suwanmanee, A. 1999. Distribution of arsenic in the environment of Amphoe Ronphibul Changwat Nakhon Si Thammarat. M.Sc. Thesis. Prince of Songkla Univ., Songkhla (Thailand). Thirunavukkarasu, O., T. Viraraghavan & K. Subramanian. 2003. Arsenic removal from drinking water using granular ferric hydroxide. Water SA 29(2): 161-170. Whitford, L.A. & G.J. Schumacher. 1973. A manual of freshwater algae. Sparks Press, Raleigh. Williams, M., F. Fordyce, A. Paijitprapapon & P. Charoenchaisri. 1996. Arsenic contamination in surface drainage and groundwater in part of the southeast Asian tin belt, Nakhon Si Thammarat Province, southern Thailand. Environ. Geol. 27: 16-33. Wongrat, L. 2001. Phytoplankton. Kasetsart Univ. Press, Bangkok. Yan, N.D. 1979. Phytoplankton community of an acidified, heavy metal-contaminated lake near Sudbury, Ontario. Water Air Soil Poll. 11: 43-55. Zhang, Z., W. Qu, S. Jiang & H. Zhu. 2006. Blue-green algae is predominant in Dianshan Lake. Aquat. Ecosyst. Health Manag. 9(1): 55-58.